Patch utilization by three species of Chilean rodents differing in body size and mode of locomotion.
Foraging behavior and habitat selection are multivariate phenomena that are influenced by intrinsic characteristics of the consumers as well as extrinsic factors of the environment. The foraging ecology and micro-habitat use of rodents have been well studied as a way to understand mechanisms of coexistence in ecological communities, particularly of heteromyid rodents in arid regions of North America (Price 1986, Kotler and Brown 1988, Reichman and Price 1993). From this research, a general pattern involving species with different morphologies has emerged: bipedal kangaroo rats (Dipodomys spp.) and kangaroo mice (Microdipodops spp.) frequent open spaces ("open patches") between canopies of shrubs, and quadrupedal pocket mice (Chaetodipus spp. and Perognathus spp.) occur relatively more in areas under shrub canopies ("covered patches"; Kotler 1984, Price 1986, Longland and Price 1991, Reichman and Price 1993). Besides the differences in locomotion among the species, the small body size (8-39 g) of pocket mice differs from the larger size (40-180 g) of kangaroo rats, and coexisting species normally do not overlap in size (Bowers and Brown 1982). Risk of predation is thought to be one of the most important (but not exclusive) causes of such patterns of foraging and space use (Kotler 1984). Explanations for such patterns have assumed that morphology (i.e., mode of locomotion and body size) affects the capacity to perform activities related to fitness, and that each morphological type does best in only one microhabitat (Longland and Price 1991; see also Price and Brown 1983, Reichman and Price 1993).
A large literature now exists showing several effects of predation risk on foraging decisions (Lima and Dill 1990, Ylonen and Magnhagen 1992, Houston et al. 1993). Different species can differ greatly in strategies for avoiding predation and obtaining food (e.g., Valone and Lima 1987). Specific strategies may, in turn, provide mechanisms of coexistence and thus contribute to community composition (Lima and Valone 1991, Kotler et al. 1994). Several studies of desert rodents have investigated the foraging ecology and mechanisms of coexistence in diverse communities (e.g., Reichman and Oberstein 1977, Kotler 1984, Brown et al. 1994a, b). However, there is little information on how species differ in resource exploitation beyond analyses of microhabitat or patch use. For instance, despite the large amount of information on community structure (Kotler and Brown 1988, Reichman 1991) and food hoarding and central-place foraging (Daly et al. 1992, Jenkins and Peters 1992), few studies explicitly connect these phenomena.
The hypothesis explaining patterns of space use based on predation risk suggests that the ability to escape and/or avoid predation is a main component of fitness. Morphology would be related to escape/avoidance capacity in different patches, with large, bipedal rodents being comparatively safer in open microhabitats and small quadrupeds being safer in covered patches (Kotler 1984, Price 1984, Longland and Price 1991). This hypothesis is based on the fact that risk of predation, in particular by visually orientated predators, is higher in open areas (Kotler 1984, Brown et al. 1988, Longland and Price 1991), and that bipedality seems to confer advantages in avoiding predation through enhanced locomotor performance (Bartholomew and Caswell 1951, Eisenberg 1975, Thompson 1982, Djawdan and Garland 1988, Djawdan 1993). Therefore, bipedal heteromyids would have an advantage in moving between covered patches and exploiting open patches (Thompson 1982). Because many species confront conflicting demands between avoiding predation and obtaining resources, comparative studies assessing food transportation, central-place foraging, and predation-risk avoidance seem valuable.
The abundance of information on heteromyid behavioral, community, and evolutionary ecology has led to their use as textbook examples (e.g., Krebs 1994) and to extending explanations for heteromyids to other rodent groups (Brown et al. 1979, Mares 1983, 1993a, Price and Brown 1983, Kotler and Brown 1988, Reichman 1991, Kerley and Whitford 1994, Kotler et al. 1994, Shenbrot et al. 1994). Nevertheless, the validity of these generalizations has been challenged, and several authors have called for similar studies with different rodents from distinct regions of the world (Mares 1983, 1993a, Kotler et al. 1994, Morton et al. 1994, Shenbrot et al. 1994). Further, there still seems to be some degree of controversy about the relative importance of body size and mode of locomotion for rodent foraging behavior (Price and Brown 1983, Harris 1984, Brown et al. 1988); studies in other systems could help to resolve this controversy.
In this paper, I describe experiments on the foraging behavior of coexisting sigmodontine rodents (Muridae) from the Chilean matorral. I was particularly interested in assessing the way different co-occurring species utilize food patches under different levels of potential predation risk. Because the spatial and temporal distribution of predation risk is an important determinant of foraging behavior in different taxa (Lima and Dill 1990, Ylonen and Magnhagen 1992), the predation-risk hypothesis seems appropriate for other systems. However, the particular ecology of different systems must be taken into account before making specific predictions.
The use of space by rodents in the Chilean matorral is also strongly influenced by the risk of predation (see Mooney 1977, Rundel 1981 for descriptions of the matorral region of central Chile). In general, local rodents preferentially use covered patches with lower predation risk (Jaksic 1986, Jaksic and Simonetti 1987, Simonetti 1989). Raptors are the main rodent predators, whereas carnivorous mammals are relatively unimportant (Jaksic et al. 1981, 1993). Chilean snakes rarely, if ever, prey on rodents (Greene and Jaksic 1993). Important food sources such as shrub seeds and insects (Meserve 1981) are more abundant in covered patches (Simonetti 1989), but open zones are also rich in herbs and herb seeds (Simonetti 1989, Vasquez 1992). The spatial distribution of predation risk is similar to that of other regions, being higher in open areas (Jaksic 1986, Jaksic and Simonetti 1987, Simonetti 1989).
Rodent body size is a key feature used by Chilean predators in diet selection (Jaksic 1989). Despite variations in the relative density and vulnerability to predation of different rodent species, local predators seem to prefer larger rodent prey (Jaksic 1986, 1989, Meserve et al. 1987, Iriarte et al. 1989). Thus, matorral rodents with larger body size would experience greater predation risk than smaller species. This pattern differs from those shown in other regions. In North American arid regions, as well as in Israel, smaller rodents seem to experience greater predation risk (Kotler 1984, 1985, Kotler et al. 1991, Brown et al. 1994a, Bouskila 1995; but see Kotler et al. 1988). It should be noted that information on a predator's diet does not necessarily show the actual attack intensity or predation risk that a prey species may experience. However, the most parsimonious assumption seems to be a positive relationship between realized predation (i.e., predator's diet) and predation risk (see Longland and Price 1991).
Chilean sigmodontines comprise several quadrupedal species of different body sizes. In addition, one species, Oligoryzomys longicaudatus, with longer hind legs in proportion to its body size than other Chilean rodents, has a certain degree of bipedality (Mann 1978). Although this species travels quadrupedally at low speed, it often moves saltatorially, particularly when running and escaping (Vasquez 1994b). These are precisely the conditions in which bipedalism seems to be advantageous over quadrupedalism (Thompson 1982, Djawdan and Gardland 1988, Djawdan 1993, Mares 1993a, b, Kotler et al. 1994). Despite similar overall microhabitat preferences, O. longicaudatus biases its activity toward open patches more than do other coexisting rodent species (Simonetti 1989). All matorral sigmodontines are primarily nocturnal (Iriarte et al. 1989) and decrease their activity in response to moonlight (Simonetti 1989). Further, they respond with characteristic evasive behaviors when confronting raptor models (Simonetti 1989, Vasquez 1994a).
Considering the particular features of organisms and habitats in the matorral, specific predictions can be made. A surrogate of predation risk such as nocturnal illumination level should differentially affect the foraging behavior of rodents with distinct morphologies. In particular, rodents with larger body size should be more affected than smaller species, independently of locomotion. If bipedality confers lower vulnerability to predation, predation risk should affect quadrupedal species more than bipedal species for a given body size. To test these predictions, I carried out experiments with three coexisting sigmodontine species: Phyllotis darwini, Abrothrix olivaceus, and O. longicaudatus. I measured several aspects of patch utilization and food consumption from patches with contrasting levels of nocturnal illumination, a surrogate for perceived and/or potential predation risk.
MATERIALS AND METHODS
Adult specimens of the three sigmodontine species were captured in four different sites in the Chilean matorral where they coexist (Vasquez 1992). Experiments took place within 2 wk after capture. Although O. longicaudatus does not have a fully bipedal morphology like rodents of the genera Jaculus or Dipodomys, I will refer to this species as bipedal to emphasize the difference in escape mode compared with the other species (Vasquez 1994b). In general, P. darwini is 1.62 times larger in body size than the other two species (see Jaksic et al. 1981 and Meserve et al. 1993 for independent data on body mass). Therefore, the three species can be classified in the following manner: P. darwini, a large quadruped, with a body mass of 60.3 [+ or -] 3.5 g (mean [+ or -] 1 SE, n = 20); A. olivaceus, a small quadruped, 30.0 [+ or -] 1.9 g (n = 18); and O. longicaudatus, a small biped, 29.9 [+ or -] 2.4 g (n = 13). Seeds are the most important food sources of P. darwini and O. longicaudatus. Although A. olivaceus is more omnivorous, frequently its diet is also composed mostly of seeds (Glanz 1977, Meserve 1981). The three species can live on a seed diet for several weeks in the lab (Vasquez 1992), are common in central Chile, and have nocturnal habits (Iriarte et al. 1989).
The experiments were carried out in four plywood arenas, each measuring 2.2 x 1.6 x 1.0 m (length x width x height). The floor of each arena was covered with sand to a depth of 3 cm, and a plastic refuge box (25 x 25 x 10 cm) was placed in one corner. Food (sunflower seeds, Helianthus annuus) was provided in metallic trays (45 x 45 cm, 2.5 cm deep) covered with sand, following Brown (1988) and Brown et al. (1988).
One tray was supplied per arena; it was located 1.5 m from the refuge and buried to produce a smooth, overall sand surface. Because the spatial distribution of food is known to affect the foraging behavior of rodents (e.g., different harvest rates from aggregated and dispersed seeds; Reichman and Oberstein 1977, Price 1978, Price and Reichman 1987), two distinct distributions were offered, defined as clumped (occupying an area of 10 x 10 cm in the seed tray) and dispersed (occupying the whole seed tray). In both distributions, the supply of food on the seed tray was 120 seeds per trial. Although both distributions were actually aggregated, they mimicked contrasting distributions and actual densities within the natural range occurring in the Chilean matorral (Vasquez 1992).
Because nocturnal illumination level has been shown to be a surrogate of the potential and actual predation risk experienced by a number of rodent species (e.g., Clarke 1983, Brown et al. 1988, Kotler et al. 1991), I used dark and bright nights to mimic conditions of low and high predation risk, respectively. Full moon and moonless nights were reproduced in the laboratory. Natural nocturnal light intensities were recorded in the field with a Li-Cor Q-12588 sensor connected to an automatic recording datalogger (Li-Cor LI-1000). These were then simulated by using a rheostat and 25-W white incandescent bulbs suspended 2 m above each arena. Full moonlight had an intensity of 2.0 lux. Although the sensor was not sensitive enough to register the light intensity on moonless nights, this illumination level was not total darkness, so it was reproduced with a minimal light intensity similar to that observed in the field with the naked eye during moonless nights. The order of presentation of dark and bright conditions and clumped and dispersed food was chosen randomly. When they were not taking part in experiments, animals were maintained in plastic cages with natural photoperiod and temperature, and with food and water ad libitum.
Patch utilization and food consumption. - I evaluated patch consumption (number of seeds consumed in the exposed tray), consumption in refuge (number of seeds carried to and consumed in the refuge), and total consumption (total number of seeds consumed regardless of site in the arena). Previous experiments showed that the three species do not consume the pericarp of sunflower seeds; this facilitates the quantification of seed consumption according to where pericarps are found (Vasquez 1992). One individual per arena was tested in each trial. Trials lasted 16 h [2 h daylight: 12 h night (moonless or moonlight night): 2 h daylight]. Each animal was tested in four trials (bright night, dispersed seeds; bright, clumped; dark, dispersed; and dark, clumped). This protocol evaluates patch-utilization efficiency and not patch choice (Harris 1984). The order of trials was randomized for each individual. After each trial, animals were recaptured, the sand was sifted to extract unconsumed seeds and remaining pericarps, and the response variables were quantified for each individual. Given that the response variables were interrelated, I analyzed the data using a protected multivariate analysis of variance for repeated measures. Following Scheiner (1993), the method comprises a MANOVA to assess global effects, and repeated-measures ANOVAs if the MANOVA shows significant results. Multiple comparisons were carried out using Tukey tests with [Alpha] = 0.05. Data were log transformed (Sokal and Rohlf 1995) to meet the assumptions of MANOVA. Figures show back-transformed data.
Food carrying. - In trials independent from those in which patch utilization and food consumption were measured, I made direct observations of food carrying to the refuge to estimate the mean number of seeds carried per trip. Observations of food carrying from the open tray to the refuge were made from a blind situated at one side of one of the arenas. A clumped distribution of seeds (n = 120) was provided in each trial under half moonlight conditions. Animals were allowed to carry seeds spontaneously. The number of trips between the seed patch and the refuge was recorded for [approximately equal to]3 h for each individual tested. A one-way ANOVA was used to assess differences in seed carrying among species.
Patch utilization and food consumption
The MANOVA showed significant overall main effects for species and illumination, whereas the spatial distribution of seeds did not have any effect (Table 1A). Further, illumination x species was the only significant interaction. Nocturnal illumination level significantly affected all food consumption variables for P. darwini and A. olivaceus (Table lB), but none for O. longicaudatus (Tukey tests, [Alpha] = 0.05; [ILLUSTRATION FOR FIGURE 1-3 OMITTED]). When both seed spatial patterns were pooled together, under bright light conditions, mean patch consumption decreased 53.9% (from a mean of 84.8 to 39.1 seeds consumed) and 58.1% (22.7 to 9.5 seeds) for P. darwini and A. olivaceus, respectively [ILLUSTRATION FOR FIGURE 1 OMITTED]. Bright nights also elicited an increase in the amount of food carried to the refuge in these two species. During bright nights, mean consumption in the refuge increased 10.5 and 3.1 times for P. darwini and A. olivaceus, respectively [ILLUSTRATION FOR FIGURE 2 OMITTED]. Although P. darwini carried few seeds during dark nights, when most of the food was consumed in the seed patch, A. olivaceus always carried some seeds to the refuge. Moreover, large proportions of these seeds were not consumed, but stored in the refuge [ILLUSTRATION FOR FIGURE 2 OMITTED]. During dark nights, this species consumed a mean 37.5% of the total seeds carried to the refuge, whereas under bright illumination it consumed 51.5% [ILLUSTRATION FOR FIGURE 2 OMITTED]. This was not the case for the other two species, which consumed almost all seeds carried to the refuge (99.7% and 98.6% for P. darwini and O. longicaudatus, respectively; [ILLUSTRATION FOR FIGURE 2 OMITTED]). The overall mean for O. longicaudatus was calculated with a small sample size, because this species transported almost negligible quantities of seeds to the refuge in all experimental conditions [ILLUSTRATION FOR FIGURE 2 OMITTED]. Therefore, this figure should be taken with caution.
Overall, P. darwini had the highest total consumption [ILLUSTRATION FOR FIGURE 3 OMITTED], which is not surprising since it had the largest body size among the three species. However, it was also the species that changed most between conditions of nocturnal illumination, decreasing its total food intake by 14.5% during bright nights (from a mean of 95.5 to 81.6 seeds consumed; [ILLUSTRATION FOR FIGURE 3 OMITTED]). A. olivaceus decreased its total consumption 10.9% under bright light conditions (from 46.6 to 41.5 seeds; [ILLUSTRATION FOR FIGURE 3 OMITTED]). Curiously, this species did not compensate for this decrease by consuming more seeds in the refuge, even though it had transported enough seeds to do so [ILLUSTRATION FOR FIGURE 2 OMITTED]. O. longicaudatus did not show any significant change in total consumption [ILLUSTRATION FOR FIGURE 3 OMITTED].
Phyllotis darwini transported more seeds per trip than did the other two species (Table 2; one-way ANOVA: [F.sub.2,17] = 17.92, P [less than] 0.001). This was expected, given its larger body size. The numbers of seeds carried per trip by A. olivaceus and O. longicaudatus did not differ significantly (Table 2), although this is based on limited data for O. longicaudatus because of the very few trips quantified. These data allowed me to estimate the minimum mean distance travelled by each species during the food consumption experiments, given that the total number of seeds transported to the refuge was known (Table 2). On average, P. darwini travelled 8.8 times longer during bright nights than during dark nights (from a mean of 5.6 m to 49.5 m). In both conditions of illumination, A. olivaceus moved more than any other species, and increased its travelling distance 2.2 times under bright illumination. Because O. longicaudatus transported very few seeds to the refuge, its travelling distances were very small under both conditions of illumination (Table 2). Of course, these calculations may underestimate the real distance travelled by each species, because they do not consider any other movement made by the animals when they did not carry seeds to the refuge, and they assume straight trips between refuge and food patch.
A surrogate of predation risk (i.e., illumination), but not the spatial distribution of food, significantly affected the foraging behavior of two of the three rodent species studied. Phyllotis darwini and Abrothrix olivaceus changed their foraging behavior with changes in nocturnal illumination. P. darwini seemed to be the species most sensitive to increased illumination, diminishing its use of the food patch for patch consumption, increasing its food consumption in the refuge, and, more importantly, decreasing its total food [TABULAR DATA FOR TABLE 1 OMITTED] consumption. This species also increased total travelling distance (for seed transportation) almost ninefold with higher illumination, resulting in higher energetic expenditure (Vasquez 1994a). Although A. olivaceus showed a similar overall pattern, it was not so strong. These changes show a sensitivity to potentially risky conditions, and they are in agreement with qualitative predictions derived from foraging theory for decision making under predation risk (Lima and Dill 1990, Houston et al. 1993). When there is a trade-off between obtaining food and avoiding predation, an increase in central-place foraging under higher risk may be adaptive (Lima et al. 1985, Vasquez 1994a). Several central-place foraging species change the degree of food carrying in response to predation risk and/or distance tO refuge (Lima et al. 1985, Valone and Lima 1987, Vasquez 1994a). These plastic behavioral responses may, in addition to other behaviors such as patch/microhabitat selection, contribute to the coexistence of species. Oligoryzomys longicaudatus did not show any significant change in foraging with changes in nocturnal light levels, suggesting that it is the least sensitive species and that, indeed, it probably would not perceive or experience any increase in predation risk as a product of increased environmental illumination. According to the differential responses shown to distinct levels of nocturnal illumination, it is possible to propose a ranking of sensitivity to potential predation risk for the species used in this study. From less to more sensitive, this is: O. longicaudatus [less than] A. olivaceus [less than] P. darwini.
The lack of effect of food distribution for any of the species studied may be due to the limited variation in spatial distribution of food offered, which was within the natural range occurring in the Chilean matorral. In this region, seeds conform to a contagious distribution at different levels of analysis (in different habitats, microhabitats, and seasons), varying only in the degree of aggregation (Vasquez 1992). Further, the degree of diet specialization for seeds by Chilean rodents is not as high as for heteromyids (Meserve 1981). These factors might influence the development of specializations [TABULAR DATA FOR TABLE 2 OMITTED] for food distribution patterns. However, it may also be that the range of seed distributions offered in the experiment was insufficient to detect possible specializations, particularly because patch limits in the experimental setup did not coincide with other physical features. Further, rodents may have recognized as patch boundaries the discrete edge of the tray rather than the more vague border of each set of seeds. Theoretically, however, resource distribution should affect foraging efficiency (Iwasa et al. 1981, Vasquez 1995). The selective use of different seed distributions is considered one of the most important factors contributing to coexistence among North American desert rodents (Reichman and Oberstein 1977, Hutto 1978, Price 1978, Harris 1984, Reichman and Roberts 1994). Certainly, further research is still needed to assess the generality of hypotheses based on resource distribution (see Reichman and Price 1993).
Results of this study suggest that body size has a substantial influence on foraging behavior under conditions mimicking high predation risk. Overall, during dark nights (low predation risk), species with different body sizes showed somewhat similar patterns of patch utilization. The variations occurred when nocturnal illumination was increased. The species with larger body size (P. darwini) changed its foraging behavior proportionately more than did the smaller species (A. olivaceus and O. longicaudatus). Although based on one species only, this suggests that a large body size could confer a greater sensitivity and, hence, greater vulnerability, to predation. In fact, predators from central Chile prefer larger prey among sigmodontine rodents (Fulk 1976, Jaksic 1986, 1989, Meserve et al. 1987, Jaksic et al. 1993). On the other hand, type of locomotion is an important factor in the ability to exploit potentially risky patches and to transport food to cover. With increased illumination, the two quadrupedal species (P. darwini and A. olivaceus), carried food to the refuge, whereas the bipedal species did not show any significant change. This finding supports the idea that bipedal rodents have an advantage in exploiting risky patches (Brown et al. 1988, Kotler et al. 1994), and that the phenotypic features of O. longicaudatus allow it to use riskier patches without needing to change its foraging behavior. Like bipedal heteromyids, O. longicaudatus seems to be at less risk than quadrupedal species in open patches. Although all matorral sigmoriontines restrict most of their activity to covered patches (where overall food abundance is higher), O. longicaudatus uses open (riskier) patches more frequently (Simonetti 1989). As has been found for rodents from other regions, bipedality may enable animals to experience less risk from predators because it permits quicker escape velocities (accelerations), allows more erratic trajectories with sudden changes in direction, and/or allows greater endurance while running (Djawdan and Garland 1988, Djawdan 1993, Vasquez 1994b). In fact, bipedality is ubiquitous in arid regions, where rich resource patches are either high in predation risk or are surrounded by areas with higher risk of predation. In such environments, any phenotypic feature (behavioral, morphological, and/or physiological) that enables animals to use risky patches may be adaptive.
The change in the primary feeding place from the food patch to the refuge, shown by P. darwini and A. olivaceus, occurs concurrently with an increase in perceived and/or potential predation risk. This facultative central-place foraging would occur at a microhabitat scale, over a range of distances relatively close to the refuge (see Vasquez 1994a). Although it was not quantified, both quadrupedal species spent more time out of the refuge during dark than bright nights. Analysis of an optimal strategy of facultative central-place for aging due to predation risk would need to consider, among other factors, prey handling and travel time. Depending on their actual values, it could predict different strategies of staying in the food patch and/or travelling to the refuge. For example, if handling time is very short, the most efficient strategy could be to consume food in the exposed, risky patch rather than making several trips between food patch and refuge (Lima et al. 1985, Newman 1991). The bipedal species O. longicaudatus always consumed food in the exposed patch. This pattern is also observed in bipedal heteromyids; they preferentially use and exploit open microhabitats (Kotler 1984, Brown et al. 1988). Although, to my knowledge, there is no study linking food transportation with predation risk in heteromyids, differences may exist, considering that heteromyids have specialized cheek pouches to carry seeds (Nikolai and Bramble 1983; see also Longland 1994 for a study of caching behavior and effects of predation risk).
In general, the influences of predation risk and morphology on foraging behavior seem to be somewhat different for Chilean sigmodontines and North American heteromyids. The form most sensitive to surrogate predation risk in the matorral is a large quadruped, whereas in North America it is a small quadruped. The morph least sensitive to nocturnal illumination in the matorral is a small biped, whereas in the heteromyid system it is a large biped. Therefore, the overall patterns for bipedality seem to be similar (as far as patch utilization is concerned), but different patterns exist for body size. Another morphological feature related to predator avoidance, the auditory bullae, much enlarged in heteromyids, is not particularly developed in Chilean sigmodontines (Simonetti 1986). Although rodent bipedality has been considered an adaptation for desert environments, it is not necessarily a unique alternative, and different phenotypic traits may evolve in arid regions (Mares 1993a, Kotler et al. 1994). The development of adaptive traits may follow quite different paths in distinct lineages (Williams 1992). Antipredator adaptations in heterogeneous environments have been postulated to conform to two parsimonious phenotypic variations: morphological or behavioral (Sih 1987, McLean and Godin 1989). This idea is consistent with my results: morphologically, bipedality can be seen as an adaptation to avoid and/or escape predation (Djawdan and Garland 1988, Djawdan 1993, Vasquez 1994b); behaviorally, facultative central-place foraging could also be an adaptation (Vasquez 1994a). It is clear that predation has important consequences in shaping individuals, populations, and communities both evolutionarily and ecologically (Taylor 1984, Kerfoot and Sih 1987, Boucot 1990, Kotler et al. 1994). This study supports existing evidence that surrogates of predation risk affect the foraging ecology of rodent species. However, it also pinpoints the necessity to take into account the particular features of the system under study when giving specific explanations.
This work was done as partial fulfilment for the degree of M.Sc. at the Facultad de Ciencias, Universidad de Chile, Santiago, Chile. I wish to thank my advisor J. A. Simonetti and the thesis committee, F. Bozinovic, F. M. Jaksic, M. Rosenmann, and J. L. Yanez for discussions and comments. I also appreciate comments made by M. A. Rodriguez-Girones, B. Kotler, J. Newman, and two anonymous reviewers. Many people at the Universidad de Chile, too numerous to name individually, are acknowledged for discussion, support and, above all, for their friendship. This work was supported by grants DTI 2596-8934 from the Universidad de Chile to J. A. Simonetti, and FONDECYT 847-89 to R. O. Bustamante. During the study, the author was supported by DTI and Facultad de Ciencias, Universidad de Chile. Final writing was partially supported by Presidente de la Republica scholarship (Mideplan, Chile), ORS award scheme (UK), Pembroke College, Oxford, and FONDECYT 3950023-95 to R. A. Vasquez.
Bartholomew, G. A., and H. H. Caswell, Jr. 1951. Locomotion in kangaroo rats and its adaptive significance. Journal of Mammalogy 32:155-169.
Boucot, A. J. 1990. Evolutionary paleobiology of behavior and coevolution. Elsevier, New York, New York, USA.
Bouskila, A. 1995. Interactions between predation risk and competition: a field study of kangaroo rats and snakes. Ecology 76:165-178.
Bowers, M. A., and J. H. Brown. 1982. Body size and coexistence in desert rodents: chance or community structure? Ecology 63:391-400.
Brown, J. H., O. J. Reichman, and D. W. Davidson. 1979. Granivory in desert ecosystems. Annual Review of Ecology and Systematics 10:201-227.
Brown, J. S. 1988. Patch use as an indicator of habitat preference, predation risk, and competition. Behavioral Ecology and Sociobiology 22:37-47.
Brown, J. S., B. P. Kotler, and W. A. Mitchell. 1994a. Foraging theory, patch use, and the structure of a Negev desert granivore community. Ecology 75:2286-2300.
Brown, J. S., B. P. Kotler, R. J. Smith, and W. O. Wirtz, II. 1988. The effect of owl predation on the foraging behavior of heteromyid rodents. Oecologia 76:408-415.
Brown, J. S., B. P. Kotler, and T. J. Valone. 1994b. Foraging under predation: a comparison of energetic and predation costs in rodent communities of the Negev and Sonoran deserts. Australian Journal of Zoology 42:435-448.
Clarke, J. A. 1983. Moonlight's influence on predator/prey interactions between Short-eared Owls (Asio flammeus) and deermice (Peromyscus maniculatus). Behavioral Ecology and Sociobiology 13:205-209.
Daly, M., L. F. Jacobs, M. I. Wilson, and P. R. Behrends. 1992. Scatter-hoarding by kangaroo rats (Dipodomys merriami) and pilferage from their caches. Behavioral Ecology 3:102-111.
Djawdan, M. 1993. Locomotor performance of bipedal and quadrupedal heteromyid rodents. Functional Ecology 7: 195-202.
Djawdan, M., and T Garland, Jr. 1988. Maximal running speeds of bipedal and quadrupedal rodents. Journal of Mammalogy 69:765-772.
Eisenberg, J. F. 1975. The behavior patterns of desert rodents. Pages 189-224 in I. Prakash and P. K. Ghosh, editors. Rodents in desert environments. Dr Junk, The Hague, The Netherlands.
Fulk, G. W. 1976. Owl predation and rodent mortality: a case study. Mammalia 40:423-427.
Glanz, W. E. 1977. Comparative ecology of small mammal communities in California and Chile. Dissertation. University of California, Berkeley, California, USA.
Greene, H. W., and F. M. Jaksic. 1993. The feeding behavior and natural history of two Chilean snakes, Philodryas chamissonis and Tachymenis chilensis (Colubridae). Revista Chilena de Historia Natural 65:485-493.
Harris, J. H. 1984. An experimental analysis of desert rodent foraging ecology. Ecology 65:1579-1584.
Houston, A. I., J. M. McNamara, and J. M. C. Hutchinson. 1993. General results concerning the trade-off between gaining energy and avoiding predation. Philosophical Transactions of the Royal Society of London B 341:375-397.
Hutto, R. L. 1978. A mechanism for resource allocation among sympatric heteromyid rodent species. Oecologia 33: 115-126.
Iriarte, J. A., L. C. Contreras, and F. M. Jaksic. 1989. A long-term study of a small-mammal assemblage in the central Chilean matorral. Journal of Mammalogy 70:79-87.
Iwasa, Y., M. Higashi, and N. Yamamura. 1981. Prey distribution as a factor determining the choice of optimal foraging strategy. American Naturalist 117:710-723.
Jaksic, F. M. 1986. Predation upon small mammals on shrub-lands and grasslands of southern South America: ecological correlates and presumable consequences. Revista Chilena de Historia Natural 59:209-221.
-----. 1989. What do carnivorous predators cue in on: size or abundance of mammalian prey? A crucial test in California, Chile, and Spain. Revista Chilena de Historia Natural 62:237-249.
Jaksic, F. M., H. W. Greene, and J. L. Yanez. 1981. The guild structure of a community of predatory vertebrates in central Chile. Oecologia 49:21-28.
Jaksic, F. M., P. L. Meserve, J. R. Gutierrez, and E. L. Tabilo. 1993. The components of predation on small mammals in semiarid Chile: preliminary results. Revista Chilena de Historia Natural 66:305-321.
Jaksic, F. M., and J. A. Simonetti. 1987. Predator/prey relationships among terrestrial vertebrates: an exhaustive review of studies conducted in southern South America. Revista Chilena de Historia Natural 60:221-244.
Jenkins, S. H., and R. A. Peters. 1992. Spatial patterns of food storage by Merriam's kangaroo rats. Behavioral Ecology 3:60-65.
Kerfoot, W. C., and A. Sih. 1987. Predation: direct and indirect impacts on aquatic communities. University of New England Press, Hanover, New Hampshire, USA.
Kerley, G. I. H., and W. G. Whitford. 1994. Desert-dwelling small mammals as granivores: intercontinental variations. Australian Journal of Zoology 42:543-555.
Kotler, B. P. 1984. Risk of predation and the structure of desert rodent communities. Ecology 65:689-701.
-----. 1985. Owl predation on desert rodents which differ in morphology and behavior. Journal of Mammalogy 66: 824-828.
Kotler, B. P., and J. S. Brown. 1988. Environmental heterogeneity and the coexistence of desert rodents. Annual Review of Ecology and Systematics 19:281-307.
Kotler, B. P., J. S. Brown, and O. Hasson. 1991. Factors affecting gerbil foraging behavior and rates of owl predation. Ecology 72:2249-2260.
Kotler, B. P., J. S. Brown, and W. A. Mitchell. 1994. The role of predation in shaping the behavior, morphology, and community organisation of desert rodents. Australian Journal of Zoology 42:449-466.
Kotler, B. P., J. S. Brown, R. J. Smith, and W. O. Wirtz, II. 1988. The effects of morphology and body size on rates of owl predation on desert rodents. Oikos 53:145-152.
Krebs, C. J. 1994. Ecology: the experimental analysis of distribution and abundance. Fourth edition. Harper Collins, New York, New York, USA.
Lima, S. L., and L. M. Dill. 1990. Behavioral decisions made under the risk of predation: a review and prospectus. Canadian Journal of Zoology 68:619-640.
Lima, S. L., and T. J. Valone. 1991. Predators and avian community organization: an experiment in a semi-desert grassland. Oecologia 86:105-112.
Lima, S. L., T. J. Valone, and T. Caraco. 1985. Foraging-efficiency-predation-risk trade-off in the grey squirrel. Animal Behaviour 33:155-165.
Longland, W. S. 1994. Effects of artificial bush canopies and illumination on seed patch selection by heteromyid rodents. American Midland Naturalist 132:82-90.
Longland, W. S., and M. V. Price. 1991. Direct observations of owls and heteromyid rodents: can predation risk explain microhabitat use? Ecology 72:2261-2273.
Mann, G. 1978. Los pequenos mamiferos de Chile. Gayana (Zoologia, Chile) 40:1-342.
Mares, M. A. 1983. Desert rodent adaptation and community structure. Great Basin Naturalist Memoirs 7:30-43.
-----. 1993a. Heteromyids and their ecological counterparts: a pandesertic view of rodent ecology and evolution. Pages 652-714 in H. H. Genoways and J. H. Brown, editors. Biology of the Heteromyidae. Special Publication Number 10. American Society of Mammalogists.
-----. 1993b. Desert rodents, seed consumption, and convergence. Bioscience 43:372-379.
McLean, E. B., and J.-G. J. Godin. 1989. Distance to cover and fleeing from predators in fish with different amounts of defensive armour. Oikos 55:281-290.
Meserve, P. L. 1981. Trophic relationships among small mammals in a Chilean semiarid thorn scrub community. Journal of Mammalogy 62:304-314.
Meserve, P. L., J. L. Gutierrez, L. C. Contreras, and F. M. Jaksic. 1993. Role of biotic interactions in a semiarid scrub community in north-central Chile: a long-term ecological experiment. Revista Chilena de Historia Natural 66:225-241.
Meserve, P. L., E. J. Shadrick, and D. A. Kelt. 1987. Diets and selectivity of two Chilean predators in the northern semi-arid zone. Revista Chilena de Historia Natural 60:93-99.
Mooney, H. A. 1977. Convergent evolution in Chile and California: mediterranean climate ecosystems. Dowden, Hutchinson and Ross, Stroudsburg, Pennsylvania, USA.
Morton, S. R., J. H. Brown, D. A. Kelt, and J. R. W. Reid. 1994. Comparisons of community structure among small mammals of North American and Australian deserts. Australian Journal of Zoology 42:501-525.
Newman, J. A. 1991. Patch use under predation hazard: foraging behavior in a simple stochastic environment. Oikos 61:29-44.
Nikolai, J. C., and D. M. Bramble. 1983. Morphological structure and function in desert heteromyid rodents. Great Basin Naturalist Memoirs 7:44-64.
Price, M. V. 1978. Seed dispersion preferences of coexisting desert rodent species. Journal of Mammalogy 59:624-626.
-----. 1984. Microhabitat use in rodent communities: predator avoidance or foraging economics? Netherlands Journal of Zoology 34:63-80.
-----. 1986. Structure of desert rodent communities: a critical review of questions and approaches. American Zoologist 26:39-49.
Price, M. V., and J. H. Brown. 1983. Patterns of morphology and resource use in North American desert rodent communities. Great Basin Naturalist Memoirs 7:117-134.
Price, M. V., and O. J. Reichman. 1987. Distribution of seeds in Sonoran desert soils: implications for heteromyid foraging. Ecology 68:1797-1811.
Reichman, O. J. 1991. Desert mammal communities. Pages 311-347 in G. Polis, editor. The ecology of desert communities. University of Arizona Press, Tucson, Arizona, USA.
Reichman, O. J., and D. Oberstein. 1977. Selection of seed distribution types by Dipodomys merriami and Perognathus amplus. Ecology 58:636-643.
Reichman, O. J., and M. V. Price. 1993. Ecological aspects of heteromyid foraging. Pages 539-574 in H. H. Genoways and J. H. Brown, editors. Biology of the Heteromyidae. Special Publication Number 10. American Society of Mammalogists.
Reichman, O. J., and E. Roberts, 1994. Computer simulation analysis of foraging by heteromyid rodents in relation to seed distributions: implications for coexistence. Australian Journal of Zoology 42:467-477.
Rundel, P. W. 1981. The matorral zone of central Chile. Pages 175-201 in F. Di Castri, D. W. Goodall, and R. L. Specht, editors. Mediterranean type shrublands. Elsevier, Amsterdam, The Netherlands.
Scheiner, S. M. 1993. MANOVA: multiple response variables and multispecies interactions. Pages 94-112 in S. M. Scheiner and J. Gurevitch, editors. Design and analysis of ecological experiments. Chapman and Hall, New York, New York, USA.
Shenbrot, G. I., K. A. Rogovin, and E. J. Heske. 1994. Comparison of niche-packing and community organisation in desert rodents in Asia and North America. Australian Journal of Zoology 42:479-499.
Sih, A. 1987. Predators and prey lifestyles: an evolutionary and ecological overview. Pages 203-224 in W. C. Kerfoot and A. Sih, editors. Predation: direct and indirect impacts on aquatic communities. University of New England Press, Hanover, New Hampshire, USA.
Simonetti, J. A. 1986. Microhabitat use by small mammals in central Chile. Dissertation. University of Washington, Seattle, Washington, USA.
-----. 1989. Microhabitat use by small mammals in central Chile. Oikos 56:309-318.
Sokal, R. R., and F. J. Rohlf. 1995. Biometry. Third edition. Freeman, San Francisco, California, USA.
Taylor, R. J. 1984. Predation. Chapman and Hall, London, UK.
Thompson, S. D. 1982. Microhabitat utilization and foraging behavior of bipedal and quadrupedal heteromyid rodents. Ecology 63:1303-1312.
Valone, T. J., and S. L. Lima. 1987. Carrying food items to cover for consumption: the behavior of ten bird species feeding under the risk of predation. Oecologia 71:286-294.
Vasquez, R. A. 1992. Exito de forrajeo: comparaciones interfenotipicas en roedores. Thesis. Universidad de Chile, Santiago, Chile.
-----. 1994a. Assessment of predation risk via illumination level: facultative central place foraging in the cricetid rodent Phyllotis darwini. Behavioral Ecology and Sociobiology 34:375-381.
-----. 1994b. Bipedalismo de escape en Owzomys longicaudatus (Rodentia: Cricetidae). Medio Ambiente (Chile) 12:22-26.
-----. 1995. Decision making in variable environments: individuals, groups, and populations. Dissertation. University of Oxford, Oxford, UK.
Williams, G. C. 1992. Natural selection: domains, levels, and challenges. Oxford University Press, Oxford, UK.
Ylonen, H., and C. Magnhagen. 1992. Predation risk and behavioural adaptations of prey: ecological and evolutionary consequences. Annales Zoologici Fennici 29:179-320.
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|Author:||Vasquez, Rodrigo A.|
|Date:||Dec 1, 1996|
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