Adaptive Physiology of Heteromyid Rodents

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Great Basin Naturalist Memoirs

Volume 7 Biology of Desert Rodents Article 5

8-1-1983

Adaptive physiology of heteromyid rodents

Richard E. MacMillen Department of Ecology and Evolutionary Biology, University of California, Irvine, California 92717

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Recommended Citation MacMillen, Richard E. (1983) "Adaptive physiology of heteromyid rodents," Great Basin Naturalist Memoirs: Vol. 7 , Article 5. Available at: https://scholarsarchive.byu.edu/gbnm/vol7/iss1/5

This Article is brought to you for free and open access by the Western North American Naturalist Publications at BYU ScholarsArchive. It has been accepted for inclusion in Great Basin Naturalist Memoirs by an authorized editor of BYU ScholarsArchive. For more information, please contact [email protected], [email protected]. 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 aridity, with larger quadrupedal taxa being more mesic (and primitive), and smaller quadrupeds and all bipeds more xeric. 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 advantages as revealed in treadmill studies. Large quadmpedal heteromyids have adaptive physiologies suitable for more mesic habitats, but smaller quadrupeds 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- ized, and the bipedal members {Dipodomys, eromyidae are distributed along a pro- Microdipodops) are the more specialized. In nounced gradient of water availability in the addition, the quadrupedal members span the New World ranging from the wet tropics of entire distributional range and nearly the en- Central and South America to the driest tire size range of the family, but the bipedal deserts of North America (Hall 1981). This forms are confined to semiarid and arid habi- present-day distribution mimics the paleo- tats, and (with the exception of the small-in- climatological history of the family, starting size Microdipodops) occupy the upper por- with a tropical ancestry, followed by an tion of the size spectrum (Hall 1981). By in- in adaptive radiation throughout the Tertiary spection (Hall 1981), there is a strong posi- response to progressive aridity and sea- tive correlation within the quadrupedal sonality of rainfall, and culminating in the di- heteromyids between body size and moistness verse favma of desert heteromyids with which of the habitat, suggesting that reductions in we are so familiar (Axelrod 1958, Hall 1981, body mass may confer a selective advantage Reeder 1956, Wood 1935). With this in mind, upon quadrupedal heteromyids living in it is my contention that tropical heteromyids more arid habitats; on the other hand, the may be viewed at least ecologically as ances- arid-adapted bipeds are commonly relatively tral models of early heteromyids, the desert large and show no apparent relationship be- forms as advanced derivatives, and those oc- tween the body mass of individual species cupying intermediate habitats as transitional and habitat aridity, suggesting a linkage be- fonns. Thus, extant species should provide us bipedality and aridity independent of with important clues concerning the evolu- tween tionary and ecological trajectories of the fam- body mass. certain aspects of water ily at the levels of physiology, morphology, Herein, I explore hetero- and behavior. and energy regulatory physiology of The quadrupedal heteromyid genera (Het- myid rodents, paying particular attention to eromijs, Liomys, Perognathits), at least with patterns related to habitat, body mass, respect to locomotion, are the more general- and/or locomotor mode.

hosted Brigham Young 'From the symposium "Biology of Desert Rodents," presented at the annual meeting of the A Society of Mammalogists, by University, 20-24 June 1982, at Snowbird, Utah.

^Department of Ecology and Evolutionary Biology, University of California, I California 92717.

65 66 Great Basin Naturalist Memoirs No. 7

species, body mass might be positively correlated with moistness of the habitat and nega- HETEROMYIDAE tively correlated with economical water regulation, MacMillen and Hinds (1983) un- dertook an examination of water regulatory efficiency in extant heteromyids that includ- Di Dodom vs ed both quadrupedal and bipedal members across the entire taxonomic, distributional,

MASS (g) and size ranges of the family. This examination was based on a model that predicted Fig. 1. The double logarithmic relationships between water regulatory efficiency (T^ (a MWP = EWL) and that water regulatory efficiency is negatively body mass in 5 genera and 13 species of heteromyid ro- related to body mass and positively related to dents. Regression lines are provided for all species (solid ambient temperature. Our criterion of water line) and Perognathus spp. (dot-dash line), and both have regulatory efficiency is that ambient temper- significant slopes (F test, P < .05). The horizontal line (dashed) represents the average value for all Dipodomtjs, ature (Ta) at which the major avenue of water which did not have a significant regression. The regres- input (metabolic water production, MWP) lines fit all values for species; the sion are to the each just balances the major avenue of water out- regression equations are T^ (S (MWP = EWL) = 29.682g-<^l3''' put (evaporative water loss, EWL). Thus, the in all 13 heteromyid species, and \ (a (MWP = EWL) = 31.078g-"^'^ in Perognathm spp.; model predicts that those species achieving the mean value for Dipodomys spp. is 18.1 ± SD 0.6 C. water balance (MWP = EWL) at the highest The heteromvid species employed span the geographic, TaS are the most efficient in water regulation, climatological, and body mass ranges of the family and being able to subsist exclusively on air-dry include Dipodomys deserti, D. merriami, D. ordii, D. seeds to meet both energy and water needs panamintinus, Heteromys desmarestianus, Liomys irro- ratus, L. salvini, Micwdipodops megacephalus, Per- while active on the surface even under warm ognathus baileyi, P. fallax, P. flatus, P. hispidus, and P. conditions. A test of the model in which we kmgimembris. After MacMillen and Hinds (in press). evaluated simultaneously MWP and EWL from Ta = 5-35 C in 117 individuals, 13 spe- Water Regulatory Efficiency cies and 5 genera of heteromyids, confirms our predictions for the family in general (Fig. Numerous accounts in the literature attest 1). However, when the two most speciose to the relatively great powers of water con- genera (Perognathus, Dipodomys) are treated servation in heteromyid rodents, and indicate separately, Perognathus spp. conform even that the arid-adapted forms (Dipodomys, Mi- more strongly (possess a steeper slope) to the cwdipodops, Perognathus) are conservative model, but in Dipodomys spp. water regu- often to the point of exogenous water inde- latory efficiency is fixed at an intermediate pendence (MacMillen 1972, Schmidt-Nielsen level independent of body mass (Fig. 1). This et al. 1948; pers. obs.), and the more mesic intergeneric break in patterns of water regu- adapted forms (Heteromys, Liomys) are less latory efficiency coincides with a break in conservative in their water economies and re- body mass (ca 35g) and a break in locomotor quire dietary augmentation of exogenous wa- mode, points whose relevances will be dis- ter (Hudson and Rummel 1966, Fleming cussed later in this paper. 1977). I (MacMillen 1983) have argued that the conservative nature of heteromyid water economy, regardless is of habitat, likely Basal Metabolic Rate linked to the family's dietary specialism, granivory: this is became rodents in particu- It has long been known that the basal lar depend upon a common resource packet metabolic rates (BMR) of mannnals are loga- to meet nutrient, energy, and water needs, rithmically correlated with bodv mass (Klei- and those that u.se the driest packets (seeds) ber 1932). This scaling of BMR with body are the most conservative in their water mass in mammals was statistically refined by economies. Brody (1945) and Kleiber (1961) to provide With the supposition that heteromyids are indistinguishable regression equations for relatively conservative in their water econo- predicting BMR for mammals of any known mies, and that, at least for the quadrupedal 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 ::_-.f^ ^BRODY have BMR reduced below the expected lev- ^^XKLEIBER els. Hudson and Rummel (1966) confirmed this suggestion for the subtropical species

Liomys salvani ( = L. salvini?) and L. irro- .Jj. 10 50 100 ratiis; more recently McNab (1979) has MASS (g) through a search of the literature shown and • Perognafhus BDipodomys •Heteromys his own measurements that, of the hetero- AMicrodipodops Liomys myid species for which measurements were available (12 species, all 5 genera), only a Fig. 2. The double logarithmic relationship between tropical Heteromys {H. anomalus) possessed a mass-specific basal metabolic rate and body mass in heteromyid rodents, using the same species as indicated in BMR at or exceeding the Kleiber prediction- Figure 1. The dashed line is the allometric expectation all others were reduced. Furthermore, for eutherian mammals from Brody (1945); the dot-dash McNab's (1979) analysis revealed the BMRs line is the expectation for eutherians from Kleiber of Perognathiis spp. were not only reduced, (1961). The solid line is fit to the data for heteromyids by the regression equation BMR = 3.69 W(g)-0-28 (Sy, = but also were independent of body mass; it is .010, Sb = .028, r2 = 0.504). The geometric symbols interesting to note that the four Perognathiis represent different genera as indicated on the figure. measurements were from four different The BMR values employed in this analysis are the two laboratories. lowest measures of Vq, for each individual at that T^ in thermal neutrality for which the mean Vo, of that spe- Our studies of water-regulatory efficiency cies was lowest (after Hinds and MacMillen, in prepara- as described above and in MacMillen and tion; data collection as in MacMillen and Hinds, in Hinds (1983) provide a rich data base from a press). single laboratory for comparing mass-related

aspects of water and energy metabolism both heteromyids we tested is depressed below the within the family Heteromyidae, and with values predicted by either the Brody (1945) eutherian mammals in general. We are pre- or Kleiber (1961) relationships (Fig. 2). paring a major synthesis of heteromyid meta- Correcting for SDA would yield even bolic allometry (Hinds and MacMillen, in greater depressions. The slope of the regres- preparation), and so the following summarize sion line relating BMR to mass of hetero- only briefly the most pertinent information myids (-0.28) is statistically indistinguishable related to BMR. from that of Brody (-0.27) and Kleiber Because our criterion of water regulatory (-0.25). Using the raw data of Brody (1945), a efficiency required that our animals be oxi- direct comparison can be made of elevation dizing food of known composition at the time between his and the heteromyid data sets, of measurement of oxygen consumption which shows that, at the mean body mass (ca (V02), our animals were not postabsorptive 30g) of the heteromyids employed, hetero- when measured in thermal neutrality, and myid BMR is significantly (P < .05) reduced hence did not conform strictly to the require- by 1 1 percent of that predicted for eutherian ments for BMR. The animals were oxidizing mammals in general (following method of millet (81.4 percent carbohydrate, 5.1 per- comparing elevations by Snedecor 1956 and cent lipid, 13.5 percent protein), which Zar 1974). Of the 13 heteromyid species in- should elevate metabolic rate due to the spe- cluded in Figure 2, 5 {Dipodomys deserti, D. cific dynamic action (SDA) of food utilization merriami, Perognathiis haileyi, P. fallax, P. by about 9 percent above basal levels (Brody longimembris) are from severe desert scrub 1945). In spite of the possible influence of habitats, and their BMR collectively is re-

SDA on metabolic rate of our specimens, it is duced by 24 percent below that predicted for apparent that the basal metabolic rate of the eutherians. Great Basin Naturalist Memoirs No. 7

Lastly, the 5 Perognathus spp. conform body mass (Taylor et al. 1970). The first sug- strongly to the relationship between BMR gestion that bipedal hopping might confer and body mass, with no indication of the unusual energetic benefits was by Dawson mass-independent relationship reported by and Taylor (1973), who reported that red McNab (1979) on data emanating from sever- kangaroos, while hopping, effectively had al laboratories. Since two of the four Pe- energetic costs that were independent of run- rognathus species included in McNab's (1979) ning speed, i.e., a bipedal plateau. Shortly analysis were also employed in ours {P. long- thereafter Fedak et al. (1974) reported data imemhris, P. hispidiis) the discrepancy is suggesting that for small animals (< lOOOg) likely due to interlaboratory differences in the cost of transport for bipeds (exclusively to interspecific measuring BMR rather than birds) is less than that for quadrupeds (ex- deviations in metabolism. This attests to the clusively mammals). This contention was re- of using only data collected from importance versed by Fedak and Seeherman (1979) and a single laboratory when undertaking meta- Paladino and King (1979), who demonstrated bolic comparisons at lower taxonomic levels. independently, using a more extensive data Thus, it is concluded tliat heteromyid ro- set including quadnipedal mammals and liz- dents have reduced BMR (and metabolic ards and bipedal birds and mammals, that rates in general) and that the reductions are there is no difference in the scaling of energy not only recognizable at the taxonomic level, requirements for locomotion between bipeds but are most pronounced in those members and quadrupeds, but only differences be- living imder more arid conditions. tween clumsy and graceful runners. But these latter studies, as opposed to Dawson and Bipedal Locomotion Taylor's (1973) with the kangaroo, employed animals that were either two-legged bipeds The fact that heteromyids are divided in (primates and birds) or four-legged quad- locomotor habits into quadrupedal and bi- rupeds (other mammals and lizards), and not pedal forms, and that the latter are confined mammals that at slower running speeds are to semiarid and arid habitats within the fam- pentapedal (kangaroos) or quadnipedal (for ily distribution, suggests the presence of ad- example, heteromyids), but then become bi- vantages inherent in bipedalism tliat favor an pedal at faster speeds. arid existence. Howell (1933) observed that Dawson (1976) and Baudinette et al. (1976) Dipoclornys occurred predominantly in open measured the energetic costs of locomotion terrain, where bipedality conferred a com- in two species of Australian murid hopping bination of fast, erratic movements and bal- mice {Notomys cervinus and N. alexis, respec- ance that enhanced predator escape to the tively) that are ecological and physiological extent "that no mammal can catch this ro- equivalents to bipedal heteromyids (MacMil- dent in fair chase, but only in stealth." Also len and Lee 1969, 1970). Both species had favoring the hypothesis that bipedality in similar patterns relating oxygen consumption Dipodornys aids primarily in predator escape (Vq^) to running speed with a positive linear and avoidance were Bartholomew and Cas- relationship at slower speeds (< 2.0 km/h) well (1951), who stated "the entire economy and a plateau at higher speeds (> 2.0 km/h). of the animal is set up for efficient evasion of Dawson (1976) reports intermittent use of danger in areas relatively devoid of cover, both quadrupedal running and bipedal hop- which emphasizes that survival in this species ping at plateau speeds, but Baudinette et al. has been dependent upon a series of mutually (1976) report only quadrupedal running. In supporting adaptations of which its locomo- addition, Dawson (1976) suggests that the tor equipment is the most obvious." plateau in N. cervinus is aerobic and there- Recently, investigators have measured the fore represents a real energetic savings re- actual costs of locomotion through indirect lated to elastic energy storage compared to calorimetry of mammals nmning on tread- that during strictly quadrupedal running. mills. These studies have concentrated on Baudinette et al. (1976) are less committal quadrupedal ninning and show considerable and imply that the plateau may be either an uniformity in the scaling of energetic costs to aerobic one dependent upon elastic storage. 1983 Biology of Desert Rodents 69

or it may be purely anaerobic, occurring at of aerobic capacity. the level maximal Clear- -J»VC02 ly this plateau can represent an energy- V02 conserving mechanism only if aerobic. My recent treadmill studies of the meta- 14 4 1^ 6. 6 -># 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- 3 2 cies of small bipeds (0.03 to 3.0 kg; Rodents: a QoaoOooRQ

Heteromyidae: Dipodotnys merriami, D. J i 1 I I deserti; Pedetidae: Pedetes capensis; Marsu- pialia: Macropodidae: Bettongia penicillata) show no aerobic bipedal plateau while hopping 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). 2 3 4 5 6 To confirm further the presence or absence VELOCITY (km/h) of in spp., si- a bipedal plateau Dipodomys Fig. 3. A. The relation between oxygen consumption multaneous measurements of Vog and Vco2 (Vq,) and carbon dioxide production (V^o,) and velocity were made in D. ordii while running on a in Dipodomys ordii running on a treadmill at Tg = 20 C. The treadmill was enclosed in a Plexiglas chamber treadmill, and of blood lactate immediately through which air was pulled at a rate of 4.1 L/min. after results are reported in Rmning. The Vq, and Vcoo were measured with an Applied Electro- Figure 3. At low running speeds (<3.0 km/h) chemistry S-3A oxygen analyzer and an Infrared In- dustries All measurements V02' Vcog^ and blood lactate are positively carbon dioxide analyzer. were corrected to STPD. The dashed line is fit to the and linearly related to speed. At higher run- Vq data between 1 and 3 km/h by linear regression ning speeds 3.0 km/h) Vq^ plateaus dis- (> analysis and is described by the equation cm-^/g'h = tinctly, Vcog continues to increase linearly 0.91(km/h) + 4.46 (Sy, = 6.58, Sb = 0.60, i^ = 0.64); but with a shallower slope, and blood lactate the line has a significant positive slope (F test, P < .05). The solid line is fit to the '^^^'^ between 1 and 3 continues to increase sharply, but with the Vco, km/h, and between 3 and 6 km/h. Both have significant possibility of a plateau at 4.0 and 5.0 km/h. slopes, and are described by the equations cni''/g*h = At 4.0 there is Ruining speeds above km/h 1.65(km/h) -I- 2.88 (Sy, = 0.67, Sb = 0.43, i^ = 0.81) = a distinct decline in the willingness of indi- and cm3/g-h = 0.36(km/h) -I- 6.83 (S^, = 0.58, Sb

r^ = numbers represent the number of viduals to Rm, with typically less than one- 0.89, 0.21). The measurements obtained at each speed from a total of 13 half of the individuals that readily ran at individuals. Solid circles represent mean V^Og measure- lower speeds willing to run at the higher ments, hollow circles represent mean Vq, measure- speeds sufficiently long (2-3 min) to reach ments, vertical lines represent the interval A ± 1 SD, values steady state. It is unlikely that this unwilling- and hollow squares represent mean RQ ness to run at higher speeds for even short (Vc02/V02). B. The relation between blood lactate and velocity m periods of time was due to hyperthermia. As D. ordii running on a treadmill at Ta = 20 C. Each ani- Wunder (1974) has noted, no inhibition of mal was allowed to mn at one speed for 2-5 min during running in D. ordii accompanied moderate 'CO2 and these measurement.s are depicted in Fig. 3A. It was then im- hyperthermia while Rmning at lower speeds included in the data mediately removed, a blood sample was taken from the (<1.8 km/h), but did for prolonged periods orbital sinus within 30 sec of removal, and the whole of time (10-15 min). The transition from blood placed in perchlorate solution. Lactate concentra- quadrupedal to bipedal running occurs be- tion was determined using a Boehringer-Mannheim lac- tween 3.0 and 4.0 km/h, with most of the Vq^ tate test kit. Each hollow triangle represents one value with a total of ten values (in- plateau coincident with bipedal locomotion. from a different individual, dividuals). The solid line is fit to the data by regression I am convinced, however, that the Vq^ analysis and is described by the equation mg% = 46.234 plateau depicted in Figure 3 is anaerobic, (km/h) - 13.638 (i^ = 0.825); the slope is significant (F and therefore cannot be construed as an test, P < .05). .

70 Great Basin Naturalist Memoirs No. 7 energy-conserving mechanism. The mean Vq^ the use of force plates and X-ray cine- between 3.0 and 6.0 km/h (7.34 ± SD 0.57 matography bipedal hopping in Dipodomys cmVg.h; N = 52) falls within the 95 percent spectabilis and conclude that elastic storage confidence intervals predicted for maximal of energy in this kangaroo rat is much less aerobic capacity (Vq^ max) in a small mam- than in kangaroos. mal (X body mass = 52.7 g) from Lechner's The adaptive significance of bipedality in (1978) allometric relationship: heteromyids has yet to be demonstrated with rigorous laboratory and field tests. The most V02 max = 0.499 W 678 plausible current explanation is the original one proposed by Howell (1933) and Bartholo- (V02 is in cmVmin, and W is mass in g). mew and Caswell (1951) that bipedality aids

The mean V02 for D. ordii between 3.0 and in predator avoidance and escape. I believe it falls 6.0 km/h, however, below the 95 per- is additionally possible that bipedality con- cent confidence intervals for S/q^ max as prefers other locomotor advantages not readily dicted by Taylor et al. (1980): translatable into energetic currency, such as enhancing acceleration and burst speeds. Vo^max = 1.92W.809 These ideas have yet to be tested. (V02 is in cmVsec, and W is mass in kg). Use of Torpor Lechner's (1978) relationship included Vo^ max induced by cold, helium-oxygen mixtures Torpor (or natural hypothermia), in which or running, in 14 small mammals species (< body temperature and energy metabolism are 2.6 kg), 11 of which were rodents. Taylor et reduced well below normothermic levels, ei- al. (1980) confined their measurements to ther on a circadian basis or for longer peri- treadinill running, with the majority of their ods, is well documented in virtually all heter- mammals large (> 2.6 kg) or very large; of omyids whose mean body masses are the 21 species for which measurements are typically less than 40 g (i.e., all Perognathiis reported, only 4 are rodents while 11 are un- spp., Microdipodops paUidus, and M. mega- gulates. It is difficult to resolve the dis- cephahis, pers. obs., Bartholomew and Cade crepancies between these two relationships, 1957, Bartholomew and MacMillen 1961, as their data bases differ taxonomically, Cade 1964, Tucker 1965, Wang and Hudson methodologically, and by body mass. Our 1970, Wolff and Bateman 1978). In larger protocol is most similar to that of Lechner quadrupedal heteromyids (i.e., Heteromys, (1978) in terms of taxonomy and body mass, Liomys) torpor has not been observed (pers. and resembles that of Taylor et al. (1980) obs., Fleming 1977, Hudson and Rummel methodologically 1966). Torpor appears to be a weakly devel- Additional confirmation that the Vq^ oped capacity in Dipodomys, having been plateau reported above for D. ordii is an- documented in D. merriami (Dawson 1955, aerobic comes from the analysis of blood lac- Carpenter 1966, Yousef and Dill 1971), D. tate following nmning at the highest speeds panamintinus (Dawson 1955) and observed tested. The mean of four values for D. ordii in D. deserti (pers. obs.). In all instances tor- after ninning 2-3 min at 4.0 and 5.0 km/h is por in Dipodomys spp. was induced by star- 201.9 ± SD 34.8 mg percent. This mean, and vation and/ or cold stress, and frequently re- three of the four values fall within the 95 sulted in death during torpor or after arousal. percent confidence intervals around the In the few Dipodomys spp. in which torpor mean (190.7 ± SD 9.1 mg percent) of blood has been documented it appears to be best lactate levels of 9 mammalian species nm- (but still weakly) developed, as a circadian ning on treadmills at Vo^ max, as reported by phenomenon, in the smallest species, D. mer-

Seeherman et al. 1981. The fourth value lies riami (> 35 g). I have seen no convincing above the confidence intervals. Thus, it is ap- evidence that torpor in Dipodomys spp. is an parent from the perspectives of Vq^ and ecologically meaningful phenomenon. blood lactate levels that the bipedal plateau Among Perognathiis spp., there appear to we observed in D. ordii is anaerobic. Finally, be two prevailing patterns in the use of tor-

Biewener et al. (1981) have examined with por: (1) those that emplov it as an emergency 1983 Biology of Desert Rodents 71 energy-conserving mechanism for short peri- bouts is related to ambient temperature and ods of time (one to several days) to avoid food supply in such a way that individuals in- temporarily inhospitable surface conditions variably maintain body weight and accumu- {P. californicus. Tucker 1962; P. flavtis, late seeds, even at very low temperatures and Wolff and Batemann 1978); and (2) those that on seed rations reduced considerably below are or nearly are obligate hibernators, and the normothermic requirement. An addition- abandon surface activity for several months al example of precision of energetic control each winter (P. longimembris, Kenagy 1973; while using torpor is seen in Perognathus par-

P. parvus, Meehan 1976). The determinants vus (Meehan 1976). This species is an obli- of one pattern or the other are unknown, but gate hibernator, and in Great Basin habitats they are not taxonomic because both patterns in California is dormant in burrows typically occur in each subgenus. In Microdipodops from November through March, employing spp., torpor appears to be employed on a periodic bouts of torpor that may last as long short-term basis, as both species can be as eight days interrupted by only brief (< trapped all year, even during winter on sub- one day) periods of arousal. In the laboratory freezing nights, except for those occasions during winter months P. parvus establishes when the substrate is frozen (Brown and Bar- large seed hoards (i.e., an energy surplus) and, tholomew 1969, Hall 1946; pers. obs.). In while maintained at ambient temperatures both Perognathus and Microdipodops, as in equivalent to winter burrow temperatures (ca Dipodomys, the periodicity of torpor seems 5 C), spontaneously enters torpor; torpor to be based on a circadian schedule with indi- bouts are initially circadian followed by pro- viduals initially torpid during the usual gressive increases in duration until, com- daylight hours and normothermic at night monly, individuals are torpid for five or more (Brown and Bartholomew 1969, Carpenter days at a time. Meehan's data imder simu- 1966, French 1977, Meehan 1976, Tucker lated winter conditions indicate that individ-

1962). If conditions that foster the use of tor- uals are torpid, with body temperature (Tb) por prevail, whether it be in obligate hi- approximating T^, 90 percent of the time, bernators or short-termers, circadian bouts of and expend only 16 percent of the energy torpor may extend into those of greater dura- that would be expended if normothermic in tion, some lasting several days (Brown and an insulated nest in the burrow; this energy Bartholomew 1969, French 1977, Meehan savings would obviously be increased several-

1976). Whether torpor be circadian or of fold if compared with the cost of nightly for- longer duration, or whether the use of torpor aging on the surface. bouts be confined to short periods of in- The magnitude of energetic savings while hospitable surface conditions or to a com- torpid is demonstrated in Figure 4, which plete winter season, its adaptive significance shows that at T^ = 2 C (approximating win- to these granivores is linked primarily to ter burrow temperatures) the metabolic cost energy conservation, enabling its prac- for torpid mice is 3 percent of that for resting titioners to subsist for short or longer periods nontorpid animals. The extraordinary preci- in underground burrows on a finite energy sion of thermoregulatory control while torpid store in the form of seed hoards at a fraction is also demonstrated in Figure 4: at T^s be- of the energetic cost they would expend if tween 2 and -2 C (and at a Tb barely above continually normothermic (Brown and Bar- freezing) P. parvus is capable of activating tholomew 1969, Kenagy 1973, Meehan 1976, the heat production machinery sufficient to Tucker 1966). maintain Tb at or slightly above 2 C. Thus, For torpor to serve efficiently as an with tissues approaching freezing, these ani- energy-conserving mechanism in hetero- mals are capable of maintaining a constant myids, its use must be accompanied by preci- body temperature at very low metabolic cost, sion of control. Such precision has been dem- thereby avoiding prohibitively costly normo- onstrated in Microdipodops pallidus by thermia and at the same time ensuring con- Brown and Bartholomew (1969), who have tinuing survival throughout a winter season shown that periodicity and duration of torpor of underground dormancy. 72 Great Basin Naturalist Memoirs No. 7

c 6 1983 Biology of Desert Rodents 73 ecologically) ancestral and transitional would Both Perognathus and Dipodoniys were have persisted through the present in habitats present in upper Tertiary times (Lindsay of appropriate rainfall and seed production 1972, Shotwell 1967, Reeder 1956, Wood patterns, most typically in tropical and sub- 1935), long before the formation of true tropical settings. deserts in southwestern North America (Ax- Tlie next sequence of events followed con- elrod 1950). Voorhies (1974, 1975) has de- tinuing reductions in mass of quadrupedal scribed as fossils a Perognathus sp. and a bi- heteromyids down to about 35-40 g, at pedal kangaroo rat (Eodipodomys which some critical event(s) occurred, result- celtiservator) preserved in their burrows in ing in the locomotor dichotomy between early Pliocene deposits in northeastern Ne- quadrupedality and bipedality (and the even- braska. Preserved with them were seed tual origins and adaptive radiations of Pe- hoards indicative of their granivorous habits, rognathus and Dipodoniys). During the devel- and their habitat was interpreted to be a riv- opment of this dichotomy, water regulatory erine area traversing a grassland with a mild, efficiency became fixed at an intermediate equable climate. Shotwell (1967) describes level and independent of mass in Dipodomijs; fossil Dipodornys spp. and Perognathus spp. in Perognathus, as in other quadrupedal het- from the middle Pliocene of Oregon with no eromyids, water regulatory efficiency con- reference to probable habitat, and Lindsay tinued to increase concomitant with further (1972) reports the presence of Perognathus reductions in body mass as the prevailing spp. in middle Miocene deposits in what is pattern of increasing aridity continued. Also, now the Mojave Desert of California, again it is suspected that the capacity for torpor with no reference to probable habitat. It is was developed just prior to the dichotomy in apparent that Perognathus and Dipodornys locomotion, and at some critical, relatively were geographically wide-spread throughout small mass (ca 40 g) at which the costs of much of southwestern North America in up- quadnipedal foraging during periods of exper Tertiary times, and inhabited areas pre- cessive energy demand (low temperatures dominantly grassland and semiarid in nature and/ or reduced seed availability) exceeded (Reeder 1956). the benefits. Torpor would represent a phys- The formation of true deserts resulted from iological alternative to relieve either tempo- the late Pliocene-Pleistocene uplift of the rarily or for longer periods the energetic Sierra Nevada-Cascade axis, together with trade-off in the inefficiency of locomotion in- the transverse and peninsular ranges of Cali- herent with smaller mass: during energeti- fornia and Baja California and the ensuing cally stressful periods or seasons for surface rainshadow effect (Axelrod 1950, 1958). Pe- activity, the energetic savings of torpor in rognathus and Dipodoniys, representing lin- the burrow might more readily promote posi- eages that for many millions of years had tive energy balance. An alternative explana- been subjected to progressive aridity, likely tion for the evolution of torpor in smaller were preadapted to a desert existence, and heteromyids as a trade-off for locomotor in- occupied this still more arid, new environ- efficiency might simply be the inability of in- ment without much further modification. dividuals of small mass (and a high sur- Bipedalism, as exhibited by Dipodornys face:volume ratio) to increase heat species, would by my scenario have devel- production sufficiently to offset heat loss dur- oped in semiarid, open habitats, likely grass- ing extreme cold, resulting in hypothermia. lands, as an aid in traversing the expanses be- This alternative would be independent of tween foraging sites. It represents an food-finding ability. The evidence that torpor adaptation tliat could then readily be ex- was developed in heteromyids at or prior to ploited in desert habitats. Although there is the locomotor dichotomy is that it occurs in no evidence that bipedal locomotion in Di- both Perognathus and Dipodoniys (see ear- podornys confers a direct energetic advantage lier); it is a finely timed energy-conserving (Fig. 4), I think there can be no question that device in the former (Fig. 3), but is only la- it provides some as yet undefined relief (i.e., tently present in the latter and is likely a rel- foraging advantage) from energetic con- ictual capacity. straints that would be imposed on a quad- 74 Great Basin Naturalist Memoirs No. 7 ruped of the same mass and habitat. The evi- and Dipodomys: they are small in size with dences for this statement are these: (1) in low absolute energy requirements and ef- spite of relatively large mass and large abso- ficient water regulatory capacities; they uti- lute energy requirements while living in hab- lize torpor most propitiously; and they are itats of limited seed production, torpor is sel- bipedal. They are deserving of more dom if ever used; (2) a fixed, intermediate attention. level of water regulatory efficiency restricts The family Heteromyidae is a rather di- seed usage to those higher in carbohydrate verse group of rodents with respect to their composition and therefore higher in MWP adaptive physiology. Yet, when interpreted

(MacMillen and Hinds, 1983); and (3) cheek in light of locomotor and size differences pouch volume (i.e., food-carrying capacity) in within the family, together with paleoclima- granivorous Dipodomijs spp. is independent tological histories, discernible patterns that are consistent both evolution- of body mass, but it is strongly and positively emerge correlated with body mass in quadrupedal arily and ecologically. heteromyids (Morton et al. 1980). Thus, ac- companying bipedality in Dipodomys are Acknowledgments several characteristics that can be construed as energetically liberal, at least in comparison Much credit for idea formulation, data col- with their quadrupedal cousins, whom they lection and reduction, and field companion- typically exceed in biomass when sympatric ship is given to D. S. Hinds. Thanks are extended to L. Bretz K. (pers. obs.). Yet to be demonstrated are the W. and G. for additional aid in data collec- direct advantages of bipedality in hetero- Cunningham tion and reduction, to R. W. Putnam for aid myids; among these is the likelihood of en- in blood lactate determinations, and to Barb hancing predator avoidance and escape, but MacMillen for typing the manuscript. Con- others should not be dismissed without trial. tinuing appreciation is extended to Hi Ho Sai Another mystery among heteromyids, at Gai. Financial support for this study was pro- least to me, is Microdipodops, which inhabits vided by NSF grants DEB-7620116 and exclusively Great Basin deserts. Their habi- DEB-7923808. tats are not only arid but of high elevation, and, therefore, have markedly truncated growing seasons. They are mysterious be- Literature Cited cause virtually nothing is known of their ori- AxELBOD, D. I. 1950. The evolution of desert vegetation gins, or whether they are more closely re- in western North America. Carnegie Inst. Wash- lated to Perognathus or Dipodomys. ington, Publ. 590:215-360. Authorities align them more closely with one 1958. Evohition of the Madro-Tertiarv Geoflora. or the other (Hafner 1978, Lindsay 1972), not Bot. Rev. 24:433-509. Bartholomew, G. A., and T. Cade. 1957. Temper- particularly close to either (Reeder 1956), or J. ature regulation, and aestivation in the little change their minds (Wood 1931, 1935). This pocket mouse, Perognathus longimembris. J. lack of agreement is due largely to the ab- Mammal. .38:60-72. sence of a fossil record. It is due in part, too, Bartholomew, G. A., Jr., and H. H. Caswell, Jr. 1951. to the bipedal mode of locomotion in Micro- Locomotion in kangaroo rats and its adaptive significance. Mammal. 32:155-169. dipodops and the assumption that this implies J. Bartholomew, G. A., and R. E. MacMillen. 1961. Ox- close relatedness to Dipodomys. Nevertheless, ygen consumption and hibernation in the kan- Wood (1935) emphasizes that bipedalism has garoo mouse, Microdipodops pallidus. Phvsiol. arisen several times independently in hetero- Zool. 34:177-183. Baudinette, R. v., K. a. Nagle, and R. A. D. Scott. myids, including extinct lineages only re- 1976. Locomotory energetics in a marsupial [Ant- motely related to extant genera; I see no rea- echinomijs spenceri) and rodent {Xotoinys alexis). son to doubt an independent origin of Experientia 32:583-584. bipedalism in Microdipodops. Microdipodops Biewener, a., R. M. Alexander, and N. C. Heglund. are also mysterious from a physiological 1981. Elastic storage in the hopping of kangaroo rats {Dipodomifs spectabilis). ]. Zool., London point of view. To me they represent an enig- 195:369-383. matic compromise that combines the water Bhody, S. 1945. Bioenergetics and growth. Rheinhold and energy regulatory virtues of Perognathus Publ. Co.. New York. 1023 pp.' 1983 Biology of Desert Rodents 75

Brown, H., and G. A. Bartholomew. 1969. Period- 1983. Water regulation in Peromyscus. J. J. icity and energetics of torpor in the kangaroo Mamm. 64:38-47. mouse, Microdipodops pallidas. Ecology MacMillen, R. E., and A. K. Lee. 1969. Water metab- 50:705-709. olism of Australian hopping mice. Comp. Bio- evolution torpidity in chem. Physiol. Cade, T. J. 1964. The of rodents. 28:493-514. Acad. Scient., Ann. Fenn. A. IV. 71/6:79-112. 1970. Energy metabolism and pulmocutaneous Carpenter, R. E. 1966. A comparison of thermoregula- water loss of Australian hopping mice. Comp. tion and water metabolism in the kangaroo rats Biochem. Physiol. 35:355-369. Dipodomijs agilis and Dipodomys merriami. Univ. MacMillen, R. E., and D. S. Hinds. 1983. Water regu- California Publ. Zool. 78:1-36. latory efficiency in heteromyid rodents: a model T. 1976. Energetic cost of locomotion in and its application. Dawson, J. Ecology 64:152-164. R. E., Australian hopping mice. Nature 259:305-307. MacMillen, and J. E. Nelson. 1969. Bioenerget- Dawson, T. and C. R. Taylor. 1973. Energetic cost ics and body size in dasyurid marsupials. J., Amer. J. of locomotion in kangaroos. Nature 246:313-314. Physiol. 217:1246-1251. Dawson, W. R. 1955. The relation of oxygen con- McNab, B. K. 1979. Climatic adaptation in the energet- to in ics of heteromyid rodents. sumption temperature desert rodents. J. Comp. Biochem. Mammal. 36:543-553. Physiol. 62A:813-820. Fedak, M. a., B. Pinshow, and K. Schmidt-Nielsen. Meehan, T. E. 1976. The occurrence, energetic signifi- running. cance and initiation of spontaneous torpor in 1974. Energy cost of bipedal Amer. J. the Physiol. 227:1038-1044. Great Basin pocket mouse, Perognathus parvus.

A., 1979. Unpublished dissertation, Univ. of California, Ir- Fedak, M. and H. J. Seeherman. Reappraisal of energetics of locomotion shows identical costs vine. Ill pp. in bipeds and quadmpeds including ostrich and Morrison, P. R. 1948. Oxygen consumption in several basal conditions. horse. Nature 282:713-715. mammals under J. Cell. Comp. Fleming, T. H. 1977. Responses of two species of tropi- Physiol. 31:281-292. cal heteromyid rodents to reduced food and wa- Morton, S. R., D. S. Hinds, and R. E. MacMillen. ter availability. 1980. Cheek pouch capacity in heteromyid ro- J. Mammal. 58:102-106. French, A. R. 1977. Periodicity of recurrent hypother- dents. Oecologia 40:143-146.' v., mia during hibernation in the pocket mouse, Pe- Paladino, F. and J. R. King. 1979. Energetic cost of rognathiis Physiol. terrestrial locomotion: biped and quadruped run- longimembris. J. Comp. 115:87-100. ners compared. Rev. Can. Biol. 38:321-323. Reeder, W. G. 1956. A review of Tertiary rodents of the Hafner, J. C. 1978. Evolutionary relationships of kangaroo mice, family Heteromyidae. Unpublished dissertation. Genus Microdipodops. J. Mammal. 59:354-365. Univ. of Michigan, Ann Arbor. 618 pp. Hall, E. R. 1946. Mammals of Nevada: Univ. of Califor- Schmidt-Nielsen, B., K. Schmidt-Nielsen, A. Brokaw, nia Press, Berkeley and Los Angeles. 710 pp. and H. Schneiderman. 1948. Water conservation Cell. Physiol. 1981. The mammals of North America. Vol. 1, in desert rodents. J. Comp. 2d ed., John Wiley and Sons, New York. 600 pp. 32:331-360. R. O. Maloiy, Hinds, D. S., and R. E. MacMillen. In preparation. Seeherman, H. J., C. Taylor, G. M. and Scaling of energy metabolism and evaporative R. B. Armstrong. 1981. Design of mammalian water loss in heteromyid rodents. respiratory system. II. Measuring maximum aero- Howell, A. B. 1933. The saltatorial rodent Dipodomijs: bic capacity. Resp. Physiol. 44:11-23. A. 1967. Late Tertiary geomyoid rodents the fimctional and comparative anatomy of its Shotwell, J. muscular and osseous systems. Proc. Amer. Acad. of Oregon. Univ. Oregon Mus. Nat. Hist. Bull. Arts and Sci. 67:377-536. 9:1-51. Snedecor, G. W. 1956. Statistical methods. Iowa State Hudson, J. W., and J. A. Rummel. 1966. Water metabolism and temperature regulation of the primi- College, Ames. 534 pp. L. Raab. tive heteromyids, Liomys salvani and Liomys ir- Taylor, C. R., K. Schmidt-Nielsen, and J. roratus. Ecology 47:.345-354. 1970. Scaling of energetic cost of running to body Physiol. Kenagy, 1973. Daily size in mammals. Amer. J. G. J. and seasonal patterns of activity and energetics in a heteromyid rodent com- 219:1104-1107. munity. Ecology 54:1201-1219. Taylor, C. R., G. M. O. Maloiy, E. R. Weibel, V. A. Z. Kamau, H. Seeherman, and Kleiber, M. 1932. Body size and metabolism. Hilgardia, Langman, J. M. J. b:315-353. N. C. Heglund. 1980. Design of the mammalian III. Scaling maximum aerobic 1961. The fire of life. John Wiley and Sons, New respiratory system. mass: wild and domestic mam- York. 454 pp. capacity to body Lechner, a. mals. Resp. Physiol. 44:25-37. J. 1978. The scaling of maximal oxygen E. Burke, and consumption and pulmonary dimensions in small Thompson, S. D., R. E. MacMillen, M. of biped- mammals. Resp. Physiol. 34:29-44. C. R. Taylor. 1980. The energetic cost mammals. Nature Lindsay, E. H. 1972. Small mammal fossils from the al hopping in small Barstow formation, California. Univ. California 287:223-224. in the California Publ. Ceol. Sci. 93:1-104. Tucker, V. A. 1962. Diurnal torpidity MacMillen, R. E. 1972. Water economy of nocturnal pocket mouse. Science 1.36:380-381. thermal con- desert rodents. Symp. Zool. Soc. London 1965. Oxygen consumption, 31:147-174. ductance, and torpor in the California pocket 76 Great Basin Naturalist Memoirs No. 7

californiciis. Cell. cycles of (Heteromijidae). mouse, Perognathiis J. Comp. Perognathiis flaviis J. Physiol. 65:393-403. Mammal. 59:707-716. 1966. Diurnal torpor and its relation to food Wood, A. E. 1931. Phylogeny of the heteromyid ro- consumption and weight changes in the Califor- dents. Amer. Mus. Novitates 501:1-19. nia pocket mouse Perognathiis californiciis. Ecol- 1935. Evolution and relationships of the hetero- ogy 47:245-252. myid rodents with new forms from the Tertiary R. 1974. Fossil pocket mouse burrows in VooRHiES, M. of western North America. Carnegie Museum. Nebraska. Amer. Midi. Nat. 91:492-498. Ann. 24:73-261. 1975. A new genus and species of fossil kangaroo WuNDER, B. A. 1974. The effect of activity on body tem- rat and its burrow. Mammal. 56:160-176. J. perature of Ord's kangaroo rat {Dipodomijs ordii). Wang, L. C, and W. Hudson. 1970. Some phys- J. Physiol. Zool. 47:29-36. iological aspects of temperature regidation in the YousEF, M. K., and D. B. Dill. 1971. Daily cycles of hi- normothermic and torpid hispid pocket mouse, bernation in the kangaroo rat, Dipodomijs mer- Perognathiis hispidus. Comp. Biochem. Physiol. 8:441-446. 32:275-293. riami. Cryobiology Zar, H. 1974. Biostatistical analysis. Prentice-Hall, O., 1978. Effects of J. Wolff, J. and G. C. Bateman. food availability and ambient temperature on torpor 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 activity throughout the winter in larger species to extended periods of torpor by smaller pocket mice. The rodents forage 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 characteristic of the group of rodents.

Observational and anecdotal information conditions (e.g., with light-amplifying de- pertinent to heteromyid behavior is present vices). The rodents also are ammenable to in the literature beginning around the turn of laboratory manipulation and observation, al- the century. Although these early pieces of though breeding these rodents in the labora-

information are valuable in themselves, they tory is difficult. In addition, the seeds the ro- offer no coherent view of behaviors across dents eat are particulate and thus relatively geographic or taxonomic boundaries. The easy to quantify and analyze in studies of diet landmark work of Eisenberg (1963) provided choice and foraging. With these distinctive a turning point, and much of the work on features in mind, I will discuss heteromyid heteromyid behavior since that time has used activity patterns, foraging, spacing, territo- heteromyids as tools to answer questions of a riality and aggression, reproduction, anti- more general and conceptual nature. predator behavior, burrow construction, sen- Although heteromyids suffer from many of sory abilities, and personal care. When I the same problems other mammals do for be- mention heteromyids in the context of some havioral studies (e.g., nocturnal activity and specific behavior, it is not to imply that all subterranean burrows and nests), they do of- heteromyids exhibit that behavior. Readers fer some distinctive benefits. For example, all should note the citations and recognize that heteromyids possess external fur-lined cheek the generalizations actually refer to the spe- pouches that are used during foraging for cific animals studied by the authors cited. gathering seeds. Thus, whereas most animals Activity eat their food as they collect it, heteromyids have separate collecting and ingesting behav- Activity patterns are usually inferred from iors. Also, some heteromyids (kangaroo rats the number of individuals in a population ac- and kangaroo mice) exhibit a distinctive sal- tive during specific times of a diel or annual tatorial bipedal locomotion important for cycle. This should probably be considered a foraging and/ or predator avoidance behav- population phenomenon and I will concen- iors. The deserts inhabited by heteromyids trate on what aspects of the environment tend to be relatively open, allowing observa- might generate those patterns and briefly dis- tion of these types of activities under special cuss torpor and its use.

of the American Society of Mammalogists, hosted by Brigham Young 'From the symposia . Biology^^ of Desert Rodents," presented at the annual meeting University, 20-24 June 1982,82, at Snowbird, UtahUtah. ^Division of Biology, Kansas State University, Manhattan, Kansas

77 78 Great Basin Naturalist Memoirs No. 7

In general, heteromyids respond to pre- and Van De Graaff (1973) noted that during dictable daily and seasonal cyclical patterns one extremely hot summer, activity of indi- in their environments as well as specific pre- vidual kangaroo rats was reduced but pocket dictable weather phenomena. Heteromyids mice remained active. are primarily nocturnal (Kenagy 1973a, Two miscellaneous features of heteromyid Lockard 1978, Reichman and Van De Graaff activity need to be mentioned. Schmidley

1973), although diurnal activity is occasion- and Packard (1967) noted that four species of ally noted. Relatively high winds or precipi- pocket mice could swim by treading water tation can decrease or halt normal nocturnal for approximately one minute before becom- activity (Kenagy 1973a, Lockard 1978). On ing exhausted, floating, eventually losing two occasions I have noted, after an evening coordination, and drowning. Stock (1972) thunderstorm, that all wet individuals in found that nine species of kangaroo rats were traps were juveniles and all the adults were "good" swimmers in artificial ponds and dry, suggesting that adults did not come out aquaria. Finally, Kenagy and Enright (1980) show that the activity of D. merriaini in the to forage imtil after evening rains. There is for five prior conflicting evidence for moonlight avoidance laboratory was depressed days to a large earthquake, especially in the pre- in heteromyids. Kenagy (1976a) and Schroder midnight phase. This reduced activity (1979) noted no moonlight avoidance in abruptly disappeared the night after the kangaroo rats, but Kaufman and Kaufman earthquake. (1982) and Lockard and Owing (1974) suggest they do avoid moonlight. It should be noted that these stvidies were in different Foraging areas on different species. Evidence presented by Lockard (1978) may provide an ex- Desert heteromyids are primarily gra- planation of the disparity in the other re- nivorous (Bradley and Mauer 1971, Brown et ports. He suggests that Dipodomys spectabilis al. 1979, Reichman 1975, 1978), although may avoid moonlight, presumably because of they may seasonally ingest large quantities of increased susceptibility to predation, during green vegetation and insects. One study sug- times of the year when food is abundant, but gests that as individual kangaroo rats encoun- be forced into periods of moonlight activity ter water stress by eating too many high- when resources are scarce. Rosenzweig protein mesquite seeds, they switch to eating (1974) presents a conceptual explanation for the herbaceous seed pods (Schmidt Nielson et this phenomenon. al. 1948). Many species of heteromyids can Various aspects of heteromyid activity re- apparently go without drinking free water late to temperature and rainfall (French for long periods of time, supporting them- 1975, Kenagy 1973a, 1976a). Reichman and selves on metabolic water from food items Brown (1979) elaborate on these aspects of (see MacMillen, this volume). Eisenberg activity and note, along with Brown and Bar- (1963) noted that young heteromyids eat sol- tholomew (1969), that the amount of food is id food from the time their incisors erupt. also important in determining above-ground There are important exceptions to the spe- activity. When temperature or food avail- cialized granivory exhibited by heteromyids. ability is low (usually in the winter; French Kenagy (1972, 1973b) detailed the use of salt- 1976), small heteromyids will tend to go into bush leaves (Atriplex) by Dipodomys rnicrops. or stay in torpor for extended periods of time Individuals of this species use their chisel- (perhaps up to 5 months; Reichman and Van shaped teeth to strip away the salt-laden epi- Dc Graaff 1973). Apparently, larger hetero- dermis of the Atriplex leaves before ingesting myids (approximately 18g -I-) rarely use tor- them. Csuti (1979) noted a similar behavior por (Bartholomew and MacMillen 1961, Eis- and suggested that it was innate because indi- enberg 1963, French 1976, Kenagy 1973a, viduals from areas without saltbush devel- O'Farrell 1974, 1980). Whereas small homeo- oped the behavior as juveniles as quickly as therms are probably more affected by cold those from areas where saltbush was preva- temperatures than large ones, the larger spe- lent, but Dipodomys ordii never learned the cies may be more affected by heat. Reichman leaf-stripping behavior. Reichman (1975, 1983 Biology of Desert Rodents 79

1978) and Tappe (1941) noted the high use of 1951) and kangaroo mice. This contrasts with insects seasonally, and Vorhies and Taylor the quadrupedal locomotion of the pocket (1922) report an observation of a kangaroo mice (Bartholomew and Gary 1954). Signifi- rat chasing and catching a moth. Kenagy and cantly, almost no overlap in body size occurs Hoyt (1980) report the reingestion of feces by between the quadrupedal pocket mice and D. microps and show that the animals differ- bipedal kangaroo rats, although kangaroo entially ingest those fecal pellets that are rel- mice are small and the quadrupedal P. his- atively low in inorganic ions and relatively pidis approaches the size of some of the high in nitrogen and moisture. smallest kangaroo rats. Currently some ques- The diets of heteromyids apparently affect tion over the adaptive significance of these other behaviors. For example, several authors different locomotory techniques exists; this have noted the relationship between the in- will be discussed later by Price and Brown gestion of green vegetation and subsequent (this volume). reproduction (Kenagy and Bartholomew There are indications that some desert het- 1981, Reichman and Van De Graaff 1975, eromyids climb occasionally or extensively. Van De Graaff and Balda 1973). There also is Kenagy (1972) details the climbing of D. mi- apparently a relationship between the inges- crops in saltbushes to obtain leaves, and Ro- tion of ants by heteromyids and subsequent senzweig and Winakur (1969) suggest that infection by alimentary canal helminths, al- there may be a vertical component to hetero- though the effect of this infection on individ- myid foraging. I have observed large D. spec- uals is unclear (Gamer et al. 1976). tahalis climbing in Ephedra to harvest flow- of the most striking aspects of the for- One ers, but did not find heteromyids climbing in aging behavior of desert heteromyids is the bushes in an earlier study (Reichman 1979). short length of time they actually spend There seems to be an inverse relationship above ground searching for food. Schreiber between the size of a heteromyid species and (1973) reports total foraging times of up to the distance it travels while foraging during a five hours per night for P. parvus, although night (Bowers 1982, Thompson 1982a,b, and most other reports are for significantly short- in review). This is true for both average dis- er periods. Kenagy (1973) reports total times tance between stops and total distance averaging one hour, which includes time through the night. Thompson (1982a, 1984) spent in the burrow on return trips. The short reports average distances between foraging amount of time spent foraging is less striking stops of 7.52 m, 5.02 m, and 2.65 m for D. when it is recognized that seeds are a rela- deserti, D. merriami, and P. longimembris, re- tively rich resource that can occur in high- spectively. I have observed individual D. density patches (Reichman and Oberstein merriami moving up to 45 m before stopping 1977). A parameter that is perhaps more sig- to forage, and other authors have observed nificant ecologically than simple total for- similar distances (Bowers 1982, Thompson aging time is the time spent at each foraging 1982a,b). Schroder (1979) found that adult D. stop (time in a patch) and the time (and dis- spectabilis spent less than 22 percent of their tance) between patches. Bowers (1982) noted than 6 from their burrows, but that in a three-species commimity the small- time more m average 68 per foraging trip, and est pocket mice exhibited the shortest times that they m foraging travels. Ke- within and between patches, and kangaroo total 350 m per night in running rats had the longest times for both. An nagy (1973a) reported a maximum chased as 32 intermediate-sized pocket mouse was also in- speed for a kangaroo rat being of kph termediate in these two time parameters. kph, and I have calculated speeds 16 forag- Thompson (1984) also found that the relative- in the field for individual D. merriami ly larger bipeds spend more time stopped, ing freely (i.e., not being chased). Average and travel longer distances between stops, foraging speeds are probably significantly less, than the smaller quadrupeds. as Thompson (1984) reports mean speeds in Another distinctive feature of desert heter- transit of 6.28, 3.27, and 1.76 kph for D. omyid foraging is the bipedal hopping of the deserti, D. merriami, and P. longimembris, kangaroo rats (Bartholomew and Caswell respectively. 80 Great Basin Naturalist Memoirs No. 7

Once an animal begins to forage, a number as he describes how the rodents then sift the of senses apparently play roles in detecting soil they have excavated for seeds. Kenagy seeds. Generally, heteromyids seem to be (1972) and Csuti (1979) describe other food very aware of their surroundings, perhaps us- acquisition behaviors associated with ing vision to orient and note changes in their vegetation. local environment (Hall 1946), although Once a food item is secured, a heteromyid Reichman and Oberstein (1977) did not find can either eat the item immediately or put it visual cues to be important in laboratory in its cheek pouches for transport and stor- studies of foraging. Once general areas for age. This separates the gathering and eating foraging are located and entered, olfaction process and has important implications for probably becomes important for seed detec- foraging. From my observation, a heteromyid tion. Reichman and Oberstein (1977) found rarely eats an item at the collection site, but, that kangaroo rats in a laboratory experiment rather, pouches it and returns to the burrow. were able to detect seeds to a depth of up to Presumably, the burrow provides a more 20 cm, and the authors present a regression equable environment in which to sort seeds than does the surface, which is hotter (or equation for the relationship between seed colder in winter), drier, and rich in predators. detection by captive kangaroo rats and the Reichman (1977) has shown that although depth/size of a buried packet of seeds. Lock- heteromyids do not apparently gather food ard and Lockard (1971) and Reynolds (1958) into their pouches in the exact proportions present infonnation from the field dealing available, a more diverse sample of seeds is with the accuracy of underground seed de- found in the pouches than ingested, sugges- tection, and Johnson and Jorgensen (1981) ting that the rodents do gather items they do suggest that soil moisture is important for not subsequently ingest. Animals without seed detection by olfaction. Reichman (1981) cheek pouches would usually eat a food item discusses the nature of olfaction as a cue for as it was obtained. Morton et al. (1980) show foraging heteromyids. that cheek pouch volume scales positively In an intriguing study, Lawhon and Hafner with body mass in grams (volume of cheek (1981) show that tactile cues may be the final pouches in cm^ = 0.065 mass^^^^. They also sense used to judge the nature of a food item. suggest that a heteromyid could fulfill its to- They foimd differences between species in tal daily requirement with one full load of tactile abilities, and found that individuals seeds from its pouches. This, plus the obser- most often misjudged nonedible food items vation that animals rarely are captured with that resembled edible items in shape or tex- full pouches (Reichman 1978), presents a ture, regardless of weight or overall dimen- puzzling question as to why individuals sions. The tactile input discussed by Lawhon would return to their burrows before filling and Hafner (1981) comes from actual touch- their pouches. Nickolai and Bramble (this ing with the forepaws, and is probably im- volume) offer an interesting explanation. portant and effective for an animal with its The husking of seeds is highly variable be- eyes on top of its head. Eisenberg (1963) re- tween species and individuals, although Ro- ported another use of tactile senses involving senzweig and Sterner (1970) suggest that rel- the long vibrissae of the rodents. He noted ative husking rates are a phenomenon that that even rapidly rimning or hopping rodents might promote coexistence between sym- leave trails in the sand from their dragging patric heteromyid species. The authors show vibrissae, and he suggested this that assists that larger species husk more rapidly than the animals in maintaining their balance smaller species, but that the smaller species while niiuiing. are more efficient per gram of body weight. Once heteromyids find a seed or patch of Rosenzweig and Sterner (1970) used relative- seeds, they excavate in a manner typical of ly large domestic seeds and it is not known rodents, using the forepaws for the initial ex- how this relationship would extrapolate to cavation and moving the soil to the rear, smaller, native seed species. where it is kicked out by the hind legs (Eisen- There are several additional foraging be- berg 1963). Eisenberg alludes to the tactile haviors exhibited by desert heteromyids. Vor- cues discussed by Lawhon and Hafner (1981) hies and Taylor (1922) suggest that individual 1983 Biology of Desert Rodents 81 heteromyids might rob the seeds stores of the cheek pouches and cache environments other individuals. Tappe (1941) and Clark of these rodents, and that some of these fungi and Comanor (1973) found that heteromyids could have important impUcation for cache occasionally dig into ant mounds, presumably management behaviors. to secure seeds. Heteromyids also eat many The benefits of caching could include long- insects (Reichman 1975, 1978), and I have term storage for periods of low production, foimd cheek pouches full of headless ants. enhancing nutritional and/or moisture condi- These ants may have been "husked" to mini- tions of the seeds, and protection of seeds mize the probability that the consumer from robbing by other granivores. would be bitten. One peculiar behavior noted Several aspects of heteromyid foraging be- by Benson (1935) was that of a D. deserti havior, as mediated through anatomy and kicking sand over a novel food item placed physiology, have been implicated in the com- near a burrow by Benson. munity structure of the rodents (see Price and One of the most intriguing aspects of het- Brown, this volume). Although much con- eromyid behavior is the caching of seeds. troversy remains, most investigators agree Voorhies (1974) has found cached seeds asso- that the bipedal /quadrupedal relationships, ciated with fossil pocket mouse burrows that cheek pouches and seed storage, microhabitat are nearly 10 million years old, so it is an an- choice and use, and seed patch density selec- cient behavior, perhaps associated with the tion are important behavioral components development of cheek pouches. Relatively that impinge on community structure. Reich- little is caching known about by pocket mice man (1981) has suggested that the biped- (Blair 1937) or small kangaroo rats, but most al/quadrupedal difference could help pro- of the large kangaroo rat species are known mote coexistence between kangaroo rats and for their elaborate burrows in which they pocket mice, but this has recently been store large quantities of seeds (Culbertson brought into question by Thompson et al. 1946, Hawbrecker 1940, Reynolds 1958, (1980), who have shown that bipedal locomo- Shaw 1934, Tappe 1941, Vorhies and Taylor tion is no more energetically efficient than 1922). Some species store on the surface as quadrupedal locomotion for similar-sized in- well as below ground (D. heennani, Tappe dividuals. Seed size selection behaviors have 1941; D. ingens, Shaw 1934), but most store been suggested as means of coexistence seeds below ground. The piles are usually (Brown 1975, Mares and Williams 1977), but sorted by species, even if they have been other authors have questioned the sufficiency gathered from mixed-species patches, and of this explanation (Lemen 1978, Smigel and some of the quantities are huge. Vorhies and Rosenzweig 1974). Numerous studies have Taylor (1922) report caches of from 5 to 5750 suggested habitat selection as a means of co- gms for D. spectibalis, Shaw (1934) found existence among sympatric heteromyids caches of from 1 to 8V4 quarts, and Tappe (Lemon and Rosenzweig 1978, M'Closkey (1941) foimd dozens of caches. 1980, 1981, O'Dowd and Hay 1980, Rosen- Eisenberg (1963) discusses caching by sev- zweig 1973, Rosenzweig and Sterner 1970, eral species in the laboratory and found a and Winakur 1969, Stamp and possible tendency for females to cache more Rosenzweig 1978, Thompson 1982a, b) and other than males. Lawhon and Hafner (1981) show Ohmart density selection is that pocket mice cache more of the seeds authors state that patch Price 1978, Trombu- available than kangaroo rats, and that hoard- important (Hutto 1978, 1980, Wondolleck 1978, but ing is greater in the fall and spring than in lak and Kenagy 1980) and related the winter. Although little is known about see Frye and Rosenzweig the underground regimes of cache manage- to both seed size selection and habitat selec- ment and use, Kenagy (1973) noted that tion through seed distribution (Reichman kangaroo rats are quite active underground 1981, Reichman 1983, Reichman and Ober- during the 23 hours a day they are not above stein 1977). It is intuitive that all these behav- ground foraging. Studies I have recently be- iors could be, and probably are, important gun with D. T. Wicklow reveal that approx- components of community phenomena noted imately 20 species of fungi can be found in in the heteromyids (Bowers and Brown 1982). 82 Great Basin Naturalist Memoirs No. 7

Further research is mandatory before a cohe- would place pressure on the animals to devel- rent picture of the relative importance of op exceptional hearing. Another indication of these behaviors, and the communities and lo- the excellent hearing in heteromyids is en- cahties where they are important, is estab- larged auditory bullae, most notable in the hshed. In addition, other behaviors, such as kangaroo rats. Not only is their hearing good, predator avoidance, may be important in de- but kangaroo rats have also developed espe- termining desert heteromyid rodent commu- cially acute reception at those frequencies of nity structure. sound made by a rattlesnake's rattle and an owl's wing (Webster 1962). In other studies, Predator Avoidance Behavior Webster and Webster (1971, 1972, 1980) have shown that kangaroo rats can effective- Heteromyids Hve in an environment rich in ly detect predators with either vision or hear- predators (Hall potential and Kelson 1959). ing, but if both senses are eliminated the rats Vorhies and Taylor (1922) list numerous usually succumb to predators. predators on D. spectabilis and note that, of Bartholomew and Caswell (1951), Thomp- 592 owl pellets they examined, 230 contained son (1982a), and Hay and Fuller (1981) sug- kangaroo rat remains. One means of avoiding gest that the bipedal locomotion and rico- predators is color crypticity, and Benson chetal bounding of kangaroo rats might be (1933) shows that many rodents in the south- primarily an adaptation to predator avoid- western United States include substrate color ance. Certainly the irregular hopping would matching in their repertoire of predator be distracting to a predator, and Eisenberg avoidance schemes. (1975) notes that kangaroo rats immediately

Heteromyids seem to have a general hop away when a rattlesnake is nearby. Hay awareness of their surroundings and are very and Fuller (1981) found that heteromyids are sensitive to peculiar sounds and sights. Eisen- more selective in their diet choice when they berg (1963) notes that novel items in their forage in the open than when they forage in cage elicit attention, and occasionally dis- the presumed relative safety of a shrub, and placement behaviors such as digging. Hall the authors suggest that this selectivity may (1946) states that heteromyids are drawn at be due to predator pressures in the open. The night to newly disturbed areas (e.g., a boot opposite prediction, that of low selectivity in heel dragged in the soil surface), and many the open, could be made if predator pressures investigators are familiar with kangaroo rats are high in the open areas. In this explana- burying traps under a pile of dirt. Some het- tion, heteromyids would move rapidly eromyids are known to plug their burrows at through the open areas, gathering seeds in- night (Chapman and Packard 1974; Compton discriminantly into their pouches, making the and Hedge 1943), and this may partially be a critical diet choices later in the relative response to potential predation. safety of their burrows (Reichman 1977, As discussed in the section under activity 1981). patterns, heteromyids seem to avoid environmental conditions, such as bad weather or Spacing, Territories, and Aggression bright moonlight, that might hamper their ability to detect predators or make them For the most part, heteromyids are solitary more obvioiLS to predators. Apparently, both animals (Blair 1937, 1943, Dixon 1959, Schef- hearing and sight are important components fer 1938), living singly in their burrows (Eis- of predator detection. Webster (1962) and enberg 1963 and Martin 1977 describe them Webster and Webster (1971, 1972, 1980) as "asocial"). Monson and Kessler (1940) have documented the extremely accurate foimd only 3 of 44 burrows with more than hearing of kangaroo rats, especially for low- one individual D. spectahalis, and Monson frequency sounds, and tliey suggest that this (1943) found 41 of 53 mounds to be singly oc- has developed in response to predator detec- cupied. Several of the dual occupancy bur- tion. Desert conditions may be poor for rows had two adults, but most were females soimd transmission (hot and drv), and this and their offspring. Some species are noted 1983 Biology of Desert Rodents 83 for having more than one burrow, and Chap- characteristics of the dorsal gland in five spe- man and Packard (1974) report that male D. cies of kangaroo rats, and discusses its pos- merrianii average 6-7 burrows and females sible role of scent marking. have approximately 5 burrows each. Current Another behavior that may be related to observations in the field by several in- territorial pronouncements is drumming with vestigators suggest that this may be more the hind feet. It is relatively easy to get an common than is generally thought. Individ- adult D. spectabalis to respond with drum- uals occupying more than one nest may ex- ming by tapping lightly on their mound. Eis- plain why in some areas a large percentage enberg (1963) noted drumming in Di- of burrows appear to be unoccupied. Schro- podomys, Perognathus, and Microdipodops der and Geluso (1975) found 42 of 121 D. species in relation to aggression, and teeth spectahilis mounds unoccupied. All mounds chattering in the same context. Kenagy combined showed a uniform spatial distribu- (1976b) observed drumming in the field dur- tion, whether occupied or not. ing a contest between male kangaroo rats, Data on the home range size of hetero- eventually leading to copulation between one myids are scattered throughout the literature, of the males and a female. but one feature that seems to emerge is that Overt aggression between individual heter- home ranges are not directly related to the omyids may be rare, or simply rarely seen. average body size for a species. Small pocket Eisenberg (1963) provides extensive informa- mice frequently exhibit home ranges near the tion of the types of aggressive interactions size of larger species (Chew and Butterworth generated in a laboratory setting, and excel- a 1964), and Schroder (1979) reported smaller lent descriptions of the modes of attack and home range for D. spectahilis than D. mer- associated behaviors such as scratches and riami. There are reports that males have growls. The general trend in Eisenberg's lab- larger home ranges than females (Maza et al. oratory study, and those of Hoover et al. 1973) and that the home ranges of male and (1977)' and Blaustein and Risser (1974, 1976) female kangaroo rats overlap extensively is for large individuals of one species to even- (O'Farrell 1980). Holdenreid (1957) and tually win over smaller individuals of another Flake and Jorgensen (1969) report no differ- species, although the effort involved varied ence in dispersal rates between males and fe- greatly. Congdon (1974) notes a similar rela- males in a population, although it is primari- tionship in the field, and Vorhies and Taylor ly the juveniles that disperse. Recent work by (1922) describe fights in the laboratory be- Tom Jones (see Munger, Bowers, and Jones, tween D. spectabalis and D. merriami that this volume) suggests that individual kan- are "savage and to the death." I have video- garoo rats do not move far from their natal tapes of a kangaroo rat pouncing on a pocket burrow. mouse at a rich pile of seeds. Conversely, I Although areas around a home burrow are have watched two separate D. merriami not as aggressively defended as are territories chase adult D. spectabalis away from a forag- of other mammals (Eisenberg 1981), hetero- Aggression can be related to the sex myids apparently do show some degree of ing area. reproductive condition of the partici- territoriality, as manifested by aggression and and and Kenagy (1976b) possibly by scent marking, although the latter pants (Eisenberg 1963), provides an excellent description of aggres- proposition is unproven. Eisenberg (1963) de- between two males scribes various types of marking, including a sion observed in the field perineal drag, and suggests these are for terri- courting a female. heteromyids will have ag- torial identification. Borchett et al. (1976), Upon occasion, nonheteromyids. I have Griswold et al. (1977), Laine and Griswold gressive bouts with off Peromyscus (1976), and Randall (1981a, b) present details observed kangaroo rats chase of sand bathing by kangaroo rats and suggest individuals at artificially placed seed piles, that the odors produced may connote infor- and Shaw (1934) notes similar events. McCue mation about the species, sex, and possibly and Caufield (1979) report a grasshopper reproductive condition of the depositor. mouse attacking and dismantling a kangaroo Quay (1953) notes the sexual and seasonal rat in daylight hours. 84 Great Basin Naturalist Memoirs No. 7

Reproduction and Parental Care The gestation period is relatively short

(18-30 days; Butterworth 1961, Day et al. Desert heteromyids generally have one or 1956, Holdenreid 1957) and is almost always two litters a year. Females are usually in es- accompanied by nest building on the part of trus for specific periods, but males may be the female (Eisenberg 1963). Eisenberg scrotal the entire year (Bradley and Mauer (1963) reports that most births occur during 1971, Reichman and Van De Graaff 1973). the day and, though mothers will eat any Juvenile female kangaroo rats develop swol- dead neonates, no aggressive behavior is sub- len vaginas at about six weeks and can consequently demonstrated toward their surviv- ceive at 12 weeks (Eisenberg 1963). ing offspring. The young are born in a rela- Observation of coiu-tship and reproduction tively precocial state (Eisenberg 1963). At are rare from the field, although Engstrom the time of birth, the female stand or lie and Dowler (1981) and Kenagy (1976b) pro- may her side, assisting the process vide interesting field observations. Daly et al. on with her forepaws (Butterworth (1980) note that D. agilis and D. merriami in teeth and 1964, Eisen- reproductive condition prefer traps that con- berg 1963). Subsequent to parturition, the fe- tain conspecific odors, whereas non- male ingests the placenta. Van De Graaff reproductive individuals show no preferences (1973) notes that the bone formation in the between odorized and odor-neutral traps. extremities of kangaroo rats is greater than The preferences appear to be independent of for similarly aged pocket mouse embryos and the sex of the donor and the recipient. Labo- juveniles, which still have major limb com- ratory studies suggest that near the onset of ponents made of cartilage. Eisenberg (1963) estrus males become more tolerant of and in- notes that muscular coordination seems to de- terested in females (Eisenberg 1963, Martin velop in the young from anterior to posterior. 1977). Prior to that, males and females can be Parental care is carried out entirely by the very aggressive toward each other (But- female. She crouches to nurse the young, and terworth 1961), or live in the same arena she will move them about the nest by car- without aggression (Eisenberg and Isaac rying them in her teeth with a grasp behind 1963). Eisenberg (1963) reports that, as the the neck (Eisenberg 1963, Tappe 1941). The time for copulation nears, a male and a fe- female may plug the entrance to the nest male may share a common nest box for one chamber when she is not in the nest (Eisen- night, after which they return to their own berg 1963). As weaning approaches, the fe- nest boxes and a peaceful coexistence. male will begin to ignore her young, eventu- A number of studies describe the cop- ally even shoving them away as they try to ulatory behavior of various heteromyids nurse. As the siblings begin to leave the nest, (Behrends 1981, Dewsbury 1972, Eisenberg dominance hierarchies are already being es- and Isaac 1963, Hayden et al. 1966), and Eis- tablished (Eisenberg 1963). LeVick (1982) enberg (1963) describes an elaborate protocol does not find any ultrasonic communication for reproductive behavior in the heteromyid between mothers and their offspring in D. or- species he studied in the laboratory. Basi- dii, but both he and Eisenberg (1963) report a

cally, there is some mutual attention in the broad range of audible sounds from infants few minutes prior to copulation. Sub- aged 2-14 days. Fourteen days corresponds sequently, the male mounts the female from to the time the young begin to eat solid foods the rear while she exhibits lordosis. After sev- and move from the nest (LeVick 1982). eral seconds to several minutes of thrusting and presumably ejaculating, the male dis- Burrow Construction moimts and shows little interest in the female. In some cases, one or the other of the An inverse relationship appears to exist be- sexes may msh the other, inciting another tween the size of a heteromyid species and

copulatory bout. Hayden et al. (1966) re- the amount of information on its burrows ported that some pairs fall on their sides dur- that has been published. This could be being copulation and continue to copulate in cause a similar relationship exists between this position. the complexity of the burrows and the size of 1983 Biology of Desert Rodents 85

the species. Generally, pocket mice have rel- built higher. Best (1972) notes that it takes atively simple burrows and the largest kan- from 23 to 30 months to build what would be garoo rats are known for their large, con- considered a mature mound. Mounds that are spicuous, and complex mounds and burrow left vacant begin to deteriorate noticably systems. within a month and are almost completely Blair (1937) reports that the burrow of P. gone within a year. hispidis is rather short and simple, with only one entrance and one nest chamber. Scheffer Sensory Abilities (1938) notes that the burrows of P. parvus are Although not much is known about the also simple, but may include a hairpin turn sensory abilities of heteromyids, some indirectly under the opening, and run to a triguing work has been carried out with the depth of 76 inches. Chapman and Packard hearing ability of kangaroo rats. Heffner and (1974) found that female P. merriami have Masterson (1980), Webster (1962), and Web- more complex burrows than males, and that ster and Webster (1971, 1972, 1980) have the adults frequently plug unused burrow noted the impressive hearing ability of kan- openings. Eisenberg (1963) found Micro- garoo rats across a broad range of frequencies dipodops burrows in loose sandy soil, and (1-60 KHz). Heffner and Masterson (1981) other authors have noted the soil texture also note that kangaroo rats are particularly where biu-rows are constructed (Anderson good at locating the origin of a sound, and and Allred 1964, Compton and Hedge 1943, Webster (1962) details the hearing of kan- Deynes 1954, Tappe 1941, Vorhies and Tay- garoo rats in relation to sounds made by lor 1922). In desert areas burrows are usually predators. I have noted while watching kan- obvious around the base of shrubs where garoo rats in the field that they are startled loose, windblown soil accumulates, providing only by certain kinds of noises. All loud a good location for burrow construction. Ke- noises get their attention, but metallic clicks nagy (1973a) gives information of the con- seem less disturbing than scratching noises struction of the burrows of P. longimembris, made by a boot in the dirt. D. merriami, and D. microps in the field, and Pocket mice and kangaroo rats can appar- Eisenberg (1963) gives details for several spe- ently smell seeds in the soil, even to great cies in the laboratory, including descriptions depths (Lockard and Lockard 1971). Reich- of the actual digging behaviors. man and Oberstein (1977) show the relation- The most extensive information about bur- ship between the ability of a kangaroo rat to row construction is available for the large detect a seed patch and the size/depth of the species of kangaroo rats, including D. spec- seeds and Reichman (1981) discusses olfaction tabalis (Best 1972, Holdenreid 1957, Monson and seed detection ability. Although it is dif- 1943, Monson and Kessler 1940, Vorhies and ficult to determine whether rodents cannot Taylor 1922), D. veniistus (Hawbreker 1940), smell an item or simply choose not to seek it,

D. heermani (Tappe 1941), D. ingens (Shaw it does appear that kangaroo rats have better 1946), and D. nitratoides (Culbertson 1946, olfactory ability than do pocket mice. Daly Fitch 1948). Generally these large species et al. (1980) noted that certain rodents, in- have mounds that are approximately two or cluding kangaroo rats, responded to odorized three meters in diameter and rise from one- traps, preferring them if the respondents half meter to one meter above the ground. were in reproductive condition.

Through the mound and down into the I know of no studies on the vision of heter-

ground pass numerous Rmways. Connected omyids, but it is pertinent to note that their to the Rmways are various nests and large, eyes are on top of their rounded heads, mak- flask-shaped caches where seeds are stored. ing vision ventrally and forward somewhat Some of the caches are walled off, but most restricted. remain open. The mounds are constructed by the rat kicking dirt with its hind legs up on Personal Care top of the existing structure. Through time,

the area surrounding the burrows is slightly Personal care seems to be accomplished by with lowered by the excavation, and the mound is two major behaviors. One is associated 86 Great Basin Naturalist Memoirs No. 7 autogrooming and washing, and another with rodent would forage. The pouches make the care of the dorsal gland possessed by gathering food and eating food two different many heteromyid species. Eisenberg (1963) events ecologically and allow the possessor to details the grooming sequences of various quickly gather food while foraging before re- heteromyid species. Grooming frequently oc- turning to the relatively safe burrow where curs shortly after awakening, and includes appropriate dietary decisions can be made. scratching with the teeth and claws, combing Pouches also allow the animals to gather the fur and cheek pouches, and washing with large quantities of seeds when they are avail- saliva. The animals also apparently bite off able. The surplus seeds can then be stored any ectoparasites they can locate and reach and used at a later date when resources are (Vorhies and Taylor 1922, found fleas of the perhaps less abundant, thus leading to elabo- genera Ctenophthalium and Trombicula on rate caching behaviors. Even the use of a bannertailed kangaroo rats). food resource such as seeds is adaptive in a presence of a dorsal gland on many The desert setting, as seeds are rich in energy and kangaroo rats has been noted for some time, nutrients and thus require less time spent in and Quay (1953) has investigated its struc- the hostile above-ground environment, and ture. Kangaroo rats with active glands appar- seeds persist in the soil through time. ently groom the secretions over their bodies A final specialization is in degree, not kind. regularly (Griswold et al. 1977, Borchett et Heteromyids, and especially kangaroo rats, al. 1976, Randall 1981a, b). Although some of have exceptionally good hearing, which ap- the secretion on the hair may assist in reduc- parently serves them well in the desert where ing evaporative water loss (Quay 1965) or sound may travel poorly. What is particu- serve as insulation (Randall 1981a, b), too larly striking about their hearing is its appar- much is apparently detrimental and is ent fine tuning for the sounds made by two groomed off, usually by sandbathing (Randall major predators on the animals, rattlesnakes 1981a, b). and owls. Several areas of heteromyid behavior re- Summary main poorly understood or controversial. Al- though much is known about foraging behav- In many ways the behavior of desert heter- ior, several important groups of heteromyids omyids is similar to what is known about (e.g., the kangaroo mice and the large kan- other nocturnal rodents. At the level of preci- garoo rat species) are underrepresented in sion available from the current data, it ap- the literature. The ways in which differences pears that their basic ways of securing food, in foraging affect heteromyid rodent commu- courting and reproducing, and protecting nity structure are currently being hotly de- themselves from the environment and pred- bated, as are body size relationships within

ators are much like those of other rodent the family. Almost nothing is known about families (Eisenberg 1981). A few anatomical the effects of predation on rodent behavior and physiological specializations, however, and community structure, even though most

give the desert heteromyids some distinctive would agree that it is important. As tech- behavioral capacities. Certainly one is the bi- niques for behavioral observation expand, we pedal locomotion used by kangaroo rats and can expect more of the important pieces to kangaroo mice. This is rare for small mam- the heteromyid puzzle to be fitted in. mals, and it apparently is not an especially We tend to think of the desert as being an efficient means of locomotion for a small (i.e., especially harsh environment, and for hu-

low mass) animal (Biewener et al. 1981). Per- mans it is. As this chapter, and others in this haps bipedality simply provides a means of symposium, have shown, however, the desert rapid locomotion for moving through the can be much more hospitable to an animal

open to forage or avoid predators. that is adapted to its extremes. It seems safe A second feature, possessed by all hetero- to assume that most of the behaviors exhib- myids, is cheek pouches. Pouches, used for ited by desert heteromyids are in some gener- the temporary storage of seeds while forag- al or specific way tied to the physical envi- ing, grossly alter the manner in which a ronment in which they flourish. 1983 Biology of Desert Rodents 87

Bowers, M., and H. Brown. 1982. Acknowledgments J. Body size and coexistence in desert rodents: chance or community structure? Ecology 63:391-400. thanks are extended to Dr. My Robert Bradley, W. G., and R. Mauer. 1971. Reproduction Kruli, dean of the Graduate School at Kansas and food habits of Merriam's kangaroo rat, Dipo- domys merriami. State University, who provided support for J. Mammal. 52:497-507. Brown, H. 1975. Geographical ecology of desert ro- this symposium. I also thank Jim Brown for J. dents. Pages 315-341 m M. L. Cody and Dia- his efforts on behalf of the symposium, and J. mond, eds. Ecology and evolution of commu- Mary Price, Jan Randall, and Cindy Rebar nities. Harvard University Press, Cambridge, for their helpful comments. An anonymous Massachusetts. Brown, H., and G. A. Bartholomew. reviewer also provided essential assistance. J. 1969. Period- icity and energetics of torpor in the kangaroo mouse, Microdipodops pallidus. Ecology 50:705-709. Literature Cited H., Brown, J. O. J. Reichman, and D. W. Davidson. 1979. Granivory in desert ecosystems. Ann. Rev. Anderson, A. O., and D. M. Allred. 1964. Kangaroo Ecol. Syst. 10:201-227. rat burrows at the Nevada Test Site. Great Basin Butterworth, B. B. 1961. The breeding of Dipodomys Nat. 92:93-101. deserti in the laboratory. J. Mammal. 42:41.3-414. Bartholomew, G. A., and G. R. Gary. 1954. Locomo- 1964. Parental relations and the behavior of tion .35:386-392. in pocket mice. J. Mammal. juvenile kangaroo rats (Dipodomys) in captivity. Bartholomew, G. A., and H. Gaswell. 1951. Locomo- Southwest. Nat. 8:213-220. tion in kangaroo rats and its adaptive signifi- Chapman, B., and R. L. Packard. 1974. An ecological 32:1.55-169. cance. J. Mammal. study of Merriam's pocket mouse in southern Bartholomew, G. A., and R. E. MacMillen. 1961. Ox- Texas. Southwest. Nat. 19:281-291. ygen consumption, estivation, and hibernation in Chew, R., and B. B. Butterworth. 1964. Ecology of ro- the kangaroo mouse, Microdipodops pallidas. dents in Indian Cove (Mojave Desert) Joshua Physiol. Zool. .34:177-183. National California. Tree Monument, J. Mam- Behrends, p. 1981. Gopulatory behavior of Dipodomys mal. 45:203-225. microps (Heteromyidae). Southwest. Nat. Clark, W. H., and P. Comanor. 1973. The use of west- 25:,562-563. ern harvester ant, Pogonomyrmex occidentalis Benson, S. B. 19.33. Goncealing coloration among some (Cresson), seed stores by heteromyid rodents. desert rodents of the southwestern United States. Occas. Papers Biol. Soc. of Nevada .34:1-6. Univ. California Publ. Zool. 40:1-70. CoMPTON, L. v., and R. F. Hedge. 1943. Kangaroo rat Benson, S. 1935. protective habit of Dipodomijs A burrows in earthen structures. J. Wildl. Mgt. deserti. 16:67-68. J. Mammal. 7:306-316. Best, T. 1972. Mound development by a pioneer popu- of habitat quality of diets of Congdon, J. 1974. Effect lation of rats, bannertailed kangaroo Dipodomijs three sympatric species of desert rodents. J. spectabalis baileiji Goldman in eastern New Mex- Mammal. 55:659-662. ico. Amer. Midi. Nat. 87:201-206. CsuTi, B. 1979. Patterns of adaptation and variation in Biewener, a., R. M. Alexander, and N. C. Heglund. the Great Basin kangaroo rat (Dipodomys mi- 1981. Elastic energy storage in the hopping of crops). Univ. California Publ. Zool. 111:1-69. kangaroo rats Zool. of the natural his- {Dipodomijs spectabalis). J. Culbertson, a. E. 1946. Observations 195:.369-383. tory of the Fresno kangaroo rat. J. Mammal. Blair, W. F. 1937. Burrows and food of the prairie 27:189-203. 18:188-191. P. Bahrends. 1980. Factors pocket mouse. J. Mammal. Daly, M., M. Wilson, and 1943. Populations of deer mice associated with affecting rodents' responses to odors encountered small mammals in the mesquite areas of south in the field: experiments with odor-baited traps. New Mexico. Cont. Lab. Vert. Biol., Univ. Mich. Behav. Ecol. and Sociobiol. 6:323-329. 21:1-40. B., A. Woodbury. 1956. Ord's Day, H. J. Egoscue, and Blaustein, a., and a. Risser. 1974. Dominance rela- kangaroo rat in captivity. Science 124:485-486. tionships of the dark kangaroo mouse (Micro- Denyes, H. a. 1954. Habitat structure and the digging

dipodops megacephalus) and the little pocket ability of certain pocket mice. J. Mammal. mouse (Pewgnathus longimembri.s) in captivity. 35:45.3. Great Basin Nat. 34:312-316. Dewsbury, D. 1972. Patterns of copulatory behavior in 1976. Interspecific interactions between three male mammals. Quart. Rev. Biol. 47:1-33. sympatric species of kangaroo rats (Dipodomijs). Dixon, K. L. 1959. Spatial organization in a population Anim. Behav. 24:381-385. of Nelson's pocket mouse. Southwest. Nat.

BoRCHETT, P., S. 1976. 3:107-113. J. Griswold, AND R. Branchek. 1963. behavior of heteromyid rodents. An analysis of sandbathing and grooming in the Eisenberg, J. The Zool. 69:1-100. kangaroo rat (Dipodomys merriami). Anim. Be- Univ. California Publ. desert rodents. hav. 24:347-353. 1975. The behavior patterns of in I. Prakash and P. K. Ghosh, eds. Bowers, M. 1982. Foraging behavior in heteromyid ro- Pages 189-224 desert environments. W. Junk, The dents; field Rodents in evidence of resource partitioning. J. Mammal. 63:361-367. Hague, The Netherlands. 88 Great Basin Naturalist Memoirs No. 7

radiations. Univ. of Chi- 1981. The mammalian Kaufman, D., and G. Kaufman. 1982. Effects of Press, Chicago. 610 cago pp. moonlight on activity and microhabitat use by EisENBERG, AND D. E. IsAAC. 1963. The reproduction J., rat ordii). Ord's kangaroo (Dipodomys J. Mam- of heteromyid rodents in captivity. Mammal. J. mal. 63:309-312. 44:61-67. leaves: Kenagy, G. J. 1972. Saltbush excision of hypersa- Engler, M., and R. C. Dowler. 1981. Field observa- line tissue bv a kangaroo rat. Science ' tions of mating behavior in Dipodomijs ordii. J. 178:1094-1096. 62:384-386. Mammal. 1973a. Daily and seasonal patterns of activity Fitch, H. S. 1948. Habits and economic relationships of and energetics in a heteromyid rodent commu- the Tulare kangaroo rat. Mammal. 29:5-35. J. nity. Ecology 54:1201-1219. Flake, L., C. D. Jorgensen. 1969. Invasion of a and 1973b. Adaptations for leaf-eating in the Great "trapped out" southern Nevada habitat by Pe- Basin kangaroo rat, Dipodomys microps. Oeco- rognathtis Great Basin Nat. longimembris. logia 12:,38.3-412. 29:143-149. 1976a. The periodicity of daily activity and its French, A. 1976. Selection of high temperatures for hi- seasonal changes in free-ranging and captive bernation by the pocket mouse, Perognathus kangaroo rats. Oecologia 24:105-140. longimembris: ecological advantages and energet- 1976b. Field observations of male fighting, ic consequences. Ecology 57:185-191. drumming, and copulation in the Great Basin N. 1975. Activity patterns of a desert rodent. French, rat, kangaroo Dipodomys microps. J. Mammal. Pages 225-239 in I. Prakash and P. Ghosh, eds. 57:781-785. Rodents in desert environments. W. Junk, The A. 1981. Effects Kenagy, G. J., and G. Bartholomew. Hague, The Netherlands. of day length, temperature, and green food on Frye, R. ]., AND M. L. RosENZWEiG. 1980. Clump size testicular development in a desert pocket mouse selection: a field test with two species of Di- Perognathus formosus. Physiol. Zool. 54:62-73. podomijs. Oecologia 47:323-327. T. 1980. Kenagy, G. J., and J. Enright. Animal behav- Garner, H., L. W. Richardson, and L. Felts. 1976. ior as a predictor of earthquakes: an analysis of Alimentary helminths of Dipodomijs ordii: effects rodent activitv rhvthms. Zeit. Tierpsychol. on the host population. Southwest. Nat. 52:269-284.

21:327-334. Kenagy, G. J., and D. Hoyt. 1980. Reingestion of feces in rodents and its daily rhvthmicitv. Oecologia Griswold, J., G. BoRCHETT, P. Branchek, and J. Bensko. 1977. Condition of the pelage regulates 44:403-409.

grooming behavior in the kangaroo rat {Di- Laine, H., and J. G. Griswold. 1976. Sandbathing in rats podomys merriami). Anim. Behav. 25:602-608. kangaroo (Dipodomys spectabalis). J. Mam- Hall, E. R. 1946. Mammals of Nevada. Univ. of Califor- mal. 57:408-410. L.\whon, D., and M. Hafner. 1981. Tactile discrimina- nia Press, Los Angeles. 710 pp. tory ability foraging strategies in Hall, E. R., and K. Kelson. 1959. Mammals of North and kangaroo rats pocket (Rodentia:Heteromyidae). America. Ronald Press, New York. and mice Oecologia 50:303-309. Hawbrecker, A. C. 1940. The burrowing and feeding Lemon, C. 1978. Seed size selection in heteromyids: a habits of Dipodomys venustus. J. Mammal. second look. Oecologia 35:13-19. 22:388-396. Lemon, C, and M. L. Rosenzweig. 1978. Microhabitat M. E., P. Hay, and J. Fuller. 1981. Seed escape from selection in two species of heteromvid rodents. heteromyid rodents: the importance of micro- Oecologia 33:127-135. habitat ' and seed preference. Ecology LaVick, P. 1982. Maternal response to neonate vocali- 62:1395-1399. J. zations in Ord's kangaroo rat (Dipodomys ordii). Hayden, p., Gambino, and R. G. Lindberg. 1966. J. J. Southwest. Nat. 27:122-123. Laboratory breeding of the little pocket mouse, Lockard, R. B. 1978. Seasonal change in the activity Perognathus longimembris. Mammal. J. pattern of Dipodomys spectabalis. Mammal. 47:412-423. J. 59:563-568. Hekkner, H., and B. Masterson. 1981. Hearing in R. B., S. 1971. prefer- Lockard, and J. Lockard. Seed Glires, domestic rabbit, cotton rat, feral house ence and buried seed retrieval of Dipodomys mouse, and kangaroo rat. .\ccoustical Soc. J. deserti. J. Mammal. 52:219-221. .Amer. 68:1584-1599. Lockard, R. B., and D. Owing. 1974. Seasonal variation R. HoLUENREiD, 1957. Natural history of the banner- in moonlight avoidance by bannertiiil kangaroo tailed kangaroo rat in New Mexico. Manunal. rats. J. J. Mammal. 55:189-193. .38:3.30-350. Mares, M., and D. F. Williams. 1977. Experimental Hoover, K., W. G. Whitford, and P. Flavill. 1977. support for food particle size resource allocation Factors influencing the distribution of two spe- in heteromyid rodents. Ecology 58:1186-1190. cies of Perognathus. Ecology 58:877-884. Martin, R. E. 1977. Species preference of allopatric and HiTTo, R. 1978. A mechanism for resource allocation sympatric populations of silky pocket mice. among sympatric heteromvid rodent species. Genus Perognathus (Rodentia:Heteromvidae). Oecologia 33:115-126. Amer. Midi. Nat. 198:124-136. John,son, T., and C. Jorgensen. 1981. Ability of desert Maza, B., N. R. French, and A. P. Aschwanden. 1973. rodents to find buried seeds. Home range dynamics in a population of hetero- J. Range Mgt. rodents. 34:312-314. myid J. Mammal. 54:405-425. 1983 Biology of Desert Rodents 89

P., 1979. McCuE, AND J. Caufield. Photographic docu- Reichman, O. J., and J. H. Brown. 1979. The use of tor- mentation of predation on ordii Dipodomys by por by Perognathus atnplus in relation to re- Onychomys leucogaster. Abstracts of the 59th source distribution. J. Mammal. 60:550-555. meeting of the American Society of Reichman, O. J., and D. Oberstein. 1977. Selection of Mammalogists. seed distribution types by Dipodomys merriumi M'Closkey, R. 1980. Spatial patterns in types of seeds and Perognathus ampins. Ecology 58:636-643.

collected by four species of heteromyid rodents. Reichman, O. J., and K. Van De Graaff. 1973. Seasonal Ecology 61:486-489. reproductive and activity patterns of five species 1981. Microhabitat use in coexisting desert ro- of Sonoran Desert rodents. Amer. Midi. Nat. dents: the role of population density. Oecologia 90:118-126. 50:310-315. 1975. Influence of green vegetation on desert rodent reproduction. Mammal. 53:503-506. MoNSON, G. 1943. Food habits of bannertail kangaroo J. rats in Wildl. 7:98-102. Reynolds, H. G. 1958. Ecology of Merriam's kangaroo Arizona. J. Mgt. rat on the grazing lands of MoNSON, G., AND W. Kessler. 1940. Life history notes southern Arizona. Ecology 31:456-463. on the bannertail kangaroo rat, Merriam's kan- RosENZwEiG, M. L. 1973. Habitat selection experiments garoo rat, and the white-throated woodrat in with a pair of coexisting heteromyid southern Arizona and New Mexico. Wildl. species. J. Ecology 54:111-117. Mgt. 4:37-43. 1974. On the optimal above ground activity of Morton, S., R. Hinds, and R. E. MacMillen. 1980. bannertail kangaroo rats. Mammal. 55:193-199. Cheek pouch capacity in heteromyid rodents. J. RosENZwEiG, M. L., and p. Sterner. 1970. Population Oecologia 46:143-146. ecology of desert rodent communities: body size O'DowD, D. and M. Hay. 1980. Mutualism between J., and seed husking as a basis for heteromyid coexis- harvester ants and a desert ephemeral: seed es- tence. Ecology 51:217-224. cape from rodents. Ecology 61:531-540. RosENZwEiG, L., 1969. M. AND J. WiNAKUR. Population M. 1974. Seasonal activity patterns of ro- O'Farrell, ecology of rodent communities: habitats and en- dents in a sagebrush community. Mammal. J. vironmental complexity. Ecology 50:558-572. 55:809-823. ScHEFFER, T. H. 1938. The pocket mice of Washington 1980. Spatial relationships of rodents in a sage- and Oregon in relation to agriculture. USDA brush community. Manmial. 61:589-605. J. Tech. Bull. 608. 15pp. Price, M. V. 1978. Seed dispersal preferences in co- R. L. 1967. Schmidley, D. J., AND Packard. Swimming existing desert rodents. 59:624-626. J. Mammal. ability in pocket mice. Southwest. Nat. Quay, W. B. 1953. Seasonal and sexual differences in the 12:480-482.

dorsal skin of rats B. .\. gland kangaroo (Dipodomys). J. Schmidt-Nielsen, K., Schmidt-Nielsen, and Mammal. 34:1-14. Brokaw. 1948. Urea excretion in desert rodents Cell. Physiol. 1965. Variation and taxonomic significance in exposed to high protein diets. J. sebaceous caudal glands of pocket mice (Ro- 32:361-380. dentia:Heteromyidae). Southwest. Nat. ScHREiBER, K. 1973. Bioenergetics of rodents in the 10:282-287. northern Great Basin desert. Unpublished dissertation. Univ. of Idaho, Moscow. Randall, J. 1981a. Comparisons of sandbathing and D. 1979. Foraging behavior and home grooming in two species of kangaroo rat. Anim. Schroder, G. kangaroo rat Behav. 29:1213-1219. range utilization of the bannertail (Dipodomys spectabalis). Ecology 60:657-665. 1981b. Olfactory communication at sandbathing Schroder, G. D., and K. N. Geluso. 1975. Spatial dis- rats. loci by sympatric species of kangaroo J. tribution of Dipodomys spectabalis mounds. Mammal. 62:12-19. J. Mammal. 56:363-368. Reichman, O. 1975. Relationships of desert rodent J. Shaw, W. T. 1934. The ability of the giant kangaroo rat diets to available resources. Mammal. J. as a harvester and storer of seeds. Mammal. 56:731-751. J. 15:275-286. 1977. Optimization of diets through food prefer- Smigel, B., and M. L. Rosenzweig. 1974. Seed selection ences by heteromyid rodents. Ecology in Dipodomys merriami and Perognathus penicil- 58:454-457. latus. Ecology 55:329-339. 1978. Ecological aspects of the diets of Sonoran Stamp, N., and R. Ohmart. 1978. Resource utilization Desert rodents. Mus. North. Arizona Res. Rep. 15 by desert rodents in the Lower Sonoran Desert. 96 pp. Ecology 59:700-707. 1979. Desert granivore foraging and its impact Stock, D. 1972. Swimming ability in kangaroo rats. on seed densities and distributions. Ecology Southwest. Nat. 17:98-99. 60:1085-1092. Tappe, D. T. 1941. Natural history of the Tulare kan- 1981. Factors influencing foraging in desert ro- rat. 22:117-148. garoo J. Mammal. dents. Pages 195-213 in A. C. Kamil and T. D. Thompson, S. D. 1982a. Microhabitat utilization and Sargent, eds. Foraging behavior: ecological, etho- foraging behavior of bipedal and quadrupedal logical, and psychological approaches. Garland- heteromyid rodents. Ecology 63:1303-1312. species composition of STMP Press, New York. 1982b. Structure and species assemblages: effects of Reichman, In variation desert heteromyid O. J. press. Spatial and temporal simple habitat manipulation. Ecology in seed distribution in Sonoran Desert soils. Jour, a 63:1313-1321. of Biogeography. 90 Great Basin Naturalist Memoirs No. 7

In press. Bipedal hopping and seed dispersion VoRHiEs, C. T., AND W. P. Taylor. 1922. Life history of selection by heteromyid rodents: the role of loco- the kangaroo rat Dipodomijs spectabalis spec- motion energetics. Ecology 65. tabalis Merriam. Bull. U.S.D.A. 1091-1-40.

Thompson, S. D., R. E. MacMillen, E. M. Burke, a.nd Voorhies, M. R. 1974. Fossil pocket mouse burrows in C. R. Taylor. 1980. The energetic costs of biped- Nebraska. Amer. Midi. Nat. 91:492-498. Webster, D. 1962. A fimction of the enlarged middle al hopping in small mammals. Nature ear cavities of the kangaroo rat, 287:223-224. Dipodomys. Physiol. Zool. .35:248-255. S. 1980. Effects of Trombulak, C, and G. J. Kenagy. Webster, D., and M. Webster. 1971. Adaptive values seed distribution and competitors on seed har- of hearing and vision in kangaroo rat predator vesting efficiency in heteromyid rodents. Oeco- avoidance. Brain Behav. Res. 4:310-322. logia 44:342-346. 1972. Kangaroo rat auditory threshold before Van De Graaff, K. 1973. Comparative developmental and after middle ear reduction. Brain Behav. Res. desert rodents, Pero- osteology in three species of 5:41-53. rnyscus eremictis, Perognathus intenneclius, and 1980. Morphological adaptations of the ears in merriarni. Mammal. 54:729-41. Dipodomijs J. the rodent family Heteromyidae. Amer. Zool. Van De Graaff, K., and R. P. Balda. 1973. Importance 20:247-254. of green vegetation for reproduction in the kan- T. WoNDOLLECK, J. 1978. Foragiug-arca separation and garoo rat, merriarni merriarni. Dipodomijs J. overlap in heteromyid rodents. J. Mammal. Mammal. .54:509-512. 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 knowledge 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. interspecific interactions leading to habitat specialization. Genetic Structure: Despite a number of studies on desert rodent systeniatics, little is known of the genetic structure of desert rodent populations. Behavioral, demographic, indirect genetic, and direct genetic evidence can be used to detect deviations from panmixia.

Although desert rodents have been the sub- More recently studies have focused on inter- ject of hundreds of studies on a number of actions among rodent species. In addition to levels (e.g., physiology, behavior, population discussing these factors, we consider pre- ecology, community ecology, and system- dation and parasitism and argue that both are atics), it is not yet feasible to make general worthy of study, although little evidence ex- conclusions as to the relative importance of ists concerning their importance. various factors in determining the abundance, distribution, and genetic structure of popu- Food and Water lations of desert rodents. This article is de- signed to help remedy this problem. We con- Perhaps the best-documented pattern of sider the possible importance of each of a desert rodent abundance is increased popu- number of factors, reviewing the relevant lit- lation growth and reproduction following erature to determine what is known at pres- rainfall and the growth of plants, particularly ent, then suggesting ways in which the gaps annuals. This pattern has been shown to hold in our knowledge can be filled. for many rodent species in many geographi- With few exceptions, we have limited our cal areas (Reynolds 1958, Chew and But- treatment to the nocturnal rodents that in- terworth 1964, Beatley 1969, Bradley and habit the deserts of North America. In addi- Mauer 1971, Van de Graff and Balda 1973, tion, much of our treatment concerns rodents Newsome and Corbett 1975, O'Farrell et al. of the family Heteromyidae, a bias that re- 1975, Reichman and Van de Graff 1975, sults in large part from the greater amount of Whitford 1976, Dunigan et al. 1980, Petrys- work done on that group relative to other zyn 1982). The exact timing of rainfall is at groups. least as important as the total amount. Both Beatley (1974) and Petryszyn (1982), working Abundance and Dynamics in deserts with very different precipitation Discussion of factors affecting the abun- patterns, have shown that rainfall early in dance and dynamics of desert rodent popu- winter is important in germination and early lations has, in the past, centered on the im- growth, and rainfall in the spring is necessary portance of food, water, and vegetation. for further growth and flowering.

Brigham Young 'From tlie symposium "Biology of Desert Rodents," presented at the annual meeting of the American Society of Mammalogists, hosted by 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 to distinguish among the relative importance account for this apparent dependence of ro- of water, energy, and nutrients (all of which dent populations on plant growth; all are are more available following favorable based primarily on reproductive responses to weather conditions) in leading to population external factors, not on effects on survivor- increases of desert rodents. ship. First, Chew and Butterworth (1964) Several studies and observations, other suggested that rodents may consume hormon- than the above correlative studies that led to al substances within the plants that initiate the formulation of these hypotheses, bear on reproduction. Such a triggering mechanism this question. Breed (1975) showed that water has been demonstrated for microtines (Berger deprivation resulted in reduced reproductive et al. 1981 and refs. therein). Second, Chew activity in female Australian hopping mice and Butterworth (1964) and Van de Graaff {Notomys alexis), as measured by ovarian and and Balda (1973) found that rodents gained uterine weights and follicular development. weight at times of plant growth or in areas In another laboratory experiment, Yahr and where green vegetation was present and ar- Kessler (1975) found that reproductive activi- gued that ingesting green vegetation im- ty ceased in Mongolian gerbils {Meriones proves general body condition, enabling indi- iinguicidatus) that received lettuce only once viduals to reproduce. Third, Beatley (1969), a week but continued in control animals that Bradley and Mauer (1971), and Reichman received daily lettuce rations. In this study, and Van de Graaff (1975) found an increased the effect of water and nutrient availability availability or consumption of green vegeta- are confounded because lettuce may contain tion during or prior to reproduction and ar- required nutrients as well as water. Soholt gued that water and vitamins in the plants (1977) found that free water intake in lactat- are necessary to compensate for increased de- ing Dipodomys merriami increased by more mands during gestation and lactation. Defi- than 200 percent over that of non- ciencies in vitamins (such as A or E) can lead reproductive females, though gestating fe- to sterility or fetal death (Wright 1953). Fi- males exhibited no increase. However, be- nally, based on the common trend that in- cause carrots were used as the source of free creased growth of annuals is a prelude to in- water, it is not possible to distinguish be- creased availability of seeds and insects, tween the importance of water and any nu- O'Farrell et al. (1975), Reichman and Van de trients that carrots may contain. Further- Graaff (1975), Whitford (1976), and Dunigan more, these experiments do not demonstrate et al. (1980) suggested that increased repro- an absolute need for free water during lacta- duction may depend on increased food tion because females were not actually de- availability. prived of free water; they simply showed an The problem of distinguishing among these increase in water use. hypotheses can be made more tractable if we Two studies have shown a correlation be- recast them to reflect requirements that are tween the density of Neotoma populations common to all animals: water, energy, and and the local abundance of Opuntia cactus nonenergetic nutrition (simply termed nutri- (Brown et al. 1972, Cameron and Rainey

tion below; includes essential fatty acids, 1972, Olsen 1976), although it is unknown amino acids, vitamins, and minerals). First, whether the correlation is due to increased the "hormonal substances" hypothesis is food and water availability or to increased probably based on a proximate mechanism. protection against predators (woodrats often Rodents should not come to rely on an exter- used cactus joints in constructing nests; nal cue, such as a hormonal substance, unless Brown et al. 1972). In addition, Petryszyn that cue is tied to some ultimate benefit such (1982) found that N. alhigula densities failed as water, energy, or nutrients. Second, in- to respond to a single winter of higher than creased "general body condition" is probably average rainfall, but did respond to two con- due to the increased availability of water, secutive good years. This can be interpreted energy, and/or nutrients. Finally, "increased to indicate that the abundance of annual food availability" confounds the effects of plants (which would respond to a single good energy and nutrition. The problem, then, is winter) does not limit woodrat populations 1983 Biology of Desert Rodents 93 but the growth of perennial plants (which There are several reasons for this. First, spe- perhaps only respond to consecutive good cies of desert rodents may vary in their re- years) may limit woodrat populations (Petrys- quirements. This is illustrated by Christian's zyn pers. comm.). (1979a) finding that three species of Namib By providing a source of supplemental wa- Desert rodent responded in different ways to ter, Christian (1979a) was able to cause an in- the addition of water. It is apparent that crease in reproductive activity in two species physiological differences among species must and increased density in one species in a l3e considered when assessing the effects of community of three species of Namib Desert various factors on abundance. rodents. The species most ecologically similar Second, geographical differences in the to North American heteromyids because of stressfulness of the environment may be im- its superior ability to conserve water {Desmo- portant. For example, all studies that showed dillus aurictilaris; Christian 1979b) was little population responses not tied to increased affected; Christian (1979a) argued that fac- water availability were carried out in rela- tors other than the availability of water de- tively benign (with respect to water stress) environments: south central termine its population size. The two species Washington (O'Farrell al. more similar to North American desert crice- et 1975), Chihuahuan Desert above 1000 elevation tids or sciurids (they are poorer at water con- m (Whitford 1976, Munger, in preparation), servation than D. aiiricularis; Christian Brown and and short grass prairie (Abramsky 1978). 1979b) did respond to supplemental water, The studies that showed an apparent reproduc- indicating that the availability of water is im- tion dependence on free water were carried portant in determining the abundance of out in the more stressful lower Sonoran these species. Desert, Mojave Desert, and Namib Desert. Two observations indicate that availability To resolve this problem, water and food ad- of green matter and the water or nutrients dition experiments should be performed in contained therein are not a requisite for re- the harsher lower deserts as well as in the production. O'Farrell et al. (1975) found that relatively benign higher deserts. female Perognathus parvus sometimes re- Third, insects, whose populations often remained lactating for more than a month after spond to increased plant growth, may pro- vegetation had dried up; vegetation may vide a source of moisture for several months have been required for initiation of reproduc- after annual plants have died. tion, but not for lactation. Whitford (1976) Finally, although these hypotheses have observed a population increase during a year been couched in terms of the effects of vari- in which there was virtually no growth of ous factors on reproduction, these same fac- green matter. tors are likely to affect survivorship as well. The importance of energy or nutrients is Probably because of the energetic and nutri- indicated by two studies in which seeds were tive demands of reproduction, survivorship of added to experimental plots. Addition of breeding adults tends to be negatively associ- seeds to plots in short grass prairie caused an ated with the degree of reproductive activity invasion of seed-eating Dipodomys ordii (French et al. 1974, Conley et al. 1977) and (Abramsky 1978). Addition of seeds to plots thereby negatively correlated with the in the western Chihuahuan desert caused a amount of rain-induced plant growth (Chris- threefold increase in numbers of the largest tian 1980). Juvenile survivorship, on the species at the site (D. spectabilis) but a slight other hand, should be increased by the in- decrease in of smaller species numbers creased availability of food and water. This (Brown and Munger, in preparation). pattern was found by Whitford (1976). who The results of the studies discussed here in- showed that the survivorship of young heter- dicate that it is unlikely that variation in a omyids was much lower in a year with a poor single factor, whether it be water, energy, or seed crop than in years with good crops. In- nutrients, will be able to account for all situa- creased juvenile survivorship may have con- tions where desert rodent population in- tributed directly to increased densities shown creases are correlated with bouts of rainfall. by the studies cited above, or indirectly via 94 Great Basin Naturalist Memoirs No. 7

reproduction in adults: increased probability amount of evidence, much of it indirect, ar- of survivorship of young during years of high gues that food is limiting for many species of plant growth and subsequent plant avail- desert rodents, especially granivorous species. ability may be the ultimate factor that leads As discussed above, increases in population adults to reproduce in those years (Reichman density follow periods of high precipitation and Van de Graaff 1975). and seed production (Reynolds 1958, Beatley

As noted above, desert rodent populations 1969, 1976, French et al. 1974, O'Farrell et appear to be strongly influenced by the al. 1975, Whitford 1976, Dunigan et al. 1980, growth of plants following sufficient rainfall. Petryzsyn 1982), and invasions or population

One might ask then whether it is necessary to increases of seed-eating rodents follow the even consider factors other than food and addition of seeds (Abramsky 1978, Brown and water, since the availability of water, energy, Munger, in preparation). In addition, den- and nutrients seems to explain a large part, if sities of seed-eating rodents increased in re- not all, of the variation in desert rodent sponse to the removal of ants (Brown and abundance. We strongly feel that other fac- Davidson 1979) and, along a geographic tors should be considered, if only to rule gradient of increasing precipitation and pro- them out. Below we describe a series of stud- ductivity, population density, biomass, and ies on desert annual plants that illustrates the species diversity of seed-eating rodents tend need to consider other factors. to increase (Brown 1973, 1975). Furthermore,

The abundance of desert annual plants is, woodrat populations appear to be limited by as mentioned above, dependent on the pat- the amount of green matter available to them tern and amount of rainfall. Other factors (Brown et al. 1972, Cameron and Rainey have been shown to be important as well. 1972, Olsen 1976). First, intraspecific evidence appears to limit A number of studies indicate the probable the number of seeds that germinate (Inouye importance of rodent-rodent interactions. 1980). Second, large-seeded species of annual Cameron (1971) concluded that, where the plants appear to be able to outcompete two species are sympatric, Neotonia fuscipes N. their small-seeded species, but seed predators (es- excludes lepida from preferred food pecially rodents) apparently prefer larger plant. Frye (in press) showed experimentally that merriami were excluded seeds. Rodents decrease the abundance of Dipodomys from seed resources near the mounds of the large-seeded species, thereby indirectly in- larger D. spectahilis. A number of authors creasing the abundance of small-seeded spe- have shown that desert rodents differentially cies (Inouye et al. 1980). And third, if large- utilize microhabitats (Brown and Lieberman seeded species do attain high densities (as 1973, Brown 1973, 1975, Lemen and Rosenz- they do in rodent exclosures) they are subject weig 1978, Price 1978a, Wondolleck 1978) or to attack by a parasitic fimgus that causes a habitats (Rosenzweig 1973, Schroeder and large decrease in fecundity (Inouye 1981). Rosenzweig 1975, Hoover et al. 1977, War- With this example in mind, we proceed to ren 1979). That this differential use is caused consider the importance of interspecific in- by interspecific interactions is indicated by teractions, predation, and parasitism in deter- studies that have shown a shift in micro- mining the abundance of desert rodents. habitat use as a result of experimental removal (Price 1978a, Wondolleck 1978) or a natu- Interspecific Interactions ral lack (Larsen 1978) of putative competitor species. In addition, although food may not A population of a given species of desert be the basis of the response, the granivorous rodent does not live in the absence of other D. ordii expanded its microhabitat use in re- organisms. In the following section, ad- we sponse to removal of the omnivore Onych- dress the possible importance of interspecific omys leucogastcr (Rebar and Conley, in prep- interaction in determining the abundance of aration). Exclusion of one species by another desert rodents. from a preferred resource or microhabitat For competition among species to occur, can potentially lead to a reduction in popu- some resource must be limiting. A substantial lation size for the former species. 1983 Biology of Desert Rodents 95

Removal experiments that measure mimer- may be that the interaction between similar- ical response are even stronger evidence of sized species has been sufficient, over evolu- the importance of interspecific interaction. tionary time, to discourage utilization of a Unfortrmately, few such studies have been common set of resources (see discussion un- done. Schroeder and Rosenzweig (1975) per- der habitat selection). formed reciprocal removals of D. ordii and D. Second, by examining the bases of these in- merriami but found that neither species re- teractions in detail, a great deal can be learned sponded to removal of the other. Munger and about their impact on population dynamics. For what resource are these rodents Brown (1981) found a 3.5-fold increase in the competing? Does the interaction involve ex- population density of small granivorous ro- ploitation or interference competition? dents following the absolute removal of three species of Dipodomys. In a third study, Eide- miller (1982) performed reciprocal removals Predation of the herbivorous Neotoma lepida and the granivorous Perognathus fallax. Three species The most direct way to assess the effect of of omnivorous Peromyscus responded with a predation on desert rodent populations is to twofold increase to N. lepida removal but remove predators then measure any response failed to respond to P. fallax removal. The re- there may be in the abundance and distribu- sponse of N. lepida to the removal of P. fallax tion of the rodents. Much information about and the reciprocal response were minor. predator-prey interactions can also be gath- To further assess the importance of inter- ered through detailed observations of popu- specific interactions, more removal experi- lation numbers, distribution, and behaviors of ments must be performed. To be of value, predators and prey as shown by what is un- these experiments must be properly repli- doubtedly the most complete study of the ef- the cated; a surprising number of studies appear- fects of predation on population dynamics of a small mammal: the work of Errington ing in the literature lack experimental rep- (1943, 1946) on muskrats {Ondatra zibethica) lication (Hayne 1975). and their primary predator, mink {Mustela A number of questions can be addressed vison). Unfortunately, no study approaching with these studies. First, how general are the this quality has been performed on desert ro- results of the experiments discussed here? An- dents and their predators (perhaps because other, is the result affected by the identity of much of their activity is nocturnal); there- the species studied, by the habitat in which fore, we must rely primarily on indirect evi- the study was conducted, by the presence of dence in this section. other competitor or predator species (which Errington's work illustrates a further point: may be affected by historical factors such as the scale on which the results ar- viewed colonization events or ecological bot- drastically affects the interpretation. Al- tlenecks), by the season in which the study though large numbers of muskrats are killed was performed, or by the temporal pattern of by mink and other predators, Errington resource availability? One tenuous pattern (1946, 1956) argued that predation is over- is similar-sized species that emerges that rated as a factor controlling muskrat popu- (Schroeder failed to respond to removals and lations. Instead, he argued that population dissimilar-sized Rosenzweig 1975), whereas size is controlled by the availability of terri- species responded to removals (Munger and tories; predation primarily affects the surplus Brown 1981; although this was not true in all individuals (those without territories) of a cases for Eidemiller 1982). Such a general- population and is only one of a number of ization contradicts other studies that suggest factors that affect surplus animals of the pop- that the intensity of pair-wise interactions ulation. Although he may be correct that ter- among granivorous rodents increases with ritory number limits population numbers and body-size similarity (Brown 1973, 1975, density within a marsh, it is predation that Brown and Lieberman 1973, Mares and Wil- makes areas outside the marsh unsafe, ulti- liams 1975, Bowers and Brown 1982). As dis- mately limiting the number of territories that presence of cussed by Schroder and Rosenzweig (1975), it can be safely occupied. If it is the 96 Great Basin Naturalist Memoirs No. 7

mink that prevents muskrats from success- The effect of other factors, such as produc- fully colonizing areas near the marsh (where tivity, competition, and parasitism, may be

food and water are accessible), then pre- manifest primarily through predation. It is dation would have to be considered to be a likely that a decrease in productivity, an in- factor important in limiting distribution and crease in competition, and an increase in par- therefore total population size of muskrats. asitic load will all require rodents to spend On a within-habitat scale, predation appears more time foraging to meet energetic re- to be imimportant. On a between-habitat quirements. This, in turn, will increase their scale, it may contribute substantially to the exposure to predators, and potentially di- limitation of the population. rectly affect abundance.

Errington's studies illustrate both a direct It is somewhat easier to examine indirect effect (increased death rate: those individuals effects of predation because these often in- that do not possess safe territories are often volve morphologies and behaviors that may killed) and an indirect effect (habitat selec- be more easily studied than density effects. tion: given a choice, muskrats will selectively Behaviors and morphologies that lead to a re- live in habitats that are relatively safe) of duction in the probability of being killed predation on abundance and distribution. In should evolve in desert rodents. If these be- desert rodent populations, direct effects of haviors and/or morphologies are costly or re- predation have yet to be demonstrated, duce resources available to a population (for though a number of studies have shown that example by restricting foraging to certain mi- desert rodents are, in fact, killed by a number crohabitats), then predation can potentially of predators, e.g., owls, carnivores, and have an indirect effect of lowering popu- snakes (French et al. 1967, Egoscue 1962, lation size. Webster and Webster 1971, Lay 1974, Ryck- Several studies indicate that one indirect man et al. 1981, Munger, pers. obs., Jones, effect involves microhabitat selection. Quad- pers. obs.). rupedal desert rodents forage substantially French et al. (1967) tried to estimate the more under and around bushes than out in direct effect of kit fox (Vulpes macrotis) pre- the open (Brown and Lieberman 1973, Ro- dation on the survivorship of desert rodents senzweig 1973, Price 1978a, Wondolleck by comparing longevity (which included loss 1978, Thompson 1982a). Though this may be by emigration) in unfenced populations (sub- due in part to differences in resource avail- ject to losses by emigration and predation by ability (Reichman 1975, Brown et al. 1979a), kit foxes and other predators such as snakes) a number of authors have argued that these with longevity in fenced populations (from rodents favor bush microhabitats to avoid at- which kit foxes were excluded and out of tacks by visually oriented predators (Rosen- which emigration was not possible). The ef- zweig 1973, O'Dowd and Hay 1980, Thomp- fect of emigration (measured in another study son 1982a, Kotler, in press). at 25 percent per year) was subtracted from Four studies provide experimental evi- the sum of all effects on longevity of the dence consistent with the notion that pre- fenced population. They concluded that kit dation importantly affects microhabitat selec- fox predation was unimportant in affecting tion. Thompson (1982b) was able to increase longevity, though predation by other pre- the density of quadrupedal rodents in an area dators may have been important. Although by constructing artificial shelters in the open this approach was novel, it suffers an impor- spaces between bushes. By increasing the tant flaw: the calculations of French et al. amount of cover available, the shelters may (1967) are overly sensitive to the values en- have allowed the rodents to utilize areas they tered into their equations. For example, a de- previously avoided, resulting in an increased crease in the emigration value used from 25 population size. Because measures of seed to 24 percent results in a sixfold increase in density failed to show any effect by the shel-

the apparent importance of kit fox predation. ters on resource distribution, it is unlikely Since no confidence intervals are given for that the density increase was caused by any of their values, the exact importance of changes in the resource base. Rosenzweig this sensitivity is unknown. (1973) decreased the number of Perognathus 1983 Biology of Desert Rodents 97 penicillatus captured by experimentally re- Several other studies indicate that pre- moving shrubby vegetation. The rapidity of dation may be an important selective force in the response indicates that it is unlikely that desert rodents. First, timing of foraging activ- the rodents were responding to a change in ity is sensitive to moonlight; presumably in- resources. O'Dowd and Hay (1980) showed creased light increases the probability of that the probability that desert rodents ex- being preyed upon (Lockard and Owings ploit artificial seed patches varies with the 1974, Rosenzweig 1974, Kaufman and Kauf- distance of those seeds to the nearest bush man 1982). Second, individuals of the island- dwelling (presumably a measure of the danger of being Neotoma lepida latirostra spend more time away from the nest preyed upon) but not with the quality of and travel in more open areas than their mainland those patches. counterparts, presumably due to a lack of The results of these three studies are open predators on the island (Vaughan and to an alternate explanation. The ultimate rea- Schwartz 1980). Third, desert rodents in sev- son that quadrupedal rodents prefer bushy eral families possess auditory and locomotory microhabitats may be that bushes have been specializations (Bartholomew and Caswell associated (over evolutionary time) with par- 1951, Webster 1962, Webster and Webster ticular resource distributions and are present- 1975, Lay 1972) that have shown to be im- ly used rodents as cues favor- by proximate to portant in aiding these rodents in avoiding able resource patches. In the studies of attacks of predators (Webster and Webster Rosenzweig (1973) and Thompson (1982b), 1971). These rodents also possess pelages the rodents may have responded to changes which match the substrate on which they oc- in the proximate cue even though the ulti- cur (Dice and Blossom 1973). It should be mate factor remained unchanged. The oppo- noted, however, that demonstrating the im- site may have occurred in the study of portance of predation on the evolution of be- O'Dowd and Hay (1980): the rodents may havioral and morphological traits does not have failed to respond to changes in the ulti- demonstrate its importance in affecting abun- mate factor (seeds) because there was no dance and distribution. change in the proximate cue. Obviously, much work needs to be done By manipulating a factor other than micro- before the importance of predation can be habitat, Kotler (in press) avoided this prob- assessed. Indirect studies need to be bolstered lem. He reasoned that, because many pred- by determining whether the ultimate factor ators of nocturnal desert rodents rely on responsible for such behaviors as avoidance visual cues, the rodents should use the of open microhabitats is based on resource This task amount of illumination in the environment to distribution or predator avoidance. difficult if behaviors are inflexibly assess their risk of being preyed upon. Using will prove tied to proximate cues. Studies that measure artificial light sources, Kotler experimentally the direct effect of predation on abundance increased the amount of illumination, causing and local distribution should be attempted as four of the six species at his study site to re- well, perhaps using island systems (cf. duce their use of open habitats, indicating Vaughan and Schwartz 1980) or areas where that the utilization of microhabitats by these predators have been subjected to control species is sensitive to the risk of being preyed programs. upon. It is interesting to note that one species, D. deserti, responded to increased light only when resources in bushy microhabitats Parasitism were augmented, indicating that resource availability and risk of predation may inter- The role that parasitism may play in af- act in affecting behavior. The two remaining fecting the abundance and distribution of species made little use of open microhabitats desert rodents has been given little consid- prior to experimental treatment; a decrease eration, even in comparison with the small in the use of open areas by these species amount of attention given predation. There would therefore be difficult to cause or are several reasons for this. First, antiparasite detect. adaptations (such as immune response) are 98 Great Basin Naturalist Memoirs No. 7

not easily recognized and the effects of para- ing discussion is based on Anderson and May, sites are often indirect and subtle. Second, 1982a). because it is difficult to manipulate parasite The reproductive rate (and therefore fit- loads under field conditions, it is not easy to ness) of a parasite is governed by three fac- study the importance of parasites. Third and tors. A higher reproductive rate will result perhaps most important, biologists often be- from (all else being equal): higher probability lieve that parasites have little ecological im- of infection in an iminfected host when en- portance (but see Price 1980 and Anderson countered by an infected host (higher trans- and May, 1982a). This is based on the notion mission rate), lower rate at which a host re- that parasites should evolve to minimize their covers from a parasitic infection (lower their its host, effect on hosts: by damaging a recovery rate), and lower probability that a reduce its parasite would supposedly chances host dies as a result of an infection (lower of reproducing. virulence). If the reproductive rate of a para- In arguing that parasites are worthy of site depended solely on its virulence, but if consideration in the population biology of virulence was not tied to the transmission desert rodents, we will consider two ques- rate or recovery rate, it would be reasonable tions. First, how might parasites affect abun- to expect the parasite to evolve to have a dance and distribution and, second, what is negligible effect on the host. However, these the evidence that parasites can be important parameters are interrelated, at least in some in affecting abundance and distribution? For systems. In the myxoma virus-rabbit system this latter question, we consider a number of for instance, hosts infected with more viru- systems outside desert rodents as well as re- lent strains of virus had a slower recovery viewing the meager evidence pertaining to rate and a higher transmission rate than hosts desert rodents. infected with strains of low virulence (Ander- Parasites (which we consider here to in- son and May, 1982a). Given the character of clude viruses through parasitic arthropods) these interrelationships, parasites should can affect abundance both by lowering survi- evolve to some intermediate rate of viru- vorship and by consuming energy that might lence, low enough to prevent a premature otherwise go to host reproduction, thereby death of the host but high enough to retard reducing fecimdity. Anderson and May (1978, recovery and facilitate transmission. This is 1979, 1982b), Anderson (1978), and May and what has happened in the myxoma- rabbit Anderson (1978, 1979) provide excellent dis- system (Fenner and Ratcliff 1965, Anderson cussions of the dynamics of parasite and host and May, 1982a). The virus introduced was populations. They argue that the ability of a extremely virulent; nearly 100 percent of the parasite to regulate a host population is en- infected rabbits died quickly. Eventually the hanced by factors that promote the stability stabilized that the preva- of the parasite-host dynamics, such as over- system such most viral strains dispersion of parasites, density-dependent re- lent were of neither very high straints on the growth of parasites within nor very low virulence, but somewhat inter- hosts, and a nonlinear relationship between mediate in their effect. parasite burden and host death rate. They do Studies of the effect of parasites on small not mention another very important stabiliz- mammal hosts are relatively rare. In addition, ing factor: the presence of a second host spe- a number of these studies have questionable cies that does not suffer pathological effects worth in assessing the importance of parasites from infection— a reservoir for the parasite in natural situations. First, some studies use (Baltazard et al. 1952, cited in Nelson 1980). laboratory animals as hosts, a practice that Reservoir hosts may be especially important ignores the importance of coevolution of par- in affecting distribution (see discussion asites and their hosts. Second, many studies below). are correlative: a measure of host condition is If parasites are to be important in regu- tied to parasite load. Such correlative studies lating the abundance of the host, they must do not allow us to assign cause, since some maintain enough virulence to reduce the sur- other factor, such as poor nutrition, may have vivorship or fecimdity of the host (the follow- led to both poor condition and high parasite 1983 Biology of Desert Rodents 99 load. Laboratory studies that utilize experi- Two strategies of study can increase our mental variations in parasite load will allow knowledge of the importance of parasitism in us to assess the effect of parasites on survivor- desert rodent populations. First, laboratory ship and fecundity. Only by performing field studies utilizing wild rodents and their natu- studies in which parasite loads are manipu- ral parasites can be used to make precise lated on the scale of the population will we quantitative measures of the effect of parasite know if the effects of parasites on survivor- loads on parameters important to the demog- ship and fecundity translate into actual ef- raphy of a population. Second, field studies fects of population regulation. For illustra- should be attempted in which internal parasite loads are tive purposes, we will list several examples of manipulated by administering apparent importance of parasites on de- the appropriate drug to a portion of a population and external parasites are mographic parameters of mammals (other ex- manipulated, perhaps at burrow sites, using techniques amples can be found in Davis and Anderson used to control the ectoparasites of domestic 1971, and Price 1980): Infections of Per- animals (e.g., flea collars). Such studies should omysctis leucopus by Cuterebra fontinella yield further information on the effects of (bot fly) are correlated with reduced hemato- parasitism demographic parameters and, per- crit (Childs and Cosgrove 1966); delayed fe- haps, on the effect of parasitism on rodent male maturity, delayed litter production, and abundance. reduced male fertility (Cranford 1980); they may also cause reduced size of reproductive organs in subadult males, but have no dis- Distribution cernible effect on the size of adult reproduc- In this section, address tive organs (Timm and Cook 1979). Epizoot- we two basic questions. First, what factors are important in de- ics occasionally decimate populations of fining the geographic ranges of desert ro- Ondatra zibethica (Errington 1954). In- dents? Second, within the range of a species, fections by lungworms {Protostrongijlus spp.) why doesn't that species occur ubiquitously are thought to be very important in decreas- over all habitats? That is, what factors lead to ing siuA'ivorship in bighorn sheep in North patterns of local distribution? As will be seen, America (Forrester 1971). many of the factors important in determining What evidence exists that the abundance abundance should also affect patterns of local of desert rodents may be affected by para- geographic distribution. sitism? Numerous studies have shown that After a brief discussion of physical barriers, desert rodents are often infected by a number we will address the importance of three of parasites—plague virus, nematodes, ces- abiotic factors (temperature, moisture, and todes, spirochaetes, mites, fleas, and ticks substrate) and four biotic factors (vegetation, (Eads and Hightower 1952, Read and Mille- competition, predation, and parasitism) to lo- man 1953, Grundinan 1957, 1958, Reisen and cal and geographic distribution. It is common Best 1973, Bienek and Klikoff 1974, King and for two or more factors to interact in a syner- Babero 1974, Whitaker and Wilson 1974, gistic manner. In the discussion below, the O'Farrell 1975, Egoscue 1976, Garner et al. most common example of synergism is the in- 1976, Maser and Whitaker 1980, Ryckman et teraction of temperature, moisture, and sub- al. 1981). However, to our knowledge, very strate to produce patterns in the distribution few studies have mentioned the effects of of vegetation, which in turn appears to affect these parasites on their hosts. Garner et al. the distribution of desert rodents. (1976) indicated that Dipodomijs ordii individuals infected with cestodes had a reduced amount of axillary and groin fat. Several Physical Barriers studies of gastric parasites have noted that the stomach of the host appears distended, ir- Physical barriers (e.g., habitat dis- ritated, or simply filled with parasites (Gar- continuities, mountain ranges, rivers) often readily ner et al. 1976, Grundman 1958, King and persist over long periods of time, are Barbero 1974). No study has assessed the ef- discernible, and, for desert rodents, can be fect of parasitism on population size. put on maps (e.g., Hall 1946, Durrant 1952, 100 Great Basin Naturalist Memoirs No. 7

Hall and Kelson 1959, Hall 1981). In general important in creating barriers to dispersal these barriers represent both the proximate and, ultimately, could be used to account for and ultimate factors that circumscribe the the distribution of Dipodornys in California. geographic distributions of species. The observations that D. merriami has rela- Hall (1946), Durrant (1952) and, more re- tively little ability to regulate body temper- cently, Brown (1973, 1975), and Brown and ature (Dawson 1955) and that the northern

Lieberman (1973) noted striking differences extent of its distribution is coincident with in the composition of rodent communities in the 30 F isotherm for average January tem- the eastern and western Great Basin desert. peratures (Reynolds 1958) suggests that low They suggested that eastern Great Basin winter temperatures may limit the range of desert communities are depauperate and that this species to warm desert habitats. Gaby orographic barriers limited certain spe- have (1972) found that D. merriami (an inhabitant cies (e.g., D. deserti, D. merriami, Micro- of low, hot deserts) and D. ordii (which tends dipodops pallidus) to western habitats. Phys- to inhabit higher, cooler deserts) have inter- ical barriers often can be invoked to account specific differences in temperature- for the limits of spatial distribution on at dependent metabolic rates that correspond to least one range boimdary of many desert het- the different requirements of their ranges. In eromyid, cricetid, and sciurid species in these experiments D. ordii was less tolerant of North America (Hall and Kelson 1959, Hall high temperatures than D. merriami; D. mer- 1981). Besides orographic barriers, rivers ap- riami had a higher metabolic rate at low am- pear to play a significant role in limiting the bient temperatures. Unfortunately, it is un- distribution of populations of a species. clear what role these intrinsic differences Range boundaries of Perognathus formosus, play in affecting geographic distributions. P. spinatus, P. penicillatus, P. intermedins, The question becomes one of cause and ef- Ammospennophilus leucuriis, and A. harrisii fect: are D. merriami populations limited to are partially coincident with the Colorado warm desert regions because they are unable River. The high frequency with which phys- to cope physiologically with colder temper- ical barriers limit species' distributions cor- atures, or are the metabolic differences be- roborate other empirical data that suggest tween these kangaroo rats merely a result of that mammals are relatively poor dispersers local adaptation to contrasting environmental across imsuitable habitats (Carlquist 1965; conditions? Brown 1971, 1975). Physiological research has long demonstrated, through the study of functional adap- Abiotic Factors: tations, the high premiums placed on water Temperature, Moisture, Substrate conservation for rodents in desert habitats Abiotic factors that vary in a continuous or (Howell and Gersh 1935, Schmidt-Nielsen et mosaic manner are also important in circum- al. 1948, Schmidt-Nielsen and Schmidt- scribing geographic ranges and affecting lo- Nielsen 1951). More recently, negative effect cal distribution, although their effects are of increased ambient temperature on water usually more subtle than those of the highly balance has been elucidated (MacMillen and visible physical barriers just discussed. In Christopher 1975). Beatley (1969a, 1976) many situations, cause and effect relation- noted that a species must necessarily be lim- ships may be confounded by synergistic inter- ited to areas where positive water balance (a actions among variables and by an inability hinction of interaction of temperature, avail- to distinguish proximate from ultimate fac- able moisture, and the physiology of the spe- tors. In the next section, we first discuss how cies in question) can be maintained. single abiotic factors can limit distributions, Howell and Gersh (1935) first quantified then deal with the problem of synergism. the urine-concentrating capacities of Di- Correlations between the distribution of podomijs and found substantial interspecific desert rodent species and various measures of variation. That this capacity at least corre- temperature have been reported in the liter- sponds to distribution is indicated by studies ature for many years. Sixty years ago, Grin- comparing D. merriami and Dipodomys of nell (1922) suggested that temperature was less arid habitats: D. merriami has a higher 1983 Biology of Desert Rodents 101 urine-concentrating ability (comparison with which P. penicillatus is experimentally re-

D. agilis; Carpenter 1966) and a lower rate of moved to see if P. intermedins is, in fact, be- body water tiunover (comparison with D. mi- haviorally relegated to less-preferred habitats crops; Mullen 1971). by P. penicillatus were not performed. Nev- Substrate characteristics also appear to af- ertheless, the data strongly suggest that phys- fect distributional patterns of desert rodents. iological differences between these species Grinnell (1922) suggested that desert rodents mediate the interspecific interactions that de- are limited in geographic distribution via the termine the local distributions of these matching of pelage coloration with color species. tone of tlie background, though this may be a More recently, hypotheses that focus on in- matter of local adaptation. Other studies con- terspecific interactions and differential forag- tend that both local and geographical distri- ing behaviors have been invoked to account butions of desert rodents are limited to those for patterns of substrate philopatry in some areas with soil conditions that do not inhibit rodent species. Reichman and Oberstein the burrowing habits of a given species. (1977) and Price (1978b) have suggested that Dipodomijs deserti appears to be restricted to divergent body sizes and morphologies of deep sand areas, a substrate that is conducive heteromyid species reflect adaptations for ex- to the construction of large, deep burrow sys- ploiting different seed dispersions. Seed den- (Grinnell Hall tems 1914, 1946, Reynolds sity and dispersion appear to be affected by Roth Dipodomijs is of- 1958, 1978). merriami microtopography and soil structure (Reich- ten excluded from areas that have a surface man and Oberstein 1977, Bowers 1979, layer of rocks, heavy clay, sulphate crust, or 1982). Areas with fine substrates permit the hard-pan because of the difficulty in digging accumulation of dense seed aggregations by burrows in such soil types (Vorhies and Tay- trapping windblown seeds in depressions, lor 1922, Hardy 1945, Hall 1946, Huey 1951, whereas on substrates consisting of larger soil Reynolds 1958). In fact, Huey (1951) sug- particles, seeds are trapped individually. Be- gested that this was the main factor con- cause of their larger size and saltatorial loco- trolling the geographic distribution of D. motion, Dipodomijs are thought to specialize m.erriami below 4500 feet in western North on the exploitation of seed clumps that pro- America. vide large energy returns per unit time. The complex nature of physiological inter- Therefore, the distribution of Dipodomijs actions (primarily through the dissipation of should be coincident with fine substrates. In heat and conservation of water) with burrow contrast, the smaller, quadrupedal Pe- environments suggests that local distributions rognathus are thought to forage for more dis- may be affected by soil type (Gaby 1972, persed (individual) seeds and, consequently, Hoover 1973) as well as the potential for bur- should prefer areas with larger soil particle row ventilation via surface winds (Kay and sizes. Differential substrate utilization be- Whitford 1978). Such speculation is sup- these genera has been documented at ported by some novel work that employs tween habitat level (WondoUeck 1978, physiological and behavioral data to account the local priori reason why for the distribution of two species of Pe- Bowers 1979); there is no a might not be working to rognathus in New Mexico. This work (Hoo- the same mechanism distributional patterns as ver et al. 1977) suggests that P. intermedins affect geographical can tolerate a wide range of burrow micro- well. climates but is behaviorally excluded by P. penicillatns from substrates that have a high Vegetation heat buffering capacity (the preferred bur- temperature, row sites of P. penicillatus). If P. penicillatus Possibly the greatest effect of can tolerate only a small range of burrow mi- moisture, and substrate is a synergistic one, vegetative croclimates and is behaviorally dominant to affecting the local patterns of plant P. intermedins, this is an example of an in- structure and the distribution of certain cluded niche (Colwell and Fuentes 1975). species. Dice and Blossom (1937) suggested Unfortunately, definitive experiments in that the physiognomy of the vegetation was 102 Great Basin Naturalist Memoirs No. 7 an important factor in determining the distri- the dunes themselves, seeds will tend to ac- bution of desert rodent species. More recent- cumulate in depressions, thereby further con- ly, positive relationships between annual pre- centrating the resource, making it more ef- cipitation and perennial plant species diver- ficient for kangaroo rats to harvest. sity, density and size (Beatley 1969, Brown The interaction of climatic and substrate 1973, Hafner 1977), as well as perennial and variables affect the distribution of certain annual seed standing crop (Lieberman 1974) plant species or types (e.g., the associations of have been established. That D. merriami is Shelford 1913) to which, in turn, are closely limited in geographic distribution to areas re- tied the distribution of some desert rodents. ceiving less than 25 cm of annual precipi- For example, it is well documented that the tation (Reynolds 1958) and prefers habitats of distribution of D. microps is coincident with little vegetative cover (Hall 1946, Lidicker the distribution of chenopods of the genus 1960, Brown and Lieberman 1973, Rosenz- Atriplex (Grinnell 1933, Jorgensen 1963, Ke- weig 1973, Schroder and Rosenzweig 1975) nagy 1972a, b), upon which it is phys- suggest an indirect effect of moisture on lim- iologically and morphologically adapted to iting habitat characteristics for some species. feed (Kenagy 1972a, b; but see Csuti 1979).

By comparison, D. ordii is apparently limited Atriplex, in turn, is usually limited to alkali in distribution to more grassy habitats that flats surrounding dry basins of Pleistocene have an annual precipitation of more than 25 Lakes (Hall and Dale 1939, Munz and Keck cm (Reynolds 1958, Schroder and Rosenz- 1959). weig 1975). A similar relationship may occur Field observations (Hall 1946, Cameron on a geographic scale: D. merriami has ex- 1971, Brown et al. 1972, Cameron and Rain- panded its geographic range to include over- ey 1972, Olsen 1975) have documented rela- grazed grassland (now desert scrub) habitats tionships between the presence of cricetid ro- that once were more typical of D. ordii habi- dents and succulent desert vegetation. It is tats (Reynolds 1958). likely that this pattern results from the need Precipitation, through its effect on the of some species of Peromijscus and Neotoma quantity of available food (seed) resources, to consume succulent vegetation to maintain may also affect the geographical distribution positive water balance (Olsen 1975). of some desert rodent species. Frye (pers. comm.) found that most species of large (> Interspecific Interactions 100 g) Dipodomys species are restricted to those areas that predictably receive sub- Comparative physiological data do not al- stantial annual precipitation. It is likely that ways account for differences in the local dis- the relatively large amoimt of food resources tribution of closely related species, and other required by rodents of large body size causal and effect mechanisms must be in- coupled with the constraints of finite forag- voked. Lee (1963), in an investigation of the ing areas limits large species to more produc- physiological adaptations of N. lepida and N. tive areas. A potential exception to this pat- fuscipes to arid and semiarid habitats, found tern is D. deserti, which often occurs in areas no physiological bases for the observed dif- of the Mojave and southwestern Great Basin ferences in local distribution where the spe- deserts that receive little precipitation. Al- cies ranges overlap. A study focusing on the though the total amount of resources pro- competitive relationship of these species in duced in these areas is probably com- the Mojave Desert of southeastern California paratively small, D. deserti is restricted to found that these species are distinctly sepa- sand-dune habitats, which should be richer rated in most aspects of the habitat (Cameron than surrounding habitats. This is because 1971). Dietary studies, however, revealed food resources will be concentrated in dune that, when allopatric, both N. fuscipes and N. areas on two different scales by the action of lepida prefer a common food plant {Quercus surface winds. First, the same wind patterns turbinella), whereas N. lepida switches to a that transport sand from the surroiuiding val- less preferred species {Junipenis californica) ley and concentrate it into dunes will trans- when sympatric with N. fuscipes. An port seeds to dune areas as well. Second, on investigation of behavioral interactions 1983 Biology of Desert Rodents 103

(Cameron 1971) suggested that N. fuscipes is high vegetative cover, perhaps as a refuge dominant over N. lepida, relegating the latter from predation, it is thought that saltatorial to areas of low Qtiercus density, and con- kangaroo rats use open, poorly vegetated trolling the preferred food resource via habi- areas to a significant extent in the exploita- tat selection and defense. Such data support tion of food resources. The experimental the premise that interspecific competition for work of Thompson (1982b), O'Dowd and limited food resources affects patterns of lo- Hay (1980), and Kotler (in press) provides cal distribution. evidence that predation is important in determining The differential occurrence of Dipodomys microhabitat use. However, predation is not and Perognathus in different, but contiguous, the sole factor influencing microhabitat use. microhabitats has been documented by nu- If predation alone affects the differential use of micro- merous studies focusing on the local distribu- habitats and habitats by Perognathus and tion of these genera. This body of data repre- Dipodomys, the experimental removals of sents the best-documented pattern of habitat Dipodomys by Wondolleck (1978) and Price use by desert rodents. Perognathus tend to in- (1978a) should not have caused shift in mi- habit areas of high vegetation cover (Arnold crohabitat use by Perognathus. In all proba- 1942, Hall 1946, Reynolds and Haskel 1949, bility, properties of the resource base that Reynolds 1950, Rosenzweig and Winakur vary according to habitat microtopography 1969, Feldhammer 1979, Brown and Lieber- interact with locomotory differences in for- man 1973, Rosenzweig 1973, Price 1978a, aging of Dipodomys and Perognathus to help Wondolleck 1978) and coarse substrate types produce the observed differences in habitats (Hardy 1945, Hall 1946, Rosenzweig and utilized. The competition hypothesis couches et al. Winakiu- 1969, Brown 1975, Hoover patterns of habitat use in terms of the ability 1977, Wondolleck 1978). In contrast, Di- of a species to exploit a resource base that podomys, on a local scale, tend to be found in varies on a spatial scale. But there are several more open microhabitats with finer substrate variations on this general theme, and even (Hall 1946, Lidicker 1960, Rosenzweig and the mode of competition (e.g., exploitation Winakur 1969, Brown and Lieberman 1973, vs. interference) has been a subject of much Wondolleck 1978, Price 1978a; for a com- discussion. plete review, see Brown et al. 1979b; but see Much evidence suggests that desert gran- Thompson 1982a). ivorous rodents subdivide seed resources by In the section on abundance, we briefly exploiting different seed dispersions. As dis- discussed two mechanisms, based on com- cussed above, seed density and dispersion ap- petition and predation, that have been hy- pear to be influenced by microtopography pothesized to account for differential utiliza- and vegetative structure (Reichman and tion of microhabitats by Dipodomys and Oberstein 1977). Consequently, it is hypoth- Perognathus. The predation hypothesis is esized that the microhabitat affinities shown based on the early observations that Di- by desert rodents may exist because micro- podomys is better adapted to avoid pre- habitats differ in the degree to which they dation, via locomotory (Bartholomew and contain clumped seeds. Large saltatorial Caswell 1951) and auditory (Webster 1962) Dipodomys forage mainly in open, specializations, when compared with the vegetation-free habitats where windblown more quadrupedal Perognathus (although Pe- seeds accumulate in depressions or adjacent rognathus was subsequently shown to share to objects acting as windbreaks (Reichman most of the auditory specializations found in and Oberstein 1977, Bowers 1982). Thus, bi- Dipodomys; Webster and Webster 1975). pedal kangaroo rats are thought to forage Consequently, Perognathus are thought to oc- from seed clump to seed clump, spending cupy areas of high vegetative cover mainly as little time in the interspersed seed-poor areas a result of predation pressure that covaries (but see Frye and Rosenzweig 1980). By con- with local vegetative physiognomy (Rosen- trast, Perognathus and other quadrupeds for- zweig 1973, Thompson 1982a). Even though age under bushes (Brown and Lieberman recent work of Thompson (1982a) has dem- 1973, Rosenzweig et al. 1975, Price 1978a), onstrated that Dipodomys also use areas of where seeds are more uniformly distributed. 104 Great Basin Naturalist Memoirs No. 7

Although such a scheme is supported by geographic distributions of certain rodent both theoretical (Reichman 1980) and em- species. Bowers and Brown (1982) found that pirical (see Brown et al. 1979b for a review) those rodent species that a priori were most data, the actual mechanisms resulting in spa- likely to compete (e.g., similar-sized species tial segregation of Dipodomys and Pe- of the granivore guild) overlapped less in rognathtts on a local level are unclear. In par- their geographic ranges and cooccur less of- ticular, do DipodojJiys use aggression to ten in local communities than a null model competitively exclude Perognathus from the predicted. In contrast, overlaps between and seed-rich, open areas as suggested by Hutto cooccurrences of pairs with different trophic (1978) and Trombulak and Kenagy (1980), or affinities (e.g., interguild comparisons) did are the patterns of microhabitat use merely not differ from the random model. the result of more proficient exploitation of seed clumps by Dipodomys relative to Pe- Size rognathus (Reichman and Oberstein 1977, Body WondoUeck 1978, Price 1978b)? Body-size, per se, may also play a role in Congdon (1974) reported an instance determining the distribution of desert rodent where interspecific aggression of D. deserti species by affecting the way rodents use cer- toward D. merriami appeared to be depen- tain resources. Grinnell (1914) and Hall dent on the amount of available resources. In (1946) noted that an intermediate-sized het- periods of low resource availability, D. mer- eromyid, D. merriami, was found in nearly riami and D. deserti cooccurred in habitats every desert habitat, whereas the larger D. with sand substrates, but when the resource deserti was more restricted in habitat. From base was augmented, indirectly, by an intense this pattern Grinnell (1914) concluded that summer storm, D. merriami moved into non- larger species usually have more restricted sandy habitats, presumably to avoid the ag- habitat utilization patterns and more circum- gressively dominant D. deserti (Congdon scribed geographic ranges than their smaller 1974). This pattern may result from several relatives. More recently, Mares and Williams factors. First, resources may have become (1977) reported the result that intermediate- dense enough following the storm to become sized species of Perognathus and Dipodomys economically defensible (Brown 1964) by D. occupy the northern and eastern range limits deserti. Second, increased resource avail- of the family, whereas, in the center of heter- ability may have allowed D. deserti to spend omyid diversity, an array of smaller and less time foraging and more time engaged in larger species are syntopic with intermediate- aggressive interactions (see Caraco 1979). sized species. Bowers (in preparation) in- Although instances of aggression in desert vestigated the relationship between geogra- rodents have been reported many times (Hall phic range and body size for 46 heteromyid

1946, Eisenberg 1963, Christopher 1973, Ke- species and suggested that body size is an im- nagy 1976, Blaustein and Risser 1976, Hutto portant factor in affecting the extent of a 1978, Trombulak and Kenagy 1980), its role species distribution. Intermediate and very

in determining local distributions is unclear. small species are characterized by having In most cases, the appropriate experiments large distributions, but small and large heter- have not been done (but see Frye, in press). omyids have relatively small ranges. As many In fact, some authors (Brown and Lieberman economic, physiologic, and behavioral char- 1973, Brown et al. 1979, Bowers and Brown acteristics covary with body size (Eisenberg 1982) contend that for granivorous desert ro- 1963, Rosenzweig and Sterner 1970, French

dents it is very rare that the distribution of 1976, Reichman and Brown 1979), it is diffi- resources is sufficiently dense for inter- cult to attach cause and effect relationships specific aggression to be an economically fea- between certain biological properties and ge- sible strategy. ographic range. However, patterns of re- Interspecific interactions that affect pat- source use and the propensity of a species to terns of habitat use, on a local scale (Rosenz- enter food-induced torpor, both of which weig et al. 1975, Price 1978a, Brown et al. change with body size (Rosenzweig and Ster- 1979b), might also play a role in limiting the ner 1970, Brown and Lieberman 1973, Mares 1983 Biology of Desert Rodents 105 and Williams 1977, Reichman and Brown Such competition-based habitat selection 1979), appear to be of particular importance neither requires nor precludes interspecific in the determination of geographic aggression. Furthermore, habitat selection distribution. may be dependent on contemporary inter- Hypotheses regarding geographic distribu- actions or, if interactions occur over a very tion are almost impossible to test via manipu- long time, species may evolve inflexible behavioral, morphological, lation. However, it seems plausible that many or physiological adaptations that of the ecological factors important in affect- can enforce habitat selection even in the temporary ing local distribution should also affect the absence of the competitor species. The evolution of inflexible extent of the geographical distribution of a habitat selection was invoked by Shroeder species and, therefore, that geographic distri- and Rosenzweig (1975) to explain the result bution can be studied, via inference, through that reciprocal removals of D. merriami and studies at the local level. At best, the projec- D. ordii failed to result in either a wider tion of locally studied factors to explain large range of habitats used or density change in scale patterns is myopic. However, such an the target species when the congener was approach has been employed in other sys- absent. tems with apparent success (see Glazier 1980, How can it be determined if a specific case Reaka 1980, Brown 1981). of affinity for a certain type of substrate or vegetation results from competition-based Habitat Selection habitat selection? If habitat selection is based on contemporary interactions, removal ex- Throughout our discussion of distribution, periments (as we called for in the Pe- we have given many examples of habitat or rognathus intermedius-P. penicillatus system) microhabitat affinity. An important problem should suffice. If, on the other hand, habitat that remains is to determine whether these selection has evolved to inflexibility, then affinities are completely due to physiological simple removal experiments will not dis- or physical hmitation (which has often been tinguish between competition-based habitat implicit in our discussion, especially of abiot- selection and a complete lack of competition: ic factors), or whether these affinities result no response would be expected in either case. at least in part from habitat selection Study of "natural experiments" is then called originating from competitive interactions. for. If a species expands its use of habitats in Rosenzweig (1979, 1981) has developed mod- geographic areas where the putative com- that els of competition-based habitat selection petitor is absent, then the contention in causing habitat that can be illustrated as follows. Imagine a competition is important species. A, that prefers habitat type a over a selection is supported. different type, b, perhaps because it is more efficient at harvesting resources in a. At low Predation and Parasitism densities, all A will be found in habitat a. As the density of increases, however, the fit- A Distribution may also be affected by pre- ness of individual in will gradu- A habitat a dation and parasitism. The probability of ally decrease (because of resource degrada- being preyed upon may be so high in certain tion); eventually, habitat a will be degraded habitats that some species are either extermi- to a point where a and b are equal in quality. nated in those areas or individuals are unwill- At this point, A should inhabit b as well as a; ing to enter them. Although there are no an observer would detect no habitat affinity documented cases of habitat or range restric- (though a difference in density could exist). tion that are directly attributable to pre-

Now introduce species B, which prefers habi- dation, it -has been speculated (Brown, pers. tat b because it is more efficient at harvesting comm.) that the range of the kangaroo resources there. Because they prefer b over a, mouse, Microdipodops pallidus, may be re- B will tend to degrade habitat b, reducing stricted by the presence of the sidewinder the fitness of A on b, leading A to inhabit rattlesnake (Crotalus cerastes); these two only habitat a. dune specialists do not appear to cooccur on 106 Great Basin Naturalist Memoirs No. 7 dune systems even though their ranges abut. extensive study of host-parasite dynamics This pattern may occur because the kangaroo within each system considered. mice appear to be particularly vulnerable to attacks by sidewinders (which are pit vipers); instead of hopping away when attacked by a Population Structure predator (as kangaroo rats do; Webster and In this section we will discuss two aspects Webster 1971), they simply remain motion- of population structure: breeding structure less (Brown, pers. comm.). (who mates with whom) and certain aspects Parasites may be important in determining of spatial structure, primarily home range use distribution as well. Barbehenn (1969) devel- and dispersal. We are mainly interested in oped a hypothesis in which competitive ex- the effects of these on population genetic clusion of one species by another species is structure, which we define here as the way in resisted by "germ warfare" on the part of the which a population deviates from panmixia. competitively inferior species. In the simplest Deviation from panmixia can have several scenario discussed by Barbehenn, if the inferi- important effects on the evolutionary dynam- or species harbors a parasite to which it has ics of populations. evolved resistance and if the parasite is re- 1. Fixation of alleles by random drift is stricted to certain habitats by requirements more likely to occur with small, effective of the intermediate host or vectors, then population size and discrete subpopulations, those habitats will provide refuges for the in- than in large panmictic populations. Drift is ferior species; individuals of the com- important in one model of evolution, em- petitively superior species that invade this bodied in the shifting balance theory of habitat will be killed by parasites. Cornell Wright (1977), but is imnecessary or even a (1974) extended this hypothesis in an attempt hindrance for evolution in models that as- to explain distributional gaps between consume panmixia (Haldane 1924, Fisher 1930). geners. In this case, each host species carries 2. Localized extinctions, which are impor- a strain or species of parasite (to which it is tant in most scenarios of group selection (e.g., resistant) but is killed when infected by the Wilson 1977, Gilpin 1975) and island bio- parasite carried by the other host species. geography (MacArthur and Wilson 1967, Where the ranges of these host species abut, Brown 1971), are more likely to occur in sub- individuals of both species would be killed by populations that are small and discrete. parasites carried by the other species. In both 3. Demic structure and resistance to immi- these models, the interactions between the gration may reduce the impact that gene parasite and the resistant host are relatively flow has in maintaining species integrity and stable; therefore it is unlikely that reduced thereby make interpopulation divergence virulence need evolve. more likely (Anderson 1970; but see Baker One example of the effect of parasites on 1981). distributions is the contraction of the range 4. The evolution of some social and al- of the moose {Alces alces) in the face of the truistic behaviors is thought to partially de- expansion of the whitetail deer {Odocoileus pend on subpopulation groupings that are virginianus) range, which is thought to be based on kin ties (e.g., Hamilton 1972, Sher- caused by meningeal worms harbored by the man 1977, Michod 1979, 1980) or possession whitetail deer that are fatal to the moose of traits common to members of a group (Price 1980). Another possible example in- (Wilson 1977). volves Peroniyscus maniculatus and Neotoma 5. High variance in reproductive success cinerea inhabiting lava caves in northeastern can result from competition for mating op- California. Peroniyscus maniculatus harbors portunities (typically among males), active bubonic plague; populations of A^ cinerea in choice of mates by members of one sex, or these caves are occasionally exterminated by differential survival of young. Differential re- outbreaks of disease (Nelson and Smith 1976). productive success among members of one or Absolutely nothing is known of the impact both sexes will not only lead to reduced ef- of parasites on the distribution of desert ro- fective population size (Wright 1940, Patton dents. To gain this knowledge will require and Feder 1981), but it will also lead to more 1983 Biology of Desert Rodents 107 rapid evolution within populations since se- some females exclusive of other males. On lective pressures due to variance in reproduc- the other hand, if males do not defend the tive success are more pronounced than when areas of females, one expects to find extensive mating is random within populations (Wilson overlap between males; exclusive access to et al. 1975). females by certain males should be rare. This At least four types of evidence can be used latter pattern of home range overlap charac- to study population structure: behavioral, de- terizes D. merriami; male-male overlap of mographic, indirect genetic, and direct ge- home ranges is extensive and the home range netic. will treat each in turn describe We and of each female is overlapped by the home what is known for desert rodents, covering ranges of several males (O'Farrell 1980; primarily heteromyids. Jones, 1982). Data on dispersal behavior are also useful in understanding population structure. Dis- Behavioral Evidence persal data are lacking for most desert ro- Behavioral evidence can be used to infer dents, but in those species that have been the importance and probable effect of vari- studied there appears to be a low degree of ous mechanisms in structuring populations. individual vagility. Jones (1982) measured In some desert rodents, male dominance may distances moved by juvenile D. spectabilis play an important role in breeding structure. and D. merriami. He was able to detect suc- There is evidence suggesting that, among cessful dispersal moves of up to 0.9 km (15 to some kangaroo rats, certain males may de- 20 home range diameters), yet he found that fend the burrows of females against other among those juveniles surviving to reproduc- males. Kenagy (1976) observed two male D. tive maturity, less than 25 percent of D. spec- fighting at the of a female, microps mound tabilis and only 11 percent of D. merriami and saw the winner copulate with the female. dispersed to areas not adjacent to their natal Similarly, Randall (pers. comm.) observed sites. Most of these cases of dispersal involved one D. spectabilis defend the mound of a fe- movements of less than three home range di- male against several other males. In the ameters. The possibility of long distance dis- thom-forest-inhabiting heteromyid Liomys persal (>0.9 km) cannot be ruled out, salvini, Fleming (1974) found that size was a though. French et al. (1974) measured dis- good predictor of dominance and that larger persal up to 0.9 km in Perognathus formosus males were surrounded by more potential (whose home range diameter is less than half mates than were smaller males. that of D. merriami; Maza et al. 1973) and In the northern grasshopper mouse, determined that more individuals dispersed OnycJiomys leucogaster, there is some evi- short distances and more dispersed long dis- dence that males and females form at least tances than would be expected if individuals temporary pair bonds, a behavior that would simply moved to the nearest vacancy. In tend to reduce variance in male reproductive other words, although most individuals made success. First, Ruffer (1965) observed male only very short dispersal moves (as was parental care in the laboratory. Second, Ego- for D. merriami and D. spectabilis), scue (1960) found that, even at low densities, shown individuals that members of a male-female pair of O. leuco- there were a few P. formosus distance. The possibility that gaster were often caught in adjacent traps, moved a great similar indicating that they lived or traveled togeth- D. merriami and D. spectabilis make needs to be checked by er. A similar pattern occurs in Peromysctis long distance moves over at eremicus (Munger, mipubl. data). studying dispersal in these species Patterns of home range overlap can also be least 40 home range diameters (2 km). used to infer breeding structure. For instance, Information on the extent of dispersal in and if males defend the burrows of females, as has other desert rodents is sketchy. Allred been observed for D. spectabilis and D. mi- Beck (1963) found that the average distances crops, there might be little home range over- between most widely separated capture loca- lap between males, and the home ranges of tions for each individual were greatest for certain males might include the mounds of Onychomys torridus males and Peromyscus 108 Great Basin Naturalist Memoirs No. 7

maniciilatus males, somewhat less for O. tor- breeding structure of a population is un- ridus females, P. maniciilatus females, and D. known, but it seems that they would increase merriami, and still less for D. microps and the number of female home ranges to which Perognathus longimembris. Among D. mi- a given male has access. And fourth, dis- crops, for which the average distance be- persers will have no effect on population tween capture locations was about 76 m, 79 structure unless they breed or otherwise dis- percent of males (n = 183) and 87 percent of rupt the breeding structure of the residents. females (n = 126) ranged less than 122 m. Liebold and Munger (in preparation) have Among P. longimembris most animals of both shown that dispersing female D. merriami sexes ranged less than 30 m (n = 102). Such tend to be less successful at breeding than data suggest that D. microps and P. long- their nondispersing counterparts, indicating imembris are quite sedentary. Roberts and that their effect on population genetic struc- Packard (1973) reported that the average ture might be less than would be expected home range size in the Texas kangaroo rat D. from examining dispersal behavior alone. elator was .08 ha, and that the maximum distance moved between traps was 87 m for Demographic Evidence males and 109 m for females. It is not clear in what portion of the movements either Breeding structure is also partially depen- study represent daily movements about the dent on demography. The number of breed- home range as opposed to dispersal or shifts ing individuals and the variance in their life- in home range boundaries. To imderstand the time reproductive success may be influenced effects of these movements on population by survivorship and longevity. For example, genetic structure, we need to know the distri- a few individuals may survive to adulthood bution of movements in terms of home range and live through several breeding seasons, to determine what fraction of an animal's but most individuals either do not survive to movements bring it into contact with individ- reproductive maturity or reproduce only uals they do not normally encounter within once. In this situation, the reproductive out- their own home ranges. It is also unclear put of a population is concentrated in a small from these data which movements represent number of long-lived adults. The contrasting permanent shifts in home ranges vs. tempo- situation is one in which longevity is nearly rary excursions out of the usual home range. equal for all adults so that those individuals We emphasize that these sorts of behav- reaching reproductive maturity all reproduce ioral data are, by themselves, insufficient to once or twice and then die. In this case the determine how populations are structured. lifetime reproductive contributions of all There are several reasons for this. First, adults might be more nearly equal than in though some dominant males may defend fe- the former situation. Both of these age struc- males, subordinate males may steal cop- tures are found in heteromyids. The latter ulations and thus dilute the effects of territo- characterizes L. salvini. Annual turnover is rial defense. Second, the timing of mating nearly complete; young are born in the may be crucial. An observer might see sever- spring and by the next breeding season year- al males copulating with a female, but it may lings make up nearly 100 percent of the pop- be that only the male that mates with her at ulation (Fleming 1974). Dipodomys spec- peak receptivity during estrus will success- tabilis appears to be an example of the other fully fertilize her. Third, among heteromyids, situation. Holdenreid (1957) studied a popu- individuals occasionally make long forays (3 lation near Santa Fe for 27 months, and to 4 home range diameters) away from their stated that "the population was composed of usual home ranges. Maza et al. (1973) report- a few well-established individuals remaining ed that these long distance excursions are continually on the area and a much larger correlated with reproductive activity in P. number of animals that remained for only a formosus. Long-distance forays also occur in few days or months" (p. 338). In general,

D. merriami and D. microtis (A 11 red and Beck desert rodents tend to be long lived relative 1963) and in D. spectabilis (Jones, 1982). The to nondesert rodents (Smith and Jorgensen actual influence of these excursions on the 1975, Conlev et al. 1976; members of some 1983 Biology of Desert Rodents 109

Perognathus species may live up to five years, from random mating. Furthermore, sample French et al. 1967). In most cases, however, sizes from any one population are often too it is unknown whether there is a high vari- small to allow statistical tests. Finally, it is ance in survivorship that might lead to a not possible to determine if the samples from large differential in reproductive success. any one study site are from one or several subpopulations; population structure will af- Indirect Genetic Evidence fect the interpretation (Patton and Feder 1981). Indirect genetic evidence concerning pop- Two studies do provide some indirect ge- ulation structure can be gathered by deter- netic evidence concerning structure in desert mining if genotypic frequencies deviate from rodent populations. Using a pelage character, an expectation based on random mating. Ras- Blair (1947) showed no deviation from ran- mussen (1964) found a deficiency of hetero- dom expectation within subpopulations of Pe- zygotes of blood group loci in Peromyscus romyscus rnaniculatus blandus. In addition, maniculatus, implied that inbreeding was the there was little divergence of subpopulations cause, and calculated a relatively small ge- from nearby (less than 5 km) subpopulations, netic neighborhood size of 10-75 individuals. indicating that dispersal between sub- Selander found a deficiency of hetero- (1970) populations does occur. More distantly sepa- zygotes in a population of house mice and rated subpopulations did diverge, however. from this inferred that the population was Johnson and Selander (1970) gave diagrams structured into small denies (but see Baker showing the spatial associations of genotypes 1981). He strengthened his assertion by citing at four loci in D. merriami, and described two behavioral studies that showed an organiza- of the loci as having clumped distributions of tion into families or tribes. Patton and Feder alleles. They suggested that this pattern calculated statistics (Wright (1981) F 1965, might indicate a low level of dispersal and Nei 1975) for populations of bot- Thomomys some inbreeding, though no statistical test of tae. The measure of random mating within a the pattern was presented. Their findings are population can be decomposed into two (Fit) at least consistent with the findings of Jones parts, deviation from random mating among (1982) for dispersal distances of D. merriami. subpopulations (Fst) and nonrandom mating within a subpopulation (Fjs). Patton and Feder showed significant diver- a amount of Direct Genetic Evidence gence among subpopulations, but results were equivocal for within-subpopulation Indirect evidence yields only the knowl- matings. Schwartz and Armitage (1980) sim- edge that some deviation from panmixia has ilarly calculated F statistics from electro- occurred, but does not determine which phoretic data on yellow-bellied marmots mechanism causes the deviation. This is illus- Mamiota flaviventris. They found evidence trated by the findings of Patton and Feder for considerable gene flow between colonies (1981): the deviations from random mating and no evidence for inbreeding, and thus they observed within subpopulations of goph- concluded that it is unlikely that evolution in ers may not have been due to inbreeding but these marmots is accelerated by fixation of instead to demic structure within the alleles via inbreeding within colonies. subpopulation. Relatively little indirect genetic evidence Direct genetic evidence, on the other exists concerning the breeding structure of hand, ties a genetic effect to the mechanism desert rodent populations. Studies that mea- causing it. For instance, by identifying geno- sure allelic diversity are typically concerned types at a number of polymorphic loci for all with systematics at the subspecies level or individuals within a population, it is often above, or with describing the amount of vari- possible to determine precisely what success- ation that exists in populations. The pub- ful matings have occurred in the population. lished data are usually genie, not genotypic, Patton and Feder (1981) used this technique frequencies and values of overall hetero- to show that relatively few males of the zygosity and polymorphism; genotypic fre- pocket gopher Thomomys bottae fathered quencies are required to detect deviations most of the young in their study area. 110 Great Basin Naturalist Memoirs No. 7

Hanken and Sherman (1981) used it to dem- structure. We suggested above how differ- onstrate multiple paternity in Belding's ences in age structure, longevity, and survi- ground squirrel {Spemiophilus beldingi litters. vorship schedules might lead to more or less Foltz and Hoogland (1981) determined that variance in lifetime reproductive success of most litters of the black-tailed prairie dog adults. In species like D. spectabilis, where a Cynomys ludovicianus were sired by resident few individuals live through several breeding males within the home coterie, indicating seasons but most individuals have much that coteries were the units of reproduction shorter lifespans, a core of long-lived individ- within the population as well as the units of uals may make a disproportionately large social structure. Foltz (1981) also used ge- contribution to later generations. It would be netic evidence to determine that female old- useful to know what proportion of the breeding adults in later generations are actually field mice Peromyscus polionotiis usually descendants of these long-lived individuals. mate with the same male for consecutive lit- And how does reproductive success vary with ters, thus demonstrating long-term mo- age? Are older males more successful at com- nogamy in this species. As yet, there are no peting for mates? This would further increase published studies showing direct genetic evi- variance in male reproductive success in situ- dence of structure in desert rodent popu- ations where only a small proportion of males lations, but work is under way for two spe- live into their second or third breeding sea- cies, D. spectabilis and D. merriami. son. These questions are probably best pur- Clearly, there are opportunities for more sued in long-term mark-recapture studies of research on the structure of desert rodent natural populations combined with direct populations, and what we now know suggests genetic determination of maternity and some interesting possibilities. One of these paternity. concerns deme size and the extent of sub- Population structure in desert rodents may structuring of populations. Two lines of evi- also be related to fluctuations in density; such dence, the description by Johnson and Selan- periodic decreases in population size are der (1970) of clumped distributions of alleles known to occur (Beatley 1969, French et al. and observations by Jones (1982) of short dis- 1974, Whitford 1976, Petryszyn 1982). These persal distances, suggest a substantial demic decreases may cause genetic bottlenecks, re- structure in D. merriami populations. The ex- ducing the amount of genetic diversity with- tent of gene flow within populations is uncer- in subpopulations. To what extent do these tain, though. Turnover rates are quite high in decreases in density affect effective popu- D. merriami (80-90 percent annually; Jones, lation size? Furthermore, the rate of dispersal 1982), which would tend to increase gene between subpopulations may vary with den- flow. Furthermore, we do not know the ex- sity. Higher interdemic dispersal rates at tent of long-distance dispersal (greater than peak densities might partially or completely 20 home range diameters), nor do we under- offset the reductions in variability that possi- stand what role, if any, is played by excur- bly result from population crashes. Determin- sions to areas outside the usual home range. ing the importance of density fluctuations Do individuals making these excursions find and interdemic dispersal for population ge- mates in areas several home range diameters netic structure would require monitoring ge- from their own home range, or are they more netic makeup over large areas and over a one, successful at finding mates among their im- time long enough to cover at least and mediate neighbors, with whom they are pos- preferably more, cycle(s) of population decline and increase. sibly more familiar? Genetic studies in which marker alleles are introduced in natural populations (cf. Anderson et al. 1964, Baker Acknowledgments 1981) would help answer these questions and would aid in determining the rate of gene A portion of this manuscript was presented flow within and among subpopulations. in a symposiimi on the biology of desert ro- Other questions concern the effects of age dents at the sixty-second annual meeting of and breeding stnicture on population genetic the American Society of Mammalogists. We 1983 Biology of Desert Rodents 111

1976a. Rainfall and fluctuating plant popu- thank O. J. Reichman and James Brown for lations in relation to distribution and numbers of inviting us to participate. Constructive criti- desert rodents in Southern Nevada. Oecologia cism by Christine Flanagan, Daniel Thomp- (Berl.) 24:21-42. son, Robert Chew, and Eric Larsen was par- Bif.nek, G. K., and L. G. Klikoff. 1974. Parasitological ticularly important in developing this evidence of arthropods as food for Dipodomys manuscript. We gratefully acknowledge E. L. merriami vulcani. Amer. Midi. Nat. 92:251-252. Blair, W. Cockrum, Robert Frye, Thomas Gibson, F. 1947. Estimated frequencies of the buff and gray genes (G,g) in adjacent populations of Donald Kaufman, James Patton, Yar Petrys- deer mice {Peromyscus numiculatus blandtis) liv- zyn, and an anonymous reviewer for valuable ing on soils of different colors. Contrib. Lab. discussion and/ or comments on earlier drafts Vert. Biol. Univ. Michigan 36:1-16. Blaustein, a. R., A. of this manuscript, and Jill Smith for typing and C. Risser. 1974. Dominance the manuscript. relationships of the dark kangaroo mouse {Micro- dipodops megacephalus) and the little pocket mouse {Perognathus longimembris) in captivity. Great Basin Nat. 34:312'/4 16. Bowers, M. A. 1979. Coexistence of desert rodents: a Literature Cited multivariate analysis. Unpublished thesis. Brig- ham Young Univ. 76 pp. Abramsky, Z. 1978. Small mammal community ecology: 1982. Foraging behavior of heteromyid rodents: field evidence of resource partitioning. changes in species diversity in response to manip- J. Mam- ulated productivity. Oecologia (Berl.) 34:113-123. mal. 63:361-367. Allred, D. M., and D. E. Beck. 1963. Range of move- 1983. Relationship between body size and geo- ment and dispersal of some rodents at the Ne- graphic distribution in heteromyid rodents. In vada Test Site. 44:190-200. preparation. Atomic J. Mammal. A., Anderson, P. K. 1970. Ecological structure and gene Bowers, M. and J. H. Brown. 1982. Body size and flow in small mammals. Symp. Zool. Soc. Lon- coexistence in desert rodents: chance or commu- don. 26:299-325. nity structure? Ecology 62:391-400. Anderson, P. K., L. C. Dunn, and A. B. Beasley. 1964. Bradley, W. G., and R. A. Mauer. 1971. Reproduction Introduction of a lethal allele into a feral house and food habits of Merriam's kangaroo rat, Di- mouse population. Amer. Nat. 98:57-64. merriami. 52:497-507. podomys J. Mammal. Anderson, R. M. 1978. The regidation of host popu- Breed, W. G. 1975. Environmental factors and repro- lation growth by parasitic species. Parasitology duction in the female hopping mouse, Notornys 76:119-157. alexis. Fertil. 45:273-281. J. Reprod. Anderson, R. M., and R. M. May. 1978. Regulation and 1971. mountaintops: non- Brown, J. H. Mammals on stability of host-parasite population interaction. equilibrium insular biogeography. Amer. Nat. I. Regulatory processes. Anim. Ecol. J. 105:467-478. 47:219-247. 1973. Species diversity of seed-eating desert ro- 1979. Population biology of infectious diseases. dents in sand dune habitats. Ecology 54:775-787. Part I. Nature 280:361-367. 1975. Geographical ecology of desert rodents. In 1982a. Coevolution of hosts and parasites. Para- eds.. Ecology M. L. Cody and J. M. Diamond, sitology 85:411-426. and evolution of communities. Harvard Univ. 1982b. Population biology of infectious diseases. Press, Cambridge, Massachusetts. Springer- Verlag, New York. 1981. Two decades of homage to Santa Rosalia: Arnold, L. W. 1942. Notes on the life history of the toward a general theory of diversity. Amer. Zool. sand pocket mouse. Mammal. 23:339-341. J. 21:877-888. Baker, A. E. M. 1981. Gene flow in house mice: in- Brown, H., and D. W. Davidson. 1977. Competition troduction of a new allele into a free-living popu- J. between seed-eating rodents and ants in desert lation. Evolution 35:243-258. ecosystems. Science 196:880-882. Baltazard, M., M. Bahmanyar, C. Modifi, and B. Brown, H., D. W. Davidson, and O. Reichman. Seydian. 1952. Le foyer de peste du Kurdistan. J. J. 1979a. An experimental study of competition be- Bull. Wld. Hlth. Org. 5:441-472. seed-eating desert rodents and ants. .Amer. Barbehenn, K. R. 1969. Host-parasite relationships and tween 19:1129-1143. species diversity in mammals: an hypothesis. Zool. H., G. A. Lieberman. 1973. Resource uti- Biotropica 1:29-35. Brown, J. and of seed-eating rodents in Bartholomew, G. A., and H. H. Caswell. 1951. Loco- lization and coexistence 54:788-797. motion in kangaroo rats and its adaptive signifi- sand dune habitats. Ecology cance. 32:155-169. Brown, H., G. A. Lieberman, and W. G. Dengler. J. Mammal. J. Beatley, of desert rodents on 1972. Woodrats and cholla: dependence of a J. C. 1969. Dependence winter annuals and precipitation. Ecology small mammal population on the density of cacti. 50:721-724. Ecology .53:310-313. their environ- H.^ C. Munger. 1983. Experimental 1974. Phenological events and Brown, J. and J. mental triggers in Mojave Desert ecosystems. manipulation of desert rodent communities: spe- Ecology 55:856%63. cies removal and food addition. In preparation. 112 Great Basin Naturalist Memoirs No. 7

Brown, H., O. Reichman, and D. W. Davidson. J. J. W., Davis, J. and R. C. Anderson. 1971. Parasitic dis- Rev. 1979b. Granivory in desert ecosystems. Ann. eases of wild mammals. Iowa State Univ. Press, Ecol. Syst. 10:201-227. Ames, Iowa. L. 1964. evolution of diversity in avian Brown, J. The Dawson, W. R. 1955. The relation of oxygen con- territorial systems. Wilson Bull. 76:160-169. to in desert rodents. sumption temperature J. P. N. E. P. D. Burger, J., C. Negus, H. Sanders, and Mammal. 36:543-553. Gardner. 1981. Chemical triggering of reproduc- Dice, L. R., and P. M. Blossom. 1937. Studies of mam- tion in Microtus montanus. Science 214:69-70. malian ecology in southwestern North America Cameron, G. N. 1971. Niche overlap and competition in with special attention to the colors of desert 52:288-296. Inst. Publ. woodrats. J. Mammal. mammals. Carnegie Washington, 485. Cameron, G. N., and D. G. Rainey. 1972. Habitat utili- Dunigan, p. F. X., Jr., W. Lei, and W. H. Rickard. zation by Neotoma lepida in the Mojave Desert. 1980. Pocket mouse population response to win- 53:251-266. ter precipitation and drought. Northwest Sci. J. Mammal. Caraco, T. 1979. Time budgeting and group size: a test 54:289-295. of theory. Ecology 60:618-627. DuRRANT, S. D. 1952. Mammals of Utah: taxonomy and Univ. Carlquist, S. 1965. Island life. Natural History Press, distribution. Kansas Publ., Lawrence. Garden City, New York. Eads, R. B., and B. G. Hightower. 1952. Blood parasites of southwest Texas rodents. Parasitol. Carpenter, R. E. 1966. A comparison of thermoregida- J. 38:89%0. tion and water regidation in the kangaroo rats Egoscue, H. 1960. Laboratory and field studies of the Dipodomys agilis and Dipodomys merriami. Univ. J. northern grasshopper mouse. Mammal. California Publ. Zool. 78:1-36. J. 41:99-110. Chew, R. M., and B. B. Butterworth. 1964. Ecology of 1962. Ecology and life history of the kit fox in rodents in Indian Cove (Mojave Desert), Joshua Tooele County, Utah. Ecology 43:481-497. Tree National Monument, California. Mam- J. 1976. Flea exchange between deer mice and mal. 45:203-225. some associated small mammals in Western Childs, H. E., Jr., and G. E. Cosgrove. 1966. A study Utah. Great Basin Nat. 36:478-480. of pathological conditions in wild rodents in ra- B. 1982. its role in Eidemiller, J. Omnivory: the ecology dioactive areas. Amer. Midi. Nat. 76:309-324. of desert cricetine rodents. Unpublished dis- Christian, D. P. 1979a. Comparative demography of sertation. Univ. of California, Irvine, California. three Nainib Desert rodents: responses to the F. 1963. of ro- Eisenberg, J. The behavior heteromyid provision of supplementary water. Mammal. J. dents. Univ. California Publ. Zool. 69:1-114. 60:679-690. Errington, p. L. 1943. An analysis of mink predation 1979b. Physiological correlates of demographic upon muskrats in the north central United States. patterns in three sympatric Namib Desert ro- Iowa Agr. Exp. Stn. Res. Bull. 320:797-924. dents. Physiol. Zool. 52:329-339. 1946. Predation and vertebrate populations. Q. 1980. Patterns of recovery from low numbers in Rev. Biol. 21:144-177, 221-245. Namib Desert rodents. Acta Theriol. 1954. The special responsiveness of minks to 25,36:431-450. epizootics in muskrat populations. Ecol. Monogr. Christopher, E. A. 1973. Sympatric relationships of the 24:377-393. kangaroo rats, Dipodomys merriami and Di- 1956. Factors limiting higher vertebrate popu-

agilis. lations. 124:303-307. podomys J. Mammal. 54:317-326. Science CoLWELL, R. K., AND E. R. FuENTES. 1975. Experimental Feldhamer, G. a. 1979. Vegetative and edaphic factors studies of the niche. Ann. Rev. Ecol. Syst. affecting abundance and distribution of small 6:281-310. mammals in southeast Oregon. Great Basin Nat. of 39:207-218. CoNGDON, J. 1974. Effect habitat quality on distributions of three sympatric species of desert rodents. Fenner, F., and F. N. Ratcliffe. 1965. Myxomatosis. 55:659-662. Cambridge Univ. Press, Cambridge, J. Mammal. W., D. Massachusetts. CoNLEY, J. Nichols, and A. R. Tipton. 1977. Re- Fisher, R. A. 1930. The genetical theory of natural se- productive strategies in desert rodents. In R. H. lection. Clarendon Press, Oxford. (2d rev. ed. Wauer and D. H. Riskind, eds.. Transactions, 1958, Dover Publ.) symposium on the biological resources of the Fleming, T. H. 1974. Social organization in two species Chihuahuan Desert region. United States and of Costa Rican heteromvid rodents. Mammal. Mexico. U.S. Park Service, Washington, D.C. J. 55:543-561. Cornell, H. 1974. Parasitism and distributional gaps FoLTz, D. W. 1981. Genetic evidence for long-term between allopatric species. Amer. Nat. monogamy in a small rodent Peromyscus polion- 108:880-883. ottis. Amer. Nat. 117:665-675. Cranford, 1980. J. Coevolved adaptations in the host W., L. 1981. .Analysis of FoLTZ, D. and J. HooGLAND. parasite association of Peromyscus leucopus and the mating system in the black-tailed prairie dog Cuterebra fontinella. Abstracts of papers pre- {Cynomys ludovicianus) bv likelihood of pater- sented at 61,st meeting of the Society of American nity. J. Mammal. 62:706-712. Mammalogi.sts. 1971. Forrester, D. J. Bighorn sheep lungworm-pneu- R. CsuTi, B. a. 1979. Patterns of adaptation and variation monia complex. In J. N. Davis and C. Ander-

in the Great Basin kangaroo rat, Dipodomys rtii- son, eds., Parasitic diseases of wild mannnals. crops. Univ. California Publ. Zool. 111:1-69. Iowa State Univ. Press, Ames. 1983 Biology of Desert Rodents 113

French, N. R. 1976. Selection of high temperatures for P. Hanken, J., and W. Sherman. 1981. Multiple pater- hibernation by the pocket mouse, Perognathiis nity in Belding's ground squirrel litters. Science hngimembris: ecological advantages and energet- 212:.351-353. ic consequences. Ecology 57:185-191. Hardy, R. 1945. The influence of types of soil upon local N. R, B. G. Maza, A. P. French, and Aschwanden. distribution of small mammals in southwestern 1967. Life spans of Dipodoniys and Perognathus Utah. Ecol. Monogr. 15:71-108. in the Mojave Desert. 48:537-548. J. Mammal. Hayne, D. W. 1975. Experimental designs and statistical N. R., B. French, G. Maza, H. O. Hill, A. P. analyses in small mammal population studies. In Aschwanden, and H. W. Kaaz. 1974. A popu- D. P. Snyder, ed.. Populations of small mammals lation study of irradiated desert rodents. Ecol. under natural conditions, V. 5, Special Publ. Monogr. 44:45-72. Series, Pymatuning Lab. of Ecol., Univ. of In press. field in- Frye, R. J. Experimental evidence of Pittsburgh. terspecific aggression between two species of HoLDENREiD, R. 1957. Natural history of the bannertail kangaroo rats (Dipodomys). Oecologia (Berl.) kangaroo rat in New Mexico. J. Mammal. R. L. 1980. size Frye, J., and M. Rosenzweig. Clump 38:330-350. selection: a field test with two species of Di- Hoover, K. D. 1973. Some ecological factors influencing podomys. Oecologia (Berl.) 47:323-327. the distributions of two species of pocket mice Gaby, R. 1972. Differential niche utilization by two spe- (genus Perognathus). Unpublished dissertation. cies of kangaroo rat (genus Dipodomys). Unpub- New Mexico State Univ., Las Cruces. 75 pp. lished dissertation. New Mexico State Univ., Las Hoover, K. D., W. G. Whitford, and P. Flavill. 1977. Cmces. 71 pp. Factors influencing the distributions of two spe- Garner, H. W., L. W. Richardson, and L. A. Felts. cies oi Perognathus. Ecology 58:877-884.

1976. Alimentary helminths of Dipodomys ordii: Howell, A. B., and I. Gersh. 1935. Conservation of wa- effects on the host population. Southwest. Nat. ter the 16:1-9. by rodent Dipodomys. J. Mammal. 21:327-334. Huey, L. M. 1951. The kangaroo rats (Dipodomys) of Glazier, D. S. 1980. Ecological shifts and the evolution Baja California, Mexico. Trans. San Diego Soc. of geographically restricted species of North Nat. Hist. 11:205-256. 7:63-83. American Peromyscus. J. Biogeogr. Hutto, R. L. 1978. A mechanism for resource allocation Gilpin, M. E. 1975. Group selection in predator-prey among sympatric heteromyid rodent species. communities. Princeton Univ. Press, Princeton, Oecologia (Berl.) 33:115-126.' New Jersey. Inouye, R. S. 1980. Density-dependent germination re- 1914. of sponse bv seeds of desert annuals. Oecologia Grinnell, J. An account the mammals and birds of the lower Colorado Valley. Univ. Califor- (Berl.) 46:235-238. nia Publ. Zool. 12:51-294. 1981. Interactions among unrelated species: 1922. A geographical study of the kangaroo rats granivorous rodents, a parasitic fungus, and a of California. Univ. California Publ. Zool. shared prey species. Oecologia (Berl.) 49:425-427. R. S., G.'s. Byers, and H. Brown. 1980. Ef- 24:1-174. Inouye, J. fects of predation and competition on survivor- 1933. Review of the recent mammal fauna of ship, fecundity, and community structure of California. Univ. California Publ. Zool. desert annuals. Ecology 61:1344-1351. 40:71-234. Johnson, W. E., and R. K. Selander. 1971. Protein vari- Grundman, a. W. 1957. Nematode parasites of mam- ation and systematics in kangaroo rats (genus mals of the Great Salt Lake Desert of Utah. J. Dipodomys).' Syst. Zool. 20:377-405. Parasitol. 43:105-112. Jones, W. T. 1982. Natal nondispersal in kangaroo rats. 1958. Cestodes of mammals from the Great Salt Unpublished dissertation. Purdue Univ. West La- Lake Desert region of Utah. Parasitol. J. fayette. 185 pp. 44:425-429. JoRGENSEN, C. D. 1963. Spatial and time distribution of Hafner, M. S. 1977. Density and diversity in Mojave Dipodomys microps occidentalis within distinct Desert rodent and shrub communities. Anim. J. plant communities. Ecology 44:183-187. Ecol. 46:925-938. Kaufman, D. W., and G. A. Kaufman. 1982. Effect of Haldane, B. S. 1924. mathematical theory of natu- J. A moonlight on activity and microhabitat use by ral selection and artificial selection: Part 1. Cam- Ord's kangaroo rat (Dipodomys ordii). J. Mam- bridge Phil. Soc. Trans. 23:838-844. mal. 63:309-312. Hall, E. R. 1946. Mammals of Nevada. Univ. of Califor- Kay, D. a., and W. G. Whitford. 1978. The burrow en- nia Press, Berkeley and Los Angeles. 710 pp. vironment of the bannertailed kangaroo rat, Di- 1981. The mammals of North America. Ronald podomys spectabilis, in south central New Mexi- Press, New York. co. Amer. Midi. Nat. 99:270-279. races of 1972a. Saltbush leaves: excision of hy- Hall, E. R., and F. H. Dale. 1939. Geographic Kenagy, G. J. the kangaroo rats, Dipodomys microps. Occas. persaline tissue by a kangaroo rat. Science Papers Mus. Zool., Louisiana State Univ. 4:47-63. 178:1094-1096. in the Great Hall, E. R., and K. R. Kelson. 1979. The mammals of 1972b. Adaptations for leaf eating microps. Oeco- North America. Ronald Press, New York. Basin kangaroo rat, Dipodomys Hamilton, W. D. 1972. Altruism and related phenome- logia (Berl.) 12:383-412. observations of male fighting, na, mainly in social insects. Ann. Rev. Ecol. Syst. 1976. Field Great Basin 3:193-232. drumming, and copulation in the 114 Great Basin Naturalist Memoirs No. 7

rat, kangaroo Dipodonnjs microps. J. Mammal. MoNSON, G., AND W. Kessler. 1940. Life historv notes 57:781-785. on the bannertailed kangaroo rat, Merriam's King, S. R., and B. B. Babero. 1974. Helminths of kan- kangaroo rat, and the white-throated woodrat in rats, in with re- garoo Dipodomys spp., Nevada Arizona and New Mexico. J. Wildl. Mgt. 4:37-43. ports of other worm parasites from these hosts. Mullen, R. K. 1971. Energy metabolism and body wa- Proc. Helminthol. Soc. Washington 41:241-248. ter turnover rates of two species of free-living KoTLER, B. In press. Predatory risk and the community kangaroo rats, Dipodomys merriami and Di- structure of desert rodents. Ecology. podomys microps. Comp. Biochem. Phvsiol. Larsen, E. 1978. Habitat partitioning among coexisting 39:379-390.

desert rodents: two examples of species packing. Munger, J. C, AND J. H. Brown. 1981. Competition in Unpublished thesis. Utali State Univ., Logan. 44 desert rodents: an experiment with semi- permeable exclosures. Science 211:510-512. pp. P. A., D. D. Keck. flora. Lay, D. M. 1972. The anatomy, physiology, and fimc- MuNZ, AND 1959. A California Univ. of California Press, Berkelev Los tional significance of specialized hearing organs and Angeles. 1.38:41-120. in gerbilline rodents. J. Morphol. Nei, M. 1977. F-statistics and the analysis of gene diver- 1974. Differential predation on gerbils {Me- sity in subdivided populations. Hum. Genet., riones) by the little owl Athene brahma. Mam- J. Ann. 41:225-233. mal. 55:608-614. Nelson, B. C. 1980. Plague studies in California, USA: Lee, a. K. 1963. The adaptations to arid environments the roles of various species of sylvatic rodents in in woodrats of the genus Neotoma. Univ. Califor- plague ecology in California, USA. Proc. 9th Ver- nia Publ. Zool. 64:57-96. tebrate Pe.st Conf. 9:89-96. Leibold, M., and C. MuNGER. 1983. Patterns of dis- J. Nelson, B. C, and C. R. Smith. 1976. Ecological effects persal in Dipodomys merriami and D. spectabilis of a plague epizootic: the activities of rodents in- in southeastern Arizona. In preparation. habiting caves at Lava Beds National Monument, a., L. RosENZWEiG. 1978. Micro- Lemen, C. and M. California. J. Med. Entomol. 13:51-61. habitat selection in two species of heteromyid ro- Newsome, a. E., and L. K. Corbett. 1975. Outbreaks of dents. Oecologia (Berl.) .33:13-19. rodents in semiarid and arid Australia: causes, LiDiCKER, W. Z., 1960. analysis of intraspecific Jr. An preventions, and evolutionary considerations. In variation in the kangaroo rat Dipodomys mer- L. Prakash and P. K. Ghosh, eds., Rodents in riami. Univ. California Pub!. Zool. 67:125-218. desert environments. W. Junk, The Hague, The LiEBERMAN, G. A. 1974. Species diversity and abundance Netherlands. of desert rodents in several southwestern deserts. O'DowD, D. J., AND M. E. Hay. 1980. Mutualism be- Unpublished dissertation. Princeton Univ., tween harvester ants and a desert ephemeral: Princeton, New Jersey. seed escape from rodents. Ecology 63:5.31-540. LocKARD, R. B., AND D. H. OwiNGs. 1974. Seasonal vari- O'Farrell, M. 1980. Spatial relationships of rodents in a ation in moonlight avoidances by bannertail sagebnish community. J. Mammal. 61:589-605. kangaroo rats. Mammal. 55:189-193. J. O'Farrell, T. P. 1975. Small mammals: their parasites MacArthur, R. H., E. O. 1967. theo- and Wilson. The and pathologic lesions on the arid lands ecology ry of island biogeography. Princeton Univ. Press, reserve, Benton County, Washington, USA. Princeton, New Jersey. Amer. Midi. Nat, 93:377-387. MacMillen, R. E., and E. A. Christopher. 1975. The T. P., R. R. D. O'Farrell, J. Olson, O. Gilbert, and J. water relations of populations noncaptive two of Hedlund. 1975. A population of Great Basin desert rodents. In N. F. Hadley, ed.. Environ- pocket mouse, Perognathtis parvus, in the shnib- mental physiology of desert organisms. Dowden, steppe of south-central Washington. Ecol. Mon- Hutchinson Ross, Stroudsberg. and ogr. 45:1-28. Mares, M. A., and D. F. Williams. 1977. Experimental Olsen, R. W. 1976. Water as a limiting factor for a pop- support for particle size food resource allocation ulation of woodrats. Southwest. Nat. 21:391-398. in rodents. 58:454-457. heteromyid Ecology L., 1981. Patton, J. AND J. H. Feder. Microspatial ge- Maser, C, and O. Whitaker, 1980. Mites found J. Jr. netic heterogeneity in pocket gophers: non-ran- in the fur of a small sample of heteromyid ro- dom breeding and drift. Evolution 35:912-920. dents from Oregon. Northwest Sci. 54:279-280. Petryszyn, Y. 1982. Population dynamics of nocturnal May, R. M., and R. M. Anderson. 1978. Regulation and desert rodents: a nine year study. Unpublished stability of host-parasite population interactions. dissertation. Univ. of Arizona, Tucson, .\rizona. II. Destabilizing processes. Anim. Ecol. J. 108 pp. 47:249-267. Prk:e, M. V. 1978a. The role of microhabitat in struc- 1979. Population biology of infectious diseases: turing desert rodent communities. Ecology Part II. Nature 280:455-461. 59:910-921.

Maza, B. C, N. R. French, and .'\. P. Aschwanden. 1978b. Seed dispersion preferences of coexisting 1973. range dynamics in species. 59:624-626. Home a population of desert rodent J. Mammal. heteromyid rodents. Price, P. 1980. biology parasites. J. Mammal. 54:405-425. W. Evolutionary of Michod, R. 1979. Genetical aspects of kin .selection: ef- Princeton Univ. Press, Princeton, New Jersey.

fects of inbreeding. R\SMt'ssEN, D. I. 1964. Blood group polymorphism and J. Theor. Biol. 81:223-2.33. 1980. Evolution of interactions in family-struc- inbreeding in natural populations of the deer tured populations: mixed mating models. Ge- mouse Peromysctis maniculatiis. Evolution netics 96:275-296. 18:219-229. 1983 Biology of Desert Rodents 115

Read, C. P., and R. E. Millemann. 1953. Helminth par- Roth, E. 1978. Evolutionary significance of adaptations asites in kangaroo rats. Univ. C^alifornia Puhl. in heteromyid rodents in Baja California, Mexico. Zool. 59:61-80. Unpubli.shed dissertation. Univ. of Arizona, Reaka, M. L. 1980. Life history patterns and body size Tucson. in a guild of coral-dwelling mantis shrimps. Evo- RuFFER, D. G. 1965. Sexual behavior in the northern lution 34:1019-1030. grasshopper mouse (Onychomys leucogaster). Rebar, C, and W. Conley. 1983. Interactions in micro- Anim. Behav. 13:447-452. habitat use between Dipodomys ordii and Onifch- Ryckman, R. E., E. F. Archbold, and D. G. Bentlev. omys leucogaster. In preparation. 1981. The Neotoma group in North and Central Reichman, O. 1975. Relation of desert rodent diets J. to America: a checklist, literature review, and com- available resources. J. Mammal. 56:731-751. prehensive bibliography (Rodentia:Cricetidae: 1981. Factors influencing foraging patterns in Cricetinae). Bull. Soc. Vector Ecol. 6:1-92. desert rodents. In A. Kaniil and T. Sargent, eds., Schroder, G. D., and M. L. Rosenzweig. 1975. Per- Foraging behavior: ecological, ethological, and turbation analysis of competition and overlap in psychological approaches. Garland Press, New habitat utilization between Dipodomys ordii and York. Dipodomys merriami. Oecologia (Berl.) 19:9-28. O. Schmidt-Nielsen, B., and K. Reichman, J., and J. H. Brown. 1979. The use of tor- Schmidt-Nielsen. 1951. A por by Perognathus amplus in relation to re- complete account of the water metabolism in source distribution. kangaroo rats and an experimental verification. J. Mammal. 60:550-555. J. Cell. Comp. Physiol. ,38:165-181. Reichman, O. J., and D. Oberstein. 1977. Selection of Schmidt-Nielsen, B., seed distribution types by Dipodomys merriatni K. Schmidt-Nielsen, K. Brokaw, and Perognathus amplus. Ecology 58:636-643. and H. Schneiderman. 1948. Water conservation in desert rodents. Cell. O. K. J. Comp. Physiol. Reichman, J., and M. Van de Graaff. 1975. Asso- 32:331-360. ciation between ingestion of green vegetation Schwartz, O. A., and K. B. ,\rmitage. and desert rodent reproduction. 1980. Genetic J. Mammal. variation in social mammals: the 56:503-506. marmot model. Science 207:665-667. Reisen, W. K., and T. L. Best. 1973. An ectoparasite Selander, R. K. 1970. Behavior and genetic variation in survey of Dipodomys ordii (Ro- natural populations. Amer. Zool. 10:53-66. dentia:Heteromyidae) from central Oklahoma. Shelford, V. E. 1913. Animal communities in temper- Entomol. Soc. Amer., Ann. 66:599-601. ate America. Univ. of Chicago Press, Chicago. Reynolds, H. G. 1950. Relation of Merriam's kangaroo Sherman, P. K. 1977. Nepotism and the evolution of rats to range vegetation in southern Arizona. alarm calls. Science 197:1246-1253. Ecology 31:456-463. Smith, H. D., and C. D. Jorgensen. 1975. Reproductive 1958. Tlie ecology of the Merriam's kangaroo biology of North American desert rodents. In I. rat (Dipodomys merriami Mearns) on the grazing Prakash and P. K. Gho.sh, eds.. Rodents in desert lands of Arizona. Ecol. Monogr. 28:111-127. environments. W. Junk, The Hague, The Reynolds, H. G., and H. S. Haskell. 1949. Life history Netherlands. notes on Price and Bailey pocket mice of south- SoHOLT, L. F. 1977. Consumption of herbaceous vegeta- ern Arizona. J. Mammal. .30:150-156. tion and water during reproduction and devel- D., Roberts, J. and R. L. Packard. 1973. Comments on opment of Merriam's kangaroo rat, Dipodomys movements, home range, and ecology of the merriami. Amer. Midi. Nat. 98:445-457.

Texas rat elator. Thompson, S. utilization kangaroo Dipodomys J. Mam- D. 1982a. Microhabitat and mal. 54:957-962. foraging behavior of bipedal and quadrupedal Rosenzweig, M. L. 1973. Habitat selection experiments heteromyid rodents. Ecology 63:1303-1312. with a pair of coexisting heteromvid rodent spe- 1982b. Structure and species composition of cies. Ecology .54:111-117. desert heteromyid assemblages: effect of a simple 63:1313-1321. 1974. On the optimal above-ground activity of habitat manipulation. Ecology TiMM, R. M., and E. F. Cook. 1979. The effect of bot fly bannertail kangaroo rats. 55:193-199. J. Mammal. larvae on reproduction in white-footed mice, Pe- 1979. Optimal habitat selection in two-species romyscus leucopus. Amer. Midi. Nat. 101: competitive systems. Fortschr. Zool. 25:283-293. 211-217. 1981. A theory of habitat selection. Ecology Trombulak, S. C, and G. Kenagy. 1980. Effects of 62:327-336. J. seed distribution and competitors on seed har- Rosenzweig, M. L., B. Smigel, and A. Kraft. 1975. Pat- vesting efficiency in heteromyid rodents. Oecol- terns of food, space and diversity. In I. Prakash ogia (Berl.) 44:342-346. and P. K. Ghosh, eds. Rodents in desert environ- Van de Graaff, M. M., and R. P. Balda. 1973. Impor- ments. W. Junk, The Hague, The Netherlands. tance of green vegetation for reproduction in the Rosenzweig, M. L., P. Sterner. 1970. Popu- and W. kangaroo rat Dipodomys merriami merriami. J. lation ecology of desert rodent communities: Mammal. 54:509-512. body size and seed-husking as bases for hetero- Vaughan, T. a., and S. T. Schwartz. 1980. Behavioral

myid co-existence. Ecology 51:217-224. ecology of an insular woodrat. J. Mammal. Rosenzweig, L., 1969. Population 61:205-218. M. and J. Winakur. history of ecology of desert rodent communities: habitats VoRHiES, C. T., AND W. P. Taylor. 1922. Life and environmental complexity. Ecology the kangaroo rat, Dipodomys spectabilis spec- 1091:1-40. 50:558-572. tahilis merriam. U.S. Dept. Agr. Bull. 116 Great Basin Naturalist Memoirs No. 7

Warren, P. L. 1979. Plant and rodent communities of chromosomal evolution. Proc. Natl. .\cad. Sci. Organ Pipe National Monument. Unpublished USA 72:5061-5065. thesis. Univ. of Arizona, Tucson. 74 pp. Wilson, D. S. 1977. Structured denies and the evolution Webster, D. B. 1962. A fimction of the enlarged of group advantageous traits. Amer. Nat. middle-ear cavities of the kangaroo rat, Di- 111:157-185. .35:248-255. T. podomys. Physiol. Zool. WoNDOLLECK, J. 1978. Foragc-area separation and in Webster, D. B., and M. Webster. 1971. Adaptive value overlap heteromvid rodents. J. Mammal. of hearing and vision in kangaroo rat predator 59:510-518. avoidance. Brain Behav. Evol. 4:310-.322. Wright, S. 1953. Applied physiology. Oxford Univ. 1975. Auditory systems of Heteromyidae: func- Press, London. tional morphology and evolution of the middle 1940. Breeding structure of populations in rela- ear. 146:343-376. tion to specification. 74:232-248. J. Morphol. Amer. Nat. O., N. 1974. Host distri- 1965. The interpretation of population structure Whitaker, J. Jr., and Wilson. bution lists of mites (Acari), parasitic and phoret- by F-statistics with special regard to systems of

ic, in the hair of wild mammals of North Ameri- mating. Evolution 19:395-420. ca, North of Mexico. Amer. Midi. Nat. 91:1-67. 1977. Evolution and the genetics of populations. Whitford, W. G. 1976. Temporal fluctuations in den- Vol. 3. Univ. of Ghicago Press, Chicago.

sity diversity in populations. p., S. and desert rodent J. Yahr, and Kessler. 1975. Suppression of repro- Mammal. 57:351-369. duction in water-deprived Mongolian gerbils Wilson, A. C, G. L. Bush, S. M. Case, and M. C. {Meriones ungiticulatus). Biol. Reprod. King. 1975. Social structuring and rate of 12:249-254. PATTERNS OF MORPHOLOGY AND RESOURCE USE IN NORTH AMERICAN DESERT RODENT COMMUNITIES'

V. Price- M. and J. H. 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 explanation 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 relationships between morphology, foraging and predator-avoidance abilities, and behavior. We think such "microecological" 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 Our aim here is not to review exhaustively ecology is identification of factors that deter- what is known about desert rodent commu- mine the number, relative abundances, and nities, since several other authors have made phenotypic attributes of coexisting species. recent contributions of this sort (Brown 1975,

Rodents of North American deserts were im- Rosenzweig et al. 1975, Brown et al. 1979). portant in the development of this major sub- Instead, we will provide an updated over- discipline of ecology, mostly through the view of the general characteristics of these work of several influential naturalists— among communities, discuss the alternative hypoth- them Joseph Grinnell and C. Hart Merriam— eses that have been advanced to explain those who developed their ideas about limits to an- characteristics, and outline the evidence that imal distributions in large part from observ- bears on the alternatives. Finally, we will ing small mammals in the western United suggest directions for further research. We States. Their ideas have subsequently been will focus on the specialized seed-eaters of incorporated into a sophisticated body of North American deserts because much less is mathematical theory, the recent devel- known about other desert rodents, but we opment of which was stimulated primarily by will attempt to indicate when observations G. Evelyn Hutchinson and Robert H. Mac- from other dietary guilds or geographic re- Arthur (see MacArthur 1972, Hutchinson gions fit the patterns we describe. 1978). Desert rodents in general still figure heavily in commimity ecology, being widely General Patterns used for testing general theories of commu- Natural History nity organization under field conditions. They are especially suitable for such studies The rodent fauna of North American because they are small, abundant, diverse, deserts is dominated by members of the Het- and easily captured in the field and observed eromyidae, a New World family whose re- in the laboratory, and because unrelated markable similarity to unrelated Old World groups have independently colonized geo- and Australian desert forms is a textbook ex- graphically isolated arid regions. ample of convergent evolution. Like jerboas,

by Brigham Young 'From the symposium "Biology of Desert Rodents," presented at the annual meeting of the American Society of Mammalogists, hosted 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 French et al. 1974, Brown et al. 1979, are primarily granivorous and can subsist M'Closkey 1980, Petryszyn 1982, Munger et without a source of free water. They are also al., this volume). Casual observation of cli- nocturnal, live in burrows, and inchide both matic correlates of rodent "plagues" in other bipedal hopping {Dipodomys, Microdipodops) regions suggests that this is probably true in and quadrupedal bounding forms {Perog- all deserts (see references in Prakash and nathus). A more complete analysis of mor- Ghosh 1975). phological, behavioral, and ecological sim- Species diversity seems to be influenced by ilarities among unrelated desert rodents can several factors, the most obvious of which is be found in Eisenberg (1975), Brown et al. habitat complexity (Rosenzweig and Winakur (1979), and Mares (this volume). 1969, M'Closkey 1978). Positive correlations Some of the convergent features of these between diversity and habitat complexity are groups, such as xerophytic physiology and common in animal communities (MacArthur burrowing habit, are clearly responses to the 1972, Schoener 1974, Hutchinson 1978), and extreme temperatures and low rainfall that occur because coexisting species usually characterize deserts. Others, such as gra- differ in affinities for areas of particular topo- nivory, are probably indirect consequences of graphic or vegetation structure. If it is suffi- plant responses to frequent and unpredic- ciently productive, an area that is struc- table droughts. Many desert plants have turally complex can be inhabited by several adopted an "ephemeral" life history, in species, each of which specializes on a differ- which they survive unfavorable periods as ent microhabitat. Interspecific differences in seeds or (less often) as underground storage microhabitat affinity appear to be character- organs (Noy-Meir 1973, Solbrig and Orians istic of all desert rodent communities that 1977); and the resulting pool of dormant have been examined (cf. references in Pra- seeds in the soil provides a relatively abun- kash and Ghosh 1975). Among heteromyids, dant and persistent food source for a variety the bipedal kangaroo rats and kangaroo mice of birds, rodents, and ants (Noy-Meir 1974, are associated with sparse perennial vegeta- Brown et al. 1979). The significance of still tion and tend to forage in open micro- other features of desert rodents, such as prev- habitats, whereas the quadrupedal pocket alence of bipedal locomotion, remains a mat- mice are associated with dense perennial veg- ter of debate, but these features probably re- etation or rocky areas and prefer micro- flect constraints on predator avoidance or habitats under tree or shrub canopies (Ro- foraging strategies imposed by tlie physical senzweig and Winakur 1969, Rosenzweig structure of desert vegetation and soils (see 1973, Brown and Lieberman 1973, Brown Bartholomew and Caswell 1951, Brown et al. 1975, Price 1978b, Harris unpublished. Price 1979, Thompson et al. 1980, Reichman 1981, and Waser 1983). This pattern also appears Thompson 1982a,b). to occur in African deserts where bipedal jerboas are associated with open areas more Proximate Factors Affecting than are quadrupedal gerbils (e.g., Happold Abundance and Diversity 1975). Several experimental studies indicate that There is considerable evidence that indi- vegetation structure influences not just the vidual reproductive success and population number of species in North American com- densities of rodents in North American munities, but also the identities and relative deserts are limited by seed production of abundances of those species. Rosenzweig ephemeral plants, whose germination and (1973) altered a number of small plots by growth is directly tied to the amount of pre- clearing shrubs from some and augmenting cipitation falling during certain seasons (Noy- brush on others. These manipulations resulted Meir 1973). Reproductive rates of individual in significant local shifts in species composi- rodents, as well as population densities, show tion: Perognathus pcniciUatus increased in extensive temporal and geographical fluctua- density on augmented plots and decreased on tions that are closely correlated with varia- cleared plots, but Dipodomys merriami re- tion in precipitation (Brown 1973, 1975, sponded in the opposite way. Similarly, Price 1983 Biology of Desert Rodents 119

(1978b) removed half of the small shrubs seasonal variations in species occupying giv- from 25 sites within a 3.2 ha area and found en habitats (cf. Congdon 1974, Meserve 1974) predictable increases in the density of D. and for species turnover between local habi- merriami, the species that showed the most tats that differ in structure. There is not as pronounced preference for foraging in open yet sufficient evidence to evaluate rigorously spaces. Furthermore, the magnitude of local these productivity-based explanations of spe- changes in density of this species was corre- cies diversity, although they are consistent lated with the amount of shnib cover re- with results of one experimental study: arti- moved. After adding cardboard "shelters" be- ficial augmentation of seeds in a short-grass tween shrubs to experimental plots, prairie enhanced local species diversity by in- ducing invasion Thompson (1982b) observed increased abun- of a specialized granivore, Dipodorny.s ordii (Abramsky 1978). dance of species normally associated with Brown (1973, 1975) has pointed out that shrubs and decreased abimdance of kangaroo historical factors, in addition to productivity rats. "Natural" temporal or spatial changes in and habitat structure, can influence the num- vegetation appear to result in similar shifts in ber of species in heteromyid communities. rodent species composition that can be pre- He found that geographically isolated sand dicted from knowledge of microhabitat pref- dunes were inhabited by fewer species than erences (Rosenzweig and Winakur 1969, would be expected on the basis of their pro- Beatley 1976, Hafner 1977, Price 1978b, ductivity, and attributed this to decreased Price and Waser 1983). colonization rates of isolated "islands" of Among habitats that are similar in struc- suitable habitat. Historical constraints have ture, the number of rodent species increases also been invoked to account for the low di- with the predictability of annual amount and versity of rodents in South American and precipitation, which determines seed produc- Australian deserts (Brown et al. 1979). tion as well as shrub density (Brown 1973, 1975, Hafner 1977, Brown et al. 1979). The most arid parts of the Colorado and Mojave Morphological Configuration typically one or two species deserts have only of Rodent Commimities of heteromyids, whereas structurally similar but more productive areas in the Sonoran, In addition to pronounced divergence in Chihuahuan, and Great Basin deserts some- microhabitat affinities, a salient feature of times support as many as four or five species. heteromyid communities is that coexisting As might be expected, average population species differ in body size more than would densities and total rodent biomass also tend be expected if communities were random as- to be positively correlated with increased semblages of species (Fig. 1; Brown 1973, seed abundance, but it is less clear why spe- 1975, Brown et al. 1979, Bowers and Brown cies diversity should exhibit such a pattern. 1982). Such body size divergence is by no MacArthur (1969, 1972) showed that this cor- means unique to desert rodent communities; relation is expected of commimities com- in fact, it is so ubiquitous that nearly constant posed of species limited by a single resource. size ratios among coexisting species have In such resource-limited systems, species that been given the name "Hutchinson's ratios," specialize on a subset of available resources after the ecologist who drew attention to can persist only when overall production is them (Hutchinson 1959, Horn and May 1977, high enough to supply some minimal amount Lack 1971, MacArthur 1972). Heteromyid of the preferred subset during poor years. In communities are, however, one of the few has unproductive regions, abimdance of the ap- cases for which observed size spacing different from propriate resources may often fall below the been shown to be statistically et al. 1979, threshold level, causing the consumer popu- random null models (cf. Strong Sim- lations that depend on them to go extinct lo- Bowers and Brown 1982, Petersen 1982, interesting cally. Brown (1973) has proposed this expla- berloff and Boecklen 1981). It is not show size nation for geographic diversity-productivity to note that desert cricetids do and that in- correlations in heteromyid communities. A patterns typical of heteromyids, carnivorous similar explanation would also account for cluding the omnivorous and 120 Great Basin Naturalist Memoirs No. 7

100. 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. panamintinus; 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). 1983 Biology of Desert Rodents 121

gence in body size, shape, and microhabitat required to harvest seeds, and if body size affinity that characterizes heteromyid rodent and shape influence the efficiency of harvest communities. The first proposes that these in a particular microhabitat. Under these features reflect divergent predator avoidance conditions, animals can be expected to rank strategies that have evolved because there and utilize microhabitats on the basis of har- can be no single "best" escape strategy in vest rates. heterogeneous environments (cf. Rosenzweig Little progress has been made in determin- 1973, Thompson 1982a,b, Webster and Web- ing the relative importance of predation and ster 1980). An escape behavior that works harvest efficiency in shaping characteristics well away from cover, for example, may be of heteromyid communities, although authors often ineffective in dense brush either because invoke one or the other factor exclusively to explain shrubs impose physical constraints on move- microhabitat preferences or morphological attributes (cf. ment or contain different types of predators. Eisenberg 1963, Rosenzweig 1973, Brown 1973, Price 1978b, It is not difficult to imagine that morphology Thompson et al. 1980, Webster and Webster determines how easily an animal can be de- 1980, Reichman 1981, Thompson 1982a, b). tected and which escape strategies it can use The problem with treating these as alterna- effectively. If each microhabitat requires a tive hypotheses is that both factors may in- different escape strategy, then a particular fluence foraging behavior. According to op- morphology defines the relative risk associ- timal behavior models (cf. MacArthur and ated with foraging in different microhabitats. Pianka 1966, Pyke et al. 1977, Werner and The predation hypothesis can account for as- Mittelbach 1981), animals should rank micro- sociations between heteromyid form and mi- habitats according to the fitness gain realized crohabitat if animals rank microhabitats on while using them. Because fitness gain is a the basis of risk, and forage selectively in the complex function of resource harvest rates safest areas. This would cause species differ- discounted by expected costs or risks, inter- ing in morphology to differ in their ranking specific differences in microhabitat choice and use of microhabitats. Predation could could come about if species differ in their also interact availability with food to account abilities to harvest resources and/ or to avoid for diversification of form within commu- physiological stress or predation in particular nities, if predation pressure restricts the mi- microhabitats. It is difficult to devise an ex- crohabitats in which each species can forage perimental protocol that would directly dis- efficiently, so that some microhabitats are in- tinguish the relative importance of harvesting itially utilized less intensively than others. In efficiency and predator avoidance in deter- this case seeds would tend to accumulate in mining microhabitat choice, since this re- those microhabitats that are risky for resident quires that each factor be varied separately— species, such microhabitats would even- and and predation risk is not especially suscep- tually be colonized by species whose mor- tible to effective manipulation. phology and escape behavior allow their safe Until direct experimental tests of the "pre- use. dation" and "harvest efficiency" hypotheses The second hypothesis (cf. Brown 1975, can be devised, we feel the best way to begin Price 1978b, M'Closkey 1978) proposes that evaluating their importance is to examine in divergence in morphology and microhabitat detail the plausibility of the assumptions affinity is the outcome of competition for about morphology and behavior upon which seed resources. A predicted outcome of com- they are based, and to scrutinize community- petition is divergence among competitors in wide patterns for any that might be inconsis- use of limited resources, and in morphologi- tent with one or the other hypothesis. We cal and behavioral traits that influence the will concentrate on such an analysis in the efficiency with which particular types of re- rest of this section. sources can be utilized (MacArthur 1972, Lawlor and Smith 1976). This hy- Maynard Evidence for the Role of Predation pothesis can account for observed micro- rep- habitat affinities if microhabitats differ in the There can be no doubt desert rodents types of seeds they contain or in the methods resent a major food source for a variety of 122 Great Basin Naturalist Memoirs No. 7 predators. In North America, hawks, owls, mice exhibited reduced activity in the labora- snakes, and carnivorous mammals have been tory when light intensities exceeded levels reported to take rodents, and populations of typical of clear moonless nights. Similarly, all these predators are dense enough to repre- Lockard and Owings (1974, but see Schroder sent a significant source of mortality (cf. 1979) reported reductions in visitation to Pearson 1966). The importance of predation feeding stations by free-ranging Banner-tailed as a selective agent is further suggested by Kangaroo Rats during periods of moonlight. widespread correspondence between pelage Kaufman and Kaufman (1982) observed few- and substrate colors in desert rodents (Benson er kangaroo rats on standard nightly road 1933, Dice and Blossom 1937). This substrate censuses and observed more animals on visually hunt- matching has evolved because shaded than unshaded sides of the road when predators selectively attack individuals ing the moon was up. Burt Kotler (pers. comm.) that contrast with their background (Dice experimentally manipulated light levels in 1945, 1947, Smith et al. 1969, Bishop 1972, the field with lanterns and observed de- Kaufman 1974). creased foraging by desert rodents at seed Estimates of potential predation rates for trays when light levels approached those of kangaroo rats have come from experiments bright moonlight. Although these authors comparing disappearance rates of marked in- concluded that overall kangaroo rat and dividuals whose hearing had or had not been deer-mouse activity is sensitive to risk of pre- impaired experimentally (Webster and Web- dation, there is no direct evidence that the ster 1971). Thirty-three percent of normal effect of moonlight on activity has to do with and sham-operated animals disappeared predation risk. It is conceivable, for example, within a month of being released, along with that animals avoid bright light simply be- 78 percent of the deafened animals. Most of cause it is uncomfortable for dark-adapted the latter disappeared during the dark phase eyes. of the moon. Although it is impossible to tell There is also little evidence that micro- what part of the 33 percent loss of normal habitat use is influenced by predation risk. animals was caused by predation rather than Dice (1947) found that artificial bvishes re- dispersal, the 45 percent increment in loss of duced the number of deer mice taken by deafened animals suggests that predators may owls in experimental rooms, and Lay (1974) be a potentially important source of mor- remarked that owls were less successful in at- tality, at least for unwary or weakened tacking mice near an obstruction such as a animals. wall; this leads one to expect that mice are There is some evidence that rodents re- safer in structurally complex areas. Blair spond behaviorally to risk of predation, but it (1943) did not note, however, that deer mice is mostly inferred indirectly from evidence restricted their activity in the center of the relating light intensity to rodent activity, or relative to low-risk areas near walls or to predator success. Dice (1945) observed room that owls have difficulty detecting immobile the nest box when light intensities were high. prey at light intensities lower than about 7.3 Burt Kotler (pers. comm.) found that kan- X 10 ' foot-candles (values equivalent to that garoo rats spent a greater proportion of their under dense foliage on a cloudy night). Al- time under shrubs when he had increased though owls can also use hearing to locate light levels experimentally with lanterns. active prey, it is reasonable to expect hunting Taken altogether, these studies suggest that success to be higher on moonlit nights, unless light influences overall activity and micro- prey experience a correspondingly greater habitat use, but the inference that these be- ability at high light levels to detect and es- havioral changes are responses to enhanced cape from approaching predators. Webster predation risk remains tenuous. Clearly, more and Webster's (1971) observation that deaf- experimental work needs to be done. It is es- ened kangaroo rats disappeared primarily in pecially important to determine the relation- the dark phase of the moon would suggest ship between light intensity, microhabitat, tliat light can help prey as well as predator. and predation risk for different kinds of In any event, Blair (1943) noted that deer desert rodent. 1983 Biology of Desert Rodents 123

Although there are interspecific differ- subduing large prey and therefore consume ences in the ease with which rodents can es- smaller prey on average than do large pred- cape detection or attack by particular predators. In some animals, such as barnacles (cf. ators, it is not known how these behaviors are Connell 1975), an individual becomes im- related to differences in body size or shape. mune to predation once it has grown to some From the experiments of Dice (1947), Lay threshold size. Large size in heteromyids (1974), Kaufman (1974) and Webster (1962, may, therefore, confer some immunity from

Webster and Webster 1971), it appears that small predators on the one hand, but on the deer mice (Perornyscus) are much more vul- other could make them more conspicuous nerable to owls than are kangaroo rats {Dipo- and desirable for larger predators, which domys) or gerbils (Meriones); the latter two would then concentrate their efforts on these groups often remained unscathed after a preferred large prey. night's confinement in a bare room with a It is unfortunate that nobody has compared hungry owl. Several features of kangaroo rats predator escape abilities of pocket mice and have been related to their remarkable ability kangaroo rats directly, because the former to avoid predators (Bartholomew and Cas- are often assumed to lack the kangaroo rat's well 1951, Webster 1962, Webster and Web- facility in escaping predators. This assump- ster 1971, 1980). Their inflated middle ear tion is based on differences in morphology cavities enhance sensitivity to the low-fre- between heteromyid genera that are qual- quency sounds made by striking snakes and itatively similar to differences between heter- owls, and enlarged, dorsally placed eyes are omyid and cricetid rodents as a whole. It sensitive to sudden movements in dim light. may well be unwarranted. Webster and Kangaroo rats with either or both sensory Webster (1975, 1980) have examined the modes intact readily avoid attack by leaping morphology and sensory physiology of heter- suddenly upward or backward out of reach of omyid ears. They calculate that ears of all the predator. Elongated hind feet and tails three of the desert genera {Dipodornys, Mi- appear to facilitate these maneuvers, which crodipodops, Perognathus) have a theoretical are effective for predators like owls and best transmission of 94-100 percent of the in- snakes that cannot easily change trajectory cident acoustical energy reaching the outer during an attack. Because deer mice lack ears ear. This theoretical efficiency is achieved by specialized for detecting low-frequency enlargement of the tympanic membrane in soimd as well as specialized anatomy to facil- Dipodornys and Microdipodops, the two forms itate leaping, it is not clear whether they do with inflated auditory bullae, whereas it is not avoid owls effectively because they can- achieved by reduction of the stapes footplate not detect them in time, or because they can- in Perognathus. Actual sensitivity of Di- not use erratic leaping as an escape response. podmnys and Microdipodops ears to low fre- The former explanation seems more likely. quency sounds (less than about 3 k Hz) ap- Lay (1974) noted that Perornyscus made no pears greater than that of Perognathus, attempt to escape owl attack until after they judging from the sound intensity required to were captured, as though they were unaware produce a 1 juV cochlear microphonic (Web- of the predator's approach. He also noted ster and Webster 1980). This is to be ex- that Meriones, which have enlarged auditory pected from the relatively greater reduction bullae like kangaroo rats but lack their ex- in stiffness relative to mass of the middle ear treme bipedal adaptations, could effectively apparatus that is achieved by using enlarged jump or run out of the owl's way. Thus it ap- tympanic membrane rather than reduced os- pears that detection of predators is more crit- sicle mass to achieve overall auditory sensi- ical for survival than leaping ability. tivity. Although suggestive, these results are Although size apparently is important in not conclusive because cochlear micro- determining prey choice by certain predators phonics do not show actual auditory thresh- (cf. references in Hespenheide 1975, Wilson olds; behavioral studies will be necessary to

1975), it is not obvious how size influences determine to what extent the lower sensi- net predation risk among desert rodents. In tivity of Perognathus ears actually impairs general, small predators are less efficient at their ability to detect predators in nature 124 Great Basin Naturalist Memoirs No. 7

(Webster and Webster 1971). If there is a dif- 90-100 percent of millet seeds widely dis- ference between pocket mice and kangaroo persed on the soil surface in a night's time rats in susceptibility to predation it is more (Brown, unpublished); and oats sprinkled likely a function of sensory than locomotory near traps during a recent field trip to Kelso capabilities. There is no evidence that pocket Dunes, Galifornia, were harvested from 120 mice are substantially less able than bipedal of 150 traps by Dipodomys deserti (Price, to erratic leaping to avoid pred- forms use pers. obs.). In the laboratory, we have ators, even though they use quadrupedal clocked pouching rates of 16 millet seeds per bounding for straightaway running at high second in D. deserti (Price, unpublished). Fi- speeds. Bartholomew and Gary ob- (1954) nally, Monson (1943) found that D. spec- served that pocket mice are adept at erratic tabilis harvested and stored an average of leaping, an observation anyone who has tried about 20 qts of seed per month during fall to catch an escaped pocket mouse can con- seed production. The question remains, how- firm. Whether this ability to escape human ever, whether interspecific differences in pursuers implies equal facility with natural morphology imply differences in the kinds of predators is, of course, not known. seed resources that can be harvested most We conclude from this survey that pre- efficiently. dation has undoubtedly been of general im- Because differences in body size are so portance in the evolution of some aspects of pronounced among coexisting heteromyids, desert rodent behavior and morphology, but the search for correlations between size and its role in promoting divergence among co- foraging behavior has been intense. Brown existing heteromyids in morphology and mi- and Lieberman see also Brown 1975, crohabitat use has yet to be elucidated. (1973; Brown et al. 1979, Bowers and Brown 1982) initially proposed that heteromyids of differ- Evidence for the Role of Gompetition ent size partition resources in part by eating

The case for an important role of com- seeds of different size. They sieved seeds petition is stronger, but is by no means com- taken from cheek pouches and found a posi- plete. Munger and Brown (1981) recently tive correlation between body weight and av- have provided experimental evidence that erage seed size as measured by the size of heteromyids compete: removal of kangaroo sieves in which seeds settled. (This is a mea- rats results in increased densities of smaller sure of seed linear dimensions.) Lemen (1978) granivorous, but not omnivorous, rodents in subsequently reanalyzed their samples using experimental exclosures. This is the most ro- weight of hulled seeds as the measure of seed bust sort of evidence for the existence of re- size (rather than weight of the seed, hulled or source-based interspecific competition (cf. unhulled, as it was found in the pouch) and Gonnell 1975). Although such experiments found no correlation between rodent weight document the existence of competition, they and average weight of seeds taken. Labora- can tell us little about the evolutionary con- tory feeding trials generally support Lemen's sequences of this interaction for community- (1978) conclusion that body size differences level patterns of morphology and micro- do not reflect differences in seed size selec- habitat affinity. tion (Rosenzweig and Sterner 1970, Hutto The fact that seed availability limits repro- 1978; but see Mares and Williams 1977). ductive success of individuals indicates that, We have recently improved on these stud- like predation, competition must have repre- ies by offering caged heteromyids wheat sented a strong agent of natural selection, in ground to different sizes, rather than an array this case for efficient seed harvest. Anecdotal of seed species that differ in size. This con- evidence suggests that heteromyids are in- trols for confounding effects of taste prefer- deed efficient "seed-vacuuming machines." ences. We find no indication that large heter-

Lockard and Lockard (1971) found that omyids prefer large seeds; if anything, D. Dipodomys deserti could accurately pinpoint deserti harvests more small particles than do the location of a one-gram packet of millet smaller species (Fig. 3a, b; Price unpub- seed buried 20 cm in the soil. We have ob- lished). Results of these laboratory experi- served desert rodents routinely collecting ments are substantiated bv field studies of 1983 Biology of Desert Rodents 125

heteromyid food habitats, which indicate that sympatric rodents eat largely the same seed species (Smigel and Rosenzweig 1974, Reich- 2.8. man 1975, O'Connell 1979, Stamp and Oh- mart 1978). Differences in diet may reflect spatial differences in what seeds are available where the animals forage rather than intrinsic differences in what seeds are selected once they have been encountered (Reichman 1975, O'Connell 1979, M'Closkey 1980). This lack of apparent differences in seed prefer-

ence is supported by results of a preliminary laboratory study (Figure 3c; Price unpublished), in which no pronounced interspecific differences in consumption of eight seed species were observed. The discrepancy between results Brown and Lieberman (1973) obtained by sieving cheek pouch contents and those Lemen

(1978) obtained by weighing is intriguing.

We believe it is real, and that it may be the result of a body-size-dependent difference in heteromyid foraging behavior. Such a discrepancy could come about if larger heteromyids more commonly take seed heads from plants directly rather than gleaning dispersed seeds from the soil (the seed head would have a larger linear dimension than a single de- tached seed), or if the small cheek pouch volume relative to metabolic demands of smaller heteromyids (Morton et al. 1980) requires them to remove bulky husks from seeds before pouching them (a husked seed has a smaller linear dimension than an unhusked one). The former possibility could result in partitioning of seed resources, but the latter would not. In both cases, sieving would show a positive relationship between rodent and seed size, but weighing hulled seeds would not. There are other respects in which body size could influence foraging choices made by heteromyids. Price (1981, 1982a) has developed a simple model of a heteromyid foraging on a patchy seed resource. The model predicts that because harvest rates, travel speeds, and metabolic costs are allometric functions of body size, the degree to which an animal will specialize on the most profitable patches should depend on its size. Until we obtain accurate estimates of model parameters for the heteromyid system, however, we will not be able to determine 126 Great Basin Naturalist Memoirs No. 7

2.0. 1983 Biology of Desert Rodents 127 that there are no obvious differences in meta- 2.4. bohc rate between quadrupeds and bipeds travehng at the same speed. This finding does 2.0. not, however, preckide the possibiHty that 1.6. something more subtle is going on. Hoyt and Taylor (1981) were able to show that the 1.2. relationship between metabolic rate and .8^ travel velocity is not linear within a gait, and .4. that animals choose to travel at certain speeds because of this nonlinearity. If quad- 0. rupedal and bipedal animals have different preferred speeds, then there could be a real difference in their efficiency of travel that would be difficult to detect by measuring oxygen consumption of animals on a treadmill. We conclude from these preliminary observations that morphological differences among coexisting heteromyids are likely to be associated with differences in the efficiency with which various seed resources can be harvested, and consequently with differences in resource use in nature. Exactly what form resource partitioning takes, though, is still in question. The diet data reviewed earlier suggest that direct partitioning of seeds on the basis of some intrinsic property such as size, nutritional quality, or husking difficulty is not sufficient to account for observed patterns of coexistence. The conspicuous differences in microhabitat affinity among coexisting species could represent an indirect partitioning of seeds by differential patch choice if microhabitats differ in the seeds they contain or in the methods that must be used to harvest them. Detailed comparison of the seed reserves in different microhabitats has just be- gun, but preliminary results suggest substantial variation. Several workers have noted that average seed density in standard surface soil samples is higher under the canopy of shrubs than in open spaces between shrubs (cf. Goodall and Morgan 1974, Nelson and Chew 1977, Thompson 1982b). Furthermore, Reichman and Oberstein (1977) and Reich- man (1981), working in the Sonoran Desert, found that the coefficient of variation in seed density is much higher for samples taken in open spaces than for those taken under shrubs. This suggests that seeds are more clumped in open spaces. Preliminary data from another Sonoran Desert site (Price and Reichman, unpublished) extend these findings 128 Great Basin Naturalist Memoirs No. 7

seeds in the laboratory and also forages in open spaces, which appear to contain the LARGE OPEN most clumped seeds, we cannot yet be certain that any of these differences between microhabitats influence heteromyid harvest efficiencies or foraging choices; Price and her collaborators are currently studying foraging 1 r behavior in the laboratory and field to see SMALL OPEN whether this is the case. Despite the fact that we are not certain that adaptations for efficient seed harvest are ultimately responsible for microhabitat affin-

ities, there is good experimental evidence that interspecific differences in microhabitat LARGE BUSH use are sensitive to the presence of coexisting heteromyid species. Price (1978b) and Won- dolleck (1978) observed expansion and contraction in the array of microhabitats used by heteromyids when potential competitor species were experimentally removed or added, respectively. These results suggest that microhabitat specialization would diminish substantially under pressure of intraspecific com-

petition if interspecific competitors were .5 1.0 2.0 4.0 8.0 TOTAL SEED WEIGHT PER 4X4 CM SAMPLE removed permanently from an area (cf. Col- well and Fuentes 1975), and they further im- plicate competitive interactions as a major Fig. 4. Characteristics of seeds extracted from 160 cause for microhabitat preferences. The pos- 4x4 cm soil samples taken in August 1980 from each of four microhabitats at the Santa Rita Experimental sibility remains, however, that experimental Range near Tucson, Arizona. Refer to Price (1978b) for a changes in rodent densities in some way in- description of the study site and microhabitats, and to duced changes in predator density or behav- Reichman and Oberstein (1977) for a description of seed ior, and that the indirect effects of the exper- extraction techniques. A. Distribution of total weights of seed (in mg) ex- iments on predators were responsible for tracted per sample from Large Open, Small Open, microhabitat shifts. We think this is unlikely, Large Bush, and Tree microhabitats. There is significant especially since the smallest pocket mouse heterogeneity among microhabitats in seed abundance species with the most generalized morphol- (0 = 191, d.f.= 18, P < .005), which is primarily due to heavily differences between open and vegetated microhabitats ogy was the one that most used open (Large and Small Open form a homogeneous subset, as spaces (presumably the "riskiest" micro- do Large Bush and Tree). habitat) following removal of Dipodomys merriami in both sets of experiments. Never- (Fig. 4) by indicating that microhabitats theless, we hope experiments like those of differ not only in seed abundance but also in Price and Wondolleck will be repeated with the species of seed they contain and in the appropriate controls for effects of predation. density and particle size of the soil matrix In summary, we have reviewed evidence from which the seeds must be extracted. Soil that coexisting heteromyid rodents compete under shrubs and trees contains much organic for limited seed resources; that differences in debris of about the same density and particle body size and shape appear to be a.ssociated size as seeds. This could easily influence the with some differences in foraging behavior method that must be used to separate seeds and abilities; that microhabitat use is sensi- from the soil matrix. (It certainly influences tive to the presence of competitor species; the efficiency with which humans can extract that microhabitats appear to contain differ- seeds from soil samples!) Although it is in- ent seed resources; and that heteromyids may triguing that D. merriami prefers clumped prefer the types of seeds that are contained 1983 Biology of Desert Rodents 129 in the microhabitats they use in nature. All of these observations are consistent with the hy- LARGE OPEN pothesis that competition has played a major n = 346 .3. role in the evolution of two salient features of 2. heteromyid communities: divergence between coexisting species in microhabitat affinities and in body size and shape. nn I L^

-4. C/> SMALL OPEN Q n=633 ^ 3. UJ Synthesis and Prospectus (/) .2 Communities of seed-eating desert rodents < I . in North America have received such in- JLr tensive study, especially in the last decade or Z .4, LARGE BUSH so, that they are understood better than most n = l963 other terrestrial vertebrate systems. As a consequence, current views of how communities in general are organized are influenced strongly by the perspectives taken by ecolo-

^J^^^^-rr>n 1 Lr- gists who work on desert rodents. This makes TREE it imperative that we evaluate critically what n = l235 is and is not known about this model system. In the remainder of this paper we outline a way of viewing communities that integrates the divergent perspectives that have been taken by desert rodent ecologists and suggests a general direction for further research. As we have indicated in this review, a SEED SPECIES salient characteristic of heteromyid commu- Fig. 4 continued. nities is that coexisting species differ in mor- B. Species composition of seeds extracted from differ- phology and in microhabitat affinity. Few ent microhabitats. The proportional abundances of the mammalogists would argue with this state- 20 most common seed species are indicated, along with total numbers of seeds extracted (n). Again, there is sig- ment; indeed, it appears applicable to verte- nificant overall heterogeneity among microhabitats in brate communities in general. Most debate seed species composition (G = 6023, d.f. = 75, P < .005). has focused not on the existence of these pat- Large Open and Small Open form a homogeneous subset terns, but instead on the nature of the causal that is different from Large Bush or Tree, each of which mechanisms and the way that those deter- is different from all others. These data indicate that microhabitats differ not only in amounts, but also in spe- mine the number and kinds of species that cies, of seed they contain. Cep = Celtis pallida; Cb = coexist in habitats of varying structure and Cryptantha hurbigera; Cm = C. micrantha; Cp = C. productivity. There has been a tendency to pterocarpa; Fb = "faceted ball"; Fc = Filago Califor- = treat different explanations as alternative, nia; Fd = "flat disk"; Dp = Daucus ptisillus; Hsp Haplopappus sp.; = "jelly banana"; Lh = Lotus hu- mutually exclusive hypotheses, with the im- Jb mistratus; Msp = Mollugo sp.; Pa = "Panicum"; Pu = plication that accepting one means rejecting "pumpkin"; Rf = "reticulate football"; Si = "Sisym- the others. Traditionally, there have been brium"; Se = Spermolepis echinata; St = "strawberry"; two basic points of view. One emphasizes the Pr = Pectocarya recurvata; Ap = "Apium". importance of predation as a selective agent that has molded the evolution of heteromyid evolve in response to one overwhelmingly morphology, behavior, and community struc- important selective force, and that, once an ture. The other emphasizes the importance of important force has been identified, the sys- food scarcity caused by an unpredictable en- tem has been understood. It must instead be vironment and the foraging activities of the case that the behavior and morphology of competitors. an animal represent an integrated response to These traditional "one-factor" perspectives the diverse array of environmental factors naively assume that characteristics of animals that determine fitness. Therefore we feel that 130 Great Basin Naturalist Memoirs No. 7

the relevant question to address is not Which A third approach is to use detailed factor has been the most important? but in- analysis of the behavior of individuals as a ve- stead What has been the role of each factor hicle for developing testable predictions in producing the patterns we see? By adopt- about the properties of populations and com- ing the broader perspective implicit in the munities (Pulliam 1976, Werner and Mittel- second question, we reduce the risk of inter- bach 1981). Because this "microecological" preting rodent communities simplistically in approach has not yet been applied to hetero- terms only of the factors we can study con- myid rodent communities, we will elaborate veniently. To date, for example, there is little here on the method. evidence that predation has had a significant Consider the individual heteromyid rodent. effect on heteromyid community structure. To achieve genetic representation in futuie

We would be wrong, however, to conclude generations, it must be able to find sufficient from this that competition is the only factor energy and materials to grow, maintain itself, we need consider to account fully for charac- and reproduce in an environment character- teristics of these commimities. The apparent- ized by low water availability and high diur- ly overwhelming importance of competition nal and seasonal temperature fluctuations— is probably more a function of the ease with and to avoid being eaten while acquiring which one can manipulate food, habitat energy and mates. The question of the rela- structure, and competitor density,' and the tive importance of different factors for difficulty of manipulating predation risk, salient features of heteromyid community or- than a reflection of the true importance of ganization resolves itself into two questions competition relative to predation. at the individual level: (1) How is micro- A number of approaches can be used to in- habitat choice influenced by relative harvest vestigate the basis for particular community- profitability, physiological cost, and pre- level patterns. One that has been used exten- dation risk? (2) How does the morphology of sively is analysis of the patterns themselves. an individual influence its ability to harvest In this approach the expected consequences seeds and avoid predators in particular of various factors for patterns of morphology microhabitats? or resource use are developed and compared The simplest way to attack these "micro- with those exhibited by real communities. If ecological" questions is to use optimal forag- two factors yield different expected patterns, ing theory as a tool to derive predictions then in principle one can be rejected (for ex- about how the microhabitat choice of mor- ample, see Price 1982b, Strong et al. 1979). phologically distinct species ought to vary if Major problems with pattern analysis are that individuals forage so as to maximize net rate unambiguous expectations are often difficult of energy intake. By comparing observed to derive, and that very different factors of- with expected behaviors, one can ascertain ten yield similar expectations. whether constraints other than those of har- Direct experimental manipulation is an al- vest efficiency (such as predator avoidance) ternative approach that has obvious virtues, must be incorporated into foraging models to but several disadvantages as well. First, it is explain the observed microhabitat choices of often difficult to set up an appropriate and different rodent species. Of course, this ap- effective manipulation. For example, to de- proach is useful in distinguishing the relative termine the relative importance of predation importance of different constraints only if directly, one must be able to manipulate it; they yield different predicted optimal behav- and this is notoriously difficult to do in some iors. If an animal behaving so as to minimize terrestrial systems. Second, if there is no re- predation risk is predicted to behave in the sponse to a manipulation, one often doesn't same manner as one maximizing seed harvest know why. The factor could indeed be im- rates, then this approach has no power in dis- portant, but it is also possible that the manip- criminating between two very different mod- ulation was too small in scope to elicit a mea- els of behavior. In general, however, we ex- surable response, or that for one reason or pect this will not be a problem, because it another the system simply lacks the capacity seems vmlikely that the most profitable to respond. patches from a harvest efficiency point of 1983 Biology of Desert Rodents 131 view will consistently be the least risky as thus to predict how individual rodents re- well. spond to specified conditions, such as habitats Developing predictions about optimal mi- with certain physical structure, patterns of crohabitat selection is tedious, but straight- food availability, and different kinds of pred- forward because the theory is well developed ators. Unfortunately, however, these condi-

(cf. Pyke et al. 1977, Werner and Mittelbach tions themselves probably are not constants in nature, 1981). To apply it one needs to estimate but instead are variables that are known model parameters, such as how the influenced by a wide variety of factors. The short- seed resources contained in one microhabitat and long-term availability of food should depend in part differ from those contained in another, how on the foraging activities of intraspecific the expected net rate of energy harvest by an and interspecific competitors and the way these affect individual varies between microhabitats, and spatial distributions and recruitment in food plant how morphology influences these foraging populations. Similarly, the kinds of predators parameters. Armed with this knowledge, one present will be affected by the other con- can predict microhabitat preferences under specific and heterospecific prey present in an natviral or experimentally manipulated condi- area, and the predators in turn may influence tions, and test the predictions. If patterns of the abundance and distribution of prey popu- microhabitat use conform to those predicted, lations, thus affecting their interactions. If then it is in principle possible to develop these sorts of complex feedbacks are impor- testable models of niche relationships and tant in the organization of desert rodent com- competitive interactions between species munities—and we suspect that they are—then based on the assumption that interactions are they may be more easily detected and under solely exploitative in nature (cf. MacArthur stood by macroecological experimental ma- 1972, Pulliam 1976). The power of this ap- nipulations than microecological ones. For proach lies in its ability to generate simple example, a recent experiment in which we testable models of community structure added modest qualities of millet seeds to whose assumptions and predictions are ex- large areas of Chihuahuan desert habitat plicitly stated. If the model does not yield ac- (Brown and Munger, in preparation) gave the curate predictions, then the assumptions interesting result that Dipodomys spectabilis about what constraints influence behavior or increased in density and D. merriami and D. population dynamics must be wrong. Even if ordii decreased. Apparently the decline of the model is wrong, progress in under- the two smaller kangaroo rat species was a standing nature has been made, for one consequence of interference or exploitative knows that the next step is to modify the competition from the larger D. spectabilis. model so as to incorporate different assump- This response would have been difficult to tions, and test the new predictions. For exam- anticipate from microecological approaches, ples and further discussion of these points, because all three Dipodomys species should see Mittelbach (1981), Werner and Mittel- have experienced increased foraging success bach (1981), and Sih (1980, 1982). after the manipulation. A major advantage of the microecological All of this points out the limitations of our approach is that one can use it to detect the present knowledge and the need for addition- effects of factors like predation without hav- al research of many kinds. As much as we ing to manipulate predator populations di- have learned about desert rodent commu- rectly in the field. A major disadvantage is nities in the last decade or two, we have only that, although it is possible in principle to scratched the surface. Perhaps we have build models of communities from knowledge reached the stage where sufficient back- of individual behavior, in practice the num- ground work has been done to describe many ber of variables one would have to in- of the important patterns of community or- corporate into realistic behavioral models be- ganization and to suggest mechanistic hy- comes so large that the approach may turn potheses to account for these patterns. Clear- out to be unwieldy. Consider foraging behav- ly much imaginative work and many ior, for example. Microecological analyses different approaches can contribute to test- may eventually enable us to understand and ing these hypotheses. 132 Great Basin Naturalist Memoirs No. 7

Brown, H., O. Reichman, and D. W. Davidson. Acknowledgments J. J. 1979. Granivory in desert ecosystems. Ann. Rev. Ecol. Syst. 10:201-227. A great many people who share interests in CoLWELL, R. K., AND E. R. FuENTES. 1975. Experimental desert rodents have helped to develop the studies of the niche. Ann. Rev. Ecol. Syst. ideas presented here. We wish to thank espe- 6:281-310. CoNGDON, 1974. Effect of habitat quality on the distri- cially our spouses, colleagues, and students J. bution of three sympatric species of desert ro- for much intellectual stimulation; N. M. Wa- dents. 55:659-662. J. Mammal. ser and an anonymous reviewer for helpful GoNNELL, J. H. 1975. Some mechanisms producing editorial suggestions; and K. Kramer, K. structure in natural communities. In M. L. Cody and M. Diamond, eds.. Ecology and evolution Heinz, J. Munger, D. Thompson, and N. J. of communities. Press of Harvard Univ. Young for indispensable help. This research Belknap Press, Cambridge, Massachusetts. 545 has been supported by an NSF Doctoral Dis- pp. 1976. Dawson, T. J. Energetic cost of locomotion in sertation Grant, Improvement NSF Grant Australian hopping mice. Nature 259:305-.307. DEB 80-22164, Sigma Xi and University of T. R. 1973. cost of Dawson, J., and C. Taylor. Energy California, Riverside, Intramural and Faculty locomotion in kangaroos. Nature 246:313-314. Development awards to MVP, and NSF Dice, L. R. 1945. Minimum intensities of illumination under which owls can find dead prey by sight. grants (most recently DEB 80-21535) to JHB. Amer. Nat. 79:385-416. 1947. Effectiveness of selection by owls of deer- mice {Peroinyscus maniculatus) which contrast in color with their background. Contrib. Lab. Vert. Literature Cited Biol. Univ. Michigan 34:1-20. Dice, L. R., and P. M. Blossom. 1937. Studies of mam- Abramsky, Z. 1978. Small manimal community ecology: malian ecology in southwestern North America changes in species diversity in response to manip- with special attention to the colors of desert iJated productivity. Oecologia 34:113-123. mammals. Carnegie Inst. Washington, Publ. 485. F. of ro- Bartholomew, G. A., and G. R. Gary. 1954. Locomo- Eisenberg, J. 1963. The behavior heteromyid tion in 35:386-.392. dents. Univ. California Publ. Zool. 69:1-114. pocket mice. J. Mammal. Bartholomew, G. A., and H. H. Caswell, Jr. 1951. Lo- 1975. The behavior patterns of desert rodents. comotion in kangaroo rats and its adaptive signif- In I. Prakash and P. K. Ghosh, eds.. Rodents in icance. desert environments. W. Jimk, The Hague, The J. Mamma!. 32:155-169. Netherlands. 624 Beatley, J. G. 1976. Environments of kangaroo rats pp. (Dipodomys) and effects of environmental change French, N. R., B. G. Maza, H. O. Hill, A. P. A. on populations in .southern Nevada. ScHWANDEN, AND H. W. Kaaz. 1974. A popu- J, Mammal. 57:67-93. lation study of irradiated desert rodents. Ecol.

Benson, S. B. 1933. Concealing coloration among some Monogr. 44:45-72. R. desert rodents of the southwest United States. Frye, J., AND M. L. Rosenzweig. 1980. Clump size Univ. Galifornia Publ. Zool. 40:1-70. selection: a field test with two species of Di- podomys. Oecologia 47:323-327. Bishop, J. A. 1972. An experimental study of the cline of D. W., S. 1974. reserves industrial melanism in Biston betiilaria (L.) (Lepi- GooDALL, AND J. MoRGAN. Seed doptera) between urban Liverpool and rural of de-sert soils. US/IBP Res. Memo. 74-16. North Hafner, M. S. 1977. Density and diversity in Mojave Wales. J. Anim. Ecol. 41:209-243.

Blair, W. F. 1943. Activities of the chihuahua deer- Desert rodent and shrub communities. J. Anim. mouse in relation to light intensity. Ecol. 46:925-938. J. Wildl. Mgt. 7:92-97. Happold, D. C. D. 1975. The ecology of rodents in the

Bowers, M. A. 1982. Foraging behavior of heteromyid northern Sudan. In I. Prakash and P. K. Ghosh, rodents: field evidence of resource partitioning. eds.. Rodents in desert environments. W. Junk, J. Mammal. 63:361-367. The Hague, The Netherlands. 624 pp. Bowers, A., H. Hatt, R. T. 1932. The vertebral columns of ricochetal M. and J. Brown. 1982. Body size and coexistence in desert rodents: chance or commu- rodents. Bull. Amer. Mus. Nat. Hist. 63:599-738. nity stmcture? Ecology 63:.391-400. Hespenheide, H. a. 1975. Prey characteristics and predator niche width. In M. L. and M. Dia- Brown, J. H. 1973. Species diversity of seed-eating Cody J. desert rodents in sand dune habitats. Ecology mond, eds.. Ecology and evolution of comnui- 54:775-787. nities. Belknap Press of Harvard Univ. Press, 1975. Geographical ecology of desert rodents. In Cambridge, Massachu.setts. 545 pp. M. L. Horn, H. S., and R. M. May. 1977. Limits to similarity Cody, and J. M. Diamond, eds.. Ecology and evolution of communities. Belknap Press of among coexisting competitors. Nature Harvard Univ. Press, Cambridge, Mas.sachusetts. 270:660-661. 545 pp. HowKLL, A. B. 1932. The saltatorial rodent Dipodomys: the hinctional comparative anatomy of its Brown, J. H., and G. A. Lieberman. 1973. Resource uti- and hzation and coexistence of seed-eating rodents in muscular and osseous systems. Proc. .\mer. .^cad. sand dune habitats. Ecology 54:788-797. Arts and Sci. 67:377-536. 1983 Biology of Desert Rodents 133

HoYT, D. F., AND C. R. Taylor. 1981. Gait and the MuNGER, J. C, and ]. H. Brown. 1981. Competition in energetics of locomotion in horses. Nature desert rodents: an experiment with semi- 292:239-240. permeable exclosures. Science 211:510-512. Hutchinson, G. E. 1959. Homage to Santa Rosaha, or Naumov, N. p., and V. S. Lobachev. 1975. Ecology of why are there so many kinds of animals? Anier. the desert rodents of the U.S.S.R. In I. Prakash 93:145-159. Nat. and P. K. Ghosh, eds.. Rodents in desert environ- 1978. An introduction to population ecology. ments. W. Junk, The Hague, The Netherlands. Yale Univ. Press, Haven, Connecticut. New 259 624 pp. F., pp. Nelson, J. and R. M. Chew. 1977. Factors affecting HuTTO, R. L. 1978. A mechanism for resource allocation seed reserves in the soil of a Mojave Desert eco- among sympatric heteromyid rodent species. system. Rock Valley, Nye County, Nevada. Amer. Oecologia 33:115-126. Midi. Nat. 97:300-320. D. in Kaufman, W. 1974. Adaptive coloration Pe- Noy-Meir, I. 1973. Desert ecosystems: environment and romyscus polionotus: experimental selection by producers. Ann. Rev. Ecol. Syst. 4:25-51. owls. 55:271-283. J. Mammal. 1974. Desert ecosystems: higher trophic levels. Kaufman, D. W., and G. Kaufman. 1982. Effect of Ann. Rev. Ecol. Syst. 5:195-214. moonlight on activity and microhabitat use by O'Connell, M. a. 1979. Coexistence of two species of kangaroo rat ordii). Ord's {Dipodomys J. Mam- kangaroo rats (genus Dipodomys) in the Guada- mal. 63:309-312. lupe Mountains National Park, Texas. In H. H. Kennedy, M. L., and G. D. Schnell. 1978. Geographic Genoways R. Baker, eds.. and J. Biological in- variation and sexual dimorphism in Ords kan- vestigations in the Guadalupe Mountains Nation- garoo-rat, D. ordii. 59:45-59. J. Mammal. al Park, Texas. National Park Service, Washing- Lack, D. 1971. Ecological isolation in birds. Harvard ton, D.C. Univ. Press, Cambridge, Massachusetts. Pearson, O. P. 1966. The prey of carnivores during one Lay, D. M. 1974. Differential predation on gerbils (Me- cycle of 35:217- mouse abundance. J. Anim. Ecol. the little riones) by owl Athene brahma. J. Mam- 233. mal. 55:608-614. Peterson, K. E. 1982. Mammalian morphological com- Lemen, C. 1978. Seed size selection in heteromyids: a munities: random or structured? Bull. Ecol. Soc. second look. Oecologia .35:13-19. Amer. 63:69. Lemen, C, and M. L. Rosenzweig. 1978. Microhabitat Petryszyn, Y. 1982. Unpublished dissertation. Popu- selection in two species of heteromyid rodents. lation dynamics of nocturnal desert rodents: a Oecologia 33:127-135. nine year study. Univ. of Arizona, Tucson.

S. 1971. prefer- Prakash, I., and P. K. Ghosh, eds., 1975. Rodents in LocKARD, R. B., AND J. LocKARD. Seed retrieval deserti. desert environments. W. Junk, The Hague, The ence and buried seed of D. J. Mammal. 52:219-222. Netherlands. 624 pp. Price, V. 1978a. Seed dispersion preferences of co- LocKARD, R. B., AND D. H. OwiNGS. 1974. Seasonal vari- M. existing desert rodent species. Mammal. ation in moonlight avoidance by bannertail kan- J. 59:624-626. rats. 55:189-193. garoo J. Mammal. 1978b. The role of microhabitat in structuring Mares, M. A., and D. F. Williams. 1977. Experimental desert rodent communities. Ecology 59:910-921. support for food particle size resource allocation 1981. Body size and patch choice in desert ro- ill heteromyid rodents. Ecology 58:1186-1190. dents: a model for searching predators. Bull. MacArthur, R. H. 1972. Geographical ecology. Harper Ecol. Soc. Amer. 62:109. and Row, New York. 1982a. Ecological consequences of body size: a MacArthur, R. H., and E. R. Pianka. 1966. On optimal model for patch choice in desert rodents. Oecol- use of a patchy environment. Anier. Nat. ogia, in review. 100:60.3-609. 1982b. Microhabitat use in rodent communities: M'Closkey, R. T. 1978. Niche separation and assembly predator avoidance or foraging economics? Cana- in four species of Sonoran Desert rodents. Amer. dian Zool., in review. J. Nat. 112:683-694. Price, M. V., and N. M. Waser. 1983. On the relative 1980. Spatial patterns in sizes of seeds collected abundance of species: postfire changes in a coast- by four species of heteromyid rodents. Ecology al sage scrub rodent community. Ecology, in 61:486-489. review. Meserve, p. L. 1974. Temporary occupancy of a coastal Pyke, G. H., H. R. PuLLiAM, and E. L. Charnov. 1977. sage scrub community by a seasonal immigrant, Optimal foraging: a selective review of theory

the California mouse {Peromyscus caUforniciis). J. and tests. Quart. Rev. Biol. 52:137-154. 55:836-840. 1975. Relation of desert rodent diets to Mammal. Reichman, O. J. resources. 56:731-751. MiTTELBACH, G. G. 1981. Foraging efficiency and body available J. Mammal. size: a study of optimal diet and habitat use by 1976. Relationships between dimensions, bluegills. Ecology 62:1370-1386. weights, volumes, and calories of some sonoran Monson, G. 1943. Food habits of the banner-tailed desert seeds. Southwest. Nat. 20:573-586. kangaroo rat in Wildl. 7:98-102. 1981. Factors influencing foraging patterns in Arizona. J. Mgt. and T. Sargent, eds.. Morton, S. R., D. S. Hinds, and R. E. MacMillen. desert rodents. In A. Kamil ethological, and 1980. Cheek pouch capacity in heteromyid ro- Foraging behavior: ecological, dents. Oecologia 46:143-146. psychological approaches. Garland, New York. 134 Great Basin Naturalist Memoirs No. 7

D. Oberstein. 1977. Selection of Strong, D. R., Jr., L. A. Szyska, and D. S. Simberloff. Reichman, O. J., AND seed distribution types by Dipodomys merrkimi 1979. Tests of community-wide character dis- and Perognathus amplus. Ecology 58:636-643. placement against null hypotheses. Evolution RosENZWEiG, M. L. 1973. Habitat selection experiments 33:897-913. with a pair of coexisting heteromyid species. Thompson, S. D. 1982a. Microhabitat utilization and Ecology 54:111-117. foraging behavior of bipedal and quadrupedal RosENZWEiG, M. L., B. Smigel, and a. FCraft. 1975. Pat- heteromyid rodents. Ecology 63:130.3-1312.

terns of food, space, and diversity. In I. Prakash 1982b. Structure and species composition of and P. K. Ghosh, eds., Rodents in desert environ- desert heteromyid rodent species assemblages: ef- ments. W. Junk, The Hague, The Netherlands. fects of a simple habitat manipulation. Ecology 624 pp. 63:1313-1321. RosENZWEiG, M. L., AND P. Sterner. 1970. Population 1982c. Bipedal hopping and seed dispersion se- ecology of desert rodent communities: body size lection by heteromyid rodents: the role of loco- and seed husking as basis for heteromyid coexis- motion energetics. Unpubl. ms. tence. Ecology 51:217-224. Thompson, S. D., R. E. MacMillen, E. M. Burke, and L., 1969. Population C. R. Taylor. 1980. The energetic cost of biped- RosENZWEiG, M. AND J. WiNAKUR. ecology of desert rodent communities: habitats al hopping in small mammals. Nature and environmental complexitv. Ecology 287:223-224. S. 1980. Effects 50:558-571. Trombulak, C., and G. J. Kenagy. of ScHOENER, T. W. 1974. Resource partitioning in ecologi- seed distribution and competitors on seed har- cal communities. Science 185:27-39. vesting efficiency in heteromyid rodents. Oeco- Schroder, G. D. 1979. Foraging behavior and home logia 44:.342-346. range utilization of the bannertail kangaroo rat Webster, D. B. 1962. A function of the enlarged {Dipodomys spcckdiilis). Ecology 60:657-665. middle-ear cavities of the kangaroo rat, Di- SiH, A. 1980. Optimal behavior: can foragers balance podomys. Physiol. Zool. 35:248-255. two conflicting demands? Science 210:1041-1043. Webster, D. B., and M. Webster. 1971. .\daptive value 1982. Foraging strategies and the avoidance of of hearing and vision in kangaroo rat predator predation by an aquatic insect, Notonecta hoff- avoidance. Brain, Behav., Evol. 4:310-322. manni. Ecology 63:786-796. 1975. Auditory systems of heteromyidae: func- SiMBERLOFF, D., AND W. BoECKLEN. 1981. Santa Rosalia tional morphology and evolution of the middle size ratios ear. reconsidered: and competition. Evolu- J. Morph. 146:343-376. tion .35:1206-1228. 1980. Morphological adaptations of the ear in

Smith, M. H., R. W. Blessing, J. L. Carmon, and J. B. rodent family Heteromyidae. Amer. Zool. Gentry. 1969. Coat color and survival of dis- 20:247-254. placed wild and lab-reared old-field mice. Acta Werner, E. E., and G. G. Mittelbach. 1981. Optimal Tlieriol. 14:1-9. foraging: field tests of diet choice and habitat Smigel, B. VV., and M. L. Rosenzweig. 1974. Seed se- switching. Amer. Zool. 21:813-829.

lection in Dipodomys merriami and Perognathus Wilson, D. S. 1975. The adequacy of body size as a penicillatus. Ecology 55:329-339. niche difference. Amer. Natur. 109:769-784. Solbrig, O. T., 1977. and G. H. Orians. The adaptive Wondolleck, J. T. 1978. Forage-area separation and characteristics of desert plants. Scient. overlap in rodents. Amer. heteromyid J. Mammal. 65:412-421. 59:510-518. NOTICE TO CONTRIBUTORS

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