Competitive release in microhabitat use among coexisting desert rodents: a natural experiment

Summary Competitive release among desert rodents on sand dunes of differing species richness was examined in the Great Basin and Mohave Deserts, USA. Expansions in microhabitat use were exhibited by the kangaroo rats Dipodomys ordii and D. merriami (granivorous heteromyid rodents, weighing 49 and 42 g, respectively) as the number of coexisting heteromyid species decreased geographically. Perognathus longimembris, the only common small heteromyid species (7 g) exhibited no competitive release. This may be due either to the absence of competitive interactions that affect the use of space by P. longimembris or to an unacceptable increase in risk of predation that precludes the use of more open microhabitats even in the absence of kangaroo rats. The breadth of microhabitat use of an omnivorous cricetid, Peromyscus maniculatus, decreased as the density of Perognathus longimembris increased, and increased as the density of conspecifics increased. The evidence for competitive release in Dipodomys and not in Perognathus is consistent with the hypothesis that species in the same guild and of similar size compete more intensely than species of disparate size.     

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 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.     

Effect of predation risk on selectivity in heteromyid rodents

Variations in predation risk affect the costs of foraging and may therefore warrant different foraging decisions. One class of models ("higher requisite profit") predicts that foragers should become more selective when predation risk increases, as low-profitability items that do not cover the increased costs are dropped from the diet. An alternative class of models ("reduced finickiness") predicts that foragers should become less selective when predation risk increases, because selectivity requires more extensive assessment and/or search behaviour, prolonging exposure to risk. We assessed the selectivity of foraging heteromyid rodents (Merriam's kangaroo rats, Dipodomys merriami, and pocket mice, Chaetodipus spp.) by comparing differences in "giving up densities" (GUD: the quantity of cryptic food left in a patch by animals for whom the diminishing marginal gains from foraging have dropped below the threshold for continued search) for foods of different value as a measure of selectivity in patches varying in predation risk. Data collected over two field seasons revealed that heteromyids were more selective when predation risk was highest; away from the protective cover of shrubs during the full moon. These findings support the predictions of higher requisite profit models.     

The effect of barn owls (Tyto alba) on the activity and microhabitat selection of Gerbillus allenbyi and G. pyramidum

Predation plays an important role in ecological communities by affecting prey behavior such as foraging and by physical removal of individual prey. In regard to foraging, animals such as desert rodents often balance conflicting demands for food and safety. This has been studied in the field by indirectly manipulating predatory risk through the alteration of cues associated with increased risk such as cover or illumination. It has also been studied by directly manipulating the presence of predators in aviaries. Here, we report on experiments in which we directly manipulated actual predatory risk to desert rodents in the field. We conducted a series of experiments in the field using a trained barn owl (Tyto alba) to investigate how two species of coexisting gerbils (Gerbillus allenbyi and G. pyramidum) respond to various cues of predatory risk in their natural environment. The gerbils responded to risk of predation, in the form of owl flights and owl hunger calls, by reducing their activity in the risky plot relative to the control plot. The strongest response was to owl flights and the weakest to recorded hunger calls of owls. Furthermore, when risk of predation was relatively high, as in the case with barn owl flights, both gerbil species mostly limited their activity to the safer bush microhabitat. The response of the gerbils to risk of predation disappeared very quickly following removal of the treatment, and the gerbils returned to normal levels of activity within the same night. The gerbils did not respond to experimental cues (alarm clock), the presence of the investigators, the presence of a quiet owl, and recorded white noise. Using trained barn owls, we were able to effectively manipulate actual risk of predation to gerbils in natural habitats and to quantify how gerbils alter their behavior in order to balance conflicting demands of food and safety. The method allows assessment of aspects of behavior, population interactions, and community characteristics involving predation in natural habitats.     

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.     

Effects of predatory risk and resource renewal on the timing of foraging activity in a gerbil community

The foraging decisions of animals are often influenced by risk of predation and by the renewal of resources. For example, seed-eating gerbils on sand dunes in the Negev Desert of Israel prefer to forage in the bush microhabitat and during darker hours due to risk of predation. Also, daily renewal of seed resource patches and timing of nightly foraging activity in a depleting environment play important roles in species coexistence. We examined how these factors influence the timing of gerbil foraging by quantifying foraging activity in seed resource patches that we experimentally renewed hourly during the night. As in previous work, gerbils showed strong preference for the safe bush microhabitat and foraged less in response to high levels of illumination from natural moon light and from artificial sources. We demonstrate here for the first time that gerbils also responded to temporal and spatial heterogeneity in predatory risk through their timing of activity over the course of each night. Typically, gerbils concentrated their activity early in the night, but this changed with moon phase and in response to added illumination. These results can be understood in terms of the nature of patch exploitation by gerbils and the role played by the marginal value of energy in determining the cost of predation. They further show the dynamic nature of gerbil foraging decisions, with animals altering foraging efforts in response to time, microhabital, moon phase, illumination, and resource availability.     

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.     

Foraging strategies of an insectivorous marsupial,Sminthopsis youngsoni (Marsupialia: Dasyuridae), in Australian sandridge desert

This study investigated the effects of predation risk, dune position and microhabitat on foraging of the Lesser Hairy‐footed Dunnart Sminthopsis youngsoni, a small insectivorous marsupial, in the Simpson Desert of western Queensland. The intensity of foraging was assessed by establishing feeding stations (dishes containing mealworms) in open and bush microhabitats at three levels on sand dunes, and recording the numbers of prey taken by dunnarts from the stations after nightly bouts of foraging. Risk of predation was manipulated by provision of artificial illumination at alternate feeding stations on each of five occasions when trials were run. The numbers of mealworms left after feeding bouts varied inconsistently across trials, providing little evidence that dunnarts respond to habitat or predation risk while foraging. These results contrast sharply with studies of arid zone rodents, where foraging is usually sensitive to both predation risk and resource distribution. We suggest that S. youngsoni forages equally in all habitats of its sandridge environment, and experiences relatively low risk of predation whilst doing so.     

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.     

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.     

Collision-based mechanics of bipedal hopping

The muscle work required to sustain steady-speed locomotion depends largely upon the mechanical energy needed to redirect the centre of mass and the degree to which this energy can be stored and returned elastically. Previous studies have found that large bipedal hoppers can elastically store and return a large fraction of the energy required to hop, whereas small bipedal hoppers can only elastically store and return a relatively small fraction. Here, we consider the extent to which large and small bipedal hoppers (tammar wallabies, approx. 7 kg, and desert kangaroo rats, approx. 0.1 kg) reduce the mechanical energy needed to redirect the centre of mass by reducing collisions. We hypothesize that kangaroo rats will reduce collisions to a greater extent than wallabies since kangaroo rats cannot elastically store and return as high a fraction of the mechanical energy of hopping as wallabies. We find that kangaroo rats use a significantly smaller collision angle than wallabies by employing ground reaction force vectors that are more vertical and center of mass velocity vectors that are more horizontal and thereby reduce their mechanical cost of transport. A collision-based approach paired with tendon morphometry may reveal this effect more generally among bipedal runners and quadrupedal trotters.     

Predator avoidance,microhabitat shift,and risk-sensitive foraging in larval dragonflies

Summary Dragonfly larvae (Odonata: Anisoptera) are often abundant in shallow freshwater habitats and frequently co-occur with predatory fish, but there is evidence that they are underutilized as prey. This suggests that species which successfully coexist with fish may exhibit behaviors that minimize their risk of predation. I conducted field and laboratory experiments to determine whether: 1) dragonfly larvae actively avoid fish, 2) microhabitat use and foraging success of larvae are sensitive to predation risk, and 3) vulnerability of larvae is correlated with microhabitat use. I experimentally manipulated the presence of adult bluegills (Lepomis macrochirus) in defaunated patches of littoral substrate in a small pond to test whether colonizing dragonfly larvae would avoid patches containing fish. The two dominant anisopteran species, Tetragoneuria cynosura and Ladona deplanata (Odonata: Libellulidae), both strongly avoided colonizing patches where adult bluegills were present. Laboratory experiments examined the effects of diel period and bluegills on microhabitat use and foraging success, using Tetragoneuria, Ladona and confamilial Sympetrum semicictum, found in a nearby fishless pond. Tetragoneuria and Ladona generally occupied microhabitats offering cover, whereas Sympetrum usually occupied exposed locations. Bluegills induced increased use of cover in all three species, and use of cover also tended to be higher during the day than at night. Bluegills depressed foraging in Tetragoneuria and to a lesser extent in Ladona, but foraging in Sympetrum appeared unaffected. Other laboratory experiments indicated that Sympetrum were generally more vulnerable than Tetragoneuria or Ladona to bluegill predation, and that vulnerability was positively correlated with use of exposed microhabitats. Both fixed (generally low use of exposed microhabitats, diel microhabitat shifts) and reactive (predator avoidance, predator-sensitive microhabitat shifts) behavioral responses appear to reduce risk of predation in dragonfly larvae. Evidence indicates that vulnerability probably varies widely among species and even among instars within species, and suggests that spatial distributions of relatively vulnerable species may be limited by their inability to avoid predation.     

Predation hazard and seed removal by small mammals: microhabitat versus patch scale effects

Predator avoidance may involve response strategies of prey species that are time and space specific. Many studies have shown that foraging individuals avoid predators by altering microhabitat usage; alternatively, sites may be selected according to larger-scale features of the habitat mosaic. We measured seed removal by two small mammal species (Peromyscus leucopus, and Microtus pennsylvanicus) at 474 stations over an experimentally created landscape of 12 patches, and under conditions of relatively high (full moon) and low (new moon) predatory hazard. Our objective was to determine whether predator avoidance involved the selection of small-, medium-, or large-scale features of the landscape (i.e., at the scale of microhabitats, habitats, or habitat patches). We found rates of seed removal to vary more with features of whole patches than according to variation in structural microhabitats within patches. Specific responses included: under-utilization of patch edge habitats during full moon periods, and microhabitat effects that were only significant when considered in conjunction with larger-scale features of the landscape. Individuals residing on large patches altered use of microhabitats/habitats to a greater extent than those on smaller patches. Studies just focusing on patterns of microhabitat use will miss responses at the larger scales, and may underestimate the importance of predation to animal foraging behavior.     

Competition between birds and mammals: A comparison of giving-up densities between crested larks and gerbils

We combined the concept of mechanisms of co-existence with the approach of giving-up densities to study inter-taxon competition between seed-eating birds and mammals. We measured feeding behaviour in food patches to define and study the guild of seed-eating vertebrates occupying sandy habitats at Bir Asluj, Negev Desert, Israel. Despite a large number of putatively granivorous rodents and birds at the site, two gerbil species (Allenbys gerbil, Gerbillus allenbyi, and the greater Egyptian gerbil, G. pyramidum) dominated nocturnal foraging, and a single bird species (crested lark, Galerida cristata) contributed all of the daytime foraging. We used giving-up densities to quantify foraging behaviour and foraging efficiencies. A low giving-up density demonstrates the ability of a forager to profitably harvest food at low abundances and to profitably utilize the foraging opportunities left behind by the less efficient forager. Gerbils had lower giving-up densities in the bush than open microhabitat, and lower giving-up densities in the semi-stabilized than stabilized sand habitats. Crested larks showed the opposite: lower giving-up densities in the open than bush, and on the stabilized than semi-stabilized sand habitats. Despite these patterns, gerbils had substantially lower giving-up densities than crested larks in both microhabitats, all sand habitats, and during each month. Several mechanisms may permit the crested lark to co-exist with the gerbils. Larks may be cream skimmers on the high spatial and temporal variability in seed abundances. Larks may rely on insects, fruit or smaller seeds. Or, larks may rely on adjacent rocky habitats.     

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     

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.     

Effects of body size,seed density,and soil characteristics on rates of seed harvest by heteromyid rodents

Summary Although it is well established that coexisting heteromyid rodent species forage in different microhabitats, we do not yet know the basis for divergent microhabitat choice. One possibility is that seed harvest rates differ among microhabitats, and each species forages where it can extract seeds most efficiently. Microhabitats vary in several factors that could affect heteromyid foraging efficiency, including seed density, soil organic content and particle size distribution. We have explored the effect of each of these variables on harvest rates of several species feeding from petri dishes containing known densities of millet seeds embedded in soil of known particle size and density. Results indicate that the number of seeds harvested per second increases uniformly with seed density and soil density and decreases with soil particle size. Body size affects these relationships: larger animals have higher harvest rates for a given set of conditions and experience a greater relative change in harvest rate for a give change in conditions. This implies that heteromyids can be expected to exhibit species-specific microhabitat preferences while foraging in nature.