HARVARD UNIVERSITY Library of the Museum of Comparative Zoology ;REAT BASIN NATURALIST MEMOffi Brigham Young University 1 Biology of Desert Rodents mber 7 ''K. GREAT BASIN NATURALIST Editor. Stephen L. Wood, Department of Zoology, 290 Life Science Museum, Brigham Young University, Provo, Utah 84602. Editorial Board. Kimball T. Harper, Chairman, Botany; James R. Barnes, Zoology; Hal L. Black, Zoology; Stanley L. Welsh, Botany; Clayton M. White, Zoology. All are at Brig- ham Young University, Provo, Utah 84602. Ex Officio Editorial Board Members. Bruce N. Smith, Dean, College of Biological and Agricul- tural Sciences; Norman A. Darais, University Editor, University Publications. Subject Area Associate Editors. Dr. Noel H. Holmgren, New York Botanical Garden, Bronx, New York 10458 (Plant Taxonomy). Dr. James A. MacMahon, Utah State University, Department of Biology, UMC 53, Lo- gan, Utah 84322 (Vertebrate Zoology). Dr. G. Wayne Minshall, Department of Biology, Idaho State University, Pocatello, Idaho 83201 (Aquatic Biology). Dr. Ned K. Johnson, Museum of Vertebrate Zoology and Department of Zoology, Uni- versity of California, Berkeley, California 94720 (Ornithology). Dr. E. Philip Pister, Associate Fishery Biologist, California Department of Fish and Game, 407 West Line Street, Bishop, California 93514 (Fish Biology). Dr. Wayne N. Mathis, Chairman, Department of Entomology, National Museum of Natural History, Smithsonian Institution, Washington, D.C. 20560 (Entomology). Dr. Theodore W. Weaver III, Department of Botany, Montana State University, Boze- man, Montana 59715 (Plant Ecology). The Great Basin Naturalist was founded in 1939 and has been published from one to four times a year since then by Brigham Young University. Previously unpublished manuscripts in English of less than 100 printed pages in length and pertaining to the biological natural his- tory of western North America are accepted. Western North America is considered to be west of the Mississippi River from Alaska to Panama. The Great Basin Naturalist Memoirs was es- tablished in 1976 for scholarly works in biological natural history longer than can be accom- modated in the parent publication. Tlie Memoirs appears irregularly and bears no geographi- cal restriction in subject matter. Manuscripts are subject to the approval of the editor. Subscriptions. The annual subscription to the Great Basin Naturalist for private individuals is $16; for institutions, $24 (outside the United States, $18 and $26); and for student subscrip- tions, $10. Tlie price of single issues is $6 each. All back issues are in print and are available for sale. All matters pertaining to subscriptions, back issues, or other business should be di- rected to Brigham Young University, Great Basin Naturalist, 290 Life Science Museum, Pro- vo, Utah 84602. Tlie Great Basin Naturalist Memoirs mav be purchased from the same office at the rate indicated on the inside of the back cover of either journal. Sclu)larly Exchanges. Libraries or other organizations interested in obtaining either journal through a continuing exchange of scholarly publications should contact the Brigham Young Ihiiversity Exchange Librarian, Harold B. Lee Library, Provo, Utah 84602. Manuscripts. See Notice to Contributors on the inside back cover. 8-83 1 .5M 66460 ISSN 017-3614 CONTENTS Introduction. O. J. Reichman and James H. Brown 1 Evolutionarv relationships of heteromyid rodents. John C. Hafner and Mark S. Hafner ... 3 Desert rodent adaptation and community structure. Michael A. Mares 30 Morphological structure and function in desert heteromyid rodents. Joyce C. Nikolai and Dennis M. Bramble 44 Adaptive phvsiolog)" of heteromyid rodents. Richard E. MacMillen 65 Behavior of desert heteromyids. O. J. Reichman 77 Desert rodent populations: factors affecting abundance, distribution, and genetic struc- ture. James C. Mun^er. Michael A. Bowers, and W. Thomas Jones 91 Patterns of morpholo^v and resource use in North American desert rodent communities M. V. Price and J. H. Brown 117 Great Basin Naturalist Memoirs Biolojsy of Desert Rodents l^rii^hain ^'oiiiiij; Univcrsilv, l^ovo, Utah 1983 INTHODUCTION (). j. K.'ulnnair and jinii.'s II. Hi Studies of desert rodents, especially the heteromyid species of southwestern North America, have a long and illustrious history. These investigations have not only revealed many fascinating aspects of the biology of the rodents themselves, but they have also con- tributed importantly to our general under- standing of such diverse disciplines as func- tional anatomy, comparative and environmental physiology, population and community ecology, and systematics and evo- lutionary biology. The great early biologists (]. Hart Merriam, Joseph (irinnell, and Lee H. Dice were profoundly influenced by their field experiences with small mammals in the southwestern United States. Subsequently, many leading figures of American mammal- ogy have contributed to the knowledge of desert rodents. The works of these, and many other scientists, are cited in the papers of this symposium. Until the last 25 years, most of this work was primarily descriptive and was largely performed by mammalogists interested in taxonomy, classification, and geographic dis- tribution. Important systematic and bio- geographic work has continued, and by the late 195()s sufficient basic information was available to allow investigators to delve into the challenging relationships between form, function, distribution, and evolutionary his- tory. The pioneering studies of Schmidt- Nielsen and Bartholomew and his students on physiological adaptations, by Eisenberg on comparative behavior, and by the Websters on functional morphology of the ear have been followed by investigations in such di- verse disciplines as cytogenics, communitv ecology, and sociobiology. The majority of research on desert rodents has focused on representatives of the Hetero- myidae that inhabit arid regions of south- western North America. Although this sym- posium has concentrated on heteromyids, it is obvious that vast areas of the globe are cov- ered by deserts and inhabited by other ro- dents as significant biologically as hetero- myids. A glimpse of these is obtained in the paper by Mike Mares, but much more is missing— either because these proceedings were limited in time and publication space, or because so many other desert rodents are poorly known. Even within the North Ameri- can deserts there are other important grovips of rodents (e.g., cricetids and ground squir- rels), but we have chosen to concentrate on the heteromyids because of their specialized adaptations to desert environments. Perhaps more is known about the comparative anato- my, physiology, behavior, ecology, and evo- lution of these rodents than is known about any comparable group of related organisms, with the possible exceptions of Hawaiian Drosir)Mla, Galapagos finches, and West In- dian Anolis. In a very important sense, heter- omyids provide an empirical model of the 'Division of BiolotJy, Kansas State ■Department of Ecoloj^y and Evol Biology, Uni' Great Basin Naturalist Memoirs No. 7 patterns and processes involved in the adap- tive radiation of a monophyletic group to ex- ploit diverse ecological opportunities within a limited geographic range. This system is being used as a model to answer general questions and to test theoretical predictions about relationships between form and func- tion, the adaptive nature of evolutionary change, and the organization of ecological communities. In organizing the symposium and arrang- ing for its publication we had two major goals: (1) to present in one place a review and synthesis of much of what has been learned about diverse aspects of desert rodent biology, and (2) to stimulate continued and additional research by calling attention to both unanswered questions and recent ad- vances. If the published versions of the pa- pers generate as much interest, enthusiasm, and critical discussion as did the original symposium, our goals and expectations will have been exceeded. Condensed versions of these papers were presented at the 62nd Annual Meeting of the American Society of Mammalogists at Snow- bird, Utah, on 22 June 1982. We thank J. Mary Taylor, H. Duane Smith, the American Society of Mammalogists Program Com- mittee and Local Committee, the speakers, and an exceptionally attentive and inter- active audience for the success of the symposium. EVOLUTIONARY RELATIONSHIPS OF HETEROMYID RODENTS' John C. Hafner and Mark S. Hafner' Abstract.— The rodent superfamily Geomyoidea is an old, undoubtedly inonophyletic lineage having only ob- scaire affinities with other rodent groups. Geomyoid rodents, autochthonous in North America, experienced major evolutionary diversification in the Mio-Pliocene coincident with the development of the Madro-Tertiary Geoflora and the climatic trend toward increasing aridity and coolness. Extant geomyoids are divisible into two groups: (1) the Geomyidae, all members of which are fossorial, and (2) the Heteromyidae, whose members display an adaptive con- tinuum from bipedal, xeric-adapted forms to scansorial, mesic-adapted forms. These moieties, although recognizable on biochemical criteria, become particularly difficult to distinguish when paleontological data are considered. Nev- ertheless, most lines of evidence indicate that the families Heteromyidae and Geomyidae are distinct, monophyletic lineages. The extant heteromyids comprise three main lineages (including six genera) that diverged during the Eocene: (1) subfamily Perognathinae (Chaetodipus and Perognathus); (2) subfamily Dipodomyinae (Dipodoinys and Micro- dipodiips); and (.3) subfamily Heteromyinae {Lioimjs and Heteromijs). Protein differentiation has occurred at hetero- geneous rates among these major lineages. Based on available karyotypic data, the main direction of chromosomal evolution in the Heteromyidae appears to be toward increasing chromosome number. Cladistic analysis of morpho- logical characters used in previous studies supports biochemical evidence allying Microdipodops with Dipodoinys. A model is introduced to describe how heterochronic changes in ontogeny may explain the great breadth of morpho- logical diversification within the superfamily. Taxonomic recommendations at the subfamilial, generic, and sub- generic levels are provided. The most important point to be emphasized is that "Parallelism, parallelism, more parallelism and still more parallelism" is the evolutionary motto of the ro- dents in general and of the heteromyids in particular. This extends to all parts of the body. It makes the task of determining interrelationships particularly difficult, and renders exceptionally dangerous any postulates as to what the relationships of a given form may really be, if hill evidence does not exist to clear the maze of parallel adaptations for us. This shows the insuperable diffi- culties awaiting anyone who attempts a classification based on a single character or on a group of characters with a common cause. Albert Elmer Wood (19.35:250) A trio of monographs on the evolutionary biology of heteromyid rodents appeared in the early 1930s and, subsequently, has hall- marked this specialized area of scientific in- quiry. Hatt (1932) and Howell (1932) pro- vided definitive accounts of the morphology of the ricochetal forms, and Wood (1935) synthesized the then available data, gleaned from fossil and recent forms, into a coherent summarization. Interestingly, the last com- prehensive statement of the evolutionary relationships within the Heteromyidae was Wood's exhaustive treatment, now aged one- half century. However, during the past 50 years a tremendous volume of literature per- taining to heteromyid evolution has accumu- lated, justly reflecting the immense interest in these mammals. Some of the questions posed by Wood and the others have been an- swered to satisfaction, whereas the answers to other queries still elude us and await extrica- tion by future research. It is the intent of this contribution to pre- sent a compendium of the evolution of heter- omyid rodents, wherein we attempt to in- tegrate the classic morphological studies of the 1930s with the more recent systematic treatments. As a definitive statement on het- eromyid relationships, this effort may appear inchoate in a few years. However, the assimi- lation of earlier ideas with those of the pres- ent, coupled with due introspection, is neces- sary in any field of science. The study of heteromyid evolution is no exception and 'From the symposium "Biology of Desert Rodents," presented at the annual meeting of the American Society of Mammalogists, hosted by Brigham Young University, 20-24 June 1982, at Snowbird, Utah. 'Moore Laboratory of Zoology and Department of Biology, Occidental College, Los Angeles, California 90041. •Museum of Zoology and Department of Zoology and Physiology, Louisiana State University, Baton Rouge, Louisiana 70893-3216. Great Basin Naturalist Memoirs No. 7 through this reflection of the present to the past we hope to gain a profitable avenue for further investigations. The evolution of the Heteromyidae (kan- garoo rats, pocket mice, and their allies) is closely associated with that of the Geo- myidae (pocket gophers) and, consequently, tlieir taxonomic histories are necessarily in- tertwined. Together these two families form an internally cohesive superfamily (the Geo- myoidea) whose members are miited by the presence of externally opening, fur-lined cheek pouches (among other features). Geo- myoid rodents underwent major phyletic radiation from the Oligocene to Pliocene of North America, in step with the global trend toward a cooler and drier climate (Flint 1971) and the diversification and migration of geofloras (Axelrod 1950, 1958, 1976). His- toric biogeographic considerations have been presented elsewhere (e.g.. Wood 1935, Reeder 1956, Genoways 1973, Hafner, J. C., 1981a) and will not be repeated here; for general reviews see Stebbins (1981; coe volu- tion of grasses and herbivores), and Cole and Armentrout (1979; Neogene paleogeog- raphy). It is interesting to note, however, that heteromyids and geomyids represent two of the three families of living mammals autoch- thonous in continental North America (the third being Antilocapridae). As a con- sequence of the similarities in heteromyid and geomyid biogeographic histories and their intimate phyletic relationships, we have found it illuminating to include relevant geo- myid information in this review of the Heter- omyidae. Indeed, in order to appreciate fully the history of evolutionary diversification within the Heteromyidae, it is necessary first to view this family within the broader frame- work of the superfamily Geomyoidea. Review of Geomyoid Systematics The taxonomic history of the Geomyoidea began with the description of the "tucan" or "Indian mole" (probably a pocket gopher, Tliomomys) by Fernandez in 1651. According to Merriam (1895:201), both Fernandez and, later, Kerr (1792, not seen) believed the tu- can to be a large, aberrant species of mole {Sorex mexicantis Kerr 1792). Systema Na- turae (Linnaeus 1758) did not mention geo- myoids, and it was not mitil 1848 that Water- house recognized the Saccomyina ( = modern Geomyoidea) as a distinct group of New World rodents (Waterhouse 1848). In 1872, Gill recognized two closely related families within Waterhouse's Saccomyina, the Geo- myidae ( = modern Geomyidae) and the Sac- comyidae (= modem Heteromyidae). Gill (1872) imited these families under the super- familial nomen, Saccomyoidea. Weber (1904), recognizing that Saccomys Cuvier 1823 was a junior synonym of Heteromys Desmarest 1817 (see Gray, 1868 for details), first used the superfamily name Geomyoidea. The phyletic position of the Geomyoidea within the order Rodentia has long been a matter of debate. Coues (1877) considered the geomyoids to be "myomorphs" {sensii Brandt, 1855). However, Miller and Gidley (1918) and many recent workers place the geomyoids near, or within, the "sci- uromorphs" (e.g., Simpson, 1931, 1945). Most recently. Wood (1965:128) suggested that the muroid and geomyoid rodents may have shared a common ancestor within the primi- tive, protrogomorphous rodent family Sciura- vidae, and he thus placed the Geomyoidea within the suborder Myomorpha (see also Wood 1955, Wahlert 1978). Rodents of the family Eomyidae represent a third, wholly extinct group of geomyoid ro- dents present from late Eocene to Plio- Pleistocene in Europe and North America. According to Wilson (1949a, 1949b), who first placed the eomyids within the Geo- myoidea, the eomyid skull shows many sim- ilarities to both primitive heteromyids and cricetids. Wood (1955) concurs with Wilson in recognizing the Eomyidae as a primitive geomyoid group, perhaps ancestral to the Heteromyidae. However, none of the known eomyid forms appears to be directly ancestral to living geomyids or heteromyids (Wahlert 1978). The phyletic propinquity of geomyids and heteromyids, and the fact that both groups evolved imder similar environmental condi- tions in western North America, may account for the remarkable level of evolutionary par- allelism in the two groups as evidenced in the fossil record. Due, in large part, to the con- founding effects of parallelism, the taxonomy of extant geomyids has vacillated between a 1983 Biology of Desert Rodents single family classification (either the Sacco- myidae, Geomyidae, or Heteromyidae; Baird 1858, Cams 1868, Gray 1868, Alston 1876, Shotwell 1967, Lindsay 1972) or a classifica- tion composed of two families equivalent to the modem Geomyidae and Heteromyidae (Gill 1872, Cones 1877, Merriam 1895, Wood 1931, 1935, Rensberger 1971, 1973). Recent- ly, M. S. Hafner (1982) used biochemical evi- dence to demonstrate that the extant genera commonly placed in the separate families do indeed represent inclusive, monophyletic lineages, thus supporting the traditional two- family classification. Pocket Gophers: Family Geomyidae For almost a century, Merriam's (1895) monograph on the Geomyidae has stood as the definitive statement on systematic rela- tionships among extant members of the fam- ily. Merriam's work has been modified to varying degrees by Hooper (1946), Russell (1968), M. S. Hafner (1982), and Honeycutt and Williams (1982). Living geomyids are represented by five genera (six according to Honeycutt and Williams 1982), and 33 nomi- nal species, all of which are fossorial herbivores. Within early geomyids ( = Geomyinae of Shotwell 1967, and Lindsay 1972), there was a Miocene radiation in western North Ameri- ca of forms that ranged from semi-ricochetal to fossorial in habitus as inferred from both cranial and postcranial structure (Rensberger 1971, Munthe 1975). These forms are as- signed to the geomyid subfamilies Entopty- chinae and Pleurolicinae, which appear to have been early, independent geomyid side- branches not directly ancestral to later geomyids. Following the radiation and eventual ex- tinction of the Miocene entoptychines and pleurolicines, there was a Pliocene radiation of geomyine pocket gophers in western North America. Most workers agree that all subsequent geomyids had their roots in this Pliocene radiation. Details are very scarce; however Shotwell (1967) and Lindsay (1972) tentatively derive all living pocket gophers directly from the Mio-Pliocene form Para- pliosaccomys. The geological time ranges of the genera Tfiomomys, Geomys, Zygogeomys, and Pappogeomys extend from the early Blancan (late Pliocene) to the Recent of both the Great Plains and southwestern United States. Orthogeomys (subgenus Heterogeomys) is known from the Rancholabrean (late Pleistocene) of Nuevo Leon, Mexico. Ortho- geomys (subgenera Orthogeomys and Macro- geomys) are known only from Recent mate- rial (Russell 1968). Kangaroo Rats, Pocket Mice and Their Allies: Family Heteromyidae The heteromyid rodents constitute a mor- phologically and ecologically diverse assem- blage of geomyids whose fossil history dates back to middle Oligocene of western North America (see review by Wood 1935). Wood arranged the heteromyids into three sub- families (Perognathinae, Dipodomyinae, and Heteromyinae) and later recognized a fourth subfamily, the Florentiamyinae, based on the early Miocene genus Florentiamys (Wood 1936). More recent, suprageneric systematic treatments of fossil heteromyids include the works of Reeder (1956) and Lindsay (1972). Living heteromyids are traditionally sub- divided into five genera and approximately 66 species. In this paper, we will recommend that a sixth genus, Chaetodipus, be recog- nized. Analyses of suprageneric relationships among extant heteromyids include Kelly's (1969) study of bacular and penile variation, Homan and Genoway's (1978) study of hair stmcture, and M. S. Hafner 's (1982) biochem- ical analysis of intrafamilial relationships. Re- sults of each of these studies, and others, will be incorporated into the following accounts. Kangaroo Rats: Genus Dipodoinys. -The 24 species of kangaroo rats currently recog- nized are spread throughout much of western North America from south central Canada to central Mexico. Fossil material referable to Dipodoinys is known from the Barstovian (late Miocene) to the Recent of western North America. The most recent diagnosis of fossil kangaroo rats is provided by Zak- rzewski (1981; see included references). The phyletic position of Dipodomys within the Heteromyidae is an area of controversy that will be addressed in the present study. Morphologically, kangaroo rats are truly bi- zarre, and they show no obvious affinity to Great Basin Naturalist Memoirs No. 7 any other heteromyid genus. Although kan- garoo rats show a gross overall resemblance to kangaroo mice (Microdipodops), Wood (1935) and J. C. Hafner (1978) attributed shared features such as inflated auditory bul- lae and elongated hind feet to evolutionary convergence. In contrast, Reeder (1956) in- terpreted the fossil evidence to suggest a true phyletic link between Dipodomys and Micro- dipodops, the same conclusion reached by M. S. Hafner (1982) using biochemical evidence. It is hoped that our reanalysis of Wood's (1935) data, as well as new information pres- ented herein, will clarify this issue. Relative to other heteromyids, kangaroo rats have received considerable attention from systematic biologists. Studies of inter- specific relationships based on morphology include the works of Grinnell (1921, 1922), Wood (1935), Burt (1936), Setzer (1949), Lidicker (1960), Kelly (1969), Best and Schnell (1974), and Schnell et al. (1978). Phylogenies resulting from these analyses are far from concordant (see Schnell et al. 1978). Studies of interspecific relationships in Di- podornys based on karyology (Stock 1974) and protein electrophoresis (Johnson and Se- lander 1971) present still different pictures of kangaroo rat relationships. It is not within the scope of this study to reevaluate Dipod- ornys species relationships; we only wish to call attention to the need for a thorough, comprehensive analysis utilizing a broad spectrum of approaches. In view of the com- plexity of the situation, we suggest that chromosomal banding studies, DNA hybridi- zation, arid protein sequencing analyses may provide new insights to this old problem. Spiny Pocket Mice: Genus Heteromys.— Spiny pocket mice of the genus Heteromys are, by far, the least studied of all hetero- myids. To date, the genus has no fossil rec- ord. According to Hall (1981), Heteromys is represented by 10 Recent species ranging from southern Mexico to northwestern South America. Until very recently, Goldman's (1911) revision of Heteromys stood as the most recent taxonomic work focusing on in- terspecific relationships in the genus. Rogers and Schmidly (1982) have reevaluated inter- -specific relationships in Hall's (1981) H. des- murestiamis group (exclusive of H. gaumeri) using external, cranial, and bacular charac- ters and have recognized only two of five species recognized by Hall. Specific results of their analysis will be discussed in a later sec- tion of this paper. A comprehensive study of chromosomal and biochemical variation in the genus is now in progress (D. S. Rogers, pers. comm.). Heteromys shows close phyletic ties with spiny pocket mice of the genus Liomys (Goldman 1911, Wood 1935, M. S. Hafner 1982), and the two genera are placed together in the subfamily Heteromyinae. The relationship of the Heteromyinae to other heteromyid subfamilies remains obscure. Spiny Pocket Mice: Genus Liomys.— Five extant species of Liomys are currently recognized, ranging from northern Mexico to Panama. The fossil record of the genus ex- tends back to late Pliocene of Kansas (Hib- bard 1941). Goldman's (1911) revision of Liomys has been substantially updated by Genoways (1973), who subducted 6 of 11 spe- cies recognized prior to his analysis. As dis- cussed previously, Liomys shows its closest phyletic affinity to Heteromys, and the place- ment of these genera into the subfamily Het- eromyinae has never been seriously contested. Kangaroo Mice: Genus Microdipodops.— There are but two living species of kangaroo mice (M. megacephahts and M. pallidus), both forms restricted to the arid Great Basin region of western North America. Fragmen- tary fossil material (referred to M. mega- cepliahis) is known from late Pleistocene of Nevada (Miller 1979). The genus was de- scribed by Merriam (1891) and subsequently revised by Hall (1941) and J. C. Hafner (1981a). D. J. Hafner et al. (1979) affirmed the specific status of the two living forms us- ing morphological, chromosomal, and bio- chemical evidence. The genus Microdipodops is certainly the most problematic heteromyid in terms of our understanding of its phylogenetic affinities within the family. Wood' (1935: 107-1 17) dis- eased at length the morphology of Micro- dipodops relative to Dipodomys and Pe- rogruithus (subgenus Perognathus). Although he pointed out a close morphological resem- blance between Microdipodops and Pe- rogmithus (see also J. C. Hafner 1976. 1978), Wood remained equivocal as to its phyletic placement (see Wood 1935:78). Both Reeder 1983 Biology of Desert Rodents (1956) and Lindsay (1972) derived Micro- dipodops and Dipodomys from the Mio- Pliocene form Cupidinimtis and, thus, suggest dipodomyine affinities for kangaroo mice. In contrast, J. C. Hafner (1976, 1978) derived Microdipodops from perognathine stock while recognizing the possibility that kangaroo mice may represent an independent hetero- myid lineage with no close relatives in the extant faima. M. S. Hafner (1982) assessed the phylogenetic affinities of Microdipodops us- ing electrophoretic and immunological evi- dence and concluded that kangaroo mice are genetically somewhat closer to kangaroo rats than to other living heteromyids. In this study we will reexamine the phyletic position of Microdipodops relative to other hetero- myids and introduce new evidence relevant to the issue. Pocket Mice: Genus Perognathus.— The genus Perognathus, as defined prior to this study, includes 25 nominal species spanning much of western North America from south- em Canada to central Mexico. The genus ex- hibits an vmusiially long and complete fossil record extending from Lower Miocene of western North America (Reeder 1956, Lind- say 1972). In traditional treatments dating from Mer- riam (1889), Perognathus is subdivided into two subgenera, Perognathus and Chaetodipus. For reasons detailed beyond, we recommend that CJiaetodipus be elevated to full generic status and, thus, reduce the number of extant Perognathus species to a total of nine. Species groups within the genus Pe- rognathus (sensu lato) are not clearly de- lineated using the evidence available at pres- ent. Studies of interspecific relationships based on morphology include works by Mer- riam (1889), Osgood (1900), Wood (1935), and Caire (1976). Systematic treatments based on karyology include studies by Patton (1967a, 1967b) and Williams (1978).' Protein variation in the genus (with emphasis on Chaetodipus) has been analyzed by Patton et al. (1981). It appears that a complete elucida- tion of interspecific relationships within Pe- rognathus and Chaetodipus must await future studies involving finer considerations of chromosomal evolution (banding studies) and molecular change (DNA hybridization; pro- tein sequencing). Comparative Analysis of the Male Reproductive System A large body of data concerning mor- phology of the glans penis, baculum, sperma- tozoa, and accessory glands of the male re- productive system in heteromyids is now available and may be brought to bear on the issue of phyletic relationships within the fam- ily. Much of the evidence presented here is previously unpublished; in particular, we wish to call attention to the work of Kelly (1969), which is a particularly thorough anal- ysis of penile and bacular variation in hetero- myids. Figure 1 illustrates representative phalli, bacula, and spermatozoa from eight geomyoid taxa. In the interest of brevity, we have omitted detailed descriptions of the var- ious structures in individual species; for this, we refer the reader to the original literature. Glans Penis The glans penis has been shown to be a valuable tool in systematic studies of rodents (Hooper 1961, 1962, and included references, Hershkovitz 1966, Lidicker 1968, and others) but the glans penis of heteromyids has re- ceived httle attention. Noteworthy excep- tions include Kelly's (1969) study of penile variation in Dipodomys, Genoways' (1973) study of the glans penis in Heteromys and Liomys, and J. C. Hafner's (1976) analysis of penile variation in Dipodomys, Perognathus, and Microdipodops. Following is a synthesis of the results of these studies, emphasizing salient differences in penile morphology among heteromyids. Kelly (1969) and Genoways (1973) re- ported that the glans penes of Heteromys and Liomys (Fig. 1 C, D) are similar in overall structure and share several characteristics imique among heteromyids. These features (spineless phalli; glans long relative to bacu- lar length; unique urethral lappet mor- phology) may be viewed as shared-derived characters supporting the union of these gen- era into the subfamily Heteromyinae. Out- group comparison with Thomomys (Kelly 1969) supports the derived nature of penile characters used to define the Heteromyinae. Based on outgroup comparison with geo- myids, the male phalli of Dipodomys, Micro- Great Basin Naturalist Memoirs No. 7 A DIPODOMYS B MICRODIPODOPS C HETEROMYS D LIOMYS E PEROGNATHUS F CHAETODIPUS G THOMOMYS Fii;. 1. I{c-presentative plialli, l);Kiila, and siHMiiiato/oa troiu srvoii lu-k-iomv id ami one ueoiinid t;L\a. Phalli and bacula an- shown in lateral viow. To latilitatc foniparison. all illnstiations art- drawn to different scales. Sperm from Uomijs salvini (right) and lAomtjs pictus (left) are illustrated. Sperm from Hctcwimis and Thoiuoiiit/s are as vet nn- described. (Illustrations modified from Kelly, 1969, Genoways, 197.3, and J. C. Hafner, 1976). 1983 Biology of Desert Rodents dipodops, and pocket mice of the subgenus Perognathus (Fig. 1 A, B, E) have retained a broad spectnim of primitive geomyoid char- acters. The phaUus of Thomomijs (Fig. 1 G) most closely resembles that of perognathine pocket mice (Kelly 1969), and in this and other respects (see beyond) members of the subgenus Perognathus appear to be extremely conservative morphologically. The glans penis of Microdipodops is similar in most respects to that of Dipodomys (Kelly 1969). Importantly, several phallic characters shared between Microdipodops and Di- podotnys (including morphology of urethral lappets and external spines) are unique with- in the Geomyoidea and, hence, are of phy- logenetic signficance. Those features used by J. C. Hafner (1976) to suggest a close rela- tionship between Microdipodops and mem- bers of the subgenus Perognathus (cylindrical, nonelongated phalkis; dorsal groove) are now known to be present in the geomyid genus Thomomys (Kelly 1969) and are thus re- garded as shared-primitive characters. The sharply upturned distal portion of the phallus in Dipodomys (Fig. 1 A) clearly distinguishes kangaroo rats from all other heteromyid genera. The male phallus in pocket mice of the subgenus Chaetodipus (Fig. 1 F) is unique among all geomyids examined thus far (Kelly 1969, J. C. Hafner 1976). The chaetodipine penis is long and slender, lacks urethral lap- pets, and the rim of the terminal crater forms a ventlike urethral opening. The structure of the chaetodipine phallus is, doubtlessly, de- rived within the Heteromyidae. The terminal portion of the phallus in Perognathus (CJiaetodipus) hispidus (Fig. 1 H) is markedly different from that of other chaetodipine spe- cies in possessing a distinctly ornate tip. Os Baculum Bacular variation in heteromyids has re- ceived considerable attention, including studies by Burt (1936, 1960), Schitoskey (1968), Kelly (1969), Genoways (1973), Best and Schnell (1974), and J. C. Hafner (1976). Because of considerable intrageneric varia- tion in bacular morphology, the use of this structure in delineating higher-level hetero- myid relationships is very limited. A combination of three bacular features (bulbous base, stout midregion, sharply up- turned distal end) clearly distinguishes Di- podomys species from other heteromyids (Fig. 1 A). The bacula of Microdipodops, Het- eroniys, Liomijs, Tliomomys, Geomys, and Pappogeomys also have bulbous bases, and this feature appears to be primitive for the Geomyoidea. The bacula of certain pocket mice of the subgenus Chaetodipus (Fig. 1 F) have moderately to sharply upturned distal ends (Anderson 1964), a feature which ap- pears to have been derived independently in Dipodomys and CJiaetodipus. Pocket mice of the subgenus Chaetodipus are clearly distinguished from members of the subgenus Perognathus using bacular mor- phology (Burt 1936, J. C. Hafner 1976). The baculum in chaetodipine pocket mice is long relative to body length such that the soft tis- sue of the penis terminates approximately midway along the length of the Ijaculum. In perognathine pocket mice, the baculum is much shorter and soft tissue extends approx- imately two-thirds of the length of the bacu- lum. The baculum of Perognathus (Chaeto- dipus) hispidus (Fig. 1 H) possesses an ornate, trifid tip seen nowhere else in the Geomyoidea. Spermatozoan Morphology Genoways (1973) presented a rather de- tailed study of the spermatozoa of Liomys and provided a brief statement as to the rela- tive shape of the sperm head in Perognathus pemix {Heteromys was not examined). J. C. Hafner (1976) analyzed gross sperm mor- phology in Dipodomys, Microdipodops, and additional species of Perognathus. The head and neck region (minus the acrosomal tip) of representative heteromyid spermatozoa are illustrated in Figure 1. The spermatozoa of Microdipodops (Fig. 1 B) are characteristically large, with especially long heads. The head is roughly triangular in shape, with rounded vertices. The sperm tail is of medium length relative to other hetero- myid species. Species of the subgenus Pe- rognathus (Fig. 1 E) possess spermatozoa sim- ilar in general morphology to those of Microdipodops, except that the head is small- er and the tail shorter. These similarities do 10 Great Basin Naturalist Memoirs No. 7 not indicate a close phyletic relationship be- tween Microdipoclops and Perognathus (sub- genus Perognathus), inasmuch as the sperm of certain species of Liomys also share these fea- tures (Genoways 1973). The spennatozoa of chaetodipine pocket mice are easily distinguished from those of all other heteromyids (Fig. 1 F, H). Here, the sperm head resembles a somewhat elongated isosceles triangle with acute (unrounded) ver- tices. The sperm of Perognathus {Chaeto- dipus) hispidus is peculiar in some respects because the tail is very long and the neck re- gion is not discernible. In Dipodomys, the spermatozoan head ap- proximates an equilateral triangle (Fig. 1 A) and this feature alone distinguishes kangaroo rat sperm from that of other heteromyids; the apex of the sperm head is rather acute and the tail long. Accessory Glands of the Male Reproductive Tract With the exception of Gunther's (1960) de- scription of the male reproductive tract in Thomomys, no studies of geomyoid reproduc- tive tract morphology have appeared prior to this analysis. The descriptions below are taken from M. S. Hafner (1979). The male ac- cessory reproductive gland complements of 11 geomyoid genera are listed in Table 1. Mi- crotus is included in Table 1 to represent the most common muroid (outgroup) condition, i.e., all gland complements present (Arata 1964). Loss of glandular complements appears to be much more widespread among geomyid than among heteromyid taxa. Patterns in loss or retention of gland complements agree in general with patterns seen in muroid rodents (Arata 1964); for example, it is not uncom- mon to find the preputial glands absent in taxa representing either group of rodents (geomyoids or muroids), whereas the bulbo- urethral glands are present thus far in all mu- roid and geomyoid taxa examined. By far the most striking changes in the male reproductive tract of geomyoid rodents involve changes in the morphology of the ve- sicular glands (seminal vesicles). In the large majority of geomyoids (and in rodents in gen- eral), the vesicular glands are elongate, hook- or cane-shaped, translucent structures. In contrast, most specimens examined thus far of the genus Thomomys (subgenus Mega- scapheus) have tubular, translucent vesiculars (J. L. Fatton, pers. comm.), and all specimens Table 1. Male accessory reproductive gland complements in 14 geomyoid taxa (+ indicates gland complement present). Micwtus is representative of the typical nuiroid condition (Arata, 1964). Terminology as per Arata (1964). Taxa examined Tlxomomijs bottae Thomojmjs umbriniis Geomijs hursarius Ztjgogecmiijx trichopus O. (Orthogeotnys) grandis O. {Macrogeomys) heterodus rappogeoiny.s gymnurus lU'tcnmiys dcsinarc.stianus Liomys pictits Pcrogiiatit us s))iii(itus Perognathus parvus Mi( n nlipodops megm cph a I us Dipixloiuys ordii Dipodomys merriami Microtus sp. Gland complements' vmp vlp ap dp bu urlral;7'="p;;prial.° '"""°"'"'"'' P™"'"'^^ ''■P = -«"»^°''""''> prostate: ap = anterior prostate; dp = dorsal prostate; a =^;;;pullary; bu = bulbo' 'Numbers refer to shape of vesicular gland complement: (1) elongate; (2) round; and (3) short, tubular preplltia''^"n." '''""" "' '"'"""' ""'"'' '" ''*"'"'''* "" ''"""" '" ''""^'"" ''" '" '^'^ ''"'^^"'^'' °' '"^g" -"-'" '^ "^ -'"«''- '--- -^ '«' - 'he 1983 Biology of Desert Rodents 11 examined belonging to the subgenus Chaeto- dipus of the genus Perognathiis have round, smooth, yellow- to gray-colored vesicular glands (pinkish and granular in appearance in fresh specimens). The morphologies of the re- spective vesicular glands in Thonioinys and Chaetodipus are unique among those de- scribed thus far for rodents. This unusual ve- sicular morphology in the subgenus Chaeto- dipus is particularly striking in that all specimens examined belonging to the sub- genus Perognathus have more typical rodent vesicular glands. Typical Perognathus and Cliaetodipus male reproductive tracts are contrasted in Figure 2. Among the heteromyid genera examined (Table 1), Heteromys shows an unusually high level of evolutionary loss of glandular com- plements (4 of 8 glands are absent). In con- trast, all glandular complements are present in Perognathus parvus (subgenus Pe- rognathus). In Heteromys and Microdipodops, the absence of ventromedial prostates is cer- tainly a derived condition; however, it would be dangerous to link these two genera phy- logenetically based solely on the absence of a single gland complement, especially when loss of ventromedial prostates is seen in the outgroup (Geomyidae). Similarly, the pres- ence of preputial glands in Perognathus par- vus and Microdipodops should not be used to infer a special phylogenetic relationship; the genera have merely retained a gland com- plement normally present in nongeomyoid rodents. A conservative assessment of the data re- viewed above leads to five conclusions: 1. Lioinys and Heteromys show close phy- logenetic relatedness based primarily on morphology of the glans penis. 2. Dipodomys and Microdipodops are also suggested to be phylogenetically allied, again based largely on morphology of the glans penis. 3. Pocket mice of the subgenus Chaeto- dipus show only remote morphological similarities to species of the subgenus Perognathus. All aspects of the male re- productive system support this conclusion. 4. Within Cliaetodipus, P. (Chaetodipus) hispidus is unique with respect to mor- phology of the glans penis, baculum, and spermatozoa. 5. Species of the pocket mouse subgenus Perognathus show extreme morpho- logical conservatism with respect to the male reproductive system. Biochemical Variation Analyses of intrapopulation protein varia- tion in Microdipodops (D. J. Hafner et al. 1979) and Perognathus, subgenus Chaetodipus (Patton et al. 1981), have revealed levels of genetic polymorphism and heterozygosity approximately equivalent to averages sum- marized for 46 species of mammals by Nevo (1978). In contrast, the average values of polymorphism and heterozygosity measured in populations of Dipodomys (Johnson and PEROGNATHUS CHAETODIPUS Fig. 2. Ventral (left) and dorsal (right) views of the male reproductive tracts of Perognathus (Perognathus) longimembris and P. (Chaetodipus) spinatus. The urinary bladder (b) has been excised to reveal underlying acces- sory gland complements. Abbreviations as per Table 1 with following additions: caput epididymis (cap); cauda epididymis (cau); testis (t); vas deferens (vd). 12 Great Basin Naturalist Memoirs No. 7 Selander 1971, Patton et al. 1976) are only half as large as those measured in most mam- malian populations. Johnson and Selander (1971) suggest that a combination of phyloge- netic and ecological factors may explain de- pressed levels of intrapopulational genetic variation in kangaroo rats relative to other mammals. Indeed, future genetic analyses of kangaroo rat populations may find a causal Unk between ecological amplitude (niche width) and genetic variation, but a clear con- nection was not evident in Johnson and Se- lander 's (1971) study. Interpopulation genetic differentiation in Dipodoniys and Perognathiis {Chaetodipus) has been shown to be approximately com- mensurate with values measured between populations of other rodents, and mammals in general (Johnson and Selander 1971, Csuti 1979, Patton et al. 1981). Genetic studies at the intra- and interpopulation level are cur- rently in progress for the genera Lioniys and Heteroniys (D. S. Rogers, pers. comm.). Estimates of interspecific protein differen- tiation within the three heteromyid genera thus far examined {Micwdipodops, Di- podomys, and Perognathiis, subgenus Chaeto- dipus) reveal two divergent patterns. First, Micwdipodops megacephahis and M. pallidus, which are sibling species on morphological criteria (D. J. Hafner et al. 1979), are ge- netically differentiated at the appropriate "sibling species level" as defined by Zimmer- man and Nejtek (1977) based on data from 10 species of mammals. Similarly, genetic dis- tances .measured between morphologically well-differentiated species of Dipodomys (Johnson and Selander 1971) are approx- imately equivalent to those measured be- tween well-differentiated species in other mammalian taxa (Zimmerman and Nejtek 1977). In Perognathiis, on die other hand, Sarich (1975), M. S. Hafner (1979, 1982), and Patton et al. (1981) have shown that the ge- netic distance measured between perog- nathine and chaetodipine pocket mice is ex- tremely large, in fact larger than that mea- sured between Lioniys and Heteroniys. Clearly, the rate of exomorphologic change between Perognathiis and Chaetodipus has lagged far behind that of biochemical change. Moreover, all indications from com- parative rate tests suggest that protein evolu- tion has proceeded at the same rate within the perognathine and heteromyine lineages. Thus, due to extreme exomorphological con- servatism, Perognathiis and Chaetodipus are, in a sense, "cryptic genera." Studies of albumin (M. S. Hafner 1982) and transferrin (Sarich 1975) immimology in het- eromyids show Microdipodops to be extreme- ly conservative with respect to rate of pro- tein change through time. In immunological comparisons with nonheteromyid outgroups, Microdipodops shows consistently lower lev- els of protein change relative to other hetero- myids. According to Sarich (pers. comm.), the high degree of protein conservatism seen in Microdipodops is unique among taxa thus far examined immimologically belonging to sev- eral different mammalian orders. At present, we have no explanation, or even hypotheses, to accomit for extreme protein conservatism in Microdipodops. Karyotypic Evolution Chromosomal Variation Heteromyid and geomyid rodents have at- tracted a great deal of attention from evolu- tionary biologists and systematists. Interest in these rodents stems, among other reasons, from the great degree of chromosomal varia- tion across the group. Whereas karyotypic in- fonnation has been applied commonly to questions at the species level, such informa- tion has not been used adequately in assessing evolutionary relationships at higher levels. Further, the fusion paradigm of karyotypic reorganization has been invoked to the near exclusion of other possible mechanisms that alter diploid number (e.g., Thaeler 1968, Davis et al. 1971, Genoways 1973, Selander et al. 1974, Stock 1974, Williams and Gen- oways 1975, Williams 1978). The Rob- ertsonian fusion model (Robertson 1916), whereby the karyotype is reduced in diploid number through the joining of uniarmed chromosomes to form biarmed elements, has reigned as the predominant view in inter- pretations of geomyoid chromosomal evolu- tion despite there being no convincing argu- ment to support its occurrence. In geomyoid studies, empiricism has lagged well behind theoretical considerations; and other hypoth- 1983 Biology of Desert Rodents 13 eses, alternative to the fusion paradigm, have not been seriovisly considered (see also Imai and Crozier 1980). Diploid numbers are now known for repre- sentatives of all genera and subgenera within the Geomyoidea (Heteromyidae: Dipodomys, Cross 1931, Matthey 1952, 1956, Csuti 1971, Dingman et al. 1971, Fashing 1973, Stock 1974; Microdipodops D. J. Hafner et al. 1979, J. C. Hafner 1981a; Chaetodipus, Patton 1967a, 1969, 1970; Perognathus, Patton 1967b, Williams 1978; Liomijs, Genoways 1973; Heteromys, Genoways 1973, A. L. Gardner, pers. comm., D. S. Rogers, pers. comm., M. S. Hafner and J. C. Hafner, un- publ. data; Geomyidae: Geomys, Davis et al. 1971, Baker et al.' 1973, Selander et al. 1974, Williams and Genoways 1975, Hart 1978, Honeycutt and Schmidly 1979; Pappogeomys, Laguarda-Figueras et al. 1971, Berry and Baker 1972, Hart and Patterson 1974, Smolen et al. 1980, Honeycutt and Williams 1982; Thomomys, Thaeler 1968, 1972, 1973, 1974a, 1974b, 1976, 1977, 1980, Thaeler and Hinesley 1979; Thornomys, subgenus Mega- scapheus, Patton and Dingman 1968, 1970, Patton et al. 1972, Patton 1973, 1980, Patton and Yang 1977, Patton and Feder 1978, J. C. Haftier et al. 1983; Orthogeomys, M. S. Haf- ner 1979, M. S. Hafner and J. C. Hafner, un- publ. data; Zygogeomys, M. S. Hafner, 1979, M. S. Haftier and J. C. Hafner, unpubl. data). Figure 3 summarizes the chromosomal var- iability for geomyoid species. If Robertsonian chromosomal events (fusion and/ or fissions) were chiefly responsible for effecting diploid number change in the six major groups of the Geomyidae, the dots representing karyotypes within a species and species within the major groupings would be expected to be aligned in vertical patterns. It can be seen (Fig. 3A) that this does not appear to be the general case. In the Heteromyidae (Fig. 3B), a similar situ- ation exists. Within the major heteromyid groups, karyotypes are not, for the most part, aligned in vertical arrays. Lacking G- and G- banding information for most groups in the Geomyoidea, it is premature to speculate on the specific mechanisms, or actual mechan- ics, of chromosomal rearrangement. More- over, even banding data will not allow us to assess directionality of change, vis-a-vis the fusion /fission controversy. Directionality in Chromosomal Evolution Geomyoid karyotypic data do warrant a close evaluation of directionality of chromo- some number change within the superfamily, irrespective of the mechanism(s) that may be involved in the change (J. C. Hafner 1981b). The Geomyoidea, with its high degree of diploid number variation and doubtless monophyletic origin, is an appropriate group in which to examine polarity in diploid num- ber change. Are high numbers primitive with a general reductional trend, or are low num- bers primitive with an increasing trend? If no general trend is discernible, we must consider tlie possibility that both trends operate, but in separate geomyoid lineages or at different times in the history of a single lineage. In this analysis we have considered 12 ma- jor taxonomic groups (genera and subgenera listed above). Note that we include both sub- genera within the genus Thomomys (Tho- momys and Megascapheus, sensu Thaeler 1980) as well as the subgenera Chaetodipus and Perognathus of the genus Perognathus. A histogram plot of species numbers versus diploid numbers (including intraspecific chromosomal variation) reveals that the dis- tribution of geomyoid karyotypes is rather trimodal and seems to exhibit a damped os- cillatory pattern (Fig. 4). Therefore, the array of diploid numbers can be trisected into chromosomal subgroups or character states: low chromosome numbers (2n = 34-50), me- dium numbers (about 60), and high diploid numbers (68-88). Invoking the criterion of character state distribution, we first attempt to assign po- larity by using in-group analysis. According to the criterion of in-group analysis, the char- acter state that occurs most frequently within the group under study (the common state) is considered to be the primitive state (Stevens 1980:335-37, Criterion lA). The low chromosome number character state contains 47 karyotypes, the medium state 44 karyo- types, and the high number state has 27 kar- yotypes (Fig. 4). Although the evidence may not be strong, the criterion of in-group analy- sis would lead to the conclusion that lower chromosome numbers (2n = 34-64) are primitive and higher numbers (2n > 64) are derived, which is contradictory to earlier 14 Great Basin Naturalist Memoirs No. 7 GEOMYIDAE MEGASCAPHEUS ORTHOGEOMYS ZYGOGEOMYS PAPPOGEOMYS • n = 1 • n = 2 • n = 3 n = 4 60 80 HETEROMYIDAE 100 120 ARM NUMBER 140 / \^ DIPODOMYS / ' LIOMYS HETEROMYS \ • • - ''•••) \ / / •• \ 1^ ^ \ ■■ UJ Z50- ••-'^'^^^ "' >^ g -— ^""^ROf^NATHUS C» . ^ X MICRODIPODOPS ii: \,^''' CHAETODIPUS S^ n =4 m n=5 B ARM NUMBER 140 Fig. 3. (Jhromosonial variation in the Geomyoidea: A, Geoinyidae; B, Heteioniyidae. See text for data sources. Dashed lines represent the karyotype bounds; n = number of karyotype.s. Odd diploid numbers have been omitted for claritN'. 1983 Biology of Desert Rodents 15 published opinions. To view tliis in-group analysis at a higher taxonomic level, we next examine the num- ber of major geomyoid groups versus diploid numbers (Fig. 5). Again, the criterion would maintain that the most common character state across the major groupings is primitive. The low chromosome nvmiber character state contains 10 of tlie 12 major geomyoid taxa. In comparison, the medium character state contains 8 of the major taxa and the high chromosome number state contains only three major taxa {Dipodomys, Geomys, and Megascapheus; Fig. 4). The conclusion to be drawn from this refined in-group treatment, once again, is that the lower diploid numbers are primitive and the higher character state derived. Such evolutionary polarity, assigned by in- group analysis must be confirmed using other criteria. We therefore must consider out- group analysis (see Stevens 1980:337-340, Criterion IB). Following the out-group meth- od, the character state that is shared with the out-group is taken to be primitive. It has been suggested by some workers that the mur- ids stand as a distant sister group to the Geo- myoidea. The range of diploid numbers in the Muridae (Fig. 6A) is almost entirely with- in the low diploid number character state de- fined earlier; the mode for the Muridae is 2n = 48. Selecting another out-group for com- parison, the Cricetidae, again we see that the vast majority of cricetid karyotypes fall into the low chromosome number character state (mode: 2n = 48; Fig. 6B). Further, out-group comparison with the Sciuridae (Fig. 6C; mode: 2n = 38) and the Aplodontidae (2n = 46; Matthey 1973), two families commonly believed to represent primitive rodents, again corroborates the earlier assigned polarity. Thus, all out-group comparisons indicate that the low character state is primitive. One other criterion that can be used to de- termine the polarity of character states is that of correlation among character states (Stevens 1980:345-348, Criterion 5). This ar- gument is based on the assumption that primitive character states frequently occur together. As Stevens (1980) aptly noted, the criterion of correlation should be used in combination with other criteria (e.g., in- group and out-group analyses) as has been done here. One morphological character whose char- acter state polarity is reasonably well sup- ported is that of sulcation in the upper in- cisors. It seems that grooved upper incisors is 12- WlO- O UJ 8- co uj 4- OQ g2H LOW -^ MEDIUM I r 30 K K HIGH 40 50 60 DIPLOID NUMBER F F F 70 80 90 Fig. 4. Frequency distribution of the chromosome numbers in the Geomyoidea. The distribution is triniodal and skewed to the right. Odd diploid numbers have been omitted for clarity. Geomyidae: A, Zygogeomys; B, Ortho- geomys; C, Geomys; D, Pappogeomys\ E, Thoniomys; F, Megascapheus. Heteromyidae: G, Chaetodipus; H, Pe- rognathiis; I, Microdipodops; J, Heteromys; K, Liomys; L, Dipodomys. 16 Great Basin Naturalist Memoirs No. 7 plesiomorphic for groups within the Geo- myoidea, with loss of a sulcus being the de- rived state (see Merriam 1895, Wood 1935, Russell 1968). Within the Geomyidae, only one extant group totally lacks sulci in the up- per incisors. This is the smooth-toothed pock- et gophers, which include Thomomys and Megascapheus. Interestingly, pocket gophers of the subgenus Megascapheus have the high- est diploid numbers in the superfamily (Fig. 4), and Megascapheus is a major taxon that is entirely restricted to the high diploid number character state. Although it cannot be dem- onstrated that this instance of character state correlation is not due to chance alone, it is nevertheless in accord with the aforemen- tioned polarity and the general trend for in- crease in chromosome number. Within the Heteromyidae, kangaroo rats (Dipodomys) display a surfeit of derived mor- phological characters. Kangaroo rats are gen- erally large in body size, have large eyes, long hind feet, expanded auditory bullae, a middorsal sebaceous gland, a long tail, and elaborate pelage markings; doubtless, kan- garoo rats are the most morphologically de- rived members of the Heteromyidae (see beyond). Correlated highly with the derived nature of these characters is the high diploid numbers of Dipodomys. Kangaroo rats are distributed chromosomally in the medium and high diploid number character states and exhibit the highest diploid number for the Heteromyidae. This correlation criterion again supports our initially assigned polarity. We shall argue beyond that Microdipodops, which exhibits relatively low diploid numbers (2n = 40,42), is much less derived morpho- logically than is Dipodomys. Further evidence that can be used to sup- port this mode of directionality comes from recent information on Thomomys bottae pocket gophers in Colorado (J. C. Hafner et al. 1980, J. C. Hafner et al. 1983). Through- out its extensive range, T. bottae is known to have, almost without exception, 76 chromo- somes. However, a chromosomal race of T. bottae recently discovered in Colorado had 88 chromosomes (the second highest known for the Mammalia); yet allozymically it is nearly identical with the parental 2n = 76 form. Clearly, this anomalous race, character- ized by a diploid number of 88, is derived from the common 2n = 76 form. Had the 88 chromosomal race been primitive, one would have expected its level of genie divergence to be equal to or greater than levels of major protein differentiation seen within the 2n = O §6- CD CC o < F. 4- o Li- o 0:2- 30 V 50 V DIPLOID NUMBER Fig. 5. Number of genera or subgenera versus diploid number. XuMibers above lirackets indi taxa represented in the three chromosomal character states. ijor 1983 Biology of Desert Rodents 17 2n = 48 CO LU ^20 CO a: 10 DIPLOID NUMBER Fig. 6. Frequency distributions of diploid numbers for out-group comparisons: A, Muridae; B, Cricetidae; C, Sciu- ridae. Data are taken from Hsu and Benirschke (1967-1977) and Matthey (1973). Modal numbers are indicated in the figures. 18 Great Basin Naturalist Memoirs No. 7 76 form; this is not the case (see Patton and Yang 1977, J. C. Hafner et al. 1983). Impor- tantly, this study represents the only thor- oughly documented (chromosomal, allo- zymic, morphologic) demonstration of chromosomal directionality in the Geomyoidea. In view of the foregoing, it seems that there is certainly ample justification for an alternative viewpoint with respect to the di- rection of chromosomal number change in the Geomyoidea. Several statements in the literature claiming high diploid numbers to be primitive for particular heteromyid groups and for the entire Geomyoidea (e.g., Williams 1978:605) are without support. We fully realize that reductional trends may in- deed have occurred in specific geomyoid lineages; however, arguments used to support the diploid number reductional trend are weak and commonly utilize general bio- geographical and ecological explanations (e.g., Williams and Genoways 1975). As pointed out by numerous authors, such rea- soning is fraught with problems of circularity and is inadiuissible in the assignment of po- larity to character states. In contrast, in- group and out-group analyses and correlation among character states support an alternative view that low diploid numbers seem to be primitive for the Geomyoidea, and the over- all direction of karyotypic change has been that of increase in chromosome number. We shall not speculate on the mechanism of in- creased numbers at this time, but will men- tion that fission may be involved, as well as other mechanisms such as chromosome dupli- cation and addition of euchromatin or heter- ochromatin to centromeric fragments. A full discussion of karyotypic interconversions within the Geomyoidea must await the time when more karyotypes have been banded and we have a more firm understanding of the complexities of chromosomal evolution. MoRl'HOLOCICAL EvOLUTION (^ladistic Analyses of Heteromyid Relatioaships A prominent issue in the study of hetero- myid relationships is the question of the sub- familial affinity of kangaroo mice. Since Mer- riam's (1891) description of Micwdipodops there has been much controversy as to whether kangaroo mice are most closely re- lated to kangaroo rats or pocket mice (for re- view see J. C. Hafner 1978, M. S. Hafner 1982). Kangaroo rice are phenetically most similar to pocket mice (J. C. Hafner 1978), yet biochemical data indicate that they are somewhat more closely related to kangaroo rats (M. S. Hafner 1982). One might therefore hypothesize that Micwdipodops, although being a cladistically old group, is patristically primitive and the similarities it shares with pocket mice are actually symplesiomorphous. Thus, it is necessary to perform a cladistic study in which shared-derived characters (hy- pothesized on the basis of out-group com- parisons) are used to unite taxa. Accordingly, herein we evaluate this central issue in heter- omyid phvlogeny by analyzing the phenetic data of Wood (1935) and J. C. Hafner (1978), using cladistic procedures. Wood (1935) revisited.— Fifty-three characters were used by Wood (1935) in his treatment of the evolutionary relationships of kangaroo mice. Wood (1935:108) tabulated the character-state distribution for each of these characters across the heteromyid gen- era and concluded that kangaroo mice were most closely related to pocket mice. It is these tabulated data (Wood 1935:108) that are available for the present cladistic analy- sis; we have made no effort to reexamine Wood's characters and, for present purposes, accept his selection of characters and his in- terpretations concerning character ho- mologies. In our analysis of Wood's data, the Heterominae (Liomijs and Heteromys) was chosen for out-group comparison because most authors agree that it is an evolutionarily independent lineage quite removed from Pe- rognathus, Micwdipodops, and Dipodomys. Gonsequently, characters shared with Liomys and Hetewmys (see Wood 1935:108) are hy- pothesized to be primitive. Ten of Wood's original characters were omitted from the analysis (all three genera shared seven char- acters with the out-group and three other characters were ambiguous), reducing the to- tal number to 43 characters (Table 2). Tlie three possible phylogenetic hypoth- eses, showing the apportionment of the 43 morphological characters, are presented in 1983 Biology of Desert Rodents 19 Table 2. Characters used in our reanalysis of Wood (1935). Ten of the 53 characters listed by Wood (1935:108) have been omitted in the reanalysis (see text). Wood's Character (1935) number ordering Description of feature 1 1 Locomotion ricochetal 2 5 Protoloph of P* unites between hypocone and metacone. 3 7 Upper molars do not surround central lakes 4 8 Playa lake in metaloph of P* absent 5 9 Check teeth hypsodont 6 10 Occlusal pattern not elongated with crown 7 11 Teeth unrooted or form roots late in life 8 13 Bases of upper molars in orbit 9 14 Zygomatic process of Mx. expanded 10 15 End of palate not behind M^ 11 16 Pits in basioccipital absent 12 17 One pair of pterygoid fossae 13 18 Pterygoid fossae reach endocranium 14 19 Masseter separated from lOF by crest 15 20 Orbit overhung by frontal 16 21 Ethmoid foramen absent 17 22 Incipient postorbital process 18 23 Temporal fossa not distinct 19 24 Alisphenoid canal anterodorsad 20 25 Bulla extends anterad of glenoid 21 27 Squamosal perforated by bulla 22 28 Lacrymal expanded not free of Mx. 23 29 Parietal between squamosal and mastoid 24 31 Paroccipital process not latero- caudad 25 33 Knob for pulp cavity at lower edge of ascending ramus 26 34 Pit by M3, no foramen on condyloid 27 35 Cervical vertebrae fused in part 28 .36 No median ventral foramen in caudals 29 37 Notch in transverse process of caudals gently curved ,30 38 Tail tufted 31 .39 Scapula prolonged posteriorly .32 40 End of acromion not expanded .33 41 Short supinator crest 34 42 Deltoid crest ends steeply 35 43 Articulation of trapezium and scapholunar 36 44 Triangular obturator foramen 39 47 Process of pubis at front of ob- turator foramen 40 49 Cnemial crest ends at gentle slope 41 50 External and internal malleoli do not reach same level 42 51 No astragalo-cuboid contact 43 53 Metatarsal IV not the longest Figure 7A-C. Six derived characters unite Perognathus with Microdipodops (Fig. 7A), nine characters unite Perognathus with Di- podomijs (Fig. 7B), and the Microdipodops- Dipodomys association is supported by 12 synapomorphies (Fig. 7C). Hence, the tree topology in Figure 7C is most parsimonious and contradicts the concUision proferred by Wood (1935). It is interesting to note that the miu-ineUke Perognathus is lacking an autapo- morphic descriptor; we view this to be a problem not in the analysis or with the taxon, per se, but in the nature and breadth of the characters analyzed. It is possible that the association of Micro- dipodops with Dipodornys (Fig. 7C) is in- correct because the analysis does not recog- nize possible parallelisms associated with the ricochetal mode of locomotion; the apo- morphies used to imite the two taxa may be independently derived characters. To eval- uate this possibility, we remove all those fea- tures in the analysis that are shared with the distantly related bipedal form, Jacuhis (Fig. 7D-F; see Wood 1935:107-109). It can be seen in this refined analysis, controlling for ricochetal habitus characters (Fig. 7D-F), that there is still stronger support for the Mi- crodipodops-Dipodomys phylogenetic hy- pothesis (Fig. 7F) than the other two possi- bilities. However, problems exist. If the presumed synapomorphic characters uniting kangaroo mice and kangaroo rats are to be believed, then the others must be misleading. As Wood (1935) himself observed, however, parallelism is the evolutionary motto of heteromyids. Reanalysis of Hafner (1978).— In an at- tempt to resolve the Microdipodops con- troversy, J. C. Hafner (1978) compared the two kangaroo mouse species with three spe- cies of kangaroo fats and four species of pocket mice (two species each of the sub- genera Perognathus and Chaetodipus), using phenetic clustering and ordination pro- cedures. Hafner (1978) concluded that Micro- dipodops is most closely related, phenetically, to pocket mice and adduced a broad spec- trum of phenetic characters with assumed overall genotypic representation. Here we reanalyze Hafner's (1978) data hypothesizing shared-derived characters, using out-group comparison with Liomys and Heteromys (het- 20 Great Basin Naturalist Memoirs No. 7 eromyine data from Genoways 1973). A total of 17 characters was available for cladistic analysis (Table 3) after paring down Hafner's (1978:363-364) data matrix of 40 characters (quantitative characters were omitted from our analysis as well as those characters with indeterminable character-state polarity). Throughout our analysis, we have accepted as a working hypothesis that Perognathus and Chaetodipus form a clade relative to the other lineages; this assumption is supported by biochemical evidence (e.g., Sarich 1975, M. S. Hafner 1982). Figure 8 shows the three phylogenetic hy- potheses with the 17 characters (Table 3) ap- portioned among them. The results of this analysis, in accord with our above treatment of Wood's (1935) data, suggest that the most parsimonious phylogenetic hypothesis is that which links Microdipodops and Dipodomys as a clade independent of the Perognathus- Clmetodipus clade (Fig. 8C). However, the analysis is less than robust; the Perognathus- CJiuetodipus clade lacks an autapomorphic character, and tlie characters that define the Microdipodops-Dipodomys association (Fig. 8C) are dubious (fully haired soles of hind Table 3. Seventeen characters used in the reanalysis ot Hafner (1978). Quantitative characters (J. C. Hafner 1978:363-364) and characters whose character-state polaritv was indeterminable were omitted in our analysis. Character number (Haftier 1978) Description of feature 3 Lacrimals joined 4 Molars nonrooted 7 Morphology of Y chromosome metacentric 9 Urethral lappets absent 12 Sharply upturned morphology of l^aculum tip 13 Harsh pelage characteristics 15 Middorsal gland present 16 Soles of hind feet (naked, a; fullv haired, b) 17 Crested tail present 18 Flank stripes present 21 Locomotion: partially bipedal to fulh bipedal 31 Wliite side stripes on tail present 33 Molar wear patterns: enamel limited to anterior and posterior plates 34 Tail greater diameter in middle than at base or tip 35 Absence of median ventral foramina in caudal vertebrae 36 Astragalus-cuboid articulation present 40 Wliite ring at base of tail present REANALYSIS OF WOOD (l935) Fig. 7. Cladistic analvsis of morphological data presented by Wood (1935) for Pcw^nallius (F), MicnxliptHlops (M), and Dipodcmii/s (D). In A, B, and C, 43 of Wood's original 53 characters (see Table 2) are apportioned on the three possible trees, omitting those characters shared with Lioiiujs and lletcromijs. In D, E, and F, those characters shared with the ricochetal form Janihis (Dipodidae) are also oinittfd to remo\e features that are functionally related to bj^ pedality. Note the high number of autapomorphies on the /)i/)()(/<)»i[/,s branch and the conspicuous absence of aut- apomorphies on the Pcrofituithiis branch. 1983 Biology of Desert Rodents 21 feet and ricochetal mode of locomotion). Conclusions about the Microdipodops CONTROVERSY.— The above cladistic analyses of tlie data of Wood (1935) and J. C. Hafner (1978) are necessary exercises, yet the results are not imequivocal and provide us with only a preliminary insight to the problems of as- certaining phylogenetic relationships within the Heteromyidae using morphological char- acters. Both reanalyses demonstrate modest support for the recognition of the Micro- dipodops-Dipodomys clade; thus, they are in agreement with biochemical evidence. How- ever, the treatments are inchoate and there is a need for a detailed phylogenetic analysis wherein character homologies and character- state transformations are determined. As noted by many workers (e.g., Hennig 1966), the crux of any analysis and its attending ar- gmnents relies on the characters under study. Several others points emerge from the above analyses. Importantly, these cladistic treatments tabulate quantitatively the tre- mendous amount of parallelism in the hetero- myids. That the morphology of these rodents is rife with parallelisms is documented con- vincingly in Figure 7A-C. The analyses also provide a comparative measure of the degree of morphological divergence among the het- eromyid genera. In accord with intuition, these results document that Dipodomys is the most derived genus in terms of morphology (highest number of autapomorphic features; Figs. 7 and 8), the pocket mice are the least derived, and Microdipodops exhibits an inter- mediate number of derived features. Evolution of Geomyoid Morphotypes: An Hypothesis Tlie diversity of morphological forms, or morphotypes, within the superfamily Geo- myoidea eclipses that seen within any other mammalian group of comparable size. The evolution of forms as stnicturally divergent as kangaroo rats, pocket mice, and pocket gophers is commonly believed to be the re- sult of orthoselection; i.e., directional selec- tion acting on ancestral species favoring cer- tain adaptations which are accentuated in descendant species. The origin of each struc- tural novelty is thus explained in terms of its present day fimctional advantage to the ani- mal. Although it cannot be denied that a con- spicuous morphological feature present in a living animal may, and probably does, have an adaptive fimction today, we agree with Gould and Vrba (1982:13) that "current util- ity carries no automatic implication about historical origin." As Lewin (1982:1212) points out, "it is folly to infer without cau- tion the historical genesis of a feature from its current utility." Accordingly, we herein introduce a causal hypothesis, devoid of func- tional explanations, to account for the evolu- tionary origin of morphological diver- Fig. 8. Cladistic analysis of morphological data presented by J. C. Hafner (1978) for Pewgnathus (P), Chaetodipus (C), Microdipodops (M),' and Dipodomys (D). Cladograms A, B, and C reflect the three possible ways that Micro- dipodops and Dipodomys may be linked with the Perognathiis-Chaetodipus assemblage. Liomys and Heteromys are treated as an outgroup (data from Genoways, 1973). See Table 3 for list of characters. 22 Great Basin Naturalist Memoirs No. sification v/ithin the Geomyoidea. This hypothesis is expanded and supportive evi- dence is detailed elsewhere (J. C. Hafner and M. S. Hafner, in manuscript). Several years ago we observed that the conspicuous morphological features of adult kangaroo rats and kangaroo mice, most no- tably the large head and eyes, enlarged brain, long hind feet, and delicate, weakly fused skeleton, were traits commonly seen in the juvenile state of other animals. Further exam- ination revealed that kangaroo rats and kan- garoo mice possess many of the classical fea- tures characteristic of paedomorphic forms. This initial observation, coupled with the subsequent discovery that neonatal pocket gophers look remarkably like mature pocket mice, prompted further investigation culmi- nating in our hypothesis that geomyoid mor- phological transformations through phy- logeny may be the result of evolutionary epigenetics (for recent reviews see Gould 1977, Alberch et al. 1979, Alberch 1980, Lc^vtnip 1981a, 1981b, Rachootin and Thom- son 1981). In other words, regulatory changes in ontogeny may have affected the timing of gene action and rates of morphogenesis and growth and thus have led to morphological phyletic evolution in this group. Most authors would agree that pocket mice, including Perognothus, Liomijs, and Heteromijs, exliibit a generalized body plan and probably represent a good approx- imation of the ancestral geomyoid morpho- type (e.g., Eisenberg 1981:90). Our hypoth- esis suggests that perturbations in developmental "control parameters" in an- cestral (pocket-mouse-like) geomyoids, in- cluding changes in the time of onset of growth, cessation of development, and rate of growth, could deform the ancestral ontoge- netic pathway and effect phylogenetic trans- mutations in morphology leading to such di- verse forms as kangaroo mice, kangaroo rats, and pocket gophers. According to our hypothesis, paedomor- phosis in kangaroo mice and kangaroo rats may have originated via different kinds of de- velopmental perturbations. Hoth morphology and general life history of kangaroo mice sug- gest that they are progenetic descendants of pocket-mouse-like ancestors. Progenesis is the process whereby ontogeny is truncated and maturation is accelerated. Gould (1977) argues that the key to vmderstanding the im- mediate significance of shifts in devel- opmental timing (heterochrony) lies in the theory of r and K selection (life history strat- egies). Gould (1977:293) predicts that pro- genesis will be associated with r-strategists, and, indeed, early kangaroo mouse evolution Ls postulated to have occurred in an obvious r-selected environment (ephemeral sand-dune habitats in the Great Basin Desert; J. C. Haf- ner 1978); kangaroo mice possess many of the classical attributes of an r-strategist. It ap- pears that in kangaroo mice there has been progenetic truncation by precocious matura- tion and tliat this early maturation is the principal object of selection. That is, there has been a "redirection of selection" (Gould 1977) away from morphology, per se, and to- ward precocious maturation as a life history strategy; juvenilization may have been en- tirely incidental. Both morphology and general life history of kangaroo rats lead us to suggest that paedomorphosis in this group is the result of neoteny. Neoteny is fundamentally different from progenesis and involves retardation in growth rate resulting in juvenilization of the adult animal. According to Gould's (1977) hy- pothesis, neoteny is a common occurrence and may result from direct selection for juve- nile features and/or larger body size in envi- ronmental regimes that are more iC -selected. Indeed, kangaroo rats are all medium to large heteromyids possessing many of the classical features associated with tlie neotenic syn- drome (e.g., long life span, slow devel- opment, small litters, enlarged brain; J. C. Hafner and M. S. Hafner, in manuscript). The early evolution of kangaroo rats appears to have been confined to grasslands (Reeder 1956), and several living forms inhabit fairly stable, nondesert environments; those tliat are strictly desert-dwelling forms tend to buf- fer an otlierwise luistable environment by subsisting on a fairly stable resource (leaves) and/or utilizing large stores of hoarded food during periods of food scarcitv. Lastly, we suggest that pocket gophers may be hypermorphic descendants of a pocket-mouse-like ancestor. Hypermorphosis is a process wherein heterochronic per- turbation in ontogeny has led to a length- 1983 Biology of Desert Rodents 23 ened growth period producing a "per- amorphic" (as opposed to paedomorphic; Alberch et al. 1979) organism. The marked similarities between neonatal pocket gophers and adult pocket mice suggest that reproduc- tive maturation in pocket gophers has been retarded relative to exomorphological matu- ration, allowing for extreme development of somatic features prior to reproduction. Adult pocket gophers possess many of the classical features characteristic of late mammalian on- togeny, most notably a rugose, heavily os- sified skeleton that results from prolongation of somatic growth late in life. In summary, we suggest that many, per- haps most, of the flamboyant morphological modifications seen in heteromyids and geo- myids may have originated as incidental by- products of heterochronic shifts in ontogeny. Instead of acting separately on each mor- phological feature (e.g., large head, long legs, delicate skeleton, etc.), natural selection may have acted at the developmental level favor- ing the new life history strategy associated with a progenetic, neotenic, or hypermorphic animal. The paedomorphic traits invariably associated with these developmental changes (peramorphic traits in the case of hypermor- phosis) may have been "tolerated" by natural selection initially and subsequently modified (adapted) for fimctional purposes. On the other hand, certain novel traits may provide little or no functional improvement over the ancestral condition, but are maintained (as long as they are not deleterious) because they are developmentally mandated. Taxonomic Comments on the Heteromyidae Allen and Chapman 1893 The following is an up-to-date statement on the taxonomy of the Recent Hetero- myidae, necessarily reflecting the views and biases of the authors. We use as our point of departure Hall (1981) and included refer- ences. In the interest of brevity, those hetero- myid species recognized by Hall (1981) are not listed, except where we feel taxonomic comments are warranted. For species group- ings within each genus we again refer the reader to Hall (1981), but we hasten to add that species groupings within Dipodomys, Hetemmys, Perognathus, and Chaetodipus are suspect and in need of thorough reevaluation. Finally, we provide a synonymy for Chaeto- dipus, which we herein evaluate to full ge- neric rank. Our views on supraspecific rela- tionships within the family are summarized in Figure 9. Subfamily Dipodomyinae Coues 1875 Genus Dipodomys Gray 1841.— Hall (1981) recognizes 22 species of kangaroo rats, partitioned into six species groups following Setzer (1949; see Schnell et al. 1978, for dis- cussion of interspecific taxonomy in the genus). Best (1978) has used morphologic cri- teria to suggest that three species recognized by Hall, D. antiquarius Huey 1962, D. para- liits Huey 1951, and D. penisularis (Merriam 1907), are conspecific with D. agilis Gambel 1848. Biochemical (Johnson and Selander 1971) and morphological (Schmidly and Hendricks 1976) evidence has been used to suggest that D. compactus True 1899 (not recognized by Hall 1981) warrants full spe- cific status. Similarly, Patton et al. (1976) have used biochemical evidence to document specific status for D. californicus Merriam 1890. Genus Microdipodops Merriam 1891.— Herein, kangaroo mice are placed provision- ally in the subfamily Dipodomyinae, based largely on biochemical evidence (M. S. Haf- ner 1982) and comparative analysis of the male reproductive system (this study). We re- gard the many morphological similarities be- tween Microdipodops and Perognathus (Wood 1935, J. C. Hafner 1978) to be shared primi- tive features. Nevertheless, more detailed analyses at the molecular level are needed to confirm or refute the placement of Micro- dipodops within the Dipodomyinae. Two spe- cies of Microdipodops are recognized by Hall (1981). Hall's suggestion (1981:560) that M. rnegacepJiahis leticotis may warrant specific status is not supported by chromosomal or protein evidence (J. C. Hafner 1981a). Subfamily Heteromyinae Coues 1875 Genus Heteromys Desmarest 1817.— Hall (1981) recognizes 10 species of Heteromys partitioned into two subgenera, Heteromys and Xylomys. Heteromys nigricaudatus 24 Great Basin Naturalist Memoirs No. 7 Goodwin 1956 (recognized by Hall 1981) was synonymized under H. lepturus Merriam 1902 by Goodwin (1969). Rogers and Schmidly (1982) have analyzed phenetic rela- tionships in Hall's (1981) desmarestianus group (exclusive of H. gaumeri) and have syn- onymized H. longicaudatus Gray 1868, H. temporalis Goldman 1911, and H. lepturus under H. desmarestianus Gray 1868. Genus Liomijs Merriam 1902.— We have reviewed a large body of evidence support- ing the phyletic affinity of Liomijs and Heter- omijs. Hall (1981) follows Genoways (1973) in recognizing five species in the genus Liomys. Future biochemical and chromosomal band- ing studies may serve to identify species groups within the genus. Subfamily Perognathinae Coues 1875 Genus Perognathus Wied-Neuwied 1839.— Our elevation of Chaetodipus to full generic rank (see beyond) results in the in- clusion of only "silky pocket mice" (formerly referred to the subgenus Perognathus) within the genus Perognathus. Hall (1981) recog- nizes 10 species of silky pocket mice, includ- ing the problematic species P. formosus Mer- riam 1889 (see Osgood 1900). Patton et al. (1981) have shown that P. formosus is clearly referable to Chaetodipus, thus reducing the number of Recent taxa of Perognathus to nine. Genus Chaetodipus Merriam 1889.— CJmetodipus is here elevated to full generic status. Following is a synonymy and a rediag- nosis of the taxon. Genus Cluietodipus Merriam, new status Chaetudipus Merriam, 1889, N. Amer. Fauna 1:5 (25 Oc- tober). Type-species: Perognathus spinattis Mer- riam, original designation. Subgenus elevated to generic level. Diagnosis.— Size medium to large (total length 152-230; Hall 1981). Pelage generally harsh, often with spiny bristles on rump. In those species lacking harsh pelage and rump spines, tail crested distally and longer than head and body. Hair flattened in cross section with distinct trough having well-developed ridges on dorsal surface (Homan and Gen- oways 1978). Soles of hind feet naked. In- terparietal width equal to or greater than in- terorbital width. Auditory bullae not EOCENE .OLIGOCENE , MIOCENE .PLIOCENE , HETEROMYINAE y^~ ^ ■ — ■ x_ *^^ PEROGNATHINAE LIOMYS y^^ r'LnUvjNAI HUS \ \^ ^^ /• CHAETODIPUS DIPODOMYINAE -;derson, S. 1964. The systematic status of Perognathus artus and Perognathus goldmani (Rodential. .\mer. Mus. Novitates 2184:1-27. Arata, \. A. 1964. The anatomy and taxonomic signifi- cance of the male accessory reproductive glands of nniroid rodents. Bull. Florida State Mus. 9:1-42. .\xelrod, D. I. 1950. 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Mares- Abstrac:t.— Desert rodent communities are compared for evidence of convergent evolution at various levels of or- ganization, including the systemic (physiological, anatomical, etc.), autecological, and synecological. Convergence is quite pronounced at the systemic level, less pronounced at the autecological level, and even less detectable at the svnecological level. This is not to imply that community convergence does not occur, but rather that our current abilities to quantify and detect convergence at the community level are nidimentary— and our data base is still far from adequate to the task of rigorously comparing community attributes. Most research on the ecology, behavior, physiology, and community structure of desert rodents has been conducted on North American species inhabiting deserts of the United States. The patterns of species coexistence that have been elucidated in these deserts are often presumed to apply in other deserts of the world. It has become apparent in recent years, however, that the complex North .American desert system is unique in many ways, perhaps especially in the biogeographic history of its habitats and faunas, from most of the other deserts of the world. The North American deserts offer an unusually diverse fauna of desert rodents (both alpha and beta diversity are high) which evidences patterns of distribution and coexistence that excite biologists working with the mechanisms of competitive interactions. Similar studies carried out in other deserts might very well lead to a different set of ideas concerning the ways in which desert rodents manage to coex- ist and how desert communities develop over time. The present paper is an attempt to compare community struc- ture and development as well as patterns of coexistence among the various faunas of desert rodents of the world. Al- though data are sketchy for many areas, sufficient information is available to allow a preliminary comparison of methods of adaptation and coexistence to be made. Research on desert rodents began over a century ago in the United States. The earHest studies examining desert rodents were those of Coues (e.g., 1868), Coues and Allen (1877), and C. Hart Merriani and his team of in- vestigators from the old Biological Survey. In addition to the taxonomic investigations of Merriam himself (e.g., Merriam 1889) and those of his subordinates (e.g., Osgood 1900, Goldman 1911, Howell 1938), there were other .studies by contemporaries of the survey scientists (e.g., Grinnell 1932, Benson 1933, Blos.som 1933, Hall and Dale 1939). After the initial work had formed a rather firm tax- onomic foundation, field research entered the stage of natural historical, ecological, and biogeographical .studies (e.g., Taylor and Vor- hies 1923, Bailey 1931, Benson 1935, Dice and Blos.som 1937, Blair 1943, Monson and Ke.s-sler 1940, Tappe 1941, Fitch 1948). Al- though ecological and taxonomic in- vestigations continued during the mid- twentieth century, much research was cen- tered on the physiological adaptations of ro- dents to arid environments; this research was greatly stimulated by the studies of the Schmidt-Nielsens (see Schmidt-Nielsen 1964, for a review), who showed convincingly that some small mammals were well adapted physiologically to pronounced aridity. Later research has allowed a finer resolution of the mechanisms of physiological adaptation to deserts (e.g., McNab and Morrison 1963, MacMillen 1964a, 1964b, 1972, Hudson 1964a, Chew 1965, Carpenter 1966, Brown 1968, Brown and Bartholomew 1969, Mullen 1971, Abbott 1971, Whitford and Conley 1971, Maxson and Morton 1974, Baudinette 1974). Within the last 15 years, desert research in the United States has centered on problems dealing with species coexistence. It has long been remarked that the deserts of the United States support a broad diversity of species, but only since the mid-1960s have research- ers attempted both to understand the causa- tive agents of this diversity as well as the mechanisms of species coexistence. Earlier 'From Ihc symposium "Biology of Desert Rodents," presented at the annual meeting of the American Society of Mammalogists. hosted In Brigham Young University, 20-24 June 1982. at Snowbird. Utah. • » . 'Stovall Museum, University of Oklahoma, Norman, Oklahoma 73019. 30 1983 Biology of Desert Rodents 31 studies of coexistence had examined the pos- sible roles of abiotic factors on species distri- bution patterns (e.g., Hardy 1945), but later research has focused on the role of inter- specific competition as a possible determi- nant of distributional patterns (see Brown et al. 1979, for a review). Research emphasis over the last decade has centered on the body sizes of coexisting rodent species (e.g., Brown 1973, Brown 1975, Bowers and Brown 1982), the sizes of seeds taken by granivorous ro- dents (e.g.. Brown and Lieberman 1973, Mares and Williams 1977), the distribution of the seed resource in the desert and whether or not clumped seeds are favored by bipedal species (e.g., Reichman and Oberstein 1977, Wondolleck 1978, Price 1978, Hutto 1978, Trombulack and Kenagy 1980), and on the importance of microhabitat selection in maintaining coexistence (e.g., Rosenzweig 1973, 1977, 1979, Rosenzweig et al. 1975, Schroder and Rosenzweig 1975, Lemen and Rosenzweig 1978). Each of these areas of research is con- troversial. For example, Lemen (1978) has strongly criticized the proposed seed size-body size relationship, and support for his position can be garnered from Stamp and Ohmart (1978), M'Closkey (1978), and others. Ekrly indications that bipedal rodents are able to travel greater distances more rapidly and at lower energetic costs than quad- rupedal species (e.g., Dawson 1976) have been shown to be in error (Thompson et al. 1980), thus casting doubt on the validity of a linchpin in the theory relating locomotor mode (bipedality) to the habit of foraging on widely dispersed seed clumps (see also Frye and Rosenzweig 1980). Evidence for body size differences among coexisting competitors has been challenged by Conner and Sim- berloff (1979) and Rebar and Conley (in press). Even the basic premise that com- petition has helped mold desert rodent com- munities (Brown 1976, Munger and Brown 1981) has been shown to be a hypothesis that is testable only with the greatest difficulty, if it can be unambiguously tested at all (e.g., Rosenzweig 1981). The many basic studies done in the arid portions of the United States have made this region one of the best studied areas on earth. Since ecologists tend to extrapolate the re- sults of research carried on in one biome to other areas supporting apparently similar ecosystems, it is tempting to believe that as we explain patterns of coexistence or adapta- tion within the deserts of the United States we will have described these patterns for deserts around the world. As MacArthur (1972:1) noted, "To do science is to search for repeated patterns." In this brief essay I will characterize the patterns of adaptation of desert rodents that have been described largely within the conterminous United States. Realizing full well that "natural selec tion depends for its effectiveness on a series of chances" (Leigh 1971:221), I believe it is important to distinguish between local pat- terns and those of a global nature. Perhaps all important questions regarding life in deserts can be answered by studying intensively one particular geographic unit— then again, per- haps not. If all deserts are not equal, a very real problem develops in discovering which patterns are truly generalizable. The Patterns The first problem that presents itself is that of scale— does one seek patterns at the level of biochemical reactions, organ systems, or communities? The second problem is that of confounding causation. Does bipedality de- velop, for example, because of intrinsic prob- lems related to integrated locomotor design (e.g., Alexander 1975), or do such seemingly unrelated factors as seed distributions, gran- ivory, predator avoidance, and substrate all play a part in the selection of a particular type of movement? Although it is easy to be- come overwhelmed by the complexity of desert rodent adaptations, I will limit my analysis to characteristics above the purely biochemical level. This broad brush approach will give an overview of adaptations of desert rodents from the United States and will com- pare these with rodents from other parts of the world that have also successfully made the transition to desert life. I will in essence be assessing the available literature on desert rodent biology for examples of convergence, "the strongest sort of evidence for the effi- cacy of selection and for its adaptive orienta- tion of evolution" (Simpson 1953:171). 32 Great Basin Naturalist Memoirs No. 7 Physiological Adaptations Water Balance— North America Perhaps one of the most widely known traits of small mammals in desert regions is the ability to withstand water deprivation. Schmidt-Nielsen (1964) has provided the most complete summary of the complex ad- aptations associated with this ability in North American rodents (see also Schmidt-Nielsen 1975, for a discussion of the mechanisms of water conservation in desert rodents). It is clear that withstanding either low free envi- ronmental water or high solute loads de- mands numerous physiological and anatomi- cal specializations. Certainly, the North American Heteromyidae, kangaroo rats and pocket mice, are the most specialized rodents in this regard in the deserts of the United States. Their adaptations include specialized kidneys, elongated renal papillae, long nasal passages for countercurrent heat exchange, and numerous other characteristics that mini- mize water loss or increase their ability to obtain vegetational water (e.g., Schmidt- Nielsen 1964, Mullen 1971, Kenagy 1973a, Soholt 1975). Similar adaptations, although perhaps not as pronounced, are known to oc- cur in North American cricetines (e.g., Ab- bott 1971, Andersen 1973), and sciurids (e.g., Hudson 1962, Maxson and Morton 1974). In all these higher taxa, some species are ca- pable of producing fairly concentrated urine, reducing fecal and respiratory water loss, and existing on minimal inputs of free or vegeta- tional water. There is little doubt that the physiological and anatomical adaptations of desert rodents that minimize water loss en- compass all the major systems of the organ- ism. For example, Hatton et al. (1972) showed that in desert rodents the cells of that portion of the brain responsible for produc- ing vasopressin (ADH) are multinucleate, a trait that is uncommon in rodents from moist habitats; this trait is very likely related to wa- ter retention ability. They examined several species from both New and Old World deserts. As physiological studies are extended to the arid portions of Mexico, numerous other species will probably be foimd to be highly adapted for existing in an environment hav- ing minimal moisture available for ingestion. Not all rodents inhabiting North American arid areas are desert specialists (e.g., Lee 1963, Andersen 1973, MacMillen and Chris- topher 1975). Although it is clear that the ability to withstand water deprivation has a strong phylogenetic component (e.g., Hudson and Rummel 1966, Fleming 1977), it can de- velop readily in species inhabiting non- desertic habitats where water is scarce (e.g., Fisler 1963, MacMillen 1964b). Water Balance— Other Deserts Because of the widespread nature of vari- ous physiological adaptations among species of the North American fauna, one might ex- pect that similar types of adaptations would develop in other deserts. Despite the com- plexity of the suite of traits associated with water independence, this does not appear to be a particularly difficult path for evolution to follow. Indeed, water independence has developed among one or more species of ro- dents from deserts in Australia (e.g., MacMil- len and Lee 1969, Baudinette 1972), Asia (Winkelman and Getz 1962), India (e.g., Ghosh 1975), North Africa (e.g., Burns 1956, Kirmiz 1962 for Jactiliis, but see Ghobrial and Nour 1975), southern Africa (e.g., Chris- tian 1978, 1979), and Peru (Koford 1968). The extensive Monte Desert of Argentina lacks water-independent species, although EUgmodontia typus, a cricetine, is well adapted to process high concentrations of so- dium chloride (Mares 1977a). Curiously, al- though Mares (1977b) did encounter a water independent rodent in Argentina {Calomijs musculinus), it was an inhabitant of the mes- ic fringes of the desert. Only a relatively small percentage of the desert rodents of the world has been exam- ined physiologically. Similar adaptations may have developed repeatedly in all deserts of the world. There is some question as to how physiologically specialized the dipodids are (Ghobrial and Nour 1975), but there is little doubt that pronounced adaptations toward aridity have occurred in such disparate fami- lies as the Muridae, Dipodidae, Hetero- myidae, and Sciuridae. Similar adaptations will probably be found in other families of desert rodents (e.g., Octodontidae, Ctenodactvlidae). 1983 Biology of Desert Rodents 33 The apparent regularity with which phys- iological adaptations develop is illustrated by their being characteristic not only of gra- nivorovis or herbivorous rodents, but of insectivorous-carnivorous rodents (e.g., Whit- ford and Conley 1971) and small marsupials (e.g., Schmidt-Nielsen and Newsome 1962, MacFarlane 1975, Morton 1980). Mares (1975a, b, 1976, 1977c) found that not all rodents inhabiting the Monte Desert of Argentina showed pronounced levels of physiological adaptation (see also Meserve 1978). Many species inhabit that region by limiting their activities to relatively mesic microhabitats. In view of the widespread na- ture of physiological adaptation toward a xeric existence. Mares (1975a, 1976) hypoth- esized that most of the rodents of the Monte Desert had not reached the region until latest Pliocene, or even Pleistocene, times. Thus, there had not been sufficient time to evolve the complex group of physiological, ana- tomical, behavioral, and ecological attributes characteristic of desert life. Although much work remains to be done on the comparative physiology of desert ro- dents, pronounced convergence and paral- lelism have occurred in all deserts as the re- sult of similar regimens of natural selection acting on the colonizing stocks of rodents, re- gardless of their phylogenetic affinities. This convergence (or parallelism, in some cases) extends to many aspects of the behavioral- physiological-anatomical complex involved in osmotic balance. Similarities are seen in the stRicture of kidneys (e.g., Hudson 1962, Schmidt-Nielsen 1964, MacMillen and Lee 1969, Abdallah and Tawfik 1969, Fleming 1977), in their urine concentrating abilities, in the ability of the animals to withstand des- sication or elevated solute loads, in the elon- gated nasal passages for heat exchange (this characteristic is in need of comparative stud- ies), and in reduced fecal water loss. Only a few studies have been done examining other avenues of water loss in desert rodents and the adaptations that have evolved to mini- mize these losses. For example, Kooyman (1963) shows that Dipodomys merriami pro- duces a very concentrated milk (thus mini- mizing lactational water loss). Working with native Australian rodents (Notomys, Pseud- omys), Baverstock et al. (1976) found that these species did not produce exceptionally concentrated milk. A later study to examine whether or not these rodents actually re- duced the amount of milk produced during lactation (and thereby reduced water loss) was inconclusive (Baverstock and Elhay 1979). What is really needed is a broadscale study designed to examine all avenues of wa- ter loss and to compare these across taxa. Emphasis should be placed initially on gen- era that are known desert specialists (e.g., Dipodomys, Microdipodops, Perognathus, Gerbillus, Gerbillurus, Desmodillus, Me- riones, Dipus, Jaculus, Allactaga, etc.), rather than on species that inhabit only the climatic peripheries of deserts. Extreme adaptations will be more easily detected than will the fine shadings of "average" adaptations that have been modified to allow persistence only at the environmental peripheries of deserts. Other Physiological Adaptations Various secretory glands are known in desert rodents (e.g., Meriones from India, Wallace et al. 1973; Notomys from Australia, Watts 1975), but their function is not clear. The products of sebaceous glands in Di- podomys may function as other than secre- tions to aid in the care of the pelage (Quay 1953). Whether or not such glands are wide- spread among other taxa of desert rodents is unknown, but a comparative assessment of these structures could prove useful toward understanding their function. Eisenberg (1963, 1975) discusses possible olfactory com- munication in desert rodents, an area of re- search essentially unexplored in mammals, particularly desert rodents. Several species of desert rodents in the United States are known to undergo facul- tative torpor: these species include cricetine rodents, heteromyids, and sciurids (e.g., Hud- son 1964, 1967, Tucker 1966, Chew et al. 1967, Brown and Bartholomew 1969, Kenagy 1973b, Reichman and Van De Graff 1973, Reichman and Brown 1979). Presumably such a strategy allows a rodent to remain inactive during periods of resource scarcity; however, periodic torpor is not limited to rodents from xeric habitats (e.g., Hill 1977). It has been hy- pothesized that desert rodents have a lower metabolic rate (irrespective of torpor) than 34 Great Basin Naturalist Memoirs No. 7 species from mesic habitats (e.g., McNab and Morrison 1963). Hay ward (1965) questioned this idea, suggesting that stored fat reserves of laboratory animals had led to artificially low metabolic rates. McNab (1968), however, showed that lower metabolic rates for species from xeric habitats (i.e., a North American cricetine, Peromyscus crinitus, and the naked mole rat of Africa [{Heterocephalus glaher), a bathyergid]) characterized individuals whose body fat levels were well within normal lim- its. Yousef and Johnson (1975) found a corre- lation between the lower metabolic rate of various North American desert rodent species (representing three families) and reduced thyroxine secretion rate, suggesting a rela- tionship between thyroid activity and meta- bolic rate; species from xeric areas had signif- icantly lower rates of thyroid activity than species from mesic habitats. Energy metabolism in North American desert rodents has been examined in both the laboratory (e.g., Dawson 1955, Yousef et al. 1970) and in the field (e.g., Mullen 1971, So- holt 1973, Kenagy 1973b). There are very few comparative studies available on rodents from other deserts (e.g., Dawson 1976, Thompson et al. 1980). The fact that many similar adaptations are common among species of the three families of rodents inhabiting North American deserts would lead one to speculate that similar traits might be expected in other faunas. All infor- mation to date supports the idea that similar physiological strategies toward aridity have evolved independently and repeatedly throughout the world. Anatomical Adaptations North America Like physiological adaptations, anatomical specializations for desert life are essentially limitless— depending on one's scale, anatomy can be viewed from the cell to the whole or- ganism. (3i)viously, an organism evolves as an integrated luiit. Thus, viewing any structural specialization without regard to its associ- ation with function lends a certain arti- ficiality to the analysis. For example, the supraoptic nuclei described above (Hatton et al. 1972) are cellular specializations leading to gross modifications in brain tissue. These structures play a role in ADH secretion and thereby affect osmotic balance. Nevertheless, from the viewpoint of convergent evolution, it is interesting to know whether similar structures have developed and whether or not they function in similar ways. It is also instructive to learn that similar functions are performed by dissimilar structural adaptations. Bipedality Quite often, the term "desert rodent" con- notes the genus Dipodomys. Much research has centered on species of Dipodomys, and kangaroo rats are almost synonymous with "desert adaptation." Nevertheless, kangaroo rats are but one of many genera inhabiting North American deserts. It is probably be- cause of the familiarity of many scientists with Dipodomys that most desert rodents are assumed to mirror the adaptations character- istic of that single genus. Dipodomys are saltatorial and bipedal; they are also granivorous. Because of the as- sociation between bipedality and granivory in Dipodomys, a causal link between these characteristics has been suggested (e.g., Reichman and Oberstein 1977). It is instruc- tive therefore to examine bipedality in some detail. Several anatomical studies have examined bipedality in desert rodents (e.g., Hatt 1932, Howell 1932, Klingener 1964, Pinkham 1971, Kaup 1976, Berman 1979). The most exten- sive study was that of Berman (1979), who compared hind limb osteology and myology in a broad spectrum of desert rodents of the world. She noted that bipedal saltation has arisen independently in five families of ro- dents: four of these (Heteromyidae, Di- podidae, Pedetidae, and Muridae) have their bipedal species essentially restricted to xeric habitats, whereas the Zapodidae are forest species. Small bipedal saltators have also aris- en among extant and extinct marsupials. Ber- man's analyses led her to conclude that there has been a striking convergence in major musculoskeletal modifications of the hind limb of desert rodents. Similarities in struc- ture are so pronounced tiiat unrelated bipe- dal species were generally grouped more 1983 Biology of Desert Rodents 35 closely in multivariate space than were bi- pedal and quadrupedal members of the same families. Her analyses also showed that there were nimierous significant differences among desert rodents in the ways in which biped- ality had been achieved— different muscles were elongated or shortened, different me- chanical advantages had evolved, and differ- ent modifications characterized the feet. Mares (1980) examined the majority of desert rodent genera in a multivariate analy- sis of morphoecological characteristics. He noted that bipedality in North American deserts is restricted to granivores (although many obligate granivores in North America are quadrupedal), but when all desert rodents are examined, the supposed link between bi- pedality and seed eating is not found. There are bipedal granivores (e.g., Dipodomys, Car- diocranius, Stylodiptis, some Jacidus), bipedal herbivores feeding on above-ground plant parts (e.g., Pedetes, which also feed in below- ground plant parts, Pygeretmus, Alactagulus, some AUactaga); bipedal herbivores feeding on below-ground plant parts (some AUactaga, some Jacidus), bipedal herbivores eating all plant parts (e.g., some AUactaga, some Ja- cidus, Dipus, Paradipus); bipedal omnivores (some AUactaga, Notomijs); and bipedal in- sectivores (Salpingotiis, the marsupial An- techinomys). In Old World deserts, most obli- gate granivores are quadrupedal (e.g., Meriones, Gerbdlus, Tatera, Phodopus, Bra- chiones, Sekeetamys, etc.). [Information on the diets of the various genera can be found in Lobachev and Khamdamova (1972), Nau- mov and Lobachev (1975), Happold (1975), Prakash (1975), Watts (1977), and Wassif and Soliman (1979).] Thus, bipedality, when viewed on a global scale, appears to have little relation to diet; bipedal species fill all major trophic cate- gories. Although research limited to North American desert species might be interpreted as supporting a link between diet and loco- motion, I find no evidence to support this hy- pothesis in other deserts. In addition to elongated hind limbs, biped- al rodents have shortened forelimbs, prompt- ing suggestions that the freeing of the fore- limbs for stuffing food into the cheek pouches was the primary selective force lead- ing to bipedality (Bartholomew and Carey 1954). In view of the large number of bipedal rodents that lack cheek pouches (including all pedetids, dipodids, and zapodids), the many quadrupedal species that have internal cheek pouches (e.g., cricetids, sciurids, etc.), and the presence of cheek pouches in fosso- rial geomyids and quadrupedal Perognathus, Liomys, and Heteromys, there is little com- pelling support for this hypothesis. One hypothesis that has been invoked to explain bipedality (although it has been tied to the pattern of seed distribution) is differen- tial microhabitat utilization. There is some evidence that bipedal species forage in open areas more frequently than they do under shrubs (e.g., Rosenzweig and Winakur 1969, Brown and Lieberman 1973, Rosenzweig 1973, Brown 1975, Price 1978, Wondolleck 1978); this observation appears to hold for Old World desert species as well (e.g., Nau- mov and Lobachev 1975), although rigorous quantification of this pattern is needed for all deserts, particularly those of the Old World. Nevertheless, if foraging in open areas is cor- related with bipedality, then it is inferential evidence that predator avoidance is a pri- mary selective factor of locomotor mode. This is an old idea (e.g., Howell 1932) that has been restated repeatedly (e.g., Eisenberg 1975, Berman 1979, Mares 1980), but ap- pears to have merit. There is little doubt that predation is an important factor in sparse desert habitats— evolutionarily opting to for- age in open microhabitats very likely forces rodents into an entirely new adaptive mode, that of bipedality. Bipedality is also associated with other anatomical adaptations for predator avoid- ance (although some of these occur in quad- rupedal desert species as well). Enlarged bullae (e.g., Howell 1932, Webster 1962, Lay 1972) or elongated pinnae (e.g., Howell 1932, Eisenberg 1975) are probably adaptations for predator detection (e.g., Legiouix and Wisner 1955, Lay 1974). While it might be supposed that the pinnae function in thermoregulation, as is the case in Lepus (Hill and Veghte 1976), in fact, the large pinnae of AUactaga are not well vascularized and do not function in heat loss (Hill et al. 1974). Bullar hyper- trophy is common in desert rodents through- out the world and in other mammals as well 36 Great Basin Naturalist Memoirs No. 7 (e.g., Roig 1969, 1972). Fitzwater and Pra- kash (1969) described Meriones in India re- sponding to the wingbeats of avian predators by escaping into burrows. Finally, desert rodents are generally very pale colored, usually matching the desert soils (e.g., Harrison 1975, Mares 1976, Cloudsley-Thompson 1979). Most authors concur that cryptic coloration is a response to visual predators (cf., Kaufman 1974). Some bipedal species possess a conspicuous black and white tuft on the tip of the tail (almost all bipeds have long tails with a terminal tuft). Tail tufts often regenerate if the tail has been injured (Howell 1932), and it is likely that the tuft itself fimctions as a rudder that allows the animal to turn abruptly in midair, particularly since the wind resistance of the tuft acts at the end of a long lever arm. The white tail tuft may well act as a flag to con- fuse or distract predators during their pursuit and/ or as a target for predator attack, thus limiting an attack to a tail that may break quite easily and allow the rodent to escape. An examination of the morphology of desert rodents leads to the conclusion that convergent evolution of structures that re- duce the probability of predation is a major evolutionary force. Behavioral and Autecological Adaptations Behavior Eisenberg (1975) has done the most com- prehensive comparative behavioral work with desert rodents. Most are nocturnal; most live in burrows that are plugged during the day. There are many differences among spe- cies in aspects of social behavior, but many species in disjunct deserts have remarkably similar behavioral patterns. Unfortunately, little quantitative behavioral research has been done on other than North American species, and even these have been studied primarily in the laboratory. Studies on Old World species include Nel (1975), Daly and Daly ( 1975a, b), and Agren ( 1979). Some workers have examined activity pat- terns of desert rodents (e.g., Schwab 1966, Ja- hoda 1973, Kenagy 1973b, 1976, Lockard and Owings 1974, Rosenzweig 1974, French 1975, Lockard 1978). Data from the Old World are in accord with these observations (Naumov and Lobachev 1975). Generally, most desert species are nocturnal (especially bipedal species), although each desert has one or more species of diurnal rodents (usually these are herbivores, Mares 1980). Autecology Smith and Jorgensen (1975) and Conley et al. (1977) review reproductive patterns in North American desert rodents, and French et al. (1975) and Wagner (1981) review de- mographic patterns of desert species through- out the world. Heteromyids generally have small litters, relatively long life spans, low densities, and reproduce during moist and warm times of the year. A complete review of desert rodent reproduction that includes species from each desert has not been pro- duced. In addition to the above reviews, there is some general information available on reproduction for the following areas: Aus- tralia (Smith et al. 1972, Crichton 1974, Watts 1979, Aslin and Watts 1980); USSR (Naumov and Lobachev 1975); North Africa (Poulet 1972, 1978, Khammar et al. 1975, Happold 1975, Ghobrial and Nour 1975, Amirat et al. 1977); southern Africa (Nel 1978, Christian 1979, 1980, Butynski 1979); Iran (Lay 1967, Misonne 1975); India (Pra- kash 1975); Pakistan (Beg et al. 1977); Chile (Fulk 1975). Although demography has been studied in some detail in North American desert rodents (see above citations), there have been few ex- tensive demographic studies in either South American deserts or in the Old World. Most of these can be located using those citations referring to reproductive patterns (see also Pearson and Ralph, 1978, for Peru). Synecology Perhaps the most exciting area of desert ecology today is that dealing with species in- teractions and community organization. Brown et al. (1979) and Mares (1980) review much of this literature. Research done in North America would suggest that deserts support elevated levels of both species rich- ness and abundance. However, Mares (1979) 1983 Biology of Desert Rodents 37 has argued that the deserts of the United States support an unusually high diversity of species due to their unique Pleistocene his- tory of refugial formation wherein allopatric speciation processes were amplified. High relative abundance of rodents in U.S. deserts is probably related to the elevated rainfall characterizing much of the North American desert system (e.g.. Brown et al. 1979). Much U.S. desert research has been conducted in the Sonoran Desert of southern Arizona, a re- gion that some consider a semidesert due to its relatively high precipitation (e.g., Eisen- berg 1975). This preponderance of research in an extremely productive area may have led to a fairly common belief that deserts of- ten support many small mammals. Actually, most deserts seem to support few species of desert rodents at fairly low levels of abun- dance (e.g., Mares 1976, 1980, Pearson and Ralph 1978, Morton 1979, Brown 1980, Christian 1980), although some areas seem to be equally as rich in species as portions of the U.S. desert system (e.g., Nel 1978). Just how desert species manage to coexist is the major area of research at the moment, with competition assumed to be a primary selective force leading to observed patterns of microhabitat selection (Rosenzweig 1979), body size differences (Bowers and Brown 1982), or differential utilization of the seed resource (e.g., Reichman and Oberstein 1977). Little comparative work that might shed light on current controversial points has been done in deserts outside the United States, but certainly habitat specificity is a well-known factor characterizing small mam- mal communities (e.g., Hubert et al. 1977). Nevertheless, Pearson and Ralph (1978:75) found that small mammal species richness in several desert habitats in Peru could be ex- plained by "evolutionary and zoogeographic- al accident," rather than habitat selection differences. One reason that controversy surrounds co- existence studies in deserts is that most re- search to date has been descriptive and infer- ential. Studies dealing with seed selectivity by rodents have had to contend with the enormous variability in background seed lev- els and the methodological difficulties of samphng the seed resource (e.g., Brown et al. 1979). Nevertheless, recent trends have fo- cused on manipulative field experiments (particularly the work of Rosenzweig, Brown, Reichman, and their associates, see above ci- tations). Unfortunately, there has been no parallel movement in experimental research in deserts outside of the United States (or even outside the Sonoran Desert). Theory has far outstripped our empirical data base in desert ecology and experimental data are only beginning to be applied to the many hy- potheses that currently abound in the literature. Recent studies dealing with competition between distantly related taxa promise excit- ing results if they can be replicated in other deserts (e.g., Brown 1976, Brown and David- son 1977, Davidson et al. 1980). Mares and Rosenzweig (1978) have done comparative work on this topic and found different pat- terns in North and South American deserts— they offer an evolutionary explanation for different strategies of granivory in distantly related taxa. Perhaps the area of research that has been most neglected is that of comparative faunal studies. Mares (1975, 1976, 1980), MacMahon (1976), Mares et al. (1977a, b). Mares and Hulse (1977), Pearson and Ralph (1978), and Morton (1979) have attempted to compare quantitatively diverse desert rodent assem- blages. Unfortunately, such studies are ham pered by a paucity of data for deserts outside of the United States. As data accrue from current desert research, and as statistical and computational techniques are refined, there should be a great deal of information forth- coming on the ways in which desert rodent communities assemble over time. Closing Comments If one were to go into an unknown desert region, there are many predictions that could be made concerning the small mammal fauna (particularly the rodent fauna) of the area. Beginning at the most basic levels (anatomy and physiology), we could say that at least some rodents inhabiting the area would ex- hibit the following adaptations: specialized kidneys (with elongated renal papillae and micro- and macroscopic morphological adap- tations) able to concentrate the urine and perhaps process high electrolyte loads; a 38 Great Basin Naturalist Memoirs No. 7 counter-current heat exchange system in the nasal region; modified brain cells responsible for ADH secretion; lowered metabolic rate; facultative torpor; ability to exist without free water; minimization of water loss through respiratory, excretory, and defeca- tory pathways; inflated tympanic bullae or elongated pinnae; bipedality (some species)— with foreshortened forelimbs, long tails, con- centrations of muscle mass in proximal limb regions, smaller mechanical advantages for hind limb muscles, elongated distal limb seg- ments, toe reduction, terminal tuft of hair on the tail (often colored black and white); se- baceous glands would be present— sand bath- ing would be common; dorsal coloration would match the background (pale colors predominating) and countershading would be pronoimced; species living on sand would have extremely hirsute hind feet; eyes would be placed dorsally; vibrissae would be abun- dant and long; white flank markings would be common in bipedal species. There are many other physiological and anatomical traits that would very likely characterize the rodents of this unexplored desert. Above the systemic level, we could predict the possession of numerous autecological traits: noctumality would predominate (par- ticularly in bipedal species); both diurnal and nocturnal species would inhabit burrows— these would be plugged during hot periods; bipedal species would differentially forage in open microhabitats, and quadnipedal species would favor , closed microhabitats; bipedal fonns would occur in flat areas having few rocks; reproduction would be associated with the rainy season, with birth taking place after the rains— populations would peak at this time; territoriality would be pronounced; home ranges would be relatively large; survi- vorship would be high and fecunditv low (e.g., French et al. 1975); population levels would generally be low (although they are often quite high in North American deserts). Clearly, at the levels of organization from population down to cell, there are niunerous predictions that could be made regarding the suite of desert adaptations that would charac- terize our unknown species, and the lists presented are far from exhaustive. As our lev- el of understanding is refined, more and more similarities in adaptive strategies become evident. At the community level, however, our pre- dictions become more tenuous. Our hypo- thetical desert would probably possess a bi- pedal and/or a quadrupedal granivore; a micro-omnivore; a medium (squirrel)-sized diurnal omnivore; a small insectivore; a bi- pedal or a fossorial medium-sized herbivore eating below-ground plant parts; and a larger herbivore (rabbit size). Species richness would be low (although high species richness would not be surprising, particularly if the biogeographic history indicated a multiple- refugial system). Bipedality could occur in all trophic categories except the completely fos- sorial niche. Coexisting species might exhibit regular patterns of body size differences, and microhabitat selection might be the primary mechanism maintaining coexistence. Gra- nivorous rodents might show inverse relation- ships in abundance and diversity to the abun- dance and diversity of other granivores, such as ants or birds. Ants and rodents might be mutualistic over evolutionary time; thus, a lack of mammalian seed predators could prove detrimental to ant seed predators. There is some controversy as to whether or not there is convergence at the community level (Schall and Pianka 1978). Certainly community studies based in morphometries will have a proportion of their overall sim- ilarity explained by morphological con- vergence. However, since morphology often reflects function, there is strong evidence that pronounced convergence exists above the systemic level of organization. It is equal- ly clear, however, that strong commmiity convergence is yet to be demonstrated when only ecological parameters are utilized in the faunal comparisons. This is not to say that such convergent evolution does not exist, but rather that the influence of history on faunal development and our inability to quantify rigorously the many ecological attributes of a fauna (and to produce highly predictive and quantitative theories) have not yet allowed us to assess the presence or absence of commu- nity convergence. Our best work is yet to be done. The complexity of the seemingly simple desert ecosystem has not yielded to in- ferential science— the ability of experimental science to clarify the many remaining enigmas is yet to be tested. 1983 Biology of Desert Rodents 39 Literature Cited Abbott, K. D. 1971. Water economy of the canyon mouse Peromyscus crinitus stephensi. Conip. Bio- chem. Physiol. 384:37-52. Abdallah, a., and J. Tawfik. 1969. 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The biomechanical consequences of cheek pouch loading for body size and locomotor behavior yield theoretical predictive models concerning interspecific differences in foraging behavior, dietary prefer- ence, and microhabitat selection. Stnictura! modifications of the forelimb associated with use of external cheek pouches reduce the mechanical competence of these limbs for shock absorption during fast quadrupedal running. The relative size of various front and hind limb segments are correlated with quadrupedal, tripodal, and bipedal gaits in heteromyid rodents. The in- terdependence of body balance, gait, and speed are examined in Dipodomys merriami. Factors possibly contributing to the origin of bipedalism in rodents are reviewed and discussed. The heteromyid rodents of North America offer, potentially, a superb opportunity to ex- amine the importance of morphological de- sign as a determinant of behavioral and eco- logical patterns under natural conditions. This follows from the considerable range of morphologies found within this circum- scribed group as well as the impressive breadth of habitats that its living representa- tives presently occupy. Perhaps more signifi- cant is the fact that heteromyids have recent- ly become the focus of numerous investigations aimed at gaining a better un- derstanding of their biology on multiple lev- els (e.g., physiology, behavior, ecology, com- mimity level interactions). Such studies have begun to offer the kinds of information against which carefully framed hypotheses of a hmctional-morphologic nature might be critically appraised. Earlier morphologic studies on hetero- myids are primarily descriptive but also con- tain comments on form-function relationships that are, of necessity, relatively superficial and speculative. Excellent works of this type are Howell's (1932) monograph on the myol- ogy and osteology of Dipodotnys, Hatt's 'From the .symposium "Biology of Desert Rodent-s," presented at the annual University, 20-24 June 1982, at Snowbird, Utah. 'Department of Biology, University of Utah, Salt Lake City. Utah 84112. (1932) comparative study of vertebral archi- tecture in saltatorial rodents, and Wood's (1935) important survey of the fossil and Re- cent Heteromyidae. Herman's (1979) recent multivariate statistical analysis of hind limb bone and muscle morphology in bipedal ro- dents constitutes a very significant extension beyond the older comparative anatomical works. Recent functional morphologic studies have been more analytical and experimental, but also of more limited scope. Thus, Pink- ham (1976) has investigated the gaits and me- chanics of quadrupedal and bipedal running in Liomys and Dipodomys by combining high speed cinematography with force platform recordings. Using similar techniques, but also including cineradiography, Biewener et al. (1981) have studied the mechanical behavior of the major hindlimb tendons in kangaroo rats. Additional information on the ankle me- chanics of Dipodomys and the physiological properties of its associated mu.sculature has been presented by Williamson and Frederick (1977). Kaup (1975) has also commented on the biomechanical and evolutionary signifi- cance of hind limb anatomy in heteromyids. meeting of the .\nierican Society of Mammalogists, hosted by Brigham Young 44 1983 Biology of Desert Rodents 45 Of special note are the investigations of the Websters (see below) on the auditory appa- ratus of heteromyids. Not only have their studies provided a large body of comparative morphologic data, but they also offer one of the few examples wherein specific hypoth- eses concerning the adaptive value of a major morphological complex have been tested. In the present paper we briefly review the existing data on the functional morphology of heteromyid rodents and point out significant gaps in our knowledge. Considerable atten- tion is given the forelimbs and cheek pouches, two structures that have received httle attention in the past but whose struc- tural organization may place important con- straints on the behavior of these animals. Here and elsewhere we have tried to show how functional morphologic analyses can lead to predictive, testable models con- cerning the natural behavior and ecology of heteromyid rodents. Limitations of both time and materials have forced us to restrict the present dis- cussion to "desert heteromyids" of the genera Perognathiis, Dipodoniys, and Microdipodops. This is done with full knowledge that a better understanding of the fimctional anatomy and behavior of the modern heteromyines (Liomys, Heteromys) would imdoubtedly broaden our appreciation of form-fimction and evolutionary patterns within pe- rognathine and dipodomyine heteromyids and might well alter some of our conclusions. Skull and Neck Morphology Skull The most striking cranial feature of desert heteromyids and that which has received the most attention is the enlarged middle ear chambers or auditory bullae. The auditory bullae are moderately inflated in Pe- rognathiis, but grossly so in both Dipodoniys and Microdipodops (Fig. 1). Relative to over- all head size, the middle ear chambers achieve their greatest volume in the latter genus (Webster 1961). Detailed comparative morphologic data on the auditory region of heteromyids have been provided by Webster and Webster (1975, 1977, 1980). Fig. 1. Influence of auditory specialization on the feeding apparatus of desert heteromyids. A generahzed desert rodent, Neotoma lepida (A) is compared to Pe- rognathtts forinosus (B), Dipodomys merriami (C), and Microdipodops megacephalus (D). Inflation of the audi- tory bufla (stippled) reduces the area of origin of the temporalis musculature (hatched) and also restricts gape by crowding the mandible from behind. The specialized everted angle (ea) of the mandible reduces the impact of bullar inflation in heteromyids. Maximum gape between the cheek teeth (but not incisors) in Perognathiis (35°) is about equal to that in Neotoma (36°), but extreme middle ear hypertrophy has severely reduced gape in Dipodomys and Microdipodops. All skulls drawn to same length. The innovative studies of the Websters and their collaborators have gradually revealed the functional and probable adaptive signifi- cance of the modified ears of desert hetero- 46 Great Basin Naturalist Memoirs No. 7 myids. Auditory specializations in these ro- dents, and in certain Old World desert spe- cies (Lay 1972), improve the detection of rel- atively low frequency sound, especially in the 1-3 KHz range. Selective sensitivity to these frequencies has been established on the basis of physiological (Ruppert and Moushegian 1970, Vernon et al. 1971, Webster and Stro- ther 1972, Webster and Webster 1972) and behavioral experiments (Webster and Web- ster 1972). A suite of structural features ap- pear to be responsible for increased sensi- tivity to low frequency sound by lowering impedance and, hence, increasing the trans- mission of such sound from the external to in- ner ear. Among these features are: (1) a rela- tively large, compliant tympanic membrane; (2) a small, low-mass, high-leverage ossicular chain; and (3) an enlarged middle ear cham- ber. The latter feature is apparently a com- pensatory adjustment that reduces middle ear damping of the large ear drum (Legouix et al. 1954, Webster 1962, Wisner et al. 1954). Ex- perimental reduction of middle ear volume in kangaroo rats significantly reduces sensitivity to low frequency sound (Webster 1961, Web- ster and Webster 1972, 1980). Certain struc- tural modifications of the inner ear (Webster 1961, Webster and Stack 1968) and related areas of the brain (Webster et al. 1968) may also reflect selective sensitivity to low fre- quency sound in Dipodomijs. How the specialized ears of kangaroo rats might contribute to individual fitness has also been examined. Captive kangaroo rats (D. merrkimi) were tested to see how effectively and by what means they avoided the attacks of owls and rattlesnakes (Webster 1962, Webster and Webster 1971). Animals with unimpaired hearing were usually able to avoid capture by these predators even in to- tal darkness or when blinded. Those with im- paired hearing (i.e., artificially reduced middle ear volumes) could also avoid attack, but only when there was sufficient light to see the movements of the predator. Blind kangaroo rats with impaired hearing could not escape predation. A comparison of mor- tality rates between Dipodomys with normal and impaired hearing under field conditions suggests higher mortality among impaired animals, especially during dark of the moon intervals (Webster and Webster 1971). It is presumed that mortality was due chiefly to higher rates of predation upon kangaroo rats whose ability to detect low frequency sound had been reduced. Laboratory recordings in- dicate that the predatory strikes of both owls and rattlesnakes produce significant sound in the 1-3 KHz range (Webster 1962). In sum, the available data strongly imply that the specialized auditory apparatus of desert het- eromyids is indeed adaptive, and that it may confer its greatest advantage on individuals foraging under conditions of dim illumination. There has been little functional analysis of the feeding mechanism of heteromyid ro- dents. Most studies have been concerned with dental morphology as it relates to systematics and the identification of fossil materials (Lindsay 1972, Shotwell 1967, Wood 1935). The cheek teeth of modern desert hetero- myids are relatively simple and lophodont. In Dipodomys the cheek teeth are hypsodont and rootless. Enamel is confined to the ante rior and posterior faces, a condition paral- leled in the Geomyidae (Wood 1937). The mandible tends to be small (relative to head size) in all living heteromyids, but is marked- ly so in Dipodomys and Microdipodops. The smallness of the mandible causes it to be rather severely underslung. This position, to- gether with the dorsal location of the eyes (Howell 1932), assures that the movements of the hands during feeding and pouching be- havior are kept well below eye level. Inflation of the middle ear has impinged directly on the masticatory apparatus by (1) forcing a reduction of the temporalis mus- culature and (2) crowding the mandible from behind, thereby placing serious limitations on gape. The latter problem has been partially circumvented by the development of an everted angular process. Reorientation of the angular process delays its contact with the undersurface of the bulla as the jaw is opened (depressed). This permits a wider gape than would otherwise be possible. Even so, middle ear inflation restricts gape in all desert heter- omyids, but most especially in Dipodomys and Microdipodops (Fig. 1). A restriction in gape will limit the size of resistant food items that an animal can effectively gnaw. Exactly how restructuring of the posterior region of 1983 Biology of Desert Rodents 47 the lower jaw has influenced other biome- chanically important descriptors of mastica- tory fimction (e.g., force, rate, and direction of mandibular movements; organization of adductor musculature) is unknown at this time. Another prominent feature of the cranium of desert heteromyids is the strongly pro- jecting, tubular nasal region. TTie nasal pas- sage is occupied by closely spaced turbinate bones. The length of the nasal passage as well as the diameter of its individual air channels are presumably important to the water con- serving, counter-current heat exchanger pos- sessed by Dipodcnnijs (Jackson and Schmidt- Nielsen 1964, Schmidt-Nielsen et al. 1970). The relative development of the nasal region in desert heteromyids as regards their ability to detect subsurface accumulations of seeds (Frye and Rosenzweig 1980, Reichman 1979) merits examination. The interior of the skull of desert hetero- myids exhibits at least one obvious special- ization. Well-formed bony partitions project medially from the otic capsules into the space between the cerebral and cerebellar lobes of the brain. They are pronounced in Dipodomys and Microdipodops, but more modestly developed in Perognathus. These partitions, which tend to compartmentalize the brain within the cranium, appear to be true tentorial ossifications. As such they can- not be directly related to inflation of the middle ear. Whether or not such structures have any fimctional connection with the rap- id accelerations of tlie head and brain expe- rienced by bipedal heteromyids invites investigation. Neck Hatt (1932) described vertebral modifica- tions that seem to be associated with bipedal saltation in rodents. Among them are: (1) ex- treme shortening and compaction of the cer- vical region, (2) pronounced dorsiflexion ( = hyperextension) of the neck, and (3) partial or complete fusion of the anterior (excluding atlas) neck vertebrae. These specializations are common to both Old World (Dipodidae, Pedetidae) and New World (Heteromyidae) bipeds, but are most pronounced in Jaculus, Dipus, and Dipodarnys (Hatt 1932). Reorganization of the cervical region ap- pears to accomplish two functions. First, it helps to foreshorten the anterior trunk, which tends to keep the distribution of body mass rearward. This eases the problem of counter- balancing the body over the hind limbs when in the bipedal pose. Secondly, modiflcations of the neck increase its mechanical strength and stability while the animal is involved in bipedal hopping. Hatt (1932) argued that neck specialization was required to reduce bobbing of the head. This idea has been ac- cepted by many subsequent workers, but has never been experimentally verified. Hatt himself offered no functional analysis in sup- port of his model. Cheek Pouches Structure, Use and Significance External, fur-lined cheek pouches are a unique, derived feature of geomyoid rodents. They are not present at birth, but rapidly de- velop during the early postnatal period from infoldings of the facial skin (Lackey 1967). In the adult, each pouch opens externally via a long slitlike aperture. Internally, the pouch continues rearward to an expanded base that rests over the shoulder blades. Geomyids can voluntarily evert the pouches for cleaning (Vaughan 1966) and perhaps in some cases to help empty their contents. In both geomyids and heteromyids superficial facial muscula- ture is used to control the tension in the skin guarding the entrance to the pouch and a special "pouch muscle," derived (in part) from the trapezius complex, returns the everted pouch to its normal position (Chias- son 1954, Hill 1937, Howell 1932). Two fairly obvious advantages of cheek pouches are (1) reducing the time required to gather food on the surface, hence reducing exposure to predators and, (2) reducing the locomotor energy expended in foraging, by allowing an animal to collect and store a given amount of food with fewer trips. The latter may be especially important where food resources tend to be widely scattered (Reichman and Oberstein 1977). Another pos- sible advantage of external cheek pouches to desert heteromyids is that of water con- servation. Unlike internal cheek pouches (in- dependently evolved in many mammalian 48 Great Basin Naturalist Memoirs No. 7 f 26 f 34 Fig. 2. Seed pouching in Dipodomys deserti. Tracings of representative frames of slow motion film (200 fps) of D. (U-serti illustrate one complete pouching cycle. Millet seed and the kangaroo rat were placed on a glass surface and filmed from below u.sing a mirror. See text for details. groups; Murray 1975), the fur-lined pouches of heteromyids effectively isolate dry food materials from the moist mucous membranes of the oral chamber. This prevents ab.sorption of water by the food— water that would be lo.st to the environment when the food was later cached in the ground. Given the critical problems of water balance faced by desert heteromyids (see MacMillen, this volume), the savings potentially attributable to the u.se of external cheek pouches may be significant. Previous workers have noted tlie speed with which desert heteromyids are able to collect and pouch seeds. Nonetheless, the speed of food handling has been quantified only for the time required by Pewgnathus and Dipodomys to husk relatively large seeds (Rosenzweig and Sterner 1970). Some insight into the much more rapid process of pouch- ing has been gained recently from high speed films made of an adult female D. deserti col- lecting unhusked millet and sunflower seed from a gla.ss plate. High speed pouching in D. deserti is highly stereotyped. Figure 2 illustrates selected stages in a typical pouching cycle. Both fore- limbs move in synchrony and each limb serves only the ipsilateral pouch. At the in- itiation of the cycle the limbs are thrust for- ward and downward toward the seeds as the 1983 Biology of Desert Rodents 49 hands are simultaneously pronated and opened (Fig. 2: F1-F18). The hands are next closed on the seeds and then retracted to- ward the mouth (Fig. 2: F18-F26). During the retraction stage the hands are supinated so that the palms face directly upward by the time the hands are below the pouch openings (Fig. 2: F26). The forearms are next elevated such that the fingers penetrate into the ex- treme anterior end of the openings (Fig. 2: F34). In the final stage of the pouching ma- neuver, the food is released and the hands are pulled downward away from the mouth ready to commence the next cycle (Fig. 2: F41). The cine records reveal two additional as- pects of the pouching mechanism. First, the reduced first digit ( = thumb) is used in semi- opposable fashion. This small digit is held be- side the large palmar tubercle and, hence, opposes the remaining fingers (II-V) when grasping food items. Second, the pouching cycle of the forelimbs is attended by synchro- nized mandibular movements. Each time the hands are drawn toward the pouches, the mandible is pulled rearward. Opening of the mouth at this time appears to allow the hands to enter the pouches while the pouch entrances are themselves kept tightly closed to prevent the exit of seeds already within them. The backward movement of the lower jaw appears to induce tension in the lips which, during pouching, are pursed behind the incisor teeth. The tension causes the lips to draw inward away from the lateral walls of the pouch, thereby creating small gaps at the extreme front end of the pouch into which the hands are thrust. As the mandible moves forward (= jaw closing), the pouch openings are again closed and the hands withdrawn. Seed pouching in D. deserti is rapid, with a mean pouching rate for millet seed of 9.01 cycles per second. Some cycles are executed in less than 90 milliseconds. Depending on how many seeds are grasped in each hand, pouching rates range between approximately 20 and 60 millet seeds sec'. Though the con- ditions under which these values were ob- tained are admittedly artificial, they indicate the potential speed and efficiency of the pouching mechanism of Dipodomys under fa- vorable circumstances. Unfortunately, com- parable data are not yet available for Pe- rognathus and Microdipodops. Our films also hint at the mechanism by which kangaroo rats distinguish between edible and inedible items during high speed pouching. In no instance were unacceptable items recognized and rejected while in the hands. The films suggest that pouch items are quickly tested for suitability before pouching by being pinched between the pursed lips or, in the case of large items (sunflower seeds), between the lower incisors and the lips. Pinching of the food appears to be another consequence of the coupling of mandibular motion to forelimb movement. Those items judged imacceptable by the "pinch test" are then retrieved from the front end of the pouch and thrown backward beneath the animal. Mechanical Constraints Pouch size is important in that it estab- lishes the maximum quantity of food material that a heteromyid can transport. The rela- tionship between pouch size and body size might therefore influence the foraging tactics of desert heteromyid rodents. To examine this issue, Morton et al. (1980) have recently measured mean pouch volume in 13 popu- lations representing 11 species of hetero- myids and one species of geomyid {Tho- momys bottae). Volume was determined by filling the pouches of dead animals to near capacity with material of uniform size and density (unhusked millet seed; 0.71 g cm -3) and then converting the weight of the con- tents to volume. These authors predicted that pouch volume (Vp) should scale as body mass (Mb) raised to the first power (Mb^o) using the standard allometric expression (y = ax^). They argued that if this relationship existed, larger heteromyids could collect and trans- port more food relative to actual metabolic need (a Mb" '5) than small heteromyids. How- ever, their prediction for the scaling of pouch volume to body size was realized (Vp a }^\)iM3^ only when the sample was limited to small heteromyids (< 30 g) and the much larger pocket gopher (116 g). They found no statistically significant relationship between pouch volume and body size within the genus Dipodomys. To explain this finding, Morton 50 Great Basin Naturalist Memoirs No. 7 B. Fig. 3. A, Stylized illustration of anatomical relation- ship of external cheek pouch to head skeleton in Di- poikmnjs. Principal anchorage of pouch (and contents) to skeleton is to rostmm and mandible at points indicated by arrows. B, Simplified diagram of mechanics of head stability under two locomotor conditions. In .smooth bi- pedal hopping, acceleration of the head relative to pouch contents (Bh) is slight and has a largely horizontal trajectory. The opposing inertial reaction force (Fi) of the pouch load is also small and passes close to the fid- cnnn (dot) at the cranio-cervical joint. Accordingly, the force has a short moment arm (m) about the head-neck joint. The resultant destabilizing torque (= Fi*m) (clockwise) is likewise small and is opposed by a counterclockwise tortjue supplied by the neck muscula- ture (Mn). A much larger and more vertically oriented inertial reaction force (Fi') results from the rapid, steep trajectory of the .head (Pe) as is occasionally seen during predator escape. This force has a large moment arm (m') about the hilcnmi and therefore generates a much great- er destabilizing torque on the head. See text. et al. (1980) suggest that either relatively large body size, a preferred diet of high ca- loric seeds, and/or bipedalism may have re- leased kangaroo rats from normal allometric constraints. Several factors indicate that pouch volume might not increase as the first power of body ma.ss. First, such a relationship implies the maintenance of geometric similarity, a pat- tern rarely encountered within a phylogenet- ic .series encompassing an appreciable range of body size (Gould 1966). Second, in the analysis of Morton et al. an isometric rela- tionship between pouch volume and body mass was produced only when Thoniomys was included, an inclusion that seems unwar- ranted in view of its systematic position, body plan, locomotor mechanics, and forag- ing behavior. Finally, biomechanical con- straints may prohibit the maintenance of geo- metric similarity between pouch volume and body size in heteromyid rodents. All desert heteromyids use some form of saltation, quadrupedal (Perognathus) or bi- pedal {Dipodomys, Microdipodops), when moving fast. Balance and stability are bio- mechanical problems that may increase with speed, especially if the gait involves rapid changes of direction. Several distinctive structural modifications of the neck in biped- al heteromyids appear to relate to the special problem of head stability (see earlier). The mass of the head will be a critical determi- nant of any stabilization mechanism. More- over, the head must enter into any consid- eration of body balance (particularly in bipeds) since it is among the largest and heaviest structures forward of the point of limb support. Anatomically, the cheek pouches are an- chored to the head skeleton (Fig. 3A). At rest, much of the load provided by the pouch con- tents rests upon the back. However, during forward acceleration of the body, the load will tend to shift backward due to inertial lag. An appreciable fraction of this inertial force will act on the head. If the mouth is held closed, most of the inertial force acting on the mandible will be relayed to the ros- trum of the skull through the masseter muscle. The inertial load from each cheek pouch can, for mechanical purposes, be re- garded as concentrated at a single point well out on the rostrum (Fig. 3B). The same figure illustrates the functional consequences of cheek pouch load under two locomotor conditions. In slow, smooth biped- al hopping, accelerational forces are small and the resultant inertial force is nearly hori- zontal. The line of action of this force passes close to the cervicocranial joint, thereby yielding only a modest destabilizing torque on the cranium. In the second case, that of escape from a predator, the animal accel- erates very rapidly in a more vertical trajec- tory, similar to that recorded for Dipodomys merriami when avoiding the strike of snakes 1983 Biology of Desert Rodents 51 en 12 y = .2,3/- / ^_ 10 r^982 y^ y"^ 8 y^ > 6 • •^ D y^ CD 4 • / -o 2 ^ CD •^ tz / c: O) Body Weight (g) Fig. 4. Relationship of head mass to body mass in desert heteromyids (Perognathns, Dipodomys, Micro- dipodops). Negative allometry results in relatively heavi- er heads in smaller species. Restriction of the data set to bipedal forms gives the equation: Mh = .270 X Mb'''^^; r^ = .984; P < .001, where Mh is skinned head mass. (Webster 1961, Webster and Webster 1972) or for Microdipodops when escaping from an- other animal (O'Farrell and Blaustein 1974). Here the inertial force is much larger and passes further from the fulcrum between head and neck. Consequently, the destabiliz- ing moment is much greater. The same in- ertial forces will also generate mechanical problems relative to body balance about the point of limb support in the bipedal pose. Pouch loading can therefore have signifi- cant consequences for head stability and body equilibrium in heteromyid rodents, par- ticularly during rapid escape maneuvers. This fact alone might preclude a simple isometric relationship between pouch volume (which is proportional to load) and body size. Because pouch load is coupled to the head, the man- ner in which head mass changes with body size might well reflect mechanical constraints that, in turn, influence the scaling of pouch size in desert heteromyids. Both head stabil- ity and body balance must be controlled even when the pouches are empty. Head mass scales as approximately Mb"^^^ in desert het- eromyids and as Mb"''^ when the data are limited to bipedal forms {Dipodomys, Micro- dipodops) (Fig. 4). Hence, larger heteromyids have relatively lighter heads than small ones. If, in desert heteromyids, the scaling of head mass is associated with a constant level of function (i.e., stability and balance) with 30 60 90 120 Body Weight (g) Fig. 5. Allometric relationship between pouch vol- ume and body mass in desert heteromyids. Best least squares regression of standard allometric expression (y = ax'') shows that pouch volume scales with strong negative allometry (b = .799) on body mass [Vp = .085 Mb-799. j2 = 739. p < 001] The scaling of pouch vol- ume is fairly closely predicted by the scaling of head mass to body mass in all desert heteromyids (all; b = .834) or just in bipedal forms (bipeds; b = .776). Taxa are identified in Fig. 6. Data from Morton et al. 1980. the pouches unloaded, then continued func- tional equivalence will require that pouch load and pouch volume scale in the same manner as head mass ( = Mb^^^) if the density of the pouched material remains constant. The available data show that pouch volume goes as Mb"^^^*^ for desert heteromyids (Fig. 5). This is close to the prediction of pouch vol- ume made on the basis of head mass (Fig. 4), and far from the original expectation of iso- metry (Mbi<»; Morton et al. 1980). Ecological and Behavioral Implications The present model predicts that head mass and pouch load should scale isometrically with each other, but with negative allometry as regards body weight. The ratio of pouch load to head mass should remain fixed in desert heteromyids regardless of body size. The actual relationship is shown in Figure 6. If the model were correct, all points should fall on the horizontal line indicating isom- etry. Small heteromyids, in fact, clu-ster near the expected value except Perognathtts bail eyi. However, the data for Dipodomys are scattered widely above and below the refer- ence line. But the model predicts the rela- tionship between pouch load and head mass 52 Great Basin Naturalist Memoirs No. 7 °! Low o 1 3 • "D 80 Dmc rs* Pb "'^^ o O O t l^ P.h Do'c Q_ ^•v, • Dp CO CJ "O 40 • rr o a CD • Dm DO Q Q_ ^ 20 • DoA " § High O) ^ c ) 30 60 90 120 Body Weight (g) Fig. 6. Maximum pouch load as percent of skinned head mass in desert heteromyids of different body size. Load is based on maximal filling of pouches with un- husked millet seed. Data are derived from Morton et al. (1980). Each point is mean value for sample of that spe- cies or popidation. Maintenance of mechanical sim- ilarity among species requires that pouch load scale iso- metrically with head mass as indicated by horizontal line. Departure of points from this line may reflect natu- ral differences in foraging behavior and dietary prefer- ence among the taxa, particularly as regards the average density (mass/volume) of the pouch load. See text for discu.ssion. Taxa are: Dd, Dipodomys deserti; Dm, D. merriami; Dmc, D. microps; DoA, D. ordii (Arizona); DoC, D. ordii (California); Dp, D. panamintinus; M, Mi- crodipodops megacephalus; Pb, Perognathus baileiji-, Pf, r. fomiosus; Ph, P. hispidus; PI, P. longimembris; Pp, P. partus. only. It can predict pouch volume only if the physical properties (size, shape, density) of the food filling tlie pouches are the same for all species. This requires, in effect, that all de.sert heteromyids utilize identical food re- sources, a requirement clearly at odds with the actual foraging patterns of these animals (see Reichman, this volume). Because the data illu.strated in Figure 6 were obtained by filling the pouches with a uniform material (millet seed), the scatter of the points directly reflects interspecific or populational differences in relative pouch volume. Those taxa above the reference line have relatively large pouches; those below, much smaller pouch volumes. To conform to the model, species with larger pouches must, in nature, fill them with lighter materials than diose below tlie reference line. What Figure 6 offers, then, is a graphical indication of qualitative and quantitative differences in pouch contents. It suggests, for example, that Perognathus haileiji typically harvests and transports relatively lighter food items than the other Perognathus included in the sample. Similarly, the high degree of scatter within the genus Dipodoinys should reflect considerably greater diversity in foraging be- havior as compared to Perognathus. The least dense pouch materials are predicted in D. microps, an expectation not inconsistent with its tendency toward herbivory (Kenagy 1972, 1973, Csuti 1979). By contrast, the maximum pouch loads of D. merria7ni and D. deserti should average 2.48 and 2.24 times denser than those of D. microps. Still more in- triguing is the apparent disparity between the physical properties of the pouch mate- rials in California and Arizona populations of Dipodomys ordii. Several factors will determine the mean density of the pouch load. Included are the size, shape, and actual density of the individ- ual food particles. Small, round, dense items (certain seeds) should yield the densest pouch loads. Larger or more irregularly shaped items of the same particle density will pro- duce a lower density load. Bulky vegetation (including whole fruiting heads of flowers) will give still lower densities, because it does not pack tightly. Food handling behavior could also affect pouch load. For example, a rodent that husks seeds prior to pouching them is creating a much denser pouch load. Two additional behavioral-ecological pre- dictions derive from a consideration of bio- mechanical constraints imposed by pouch loading. The first is that the right and left cheek pouches should be symmetrically loaded. This follows from the fact that me- chanical stability of the head will be most easily maintained if the weight is equally dis- tributed, thereby providing for some measure of counterbalancing. Symmetrical pouch loading should be most critical to bipedal forms, less important in quadrupedal saltators (Perognathus) and of no consequence to fo.sso- rial geomyids. Next, maximal filling of the pouches in desert heteromyids ought to be on the basis of weight and not volume. As is explained be- low, maximum pouch load is probably estab- lished with regard to predation risk. If the "full pouch" threshold were indeed triggered by weight and not volume, a kangaroo rat harvesting especially dense items might re- turn to its burrow or caching area with the 1983 Biology of Desert Rodents 53 pouches only partially filled. When gathering very light items, the same animal could con- ceivably fill its pouches to their volumetric limit without ever reaching the load limit. The proposed connection between cheek pouch loading and predation again rests with simple biophysical considerations. Suppose a kangaroo rat is sifting the soil for seeds. If suddenly attacked, it will attempt to leap up and away to avoid capture. The rate with which the rodent accelerates away from the attacker is determined by the simple New- tonian relationship, a = F/m, where a is ac- celeration, m is the mass of the animal and F is the propulsive force applied to the ground. If F is the maximmn force the rodent is ca- pable of generating, it follows that maximum acceleration, maximimi take-off velocity and maximum distance covered by the leap (hold- ing take-off angle constant and ignoring aero- dynamic drag) will decline in direct propor- tion to cheek pouch load. Hence, the acceleration of a loaded heteromyid is given by the expression: a = F/(Mb -I- Mp), where Mb is the mass of the body and Mp is the ad- ditional mass added by the pouch contents. If heteromyids load their cheek pouches in constant proportion to head mass (as argued above), the potential consequences for pred- ator escape are easily ascertained. Among desert heteromyids the relative loss of accel- eration due to maximal cheek pouch loading should scale as Mbo^3_i g^ as head to body mass. Small species will therefore be more adversely affected than large ones. All other things being equal, small heteromyids should be at greater risk from predation when trans- porting a full load in the pouches. If, for ex- ample, a 110 g Dipodoniys and a 10 g Pe- rognathus were both carrying pouch loads equaling 50 percent of head mass, the max- imum rate of acceleration of the kangaroo rat would be lowered by 4.6 percent and the pocket mouse would suffer a 6.8 percent loss of function. The ability of heteromyids to accelerate sharply is imdoubtedly a key element in their defense against predators. Although vertical leaps and erratic changes of direction have been recorded for D. merriami (Webster 1962), during predator escape there is some evidence that D. microps nm directly to a burrow or bush when suddenly startled (Quinn 1983). Assuming that predation is a major factor in habitat selection, it is pos- sible, therefore, that the relative effect of pouch load could influence their choice of microhabitat. Small species might be ex- pected to forage preferentially in areas of close cover if exposure to predation and the distance to the nearest protection increases with the "openness" of the habitat. Within both Perognathus and Dipodomys the largest species should be able to successfully operate in the more open habitats since they are less handicapped by pouch load. Strictly speaking, the model predicts dif- ferences in microhabitat availability, not their actual use. On biomechanical grounds large heteromyids are not necessarily ex- cluded from areas of relatively close cover, but small species should be excluded from open areas. The range of microhabitats po- tentially exploited by heteromyids, with re- gard to the mechanics of predator escape, ought therefore to expand with increasing body size. This raises an interesting question with respect to Microdipodops, which is bi- pedal but also in the size range of Pe- rognathus. At present there are insufficient data to compare the foraging tactics of Mi- crodipodops with that of the smallest (but substantially larger) kangaroo rats (e.g., D. merriami, ordii). Theoretically, pouch loading should place a kangaroo mouse at greater risk in open habitats than even the smallest Dipodomys. Unfortunately, we do not yet know how acceleration potential actually scales with body size in heteromyids nor how diis poten- tial compares with the speed of attack by natural predators. These and other con- founding factors might conceivably alter ex- pectations of habitat restriction drawn from simple biomechanical considerations. Still, the present model based on mechanical con- straints offers straightforward predictions that are subject to testing. FoRELIMBS The forelimbs of desert heteromyids have several functional demands placed upon them. Foremost among these are food han- dling and digging. They are also involved in body support and propulsion in Perognathus 54 Great Basin Naturalist Memoirs No. 7 at all speeds, but only at comparatively slow rates of travel in Dipodomys and Microdipodops. Digging Activities Nearly all small desert mammals live be- low ground at least part of the day, where soil acts as a buffer against temperature ex- tremes and desiccation. Below 30 cm of sandy soil, soil temperature remains relative- ly constant throughout the day, despite fluc- tuations of 20 C or more at the soil surface (Kenagy 1973, Larcher 1980). Uniform tem- peratures throughout the year, however, are not achieved except at much greater soil depths. Most desert heteromyids dig elabo- rate multibranched burrow systems (Ander- son and Allred 1964, Culbertson 1946, Quinn 1983, Vorhies and Taylor 1922) where they spend the day. Typically, they emerge above groimd to forage only after sunset. Dipodomys burrows tend to have multiple entrances, which are sometimes plugged dur- ing the day (Hawbecker 1940, Tappe 1941, Vorhies and Taylor 1922). They have a max- imum depth of 30-75 cm (Anderson and Allred 1964, Culbertson 1946, Vorhies and Taylor 1922). The burrows of Perognathus tend to be less branched. Generally they have only one or two entrances and are rather deep, with nest chambers 85-193 cm below the surface (Eisenberg 1963, Kenagy 1973). Little is known about kangaroo mouse (Mi- crodipodops) burrow systems, except that those of M. pallidus and M. megacephalus are short and simple (Eisenberg 1963, O'Farrell and Blaustein 1974), a fact that may mini- mize the energetic cost of torpor (Kenagy 1973). The relative digging abilities of hetero- myids has been given very little consid- eration. There is some evidence, however, that species may partition the land available on the basis of soil composition and particle size (Hardy 1945, Hoover 1973). Some spe- cies appear to be restricted to soft friable soils, but others are able to use harder, rocky soils. This would suggest that some species may be luiable to dig in hard soils. Deynes (1954), however, found that P. merriami gil- vus and P. penniciUatus eremictts were able to dig burrows in heavy clay-loam hard pan. even though they are naturally confined to sandy soils. Digging Methods There are three main methods of digging utilized by heteromyid rodents. Very loose soils, such as dry, fine sand are often moved by pulling small piles of soil between the ani- mals' hind feet using both front limbs simul- taneously. These motions appear to be very similar to those of the forelimbs during high speed pouching of seeds. When a sufficient pile of soil has accumulated under the body, the hind limbs are used to kick the sand fur- ther back. This method of digging is used by D. merriami and D. deserti during surface for- aging and in the initiation of new tunnels. Soils of intermediate hardness are loosened by scratch digging techniques that employ the front limbs in an alternating pattern. This digging method is employed on the surface when burying seeds and foraging as well as underground when constructing or maintain- ing tunnel systems (Eisenberg 1963, 1975, Nikolai and Bramble pers. obsers). Soil loos- ened in this way may be moved with the hind feet by kicking or, when underground, the animal may turn around and push the soil with its forelimbs and chest (Eisenberg 1963). This latter method of transporting soil is in- variably used to move soil up a tunnel ramp preparatory to plugging the entrance (Eisen- berg 1963, Nikolai and Bramble pers. obsers). The soil is then usually patted into place with rapid alternating hand movements. Slow mo- tion films show the frequency of such move- ments to be approximately 11.6 cycles per second in Dipodomys merriami and 5.5 cps in Perognathus formosus when working in damp sand (Table 1). The third method of digging has been ob- -served only in Perognathus on extremely re- sistant soils. Here the animal uses its incisors Table 1. Digging rates for lieteroiiuids in damp packed sand. See text for details. Species BW (g) Digging Patting (stroke/s) (stroke/s) P. hngimembris P. fDnnosiis D. iiicnidini I), denerti 10.0 21.1 42.0 115.0 4.00 7.58 5.27 11.6 8.23 1983 Biology of Desert Rodents 55 to chew through cenientUke soils (Deynes 1954). This digging behavior is similar to that seen in the closely related Geomyidae (Hill 1937). It is conceivable that mechanical re- strictions on gape (Fig. 1) preclude this type of digging in Dipodomys and Microdipodops. Limb Morphology The forelimbs of Dipodomys and Micro- dipodops, like other bipedal rodents, are short compared to the hind limbs (Herman 1979, Howell 1932). Much of the reason for this seems to stem from the strong negative allometry of the hand relative to body size in bipeds as compared to the slight positive al- lometry in quadrupeds. The humerus is abso- lutely shorter in bipeds at all body sizes, but its length increases with body size at the same rate as in quadrupedal species (Table 4). The tiny hands of Dipodomys and Micro- dipodops probably reflect specialization for high speed seed handling and pouching. Rap- id food handling will, in turn, reduce the time an animal must forage beyond the safety of its burrow. The very high rates at which D. deserti pouches seed have already been mentioned. The small hands of the bipedal heteromyids may improve manual dexterity by providing a better fit between hand and small food items. Reduction of the hands may also facilitate high velocity movements of the foreamis by reducing the moment of inertia of the distal limb segments. A reduction of mass will permit higher rates of cyclic os- cillation without an increase in muscular force (i.e., energy expenditure). The absolutely higher rates of limb os- cillation in Dipodomys than in Perognathus while digging (Table 1) is somewhat surpris- ing. Normally, maximum limb frequency would be expected to scale negatively on body mass, as does maximum stride frequen- cy while running in quadrupedal mammals (Heglund et al. 1974). The reduced limb mass associated with the relatively smaller hands of Dipodomys is, however, unlikely to pro- vide a complete explanation for its more rap- id limb movements as compared to pocket mice. We suspect that the faster forelimb movements of Dipodomys may also be the product of historical selection for higher rates of food gleening and pouching. In desert heteromyids each of the four main digits (II- V) bears long, curved but thin claws. The claws are used extensively in bur- rowing but also appear to serve as winnow- ing rakes to snag seeds as the hands sift through fine sediment. The reduced first digit has a naillike covering. As suggested above, this finger seems to be semiopposable in Dipodomys; from its similar structure, the same function may be expected in Micro- dipodops and Perognathus. The scapula and humerus of the bipedal heteromyids resemble, in several ways, those of highly fossorial mammals. The humerus is relatively short, stout, and wide across the distal epicondyles (Howell 1932). The ratio of epicondylar width to humeral length is about .30-.33 and .33, respectively, in Dipodomys and Microdipodops as compared to .34-.36 in the pocket gopher, Thomomys. The relation- ship is .23-. 29 in Perognathus, a value similar to that of generalized quadrupedal rodents (.24-.28) and also close to the figures re- ported for Heteromys (.21) and Liomys (.26) (Wood 1935). The wide epicondyles of biped- al heteromyids and other digging mammals are associated with powerful extensor and flexor muscles of the wrist and hand as well as highly developed pronators and supinators of the forearm (Hildebrand 1982). The scap- ula of all heteromyids and geomyids has a distinct postscapular fossa (Hill 1937, Howell 1932). A similar fossa has been independently evolved in several groups of highly fossorial mammals (e.g., armadillos, badgers, etc.) and is fimctionally associated with an enlarged teres major muscle (Hildebrand 1982). This structural feature is but one of several that hint that the common ancestor of the Hetero- myidae and Geomyidae was more fossorial than the more generalized living geomyoids {Heteromys, Liomys) would indicate. In both heteromyids and geomyids the ability to pronate and supinate the forearm is especially well developed. This ability seems likely to be associated with the maneuvers re- quired (see earlier) to effectively place mate- rials in the cheek pouches. What deserves special notice are the structural special- izations that permit such forearm mobility. Unlike most mammals in which pronation and supination involve chiefly long axis rota- tion of the radius, the movement is accom- plished in geomyoid rodents primarily by 56 Great Basin Naturalist Memoirs No. 7 long axis rotation of the ulna and radius as a unit. Such exceptional motion of the ulna correlates with an extremely "loose" elbow joint in which the ulna is free to deflect in- ward and outward. A special check ligament connects the lateral epicondyle of the hu- merus to the lateral crest of the ulna. It pre- vents excessive medial deflection of the fore- arm on the humerus and serves to stabilize the otheiAvise weak elbow joint when the hand is flexed in the supine position (as in pouching and some digging maneuvers). The ligament cannot, however, strengthen elbow movements when the hand is pronated (palm down), as would be the case in quadrupedal locomotion. This raises the possibility that structural limitations may make bipedalism obligatory for larger desert heteromyids when ninning at higher speeds. The presence of a specialized elbow mechanism in hetero- myids and primitive geomyids (Thomomijs), together with its absence in selected repre- sentatives of other rodent families (i.e., Mu- ridae, Sciuridae, Cricetidae, Zapodidae, Chinchillidae), indicates that the mechanism is derived for rodents but primitive for the Geomyoidea. Hind Limbs and Locomotion The locomotor repertory of heteromyids can be divided into two major classes: biped- al and quadrupedal. Both bipedal and quad- rupedal heteromyids use quadrupedal gaits, such as the walk, half-bound and full-bound during slow progression. These gaits are very similar in their footfall pattern to the gaits used by other quadrupedal rodents (Gam- baryan 1974). At higher speeds, however, some heteromyids {Dipodoinys and Micro- dipochps) employ the bipedal hop, a gait that does not use the front limbs for support. Since much of the thnist of this gait is associ- ated with dorso- ventral oscillation of the ver- tebral column, the bipedal hop is allied with the gallop as an asymmetrical gait (Badoux 1965, Hatt 1932, Howell 1965). A question that has plagued researchers for some time is: Why did bipedalism evolve in some heteromyids and not in others? Bipedal locomotion seems certainly to permit greater specialization of the forelimbs for digging and food handling. Several researchers have also suggested that bipedal locomotion is more energetically efficient than quad- rupedalism (Dawson 1976, Dawson and Tay- lor 1973) or that bipedal locomotion is more effective in predator avoidance (Eisenberg 1975). Based on energetics studies, Dawson (1976) has argued that small bipedal mammals, in- cluding heteromyids, are able to move faster using less energy than their quadrupedal counterparts. This suggests that quadrupedal heteromyids (such as Perognathus, Heteromys, and Liornys) might have foraging strategies that do not utilize high-speed running. Sever- al ecological studies have been undertaken to test this idea (Reichman 1981, Thompson 1980, 1982a, 1982b). A high-speed bipedal gait would be most effectively used by a small desert rodent to avoid predators (avian, mammalian) while moving from its burrow to a protected forag- ing site or from one site to another. Bipedal hoppers may also be more adept than quad- rupeds at avoiding predators in open habitat due to the greater maneuverability and accel- eration offered by the bipedal hop. Further, if bipedal hopping is energetically less costly than quadrupedal nmning, then maximimi speed may be greater in bipedal hoppers than in similarly sized quadrupeds. These considerations seem to imply that quad- rupedal heteromyids might be forced to con- fine their foraging to one or two shrubs close to their burrow entrance, but bipedal hetero- myids may be free to forage imder several more widely scattered shrubs. Thompson (1980, 1982a, 1982b) has compared the forag- ing behaviors of D. deserti, D. merriami, and P. longimembris (see Table 2), and his results seem to support this hypothesis. The energetic cost of locomotion in kan- garoos increases linearly with speed during quadnipedal (pentapedal) movement, but re- mains constant or may even decrease slightly during bipedal hopping (Dawson and Taylor 1973). This contrasts sharply with the pattern of quadrupedal mammals wherein the ener- getic cost continues to increase linearly at all speeds (Taylor et al. 1970). It has been sug- gested that elastic storage of strain energy in the muscles and tendons of the hind limb and back of kangaroos may be responsible for some of their "energy savings" (Alexander 1983 Biology of Desert Rodents 57 Table 2. Comparison of foraging behaviors of bipedal and quadrupedal heteronivids Average slow Average transit No. shrubs Maximum Estimated # Digs and foraging speed between visited/ recorded BW gleans per speed shrubs foraging speed Species (g) minute (km/h) (km/h) hr (km/h) D. deserti 110 5.00' 1.25' 6.33' 8.7' 26.7^ D. merriami 36 5.99' .95' 3.20' 11.3' 22.2- P. longimembris 11 .80' .61' 1.76' 1.8' '(Thompson 1980) '(Thompson, ms.) and Vemon 1975, Dawson and Taylor 1973, Morgan et al. 1978). However, similar studies on small bipedal hoppers, such as kangaroo rats, have yielded conflicting results, with energetic savings indicated in some species (Dawson 1976) and not in others (Thompson et al. 1980, Thompson ms.). Moreover, recent work by Biewener et al. (1981) indicates that storage of elastic energy is not likely in the hind limbs of kangaroo rats due to the rela- tively thick plantar and achilles tendons. Unfortunately, all studies of locomotor energetics in bipedal hoppers have utilized treadmills. Recent experiments have shown that the gait of Dipodomys merriami is sub- stantially altered during treadmill running (Nikolai ms.). On solid ground, for example, stride length and stride frequency both in- crease with speed, but on treadmills the stride frequency remains relatively constant over a broad range of speeds. This, in itself, raises serious questions as to the validity of the energetic cost of bipedal locomotion in rodents as established by treadinill tests. The speed at which gait transitions occur are also higher during treadmill than during overground running (Table 3). Dipodomys merriami utilize three distinct gaits on treadmills and on solid ground: (1) quad- rupedal half bound, (2) tripodal half bound, and (3) bipedal hop. The tripodal half bound is a transition gait between the slower quad- rupedal half bound and the faster bipedal hop, in which only one front limb is used for support during a locomotor cycle (Fig. 7). The use of the tripodal half bound as a transi- tion gait is not completely understood, since by using only one front limb the impact load will be roughly double that where both front limbs are used. In any event, the use of short, relatively weak front limbs as effective shock absorbing devices appears to be limited to slower speeds. The transition from quadrupedal to biped- al gaits is probably not equivalent to the trot- gallop transition of quadrupedal mammals (see Heglund et al. 1974). Because the half bound and bipedal hop are both asymmetri- cal gaits, the quadrupedal-bipedal transition speed should always be higher than the trot- gallop transition speed for a quadruped of equal body weight. Nonetheless, bipedal hop- pers apparently use the quadrupedal half bound at speeds that a similarly sized quad- ruped, of normal limb proportions, would trot (Fig. 8). The trot may not be available to bipedal hoppers due to the difficulty of coordinating hind and forelimbs that differ greatly in length. Impact loading of the forelimbs will in- crease as the inverse ratio of front limb to hind limb length in running mammals (Gam- baryan 1974). When loading of the forelimbs reaches some critical level, bipeds then pre- sumably switch to rear limb support. There- fore, the speed at which the gait changes from quadrupedal to bipedal should be lower in bipedal hoppers with relatively longer hind limbs. Likewise, bipedal hoppers with similar front limb length to hind limb length ratios should have quadrupedal-bipedal tran- sition speeds that conform to a single allo- metric equation (Fig. 8). Dipodomys, which have front limb as a percentage of hind limb ratios of 38.0-43.3, have quadrupedal-bipedal Table 3. Range of speeds for each gait utilized by D. merriami on treadmill and on solid ground. Range of speeds Gait Treadmill (cm/s) Solid ground (cm/s) Quadrupedal half-bound Tripodal half-bound Bipedal hop <115 67-181 >81 <68 44-109 >60 58 LH •- LF -►■ RF H- RH h- Great Basin Naturalist Memoirs Quadrupedal No. 7 LH H LF - Tripodal H 1 RF I I RH»- LH ►■ LF - RF - RH K Bipedal I sec, Fig. 7. Gait diagrams for D. merriami. Three representative gait diagrams depict the footfall patterns of the quad- rupedal bound (top), tripodal half bound (center), and bipedal hop (bottom) at 60 cm /sec. During quadrupedal and tripodal locomotion, front limb support ends at touch-down for the hind limbs. Note that, although speed is the same for all three gaits, stride frequency is highest for the bipedal hop and stride length is greatest for the tripodal half bound. transition speeds = 3.7 (Body Weight) i"'*. Pe- detes capensis, which is morphologically very similar to Dipodomys (Berman 1979), has a ratio of 35.4 and a quadrupedal-bipedal tran- sition of 4 km/hr (Thompson et al. 1980), which is slightly lower than that predicted by the kangaroo rat equation. Kangaroos have ratios of 43.7-47.7 (Gambaryan 1974) and quadnipedal-bipedal transition speeds of 6.5 km/hr (Dawson and Taylor 1978). This is slightly above the value predicted by the Dipodomys equation (Fig. 8). Jerboas of the genus Allactaga have front to hind limb ra- tios of 27.5 (Gambaryan 1974) and therefore should have very low quadnipedal-bipedal transition .speeds. The front limb to hind limb ratio of Perognathus (55.7-57.7) indicate that it would, in theory, be able to hop bipedally only at very high speeds. The limb propor- tions of Microdipodops (51.2) predict a rela- tively high (juadnipedal-bipedal transition speed, but well below that of a similarly sized Perognathns. The ratio of forelimb length to hind limb length has been used extensively as an index of bipedality (Berman 1979, Howell 1932). It is clear that the hind limbs are elongated in bipedal hoppers and that most of the length- ening occurs in the distal segments (i.e., tibia and foot elements) (Berman 1979, Emerson ms., Howell 1932). However, whether or not the forelimbs are shortened relative to body size is the subject of some controversy (Gam- baryan 1974, Howell 1932). Most osteological measures of animal size in common use (i.e., basicranial length, thoracolumbar length, body length) are greatly modified in kan- garoo rats, and therefore of dubious value when making comparisons with more gener- alized rodent species. An exception to this is the length of the basioccipital bone of the skull, which appears to be relatively immodi- 1983 Biology of Desert Rodents 59 8- E "O CD CD Q- O -E ^ if) a O n / / / M M log BW (g) 10 Fig. 8. Gait transition speeds. The trot-gallop transition speed for quadrupeds (dashed line) is 5.5 Mb-^ (Heglund et al. 1974). The quadrupedal-bipedal transition speed for kangaroo rats (solid line) is 3.7 Mb-^'^'^ (Nikolai ms.). The measured quadrupedal-bipedal transition speeds for bipedal hoppers are: (a) Red kangaroo (18 Kg), [K], 6.5 Kin/hr (Dawson and Taylor 1973); (b) Pedetes sp. (3 Kg), [P], 4.0 Km/hr (Thompson et al. 1980); (c) D. deserti (.104 Kg), [D], 2.5 Km/hr (Tliompson et al. 1980); (d) D. merriami (.0426 Kg), [M], 2.2 Km/hr (Nikolai ms.); (e) D. merriami (.032 Kg), [M], 2.0 Km/hr (Thompson et al. 1980). See text for details. Bed in kangaroo rats, as well as in many other mammals (L. Radinsky, pers. comm.). In desert heteromyids basioccipital length scales isometrically with body mass. We have therefore used this as a standard against which limb segment lengths are compared (Table 4). The hind limbs of Dipodomys and Micro- dipodops are greatly elongated, and all three limb segments show strong positive allometry with respect to body size (Table 4). The foot and tibia are much longer in bipedal rodents than in similarly sized quadrupedal rodents, and there is a lesser difference in femur size (see also Herman 1979). It is interesting that as body size increases the relative length of the hind limb increases in bipedal hetero- myids {Dipodomys and Microdipodops). This may have important biomechanical con- sequences. Since body mass scales as a vol- ume and muscular strength as a cross section- al area (Alexander 1968), the ability of the leg muscles to absorb the shock of impact during bipedal hopping should decrease with increasing body size if geometric similarity is maintained. Increasing the length of the leg, however, will increase the contact time and thus the time course over which impact shock can be absorbed. The ratio of calcaneal length to total foot length also increases with body mass in bipedal hoppers [= .09 + .514 Mb, R2 = .72, P < .02 for 7 species of Di- podomys and Microdipodops], thus improving the mechanical advantage of the large ankle extensor muscles. The vertebral column, pelvic girdle, and hind limb musculature of bipedal hetero- myids are considerably modified compared to quadrupedal species (Berman 1979, Hatt 1932, Howell 1932). In general, the long 60 Great Basin Naturalist Memoirs No. 7 Table 4. Comparison of the allometric equations of limb segment length of bipedal heteromyids and quadrupedal rodents using basioccipital length as a standard unit of relative body size. See text for details. [Bipedal heteromyids: M. megacephaliis (1), D. merriami (2), D. ordii (3), D. microps (3), D. spectabilis (1); Quadrupedal rodents: P. long- imembris (1), P. fomiosus (3), ?. parvus (2), Tlwmomys sp. (2), Pewmyscus sp. (1), Neotoma sp. (2), Eutamicis sp. (1), Citelhis sp. (1)]. Number of animals in parentheses. Bipedal heteromyids Quadrupedal rodents ANCOVA Power Coefficient Humerus 2.9 (B.O.)ii^"° 4.1 (B.O.)i-3l°°° N.S. ooo Radius 3.0(B.O.)-85- 3.7(B.O.)ii5°°° N.S. N.S. Hand 1.9 (B.O.) ■^^°°° 2.9(B.O.)iii°" oo ° Femur 5.7(B.O.)i-29"° 5.1 (B.O.)i-3i°°° N.S. ° Tibia 7.7 (B.O.)ii9"° 5.8(B.O.)iii°" N.S. ooo Foot 8.6(B.O.)i-20°° 5.1 (B.O.) -s^"" o o N.S. •p< .05 °p < .01 •p < .001 back muscles are greatly enlarged, the pelvic girdle-sacral joint is strengthened, and the cervical and thoracic regions are shortened. The major muscle masses of the hind limbs are concentrated proximally and become highly tendinous distally to reduce the mo- ment of inertia about the hip joint during locomotion. Experimental studies indicate that at lower bipedal speeds most of the thrust at takeoff is derived from the ankle and hip extensors. The ankle extensor muscles are larger and have greater mechanical advantage in Di- podoniys and Microdipodojjs than in Liomys and Perognathiis (Herman 1979). As speed in- creases, the role of the large back muscles, .such as the longissimus series, increases with increasing back extension at takeoff. Based on angle measurements, knee extensors also play an increasing role at higher speeds (Biewe- nier et al. 1981, Pinkham 1976, Williamson and Frederick 1977). The quadniceps and hamstring muscles are probably important in shock absorption during landing. Some elastic storage may come from these muscles; how- ever, this is probably not significant for kan- garoo rats (Biewenier et al. 1981). The tail of Dipodomys is elongated, with a rectangular cross section and a terminal tail tuft. It is u.sed as a counter-rotator during bi- pedal locomotion to counteract the torque applied to the long axis of the body by the limbs. The tail reaches the highest point of its swing cycle just before touchdown. The strong tail depressor muscles (e.g., iliocau- dalis, pubocaudalis, flexores caudae) pull the tail down during the contact phase so that the tail is at its lowest point just after take-off (Fig. 9) (Nikolai ms.). The tail elevator mus- culature is linked to the large back extensor muscles in such a way that when the back is extended the tail is automatically elevated (Howell 1932). Most of the extension of the back occurs during the latter portion of the contact phase of a locomotor cycle; thus, when the tail depressor muscles are relaxed after takeoff, the tail is automatically ele- vated. Some elastic storage in the dorsal tail tendons seems likely. As the thrust of the hind limb increases with speed, the swing of the tail likewise increases to counteract torques about the center of mass (Fig. 9). During the quadRipedal half bound, the tail is limp and does not oscillate in the same manner as it does during bipedal locomotion (Nikolai, unpubl. data). Foot length scales approximately isometri- cally with tail length in kangaroo rats [foot length = .36 (tail length) ^44 R2 = .923], but shows strong negative allometry in pocket mice [foot length = 1.29 (tail length) ^^s r^ = .945]. This implies that kangaroo rats maintain geometric similarity with respect to the tail and foot length, but larger pocket mice have relatively longer tails and shorter feet. This relationship in Dipodomys is con- sistent with the presumed importance of the tail as a counter-rotator during bipedal loco motion. It has been suggested that the tuft of hair on the tip of the tail is effective as a flag to distract predators during high-speed pred- ator avoidance maneuvers. The tuft may also alter the aerodynamic properties of the tail so as to make it more effective as a rudder or counter-rotator during locomotion (Hatt 1932, Howell 1923). 1983 Biology of Desert Rodents 61 Sr ^^^^^e::^ ^r:^^^^ 80 • • '''' \- 60 . "' X^ "' ' 40 * V » • *:^r'^ 20 ^' ' ,^ Speed (m/s) Fig. 9. Use of the tail in D. merriarni. During bipedal hopping the long axis of the body shows very little rota- tion about the center of mass. During a locomotor cycle the legs exert a rotating torque on the center of mass (Pinkham 1976, Nikolai, unpubl. data). The rotation of the tail is always in a direction opposite to that of the leg (as indicated by the arrows on the tracings of repre- sentative frames from a single locomotor cycle of a D. merriarni traveling at 100 cm/sec on a treadmill). The tail reaches its highest point just prior to touch-down (A) and reaches its lowest point just after take-off (B). The maximum arc described by the base of the tail increases with increasing speed (dashed line) to counteract the torque applied by the legs. [Degrees rotation = 9.164 -I- 19.6 (speed in m/s); R2 = .80; P < .001; N = 57 for 2 D. merriarni running on a treadmill] (Nikolai, nis.). Limited data are available on the relative growth rates of the hind foot, tail, body length, and body mass for several species of desert heteromyids (Butterworth 1961, Chew and Butterworth 1959, Hayden and Gambino 1966, Lackey 1967, Reynolds 1960). How- ever, to date there has been no real attempt to determine how: (1) ontogenetic scaling of body proportions relates to the development of bipedal locomotor ability during growth; or (2) ontogeny might provide a vehicle for morphologic adaptation in the evolution of bipedalism through heterochronic mecha- nisms (e.g., Alberch et al. 1979). We suspect that a closer examination of these issues might prove especially worthwhile. Origins of Bipedalism Why has bipedalism evolved in desert ro- dents? This is a persistent question for which three main explanations have been advanced: (1) to facilitate escape from predators (Bar- tholomew and Caswell 1951, Eisenberg 1975, Hatt 1932); (2) to free the forelimbs for ef- ficient food handling (Bartholomew and Carey 1954); and (3) to reduce the energetic cost of locomotion (Dawson 1976, Reichman and Obserstein 1977). As was indicated ear- lier, recent evidence appears to discredit the latter hypothesis, leaving only predation and food handling as alternative models. The two are, however, strongly interrelated. Three general features describe bipedal ro- dents: (1) all inhabit (or forage in) relatively open habitats where the risk of predation is presumably high; (2) all are nocturnal; and (3) all tend to be solitary. The first factor has been much emphasized but may not, in fact, be the most critical. Other rodents, especially sciurids, successfully occupy open environ- ments but none are bipedal. They are, how- ever, mostly diurnal and often exhibit a high degree of sociality (Armitage 1981, Barash 1973, Sherman 1977). The close approach of a predator to such rodents is made difficult by intense illumination and the fact that the detection of predators is a responsibility shared by conspecifics within a living area. Some Dipodomys and Jaculus respond to novel objects and small predators in their ter- ritories by thumping the ground with the hind feet (Eisenberg 1975). Such behavior might conceivably alert nearby conspecifics of potential danger, but true alarm calls have not been reported for any bipedal rodent. That a predator might more closely ap- proach a solitary rodent at night seems highly probable. If so, its attack will be initiated at closer quarters, thereby demanding a more rapid and forceful response by the prey if capture is to be avoided. Dipodomys mer- riarni, for example, appears to have httle trouble in jumping away from the strikes of nearby rattlesnakes (Webster 1962, Webster and Webster 1972). Perhaps the most impor- tant advantage conferred by bipedalism is the ability to execute a rapid, controlled leap di- rectly from a feeding (or pouching) posture. Virtually all quadrupedal rodents sit semi- erect while feeding or manipulating food with the forelimbs. When forced to flee, such animals must normally drop onto the front limbs before initiating a flat trajectory leap off the rear limbs. The brief time required to do this may be of small consequence to a 62 Great Basin Naturalist Memoirs No. 7 diurnal rodent but could easily spell the dif- ference between capture and escape to a soli- tary, nocturnal animal in open terrain. Morphological specialization for leaping among vertebrate animals invariably results in elongation of the hind limbs relative to the forelimbs (Herman 1979, Howell 1965). As a consequence, the forelimbs will necessarily incur higher mechanical stresses as they act as shock absorbers to break the fall of the longer, faster bounds generated by the rear legs (Gambaryan 1974). Stress on the fore- limbs will be amplified if a high-speed bounding gait incorporates abrupt changes of direction, since the front limbs brake the for- ward momentum of the body as the turn is executed. Quadnipedal mammals with such gaits (e.g., cursorial lagomorphs, ungulates) exhibit extreme modification of the elbow to increase its resistance to injury. Long axis ro- tation of the radius and ulna is severely cur- tailed or eliminated (Hildebrand 1982, How- ell 1965). This effectively precludes pronation and supination of the hands, mak- ing them nearly useless in feeding. In all bi- pedal rodents, by contrast, the hands are used extensively in feeding and digging. There has presumably been strong selection for the rap- id, efficient use of the forelimbs in order to reduce foraging time. It is in this context that tlie evolutionary significance of bipedalism becomes clearer. This locomotor strategy seems to offer the only viable means of com- bining, in a single animal, limb special- izations and functions which are otherwise incompatible. The notion that bipedalism in rodents is di- rectly linked to the occupation of open, arid habitats is seriously contested only by the modem Zapodidae. These rodents favor mes- ic, well-vegetated environments both in the New and Old worlds. Their possible relation- ship to the Dipodidae (Eisenberg 1981, Fokin 1978) as well as the presumed bipedal habits of 7Aipus would seem to make the locomotor behavior of the.se rodents of special value in unraveling the history of bipedalism in desert rodents. However, although Zapus is unques- tionably capable of rapid, prodigious leaps, there seems to be no solid evidence that it is really capable of sustained, bipedal saltation. Slow motion films of Zaptis princeps running and leaping on solid ground as well as on a treadmill show that the forelimbs are in- volved in body support and shock absorption in every stride (Bramble and Nikolai pers. obs.). Further evidence of quadrupedal rather than bipedal bounding is found in the struc- ture of the limbs. The forelimb-hindlimb length ratio of Zapus is similar to that of bi- pedal heteromyids (i.e., Microdipodops; Ber- man 1979), but the forelimb is constructed differently. Forelimb length relative to body size is comparable to that seen in generalized quadrupedal rodents. The hand is large rather than reduced, and there are no obvious specializations favoring pronation and supi- nation of the forearm. We tentatively con- clude that true bipedal locomotion probably does not exist in the Zapodidae and that leap- ing specializations of this group have little to do with the evolutionary pathways leading to bipedal saltation in modern desert rodents. The development of bipedal saltation as seen in modern heteromyids cannot have been associated with the occupation of desert environments as we know them today. True deserts of North America appear to be of fairly recent origin (i.e., later Pleistocene; Van Devender 1977), whereas heteromyids exhibiting structural modification for bipedal saltation date from at least the later Miocene (Voorhies 1975, Wood 1935). Voorhies' (1975) recent suggestion that bipedalism may have first arisen among primitive dipodo- myines living in sandy, floodplain habitats deserves special consideration. Such re- stricted environments may occur within otherwise typical savannah habitat and may be relatively arid during periods of low rain- fall. More importantly, sandy floodplains are frequently characterized by widelv .scattered vegetation and thus qualify as "open" habi- tat. If bipedal heteromyids arose under con- ditions such as these, their distinctive lo- comotor specializations may have considerably predated other specific adapta- tions (mostly physiological) to desert life. Literature Cited Ai.nKiuH, P., S. J. Gould, C. F. Osteh, and D. B. Wake. 1979. 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Williamson, R. G., Jr., and E. C. Frederick. 1977. A functional analysis of ankle extension in the rico- chetal rodent (Dipodomijs merriami). Zbl. Vet. Med. C. Anat. Histol. Embryol. 6:157-166. WisNER, A., J. P. Legouix, and F. Petter. 1954. Etude Histologique de L'Oreille d'un Rongeur a Rulles Tympaniques Hypertrophies, Meriones crassus. Mammalia 18:.37i-374. Wood, .\. E. 19.35. Evolution and relationsliips of the heteromyid rodents with new forms from the Tertiary of western North .\inerica. (Jarnegie Mus., Ann. 24:73-262. 1937. Parallel radiation among the geomyid ro- dents. J. Manunal. 18:171-176. ADAPTIVE PHYSIOLOGY OF HETEROMYID RODENTS' Richard E. MacMillen' Abstract.— Heteromyid rodents are distributed from the New World tropics to the deserts of North America, but their habitation of deserts is relatively recent. Their evolutionary history, though, is associated with progressive arid- ity, with larger quadrupedal taxa being more mesic (and primitive), and smaller quadrupeds and all bipeds more xer- ic. The correlation between water regulatory efficiency and body mass is strongly negative in heteromyids; bipedal Dipodomys spp. have water regulatory efficiency fixed at an intermediate level independent of mass. Heteromyids generally have basal metabolic rates reduced below the eutherian level, with the greatest reductions occurring in desert species. The use of torpor as an energy-conserving device is cosmopolitan in small (<40 g) heteromyids, but is inconsequential or lacking in larger ones. Bipedalism, characteristic of Dipodomys, confers no direct energetic ad- vantages as revealed in treadmill studies. Large quadmpedal heteromyids have adaptive physiologies suitable for more mesic habitats, but smaller quad- rupeds are suited for xeric existence*^; these characteristics likely reflect an evolution from a tropical ancestry to rather recent habitation of deserts. Bipedalism occurs only in xeric-adapted forms and has no directly discernible energetic benefit; yet it appears to relieve in some unknown way the energetic constraints of foraging. The genera and species of the family Het- eromyidae are distributed along a pro- nounced gradient of water availability in the New World ranging from the wet tropics of Central and South America to the driest deserts of North America (Hall 1981). This present-day distribution mimics the paleo- climatological history of the family, starting with a tropical ancestry, followed by an adaptive radiation throughout the Tertiary in response to progressive aridity and sea- sonality of rainfall, and culminating in the di- verse favma of desert heteromyids with which we are so familiar (Axelrod 1958, Hall 1981, Reeder 1956, Wood 1935). With this in mind, it is my contention that tropical heteromyids may be viewed at least ecologically as ances- tral models of early heteromyids, the desert forms as advanced derivatives, and those oc- cupying intermediate habitats as transitional fonns. Thus, extant species should provide us with important clues concerning the evolu- tionary and ecological trajectories of the fam- ily at the levels of physiology, morphology, and behavior. The quadrupedal heteromyid genera (Het- eromijs, Liomys, Perognathits), at least with respect to locomotion, are the more general- ized, and the bipedal members {Dipodomys, Microdipodops) are the more specialized. In addition, the quadrupedal members span the entire distributional range and nearly the en- tire size range of the family, but the bipedal forms are confined to semiarid and arid habi- tats, and (with the exception of the small-in- size Microdipodops) occupy the upper por- tion of the size spectrum (Hall 1981). By in- spection (Hall 1981), there is a strong posi- tive correlation within the quadrupedal heteromyids between body size and moistness of the habitat, suggesting that reductions in body mass may confer a selective advantage upon quadrupedal heteromyids living in more arid habitats; on the other hand, the arid-adapted bipeds are commonly relatively large and show no apparent relationship be- tween the body mass of individual species and habitat aridity, suggesting a linkage be- tween bipedality and aridity independent of body mass. Herein, I explore certain aspects of water and energy regulatory physiology of hetero- myid rodents, paying particular attention to patterns related to habitat, body mass, and/or locomotor mode. 'From the symposium "Biology of Desert Rodents," presented at the annual meeting of the A University, 20-24 June 1982, at Snowbird, Utah. ^Department of Ecology and Evolutionary Biology, University of California, I Society of Mammalogists, hosted by Brigham Young California 92717. 65 66 Great Basin Naturalist Memoirs No. 7 HETEROMYIDAE Di Dodom vs MASS (g) Fig. 1. The double logarithmic relationships between water regulatory efficiency (T^ (a MWP = EWL) and body mass in 5 genera and 13 species of heteromyid ro- dents. Regression lines are provided for all species (solid line) and Perognathus spp. (dot-dash line), and both have significant slopes (F test, P < .05). The horizontal line (dashed) represents the average value for all Dipodomtjs, which did not have a significant regression. The regres- sion lines are fit to all the values for each species; the regression equations are T^ (S (MWP = EWL) = 29.682g-<^l3''' in all 13 heteromyid species, and \ (a (MWP = EWL) = 31.078g-"^'^ in Perognathm spp.; the mean value for Dipodomys spp. is 18.1 ± SD 0.6 C. The heteromvid species employed span the geographic, climatological, and body mass ranges of the family and include Dipodomys deserti, D. merriami, D. ordii, D. panamintinus, Heteromys desmarestianus, Liomys irro- ratus, L. salvini, Micwdipodops megacephalus, Per- ognathus baileyi, P. fallax, P. flatus, P. hispidus, and P. kmgimembris. After MacMillen and Hinds (in press). Water Regulatory Efficiency Numerous accounts in the literature attest to the relatively great powers of water con- servation in heteromyid rodents, and indicate that the arid-adapted forms (Dipodomys, Mi- cwdipodops, Perognathus) are conservative often to the point of exogenous water inde- pendence (MacMillen 1972, Schmidt-Nielsen et al. 1948; pers. obs.), and the more mesic adapted forms (Heteromys, Liomys) are less conservative in their water economies and re- quire dietary augmentation of exogenous wa- ter (Hudson and Rummel 1966, Fleming 1977). I (MacMillen 1983) have argued that the conservative nature of heteromyid water economy, regardless of habitat, is likely linked to the family's dietary specialism, granivory: this is became rodents in particu- lar depend upon a common resource packet to meet nutrient, energy, and water needs, and those that u.se the driest packets (seeds) are the most conservative in their water economies. With the supposition that heteromyids are relatively conservative in their water econo- mies, and that, at least for the quadrupedal species, body mass might be positively corre- lated with moistness of the habitat and nega- tively correlated with economical water regulation, MacMillen and Hinds (1983) un- dertook an examination of water regulatory efficiency in extant heteromyids that includ- ed both quadrupedal and bipedal members across the entire taxonomic, distributional, and size ranges of the family. This exam- ination was based on a model that predicted that water regulatory efficiency is negatively related to body mass and positively related to ambient temperature. Our criterion of water regulatory efficiency is that ambient temper- ature (Ta) at which the major avenue of water input (metabolic water production, MWP) just balances the major avenue of water out- put (evaporative water loss, EWL). Thus, the model predicts that those species achieving water balance (MWP = EWL) at the highest TaS are the most efficient in water regulation, being able to subsist exclusively on air-dry seeds to meet both energy and water needs while active on the surface even under warm conditions. A test of the model in which we evaluated simultaneously MWP and EWL from Ta = 5-35 C in 117 individuals, 13 spe- cies and 5 genera of heteromyids, confirms our predictions for the family in general (Fig. 1). However, when the two most speciose genera (Perognathus, Dipodomys) are treated separately, Perognathus spp. conform even more strongly (possess a steeper slope) to the model, but in Dipodomys spp. water regu- latory efficiency is fixed at an intermediate level independent of body mass (Fig. 1). This intergeneric break in patterns of water regu- latory efficiency coincides with a break in body mass (ca 35g) and a break in locomotor mode, points whose relevances will be dis- cussed later in this paper. Basal Metabolic Rate It has long been known that the basal metabolic rates (BMR) of mannnals are loga- rithmically correlated with bodv mass (Klei- ber 1932). This scaling of BMR with body mass in mammals was statistically refined by Brody (1945) and Kleiber (1961) to provide indistinguishable regression equations for predicting BMR for mammals of any known ma.ss: BMR (cm^ Oa/g.h) = 3.8 W(g)-o27 1983 Biology of Desert Rodents 67 (Brody 1945) or M=3.5W-o25 (Kleiber 1961; see MacMillen and Nelson 1969 for con- version of equations from animal-specific to mass-specific values). Rodents, too, conform in general to these allometric expectations (Morrison 1948), but Dawson (1955) was the first to suggest that heteromyid rodents may have BMR reduced below the expected lev- els. Hudson and Rummel (1966) confirmed this suggestion for the subtropical species Liomys salvani ( = L. salvini?) and L. irro- ratiis; more recently McNab (1979) has shown through a search of the literature and his own measurements that, of the hetero- myid species for which measurements were available (12 species, all 5 genera), only a tropical Heteromys {H. anomalus) possessed a BMR at or exceeding the Kleiber prediction- all others were reduced. Furthermore, McNab's (1979) analysis revealed the BMRs of Perognathiis spp. were not only reduced, but also were independent of body mass; it is interesting to note that the four Perognathiis measurements were from four different laboratories. Our studies of water-regulatory efficiency as described above and in MacMillen and Hinds (1983) provide a rich data base from a single laboratory for comparing mass-related aspects of water and energy metabolism both within the family Heteromyidae, and with eutherian mammals in general. We are pre- paring a major synthesis of heteromyid meta- bolic allometry (Hinds and MacMillen, in preparation), and so the following summarize only briefly the most pertinent information related to BMR. Because our criterion of water regulatory efficiency required that our animals be oxi- dizing food of known composition at the time of measurement of oxygen consumption (V02), our animals were not postabsorptive when measured in thermal neutrality, and hence did not conform strictly to the require- ments for BMR. The animals were oxidizing millet (81.4 percent carbohydrate, 5.1 per- cent lipid, 13.5 percent protein), which should elevate metabolic rate due to the spe- cific dynamic action (SDA) of food utilization by about 9 percent above basal levels (Brody 1945). In spite of the possible influence of SDA on metabolic rate of our specimens, it is apparent that the basal metabolic rate of the ::_-.f^ ^BRODY ^^XKLEIBER .Jj. 10 50 100 MASS (g) • Perognafhus BDipodomys •Heteromys AMicrodipodops ▼Liomys Fig. 2. The double logarithmic relationship between mass-specific basal metabolic rate and body mass in het- eromyid rodents, using the same species as indicated in Figure 1. The dashed line is the allometric expectation for eutherian mammals from Brody (1945); the dot-dash line is the expectation for eutherians from Kleiber (1961). The solid line is fit to the data for heteromyids by the regression equation BMR = 3.69 W(g)-0-28 (Sy, = .010, Sb = .028, r2 = 0.504). The geometric symbols represent different genera as indicated on the figure. The BMR values employed in this analysis are the two lowest measures of Vq, for each individual at that T^ in thermal neutrality for which the mean Vo, of that spe- cies was lowest (after Hinds and MacMillen, in prepara- tion; data collection as in MacMillen and Hinds, in press). heteromyids we tested is depressed below the values predicted by either the Brody (1945) or Kleiber (1961) relationships (Fig. 2). Correcting for SDA would yield even greater depressions. The slope of the regres- sion line relating BMR to mass of hetero- myids (-0.28) is statistically indistinguishable from that of Brody (-0.27) and Kleiber (-0.25). Using the raw data of Brody (1945), a direct comparison can be made of elevation between his and the heteromyid data sets, which shows that, at the mean body mass (ca 30g) of the heteromyids employed, hetero- myid BMR is significantly (P < .05) reduced by 1 1 percent of that predicted for eutherian mammals in general (following method of comparing elevations by Snedecor 1956 and Zar 1974). Of the 13 heteromyid species in- cluded in Figure 2, 5 {Dipodomys deserti, D. merriami, Perognathiis haileyi, P. fallax, P. longimembris) are from severe desert scrub habitats, and their BMR collectively is re- duced by 24 percent below that predicted for eutherians. Great Basin Naturalist Memoirs No. 7 Lastly, the 5 Perognathus spp. conform strongly to the relationship between BMR and body mass, with no indication of the mass-independent relationship reported by McNab (1979) on data emanating from sever- al laboratories. Since two of the four Pe- rognathus species included in McNab's (1979) analysis were also employed in ours {P. long- imemhris, P. hispidiis) the discrepancy is likely due to interlaboratory differences in measuring BMR rather than to interspecific deviations in metabolism. This attests to the importance of using only data collected from a single laboratory when undertaking meta- bolic comparisons at lower taxonomic levels. Thus, it is concluded tliat heteromyid ro- dents have reduced BMR (and metabolic rates in general) and that the reductions are not only recognizable at the taxonomic level, but are most pronounced in those members living imder more arid conditions. Bipedal Locomotion The fact that heteromyids are divided in locomotor habits into quadrupedal and bi- pedal forms, and that the latter are confined to semiarid and arid habitats within the fam- ily distribution, suggests the presence of ad- vantages inherent in bipedalism tliat favor an arid existence. Howell (1933) observed that Dipoclornys occurred predominantly in open terrain, where bipedality conferred a com- bination of fast, erratic movements and bal- ance that enhanced predator escape to the extent "that no mammal can catch this ro- dent in fair chase, but only in stealth." Also favoring the hypothesis that bipedality in Dipodornys aids primarily in predator escape and avoidance were Bartholomew and Cas- well (1951), who stated "the entire economy of the animal is set up for efficient evasion of danger in areas relatively devoid of cover, which emphasizes that survival in this species has been dependent upon a series of mutually supporting adaptations of which its locomo- tor equipment is the most obvious." Recently, investigators have measured the actual costs of locomotion through indirect calorimetry of mammals nmning on tread- mills. These studies have concentrated on quadrupedal ninning and show considerable uniformity in the scaling of energetic costs to body mass (Taylor et al. 1970). The first sug- gestion that bipedal hopping might confer unusual energetic benefits was by Dawson and Taylor (1973), who reported that red kangaroos, while hopping, effectively had energetic costs that were independent of run- ning speed, i.e., a bipedal plateau. Shortly thereafter Fedak et al. (1974) reported data suggesting that for small animals (< lOOOg) the cost of transport for bipeds (exclusively birds) is less than that for quadrupeds (ex- clusively mammals). This contention was re- versed by Fedak and Seeherman (1979) and Paladino and King (1979), who demonstrated independently, using a more extensive data set including quadnipedal mammals and liz- ards and bipedal birds and mammals, that there is no difference in the scaling of energy requirements for locomotion between bipeds and quadrupeds, but only differences be- tween clumsy and graceful runners. But these latter studies, as opposed to Dawson and Taylor's (1973) with the kangaroo, employed animals that were either two-legged bipeds (primates and birds) or four-legged quad- rupeds (other mammals and lizards), and not mammals that at slower running speeds are pentapedal (kangaroos) or quadnipedal (for example, heteromyids), but then become bi- pedal at faster speeds. Dawson (1976) and Baudinette et al. (1976) measured the energetic costs of locomotion in two species of Australian murid hopping mice {Notomys cervinus and N. alexis, respec- tively) that are ecological and physiological equivalents to bipedal heteromyids (MacMil- len and Lee 1969, 1970). Both species had similar patterns relating oxygen consumption (Vq^) to running speed with a positive linear relationship at slower speeds (< 2.0 km/h) and a plateau at higher speeds (> 2.0 km/h). Dawson (1976) reports intermittent use of both quadrupedal running and bipedal hop- ping at plateau speeds, but Baudinette et al. (1976) report only quadrupedal running. In addition, Dawson (1976) suggests that the plateau in N. cervinus is aerobic and there- fore represents a real energetic savings re- lated to elastic energy storage compared to that during strictly quadrupedal running. Baudinette et al. (1976) are less committal and imply that the plateau may be either an aerobic one dependent upon elastic storage. 1983 Biology of Desert Rodents 69 or it may be purely anaerobic, occurring at the level of maximal aerobic capacity. Clear- ly this plateau can represent an energy- conserving mechanism only if aerobic. My recent treadmill studies of the meta- bolic cost of locomotion in small bipedal and quadrupedal mammals have concentrated on heteromyid rodents. Initial results that com- pare nmning and hopping costs of four spe- cies of small bipeds (0.03 to 3.0 kg; Rodents: Heteromyidae: Dipodotnys merriami, D. deserti; Pedetidae: Pedetes capensis; Marsu- pialia: Macropodidae: Bettongia penicillata) show no aerobic bipedal plateau while hop- ping at any of the speeds tested. Further, a plateau could be induced in poorly trained individuals that ran in an oscillatory manner, but this disappeared when they were trained to Rm smoothly (Thompson et al. 1980). To confirm further the presence or absence of a bipedal plateau in Dipodomys spp., si- multaneous measurements of Vog and Vco2 were made in D. ordii while running on a treadmill, and of blood lactate immediately after Rmning. The results are reported in Figure 3. At low running speeds (<3.0 km/h) V02' Vcog^ and blood lactate are positively and linearly related to speed. At higher run- ning speeds (> 3.0 km/h) Vq^ plateaus dis- tinctly, Vcog continues to increase linearly but with a shallower slope, and blood lactate continues to increase sharply, but with the possibility of a plateau at 4.0 and 5.0 km/h. At Ruining speeds above 4.0 km/h there is a distinct decline in the willingness of indi- viduals to Rm, with typically less than one- half of the individuals that readily ran at lower speeds willing to run at the higher speeds sufficiently long (2-3 min) to reach steady state. It is unlikely that this unwilling- ness to run at higher speeds for even short periods of time was due to hyperthermia. As Wunder (1974) has noted, no inhibition of running in D. ordii accompanied moderate hyperthermia while Rmning at lower speeds (<1.8 km/h), but did for prolonged periods of time (10-15 min). The transition from quadrupedal to bipedal running occurs be- tween 3.0 and 4.0 km/h, with most of the Vq^ plateau coincident with bipedal locomotion. I am convinced, however, that the Vq^ plateau depicted in Figure 3 is anaerobic, and therefore cannot be construed as an 6. 6 3 2 -># 14 4 1^ -J»VC02 V02 ■'> a QoaoOooRQ J i 1 I I 2 3 4 5 6 VELOCITY (km/h) Fig. 3. A. The relation between oxygen consumption (Vq,) and carbon dioxide production (V^o,) and velocity in Dipodomys ordii running on a treadmill at Tg = 20 C. The treadmill was enclosed in a Plexiglas chamber through which air was pulled at a rate of 4.1 L/min. Vq, and Vcoo were measured with an Applied Electro- chemistry S-3A oxygen analyzer and an Infrared In- dustries carbon dioxide analyzer. All measurements were corrected to STPD. The dashed line is fit to the Vq data between 1 and 3 km/h by linear regression analysis and is described by the equation cm-^/g'h = 0.91(km/h) + 4.46 (Sy, = 6.58, Sb = 0.60, i^ = 0.64); the line has a significant positive slope (F test, P < .05). The solid line is fit to the Vco, '^^^'^ between 1 and 3 km/h, and between 3 and 6 km/h. Both have significant slopes, and are described by the equations cni''/g*h = 1.65(km/h) -I- 2.88 (Sy, = 0.67, Sb = 0.43, i^ = 0.81) and cm3/g-h = 0.36(km/h) -I- 6.83 (S^, = 0.58, Sb = 0.89, r^ = 0.21). The numbers represent the number of measurements obtained at each speed from a total of 13 individuals. Solid circles represent mean V^Og measure- ments, hollow circles represent mean Vq, measure- ments, vertical lines represent the interval A ± 1 SD, and hollow squares represent mean RQ values (Vc02/V02). B. The relation between blood lactate and velocity m D. ordii running on a treadmill at Ta = 20 C. Each ani- mal was allowed to mn at one speed for 2-5 min during 'CO2 and these measurement.s are included in the data depicted in Fig. 3A. It was then im- mediately removed, a blood sample was taken from the orbital sinus within 30 sec of removal, and the whole blood placed in perchlorate solution. Lactate concentra- tion was determined using a Boehringer-Mannheim lac- tate test kit. Each hollow triangle represents one value from a different individual, with a total of ten values (in- dividuals). The solid line is fit to the data by regression analysis and is described by the equation mg% = 46.234 (km/h) - 13.638 (i^ = 0.825); the slope is significant (F test, P < .05). 70 Great Basin Naturalist Memoirs No. 7 energy-conserving mechanism. The mean Vq^ between 3.0 and 6.0 km/h (7.34 ± SD 0.57 cmVg.h; N = 52) falls within the 95 percent confidence intervals predicted for maximal aerobic capacity (Vq^ max) in a small mam- mal (X body mass = 52.7 g) from Lechner's (1978) allometric relationship: V02 max = 0.499 W 678 (V02 is in cmVmin, and W is mass in g). The mean V02 for D. ordii between 3.0 and 6.0 km/h, however, falls below the 95 per- cent confidence intervals for S/q^ max as pre- dicted by Taylor et al. (1980): Vo^max = 1.92W.809 (V02 is in cmVsec, and W is mass in kg). Lechner's (1978) relationship included Vo^ max induced by cold, helium-oxygen mixtures or running, in 14 small mammals species (< 2.6 kg), 11 of which were rodents. Taylor et al. (1980) confined their measurements to treadinill running, with the majority of their mammals large (> 2.6 kg) or very large; of the 21 species for which measurements are reported, only 4 are rodents while 11 are un- gulates. It is difficult to resolve the dis- crepancies between these two relationships, as their data bases differ taxonomically, methodologically, and by body mass. Our protocol is most similar to that of Lechner (1978) in terms of taxonomy and body mass, and resembles that of Taylor et al. (1980) methodologically . Additional confirmation that the Vq^ plateau reported above for D. ordii is an- aerobic comes from the analysis of blood lac- tate following nmning at the highest speeds tested. The mean of four values for D. ordii after ninning 2-3 min at 4.0 and 5.0 km/h is 201.9 ± SD 34.8 mg percent. This mean, and three of the four values fall within the 95 percent confidence intervals around the mean (190.7 ± SD 9.1 mg percent) of blood lactate levels of 9 mammalian species nm- ning on treadmills at Vo^ max, as reported by Seeherman et al. 1981. The fourth value lies above the confidence intervals. Thus, it is ap- parent from the perspectives of Vq^ and blood lactate levels that the bipedal plateau we observed in D. ordii is anaerobic. Finally, Biewener et al. (1981) have examined with the use of force plates and X-ray cine- matography bipedal hopping in Dipodomys spectabilis and conclude that elastic storage of energy in this kangaroo rat is much less than in kangaroos. The adaptive significance of bipedality in heteromyids has yet to be demonstrated with rigorous laboratory and field tests. The most plausible current explanation is the original one proposed by Howell (1933) and Bartholo- mew and Caswell (1951) that bipedality aids in predator avoidance and escape. I believe it is additionally possible that bipedality con- fers other locomotor advantages not readily translatable into energetic currency, such as enhancing acceleration and burst speeds. These ideas have yet to be tested. Use of Torpor Torpor (or natural hypothermia), in which body temperature and energy metabolism are reduced well below normothermic levels, ei- ther on a circadian basis or for longer peri- ods, is well documented in virtually all heter- omyids whose mean body masses are typically less than 40 g (i.e., all Perognathiis spp., Microdipodops paUidus, and M. mega- cephahis, pers. obs., Bartholomew and Cade 1957, Bartholomew and MacMillen 1961, Cade 1964, Tucker 1965, Wang and Hudson 1970, Wolff and Bateman 1978). In larger quadrupedal heteromyids (i.e., Heteromys, Liomys) torpor has not been observed (pers. obs., Fleming 1977, Hudson and Rummel 1966). Torpor appears to be a weakly devel- oped capacity in Dipodomys, having been documented in D. merriami (Dawson 1955, Carpenter 1966, Yousef and Dill 1971), D. panamintinus (Dawson 1955) and observed in D. deserti (pers. obs.). In all instances tor- por in Dipodomys spp. was induced by star- vation and/ or cold stress, and frequently re- sulted in death during torpor or after arousal. In the few Dipodomys spp. in which torpor has been documented it appears to be best (but still weakly) developed, as a circadian phenomenon, in the smallest species, D. mer- riami (> 35 g). I have seen no convincing evidence that torpor in Dipodomys spp. is an ecologically meaningful phenomenon. Among Perognathiis spp., there appear to be two prevailing patterns in the use of tor- por: (1) those that emplov it as an emergency 1983 Biology of Desert Rodents 71 energy-conserving mechanism for short peri- ods of time (one to several days) to avoid temporarily inhospitable surface conditions {P. californicus. Tucker 1962; P. flavtis, Wolff and Batemann 1978); and (2) those that are or nearly are obligate hibernators, and abandon surface activity for several months each winter (P. longimembris, Kenagy 1973; P. parvus, Meehan 1976). The determinants of one pattern or the other are unknown, but they are not taxonomic because both patterns occur in each subgenus. In Microdipodops spp., torpor appears to be employed on a short-term basis, as both species can be trapped all year, even during winter on sub- freezing nights, except for those occasions when the substrate is frozen (Brown and Bar- tholomew 1969, Hall 1946; pers. obs.). In both Perognathus and Microdipodops, as in Dipodomys, the periodicity of torpor seems to be based on a circadian schedule with indi- viduals initially torpid during the usual daylight hours and normothermic at night (Brown and Bartholomew 1969, Carpenter 1966, French 1977, Meehan 1976, Tucker 1962). If conditions that foster the use of tor- por prevail, whether it be in obligate hi- bernators or short-termers, circadian bouts of torpor may extend into those of greater dura- tion, some lasting several days (Brown and Bartholomew 1969, French 1977, Meehan 1976). Whether torpor be circadian or of longer duration, or whether the use of torpor bouts be confined to short periods of in- hospitable surface conditions or to a com- plete winter season, its adaptive significance to these granivores is linked primarily to energy conservation, enabling its prac- titioners to subsist for short or longer periods in underground burrows on a finite energy store in the form of seed hoards at a fraction of the energetic cost they would expend if continually normothermic (Brown and Bar- tholomew 1969, Kenagy 1973, Meehan 1976, Tucker 1966). For torpor to serve efficiently as an energy-conserving mechanism in hetero- myids, its use must be accompanied by preci- sion of control. Such precision has been dem- onstrated in Microdipodops pallidus by Brown and Bartholomew (1969), who have shown that periodicity and duration of torpor bouts is related to ambient temperature and food supply in such a way that individuals in- variably maintain body weight and accumu- late seeds, even at very low temperatures and on seed rations reduced considerably below the normothermic requirement. An addition- al example of precision of energetic control while using torpor is seen in Perognathus par- vus (Meehan 1976). This species is an obli- gate hibernator, and in Great Basin habitats in California is dormant in burrows typically from November through March, employing periodic bouts of torpor that may last as long as eight days interrupted by only brief (< one day) periods of arousal. In the laboratory during winter months P. parvus establishes large seed hoards (i.e., an energy surplus) and, while maintained at ambient temperatures equivalent to winter burrow temperatures (ca 5 C), spontaneously enters torpor; torpor bouts are initially circadian followed by pro- gressive increases in duration until, com- monly, individuals are torpid for five or more days at a time. Meehan's data imder simu- lated winter conditions indicate that individ- uals are torpid, with body temperature (Tb) approximating T^, 90 percent of the time, and expend only 16 percent of the energy that would be expended if normothermic in an insulated nest in the burrow; this energy savings would obviously be increased several- fold if compared with the cost of nightly for- aging on the surface. The magnitude of energetic savings while torpid is demonstrated in Figure 4, which shows that at T^ = 2 C (approximating win- ter burrow temperatures) the metabolic cost for torpid mice is 3 percent of that for resting nontorpid animals. The extraordinary preci- sion of thermoregulatory control while torpid is also demonstrated in Figure 4: at T^s be- tween 2 and -2 C (and at a Tb barely above freezing) P. parvus is capable of activating the heat production machinery sufficient to maintain Tb at or slightly above 2 C. Thus, with tissues approaching freezing, these ani- mals are capable of maintaining a constant body temperature at very low metabolic cost, thereby avoiding prohibitively costly normo- thermia and at the same time ensuring con- tinuing survival throughout a winter season of underground dormancy. 72 Great Basin Naturalist Memoirs No. 7 c 6 i8 jg, ^0 ■ ° A 5 ■ o 8'° CO 4 O 03° ^^ 3 ? o 2, 1 • L o 8 70 g) quadrupedal granivores/frugivores whose cheek pouches enhanced foraging success for a single re- source packet (seeds and/ or fruits) that pro- vided virtually all nutritional needs. These ancestral heteromyids would have possessed powers of water regulation consistent with the amomit of preformed + oxidative water yielded from the food, and equivalent to that predicted for a quadrupedal heteromyid of that mass as depicted in Figure 1. At the time of their origin they likely possessed a BMR close to that typical of eutherian mammals, as in Heteromys and Liomijs (Fig. 2). From the heteromyid origin throughout the remaining Tertiary, the geographic re- gion of heteromyid evolution (southwestern North America) was subjected to progressive aridity and seasonality of rainfall (Axelrod 1958); this was most pronounced in areas oc- cupied by today's deserts (i.e., around 30° N latitude) and less pronounced with proximity to the equator. The progression of aridity and seasonality of rainfall would have resulted in shorter growing seasons, reduced primary production, and vegetational emphasis on seasonal seed production (rather than fruit) as a reproductive strategy. I envision the heter- omyid responses to these climatic and biotic changes to include tracking the increases in aridity and accompanying temporal and vol- umetric reductions in seed production with reductions in body mass; such reductions in mass would promote increases in water- regulatory efficiency consistent with water yield (MWP) from a dry foodstuff (as seen in Fig. 1) and decreases in absolute energy needs per individual. Concomitant with this would have been reductions in BMR (and overall energy metabolism) comparable to those observed in Figure 2, thereby even fur- ther decreasing absolute energy needs in hab- itats with more limited seed production. The trade-off for decreases in body mass in these .still quadrupedal forms would have been an increase in mass-related locomotor costs (Taylor et al. 1970), offset at this stage by re- ductions in BMR and continuing enhance- ment in foraging efficiency promoted by the use of cheek pouches. According to my sce- nario, species that are physiologically (and 1983 Biology of Desert Rodents 73 ecologically) ancestral and transitional would have persisted through the present in habitats of appropriate rainfall and seed production patterns, most typically in tropical and sub- tropical settings. Tlie next sequence of events followed con- tinuing reductions in mass of quadrupedal heteromyids down to about 35-40 g, at which some critical event(s) occurred, result- ing in the locomotor dichotomy between quadrupedality and bipedality (and the even- tual origins and adaptive radiations of Pe- rognathus and Dipodoniys). During the devel- opment of this dichotomy, water regulatory efficiency became fixed at an intermediate level and independent of mass in Dipodomijs; in Perognathus, as in other quadrupedal het- eromyids, water regulatory efficiency con- tinued to increase concomitant with further reductions in body mass as the prevailing pattern of increasing aridity continued. Also, it is suspected that the capacity for torpor was developed just prior to the dichotomy in locomotion, and at some critical, relatively small mass (ca 40 g) at which the costs of quadnipedal foraging during periods of ex- cessive energy demand (low temperatures and/ or reduced seed availability) exceeded the benefits. Torpor would represent a phys- iological alternative to relieve either tempo- rarily or for longer periods the energetic trade-off in the inefficiency of locomotion in- herent with smaller mass: during energeti- cally stressful periods or seasons for surface activity, the energetic savings of torpor in the burrow might more readily promote posi- tive energy balance. An alternative explana- tion for the evolution of torpor in smaller heteromyids as a trade-off for locomotor in- efficiency might simply be the inability of in- dividuals of small mass (and a high sur- face:volume ratio) to increase heat production sufficiently to offset heat loss dur- ing extreme cold, resulting in hypothermia. This alternative would be independent of food-finding ability. The evidence that torpor was developed in heteromyids at or prior to the locomotor dichotomy is that it occurs in both Perognathus and Dipodoniys (see ear- lier); it is a finely timed energy-conserving device in the former (Fig. 3), but is only la- tently present in the latter and is likely a rel- ictual capacity. Both Perognathus and Dipodoniys were present in upper Tertiary times (Lindsay 1972, Shotwell 1967, Reeder 1956, Wood 1935), long before the formation of true deserts in southwestern North America (Ax- elrod 1950). Voorhies (1974, 1975) has de- scribed as fossils a Perognathus sp. and a bi- pedal kangaroo rat (Eodipodomys celtiservator) preserved in their burrows in early Pliocene deposits in northeastern Ne- braska. Preserved with them were seed hoards indicative of their granivorous habits, and their habitat was interpreted to be a riv- erine area traversing a grassland with a mild, equable climate. Shotwell (1967) describes fossil Dipodornys spp. and Perognathus spp. from the middle Pliocene of Oregon with no reference to probable habitat, and Lindsay (1972) reports the presence of Perognathus spp. in middle Miocene deposits in what is now the Mojave Desert of California, again with no reference to probable habitat. It is apparent that Perognathus and Dipodornys were geographically wide-spread throughout much of southwestern North America in up- per Tertiary times, and inhabited areas pre- dominantly grassland and semiarid in nature (Reeder 1956). The formation of true deserts resulted from the late Pliocene-Pleistocene uplift of the Sierra Nevada-Cascade axis, together with the transverse and peninsular ranges of Cali- fornia and Baja California and the ensuing rainshadow effect (Axelrod 1950, 1958). Pe- rognathus and Dipodoniys, representing lin- eages that for many millions of years had been subjected to progressive aridity, likely were preadapted to a desert existence, and occupied this still more arid, new environ- ment without much further modification. Bipedalism, as exhibited by Dipodornys species, would by my scenario have devel- oped in semiarid, open habitats, likely grass- lands, as an aid in traversing the expanses be- tween foraging sites. It represents an adaptation tliat could then readily be ex- ploited in desert habitats. Although there is no evidence that bipedal locomotion in Di- podornys confers a direct energetic advantage (Fig. 4), I think there can be no question that it provides some as yet undefined relief (i.e., foraging advantage) from energetic con- straints that would be imposed on a quad- 74 Great Basin Naturalist Memoirs No. 7 ruped of the same mass and habitat. The evi- dences for this statement are these: (1) in spite of relatively large mass and large abso- lute energy requirements while living in hab- itats of limited seed production, torpor is sel- dom if ever used; (2) a fixed, intermediate level of water regulatory efficiency restricts seed usage to those higher in carbohydrate composition and therefore higher in MWP (MacMillen and Hinds, 1983); and (3) cheek pouch volume (i.e., food-carrying capacity) in granivorous Dipodomijs spp. is independent of body mass, but it is strongly and positively correlated with body mass in quadrupedal heteromyids (Morton et al. 1980). Thus, ac- companying bipedality in Dipodomys are several characteristics that can be construed as energetically liberal, at least in comparison with their quadrupedal cousins, whom they typically exceed in biomass when sympatric (pers. obs.). Yet to be demonstrated are the direct advantages of bipedality in hetero- myids; among these is the likelihood of en- hancing predator avoidance and escape, but others should not be dismissed without trial. Another mystery among heteromyids, at least to me, is Microdipodops, which inhabits exclusively Great Basin deserts. Their habi- tats are not only arid but of high elevation, and, therefore, have markedly truncated growing seasons. They are mysterious be- cause virtually nothing is known of their ori- gins, or whether they are more closely re- lated to Perognathus or Dipodomys. Authorities align them more closely with one or the other (Hafner 1978, Lindsay 1972), not particularly close to either (Reeder 1956), or change their minds (Wood 1931, 1935). This lack of agreement is due largely to the ab- sence of a fossil record. It is due in part, too, to the bipedal mode of locomotion in Micro- dipodops and the assumption that this implies close relatedness to Dipodomys. Nevertheless, Wood (1935) emphasizes that bipedalism has arisen several times independently in hetero- myids, including extinct lineages only re- motely related to extant genera; I see no rea- son to doubt an independent origin of bipedalism in Microdipodops. Microdipodops are also mysterious from a physiological point of view. To me they represent an enig- matic compromise that combines the water and energy regulatory virtues of Perognathus and Dipodomys: they are small in size with low absolute energy requirements and ef- ficient water regulatory capacities; they uti- lize torpor most propitiously; and they are bipedal. They are deserving of more attention. The family Heteromyidae is a rather di- verse group of rodents with respect to their adaptive physiology. Yet, when interpreted in light of locomotor and size differences within the family, together with paleoclima- tological histories, discernible patterns emerge that are consistent both evolution- arily and ecologically. Acknowledgments Much credit for idea formulation, data col- lection and reduction, and field companion- ship is given to D. S. Hinds. Thanks are ex- tended to W. L. Bretz and K. G. Cunningham for additional aid in data collec- tion and reduction, to R. W. Putnam for aid in blood lactate determinations, and to Barb MacMillen for typing the manuscript. Con- tinuing appreciation is extended to Hi Ho Sai Gai. Financial support for this study was pro- vided by NSF grants DEB-7620116 and DEB-7923808. Literature Cited AxELBOD, D. I. 1950. The evolution of desert vegetation in western North America. Carnegie Inst. Wash- ington, Publ. 590:215-360. 1958. Evohition of the Madro-Tertiarv Geoflora. Bot. Rev. 24:433-509. Bartholomew, G. A., and T. J. Cade. 1957. Temper- ature regulation, and aestivation in the little pocket mouse, Perognathus longimembris. J. Mammal. .38:60-72. Bartholomew, G. A., Jr., and H. H. Caswell, Jr. 1951. Locomotion in kangaroo rats and its adaptive sig- nificance. J. Mammal. 32:155-169. Bartholomew, G. A., and R. E. MacMillen. 1961. Ox- ygen consumption and hibernation in the kan- garoo mouse, Microdipodops pallidus. Phvsiol. Zool. 34:177-183. Baudinette, R. v., K. a. Nagle, and R. A. D. Scott. 1976. 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Small mammal fossils from the Barstow formation, California. Univ. California Publ. Ceol. Sci. 93:1-104. MacMillen, R. E. 1972. Water economy of nocturnal desert rodents. Symp. Zool. Soc. London 31:147-174. 1983. Water regulation in Peromyscus. J. Mamm. 64:38-47. MacMillen, R. E., and A. K. Lee. 1969. Water metab- olism of Australian hopping mice. Comp. Bio- chem. Physiol. 28:493-514. 1970. Energy metabolism and pulmocutaneous water loss of Australian hopping mice. Comp. Biochem. Physiol. 35:355-369. MacMillen, R. E., and D. S. Hinds. 1983. Water regu- latory efficiency in heteromyid rodents: a model and its application. Ecology 64:152-164. MacMillen, R. E., and J. E. Nelson. 1969. Bioenerget- ics and body size in dasyurid marsupials. Amer. J. Physiol. 217:1246-1251. McNab, B. K. 1979. Climatic adaptation in the energet- ics of heteromyid rodents. Comp. Biochem. Physiol. 62A:813-820. Meehan, T. E. 1976. The occurrence, energetic signifi- cance and initiation of spontaneous torpor in the Great Basin pocket mouse, Perognathus parvus. Unpublished dissertation, Univ. of California, Ir- vine. Ill pp. Morrison, P. R. 1948. Oxygen consumption in several mammals under basal conditions. J. Cell. Comp. Physiol. 31:281-292. Morton, S. R., D. S. Hinds, and R. E. MacMillen. 1980. Cheek pouch capacity in heteromyid ro- dents. Oecologia 40:143-146.' Paladino, F. v., and J. R. King. 1979. Energetic cost of terrestrial locomotion: biped and quadruped run- ners compared. Rev. Can. Biol. 38:321-323. Reeder, W. G. 1956. A review of Tertiary rodents of the family Heteromyidae. Unpublished dissertation. Univ. of Michigan, Ann Arbor. 618 pp. Schmidt-Nielsen, B., K. Schmidt-Nielsen, A. Brokaw, and H. Schneiderman. 1948. Water conservation in desert rodents. J. Cell. Comp. Physiol. 32:331-360. Seeherman, H. J., C. R. Taylor, G. M. O. Maloiy, and R. B. Armstrong. 1981. Design of mammalian respiratory system. II. Measuring maximum aero- bic capacity. Resp. Physiol. 44:11-23. Shotwell, J. A. 1967. Late Tertiary geomyoid rodents of Oregon. Univ. Oregon Mus. Nat. Hist. Bull. 9:1-51. Snedecor, G. W. 1956. Statistical methods. Iowa State College, Ames. 534 pp. Taylor, C. R., K. Schmidt-Nielsen, and J. L. Raab. 1970. Scaling of energetic cost of running to body size in mammals. Amer. J. Physiol. 219:1104-1107. Taylor, C. R., G. M. O. Maloiy, E. R. Weibel, V. A. Langman, J. M. Z. Kamau, H. J. Seeherman, and N. C. Heglund. 1980. Design of the mammalian respiratory system. III. Scaling maximum aerobic capacity to body mass: wild and domestic mam- mals. Resp. Physiol. 44:25-37. Thompson, S. D., R. E. MacMillen, E. M. Burke, and C. R. Taylor. 1980. The energetic cost of biped- al hopping in small mammals. Nature 287:223-224. Tucker, V. A. 1962. Diurnal torpidity in the California pocket mouse. Science 1.36:380-381. 1965. Oxygen consumption, thermal con- ductance, and torpor in the California pocket 76 Great Basin Naturalist Memoirs No. 7 mouse, Perognathiis californiciis. J. Cell. Comp. Physiol. 65:393-403. 1966. Diurnal torpor and its relation to food consumption and weight changes in the Califor- nia pocket mouse Perognathiis californiciis. Ecol- ogy 47:245-252. VooRHiES, M. R. 1974. Fossil pocket mouse burrows in Nebraska. Amer. Midi. Nat. 91:492-498. 1975. A new genus and species of fossil kangaroo rat and its burrow. J. Mammal. 56:160-176. Wang, L. C, and J. W. Hudson. 1970. Some phys- iological aspects of temperature regidation in the normothermic and torpid hispid pocket mouse, Perognathiis hispidus. Comp. Biochem. Physiol. 32:275-293. Wolff, J. O., and G. C. Bateman. 1978. Effects of food availability and ambient temperature on torpor cycles of Perognathiis flaviis (Heteromijidae). J. Mammal. 59:707-716. Wood, A. E. 1931. Phylogeny of the heteromyid ro- dents. Amer. Mus. Novitates 501:1-19. 1935. Evolution and relationships of the hetero- myid rodents with new forms from the Tertiary of western North America. Carnegie Museum. Ann. 24:73-261. WuNDER, B. A. 1974. The effect of activity on body tem- perature of Ord's kangaroo rat {Dipodomijs ordii). Physiol. Zool. 47:29-36. YousEF, M. K., and D. B. Dill. 1971. Daily cycles of hi- bernation in the kangaroo rat, Dipodomijs mer- riami. Cryobiology 8:441-446. Zar, J. H. 1974. Biostatistical analysis. Prentice-Hall, Inc. Englewood Cliffs, New Jersey. 620 pp. BEHAVIOR OF DESERT HETEROMYIDS' O. J. Reichnian- Abstract.— Activity patterns of desert heteromyids are characteristic of many nocturnal rodents, with a peak of activity near dusk and a second prior to dawn. Seasonal activity varies with environmental conditions, going from ac- tivity throughout the winter in larger species to extended periods of torpor by smaller pocket mice. The rodents for- age primarily for seeds, with pocket mice tending to feed under shrubs and on relatively low-density seed patches and kangaroo rats frequently foraging in the open for relatively high-density seed patches. The animals are usually solitary, with aggression exhibited between and within species. Burrow construction can be simple to extensive. Communication occurs visually, with odor (especially at sand bathing sites), and with sound (drumming). Reproduc- tive behaviors are characterized by brief courtships and copulation. Subsequent maternal behavior includes nursing, grooming, and other forms of general maintenance. Individuals spend considerable time autogrooming, presumably to enhance temperature regulation and reduce parasite attack. Although many of the behavioral patterns seen in heteromyids are similar to other rodents, locomotory and auditory specializations appear to yield behaviors charac- teristic of the group of rodents. Observational and anecdotal information pertinent to heteromyid behavior is present in the literature beginning around the turn of the century. Although these early pieces of information are valuable in themselves, they offer no coherent view of behaviors across geographic or taxonomic boundaries. The landmark work of Eisenberg (1963) provided a turning point, and much of the work on heteromyid behavior since that time has used heteromyids as tools to answer questions of a more general and conceptual nature. Although heteromyids suffer from many of the same problems other mammals do for be- havioral studies (e.g., nocturnal activity and subterranean burrows and nests), they do of- fer some distinctive benefits. For example, all heteromyids possess external fur-lined cheek pouches that are used during foraging for gathering seeds. Thus, whereas most animals eat their food as they collect it, heteromyids have separate collecting and ingesting behav- iors. Also, some heteromyids (kangaroo rats and kangaroo mice) exhibit a distinctive sal- tatorial bipedal locomotion important for foraging and/ or predator avoidance behav- iors. The deserts inhabited by heteromyids tend to be relatively open, allowing observa- tion of these types of activities under special conditions (e.g., with light-amplifying de- vices). The rodents also are ammenable to laboratory manipulation and observation, al- though breeding these rodents in the labora- tory is difficult. In addition, the seeds the ro- dents eat are particulate and thus relatively easy to quantify and analyze in studies of diet choice and foraging. With these distinctive features in mind, I will discuss heteromyid activity patterns, foraging, spacing, territo- riality and aggression, reproduction, anti- predator behavior, burrow construction, sen- sory abilities, and personal care. When I mention heteromyids in the context of some specific behavior, it is not to imply that all heteromyids exhibit that behavior. Readers should note the citations and recognize that the generalizations actually refer to the spe- cific animals studied by the authors cited. Activity Activity patterns are usually inferred from the number of individuals in a population ac- tive during specific times of a diel or annual cycle. This should probably be considered a population phenomenon and I will concen- trate on what aspects of the environment might generate those patterns and briefly dis- cuss torpor and its use. Biology of Desert Rodents," presented at the annual meeting of the American Society of Mammalogists, hosted by Brigham Young 82, at Snowbird, Utah. 'From the symposia . ^^ University, 20-24 June 1982, at Snowbird, Utah ^Division of Biology, Kansas State University, Manhattan, Kansas 77 78 Great Basin Naturalist Memoirs No. 7 In general, heteromyids respond to pre- dictable daily and seasonal cyclical patterns in their environments as well as specific pre- dictable weather phenomena. Heteromyids are primarily nocturnal (Kenagy 1973a, Lockard 1978, Reichman and Van De Graaff 1973), although diurnal activity is occasion- ally noted. Relatively high winds or precipi- tation can decrease or halt normal nocturnal activity (Kenagy 1973a, Lockard 1978). On two occasions I have noted, after an evening thunderstorm, that all wet individuals in traps were juveniles and all the adults were dry, suggesting that adults did not come out to forage imtil after evening rains. There is conflicting evidence for moonlight avoidance in heteromyids. Kenagy (1976a) and Schroder (1979) noted no moonlight avoidance in kangaroo rats, but Kaufman and Kaufman (1982) and Lockard and Owing (1974) sug- gest they do avoid moonlight. It should be noted that these stvidies were in different areas on different species. Evidence pre- sented by Lockard (1978) may provide an ex- planation of the disparity in the other re- ports. He suggests that Dipodomys spectabilis may avoid moonlight, presumably because of increased susceptibility to predation, during times of the year when food is abundant, but be forced into periods of moonlight activity when resources are scarce. Rosenzweig (1974) presents a conceptual explanation for this phenomenon. Various aspects of heteromyid activity re- late to temperature and rainfall (French 1975, Kenagy 1973a, 1976a). Reichman and Brown (1979) elaborate on these aspects of activity and note, along with Brown and Bar- tholomew (1969), that the amount of food is also important in determining above-ground activity. When temperature or food avail- ability is low (usually in the winter; French 1976), small heteromyids will tend to go into or stay in torpor for extended periods of time (perhaps up to 5 months; Reichman and Van Dc Graaff 1973). Apparently, larger hetero- myids (approximately 18g -I-) rarely use tor- por (Bartholomew and MacMillen 1961, Eis- enberg 1963, French 1976, Kenagy 1973a, O'Farrell 1974, 1980). Whereas small homeo- therms are probably more affected by cold temperatures than large ones, the larger spe- cies may be more affected by heat. Reichman and Van De Graaff (1973) noted that during one extremely hot summer, activity of indi- vidual kangaroo rats was reduced but pocket mice remained active. Two miscellaneous features of heteromyid activity need to be mentioned. Schmidley and Packard (1967) noted that four species of pocket mice could swim by treading water for approximately one minute before becom- ing exhausted, floating, eventually losing coordination, and drowning. Stock (1972) found that nine species of kangaroo rats were "good" swimmers in artificial ponds and aquaria. Finally, Kenagy and Enright (1980) show that the activity of D. merriaini in the laboratory was depressed for five days prior to a large earthquake, especially in the pre- midnight phase. This reduced activity abruptly disappeared the night after the earthquake. Foraging Desert heteromyids are primarily gra- nivorous (Bradley and Mauer 1971, Brown et al. 1979, Reichman 1975, 1978), although they may seasonally ingest large quantities of green vegetation and insects. One study sug- gests that as individual kangaroo rats encoun- ter water stress by eating too many high- protein mesquite seeds, they switch to eating the herbaceous seed pods (Schmidt Nielson et al. 1948). Many species of heteromyids can apparently go without drinking free water for long periods of time, supporting them- selves on metabolic water from food items (see MacMillen, this volume). Eisenberg (1963) noted that young heteromyids eat sol- id food from the time their incisors erupt. There are important exceptions to the spe- cialized granivory exhibited by heteromyids. Kenagy (1972, 1973b) detailed the use of salt- bush leaves (Atriplex) by Dipodomys rnicrops. Individuals of this species use their chisel- shaped teeth to strip away the salt-laden epi- dermis of the Atriplex leaves before ingesting them. Csuti (1979) noted a similar behavior and suggested that it was innate because indi- viduals from areas without saltbush devel- oped the behavior as juveniles as quickly as those from areas where saltbush was preva- lent, but Dipodomys ordii never learned the leaf-stripping behavior. Reichman (1975, 1983 Biology of Desert Rodents 79 1978) and Tappe (1941) noted the high use of insects seasonally, and Vorhies and Taylor (1922) report an observation of a kangaroo rat chasing and catching a moth. Kenagy and Hoyt (1980) report the reingestion of feces by D. microps and show that the animals differ- entially ingest those fecal pellets that are rel- atively low in inorganic ions and relatively high in nitrogen and moisture. The diets of heteromyids apparently affect other behaviors. For example, several authors have noted the relationship between the in- gestion of green vegetation and subsequent reproduction (Kenagy and Bartholomew 1981, Reichman and Van De Graaff 1975, Van De Graaff and Balda 1973). There also is apparently a relationship between the inges- tion of ants by heteromyids and subsequent infection by alimentary canal helminths, al- though the effect of this infection on individ- uals is unclear (Gamer et al. 1976). One of the most striking aspects of the for- aging behavior of desert heteromyids is the short length of time they actually spend above ground searching for food. Schreiber (1973) reports total foraging times of up to five hours per night for P. parvus, although most other reports are for significantly short- er periods. Kenagy (1973) reports total times averaging one hour, which includes time spent in the burrow on return trips. The short amount of time spent foraging is less striking when it is recognized that seeds are a rela- tively rich resource that can occur in high- density patches (Reichman and Oberstein 1977). A parameter that is perhaps more sig- nificant ecologically than simple total for- aging time is the time spent at each foraging stop (time in a patch) and the time (and dis- tance) between patches. Bowers (1982) noted that in a three-species commimity the small- est pocket mice exhibited the shortest times within and between patches, and kangaroo rats had the longest times for both. An intermediate-sized pocket mouse was also in- termediate in these two time parameters. Thompson (1984) also found that the relative- ly larger bipeds spend more time stopped, and travel longer distances between stops, than the smaller quadrupeds. Another distinctive feature of desert heter- omyid foraging is the bipedal hopping of the kangaroo rats (Bartholomew and Caswell 1951) and kangaroo mice. This contrasts with the quadrupedal locomotion of the pocket mice (Bartholomew and Gary 1954). Signifi- cantly, almost no overlap in body size occurs between the quadrupedal pocket mice and bipedal kangaroo rats, although kangaroo mice are small and the quadrupedal P. his- pidis approaches the size of some of the smallest kangaroo rats. Currently some ques- tion over the adaptive significance of these different locomotory techniques exists; this will be discussed later by Price and Brown (this volume). There are indications that some desert het- eromyids climb occasionally or extensively. Kenagy (1972) details the climbing of D. mi- crops in saltbushes to obtain leaves, and Ro- senzweig and Winakur (1969) suggest that there may be a vertical component to hetero- myid foraging. I have observed large D. spec- tahalis climbing in Ephedra to harvest flow- ers, but did not find heteromyids climbing in bushes in an earlier study (Reichman 1979). There seems to be an inverse relationship between the size of a heteromyid species and the distance it travels while foraging during a night (Bowers 1982, Thompson 1982a,b, and in review). This is true for both average dis- tance between stops and total distance through the night. Thompson (1982a, 1984) reports average distances between foraging stops of 7.52 m, 5.02 m, and 2.65 m for D. deserti, D. merriami, and P. longimembris, re- spectively. I have observed individual D. merriami moving up to 45 m before stopping to forage, and other authors have observed similar distances (Bowers 1982, Thompson 1982a,b). Schroder (1979) found that adult D. spectabilis spent less than 22 percent of their time more than 6 m from their burrows, but that they average 68 m per foraging trip, and total 350 m per night in foraging travels. Ke- nagy (1973a) reported a maximum running speed for a kangaroo rat being chased as 32 kph, and I have calculated speeds of 16 kph in the field for individual D. merriami forag- ing freely (i.e., not being chased). Average foraging speeds are probably significantly less, as Thompson (1984) reports mean speeds in transit of 6.28, 3.27, and 1.76 kph for D. deserti, D. merriami, and P. longimembris, respectively. 80 Great Basin Naturalist Memoirs No. 7 Once an animal begins to forage, a number of senses apparently play roles in detecting seeds. Generally, heteromyids seem to be very aware of their surroundings, perhaps us- ing vision to orient and note changes in their local environment (Hall 1946), although Reichman and Oberstein (1977) did not find visual cues to be important in laboratory studies of foraging. Once general areas for foraging are located and entered, olfaction probably becomes important for seed detec- tion. Reichman and Oberstein (1977) found that kangaroo rats in a laboratory experiment were able to detect seeds to a depth of up to 20 cm, and the authors present a regression equation for the relationship between seed detection by captive kangaroo rats and the depth/size of a buried packet of seeds. Lock- ard and Lockard (1971) and Reynolds (1958) present infonnation from the field dealing with the accuracy of underground seed de- tection, and Johnson and Jorgensen (1981) suggest that soil moisture is important for seed detection by olfaction. Reichman (1981) discusses the nature of olfaction as a cue for foraging heteromyids. In an intriguing study, Lawhon and Hafner (1981) show that tactile cues may be the final sense used to judge the nature of a food item. They foimd differences between species in tactile abilities, and found that individuals most often misjudged nonedible food items that resembled edible items in shape or tex- ture, regardless of weight or overall dimen- sions. The tactile input discussed by Lawhon and Hafner (1981) comes from actual touch- ing with the forepaws, and is probably im- portant and effective for an animal with its eyes on top of its head. Eisenberg (1963) re- ported another use of tactile senses involving the long vibrissae of the rodents. He noted that even rapidly rimning or hopping rodents leave trails in the sand from their dragging vibrissae, and he suggested that this assists the animals in maintaining their balance while niiuiing. Once heteromyids find a seed or patch of seeds, they excavate in a manner typical of rodents, using the forepaws for the initial ex- cavation and moving the soil to the rear, where it is kicked out by the hind legs (Eisen- berg 1963). Eisenberg alludes to the tactile cues discussed by Lawhon and Hafner (1981) as he describes how the rodents then sift the soil they have excavated for seeds. Kenagy (1972) and Csuti (1979) describe other food acquisition behaviors associated with vegetation. Once a food item is secured, a heteromyid can either eat the item immediately or put it in its cheek pouches for transport and stor- age. This separates the gathering and eating process and has important implications for foraging. From my observation, a heteromyid rarely eats an item at the collection site, but, rather, pouches it and returns to the burrow. Presumably, the burrow provides a more equable environment in which to sort seeds than does the surface, which is hotter (or colder in winter), drier, and rich in predators. Reichman (1977) has shown that although heteromyids do not apparently gather food into their pouches in the exact proportions available, a more diverse sample of seeds is found in the pouches than ingested, sugges- ting that the rodents do gather items they do not subsequently ingest. Animals without cheek pouches would usually eat a food item as it was obtained. Morton et al. (1980) show that cheek pouch volume scales positively with body mass in grams (volume of cheek pouches in cm^ = 0.065 mass^^^^. They also suggest that a heteromyid could fulfill its to- tal daily requirement with one full load of seeds from its pouches. This, plus the obser- vation that animals rarely are captured with full pouches (Reichman 1978), presents a puzzling question as to why individuals would return to their burrows before filling their pouches. Nickolai and Bramble (this volume) offer an interesting explanation. The husking of seeds is highly variable be- tween species and individuals, although Ro- senzweig and Sterner (1970) suggest that rel- ative husking rates are a phenomenon that might promote coexistence between sym- patric heteromyid species. The authors show that larger species husk more rapidly than smaller species, but that the smaller species are more efficient per gram of body weight. Rosenzweig and Sterner (1970) used relative- ly large domestic seeds and it is not known how this relationship would extrapolate to smaller, native seed species. There are several additional foraging be- haviors exhibited by desert heteromyids. Vor- hies and Taylor (1922) suggest that individual 1983 Biology of Desert Rodents 81 heteromyids might rob the seeds stores of other individuals. Tappe (1941) and Clark and Comanor (1973) found that heteromyids occasionally dig into ant mounds, presumably to secure seeds. Heteromyids also eat many insects (Reichman 1975, 1978), and I have foimd cheek pouches full of headless ants. These ants may have been "husked" to mini- mize the probability that the consumer would be bitten. One peculiar behavior noted by Benson (1935) was that of a D. deserti kicking sand over a novel food item placed near a burrow by Benson. One of the most intriguing aspects of het- eromyid behavior is the caching of seeds. Voorhies (1974) has found cached seeds asso- ciated with fossil pocket mouse burrows that are nearly 10 million years old, so it is an an- cient behavior, perhaps associated with the development of cheek pouches. Relatively little is known about caching by pocket mice (Blair 1937) or small kangaroo rats, but most of the large kangaroo rat species are known for their elaborate burrows in which they store large quantities of seeds (Culbertson 1946, Hawbrecker 1940, Reynolds 1958, Shaw 1934, Tappe 1941, Vorhies and Taylor 1922). Some species store on the surface as well as below ground (D. heennani, Tappe 1941; D. ingens, Shaw 1934), but most store seeds below ground. The piles are usually sorted by species, even if they have been gathered from mixed-species patches, and some of the quantities are huge. Vorhies and Taylor (1922) report caches of from 5 to 5750 gms for D. spectibalis, Shaw (1934) found caches of from 1 to 8V4 quarts, and Tappe (1941) foimd dozens of caches. Eisenberg (1963) discusses caching by sev- eral species in the laboratory and found a possible tendency for females to cache more than males. Lawhon and Hafner (1981) show that pocket mice cache more of the seeds available than kangaroo rats, and that hoard- ing is greater in the fall and spring than in the winter. Although little is known about the underground regimes of cache manage- ment and use, Kenagy (1973) noted that kangaroo rats are quite active underground during the 23 hours a day they are not above ground foraging. Studies I have recently be- gun with D. T. Wicklow reveal that approx- imately 20 species of fungi can be found in the cheek pouches and cache environments of these rodents, and that some of these fungi could have important impUcation for cache management behaviors. The benefits of caching could include long- term storage for periods of low production, enhancing nutritional and/or moisture condi- tions of the seeds, and protection of seeds from robbing by other granivores. Several aspects of heteromyid foraging be- havior, as mediated through anatomy and physiology, have been implicated in the com- munity structure of the rodents (see Price and Brown, this volume). Although much con- troversy remains, most investigators agree that the bipedal /quadrupedal relationships, cheek pouches and seed storage, microhabitat choice and use, and seed patch density selec- tion are important behavioral components that impinge on community structure. Reich- man (1981) has suggested that the biped- al/quadrupedal difference could help pro- mote coexistence between kangaroo rats and pocket mice, but this has recently been brought into question by Thompson et al. (1980), who have shown that bipedal locomo- tion is no more energetically efficient than quadrupedal locomotion for similar-sized in- dividuals. Seed size selection behaviors have been suggested as means of coexistence (Brown 1975, Mares and Williams 1977), but other authors have questioned the sufficiency of this explanation (Lemen 1978, Smigel and Rosenzweig 1974). Numerous studies have suggested habitat selection as a means of co- existence among sympatric heteromyids (Lemon and Rosenzweig 1978, M'Closkey 1980, 1981, O'Dowd and Hay 1980, Rosen- zweig 1973, Rosenzweig and Sterner 1970, Rosenzweig and Winakur 1969, Stamp and Ohmart 1978, Thompson 1982a, b) and other authors state that patch density selection is important (Hutto 1978, Price 1978, Trombu- lak and Kenagy 1980, Wondolleck 1978, but see Frye and Rosenzweig 1980) and related to both seed size selection and habitat selec- tion through seed distribution (Reichman 1981, Reichman 1983, Reichman and Ober- stein 1977). It is intuitive that all these behav- iors could be, and probably are, important components of community phenomena noted in the heteromyids (Bowers and Brown 1982). 82 Great Basin Naturalist Memoirs No. 7 Further research is mandatory before a cohe- rent picture of the relative importance of these behaviors, and the communities and lo- cahties where they are important, is estab- hshed. In addition, other behaviors, such as predator avoidance, may be important in de- termining desert heteromyid rodent commu- nity structure. Predator Avoidance Behavior Heteromyids Hve in an environment rich in potential predators (Hall and Kelson 1959). Vorhies and Taylor (1922) list numerous predators on D. spectabilis and note that, of 592 owl pellets they examined, 230 contained kangaroo rat remains. One means of avoiding predators is color crypticity, and Benson (1933) shows that many rodents in the south- western United States include substrate color matching in their repertoire of predator avoidance schemes. Heteromyids seem to have a general awareness of their surroundings and are very sensitive to peculiar sounds and sights. Eisen- berg (1963) notes that novel items in their cage elicit attention, and occasionally dis- placement behaviors such as digging. Hall (1946) states that heteromyids are drawn at night to newly disturbed areas (e.g., a boot heel dragged in the soil surface), and many investigators are familiar with kangaroo rats burying traps under a pile of dirt. Some het- eromyids are known to plug their burrows at night (Chapman and Packard 1974; Compton and Hedge 1943), and this may partially be a response to potential predation. As discussed in the section under activity patterns, heteromyids seem to avoid environ- mental conditions, such as bad weather or bright moonlight, that might hamper their ability to detect predators or make them more obvioiLS to predators. Apparently, both hearing and sight are important components of predator detection. Webster (1962) and Webster and Webster (1971, 1972, 1980) have documented the extremely accurate hearing of kangaroo rats, especially for low- frequency sounds, and tliey suggest that this has developed in response to predator detec- tion. Desert conditions may be poor for soimd transmission (hot and drv), and this would place pressure on the animals to devel- op exceptional hearing. Another indication of the excellent hearing in heteromyids is en- larged auditory bullae, most notable in the kangaroo rats. Not only is their hearing good, but kangaroo rats have also developed espe- cially acute reception at those frequencies of sound made by a rattlesnake's rattle and an owl's wing (Webster 1962). In other studies, Webster and Webster (1971, 1972, 1980) have shown that kangaroo rats can effective- ly detect predators with either vision or hear- ing, but if both senses are eliminated the rats usually succumb to predators. Bartholomew and Caswell (1951), Thomp- son (1982a), and Hay and Fuller (1981) sug- gest that the bipedal locomotion and rico- chetal bounding of kangaroo rats might be primarily an adaptation to predator avoid- ance. Certainly the irregular hopping would be distracting to a predator, and Eisenberg (1975) notes that kangaroo rats immediately hop away when a rattlesnake is nearby. Hay and Fuller (1981) found that heteromyids are more selective in their diet choice when they forage in the open than when they forage in the presumed relative safety of a shrub, and the authors suggest that this selectivity may be due to predator pressures in the open. The opposite prediction, that of low selectivity in the open, could be made if predator pressures are high in the open areas. In this explana- tion, heteromyids would move rapidly through the open areas, gathering seeds in- discriminantly into their pouches, making the critical diet choices later in the relative safety of their burrows (Reichman 1977, 1981). Spacing, Territories, and Aggression For the most part, heteromyids are solitary animals (Blair 1937, 1943, Dixon 1959, Schef- fer 1938), living singly in their burrows (Eis- enberg 1963 and Martin 1977 describe them as "asocial"). Monson and Kessler (1940) foimd only 3 of 44 burrows with more than one individual D. spectahalis, and Monson (1943) found 41 of 53 mounds to be singly oc- cupied. Several of the dual occupancy bur- rows had two adults, but most were females and their offspring. Some species are noted 1983 Biology of Desert Rodents 83 for having more than one burrow, and Chap- man and Packard (1974) report that male D. merrianii average 6-7 burrows and females have approximately 5 burrows each. Current observations in the field by several in- vestigators suggest that this may be more common than is generally thought. Individ- uals occupying more than one nest may ex- plain why in some areas a large percentage of burrows appear to be unoccupied. Schro- der and Geluso (1975) found 42 of 121 D. spectahilis mounds unoccupied. All mounds combined showed a uniform spatial distribu- tion, whether occupied or not. Data on the home range size of hetero- myids are scattered throughout the literature, but one feature that seems to emerge is that home ranges are not directly related to the average body size for a species. Small pocket mice frequently exhibit home ranges near the size of larger species (Chew and Butterworth 1964), and Schroder (1979) reported a smaller home range for D. spectahilis than D. mer- riami. There are reports that males have larger home ranges than females (Maza et al. 1973) and that the home ranges of male and female kangaroo rats overlap extensively (O'Farrell 1980). Holdenreid (1957) and Flake and Jorgensen (1969) report no differ- ence in dispersal rates between males and fe- males in a population, although it is primari- ly the juveniles that disperse. Recent work by Tom Jones (see Munger, Bowers, and Jones, this volume) suggests that individual kan- garoo rats do not move far from their natal burrow. Although areas around a home burrow are not as aggressively defended as are territories of other mammals (Eisenberg 1981), hetero- myids apparently do show some degree of territoriality, as manifested by aggression and possibly by scent marking, although the latter proposition is unproven. Eisenberg (1963) de- scribes various types of marking, including a perineal drag, and suggests these are for terri- torial identification. Borchett et al. (1976), Griswold et al. (1977), Laine and Griswold (1976), and Randall (1981a, b) present details of sand bathing by kangaroo rats and suggest that the odors produced may connote infor- mation about the species, sex, and possibly reproductive condition of the depositor. Quay (1953) notes the sexual and seasonal characteristics of the dorsal gland in five spe- cies of kangaroo rats, and discusses its pos- sible role of scent marking. Another behavior that may be related to territorial pronouncements is drumming with the hind feet. It is relatively easy to get an adult D. spectabalis to respond with drum- ming by tapping lightly on their mound. Eis- enberg (1963) noted drumming in Di- podomys, Perognathus, and Microdipodops species in relation to aggression, and teeth chattering in the same context. Kenagy (1976b) observed drumming in the field dur- ing a contest between male kangaroo rats, eventually leading to copulation between one of the males and a female. Overt aggression between individual heter- omyids may be rare, or simply rarely seen. Eisenberg (1963) provides extensive informa- tion of the types of aggressive interactions generated in a laboratory setting, and excel- lent descriptions of the modes of attack and associated behaviors such as scratches and growls. The general trend in Eisenberg's lab- oratory study, and those of Hoover et al. (1977)' and Blaustein and Risser (1974, 1976) is for large individuals of one species to even- tually win over smaller individuals of another species, although the effort involved varied greatly. Congdon (1974) notes a similar rela- tionship in the field, and Vorhies and Taylor (1922) describe fights in the laboratory be- tween D. spectabalis and D. merriami that are "savage and to the death." I have video- tapes of a kangaroo rat pouncing on a pocket mouse at a rich pile of seeds. Conversely, I have watched two separate D. merriami chase adult D. spectabalis away from a forag- ing area. Aggression can be related to the sex and reproductive condition of the partici- pants (Eisenberg 1963), and Kenagy (1976b) provides an excellent description of aggres- sion observed in the field between two males courting a female. Upon occasion, heteromyids will have ag- gressive bouts with nonheteromyids. I have observed kangaroo rats chase off Peromyscus individuals at artificially placed seed piles, and Shaw (1934) notes similar events. McCue and Caufield (1979) report a grasshopper mouse attacking and dismantling a kangaroo rat in daylight hours. 84 Great Basin Naturalist Memoirs No. 7 Reproduction and Parental Care Desert heteromyids generally have one or two litters a year. Females are usually in es- trus for specific periods, but males may be scrotal the entire year (Bradley and Mauer 1971, Reichman and Van De Graaff 1973). Juvenile female kangaroo rats develop swol- len vaginas at about six weeks and can con- ceive at 12 weeks (Eisenberg 1963). Observation of coiu-tship and reproduction are rare from the field, although Engstrom and Dowler (1981) and Kenagy (1976b) pro- vide interesting field observations. Daly et al. (1980) note that D. agilis and D. merriami in reproductive condition prefer traps that con- tain conspecific odors, whereas non- reproductive individuals show no preferences between odorized and odor-neutral traps. The preferences appear to be independent of the sex of the donor and the recipient. Labo- ratory studies suggest that near the onset of estrus males become more tolerant of and in- terested in females (Eisenberg 1963, Martin 1977). Prior to that, males and females can be very aggressive toward each other (But- terworth 1961), or live in the same arena without aggression (Eisenberg and Isaac 1963). Eisenberg (1963) reports that, as the time for copulation nears, a male and a fe- male may share a common nest box for one night, after which they return to their own nest boxes and a peaceful coexistence. A number of studies describe the cop- ulatory behavior of various heteromyids (Behrends 1981, Dewsbury 1972, Eisenberg and Isaac 1963, Hayden et al. 1966), and Eis- enberg (1963) describes an elaborate protocol for reproductive behavior in the heteromyid species he studied in the laboratory. Basi- cally, there is some mutual attention in the few minutes prior to copulation. Sub- sequently, the male mounts the female from the rear while she exhibits lordosis. After sev- eral seconds to several minutes of thrusting and presumably ejaculating, the male dis- moimts and shows little interest in the fe- male. In some cases, one or the other of the sexes may msh the other, inciting another copulatory bout. Hayden et al. (1966) re- ported that some pairs fall on their sides dur- ing copulation and continue to copulate in this position. The gestation period is relatively short (18-30 days; Butterworth 1961, Day et al. 1956, Holdenreid 1957) and is almost always accompanied by nest building on the part of the female (Eisenberg 1963). Eisenberg (1963) reports that most births occur during the day and, though mothers will eat any dead neonates, no aggressive behavior is sub- sequently demonstrated toward their surviv- ing offspring. The young are born in a rela- tively precocial state (Eisenberg 1963). At the time of birth, the female may stand or lie on her side, assisting the process with her teeth and forepaws (Butterworth 1964, Eisen- berg 1963). Subsequent to parturition, the fe- male ingests the placenta. Van De Graaff (1973) notes that the bone formation in the extremities of kangaroo rats is greater than for similarly aged pocket mouse embryos and juveniles, which still have major limb com- ponents made of cartilage. Eisenberg (1963) notes that muscular coordination seems to de- velop in the young from anterior to posterior. Parental care is carried out entirely by the female. She crouches to nurse the young, and she will move them about the nest by car- rying them in her teeth with a grasp behind the neck (Eisenberg 1963, Tappe 1941). The female may plug the entrance to the nest chamber when she is not in the nest (Eisen- berg 1963). As weaning approaches, the fe- male will begin to ignore her young, eventu- ally even shoving them away as they try to nurse. As the siblings begin to leave the nest, dominance hierarchies are already being es- tablished (Eisenberg 1963). LeVick (1982) does not find any ultrasonic communication between mothers and their offspring in D. or- dii, but both he and Eisenberg (1963) report a broad range of audible sounds from infants aged 2-14 days. Fourteen days corresponds to the time the young begin to eat solid foods and move from the nest (LeVick 1982). Burrow Construction An inverse relationship appears to exist be- tween the size of a heteromyid species and the amount of information on its burrows that has been published. This could be be- cause a similar relationship exists between the complexity of the burrows and the size of 1983 Biology of Desert Rodents 85 the species. Generally, pocket mice have rel- atively simple burrows and the largest kan- garoo rats are known for their large, con- spicuous, and complex mounds and burrow systems. Blair (1937) reports that the burrow of P. hispidis is rather short and simple, with only one entrance and one nest chamber. Scheffer (1938) notes that the burrows of P. parvus are also simple, but may include a hairpin turn directly under the opening, and run to a depth of 76 inches. Chapman and Packard (1974) found that female P. merriami have more complex burrows than males, and that the adults frequently plug unused burrow openings. Eisenberg (1963) found Micro- dipodops burrows in loose sandy soil, and other authors have noted the soil texture where biu-rows are constructed (Anderson and Allred 1964, Compton and Hedge 1943, Deynes 1954, Tappe 1941, Vorhies and Tay- lor 1922). In desert areas burrows are usually obvious around the base of shrubs where loose, windblown soil accumulates, providing a good location for burrow construction. Ke- nagy (1973a) gives information of the con- struction of the burrows of P. longimembris, D. merriami, and D. microps in the field, and Eisenberg (1963) gives details for several spe- cies in the laboratory, including descriptions of the actual digging behaviors. The most extensive information about bur- row construction is available for the large species of kangaroo rats, including D. spec- tabalis (Best 1972, Holdenreid 1957, Monson 1943, Monson and Kessler 1940, Vorhies and Taylor 1922), D. veniistus (Hawbreker 1940), D. heermani (Tappe 1941), D. ingens (Shaw 1946), and D. nitratoides (Culbertson 1946, Fitch 1948). Generally these large species have mounds that are approximately two or three meters in diameter and rise from one- half meter to one meter above the ground. Through the mound and down into the ground pass numerous Rmways. Connected to the Rmways are various nests and large, flask-shaped caches where seeds are stored. Some of the caches are walled off, but most remain open. The mounds are constructed by the rat kicking dirt with its hind legs up on top of the existing structure. Through time, the area surrounding the burrows is slightly lowered by the excavation, and the mound is built higher. Best (1972) notes that it takes from 23 to 30 months to build what would be considered a mature mound. Mounds that are left vacant begin to deteriorate noticably within a month and are almost completely gone within a year. Sensory Abilities Although not much is known about the sensory abilities of heteromyids, some in- triguing work has been carried out with the hearing ability of kangaroo rats. Heffner and Masterson (1980), Webster (1962), and Web- ster and Webster (1971, 1972, 1980) have noted the impressive hearing ability of kan- garoo rats across a broad range of frequencies (1-60 KHz). Heffner and Masterson (1981) also note that kangaroo rats are particularly good at locating the origin of a sound, and Webster (1962) details the hearing of kan- garoo rats in relation to sounds made by predators. I have noted while watching kan- garoo rats in the field that they are startled only by certain kinds of noises. All loud noises get their attention, but metallic clicks seem less disturbing than scratching noises made by a boot in the dirt. Pocket mice and kangaroo rats can appar- ently smell seeds in the soil, even to great depths (Lockard and Lockard 1971). Reich- man and Oberstein (1977) show the relation- ship between the ability of a kangaroo rat to detect a seed patch and the size/depth of the seeds and Reichman (1981) discusses olfaction and seed detection ability. Although it is dif- ficult to determine whether rodents cannot smell an item or simply choose not to seek it, it does appear that kangaroo rats have better olfactory ability than do pocket mice. Daly et al. (1980) noted that certain rodents, in- cluding kangaroo rats, responded to odorized traps, preferring them if the respondents were in reproductive condition. I know of no studies on the vision of heter- omyids, but it is pertinent to note that their eyes are on top of their rounded heads, mak- ing vision ventrally and forward somewhat restricted. Personal Care Personal care seems to be accomplished by two major behaviors. One is associated with 86 Great Basin Naturalist Memoirs No. 7 autogrooming and washing, and another with the care of the dorsal gland possessed by many heteromyid species. Eisenberg (1963) details the grooming sequences of various heteromyid species. Grooming frequently oc- curs shortly after awakening, and includes scratching with the teeth and claws, combing the fur and cheek pouches, and washing with saliva. The animals also apparently bite off any ectoparasites they can locate and reach (Vorhies and Taylor 1922, found fleas of the genera Ctenophthalium and Trombicula on bannertailed kangaroo rats). The presence of a dorsal gland on many kangaroo rats has been noted for some time, and Quay (1953) has investigated its struc- ture. Kangaroo rats with active glands appar- ently groom the secretions over their bodies regularly (Griswold et al. 1977, Borchett et al. 1976, Randall 1981a, b). Although some of the secretion on the hair may assist in reduc- ing evaporative water loss (Quay 1965) or serve as insulation (Randall 1981a, b), too much is apparently detrimental and is groomed off, usually by sandbathing (Randall 1981a, b). Summary In many ways the behavior of desert heter- omyids is similar to what is known about other nocturnal rodents. At the level of preci- sion available from the current data, it ap- pears that their basic ways of securing food, courting and reproducing, and protecting themselves from the environment and pred- ators are much like those of other rodent families (Eisenberg 1981). A few anatomical and physiological specializations, however, give the desert heteromyids some distinctive behavioral capacities. Certainly one is the bi- pedal locomotion used by kangaroo rats and kangaroo mice. This is rare for small mam- mals, and it apparently is not an especially efficient means of locomotion for a small (i.e., low mass) animal (Biewener et al. 1981). Per- haps bipedality simply provides a means of rapid locomotion for moving through the open to forage or avoid predators. A second feature, possessed by all hetero- myids, is cheek pouches. Pouches, used for the temporary storage of seeds while forag- ing, grossly alter the manner in which a rodent would forage. The pouches make gathering food and eating food two different events ecologically and allow the possessor to quickly gather food while foraging before re- turning to the relatively safe burrow where appropriate dietary decisions can be made. Pouches also allow the animals to gather large quantities of seeds when they are avail- able. The surplus seeds can then be stored and used at a later date when resources are perhaps less abundant, thus leading to elabo- rate caching behaviors. Even the use of a food resource such as seeds is adaptive in a desert setting, as seeds are rich in energy and nutrients and thus require less time spent in the hostile above-ground environment, and seeds persist in the soil through time. A final specialization is in degree, not kind. Heteromyids, and especially kangaroo rats, have exceptionally good hearing, which ap- parently serves them well in the desert where sound may travel poorly. What is particu- larly striking about their hearing is its appar- ent fine tuning for the sounds made by two major predators on the animals, rattlesnakes and owls. Several areas of heteromyid behavior re- main poorly understood or controversial. Al- though much is known about foraging behav- ior, several important groups of heteromyids (e.g., the kangaroo mice and the large kan- garoo rat species) are underrepresented in the literature. The ways in which differences in foraging affect heteromyid rodent commu- nity structure are currently being hotly de- bated, as are body size relationships within the family. Almost nothing is known about the effects of predation on rodent behavior and community structure, even though most would agree that it is important. As tech- niques for behavioral observation expand, we can expect more of the important pieces to the heteromyid puzzle to be fitted in. We tend to think of the desert as being an especially harsh environment, and for hu- mans it is. As this chapter, and others in this symposium, have shown, however, the desert can be much more hospitable to an animal that is adapted to its extremes. It seems safe to assume that most of the behaviors exhib- ited by desert heteromyids are in some gener- al or specific way tied to the physical envi- ronment in which they flourish. 1983 Biology of Desert Rodents 87 Acknowledgments My thanks are extended to Dr. Robert Kruli, dean of the Graduate School at Kansas State University, who provided support for this symposium. I also thank Jim Brown for his efforts on behalf of the symposium, and Mary Price, Jan Randall, and Cindy Rebar for their helpful comments. An anonymous reviewer also provided essential assistance. Literature Cited Anderson, A. O., and D. M. Allred. 1964. Kangaroo rat burrows at the Nevada Test Site. Great Basin Nat. 92:93-101. Bartholomew, G. A., and G. R. Gary. 1954. Locomo- tion in pocket mice. J. Mammal. .35:386-392. Bartholomew, G. A., and H. Gaswell. 1951. Locomo- tion in kangaroo rats and its adaptive signifi- cance. J. Mammal. 32:1.55-169. Bartholomew, G. A., and R. E. MacMillen. 1961. 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Morphological adaptations of the ears in the rodent family Heteromyidae. Amer. Zool. 20:247-254. WoNDOLLECK, J. T. 1978. Foragiug-arca separation and overlap in heteromyid rodents. J. Mammal. 59:510-518. DESERT RODENT POPULATIONS: FACTORS AFFECTING ABUNDANCE, DISTRIBUTION, AND GENETIC STRUCTURE' James C. Munger, Michael A. Bowers-, and W. Thomas Jones' Abstract.— Literature concerning North American nocturnal desert rodents is reviewed to delimit current knowl- edge of the importance of various factors to abundance, distribution, and genetic structure. In addition, strategies for further study are suggested. Abundance: That increased rodent abundance often follows flushes of annual plant growth that follow favorable rains is well established. The ultimate reason for this pattern has not been established. Competition is important as well, but predation and parasitism have received little consideration. Distribution: Pat- terns of distribution have been shown to correspond to temperature, moisture, substrate, or vegetative parameters. An important question that remains is to determine the relative importance of physiological specialization vs. inter- specific interactions leading to habitat specialization. Genetic Structure: Despite a number of studies on desert ro- dent systeniatics, little is known of the genetic structure of desert rodent populations. Behavioral, demographic, in- direct genetic, and direct genetic evidence can be used to detect deviations from panmixia. Although desert rodents have been the sub- ject of hundreds of studies on a number of levels (e.g., physiology, behavior, population ecology, community ecology, and system- atics), it is not yet feasible to make general conclusions as to the relative importance of various factors in determining the abundance, distribution, and genetic structure of popu- lations of desert rodents. This article is de- signed to help remedy this problem. We con- sider the possible importance of each of a number of factors, reviewing the relevant lit- erature to determine what is known at pres- ent, then suggesting ways in which the gaps in our knowledge can be filled. With few exceptions, we have limited our treatment to the nocturnal rodents that in- habit the deserts of North America. In addi- tion, much of our treatment concerns rodents of the family Heteromyidae, a bias that re- sults in large part from the greater amount of work done on that group relative to other groups. Abundance and Dynamics Discussion of factors affecting the abun- dance and dynamics of desert rodent popu- lations has, in the past, centered on the im- portance of food, water, and vegetation. More recently studies have focused on inter- actions among rodent species. In addition to discussing these factors, we consider pre- dation and parasitism and argue that both are worthy of study, although little evidence ex- ists concerning their importance. Food and Water Perhaps the best-documented pattern of desert rodent abundance is increased popu- lation growth and reproduction following rainfall and the growth of plants, particularly annuals. This pattern has been shown to hold for many rodent species in many geographi- cal areas (Reynolds 1958, Chew and But- terworth 1964, Beatley 1969, Bradley and Mauer 1971, Van de Graff and Balda 1973, Newsome and Corbett 1975, O'Farrell et al. 1975, Reichman and Van de Graff 1975, Whitford 1976, Dunigan et al. 1980, Petrys- zyn 1982). The exact timing of rainfall is at least as important as the total amount. Both Beatley (1974) and Petryszyn (1982), working in deserts with very different precipitation patterns, have shown that rainfall early in winter is important in germination and early growth, and rainfall in the spring is necessary for further growth and flowering. 'From tlie symposium "Biology of Desert Rodents," presented at the annual meeting of the American Society of Mammalogists, hosted by Brigham Young University, 20-24 June 1982, at Snowbird, Utah. -Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85721. 'Department of Biological Sciences, Piu-due University, West Lafayette, Indiana 47907. 91 92 Great Basin Naturalist Memoirs No. 7 Several hypotheses have been proposed to account for this apparent dependence of ro- dent populations on plant growth; all are based primarily on reproductive responses to external factors, not on effects on survivor- ship. First, Chew and Butterworth (1964) suggested that rodents may consume hormon- al substances within the plants that initiate reproduction. Such a triggering mechanism has been demonstrated for microtines (Berger et al. 1981 and refs. therein). Second, Chew and Butterworth (1964) and Van de Graaff and Balda (1973) found that rodents gained weight at times of plant growth or in areas where green vegetation was present and ar- gued that ingesting green vegetation im- proves general body condition, enabling indi- viduals to reproduce. Third, Beatley (1969), Bradley and Mauer (1971), and Reichman and Van de Graaff (1975) found an increased availability or consumption of green vegeta- tion during or prior to reproduction and ar- gued that water and vitamins in the plants are necessary to compensate for increased de- mands during gestation and lactation. Defi- ciencies in vitamins (such as A or E) can lead to sterility or fetal death (Wright 1953). Fi- nally, based on the common trend that in- creased growth of annuals is a prelude to in- creased availability of seeds and insects, O'Farrell et al. (1975), Reichman and Van de Graaff (1975), Whitford (1976), and Dunigan et al. (1980) suggested that increased repro- duction may depend on increased food availability. The problem of distinguishing among these hypotheses can be made more tractable if we recast them to reflect requirements that are common to all animals: water, energy, and nonenergetic nutrition (simply termed nutri- tion below; includes essential fatty acids, amino acids, vitamins, and minerals). First, the "hormonal substances" hypothesis is probably based on a proximate mechanism. Rodents should not come to rely on an exter- nal cue, such as a hormonal substance, unless that cue is tied to some ultimate benefit such as water, energy, or nutrients. Second, in- creased "general body condition" is probably due to the increased availability of water, energy, and/or nutrients. Finally, "increased food availability" confounds the effects of energy and nutrition. The problem, then, is to distinguish among the relative importance of water, energy, and nutrients (all of which are more available following favorable weather conditions) in leading to population increases of desert rodents. Several studies and observations, other than the above correlative studies that led to the formulation of these hypotheses, bear on this question. Breed (1975) showed that water deprivation resulted in reduced reproductive activity in female Australian hopping mice {Notomys alexis), as measured by ovarian and uterine weights and follicular development. In another laboratory experiment, Yahr and Kessler (1975) found that reproductive activi- ty ceased in Mongolian gerbils {Meriones iinguicidatus) that received lettuce only once a week but continued in control animals that received daily lettuce rations. In this study, the effect of water and nutrient availability are confounded because lettuce may contain required nutrients as well as water. Soholt (1977) found that free water intake in lactat- ing Dipodomys merriami increased by more than 200 percent over that of non- reproductive females, though gestating fe- males exhibited no increase. However, be- cause carrots were used as the source of free water, it is not possible to distinguish be- tween the importance of water and any nu- trients that carrots may contain. Further- more, these experiments do not demonstrate an absolute need for free water during lacta- tion because females were not actually de- prived of free water; they simply showed an increase in water use. Two studies have shown a correlation be- tween the density of Neotoma populations and the local abundance of Opuntia cactus (Brown et al. 1972, Cameron and Rainey 1972, Olsen 1976), although it is unknown whether the correlation is due to increased food and water availability or to increased protection against predators (woodrats often used cactus joints in constructing nests; Brown et al. 1972). In addition, Petryszyn (1982) found that N. alhigula densities failed to respond to a single winter of higher than average rainfall, but did respond to two con- secutive good years. This can be interpreted to indicate that the abundance of annual plants (which would respond to a single good winter) does not limit woodrat populations 1983 Biology of Desert Rodents 93 but the growth of perennial plants (which perhaps only respond to consecutive good years) may limit woodrat populations (Petrys- zyn pers. comm.). By providing a source of supplemental wa- ter, Christian (1979a) was able to cause an in- crease in reproductive activity in two species and increased density in one species in a community of three species of Namib Desert rodents. The species most ecologically similar to North American heteromyids because of its superior ability to conserve water {Desmo- dillus aurictilaris; Christian 1979b) was little affected; Christian (1979a) argued that fac- tors other than the availability of water de- termine its population size. The two species more similar to North American desert crice- tids or sciurids (they are poorer at water con- servation than D. aiiricularis; Christian 1979b) did respond to supplemental water, indicating that the availability of water is im- portant in determining the abundance of these species. Two observations indicate that availability of green matter and the water or nutrients contained therein are not a requisite for re- production. O'Farrell et al. (1975) found that female Perognathus parvus sometimes re- mained lactating for more than a month after vegetation had dried up; vegetation may have been required for initiation of reproduc- tion, but not for lactation. Whitford (1976) observed a population increase during a year in which there was virtually no growth of green matter. The importance of energy or nutrients is indicated by two studies in which seeds were added to experimental plots. Addition of seeds to plots in short grass prairie caused an invasion of seed-eating Dipodomys ordii (Abramsky 1978). Addition of seeds to plots in the western Chihuahuan desert caused a threefold increase in numbers of the largest species at the site (D. spectabilis) but a slight decrease in numbers of smaller species (Brown and Munger, in preparation). The results of the studies discussed here in- dicate that it is unlikely that variation in a single factor, whether it be water, energy, or nutrients, will be able to account for all situa- tions where desert rodent population in- creases are correlated with bouts of rainfall. There are several reasons for this. First, spe- cies of desert rodents may vary in their re- quirements. This is illustrated by Christian's (1979a) finding that three species of Namib Desert rodent responded in different ways to the addition of water. It is apparent that physiological differences among species must l3e considered when assessing the effects of various factors on abundance. Second, geographical differences in the stressfulness of the environment may be im- portant. For example, all studies that showed population responses not tied to increased water availability were carried out in rela- tively benign (with respect to water stress) environments: south central Washington (O'Farrell et al. 1975), Chihuahuan Desert above 1000 m elevation (Whitford 1976, Brown and Munger, in preparation), and short grass prairie (Abramsky 1978). The studies that showed an apparent reproduc- tion dependence on free water were carried out in the more stressful lower Sonoran Desert, Mojave Desert, and Namib Desert. To resolve this problem, water and food ad- dition experiments should be performed in the harsher lower deserts as well as in the relatively benign higher deserts. Third, insects, whose populations often re- spond to increased plant growth, may pro- vide a source of moisture for several months after annual plants have died. Finally, although these hypotheses have been couched in terms of the effects of vari- ous factors on reproduction, these same fac- tors are likely to affect survivorship as well. Probably because of the energetic and nutri- tive demands of reproduction, survivorship of breeding adults tends to be negatively associ- ated with the degree of reproductive activity (French et al. 1974, Conley et al. 1977) and thereby negatively correlated with the amount of rain-induced plant growth (Chris- tian 1980). Juvenile survivorship, on the other hand, should be increased by the in- creased availability of food and water. This pattern was found by Whitford (1976). who showed that the survivorship of young heter- omyids was much lower in a year with a poor seed crop than in years with good crops. In- creased juvenile survivorship may have con- tributed directly to increased densities shown by the studies cited above, or indirectly via 94 Great Basin Naturalist Memoirs No. 7 reproduction in adults: increased probability of survivorship of young during years of high plant growth and subsequent plant avail- ability may be the ultimate factor that leads adults to reproduce in those years (Reichman and Van de Graaff 1975). As noted above, desert rodent populations appear to be strongly influenced by the growth of plants following sufficient rainfall. One might ask then whether it is necessary to even consider factors other than food and water, since the availability of water, energy, and nutrients seems to explain a large part, if not all, of the variation in desert rodent abundance. We strongly feel that other fac- tors should be considered, if only to rule them out. Below we describe a series of stud- ies on desert annual plants that illustrates the need to consider other factors. The abundance of desert annual plants is, as mentioned above, dependent on the pat- tern and amount of rainfall. Other factors have been shown to be important as well. First, intraspecific evidence appears to limit the number of seeds that germinate (Inouye 1980). Second, large-seeded species of annual plants appear to be able to outcompete small-seeded species, but seed predators (es- pecially rodents) apparently prefer larger seeds. Rodents decrease the abundance of large-seeded species, thereby indirectly in- creasing the abundance of small-seeded spe- cies (Inouye et al. 1980). And third, if large- seeded species do attain high densities (as they do in rodent exclosures) they are subject to attack by a parasitic fimgus that causes a large decrease in fecundity (Inouye 1981). With this example in mind, we proceed to consider the importance of interspecific in- teractions, predation, and parasitism in deter- mining the abundance of desert rodents. Interspecific Interactions A population of a given species of desert rodent does not live in the absence of other organisms. In the following section, we ad- dress the possible importance of interspecific interaction in determining the abundance of desert rodents. For competition among species to occur, some resource must be limiting. A substantial amount of evidence, much of it indirect, ar- gues that food is limiting for many species of desert rodents, especially granivorous species. As discussed above, increases in population density follow periods of high precipitation and seed production (Reynolds 1958, Beatley 1969, 1976, French et al. 1974, O'Farrell et al. 1975, Whitford 1976, Dunigan et al. 1980, Petryzsyn 1982), and invasions or population increases of seed-eating rodents follow the addition of seeds (Abramsky 1978, Brown and Munger, in preparation). In addition, den- sities of seed-eating rodents increased in re- sponse to the removal of ants (Brown and Davidson 1979) and, along a geographic gradient of increasing precipitation and pro- ductivity, population density, biomass, and species diversity of seed-eating rodents tend to increase (Brown 1973, 1975). Furthermore, woodrat populations appear to be limited by the amount of green matter available to them (Brown et al. 1972, Cameron and Rainey 1972, Olsen 1976). A number of studies indicate the probable importance of rodent-rodent interactions. Cameron (1971) concluded that, where the two species are sympatric, Neotonia fuscipes excludes N. lepida from their preferred food plant. Frye (in press) showed experimentally that Dipodomys merriami were excluded from seed resources near the mounds of the larger D. spectahilis. A number of authors have shown that desert rodents differentially utilize microhabitats (Brown and Lieberman 1973, Brown 1973, 1975, Lemen and Rosenz- weig 1978, Price 1978a, Wondolleck 1978) or habitats (Rosenzweig 1973, Schroeder and Rosenzweig 1975, Hoover et al. 1977, War- ren 1979). That this differential use is caused by interspecific interactions is indicated by studies that have shown a shift in micro- habitat use as a result of experimental remov- al (Price 1978a, Wondolleck 1978) or a natu- ral lack (Larsen 1978) of putative competitor species. In addition, although food may not be the basis of the response, the granivorous D. ordii expanded its microhabitat use in re- sponse to removal of the omnivore Onych- omys leucogastcr (Rebar and Conley, in prep- aration). Exclusion of one species by another from a preferred resource or microhabitat can potentially lead to a reduction in popu- lation size for the former species. 1983 Biology of Desert Rodents 95 Removal experiments that measure mimer- ical response are even stronger evidence of the importance of interspecific interaction. Unfortrmately, few such studies have been done. Schroeder and Rosenzweig (1975) per- formed reciprocal removals of D. ordii and D. merriami but found that neither species re- sponded to removal of the other. Munger and Brown (1981) found a 3.5-fold increase in the population density of small granivorous ro- dents following the absolute removal of three species of Dipodomys. In a third study, Eide- miller (1982) performed reciprocal removals of the herbivorous Neotoma lepida and the granivorous Perognathus fallax. Three species of omnivorous Peromyscus responded with a twofold increase to N. lepida removal but failed to respond to P. fallax removal. The re- sponse of N. lepida to the removal of P. fallax and the reciprocal response were minor. To further assess the importance of inter- specific interactions, more removal experi- ments must be performed. To be of value, these experiments must be properly repli- cated; a surprising number of studies appear- ing in the literature lack experimental rep- lication (Hayne 1975). A number of questions can be addressed with these studies. First, how general are the results of the experiments discussed here? An- other, is the result affected by the identity of the species studied, by the habitat in which the study was conducted, by the presence of other competitor or predator species (which may be affected by historical factors such as colonization events or ecological bot- tlenecks), by the season in which the study was performed, or by the temporal pattern of resource availability? One tenuous pattern that emerges is that similar-sized species failed to respond to removals (Schroeder and Rosenzweig 1975), whereas dissimilar-sized species responded to removals (Munger and Brown 1981; although this was not true in all cases for Eidemiller 1982). Such a general- ization contradicts other studies that suggest that the intensity of pair-wise interactions among granivorous rodents increases with body-size similarity (Brown 1973, 1975, Brown and Lieberman 1973, Mares and Wil- liams 1975, Bowers and Brown 1982). As dis- cussed by Schroder and Rosenzweig (1975), it may be that the interaction between similar- sized species has been sufficient, over evolu- tionary time, to discourage utilization of a common set of resources (see discussion un- der habitat selection). Second, by examining the bases of these in- teractions in detail, a great deal can be learned about their impact on population dy- namics. For what resource are these rodents competing? Does the interaction involve ex- ploitation or interference competition? Predation The most direct way to assess the effect of predation on desert rodent populations is to remove predators then measure any response there may be in the abundance and distribu- tion of the rodents. Much information about predator-prey interactions can also be gath- ered through detailed observations of popu- lation numbers, distribution, and behaviors of predators and prey as shown by what is un- doubtedly the most complete study of the ef- fects of predation on the population dynam- ics of a small mammal: the work of Errington (1943, 1946) on muskrats {Ondatra zibethica) and their primary predator, mink {Mustela vison). Unfortunately, no study approaching this quality has been performed on desert ro- dents and their predators (perhaps because much of their activity is nocturnal); there- fore, we must rely primarily on indirect evi- dence in this section. Errington's work illustrates a further point: the scale on which the results ar- viewed drastically affects the interpretation. Al- though large numbers of muskrats are killed by mink and other predators, Errington (1946, 1956) argued that predation is over- rated as a factor controlling muskrat popu- lations. Instead, he argued that population size is controlled by the availability of terri- tories; predation primarily affects the surplus individuals (those without territories) of a population and is only one of a number of factors that affect surplus animals of the pop- ulation. Although he may be correct that ter- ritory number limits population numbers and density within a marsh, it is predation that makes areas outside the marsh unsafe, ulti- mately limiting the number of territories that can be safely occupied. If it is the presence of 96 Great Basin Naturalist Memoirs No. 7 mink that prevents muskrats from success- fully colonizing areas near the marsh (where food and water are accessible), then pre- dation would have to be considered to be a factor important in limiting distribution and therefore total population size of muskrats. On a within-habitat scale, predation appears to be imimportant. On a between-habitat scale, it may contribute substantially to the limitation of the population. Errington's studies illustrate both a direct effect (increased death rate: those individuals that do not possess safe territories are often killed) and an indirect effect (habitat selec- tion: given a choice, muskrats will selectively live in habitats that are relatively safe) of predation on abundance and distribution. In desert rodent populations, direct effects of predation have yet to be demonstrated, though a number of studies have shown that desert rodents are, in fact, killed by a number of predators, e.g., owls, carnivores, and snakes (French et al. 1967, Egoscue 1962, Webster and Webster 1971, Lay 1974, Ryck- man et al. 1981, Munger, pers. obs., Jones, pers. obs.). French et al. (1967) tried to estimate the direct effect of kit fox (Vulpes macrotis) pre- dation on the survivorship of desert rodents by comparing longevity (which included loss by emigration) in unfenced populations (sub- ject to losses by emigration and predation by kit foxes and other predators such as snakes) with longevity in fenced populations (from which kit foxes were excluded and out of which emigration was not possible). The ef- fect of emigration (measured in another study at 25 percent per year) was subtracted from the sum of all effects on longevity of the fenced population. They concluded that kit fox predation was unimportant in affecting longevity, though predation by other pre- dators may have been important. Although this approach was novel, it suffers an impor- tant flaw: the calculations of French et al. (1967) are overly sensitive to the values en- tered into their equations. For example, a de- crease in the emigration value used from 25 to 24 percent results in a sixfold increase in the apparent importance of kit fox predation. Since no confidence intervals are given for any of their values, the exact importance of this sensitivity is unknown. The effect of other factors, such as produc- tivity, competition, and parasitism, may be manifest primarily through predation. It is likely that a decrease in productivity, an in- crease in competition, and an increase in par- asitic load will all require rodents to spend more time foraging to meet energetic re- quirements. This, in turn, will increase their exposure to predators, and potentially di- rectly affect abundance. It is somewhat easier to examine indirect effects of predation because these often in- volve morphologies and behaviors that may be more easily studied than density effects. Behaviors and morphologies that lead to a re- duction in the probability of being killed should evolve in desert rodents. If these be- haviors and/or morphologies are costly or re- duce resources available to a population (for example by restricting foraging to certain mi- crohabitats), then predation can potentially have an indirect effect of lowering popu- lation size. Several studies indicate that one indirect effect involves microhabitat selection. Quad- rupedal desert rodents forage substantially more under and around bushes than out in the open (Brown and Lieberman 1973, Ro- senzweig 1973, Price 1978a, Wondolleck 1978, Thompson 1982a). Though this may be due in part to differences in resource avail- ability (Reichman 1975, Brown et al. 1979a), a number of authors have argued that these rodents favor bush microhabitats to avoid at- tacks by visually oriented predators (Rosen- zweig 1973, O'Dowd and Hay 1980, Thomp- son 1982a, Kotler, in press). Four studies provide experimental evi- dence consistent with the notion that pre- dation importantly affects microhabitat selec- tion. Thompson (1982b) was able to increase the density of quadrupedal rodents in an area by constructing artificial shelters in the open spaces between bushes. By increasing the amount of cover available, the shelters may have allowed the rodents to utilize areas they previously avoided, resulting in an increased population size. Because measures of seed density failed to show any effect by the shel- ters on resource distribution, it is unlikely that the density increase was caused by changes in the resource base. Rosenzweig (1973) decreased the number of Perognathus 1983 Biology of Desert Rodents 97 penicillatus captured by experimentally re- moving shrubby vegetation. The rapidity of the response indicates that it is unlikely that the rodents were responding to a change in resources. O'Dowd and Hay (1980) showed that the probability that desert rodents ex- ploit artificial seed patches varies with the distance of those seeds to the nearest bush (presumably a measure of the danger of being preyed upon) but not with the quality of those patches. The results of these three studies are open to an alternate explanation. The ultimate rea- son that quadrupedal rodents prefer bushy microhabitats may be that bushes have been associated (over evolutionary time) with par- ticular resource distributions and are present- ly used by rodents as proximate cues to favor- able resource patches. In the studies of Rosenzweig (1973) and Thompson (1982b), the rodents may have responded to changes in the proximate cue even though the ulti- mate factor remained unchanged. The oppo- site may have occurred in the study of O'Dowd and Hay (1980): the rodents may have failed to respond to changes in the ulti- mate factor (seeds) because there was no change in the proximate cue. By manipulating a factor other than micro- habitat, Kotler (in press) avoided this prob- lem. He reasoned that, because many pred- ators of nocturnal desert rodents rely on visual cues, the rodents should use the amount of illumination in the environment to assess their risk of being preyed upon. Using artificial light sources, Kotler experimentally increased the amount of illumination, causing four of the six species at his study site to re- duce their use of open habitats, indicating that the utilization of microhabitats by these species is sensitive to the risk of being preyed upon. It is interesting to note that one spe- cies, D. deserti, responded to increased light only when resources in bushy microhabitats were augmented, indicating that resource availability and risk of predation may inter- act in affecting behavior. The two remaining species made little use of open microhabitats prior to experimental treatment; a decrease in the use of open areas by these species would therefore be difficult to cause or detect. Several other studies indicate that pre- dation may be an important selective force in desert rodents. First, timing of foraging activ- ity is sensitive to moonlight; presumably in- creased light increases the probability of being preyed upon (Lockard and Owings 1974, Rosenzweig 1974, Kaufman and Kauf- man 1982). Second, individuals of the island- dwelling Neotoma lepida latirostra spend more time away from the nest and travel in more open areas than their mainland counterparts, presumably due to a lack of predators on the island (Vaughan and Schwartz 1980). Third, desert rodents in sev- eral families possess auditory and locomotory specializations (Bartholomew and Caswell 1951, Webster 1962, Webster and Webster 1975, Lay 1972) that have shown to be im- portant in aiding these rodents in avoiding attacks of predators (Webster and Webster 1971). These rodents also possess pelages which match the substrate on which they oc- cur (Dice and Blossom 1973). It should be noted, however, that demonstrating the im- portance of predation on the evolution of be- havioral and morphological traits does not demonstrate its importance in affecting abun- dance and distribution. Obviously, much work needs to be done before the importance of predation can be assessed. Indirect studies need to be bolstered by determining whether the ultimate factor responsible for such behaviors as avoidance of open microhabitats is based on resource distribution or predator avoidance. This task will prove difficult if behaviors are inflexibly tied to proximate cues. Studies that measure the direct effect of predation on abundance and local distribution should be attempted as well, perhaps using island systems (cf. Vaughan and Schwartz 1980) or areas where predators have been subjected to control programs. Parasitism The role that parasitism may play in af- fecting the abundance and distribution of desert rodents has been given little consid- eration, even in comparison with the small amount of attention given predation. There are several reasons for this. First, antiparasite adaptations (such as immune response) are 98 Great Basin Naturalist Memoirs No. 7 not easily recognized and the effects of para- sites are often indirect and subtle. Second, because it is difficult to manipulate parasite loads under field conditions, it is not easy to study the importance of parasites. Third and perhaps most important, biologists often be- lieve that parasites have little ecological im- portance (but see Price 1980 and Anderson and May, 1982a). This is based on the notion that parasites should evolve to minimize their effect on their hosts: by damaging its host, a parasite would supposedly reduce its chances of reproducing. In arguing that parasites are worthy of consideration in the population biology of desert rodents, we will consider two ques- tions. First, how might parasites affect abun- dance and distribution and, second, what is the evidence that parasites can be important in affecting abundance and distribution? For this latter question, we consider a number of systems outside desert rodents as well as re- viewing the meager evidence pertaining to desert rodents. Parasites (which we consider here to in- clude viruses through parasitic arthropods) can affect abundance both by lowering survi- vorship and by consuming energy that might otherwise go to host reproduction, thereby reducing fecimdity. Anderson and May (1978, 1979, 1982b), Anderson (1978), and May and Anderson (1978, 1979) provide excellent dis- cussions of the dynamics of parasite and host populations. They argue that the ability of a parasite to regulate a host population is en- hanced by factors that promote the stability of the parasite-host dynamics, such as over- dispersion of parasites, density-dependent re- straints on the growth of parasites within hosts, and a nonlinear relationship between parasite burden and host death rate. They do not mention another very important stabiliz- ing factor: the presence of a second host spe- cies that does not suffer pathological effects from infection— a reservoir for the parasite (Baltazard et al. 1952, cited in Nelson 1980). Reservoir hosts may be especially important in affecting distribution (see discussion below). If parasites are to be important in regu- lating the abundance of the host, they must maintain enough virulence to reduce the sur- vivorship or fecimdity of the host (the follow- ing discussion is based on Anderson and May, 1982a). The reproductive rate (and therefore fit- ness) of a parasite is governed by three fac- tors. A higher reproductive rate will result from (all else being equal): higher probability of infection in an iminfected host when en- countered by an infected host (higher trans- mission rate), lower rate at which a host re- covers from a parasitic infection (lower recovery rate), and lower probability that a host dies as a result of an infection (lower virulence). If the reproductive rate of a para- site depended solely on its virulence, but if virulence was not tied to the transmission rate or recovery rate, it would be reasonable to expect the parasite to evolve to have a negligible effect on the host. However, these parameters are interrelated, at least in some systems. In the myxoma virus-rabbit system for instance, hosts infected with more viru- lent strains of virus had a slower recovery rate and a higher transmission rate than hosts infected with strains of low virulence (Ander- son and May, 1982a). Given the character of these interrelationships, parasites should evolve to some intermediate rate of viru- lence, low enough to prevent a premature death of the host but high enough to retard recovery and facilitate transmission. This is what has happened in the myxoma- rabbit system (Fenner and Ratcliff 1965, Anderson and May, 1982a). The virus introduced was extremely virulent; nearly 100 percent of the infected rabbits died quickly. Eventually the system stabilized such that the most preva- lent viral strains were of neither very high nor very low virulence, but somewhat inter- mediate in their effect. Studies of the effect of parasites on small mammal hosts are relatively rare. In addition, a number of these studies have questionable worth in assessing the importance of parasites in natural situations. First, some studies use laboratory animals as hosts, a practice that ignores the importance of coevolution of par- asites and their hosts. Second, many studies are correlative: a measure of host condition is tied to parasite load. Such correlative studies do not allow us to assign cause, since some other factor, such as poor nutrition, may have led to both poor condition and high parasite 1983 Biology of Desert Rodents 99 load. Laboratory studies that utilize experi- mental variations in parasite load will allow us to assess the effect of parasites on survivor- ship and fecundity. Only by performing field studies in which parasite loads are manipu- lated on the scale of the population will we know if the effects of parasites on survivor- ship and fecundity translate into actual ef- fects of population regulation. For illustra- tive purposes, we will list several examples of apparent importance of parasites on de- mographic parameters of mammals (other ex- amples can be found in Davis and Anderson 1971, and Price 1980): Infections of Per- omysctis leucopus by Cuterebra fontinella (bot fly) are correlated with reduced hemato- crit (Childs and Cosgrove 1966); delayed fe- male maturity, delayed litter production, and reduced male fertility (Cranford 1980); they may also cause reduced size of reproductive organs in subadult males, but have no dis- cernible effect on the size of adult reproduc- tive organs (Timm and Cook 1979). Epizoot- ics occasionally decimate populations of Ondatra zibethica (Errington 1954). In- fections by lungworms {Protostrongijlus spp.) are thought to be very important in decreas- ing siuA'ivorship in bighorn sheep in North America (Forrester 1971). What evidence exists that the abundance of desert rodents may be affected by para- sitism? Numerous studies have shown that desert rodents are often infected by a number of parasites— plague virus, nematodes, ces- todes, spirochaetes, mites, fleas, and ticks (Eads and Hightower 1952, Read and Mille- man 1953, Grundinan 1957, 1958, Reisen and Best 1973, Bienek and Klikoff 1974, King and Babero 1974, Whitaker and Wilson 1974, O'Farrell 1975, Egoscue 1976, Garner et al. 1976, Maser and Whitaker 1980, Ryckman et al. 1981). However, to our knowledge, very few studies have mentioned the effects of these parasites on their hosts. Garner et al. (1976) indicated that Dipodomijs ordii indi- viduals infected with cestodes had a reduced amount of axillary and groin fat. Several studies of gastric parasites have noted that the stomach of the host appears distended, ir- ritated, or simply filled with parasites (Gar- ner et al. 1976, Grundman 1958, King and Barbero 1974). No study has assessed the ef- fect of parasitism on population size. Two strategies of study can increase our knowledge of the importance of parasitism in desert rodent populations. First, laboratory studies utilizing wild rodents and their natu- ral parasites can be used to make precise quantitative measures of the effect of parasite loads on parameters important to the demog- raphy of a population. Second, field studies should be attempted in which internal para- site loads are manipulated by administering the appropriate drug to a portion of a popu- lation and external parasites are manipulated, perhaps at burrow sites, using techniques used to control the ectoparasites of domestic animals (e.g., flea collars). Such studies should yield further information on the effects of parasitism demographic parameters and, per- haps, on the effect of parasitism on rodent abundance. Distribution In this section, we address two basic ques- tions. First, what factors are important in de- fining the geographic ranges of desert ro- dents? Second, within the range of a species, why doesn't that species occur ubiquitously over all habitats? That is, what factors lead to patterns of local distribution? As will be seen, many of the factors important in determining abundance should also affect patterns of local geographic distribution. After a brief discussion of physical barriers, we will address the importance of three abiotic factors (temperature, moisture, and substrate) and four biotic factors (vegetation, competition, predation, and parasitism) to lo- cal and geographic distribution. It is common for two or more factors to interact in a syner- gistic manner. In the discussion below, the most common example of synergism is the in- teraction of temperature, moisture, and sub- strate to produce patterns in the distribution of vegetation, which in turn appears to affect the distribution of desert rodents. Physical Barriers Physical barriers (e.g., habitat dis- continuities, mountain ranges, rivers) often persist over long periods of time, are readily discernible, and, for desert rodents, can be put on maps (e.g., Hall 1946, Durrant 1952, 100 Great Basin Naturalist Memoirs No. 7 Hall and Kelson 1959, Hall 1981). In general these barriers represent both the proximate and ultimate factors that circumscribe the geographic distributions of species. Hall (1946), Durrant (1952) and, more re- cently, Brown (1973, 1975), and Brown and Lieberman (1973) noted striking differences in the composition of rodent communities in the eastern and western Great Basin desert. They suggested that eastern Great Basin desert communities are depauperate and that orographic barriers have limited certain spe- cies (e.g., D. deserti, D. merriami, Micro- dipodops pallidus) to western habitats. Phys- ical barriers often can be invoked to account for the limits of spatial distribution on at least one range boimdary of many desert het- eromyid, cricetid, and sciurid species in North America (Hall and Kelson 1959, Hall 1981). Besides orographic barriers, rivers ap- pear to play a significant role in limiting the distribution of populations of a species. Range boundaries of Perognathus formosus, P. spinatus, P. penicillatus, P. intermedins, Ammospennophilus leucuriis, and A. harrisii are partially coincident with the Colorado River. The high frequency with which phys- ical barriers limit species' distributions cor- roborate other empirical data that suggest that mammals are relatively poor dispersers across imsuitable habitats (Carlquist 1965; Brown 1971, 1975). Abiotic Factors: Temperature, Moisture, Substrate Abiotic factors that vary in a continuous or mosaic manner are also important in circum- scribing geographic ranges and affecting lo- cal distribution, although their effects are usually more subtle than those of the highly visible physical barriers just discussed. In many situations, cause and effect relation- ships may be confounded by synergistic inter- actions among variables and by an inability to distinguish proximate from ultimate fac- tors. In the next section, we first discuss how single abiotic factors can limit distributions, then deal with the problem of synergism. Correlations between the distribution of desert rodent species and various measures of temperature have been reported in the liter- ature for many years. Sixty years ago, Grin- nell (1922) suggested that temperature was important in creating barriers to dispersal and, ultimately, could be used to account for the distribution of Dipodornys in California. The observations that D. merriami has rela- tively little ability to regulate body temper- ature (Dawson 1955) and that the northern extent of its distribution is coincident with the 30 F isotherm for average January tem- peratures (Reynolds 1958) suggests that low winter temperatures may limit the range of this species to warm desert habitats. Gaby (1972) found that D. merriami (an inhabitant of low, hot deserts) and D. ordii (which tends to inhabit higher, cooler deserts) have inter- specific differences in temperature- dependent metabolic rates that correspond to the different requirements of their ranges. In these experiments D. ordii was less tolerant of high temperatures than D. merriami; D. mer- riami had a higher metabolic rate at low am- bient temperatures. Unfortunately, it is un- clear what role these intrinsic differences play in affecting geographic distributions. The question becomes one of cause and ef- fect: are D. merriami populations limited to warm desert regions because they are unable to cope physiologically with colder temper- atures, or are the metabolic differences be- tween these kangaroo rats merely a result of local adaptation to contrasting environmental conditions? Physiological research has long demon- strated, through the study of functional adap- tations, the high premiums placed on water conservation for rodents in desert habitats (Howell and Gersh 1935, Schmidt-Nielsen et al. 1948, Schmidt-Nielsen and Schmidt- Nielsen 1951). More recently, negative effect of increased ambient temperature on water balance has been elucidated (MacMillen and Christopher 1975). Beatley (1969a, 1976) noted that a species must necessarily be lim- ited to areas where positive water balance (a hinction of interaction of temperature, avail- able moisture, and the physiology of the spe- cies in question) can be maintained. Howell and Gersh (1935) first quantified the urine-concentrating capacities of Di- podomijs and found substantial interspecific variation. That this capacity at least corre- sponds to distribution is indicated by studies comparing D. merriami and Dipodomys of less arid habitats: D. merriami has a higher 1983 Biology of Desert Rodents 101 urine-concentrating ability (comparison with D. agilis; Carpenter 1966) and a lower rate of body water tiunover (comparison with D. mi- crops; Mullen 1971). Substrate characteristics also appear to af- fect distributional patterns of desert rodents. Grinnell (1922) suggested that desert rodents are limited in geographic distribution via the matching of pelage coloration with color tone of tlie background, though this may be a matter of local adaptation. Other studies con- tend that both local and geographical distri- butions of desert rodents are limited to those areas with soil conditions that do not inhibit the burrowing habits of a given species. Dipodomijs deserti appears to be restricted to deep sand areas, a substrate that is conducive to the construction of large, deep burrow sys- tems (Grinnell 1914, Hall 1946, Reynolds 1958, Roth 1978). Dipodomijs merriami is of- ten excluded from areas that have a surface layer of rocks, heavy clay, sulphate crust, or hard-pan because of the difficulty in digging burrows in such soil types (Vorhies and Tay- lor 1922, Hardy 1945, Hall 1946, Huey 1951, Reynolds 1958). In fact, Huey (1951) sug- gested that this was the main factor con- trolling the geographic distribution of D. m.erriami below 4500 feet in western North America. The complex nature of physiological inter- actions (primarily through the dissipation of heat and conservation of water) with burrow environments suggests that local distributions may be affected by soil type (Gaby 1972, Hoover 1973) as well as the potential for bur- row ventilation via surface winds (Kay and Whitford 1978). Such speculation is sup- ported by some novel work that employs physiological and behavioral data to account for the distribution of two species of Pe- rognathus in New Mexico. This work (Hoo- ver et al. 1977) suggests that P. intermedins can tolerate a wide range of burrow micro- climates but is behaviorally excluded by P. penicillatns from substrates that have a high heat buffering capacity (the preferred bur- row sites of P. penicillatus). If P. penicillatus can tolerate only a small range of burrow mi- croclimates and is behaviorally dominant to P. intermedins, this is an example of an in- cluded niche (Col well and Fuentes 1975). Unfortunately, definitive experiments in which P. penicillatus is experimentally re- moved to see if P. intermedins is, in fact, be- haviorally relegated to less-preferred habitats by P. penicillatus were not performed. Nev- ertheless, the data strongly suggest that phys- iological differences between these species mediate the interspecific interactions that de- termine the local distributions of these species. More recently, hypotheses that focus on in- terspecific interactions and differential forag- ing behaviors have been invoked to account for patterns of substrate philopatry in some rodent species. Reichman and Oberstein (1977) and Price (1978b) have suggested that divergent body sizes and morphologies of heteromyid species reflect adaptations for ex- ploiting different seed dispersions. Seed den- sity and dispersion appear to be affected by microtopography and soil structure (Reich- man and Oberstein 1977, Bowers 1979, 1982). Areas with fine substrates permit the accumulation of dense seed aggregations by trapping windblown seeds in depressions, whereas on substrates consisting of larger soil particles, seeds are trapped individually. Be- cause of their larger size and saltatorial loco- motion, Dipodomijs are thought to specialize on the exploitation of seed clumps that pro- vide large energy returns per unit time. Therefore, the distribution of Dipodomijs should be coincident with fine substrates. In contrast, the smaller, quadrupedal Pe- rognathus are thought to forage for more dis- persed (individual) seeds and, consequently, should prefer areas with larger soil particle sizes. Differential substrate utilization be- tween these genera has been documented at the local habitat level (WondoUeck 1978, Bowers 1979); there is no a priori reason why the same mechanism might not be working to affect geographical distributional patterns as well. Vegetation Possibly the greatest effect of temperature, moisture, and substrate is a synergistic one, affecting the local patterns of vegetative structure and the distribution of certain plant species. Dice and Blossom (1937) suggested that the physiognomy of the vegetation was 102 Great Basin Naturalist Memoirs No. 7 an important factor in determining the distri- bution of desert rodent species. More recent- ly, positive relationships between annual pre- cipitation and perennial plant species diver- sity, density and size (Beatley 1969, Brown 1973, Hafner 1977), as well as perennial and annual seed standing crop (Lieberman 1974) have been established. That D. merriami is limited in geographic distribution to areas re- ceiving less than 25 cm of annual precipi- tation (Reynolds 1958) and prefers habitats of little vegetative cover (Hall 1946, Lidicker 1960, Brown and Lieberman 1973, Rosenz- weig 1973, Schroder and Rosenzweig 1975) suggest an indirect effect of moisture on lim- iting habitat characteristics for some species. By comparison, D. ordii is apparently limited in distribution to more grassy habitats that have an annual precipitation of more than 25 cm (Reynolds 1958, Schroder and Rosenz- weig 1975). A similar relationship may occur on a geographic scale: D. merriami has ex- panded its geographic range to include over- grazed grassland (now desert scrub) habitats that once were more typical of D. ordii habi- tats (Reynolds 1958). Precipitation, through its effect on the quantity of available food (seed) resources, may also affect the geographical distribution of some desert rodent species. Frye (pers. comm.) found that most species of large (> 100 g) Dipodomys species are restricted to those areas that predictably receive sub- stantial annual precipitation. It is likely that the relatively large amoimt of food resources required by rodents of large body size coupled with the constraints of finite forag- ing areas limits large species to more produc- tive areas. A potential exception to this pat- tern is D. deserti, which often occurs in areas of the Mojave and southwestern Great Basin deserts that receive little precipitation. Al- though the total amount of resources pro- duced in these areas is probably com- paratively small, D. deserti is restricted to sand-dune habitats, which should be richer than surrounding habitats. This is because food resources will be concentrated in dune areas on two different scales by the action of surface winds. First, the same wind patterns that transport sand from the surroiuiding val- ley and concentrate it into dunes will trans- port seeds to dune areas as well. Second, on the dunes themselves, seeds will tend to ac- cumulate in depressions, thereby further con- centrating the resource, making it more ef- ficient for kangaroo rats to harvest. The interaction of climatic and substrate variables affect the distribution of certain plant species or types (e.g., the associations of Shelford 1913) to which, in turn, are closely tied the distribution of some desert rodents. For example, it is well documented that the distribution of D. microps is coincident with the distribution of chenopods of the genus Atriplex (Grinnell 1933, Jorgensen 1963, Ke- nagy 1972a, b), upon which it is phys- iologically and morphologically adapted to feed (Kenagy 1972a, b; but see Csuti 1979). Atriplex, in turn, is usually limited to alkali flats surrounding dry basins of Pleistocene Lakes (Hall and Dale 1939, Munz and Keck 1959). Field observations (Hall 1946, Cameron 1971, Brown et al. 1972, Cameron and Rain- ey 1972, Olsen 1975) have documented rela- tionships between the presence of cricetid ro- dents and succulent desert vegetation. It is likely that this pattern results from the need of some species of Peromijscus and Neotoma to consume succulent vegetation to maintain positive water balance (Olsen 1975). Interspecific Interactions Comparative physiological data do not al- ways account for differences in the local dis- tribution of closely related species, and other causal and effect mechanisms must be in- voked. Lee (1963), in an investigation of the physiological adaptations of N. lepida and N. fuscipes to arid and semiarid habitats, found no physiological bases for the observed dif- ferences in local distribution where the spe- cies ranges overlap. A study focusing on the competitive relationship of these species in the Mojave Desert of southeastern California found that these species are distinctly sepa- rated in most aspects of the habitat (Cameron 1971). Dietary studies, however, revealed that, when allopatric, both N. fuscipes and N. lepida prefer a common food plant {Quercus turbinella), whereas N. lepida switches to a less preferred species {Junipenis californica) when sympatric with N. fuscipes. An investigation of behavioral interactions 1983 Biology of Desert Rodents 103 (Cameron 1971) suggested that N. fuscipes is dominant over N. lepida, relegating the latter to areas of low Qtiercus density, and con- trolling the preferred food resource via habi- tat selection and defense. Such data support the premise that interspecific competition for limited food resources affects patterns of lo- cal distribution. The differential occurrence of Dipodomys and Perognathus in different, but contiguous, microhabitats has been documented by nu- merous studies focusing on the local distribu- tion of these genera. This body of data repre- sents the best-documented pattern of habitat use by desert rodents. Perognathus tend to in- habit areas of high vegetation cover (Arnold 1942, Hall 1946, Reynolds and Haskel 1949, Reynolds 1950, Rosenzweig and Winakur 1969, Feldhammer 1979, Brown and Lieber- man 1973, Rosenzweig 1973, Price 1978a, Wondolleck 1978) and coarse substrate types (Hardy 1945, Hall 1946, Rosenzweig and Winakiu- 1969, Brown 1975, Hoover et al. 1977, Wondolleck 1978). In contrast, Di- podomys, on a local scale, tend to be found in more open microhabitats with finer substrate (Hall 1946, Lidicker 1960, Rosenzweig and Winakur 1969, Brown and Lieberman 1973, Wondolleck 1978, Price 1978a; for a com- plete review, see Brown et al. 1979b; but see Thompson 1982a). In the section on abundance, we briefly discussed two mechanisms, based on com- petition and predation, that have been hy- pothesized to account for differential utiliza- tion of microhabitats by Dipodomys and Perognathus. The predation hypothesis is based on the early observations that Di- podomys is better adapted to avoid pre- dation, via locomotory (Bartholomew and Caswell 1951) and auditory (Webster 1962) specializations, when compared with the more quadrupedal Perognathus (although Pe- rognathus was subsequently shown to share most of the auditory specializations found in Dipodomys; Webster and Webster 1975). Consequently, Perognathus are thought to oc- cupy areas of high vegetative cover mainly as a result of predation pressure that covaries with local vegetative physiognomy (Rosen- zweig 1973, Thompson 1982a). Even though recent work of Thompson (1982a) has dem- onstrated that Dipodomys also use areas of high vegetative cover, perhaps as a refuge from predation, it is thought that saltatorial kangaroo rats use open, poorly vegetated areas to a significant extent in the exploita- tion of food resources. The experimental work of Thompson (1982b), O'Dowd and Hay (1980), and Kotler (in press) provides evidence that predation is important in de- termining microhabitat use. However, predation is not the sole factor influencing microhabitat use. If predation alone affects the differential use of micro- habitats and habitats by Perognathus and Dipodomys, the experimental removals of Dipodomys by Wondolleck (1978) and Price (1978a) should not have caused shift in mi- crohabitat use by Perognathus. In all proba- bility, properties of the resource base that vary according to habitat microtopography interact with locomotory differences in for- aging of Dipodomys and Perognathus to help produce the observed differences in habitats utilized. The competition hypothesis couches patterns of habitat use in terms of the ability of a species to exploit a resource base that varies on a spatial scale. But there are several variations on this general theme, and even the mode of competition (e.g., exploitation vs. interference) has been a subject of much discussion. Much evidence suggests that desert gran- ivorous rodents subdivide seed resources by exploiting different seed dispersions. As dis- cussed above, seed density and dispersion ap- pear to be influenced by microtopography and vegetative structure (Reichman and Oberstein 1977). Consequently, it is hypoth- esized that the microhabitat affinities shown by desert rodents may exist because micro- habitats differ in the degree to which they contain clumped seeds. Large saltatorial Dipodomys forage mainly in open, vegetation-free habitats where windblown seeds accumulate in depressions or adjacent to objects acting as windbreaks (Reichman and Oberstein 1977, Bowers 1982). Thus, bi- pedal kangaroo rats are thought to forage from seed clump to seed clump, spending little time in the interspersed seed-poor areas (but see Frye and Rosenzweig 1980). By con- trast, Perognathus and other quadrupeds for- age under bushes (Brown and Lieberman 1973, Rosenzweig et al. 1975, Price 1978a), where seeds are more uniformly distributed. 104 Great Basin Naturalist Memoirs No. 7 Although such a scheme is supported by both theoretical (Reichman 1980) and em- pirical (see Brown et al. 1979b for a review) data, the actual mechanisms resulting in spa- tial segregation of Dipodomys and Pe- rognathtts on a local level are unclear. In par- ticular, do DipodojJiys use aggression to competitively exclude Perognathus from the seed-rich, open areas as suggested by Hutto (1978) and Trombulak and Kenagy (1980), or are the patterns of microhabitat use merely the result of more proficient exploitation of seed clumps by Dipodomys relative to Pe- rognathus (Reichman and Oberstein 1977, WondoUeck 1978, Price 1978b)? Congdon (1974) reported an instance where interspecific aggression of D. deserti toward D. merriami appeared to be depen- dent on the amount of available resources. In periods of low resource availability, D. mer- riami and D. deserti cooccurred in habitats with sand substrates, but when the resource base was augmented, indirectly, by an intense summer storm, D. merriami moved into non- sandy habitats, presumably to avoid the ag- gressively dominant D. deserti (Congdon 1974). This pattern may result from several factors. First, resources may have become dense enough following the storm to become economically defensible (Brown 1964) by D. deserti. Second, increased resource avail- ability may have allowed D. deserti to spend less time foraging and more time engaged in aggressive interactions (see Caraco 1979). Although instances of aggression in desert rodents have been reported many times (Hall 1946, Eisenberg 1963, Christopher 1973, Ke- nagy 1976, Blaustein and Risser 1976, Hutto 1978, Trombulak and Kenagy 1980), its role in determining local distributions is unclear. In most cases, the appropriate experiments have not been done (but see Frye, in press). In fact, some authors (Brown and Lieberman 1973, Brown et al. 1979, Bowers and Brown 1982) contend that for granivorous desert ro- dents it is very rare that the distribution of resources is sufficiently dense for inter- specific aggression to be an economically fea- sible strategy. Interspecific interactions that affect pat- terns of habitat use, on a local scale (Rosenz- weig et al. 1975, Price 1978a, Brown et al. 1979b), might also play a role in limiting the geographic distributions of certain rodent species. Bowers and Brown (1982) found that those rodent species that a priori were most likely to compete (e.g., similar-sized species of the granivore guild) overlapped less in their geographic ranges and cooccur less of- ten in local communities than a null model predicted. In contrast, overlaps between and cooccurrences of pairs with different trophic affinities (e.g., interguild comparisons) did not differ from the random model. Body Size Body-size, per se, may also play a role in determining the distribution of desert rodent species by affecting the way rodents use cer- tain resources. Grinnell (1914) and Hall (1946) noted that an intermediate-sized het- eromyid, D. merriami, was found in nearly every desert habitat, whereas the larger D. deserti was more restricted in habitat. From this pattern Grinnell (1914) concluded that larger species usually have more restricted habitat utilization patterns and more circum- scribed geographic ranges than their smaller relatives. More recently, Mares and Williams (1977) reported the result that intermediate- sized species of Perognathus and Dipodomys occupy the northern and eastern range limits of the family, whereas, in the center of heter- omyid diversity, an array of smaller and larger species are syntopic with intermediate- sized species. Bowers (in preparation) in- vestigated the relationship between geogra- phic range and body size for 46 heteromyid species and suggested that body size is an im- portant factor in affecting the extent of a species distribution. Intermediate and very small species are characterized by having large distributions, but small and large heter- omyids have relatively small ranges. As many economic, physiologic, and behavioral char- acteristics covary with body size (Eisenberg 1963, Rosenzweig and Sterner 1970, French 1976, Reichman and Brown 1979), it is diffi- cult to attach cause and effect relationships between certain biological properties and ge- ographic range. However, patterns of re- source use and the propensity of a species to enter food-induced torpor, both of which change with body size (Rosenzweig and Ster- ner 1970, Brown and Lieberman 1973, Mares 1983 Biology of Desert Rodents 105 and Williams 1977, Reichman and Brown 1979), appear to be of particular importance in the determination of geographic distribution. Hypotheses regarding geographic distribu- tion are almost impossible to test via manipu- lation. However, it seems plausible that many of the ecological factors important in affect- ing local distribution should also affect the extent of the geographical distribution of a species and, therefore, that geographic distri- bution can be studied, via inference, through studies at the local level. At best, the projec- tion of locally studied factors to explain large scale patterns is myopic. However, such an approach has been employed in other sys- tems with apparent success (see Glazier 1980, Reaka 1980, Brown 1981). Habitat Selection Throughout our discussion of distribution, we have given many examples of habitat or microhabitat affinity. An important problem that remains is to determine whether these affinities are completely due to physiological or physical hmitation (which has often been implicit in our discussion, especially of abiot- ic factors), or whether these affinities result at least in part from habitat selection originating from competitive interactions. Rosenzweig (1979, 1981) has developed mod- els of competition-based habitat selection that can be illustrated as follows. Imagine a species. A, that prefers habitat type a over a different type, b, perhaps because it is more efficient at harvesting resources in a. At low densities, all A will be found in habitat a. As the density of A increases, however, the fit- ness of individual A in habitat a will gradu- ally decrease (because of resource degrada- tion); eventually, habitat a will be degraded to a point where a and b are equal in quality. At this point, A should inhabit b as well as a; an observer would detect no habitat affinity (though a difference in density could exist). Now introduce species B, which prefers habi- tat b because it is more efficient at harvesting resources there. Because they prefer b over a, B will tend to degrade habitat b, reducing the fitness of A on b, leading A to inhabit only habitat a. Such competition-based habitat selection neither requires nor precludes interspecific aggression. Furthermore, habitat selection may be dependent on contemporary inter- actions or, if interactions occur over a very long time, species may evolve inflexible be- havioral, morphological, or physiological ad- aptations that can enforce habitat selection even in the temporary absence of the com- petitor species. The evolution of inflexible habitat selection was invoked by Shroeder and Rosenzweig (1975) to explain the result that reciprocal removals of D. merriami and D. ordii failed to result in either a wider range of habitats used or density change in the target species when the congener was absent. How can it be determined if a specific case of affinity for a certain type of substrate or vegetation results from competition-based habitat selection? If habitat selection is based on contemporary interactions, removal ex- periments (as we called for in the Pe- rognathus intermedius-P. penicillatus system) should suffice. If, on the other hand, habitat selection has evolved to inflexibility, then simple removal experiments will not dis- tinguish between competition-based habitat selection and a complete lack of competition: no response would be expected in either case. Study of "natural experiments" is then called for. If a species expands its use of habitats in geographic areas where the putative com- petitor is absent, then the contention that competition is important in causing habitat selection is supported. Predation and Parasitism Distribution may also be affected by pre- dation and parasitism. The probability of being preyed upon may be so high in certain habitats that some species are either extermi- nated in those areas or individuals are unwill- ing to enter them. Although there are no documented cases of habitat or range restric- tion that are directly attributable to pre- dation, it -has been speculated (Brown, pers. comm.) that the range of the kangaroo mouse, Microdipodops pallidus, may be re- stricted by the presence of the sidewinder rattlesnake (Crotalus cerastes); these two dune specialists do not appear to cooccur on 106 Great Basin Naturalist Memoirs No. 7 dune systems even though their ranges abut. This pattern may occur because the kangaroo mice appear to be particularly vulnerable to attacks by sidewinders (which are pit vipers); instead of hopping away when attacked by a predator (as kangaroo rats do; Webster and Webster 1971), they simply remain motion- less (Brown, pers. comm.). Parasites may be important in determining distribution as well. Barbehenn (1969) devel- oped a hypothesis in which competitive ex- clusion of one species by another species is resisted by "germ warfare" on the part of the competitively inferior species. In the simplest scenario discussed by Barbehenn, if the inferi- or species harbors a parasite to which it has evolved resistance and if the parasite is re- stricted to certain habitats by requirements of the intermediate host or vectors, then those habitats will provide refuges for the in- ferior species; individuals of the com- petitively superior species that invade this habitat will be killed by parasites. Cornell (1974) extended this hypothesis in an attempt to explain distributional gaps between con- geners. In this case, each host species carries a strain or species of parasite (to which it is resistant) but is killed when infected by the parasite carried by the other host species. Where the ranges of these host species abut, individuals of both species would be killed by parasites carried by the other species. In both these models, the interactions between the parasite and the resistant host are relatively stable; therefore it is unlikely that reduced virulence need evolve. One example of the effect of parasites on distributions is the contraction of the range of the moose {Alces alces) in the face of the expansion of the whitetail deer {Odocoileus virginianus) range, which is thought to be caused by meningeal worms harbored by the whitetail deer that are fatal to the moose (Price 1980). Another possible example in- volves Peroniyscus maniculatus and Neotoma cinerea inhabiting lava caves in northeastern California. Peroniyscus maniculatus harbors bubonic plague; populations of A^ cinerea in these caves are occasionally exterminated by outbreaks of disease (Nelson and Smith 1976). Absolutely nothing is known of the impact of parasites on the distribution of desert ro- dents. To gain this knowledge will require extensive study of host-parasite dynamics within each system considered. Population Structure In this section we will discuss two aspects of population structure: breeding structure (who mates with whom) and certain aspects of spatial structure, primarily home range use and dispersal. We are mainly interested in the effects of these on population genetic structure, which we define here as the way in which a population deviates from panmixia. Deviation from panmixia can have several important effects on the evolutionary dynam- ics of populations. 1. Fixation of alleles by random drift is more likely to occur with small, effective population size and discrete subpopulations, than in large panmictic populations. Drift is important in one model of evolution, em- bodied in the shifting balance theory of Wright (1977), but is imnecessary or even a hindrance for evolution in models that as- sume panmixia (Haldane 1924, Fisher 1930). 2. Localized extinctions, which are impor- tant in most scenarios of group selection (e.g., Wilson 1977, Gilpin 1975) and island bio- geography (MacArthur and Wilson 1967, Brown 1971), are more likely to occur in sub- populations that are small and discrete. 3. Demic structure and resistance to immi- gration may reduce the impact that gene flow has in maintaining species integrity and thereby make interpopulation divergence more likely (Anderson 1970; but see Baker 1981). 4. The evolution of some social and al- truistic behaviors is thought to partially de- pend on subpopulation groupings that are based on kin ties (e.g., Hamilton 1972, Sher- man 1977, Michod 1979, 1980) or possession of traits common to members of a group (Wilson 1977). 5. High variance in reproductive success can result from competition for mating op- portunities (typically among males), active choice of mates by members of one sex, or differential survival of young. Differential re- productive success among members of one or both sexes will not only lead to reduced ef- fective population size (Wright 1940, Patton and Feder 1981), but it will also lead to more 1983 Biology of Desert Rodents 107 rapid evolution within populations since se- lective pressures due to variance in reproduc- tive success are more pronounced than when mating is random within populations (Wilson et al. 1975). At least four types of evidence can be used to study population structure: behavioral, de- mographic, indirect genetic, and direct ge- netic. We will treat each in turn and describe what is known for desert rodents, covering primarily heteromyids. Behavioral Evidence Behavioral evidence can be used to infer the importance and probable effect of vari- ous mechanisms in structuring populations. In some desert rodents, male dominance may play an important role in breeding structure. There is evidence suggesting that, among some kangaroo rats, certain males may de- fend the burrows of females against other males. Kenagy (1976) observed two male D. microps fighting at the mound of a female, and saw the winner copulate with the female. Similarly, Randall (pers. comm.) observed one D. spectabilis defend the mound of a fe- male against several other males. In the thom-forest-inhabiting heteromyid Liomys salvini, Fleming (1974) found that size was a good predictor of dominance and that larger males were surrounded by more potential mates than were smaller males. In the northern grasshopper mouse, OnycJiomys leucogaster, there is some evi- dence that males and females form at least temporary pair bonds, a behavior that would tend to reduce variance in male reproductive success. First, Ruffer (1965) observed male parental care in the laboratory. Second, Ego- scue (1960) found that, even at low densities, members of a male-female pair of O. leuco- gaster were often caught in adjacent traps, indicating that they lived or traveled togeth- er. A similar pattern occurs in Peromysctis eremicus (Munger, mipubl. data). Patterns of home range overlap can also be used to infer breeding structure. For instance, if males defend the burrows of females, as has been observed for D. spectabilis and D. mi- crops, there might be little home range over- lap between males, and the home ranges of certain males might include the mounds of some females exclusive of other males. On the other hand, if males do not defend the areas of females, one expects to find extensive overlap between males; exclusive access to females by certain males should be rare. This latter pattern of home range overlap charac- terizes D. merriami; male-male overlap of home ranges is extensive and the home range of each female is overlapped by the home ranges of several males (O'Farrell 1980; Jones, 1982). Data on dispersal behavior are also useful in understanding population structure. Dis- persal data are lacking for most desert ro- dents, but in those species that have been studied there appears to be a low degree of individual vagility. Jones (1982) measured distances moved by juvenile D. spectabilis and D. merriami. He was able to detect suc- cessful dispersal moves of up to 0.9 km (15 to 20 home range diameters), yet he found that among those juveniles surviving to reproduc- tive maturity, less than 25 percent of D. spec- tabilis and only 11 percent of D. merriami dispersed to areas not adjacent to their natal sites. Most of these cases of dispersal involved movements of less than three home range di- ameters. The possibility of long distance dis- persal (>0.9 km) cannot be ruled out, though. French et al. (1974) measured dis- persal up to 0.9 km in Perognathus formosus (whose home range diameter is less than half that of D. merriami; Maza et al. 1973) and determined that more individuals dispersed short distances and more dispersed long dis- tances than would be expected if individuals simply moved to the nearest vacancy. In other words, although most individuals made only very short dispersal moves (as was shown for D. merriami and D. spectabilis), there were a few P. formosus individuals that moved a great distance. The possibility that D. merriami and D. spectabilis make similar long distance moves needs to be checked by studying dispersal in these species over at least 40 home range diameters (2 km). Information on the extent of dispersal in other desert rodents is sketchy. Allred and Beck (1963) found that the average distances between most widely separated capture loca- tions for each individual were greatest for Onychomys torridus males and Peromyscus 108 Great Basin Naturalist Memoirs No. 7 maniciilatus males, somewhat less for O. tor- ridus females, P. maniciilatus females, and D. merriami, and still less for D. microps and Perognathus longimembris. Among D. mi- crops, for which the average distance be- tween capture locations was about 76 m, 79 percent of males (n = 183) and 87 percent of females (n = 126) ranged less than 122 m. Among P. longimembris most animals of both sexes ranged less than 30 m (n = 102). Such data suggest that D. microps and P. long- imembris are quite sedentary. Roberts and Packard (1973) reported that the average home range size in the Texas kangaroo rat D. elator was .08 ha, and that the maximum dis- tance moved between traps was 87 m for males and 109 m for females. It is not clear what portion of the movements in either study represent daily movements about the home range as opposed to dispersal or shifts in home range boundaries. To imderstand the effects of these movements on population genetic structure, we need to know the distri- bution of movements in terms of home range to determine what fraction of an animal's movements bring it into contact with individ- uals they do not normally encounter within their own home ranges. It is also unclear from these data which movements represent permanent shifts in home ranges vs. tempo- rary excursions out of the usual home range. We emphasize that these sorts of behav- ioral data are, by themselves, insufficient to determine how populations are structured. There are several reasons for this. First, though some dominant males may defend fe- males, subordinate males may steal cop- ulations and thus dilute the effects of territo- rial defense. Second, the timing of mating may be crucial. An observer might see sever- al males copulating with a female, but it may be that only the male that mates with her at peak receptivity during estrus will success- fully fertilize her. Third, among heteromyids, individuals occasionally make long forays (3 to 4 home range diameters) away from their usual home ranges. Maza et al. (1973) report- ed that these long distance excursions are correlated with reproductive activity in P. formosus. Long-distance forays also occur in D. merriami and D. microtis (A 11 red and Beck 1963) and in D. spectabilis (Jones, 1982). The actual influence of these excursions on the breeding structure of a population is un- known, but it seems that they would increase the number of female home ranges to which a given male has access. And fourth, dis- persers will have no effect on population structure unless they breed or otherwise dis- rupt the breeding structure of the residents. Liebold and Munger (in preparation) have shown that dispersing female D. merriami tend to be less successful at breeding than their nondispersing counterparts, indicating that their effect on population genetic struc- ture might be less than would be expected from examining dispersal behavior alone. Demographic Evidence Breeding structure is also partially depen- dent on demography. The number of breed- ing individuals and the variance in their life- time reproductive success may be influenced by survivorship and longevity. For example, a few individuals may survive to adulthood and live through several breeding seasons, but most individuals either do not survive to reproductive maturity or reproduce only once. In this situation, the reproductive out- put of a population is concentrated in a small number of long-lived adults. The contrasting situation is one in which longevity is nearly equal for all adults so that those individuals reaching reproductive maturity all reproduce once or twice and then die. In this case the lifetime reproductive contributions of all adults might be more nearly equal than in the former situation. Both of these age struc- tures are found in heteromyids. The latter characterizes L. salvini. Annual turnover is nearly complete; young are born in the spring and by the next breeding season year- lings make up nearly 100 percent of the pop- ulation (Fleming 1974). Dipodomys spec- tabilis appears to be an example of the other situation. Holdenreid (1957) studied a popu- lation near Santa Fe for 27 months, and stated that "the population was composed of a few well-established individuals remaining continually on the area and a much larger number of animals that remained for only a few days or months" (p. 338). In general, desert rodents tend to be long lived relative to nondesert rodents (Smith and Jorgensen 1975, Conlev et al. 1976; members of some 1983 Biology of Desert Rodents 109 Perognathus species may live up to five years, French et al. 1967). In most cases, however, it is unknown whether there is a high vari- ance in survivorship that might lead to a large differential in reproductive success. Indirect Genetic Evidence Indirect genetic evidence concerning pop- ulation structure can be gathered by deter- mining if genotypic frequencies deviate from an expectation based on random mating. Ras- mussen (1964) found a deficiency of hetero- zygotes of blood group loci in Peromyscus maniculatus, implied that inbreeding was the cause, and calculated a relatively small ge- netic neighborhood size of 10-75 individuals. Selander (1970) found a deficiency of hetero- zygotes in a population of house mice and from this inferred that the population was structured into small denies (but see Baker 1981). He strengthened his assertion by citing behavioral studies that showed an organiza- tion into families or tribes. Patton and Feder (1981) calculated F statistics (Wright 1965, Nei 1975) for populations of Thomomys bot- tae. The measure of random mating within a population (Fit) can be decomposed into two parts, deviation from random mating among subpopulations (Fst) and nonrandom mating within a subpopulation (Fjs). Patton and Feder showed a significant amount of diver- gence among subpopulations, but results were equivocal for within-subpopulation matings. Schwartz and Armitage (1980) sim- ilarly calculated F statistics from electro- phoretic data on yellow-bellied marmots Mamiota flaviventris. They found evidence for considerable gene flow between colonies and no evidence for inbreeding, and thus concluded that it is unlikely that evolution in these marmots is accelerated by fixation of alleles via inbreeding within colonies. Relatively little indirect genetic evidence exists concerning the breeding structure of desert rodent populations. Studies that mea- sure allelic diversity are typically concerned with systematics at the subspecies level or above, or with describing the amount of vari- ation that exists in populations. The pub- lished data are usually genie, not genotypic, frequencies and values of overall hetero- zygosity and polymorphism; genotypic fre- quencies are required to detect deviations from random mating. Furthermore, sample sizes from any one population are often too small to allow statistical tests. Finally, it is not possible to determine if the samples from any one study site are from one or several subpopulations; population structure will af- fect the interpretation (Patton and Feder 1981). Two studies do provide some indirect ge- netic evidence concerning structure in desert rodent populations. Using a pelage character, Blair (1947) showed no deviation from ran- dom expectation within subpopulations of Pe- romyscus rnaniculatus blandus. In addition, there was little divergence of subpopulations from nearby (less than 5 km) subpopulations, indicating that dispersal between sub- populations does occur. More distantly sepa- rated subpopulations did diverge, however. Johnson and Selander (1970) gave diagrams showing the spatial associations of genotypes at four loci in D. merriami, and described two of the loci as having clumped distributions of alleles. They suggested that this pattern might indicate a low level of dispersal and some inbreeding, though no statistical test of the pattern was presented. Their findings are at least consistent with the findings of Jones (1982) for dispersal distances of D. merriami. Direct Genetic Evidence Indirect evidence yields only the knowl- edge that some deviation from panmixia has occurred, but does not determine which mechanism causes the deviation. This is illus- trated by the findings of Patton and Feder (1981): the deviations from random mating they observed within subpopulations of goph- ers may not have been due to inbreeding but instead to demic structure within the subpopulation. Direct genetic evidence, on the other hand, ties a genetic effect to the mechanism causing it. For instance, by identifying geno- types at a number of polymorphic loci for all individuals within a population, it is often possible to determine precisely what success- ful matings have occurred in the population. Patton and Feder (1981) used this technique to show that relatively few males of the pocket gopher Thomomys bottae fathered most of the young in their study area. 110 Great Basin Naturalist Memoirs No. 7 Hanken and Sherman (1981) used it to dem- onstrate multiple paternity in Belding's ground squirrel {Spemiophilus beldingi litters. Foltz and Hoogland (1981) determined that most litters of the black-tailed prairie dog Cynomys ludovicianus were sired by resident males within the home coterie, indicating that coteries were the units of reproduction within the population as well as the units of social structure. Foltz (1981) also used ge- netic evidence to determine that female old- field mice Peromyscus polionotiis usually mate with the same male for consecutive lit- ters, thus demonstrating long-term mo- nogamy in this species. As yet, there are no published studies showing direct genetic evi- dence of structure in desert rodent popu- lations, but work is under way for two spe- cies, D. spectabilis and D. merriami. Clearly, there are opportunities for more research on the structure of desert rodent populations, and what we now know suggests some interesting possibilities. One of these concerns deme size and the extent of sub- structuring of populations. Two lines of evi- dence, the description by Johnson and Selan- der (1970) of clumped distributions of alleles and observations by Jones (1982) of short dis- persal distances, suggest a substantial demic structure in D. merriami populations. The ex- tent of gene flow within populations is uncer- tain, though. Turnover rates are quite high in D. merriami (80-90 percent annually; Jones, 1982), which would tend to increase gene flow. Furthermore, we do not know the ex- tent of long-distance dispersal (greater than 20 home range diameters), nor do we under- stand what role, if any, is played by excur- sions to areas outside the usual home range. Do individuals making these excursions find mates in areas several home range diameters from their own home range, or are they more successful at finding mates among their im- mediate neighbors, with whom they are pos- sibly more familiar? Genetic studies in which marker alleles are introduced in natural pop- ulations (cf. Anderson et al. 1964, Baker 1981) would help answer these questions and would aid in determining the rate of gene flow within and among subpopulations. Other questions concern the effects of age and breeding stnicture on population genetic structure. We suggested above how differ- ences in age structure, longevity, and survi- vorship schedules might lead to more or less variance in lifetime reproductive success of adults. In species like D. spectabilis, where a few individuals live through several breeding seasons but most individuals have much shorter lifespans, a core of long-lived individ- uals may make a disproportionately large contribution to later generations. It would be useful to know what proportion of the breed- ing adults in later generations are actually descendants of these long-lived individuals. And how does reproductive success vary with age? Are older males more successful at com- peting for mates? This would further increase variance in male reproductive success in situ- ations where only a small proportion of males live into their second or third breeding sea- son. These questions are probably best pur- sued in long-term mark-recapture studies of natural populations combined with direct genetic determination of maternity and paternity. Population structure in desert rodents may also be related to fluctuations in density; such periodic decreases in population size are known to occur (Beatley 1969, French et al. 1974, Whitford 1976, Petryszyn 1982). These decreases may cause genetic bottlenecks, re- ducing the amount of genetic diversity with- in subpopulations. To what extent do these decreases in density affect effective popu- lation size? Furthermore, the rate of dispersal between subpopulations may vary with den- sity. Higher interdemic dispersal rates at peak densities might partially or completely offset the reductions in variability that possi- bly result from population crashes. Determin- ing the importance of density fluctuations and interdemic dispersal for population ge- netic structure would require monitoring ge- netic makeup over large areas and over a time long enough to cover at least one, and preferably more, cycle(s) of population de- cline and increase. 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Brown' Abstract.— As is true of many assemblages of ecologically similar organisms, coexisting heteromyid rodent species differ conspicuously in morphology and in microhabitat affinity. These patterns are so common that their explana- tion represents a central problem of community ecology. In the case of desert rodents, two very different factors, predation and competition, have been advanced as the ultimate cause of the patterns. We outline the wav in which each of these factors could produce observed community-level patterns and review the evidence for the action of each factor. We conclude that the "competition" hypothesis has more support at the moment, but that this is partly a result of the general lack of good experimental studies of predation in terrestrial vertebrate systems. We outline a general protocol for distinguishing the effects of predation and competition through carefid examination of relation- ships between morphology, foraging and predator-avoidance abilities, and behavior. We think such "micro- ecological" analysis of the consequences of morphology holds much promise for improving our understanding of community-level patterns of morphology and resource use. Among the basic concerns of community ecology is identification of factors that deter- mine the number, relative abundances, and phenotypic attributes of coexisting species. Rodents of North American deserts were im- portant in the development of this major sub- discipline of ecology, mostly through the work of several influential naturalists— among them Joseph Grinnell and C. Hart Merriam— who developed their ideas about limits to an- imal distributions in large part from observ- ing small mammals in the western United States. Their ideas have subsequently been incorporated into a sophisticated body of mathematical theory, the recent devel- opment of which was stimulated primarily by G. Evelyn Hutchinson and Robert H. Mac- Arthur (see MacArthur 1972, Hutchinson 1978). Desert rodents in general still figure heavily in commimity ecology, being widely used for testing general theories of commu- nity organization under field conditions. They are especially suitable for such studies because they are small, abundant, diverse, and easily captured in the field and observed in the laboratory, and because unrelated groups have independently colonized geo- graphically isolated arid regions. Our aim here is not to review exhaustively what is known about desert rodent commu- nities, since several other authors have made recent contributions of this sort (Brown 1975, Rosenzweig et al. 1975, Brown et al. 1979). Instead, we will provide an updated over- view of the general characteristics of these communities, discuss the alternative hypoth- eses that have been advanced to explain those characteristics, and outline the evidence that bears on the alternatives. Finally, we will suggest directions for further research. We will focus on the specialized seed-eaters of North American deserts because much less is known about other desert rodents, but we will attempt to indicate when observations from other dietary guilds or geographic re- gions fit the patterns we describe. General Patterns Natural History The rodent fauna of North American deserts is dominated by members of the Het- eromyidae, a New World family whose re- markable similarity to unrelated Old World and Australian desert forms is a textbook ex- ample of convergent evolution. Like jerboas, 'From the symposium "Biology of Desert Rodents," presented at the annual meeting of the American Society of Mammalogists, hosted by Brigham Young University, 20-24 June 1982, at Snowbird, Utah. 'Department of Biology, University of California, Riverside, California 92521. 'Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85721. 117 18 Great Basin Naturalist Memoirs No. 7 gerbils, and hopping mice, most heteromyids are primarily granivorous and can subsist without a source of free water. They are also nocturnal, live in burrows, and inchide both bipedal hopping {Dipodomys, Microdipodops) and quadrupedal bounding forms {Perog- nathus). A more complete analysis of mor- phological, behavioral, and ecological sim- ilarities among unrelated desert rodents can be found in Eisenberg (1975), Brown et al. (1979), and Mares (this volume). Some of the convergent features of these groups, such as xerophytic physiology and burrowing habit, are clearly responses to the extreme temperatures and low rainfall that characterize deserts. Others, such as gra- nivory, are probably indirect consequences of plant responses to frequent and unpredic- table droughts. Many desert plants have adopted an "ephemeral" life history, in which they survive unfavorable periods as seeds or (less often) as underground storage organs (Noy-Meir 1973, Solbrig and Orians 1977); and the resulting pool of dormant seeds in the soil provides a relatively abun- dant and persistent food source for a variety of birds, rodents, and ants (Noy-Meir 1974, Brown et al. 1979). The significance of still other features of desert rodents, such as prev- alence of bipedal locomotion, remains a mat- ter of debate, but these features probably re- flect constraints on predator avoidance or foraging strategies imposed by tlie physical structure of desert vegetation and soils (see Bartholomew and Caswell 1951, Brown et al. 1979, Thompson et al. 1980, Reichman 1981, Thompson 1982a,b). Proximate Factors Affecting Abundance and Diversity There is considerable evidence that indi- vidual reproductive success and population densities of rodents in North American deserts are limited by seed production of ephemeral plants, whose germination and growth is directly tied to the amount of pre- cipitation falling during certain seasons (Noy- Meir 1973). Reproductive rates of individual rodents, as well as population densities, show extensive temporal and geographical fluctua- tions that are closely correlated with varia- tion in precipitation (Brown 1973, 1975, French et al. 1974, Brown et al. 1979, M'Closkey 1980, Petryszyn 1982, Munger et al., this volume). Casual observation of cli- matic correlates of rodent "plagues" in other regions suggests that this is probably true in all deserts (see references in Prakash and Ghosh 1975). Species diversity seems to be influenced by several factors, the most obvious of which is habitat complexity (Rosenzweig and Winakur 1969, M'Closkey 1978). Positive correlations between diversity and habitat complexity are common in animal communities (MacArthur 1972, Schoener 1974, Hutchinson 1978), and occur because coexisting species usually differ in affinities for areas of particular topo- graphic or vegetation structure. If it is suffi- ciently productive, an area that is struc- turally complex can be inhabited by several species, each of which specializes on a differ- ent microhabitat. Interspecific differences in microhabitat affinity appear to be character- istic of all desert rodent communities that have been examined (cf. references in Pra- kash and Ghosh 1975). Among heteromyids, the bipedal kangaroo rats and kangaroo mice are associated with sparse perennial vegeta- tion and tend to forage in open micro- habitats, whereas the quadrupedal pocket mice are associated with dense perennial veg- etation or rocky areas and prefer micro- habitats under tree or shrub canopies (Ro- senzweig and Winakur 1969, Rosenzweig 1973, Brown and Lieberman 1973, Brown 1975, Price 1978b, Harris unpublished. Price and Waser 1983). This pattern also appears to occur in African deserts where bipedal jer- boas are associated with open areas more than are quadrupedal gerbils (e.g., Happold 1975). Several experimental studies indicate that vegetation structure influences not just the number of species in North American com- munities, but also the identities and relative abundances of those species. Rosenzweig (1973) altered a number of small plots by clearing shrubs from some and augmenting brush on others. These manipulations resulted in significant local shifts in species composi- tion: Perognathus pcniciUatus increased in density on augmented plots and decreased on cleared plots, but Dipodomys merriami re- sponded in the opposite way. Similarly, Price 1983 Biology of Desert Rodents 119 (1978b) removed half of the small shrubs from 25 sites within a 3.2 ha area and found predictable increases in the density of D. merriami, the species that showed the most pronounced preference for foraging in open spaces. Furthermore, the magnitude of local changes in density of this species was corre- lated with the amount of shnib cover re- moved. After adding cardboard "shelters" be- tween shrubs to experimental plots, Thompson (1982b) observed increased abun- dance of species normally associated with shrubs and decreased abimdance of kangaroo rats. "Natural" temporal or spatial changes in vegetation appear to result in similar shifts in rodent species composition that can be pre- dicted from knowledge of microhabitat pref- erences (Rosenzweig and Winakur 1969, Beatley 1976, Hafner 1977, Price 1978b, Price and Waser 1983). Among habitats that are similar in struc- ture, the number of rodent species increases with the amount and predictability of annual precipitation, which determines seed produc- tion as well as shrub density (Brown 1973, 1975, Hafner 1977, Brown et al. 1979). The most arid parts of the Colorado and Mojave deserts typically have only one or two species of heteromyids, whereas structurally similar but more productive areas in the Sonoran, Chihuahuan, and Great Basin deserts some- times support as many as four or five species. As might be expected, average population densities and total rodent biomass also tend to be positively correlated with increased seed abundance, but it is less clear why spe- cies diversity should exhibit such a pattern. MacArthur (1969, 1972) showed that this cor- relation is expected of commimities com- posed of species limited by a single resource. In such resource-limited systems, species that specialize on a subset of available resources can persist only when overall production is high enough to supply some minimal amount of the preferred subset during poor years. In unproductive regions, abimdance of the ap- propriate resources may often fall below the threshold level, causing the consumer popu- lations that depend on them to go extinct lo- cally. Brown (1973) has proposed this expla- nation for geographic diversity-productivity correlations in heteromyid communities. A similar explanation would also account for seasonal variations in species occupying giv- en habitats (cf. Congdon 1974, Meserve 1974) and for species turnover between local habi- tats that differ in structure. There is not as yet sufficient evidence to evaluate rigorously these productivity-based explanations of spe- cies diversity, although they are consistent with results of one experimental study: arti- ficial augmentation of seeds in a short-grass prairie enhanced local species diversity by in- ducing invasion of a specialized granivore, Dipodorny.s ordii (Abramsky 1978). Brown (1973, 1975) has pointed out that historical factors, in addition to productivity and habitat structure, can influence the num- ber of species in heteromyid communities. He found that geographically isolated sand dunes were inhabited by fewer species than would be expected on the basis of their pro- ductivity, and attributed this to decreased colonization rates of isolated "islands" of suitable habitat. Historical constraints have also been invoked to account for the low di- versity of rodents in South American and Australian deserts (Brown et al. 1979). Morphological Configuration of Rodent Commimities In addition to pronounced divergence in microhabitat affinities, a salient feature of heteromyid communities is that coexisting species differ in body size more than would be expected if communities were random as- semblages of species (Fig. 1; Brown 1973, 1975, Brown et al. 1979, Bowers and Brown 1982). Such body size divergence is by no means unique to desert rodent communities; in fact, it is so ubiquitous that nearly constant size ratios among coexisting species have been given the name "Hutchinson's ratios," after the ecologist who drew attention to them (Hutchinson 1959, Horn and May 1977, Lack 1971, MacArthur 1972). Heteromyid communities are, however, one of the few cases for which observed size spacing has been shown to be statistically different from random null models (cf. Strong et al. 1979, Bowers and Brown 1982, Petersen 1982, Sim- berloff and Boecklen 1981). It is interesting to note that desert cricetids do not show size patterns typical of heteromyids, and that in- cluding the omnivorous and carnivorous 120 Great Basin Naturalist Memoirs No. 7 GREAT BASIN DESERT - FISHLAKE VALLEY PI Mp Dm Dd GREAT BASIN DESERT - MONO LAKE Mm Ppa Do Dp MOJAVE DESERT - KELSO PI Dm SONORAN DESERT - SANTA RITA RANGE Pa Pp Pb Dm Ds SONORAN DESERT - RODEO Pf Pp Dm BODY SIZE (g) Fig. 1. Typical heteromyid rodent assemblages from three major North American deserts. The average body sizes of common species found at five sites are indicated by their position on the horizontal axis. ¥\ = Perognathus longimembris; Pf=P. flavus; Pa = P. ainphts; Pp = F. penicillatus; Ppa = F. parvus; Ph = P. baileiji; Mm = Microdipodops megacephalus; Mp = M. pallidus; Dm = Dipodomys merriami; Do = D. ordii; Dp = D. pan- amintinus; Dd = D. deserti; Ds = D. spectabilis. Note that congeners of similar body size are not common at the same site. Data taken from Brown (1973) and Price (unpublished). 100. •>•• 90. 963X-ei C7> r2. 60 z «° P < 001 (D 70. > • Q O m 60. \ Q \ >- • \ 5 50. • • O • • LlI • \ 1- 40. X .•• • \ • UJ 30. ID • < tr - 20. < 10. 50 100 150 200 250 300 350 AVERAGE ANNUAL PRECIPITATION (mm) Fig. 2. Average body size of heteromyids resident on sand dunes that differ in annual precipitation, un- weighted by relative species abundances. As species number decreases with decreasing precipitation, the smaller species drop out first. This causes a significant increase in average body size as productivity declines, until only the largest kangaroo rats remain on the most arid dunes. Data are from Brown (1973); the power fit shown on the figure is significant (Fj jg = 24.43; P < .001). cricetids along with the heteromyids in a morphological analysis obscured patterns present within the granivore guild (Bowers and Brown 1982, Petersen 1982). There have been no studies of morphological structure similar to these for desert rodent systems in continents other than North America. This is imfortunate, because there are intriguing sug- gestions of .size differences among coexisting gerbils in North Africa (Happold 1975:36) and among dipodids in the USSR (Naumov and Lobachev 1975:491). Coexisting heteromyids differ in parame- ters of body shape related to locomotory gait as well as in size. Relative to quadmpedal forms, bipeds have elongated hind feet and tails, shortened vertebral columns, and re- duced fore feet (Hatt 1932, Howell 1932). There is some association between .shape and size; in general, bipedal forms are larger (12-150 g) than quadrupedal forms (7-40 g). In addition to these within-community morphological patterns, there are striking geographical trends in body size for sand dune habitats. Figure 2 indicates that as spe- cies diversity declines along a gradient of de- creasing precipitation, average size of hetero- myids inhabiting sand dunes increases. This is not due to geographic variation in size within individual species, although such variation has been reported (Kennedy and Schnell 1978). Instead .smaller species drop out first along the gradient, until only the largest spe- cies remain in the least productive regions. It remains to be seen whether similar patterns exi.st for other habitats. Proposed Explanations for the Patterns The Hypotheses Two hypotheses have been advanced to ac- count for the conspicuous interspecific diver- 1983 Biology of Desert Rodents 121 gence in body size, shape, and microhabitat affinity that characterizes heteromyid rodent communities. The first proposes that these features reflect divergent predator avoidance strategies that have evolved because there can be no single "best" escape strategy in heterogeneous environments (cf. Rosenzweig 1973, Thompson 1982a,b, Webster and Web- ster 1980). An escape behavior that works well away from cover, for example, may be ineffective in dense brush either because shrubs impose physical constraints on move- ment or contain different types of predators. It is not difficult to imagine that morphology determines how easily an animal can be de- tected and w