The effects of owl predation on the foraging behavior of heteromyid rodents

Summary Researchers have documented microhabitat partitioning among the heteromyid rodents of the deserts of North America that may result from microhabitat specific predation rates; large/bipedal species predominate in the open/risky microhabitat and small/quadrupedal species predominate in the bush/safer microhabitat. Here, we provide direct experimental evidence on the role of predatory risk in affecting the foraging behavior of three species of heteromyid rodents: Arizona pocket mouse (Perognathus amplus; small/quadrupedal), Bailey's pocket mouse (P. baileyi; large/quadrupedal), and Merriam's kangaroo rat (Dipodomys merriami; large/bipedal). Both kangaroo rats and pocket mice are behaviorally flexible and able to adjust their foraging behavior to nightly changes in predatory risk. Under low levels of perceived predatory risk the kangaroo rat foraged relatively more in the open microhabitat than the two pocket mouse species. In response to the presence of barn owls, however, all three species shifted their habitat use towards the bush microhabitat. In response to direct measures of predatory risk, i.e. the actual presence of owls, all three species reduced foraging and left resource patches at higher giving up densities of seeds. In response to indirect indicators of predatory risk, i.e. illumination, there was a tendency for all three species to reduce foraging. The differences in morphology between pocket mice and kangaroo rats do appear to influence their behavioral responses to predatory risk.     

Microhabitat use in coexisting desert rodents—The role of population density

Summary Among some species of Sonoran Desert rodents microhabitat differences are density dependent. I studied the differences in microhabitat use among four species of heteromyid rodents (Dipodomys merriami, Perognathus amplus, P. baileyi, and P. penicillatus) at low and at high population densities. Microhabitats are defined by the abundance and size distribution of desert shrubs. During a period of low population density the rodent species showed substantial microhabitat differentiation. Following a large increase in pocket mouse (Perognathus spp.) numbers differences in microhabitat use between species disappeared. The lack of microhabitat differentiation at high density is due to microhabitat shifts rather than an expansion in the number of microhabitats used. The shifts lead to increased similarity among species in microhabitat use. Microhabitat overlap is not constant but it is highly variable and sensitive to changes in rodent abundance.     

Microhabitat selection in two species of heteromyid rodents

Summary An experiment was conducted to determine the microhabitat preferences of two heteromyid rodents, Dipodomys ordi and Perognathus flavus. This experiment used marked seeds and the atomic absorption spectrophotometer in order to study the environment as a mosiac of microhabitats. The results of our analysis indicate that these two heteromyids are microhabitat selectors. The preferences of the rodents are D. ordi: grass habitat 0.0%, near grass habitat 22.5%, open habitat 77.4% and P. flavus: grass habitat 46.2%, near grass habitat 32.2%, open habitat 21.4%. The overlap between the two species is only 0.43.     

Tactile discriminatory ability and foraging strategies in Kangaroo rats and pocket mice (Rodentia: Heteromyidae)

Summary A comparative study of seasonal food hoarding activity and tactile discriminatory ability in four species of heteromyid rodents (Dipodomys panamintinus, D. merriami, Perognathus longimembris, and P. formosus) was conducted in laboratory test arenas. Animals were tested individually to determine their treatment of seed (white millet) and seed mimics (glass beads and gravel) offered as food. In general, all animals showed low levels of millet hoarding activity during winter months with higher levels in fall and spring. Observations revealed that all species manipulated (with the forepaws) each potential food item prior to eating, pouching, or rejecting it. These tactile cues appear to surpass visual and olfactory cues as critical factors in distinguishing between food and food mimics. Pocket mice (Perognathus) showed high levels of tactile discriminatory ability which may serve as the mechanism by which they achieve high foraging efficiency in nature when filter-feeding for widely dispersed seed resources. Kangaroo rats (Dipodomys), on the other hand, are less adept at distinguishing between food and very similar non-food items. The fact that, in nature, kangaroo rats depend heavily on clumped food resources may obviate the need for highly efficient tactile discriminatory abilities.     

The influence of ambient temperature,seed composition and body size on water balance and seed selection in coexisting heteromyid rodents

Summary The water balance of three different sized coexisting species of heteromyid rodents (Dipodomys merriami ca. 39 g;Perognathus fallax ca. 23 g;Perognathus longimembris ca. 9 g) was assessed while consuming two different diets (either wheat or hulled sunflower) at ambient temperatures of 15–30°C. The metabolism of wheat as the sole food source was calculated to provide a greater metabolic water production (MWP) than the consumption of sunflower seed because of their different composition. The state of water balance was assessed by measuring urine concentrations and body weight maintenance on each diet at each temperature. Both measures showed that (i) all species were able to maintain a more positive water on the higher MWP seed, (ii) for all species there was an ambient temperature above which water balance could no longer be maintained, (iii) that this temperature was higher with the higher MWP food source and (iv) water regulatory efficiency was negatively correlated with body mass.Dipodomys showed a reduced digestive efficiency compared toPerognathus. When presented with both seedsDipodomys showed no preference for either seed irrespective of the state of water balance whilst thePerognathus species showed a tendency for an increased preference for the high MWP food source at the higher ambient temperatures. The ecological implications of these findings are discussed.     

Salivary glands of heteromyid rodents, with a summary of the literature on rodent submandibular gland morphology

The principal parenchymal elements of the submandibular glands of the heteromyid rodents Dipodomys merriami, Perognathus longimembris, Perognathus fallax, Perognathus penicillatus and Perognathus baileyi consist of acini, granular tubules and striated ducts. Acinar cells of the four species of Perognathus are aniline blue, PAS (magenta) and Alcian blue (pH 2.5) positive and metachromatic with toluidine blue and safranin. The granules of the tubule cells are orthochromatic and react with aniline blue, orange G, the PAS reagent (deep pink) and the tryptophan indicator, xanthydrol. Acinar and tubule cells of D. merriami exhibit similar reactions except for the Alcian blue stain. Acinar cells of D. merriami do not react with Alcian blue. Submandibular glands of D. merriami exhibit a sexual dimorphism of the granular tubules. There is little observable difference between the sexes in the species of Perognathus but the ratio of granular tubules to acinar elements, the degree of hypertrophy of the tubules, and the amount of mucosubstance and protein (granules) contained in their cells are different in the four species studied. Since these desert rodents have similar habitats and habits, the differences observed between the two heteromyid subfamilies studied, as well as among the four members of a single subfamily, suggest that these are inherent species variations rather than variations of adaptation to environment.     

Microhabitat segregation in two desert rodent species: the relation of prey availability to diet

Summary I studied diet in relation to microhabitat use in two desert rodents:Microdipodops megacephalus, the dark kangaroo mouse, andPeromyscus maniculatus, the deer mouse. Contrary to expectation, both species ate primarily arthropods, which were most abundant near shrubs.Peromyscus used the area near shrubs, in contrast toMicrodipodops, which used open microhabitat. As a consequence, the diet ofPeromyscus was narrower and more concentrated on abundant prey types than that ofMicrodipodops. Thus microhabitat segregation, which is frequently reported for desert rodents, is related to a diet-breadth difference between these rodents. The use of open microhabitat and low density resources byMicrodipodops, when compared with the large bipedalDipodomys and small quadrupedalPerognatus, suggests that bipedal locomotion in desert rodents is related to use of open microhabitat, and that body size is related to density of food resources.     

A mechanism for resource allocation among sympatric heteromyid rodent species

Summary Laboratory feeding experiments were conducted with Dipodomys ordii and Perognathus flavus in an attempt to discover a mechanism which might result in seed size selection. There was no marked difference in the proportions of four seed types collected whether the rodents foraged in the presence or absence of one another. However, analysis of the variability in weight of each of the seed types collected by the two species showed that when alone, the larger kangaroo rat was less effective at harvesting all of a uniformly distributed mixture of seeds. When in the presence of one another both species could harvest enough of the mixed, uniformly distributed seed to coexist indefinitely, but when the food source was presented as four large clumps the kangaroo rat's foraging effectiveness increased tremendously so that the pocked mouse was almost entirely unable to harvest any seed. These data, in light of mobility differences between large and small heteromyids, suggest a mechanism whereby the larger, more mobile kangaroo rats forage for the most readily available (large or clumped) seeds over a relatively large area. The smaller pocket mice, by virtue of their relative efficiency in harvesting seeds can utilize the less detectable seeds which are energetically too demanding for the larger kangaroo rats to harvest. Behavioral dominance of the larger animals may help prevent the smaller from utilizing the most readily available seeds. The patterns of seed size and foraging site selection described in the literature may be easily accounted for by this difference in foraging strategy.     

A mast‐seeding desert shrub regulates population dynamics and behavior of its heteromyid dispersers

Granivorous rodent populations in deserts are primarily regulated through precipitation‐driven resource pulses rather than pulses associated with mast‐seeding, a pattern more common in mesic habitats. We studied heteromyid responses to mast‐seeding in the desert shrub blackbrush (Coleogyne ramosissima), a regionally dominant species in the Mojave–Great Basin Desert transition zone. In a 5‐year study at Arches National Park, Utah, USA, we quantified spatiotemporal variation in seed resources in mast and intermast years in blackbrush‐dominated and mixed desert vegetation and measured responses of Dipodomys ordii (Ord's kangaroo rat) and Perognathus flavescens (plains pocket mouse). In blackbrush‐dominated vegetation, blackbrush seeds comprised >79% of seed production in a mast year, but 0% in the first postmast year. Kangaroo rat abundance in blackbrush‐dominated vegetation was highest in the mast year, declined sharply at the end of the first postmast summer, and then remained at low levels for 3 years. Pocket mouse abundance was not as strongly associated with blackbrush seed production. In mixed desert vegetation, kangaroo rat abundance was higher and more uniform through time. Kangaroo rats excluded the smaller pocket mice from resource‐rich patches including a pipeline disturbance and also moved their home range centers closer to this disturbance in a year of low blackbrush seed production. Home range size for kangaroo rats was unrelated to seed resource density in the mast year, but resource‐poor home ranges were larger (P < 0.001) in the first postmast year, when resources were limiting. Blackbrush seeds are higher in protein and fat but lower in carbohydrates than the more highly preferred seeds of Indian ricegrass (Achnatherum hymenoides) and have similar energy value per unit of handling time. Kangaroo rats cached seeds of these two species in similar spatial configurations, implying that they were equally valued as stored food resources. Blackbrush mast is a key resource regulating populations of kangaroo rats in this ecosystem.     

The foraging behavior of granivorous rodents and short-term apparent competition among seeds

The foraging behavior of a predator species is thought to bethe cause of short-term apparent competition among those preyspecies that share the predator. Short-term apparent competitionis the negative indirect effect that one prey species has onanother prey species via its effects on predator foraging behavior.In theory, the density-dependent foraging behavior of granivorousrodents and their preference for certain seeds are capable of inducing short-term apparent competition among seed species.In this study, I examined the foraging behavior of two heteromyidrodent species (family Heteromyidae), Merriam's kangaroo rats(Dipodomys merriami) and little pocket mice (Perognathus longimembris).In one experiment I tested the preferences of both rodent speciesfor the seeds of eight plant species. Both rodent species exhibiteddistinct but variable preferences for some seeds and avoidanceof others. However, the differences in preference appearedto have only an occasional effect on the strength of the short-term apparent competition detected in a field experiment. In anotherexperiment, I found that captive individuals of both rodentspecies had approximately equal foraging effort (i.e., timespent foraging) in patches that contained a highly preferredseed type (Oryzopsis hymenoides) regardless of seed density and the presence of a less preferred seed type (Astragalus cicer)in the patches. The rodents also harvested a large proportionof O. hymenoides seeds regardless of initial seed density;this precluded a negative indirect effect of A. cicer on O.hymenoides. But there was a negative indirect effect of O.hymenoides on A. cicer caused by rodents having a lower foragingeffort in patches that only contained A. cicer seeds than inpatches that contained A. cicer and O. hymenoides seeds. Theindirect interaction between O. hymenoides and A. cicer thusrepresented a case of short-term apparent competition thatwas non-reciprocal. Most importantly, it was caused by theforaging behavior of the rodents.     

Effects of seed distribution and competitors on seed harvesting efficiency in heteromyid rodents

Summary The foraging strategies of four naturally co-existing heteromyid rodent species were investigated: Dipodomys deserti (100 g), D. merriami (38 g), Microdipodops pallidus (13 g), and Perognathus longimembris (7 g). In 208 over-night laboratory foraging trials animals were provided with millet seed distributed in clumped and scattered patterns. Net removal of seeds from the foraging arena and amounts of seeds in cheek pouches and in caches were determined. When alone in an areana none of these species specialized extensively on either clumped or scattered seeds, although each tended to take more clumped than scattered seeds. When placed together with other individuals, animals once again tended to cache more clumped than scattered seeds in all but one paired combination of species: P. longimembris cached more scattered than clumped seeds when opposed by D. deserti. This suggests that the smaller species obtained a less preferred distribution of seeds in the face of competition. The two smaller species showed a great reduction in general foraging success in the presence of either of the two larger species. In general, a species cached less seeds when faced by larger opponent species.     

MITOCHONDRIAL DNA PHYLOGEOGRAPHY OF PEROGNATHUS AMPLUS AND PEROGNATHUS LONGIMEMBRIS (RODENTIA: HETEROMYIDAE): A POSSIBLE MAMMALIAN RING SPECIES

Substantiated cases of ring species in mammals are rare. I examined the variation in mitochondrial DNA (mtDNA) of Perognathus amplus and P. longimembris in and around Arizona to test the hypothesis proposed by Hoffmeister (1986) that these two taxa are members of a single ring species demonstrating circular overlap. Through digestion of purified mtDNA from 45 P. amplus and 35 P. longimembris with 16 type II restriction enzymes, I identified 38 distinct haplotypes that belong to eight different evolutionary lineages. I then amplified and directly sequenced a portion of the mitochondrial cytochrome-b region from individuals representative of the lineages identified by restriction fragments, and used these data for phylogeny reconstruction in both a parsimony and neighbor-joining setting. The resulting phylogeny was consistent with the ring hypothesis, but, based on the incompleteness of the ring of subspecies and the apparent timing of evolutionary events in this group, I conclude that P. amplus and P. longimembris are distinct lineages that have completed the speciation process.     

Granivory and microhabitat use in Australian desert rodents: are seeds important?

The diet and microhabitat use of two species of native Australian desert rodents, the spinifex hoppingmouseNotomys alexis and sandy inland mousePseudomys hermannsburgensis, were studied in the Simpson Desert, south-western Queensland. Contrary to expectation, both species were confirmed from analyses of their stomach contents to be omnivorous. The diets of both species varied through time in a similar manner; seeds were important in summer and especially in winter, but in autumn invertebrates constituted nearly 50% and 60% of the diet ofN. alexis andP. hermannsburgensis, respectively. Other plant material (root, leaf, floral part, stem) was found in appreciable amounts in the stomach contents of both species, and fungi were identified from a small number of individuals. Both species showed a high degree of overlap in the broad types of food they ingested (seed, plant material, invertebrates); however, there was considerably less overlap in the species of seeds eaten. Analysis of microhabitat use suggested that this difference was due to differential foraging between the species; the larger, bipedalN. alexis forages in the open more than the smaller, quadrupedalP. hermannsburgensis, which is found more commonly in or under hummocks of spinifex grass. Although our findings parallel patterns of morphological specialisation and differential foraging on seeds that have been described within communities of North American heteromyid rodents, we found little evidence that the foraging economics ofN. alexis orP. hermannsburgensis should depend solely or primarily on the distribution patterns of seeds. In the absence of dietary information, we suggest that ecological studies of desert rodents which focus solely on granivory, and neglect other important aspects of rodent foraging, can lead to a misinterpretation of species coexistence and community structure.     

Redundant or complementary? Impact of a colonizing species on community structure and function

Recent studies suggest that species with similar functional traits will have similar effects on ecosystems, but evidence for redundancy of species impacts is limited. Here we use a long‐term experiment to gain insight into functional relationships within a desert rodent community. Experimental removal of kangaroo rats, Dipodomys spp., coupled with the recent, serendipitous colonization of a single species of large pocket mouse Chaetodipus baileyi yielded treatments that differed in the diversity of large granivorous rodents present. We evaluated functional overlap of C. baileyi and the other resident large granivores (i.e. the kangaroo rats) by comparing total energy use of granivorous rodents and total abundance and species richness of small granivores across treatments before and after the arrival of C. baileyi. We found that C. baileyi almost completely compensated for the changes in these key ecosystem‐level properties caused by kangaroo rat removal, but it differentially impacted the population dynamics of individual small granivorous rodent species. Thus, its effects were largely complementary, rather than redundant, to those of the missing kangaroo rats. Although short‐term or single‐measure analyses may suggest redundancy, our results support the longstanding dictum that niches of coexisting species are often similar but rarely, if ever, identical.     

Cheek pouch capacities and loading rates of heteromyid rodents

Rodents of the family Heteromyidae are proficient gatherers and hoarders of seeds. A major component of their adaptive specialization for harvesting and transporting seeds is their spacious, fur-lined cheek pouches. Precise measurements of cheek pouch capacities are essential if ecologists are to understand the foraging ecology, possible constraints on locomotion patterns, and competitive relationships of heteromyid rodents. To measure the size of these cheek pouches and the rate at which animals load seeds into their pouches during seed harvest, we attracted 56 individuals representing ten species of heteromyid rodents to bait stations in the field and allowed them to fill their cheek pouches with seeds several times while we observed and timed the events with the aid of night-vision equipment. The largest load taken by each individual was used as an estimate of its cheek pouch capacity. At the end of observations, each subject was captured and its mass and other data gathered. The allometric relationship between cheek pouch capacity and body mass for ten species of heteromyids was significant [pouch capacity (ml) = 0.148 body mass (g)^0.992, r ²=0.91, P<0.0001]. The regression coefficient is ≈1.0, which indicates that the volume of the cheek pouches scales in direct proportion to body size. When the data were subdivided into quadrupeds (Perognathus and Chaetodipus) and bipeds (Dipodomys) (n=5 for each), the relationships between pouch capacity and body mass were significant, but the two regressions were not significantly different from each other. When all loads (full and partial) were considered, subjects filled their cheek pouches an average of 93 ± 10% of pouch capacity (n=185). Cheek pouch capacities from published studies of artificially filled pouches of heteromyids in the laboratory averaged about 40% below the field measurements obtained here. The allometric relationship between mean loading rate and body mass was also significant [seeds/s=1.067 bodymass (g)^0.830, r ²=0.85,P=0.0011), but when quadrupeds and bipeds were considered separately, the relationships were not significant. Seed densities and bulk densities were used to calculate packing coefficients for seed species, which, when used in conjunction with the allometric relationship between cheek pouch capacity and body size, can be used to estimate the maximum load carried by a heteromyid. Except for the very largest kangaroo rat species, a full pouch load of Indian ricegrass seeds represents less than the daily energy requirements of an active heteromyid. Received: 3 March 1997 / Accepted: 15 July 1997     

Mechanisms for the keystone status of kangaroo rats: graminivory rather than granivory?

Graminivory by kangaroo rats (Dipodomys spp.) was investigated as a potential mechanism for the keystone role of these rodents in the dynamics of desert grasslands. Experiments confirmed that Ord's kangaroo rats (Dipodomys ordii) cut and consumed a large proportion of the tillers of three Chihuahuan Desert tussock-forming grass species. Field observations indicated that the characteristically cut grass tillers were absent from all-rodent and medium-sized kangaroo rat exclosures, but were frequent in large-sized kangaroo rat and rabbit exclosures, indicating that the medium-sized kangaroo rats (D. ordii, D. merriami) were responsible for grass cutting. Tiller waste as a percentage of peak standing crop ranged from 7% in grassland habitats to 0.7% in Flourensia cernua shrubland. Of the 13 species of perennial, tussock-forming grasses measured, only one, Muhlenbergia porteri, had no tillers cut by kangaroo rats. This study demonstrates that the keystone role of kangaroo rats in Chihuahuan Desert grassland ecosystems is probably the result of their graminivory. Received: 28 October 1996 / Accepted: 26 February 1997     

Differential vulnerability to predation and refuge use in competing larval salamanders

The aquatic larvae of two species of salamanders coexist as a result of differences in their competitive abilities: Ambystoma talpoideum is a superior aggressor, whereas A. maculatum is a superior forager. I examined the behavioral mechanisms that permit these species to coexist with their predatory congener, A. opacum. I asked whether the two prey species differ in their vulnerability to predation and in their use of structural and spatial refugia when under the risk of predation; such inter-specific variation may allow predation to contribute indirectly to prey coexistence. Larval A. maculatum (the superior forager) was more vulnerable to predation by A. opacum than was A. talpoideum, and only the latter species significantly increased its use of structural refugia (leaf litter) in the presence of the predator. In pond enclosures, both species of prey exhibited diel patterns of microhabitat use; significantly more larvae occupied shallow regions of enclosures during the day and migrated to deeper water (a spatial refugium) at night. However, when considered separately, neither (1) the presence of a predatory larval A. opacum nor (2) an increased density of intra- and interspecific competitors significantly altered this habitat shift for either prey species. Rather, diel microhabitat usage in A. talpoideum was significantly affected by an interaction between predator presence and competitor density. My results demonstrate the importance of refugia to coexistence in this predator-prey assemblage. Furthermore, predation by A. opacum may mediate prey competition; that is, preferential consumption of A. maculatum may reduce the competitive impact of this superior forager on A. talpoideum, thus enhancing their coexistence.     

Minimal metabolism, summit metabolism and plasma thyroxine in rodents from different environments

Rodents were live-trapped in three environments (desert, intermediate and coastal) in Southern California, USA, chosen because of the taxonomic overlap of species. Upon capture, blood samples were taken and plasma thyroxine concentrations were measured. Four species (Dipodomys merriami, Perognathus fallax, Peromyscus eremicus and Peromyscus californicus) were returned to the laboratory for measurement of minimal and summit rates of metabolism. Heteromyid rodents had significantly lower plasma thyroxine concentrations (14-44 nmol l-1) than cricetid rodents (18-93 nmol l-1). Although there was significant habitat difference in plasma thyroxine levels, this influence was not constant between heteromyid and cricetid rodents. In most species, the desert individuals had the lowest plasma thyroxine concentration. Minimal metabolic rates were lower than expected in all four species, as well as in the tropical heteromyid Liomys salvini and summit metabolic rates were similarly reduced in all species. Upon capture there was considerable variation in plasma thyroxine concentration of different species (23-93 nmol l-1). However, following 10 weeks in captivity, the range and variability of plasma thyroxine levels in these species was considerably reduced (32-64 nmol l-1).