small-mammal foraging behavior: mechanisms for

Ecological Monographs, 72(4), 2002, pp. 561–577 䉷 2002 by the Ecological Society of America

SMALL-MAMMAL FORAGING BEHAVIOR: MECHANISMS FOR COEXISTENCE AND IMPLICATION FOR POPULATION DYNAMICS JOHN A. YUNGER,1,3 PETER L. MESERVE,1

AND

JULIO R. GUTIE´RREZ2

1Department

of Biological Sciences, Northern Illinois University, DeKalb, Illinois 60115 USA Departamento de Biologia, Universidad de La Serena, Casilla 599, La Serena, Chile

2

Abstract. We investigated predation risk and competition as they affected small-mammal foraging behavior in semiarid north-central Chile. Giving-up densities (GUD) of seeds were used to measure the foraging activity of the three most common small mammals at the site: degu (Octodon degus), Darwin’s leaf-eared mouse (Phyllotis darwini), and the olivaceous field mouse (Akodon olivaceus), under shrubs (cover) and in the open on predator-excluded and competitor-excluded (Octodon) plots. Experiments were conducted during both new and full moons. Monthly small-mammal censuses using standard mark– recapture techniques provided data on movement, reproduction, and long-term fluctuations in density between 1989 and 1994. Diurnal Octodon foraged more (had lower GUD) in the absence of predators (although this was confounded by a numerical increase resulting from predator exclusion), and foraged more under shrubs than in the open. However, the lack of a significant cover ⫻ predator exclusion interaction and thermoregulation studies suggest that physiological constraints play a greater role than predation risk in determining microhabitat selection by Octodon. Predation risk, as influenced by lunar light levels and predator exclusion, had only weak effects on microhabitat selection by Phyllotis. The strong tendency of Octodon to forage under cover could depress food availability, forcing Phyllotis to feed more in the open. Concomitantly, Phyllotis exhibits several morphological characters that would favor detection and avoidance of predators. There is extensive evidence that interspecific competition is the primary constraint on Akodon foraging; predation risk appears to be relatively unimportant. Akodon is also a less efficient forager than the two other species, having significantly higher GUD, on average. This is partially offset by differences in reproductive biology; Akodon exhibits extremely rapid demographic responses to favorable changes in the environment. A fourth species, Abrothrix longipilis, may coexist in the system because of its opportunistic nature, but no data are available on its foraging efficiency. These behavioral and biotic interactions occur within a background of periodic El Ninõ–Southern Oscillations (ENSO), which may ultimately contribute to species coexistence. Key words: Akodon olivaceus; Chile; competition; foraging behavior; giving-up density; microhabitat; Octodon degus; Phyllotis darwini; population dynamics; predation risk; semiarid; small mammals.

INTRODUCTION

General background To understand how species coexist within a community and the temporal dynamics of a system, it is necessary to integrate across ecological levels and scales (Bissonette 1997). For example, individuals forage to procure energy for growth, maintenance, and reproduction. However, interference from competitors, risk of predation, and physiological constraints all can influence the resource level at which an individual will abandon, or choose not to forage in, a patch. By incorporating environmental heterogeneity, while simultaneously measuring foraging behavior and manipuManuscript received 9 February 2001; revised 16 January 2002; accepted 28 January 2002. 3 Present address: Environmental Biology Program, Governors State University, University Park, Illinois 60466 USA. E-mail: [email protected]

lating biotic interactions, it may be possible to elucidate mechanisms of community composition and dynamics. Brown (1989) studied foraging behavior and coexistence of four rodent species in the Sonoran Desert. Seasonal rotation in foraging efficiency was the mechanism permitting coexistence among three of the species (Brown 1989). Spatial variation in resource abundance was presumed to be responsible for coexistence of a fourth species in the small-mammal assemblage. Selection of open vs. bush microhabitat and temporal variation in resource abundance appeared to be of relatively little importance. In the Israeli Negev Desert, live-trapping at large spatial scales (macrohabitat) showed that two species of gerbils occurred most frequently in semi-stabilized dune habitats, although under high densities, secondary habitat preferences diverged between stabilized and unstabilized dunes (Rosenzweig and Abramsky 1986, Abramsky et al. 1990). Both gerbils foraged more under low levels of lunar

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light intensity (Kotler 1984a) and beneath shrubs as opposed to open areas (microhabitat; Kotler et al. 1991). Such foraging behaviors are putative modes of reducing predation risk. In the Namib Desert, Hughes et al. (1994) studied the foraging behavior of the nocturnal dune hairy-footed gerbil (Gerbillurus tytonis) in three microhabitats: open, grass, and brush. This gerbil foraged the most in brush, followed by grass and then open areas. The authors attributed the pattern to reduced predation risk in brush and grass microhabitats. In all three microhabitats, G. tytonis foraged more under a new moon than a full moon. Effects of a putative competitor were unclear, given no patterns in microhabitat shifts as a result of the removal. Because predators were never directly manipulated, these studies provide limited insight into the influence of predation. Although Hughes et al. (1994:1397) purported to ‘‘provide direct experimental evidence on the role of predation risk. . . ,’’ lunar light levels were used as a surrogate. This approach has commonly been employed when investigating small-mammal foraging (e.g., Lockard and Owings 1974, Kotler 1984b, c, Price et al. 1984, Bowers 1988). Although it provides useful information, alternative explanations, such as thermoregulatory constraints (Goodfriend et al. 1991, Lagos et al. 1995a) or intraspecific competition, may at least partially explain the foraging regimes observed under different lunar light levels (Reichman and Price 1993). Under low levels of lunar light intensity, vertebrate predators may still be present and may forage successfully (Dice 1945). In addition, lunar light intensity is irrelevant for diurnal prey species. In this study, predator and competitor exclosures were used to test four spatial and three temporal hypotheses on small-mammal coexistence. These hypotheses, which are not mutually exclusive, were tested using natural variation in cover and light intensity. In the context of these manipulations and variation, the foraging patterns of small mammals were examined using giving-up densities (GUD), the level at which an individual ceases to use a particular resource (Brown 1988, Kotler et al. 1991, Brown et al. 1992); similar methods have been used elsewhere (e.g., Bowers et al. 1993, Bowers and Breland 1996). Most often the resource is some type of food mixed with a matrix material (e.g., sand), resulting in a diminishing rate of return as the food is consumed. Two or more predictions pertaining to foraging supported by marginally significant treatment effects would suggest that individuals are ‘‘balancing’’ multiple constraints. Finally, as part of a long-term study, it was possible to relate the GUD work to population and community dynamics. We present results on the foraging behavior of three small-mammal species in semiarid north-central Chile: the olivaceous field mouse (Akodon olivaceus, 32.3 ⫾ 5.3 g, X¯ ⫾ 1 SE), which is continuously active, Darwin’s leaf-eared mouse (Phyllotis darwini, 58.2 ⫾ 13.7 g, X¯ ⫾ 1 SE), which is nocturnal, and the degu rat (Octodon

degus, 140.9 ⫾ 20.9 g, X¯ ⫾ 1 SE), which is diurnal (Meserve and Le Boulenge´ 1987, Wilson and Reeder 1993). All three species feed largely or exclusively on plant material, including seeds. Seed utilization of the three species in decreasing order is Phyllotis, Akodon, and Octodon (Meserve 1981a, b). Hypotheses Predation risk.—Analysis of vertebrate predator diets showed that Octodon were consumed more than would be predicted based on total prey availability, followed by Phyllotis, with Akodon representing a comparatively low proportion of the predator diets (Jaksic et al. 1993, 1997). From these results, two alternative predation risk hypotheses can be suggested. First, Octodon should show a clear pattern of foraging more under shrubs, followed by Phyllotis, with Akodon exhibiting the least microhabitat preference. Alternatively, Akodon may be under moderate or high predation intensity, but are least observed in predator diets because they are good at avoiding depredation, e.g., by staying under shrubs. At the same time, the high depredation rate of Octodon could be the result of individuals spending a proportionately greater amount of time in the open. Two lines of evidence support the former hypothesis. First, preliminary field observations suggest that Akodon spent more time in the open than did Octodon. Because the vast majority of the predator assemblage includes species that have been observed to feed more in the open than in or under shrubs, Akodon may not be under high predation intensity. Second, Octodon has exhibited a significant numerical response to predator exclusion, whereas Akodon has not (Meserve et al. 1999). Acceptance of the first alternative hypothesis leads to three predictions. First, Octodon GUD should be significantly lower under shrubs than in the open, whereas there should be no significant difference in Akodon GUD between the two microhabitats. Second, Octodon should show significantly lower GUD in the absence of predators than in their presence, followed by Phyllotis and then Akodon. Third, Octodon should show the greatest shift toward foraging in the open as a result of predator exclusion, followed by Phyllotis, with little or no significant response by Akodon. Physiological constraints.—Diurnal species in warm deserts must avoid hyperthermia while foraging in open areas exposed to direct sun and in contact with sand that can be heated to relatively high temperatures. In turn, lower GUD under shrubs could be incorrectly interpreted as foraging to reduce predation risk. For a species that preferentially forages under shrubs, no change in microhabitat selection when predators are removed may indicate microhabitat selection resulting from thermoregulatory constraints. Competition.—Large body size implies competitive superiority in many taxa, including small mammals (Bowers et al. 1987). Thus, in our system, Akodon

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should be competitively dominated by Phyllotis at night, and by Octodon during the day. This leads to the prediction that Akodon should forage more (have lower GUD) in the absence of either Phyllotis or Octodon. Also, if Phyllotis or Octodon show a preference toward a particular microhabitat, this could exclude Akodon, whose GUD should be comparatively lower in an alternative microhabitat. Within- vs. between-patch foraging efficiency.— Seed distribution in deserts is commonly patchy and shows rapid spatiotemporal variation (Price and Reichman 1987). A potential trade-off occurs among individuals that emphasize patch location and interpatch movement vs. those emphasizing intrapatch foraging efficiency (i.e., having relatively low GUD). Thus, we predict that species with individuals moving long distances should have, on average, high GUD; species with individuals moving comparatively short distances should have, on average, relatively low GUD. Lunar light cycle.—The lunar light cycle may cause temporal partitioning. This hypothesis implies greater predation risk with increased lunar light intensity. Following from the previous predation risk hypothesis, we predicted that Akodon GUD would be independent of the lunar light cycle. Phyllotis should forage more under a new moon than under a full moon and should show increased foraging during a full moon on predator-excluded plots. An alternative hypothesis for Akodon is that decreased Phyllotis foraging during a full moon would result in competitive release and increased Akodon foraging. Seasonal.—Coastal north-central Chile has annual pulses of seed production correlated with a distinct wet and dry season (Gutie´rrez et al. 1997) that may contribute to the coexistence of small-mammal species. A species that shows a rapid numerical response to the initial seed pulse would be a relatively inefficient forager (high GUD overall); rapid growth and reproduction would be supported by feeding on rich patches of food. Because this would reduce the initial pulse of food, a species showing a more protracted response should be a relatively efficient forager (low GUD overall), having to obtain food from already foraged patches. ENSO.—El Ninõ–Southern Oscillations (ENSO), which generally last about one year, occur every four years on average (range: 2–10 yr; Cane 1983). In many areas of coastal Chile, ENSO events result in increased levels of precipitation followed by increased seed production (Gutie´rrez et al. 1997). Rapid increases in small-mammal density of one to two orders of magnitude have been recorded following the seed pulse (Pearson 1975, Fuentes and Campusano 1985, Meserve et al. 1995). The high densities can be maintained throughout the ENSO year, followed by declines of one to two orders of magnitude that may occur over several years (Jimeńez et al. 1992). Thus, the magnitude and temporal patterns of population dynamics resulting

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FIG. 1. Map of the IV Region (Coquimbo) in north-central Chile showing the location of Parque Nacional Fray Jorge.

from ESNOs may permit coexistence within the system. We hypothesized that a species showing a rapid numerical response as a result of the ENSO could subsequently depress resource levels. A second species, showing a more delayed numerical response, should be a more efficient forager, further depressing resource availability. This should, in turn, be followed by a corresponding decrease in the numbers of the first species. That is, a trade-off exists between reproductive potential and foraging efficiency. METHODS

Field site The study area is located in Parque Nacional Bosque Fray Jorge (71⬚40⬘ W, 30⬚38⬘ S; IV Region) ⬃100 km south of La Serena and 350 km north of Santiago, Chile near the coast (Fig. 1). This 10 000-ha park contains semiarid thorn scrub vegetation and isolated fog forests on coastal mountain ridges, which have been protected from grazing and disturbance since 1941. The study site is located in a valley (‘‘Quebrada de las Vacas’’) at an elevation of 240 m. Shrub coverage at the site, dominated by Porlieria chilensis, Proustia pungens, and Adesmia bedwellii, averages ⬃50% (Gutie´rrez et al. 1997). The climate is semiarid, with mild (⬃21⬚C)


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winter months (May–October) and warm (⬃25⬚C) dry summers. In 1991 and 1992, there was an ENSO event resulting in heavy rainfall. Rainfall was normal in 1989 (89 mm), and 1990 was a dry year (32 mm), but in 1991 and 1992, rainfall increased to 233 and 229 mm, respectively. Rainfall was close to average in 1993 (77 mm), whereas 1994 was relatively dry (35 mm). In addition to the three principal year-round members of the small-mammal assemblage already noted, four species are rare or sporadic in occurrence (Meserve et al. 1995). The co-occurrence of Thylamys elegans (mouse opossum) with the other small-mammal species may be attributed to its insectivorous diet (Meserve 1981a, b). The occurrence of Oligoryzomys longicaudatus (long-tailed rice rat) is highly sporadic. When coupled with its reproductive biology, the population dynamics and spatial distribution of O. longicaudatus suggest that this species is nomadic (Meserve et al. 1996, 1999). Consequently, T. elegans and O. longicaudatus were not considered further in this study. Abrothrix longipilis (long-haired field mouse), which is insectivorous/herbivorous, and Abrocoma bennetti (Bennett’s chinchilla rat), which is primarily herbivorous, are also present at the site, but will only briefly be considered because of their rarity. In addition to the previously noted small mammals, there are several numerically common vertebrate predators, including owls (Speotyto cunicularia, Tyto alba, Bubo virginianus) and the culpeo fox (Pseudalopex culpaeus). Most are important small-mammal predators (Fulk 1976, Jaksic et al. 1992, 1993, 1997, Meserve et al. 1987). Concentrations of these predators within park boundaries are particularly high because the park has one of the only significant areas of undisturbed semiarid scrub community in north-central Chile. Two species of snakes occur at the site (Tachymenis chilensis and Philodryas chamissonis), although neither is considered an important small-mammal predator (Jaksic 1998).

Experimental design Following initial surveys in late 1988, 16 75 ⫻ 75 m (0.56-ha) plots were established in the valley during January–March 1989 (see Meserve et al. 1996), and monthly small-mammal trapping was initiated. Since March 1989, live-trap small-mammal censuses have been conducted for four nights per month on each of the 16 plots (5 ⫻ 5 array, 15-m interval, 25 stations, two traps per station). Animals were marked with ear tags or leg bands, and data were taken on tag number, species, sex, body mass, reproductive condition, and capture location. Data were analyzed with the Capture– Mark–Recapture programs of Le Boulenge´ (1985). Minimum number known alive (MNKA) estimates per plot were used for analyses of population trends (Seber 1982). These monthly censuses provided data on: (1) small-mammal movements; (2) small-mammal density and species composition during foraging studies (Jan-


uary–February 1993); and (3) a means of relating foraging results to the longer time scale of population dynamics. The investigation used a 2 ⫻ 2 factorial design, with the factors being predation and competition by the largest small mammal (Octodon). The four treatments were located in a homogenous habitat and were assigned using a stratified random design, evenly divided among 16 plots: ⫹D ⫹P (access to degus and predators), ⫹D ⫺P (predator exclusion), ⫺D ⫹P (degu exclusion), and ⫺D ⫺P (degu and predator exclusion; Meserve et al. 1995). Terrestrial predators were excluded with 1.8 m high fencing (with a 1-m overhang) buried 40 cm deep. Avian predators were excluded by suspending polyethylene netting (15 cm diameter mesh) over the grids. Predator-accessible plots had similar fencing only 1 m high. All species other than degus could freely pass through the 2.5-cm mesh fencing; ⬃5.0 cm diameter holes allowed degu entry on degu-accessible plots. Foraging experiments.—Within each plot (experimental unit), four foraging stations were established in January 1993. Two hardware cloth cages were placed at each station, one under shrubs (cover) and one ⬃2– 3 m away from the cover of the nearest shrub (open). The cages were divided into two compartments. One side of the cage had relatively small holes (1.5 ⫻ 1.5 cm) through which only Akodon could pass. The opposing side had large holes (5.0 ⫻ 5.0 cm) through which individuals of the three common species (Akodon, Phyllotis, and Octodon) could pass. Hole size was determined by trials in which individuals were placed in hardware cloth cages with holes of different dimensions. The holes were too small and close to the ground for birds to enter (J. Yunger and P. Meserve, personal observation). During the foraging experiments, a can containing 250 g of sifted sand from the site, mixed with 10 g of oat (Avena) seeds, was placed in each compartment of the cage. This resulted in seed densities similar to those occurring naturally (Gutie´ rrez et al. 1997), although the oats were somewhat larger than natural seeds. The cages prevented birds from feeding on the seeds and partitioned foraging among smallmammal species. Differentiation based on tracks was unreliable because of the coarse sand. Ants were relatively rare at the site and were not considered important seed predators. Foraging Experiment 1 (predation).—The first experiment, conducted during a new moon, was designed to test the effects of predators on both nocturnal and diurnal small mammals, using the predator exclusion (⫹D ⫺P) and predator access plots (⫹D ⫹P). Cans containing sand and preweighed seeds were placed in the cages at dawn. Contents were collected and replaced at dusk and then again the following dawn. This protocol was repeated for a second consecutive 24-h period to determine the repeatability of the results. The two 24-h periods were treated as blocks. By collecting the seeds at dusk and dawn, it was possible to examine


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TABLE 1. Comparison of mean giving-up densities (GUD) of the olivaceous field mouse (Akodon olivaceus) and Darwin’s leaf-eared mouse (Phyllotis darwini) for main effects. GUD (mean ⫾ 1 Main effect No predator With predator Open Cover

Akodon 6.706 3.862 5.014 5.455

⫾ ⫾ ⫾ ⫾

0.492 0.325 0.459 0.452

SE )

Phyllotis

df

t

P

⫾ ⫾ ⫾ ⫾

47 47 47 47

8.462 3.331 4.786 6.816

⬍0.0001 0.0011 ⬍0.0001 ⬍0.0001

2.386 2.792 2.266 2.712

0.098 0.135 0.122 0.158

Octodon exclusion plots (t ⫽ 1.87, df ⫽ 126, P ⫽ 0.12), providing additional support that the GUDs of the two larger species were not masked by that of Akodon. Demographics and movements.—We analyzed the population data on two temporal scales, short and long term. The short-term scale (January–March 1993) included censuses conducted prior to, between, and following the foraging experiments, and was analyzed to determine if predator or competitor exclusions had a numerical effect on any of the three principal species during the foraging study. The long-term scale included data collected between March 1989 and October 1994. This range of dates provided a time series representing two years of non-ENSO dynamics, numerical responses during an ENSO event, and the decline following an ENSO. Because Octodon is diurnal and Phyllotis is nocturnal, we did not conduct a foraging experiment on competitive interactions between these two species. Accordingly, unlike the studies of Meserve et al. (1995, 1996, 1999) that provide more complete analyses of the population dynamics, the Phyllotis density analysis reported here does not include the competitor exclusion plots. The percentage of reproductively active individuals on control plots was used to compare differences in reproductive patterns among the three principal species. Males were classified as reproductively active if their testes were descended (vs. abdominal); females were classified as reproductively active if they were perforate, lactating, or visibly pregnant. Only the period September 1991–October 1994 was used for comparisons of reproductive activity, due to limited sample size. Within plots, capture records from the four controls were used to calculate the mean distance between successive captures (MDBSC) for both the short- and long-term scales. Between plots, the percentage of in-

differences between nocturnal and diurnal foraging by Akodon, using the Akodon-only side of the cage. The side with the large holes was used to determine the nocturnal foraging by Phyllotis and diurnal foraging by Octodon. Because Akodon had access to both sides of the cage, the GUD of the two larger species could potentially be obscured if Akodon had a lower GUD. However, a comparison of the GUD of the two sides of the cage for all main effects (including those of Experiments 2 and 3) showed that the means were consistently and highly significantly lower on the all-species access side (Tables 1 and 2). This indicates that Phyllotis and Octodon had lower rates of diminishing return than Akodon and that the all-species access side of the cage can be used to measure the GUD of the two larger species. Foraging Experiment 2 (lunar light).—The second foraging experiment tested the effects of predators and lunar light levels on the nocturnal species, using the ⫹D ⫹P and ⫹D ⫺P plots. The nocturnal data collected during the first night of Experiment 1 were used as the new moon treatment. Fourteen days later, the design followed in Experiment 1 was repeated with a full moon under a clear, cloudless sky. Foraging Experiment 3 (competition).—The third experiment examined the effects of interspecific competition on foraging behavior, using the ⫹D ⫹P and ⫺D ⫹P plots. Because Octodon are strictly diurnal, the experiment was conducted only during the day. Consequently, only data on Akodon GUD were collected. The protocol was the same as in Experiment 1: four stations, two cages per station, one in the open and one under a shrub. For consistency, the GUD from the Akodon-only side of the cages was used. However, there was no significant difference between GUD on the Akodon-only (7.72 ⫾ 0.42 g; X¯ ⫾ 1 SE) and all-species sides of the cages (6.85 ⫾ 0.74 g; X¯ ⫾ 1 SE) on the

TABLE 2. Comparison of mean giving-up densities (GUD) of the ovilaceous field mouse (Akodon olivaceus) and the degu (Octodon degus) for main effects. GUD (mean ⫾ 1 Main effect No predator With predator Open Cover

Akodon 8.793 8.019 8.073 8.109

⫾ ⫾ ⫾ ⫾

0.195 0.286 0.207 0.281

SE )

Octodon

df

t

P

⫾ ⫾ ⫾ ⫾

47 47 47 47

15.075 10.127 9.810 17.738

⬍0.0001 ⬍0.0001 ⬍0.0001 ⬍0.0001

3.120 3.788 4.659 2.350

0.306 0.318 0.357 0.163



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TABLE 3. ANOVA models used for analyzing Octodon degus, Phyllotis darwini, and Akodon olivaceus giving-up densities for foraging Experiment 1, predation effects.

Octodon degus and Phyllotis darwini Source of variation

Akodon olivaceus

df

Error

Source of variation

df

Error

Pred Plot(Pred) Station(Plot ⫻ Pred) Cover Block

1 6 24 1 1

Pred ⫻ Block Error Error Cover ⫻ Block Pred ⫻ Block ⫹ Cover ⫻ Block ⫺ Pred ⫻ Cover ⫻ Block

Pred Plot (Pred) Station (Plot ⫻ Pred) Cover Time Block

1 6 24 1 1 1

Pred ⫻ Cover Pred ⫻ Block Cover ⫻ Block Pred ⫻ Cover ⫻ Block Error

1 1 1 1 90

Pred ⫻ Cover ⫻ Block Pred ⫻ Cover ⫻ Block Pred ⫻ Cover ⫻ Block Error

Pred ⫻ Cover Pred ⫻ Time Cover ⫻ Time Pred ⫻ Block Cover ⫻ Block Time ⫻ Block Pred ⫻ Cover ⫻ Time Error

1 1 1 1 1 1 1 214

Pred ⫻ Block Error Error Cover ⫻ Block Time ⫻ Block Pred ⫻ Block ⫹ Cover ⫻ Block ⫹ Time ⫻ Block ⫺ 2 ⫻ Error Error Error Error Error Error Error Error

Note: Explanations for sources of variation: pred, predator exclusion vs. predator access; Block, day 1 vs. day 2.

dividuals for which interplot movements were detected was calculated at the long time scale.

Statistical analysis The three foraging experiments were analyzed as hierarchical split-plots, with plots nested within treatments and stations nested within plots ⫻ treatments, using SAS PROC GLM (SAS Institute 1990a). Plots were treated as the experimental unit to avoid pseudoreplication (Hurlbert 1984). Tables 3 and 4 outline all main effects (sources of variation), nested levels, and interactions. For brevity, only significant results from these models are presented in text. In all cases, inference was based on Type III sum-of-squares. With the exception of the block term in Experiment 1, all sources of variation were treated as fixed. The block term was treated as random to generalize the repeatability of the experiment, resulting in a mixed model. Selection of the appropriate error terms for the mixed models was accomplished using the SAS PROC GLM

RANDOM (SAS Institute 1990a) option, and follows Littell et al. (1991). All other models used the global error term. One-way ANOVA was used to test for significant differences between MDBSC; Rayn’s Q test was used for post hoc multiple comparisons (Day and Quinn 1989, SAS Institute 1990a). Chi-square goodness of fit was used to test for significant differences between the percentages of individuals moving between plots. The short-term demographic data were analyzed by MANOVA using SAS PROC GLM (SAS Institute 1990a). Time (3 mo) was used as the response variable. For the reproductive patterns and long-term population trends, a univariate repeated-measures ANOVA (rmANOVA) was used (SAS PROC GLM; SAS Institute 1990a, Winer et al. 1991, von Ende 1993). All within-subject inferences were based on Huynh-Feldt adjusted P values (Huynh and Feldt 1970). To help partition within- and between-year effects, we used a doubly-within-subjects design (Winer et al. 1991) for

TABLE 4. ANOVA models used for analyzing Phyllotis darwini and Akodon olivaceus givingup densities for foraging Experiment 2 (lunar light levels) and for Akodon olivaceus in Experiment 3 (interspecific competition). Experiment 3

Experiment 2 Source of variation

df

Source of variation

df

Pred Plot (Pred) Station (Plot ⫻ Pred) Moon Cover Pred ⫻ Cover Pred ⫻ Moon Moon ⫻ Cover Pred ⫻ Moon ⫻ Cover Error

1 6 24 1 1 1 1 1 1 90

Competitor Plot (Competitor) Station (Plot ⫻ Competitor) Cover Competitor ⫻ Cover Error

1 6 24 1 1 63

Notes: Explanations for sources of variation: pred, predator exclusion vs. predator access; moon, full moon vs. new moon; competitor, presence vs. absence of Octodon. The global error term was used in all F tests.


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TABLE 5. Doubly-within-subject repeated-measures ANOVA models used for analyzing minimum number known alive per plot for Octodon degus, Phyllotis darwini, and Akodon olivaceus during the wet season and dry season. Within-subject P values are Huyhn-Feldt adjusted.

Octodon degus and Phyllotis darwini Source of variation Between subject: Predation (Pred) Error

Within subject: Year Year ⫻ Pred Error (Year) Month Month ⫻ Pred Error (Month)

Akodon olivaceus Source of variation

df 1 6

4 4 24 5 5 30

Between subject: Predation (Pred) Competition (Comp) Pred ⫻ Comp Error

df 1 1 1 12

Within subject: Year 4 Year ⫻ Pred 4 Year ⫻ Comp 4 Year ⫻ Pred ⫻ Comp 4 Error (Year) 48 Month 5 Month ⫻ Pred 5 Month ⫻ Comp 5 Month ⫻ Pred ⫻ Comp 5 Error (Month) 60

the analysis of population fluctuations. Due to seasonal variation, separate analyses were conducted for both the wet (November–April) and dry (May–October) seasons (Table 5). Using graphical interpretations (stem-leaf plots, box plots, and quartile plots; Tukey 1977) and the ShapiroWilks statistic, W (Shapiro and Wilks 1965), generated with SAS PROC UNIVARIATE (SAS Institute 1990b), residuals from the ANOVAs were tested for significant deviations from normality. The Shapiro-Wilks statistic tests the hypothesis that data do not fit a normal distribution, and because ANOVA is robust for deviation from normality (Winer et al. 1991, Underwood 1997), alpha was set a priori at 0.01 (null hypothesis: data are normally distributed). Because the previous criteria indicated that the residuals did not differ significantly from normality, the data were not transformed. Any deviations from normality would increase the Type II error rate, resulting in more conservative tests. Homogeneity of cell variances (precluding within-subject analyses) were tested using an F-max test. RESULTS

Foraging Experiment 1 (predation).—For all three species, the predation foraging experiments had no significant block term and only one significant interaction involving the block term, indicating that the results are at least reasonably repeatable. The significant Akodon time ⫻ block interaction (F ⫽ 8.244, P ⫽ 0.004; refer to Table 3 for all Experiment 1 df values) indicated that there was increased foraging during the second night, a possible associative learning effect. Octodon foraged significantly more when predators were excluded (F ⫽ 2166.52, P ⫽ 0.012; Fig. 2a) and

FIG. 2. Significant giving-up densities (GUD) of the degu, Octodon degus, for Experiment 1: (a) foraging on predatorexcluded vs. predator-accessible plots and (b) under shrub cover vs. in the open. Panel (c) depicts the predation ⫻ cover interaction. GUD is given as grams of seeds (mean ⫾ 1 SE).

more under shrubs as opposed to in the open (F ⫽ 11 978.01, P ⫽ 0.005; Fig. 2b). This supports the prediction that Octodon responds behaviorally to predation risk. However, the predator ⫻ cover interaction was not significant (F ⫽ 4.810, P ⫽ 0.272), indicating that Octodon did not respond to a reduction in predation risk by foraging more in the open, although there was a trend toward increased foraging in the open on predator exclusion plots (Fig. 2c). These results support the

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FIG. 3. Significant giving-up densities (GUD) of Darwin’s leaf-eared mouse, Phyllotis darwini, for Experiment 1: (a) foraging on predator-excluded vs. predator-accessible plots and (b) under shrub cover vs. in the open. GUD is given as grams of seeds (mean ⫾ 1 SE).

FIG. 4. Significant giving-up densities (GUD) of the olivaceous field mouse, Akodon olivaceus, for Experiment 1: (a) foraging on predator-excluded vs. predator-accessible plots and (b) during both the day and the night. GUD is given as grams of seeds (mean ⫾ 1 SE).

physiological constraints hypothesis that thermoregulatory constraints limit the time Octodon can spend foraging in the open (Lagos et al. 1995a). The only significant treatment effect on Phyllotis foraging in Experiment 1 was predator exclusion (F ⫽ 453.67, P ⫽ 0.009). As predicted, Phyllotis foraged more in the absence of predators (Fig. 3a). There was a marginally significant trend toward lower Phyllotis GUD in the open vs. under cover of shrubs (F ⫽ 2166.50, P ⫽ 0.012; Fig. 3b). There was a marginally significant effect of predator exclusion on Akodon foraging (F ⫽ 129.57, P ⫽ 0.052; Fig. 4a). The increase in Phyllotis and Octodon foraging on predator exclusion plots was the probable cause for the reduction in Akodon foraging. Akodon also had a significant predator ⫻ time interaction (F ⫽ 13.20, P ⬍ 0.001), with higher GUD during the night on predator exclusion plots than on controls; during the day, GUDs on the predator access plots were similar to, but somewhat lower than, those on predator exclusion plots (Fig. 4b). Because Octodon is diurnal, this

would suggest that Phyllotis was primarily responsible for the decrease in Akodon foraging when predators were excluded. Foraging Experiment 2 (lunar light).—Phyllotis foraged more under a new moon than a full moon (F ⫽ 3.90, P ⫽ 0.051; Fig. 5a), suggesting the importance of reduced predation risk (refer to Table 4 for all experiment 2 df values). However, the predator ⫻ moon interaction was not significant, indicating that Phyllotis did not respond behaviorally to the exclusion of predators, and that lunar light levels play only a weak role in determining how Phyllotis perceives predation risk. Contrary to the prediction, Phyllotis foraged more in the open than under shrubs (F ⫽ 21.85, P ⬍ 0.001; Fig. 5b). However, the lack of a significant predator ⫻ cover interaction indicated that Phyllotis did not respond behaviorally to the predator exclusions, or that predation risk is of secondary importance to alternative foraging constraints. Akodon had significantly lower GUD on predator access plots (F ⫽ 8.30, P ⫽ 0.005; Fig. 6a). As in

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FIG. 5. Significant giving-up densities (GUD) of Phyllotis darwini for Experiment 2: (a) foraging during a new vs. full moon and (b) under shrub cover vs. in the open. GUD is given as grams of seeds (mean ⫾ 1 SE).

Experiment 1, this may be the result of interspecific competition. There was a significant predator ⫻ moon interaction (F ⫽ 8.12, P ⫽ 0.005) and a marginally significant moon ⫻ cover interaction (F ⫽ 3.60, P ⫽ 0.061) (refer to Table 3 for all Experiment 1 df values). Under a new moon, Akodon GUDs were lower on predator access plots than on predator exclusion plots; under a full moon, Akodon GUDs were virtually identical for the two treatments (Fig. 6b). These results provide additional support for the interspecific competition hypothesis; Phyllotis foraged more under a new moon than during a full moon, with a trend toward increased foraging on predator exclusion plots. Akodon GUDs under shrubs were relatively similar for both the new moon and full moon treatments. However, there was a shift toward increased foraging in the open under a new moon (Fig. 6c). Although Phyllotis foraged more during a new moon, this was not followed by a corresponding increase in Akodon foraging during a full moon. Thus, the alternative lunar light cycle hypothesis is refuted. Foraging Experiment 3 (competition).—Akodon olivaceus had significantly lower GUD on competitor ex-

FIG. 6. Significant giving-up densities (GUD) of Akodon olivaceus for Experiment 2: (a) foraging on predator-excluded vs. predator-accessible plots; interactions involving predation (b) during a full moon vs. new moon and (c) under shrub cover vs. in the open. GUD is given as grams of seeds (mean ⫾ 1 SE).

clusion plots (F ⫽ 20.29, P ⫽ ⬍0.001; Fig. 7). This provides direct experimental support for the competition hypothesis: in the absence of Octodon, the smaller Akodon foraged more. There was no significant competitor ⫻ cover interaction, suggesting that diurnal in-

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FIG. 7. Significant giving-up densities (GUD) of Akodon olivaceus for Experiment 3: foraging on Octodon-excluded vs. Octodon-accessible plots. GUD is given as grams of seeds (mean ⫾ 1 SE).

terspecific competition does not play a role in determining the microhabitats in which Akodon forages. Demography and movements.—At the short time scale, Octodon densities were significantly higher on the predator exclusion plots (F ⫽ 12.7, df ⫽ 1, 6, P ⫽ 0.021; Fig. 8a). Phyllotis densities were significantly lower on the predator exclusion plots (F ⫽ 14.8, df ⫽ 1, 6, P ⫽ 0.007; Fig. 8b), whereas the number of Akodon did not differ significantly between the control, competitor exclusion, and predator exclusion plots (F ⫽ 2.41, df ⫽ 1, 2, P ⫽ 0.457; Fig. 8c). The analysis of population dynamics showed that, on the long time scale, all three principal species had significant month effects; Octodon during both the wet (F ⫽ 12.20, P ⬍ 0.001) and dry (F ⫽ 15.08, P ⬍ 0.001) season and Phyllotis (F ⫽ 15.76, P ⬍ 0.001) and Akodon (F ⫽ 74.45, P ⬍ 0.001) during the wet season (refer to Table 4 for all Experiment 3 df values). In pre-ENSO, Octodon increased in densities during the first 5 mo of the dry season (Fig. 9a). During the transition from the wet to the dry season (⬃April– May), there was a decrease in densities, followed by a gradual increase in numbers during the wet season. Phyllotis exhibited a pattern very similar to that of Octodon, increasing in numbers during the first 5 mo of the wet season, followed by a decline in numbers between seasons (Fig. 9b). Significant month effects for Akodon were primarily the result of increased numbers during the ENSO. There were no clear seasonal patterns. Prior to the ENSO, Akodon were relatively rare (Fig. 9c; Meserve et al. 1995). The relatively synchronous seasonal population dynamics of Octodon and Phyllotis and the rarity of Akodon provide little or no support for the seasonal coexistence hypothesis. All three species showed highly significant numerical year effects during both the wet (Octodon, F ⫽ 88.17, P ⬍ 0.001; Phyllotis, F ⫽ 191.58, P ⬍ 0.001; Akodon, F ⫽ 365.46, P ⬍ 0.001) and dry (Octodon, F

FIG. 8. Small-mammal densities (minimum number known alive, mean ⫾ 1 SE) during the foraging experiments: (a) Octodon degus, (b) Phyllotis darwini, (c) Akodon olivaceus. Abbreviations are: ⫺D, Octodon excluded; ⫹D, Octodon present; ⫺P, predators excluded; and ⫹P, predator access.

⫽ 111.80, P ⬍ 0.001; Phyllotis, F ⫽ 60.14, P ⬍ 0.001; Akodon, F ⫽ 81.22, P ⬍ 0.001) seasons. As a result of the ENSO, Akodon and Phyllotis numbers increased synchronously starting in November 1991, although the rate of increase in Akodon quickly exceeded that of Phyllotis (Fig. 9b, c). Akodon reached a peak in January 1992, followed by a gradual 8-mo decline. They


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FIG. 9. Small-mammal densities (minimum number known alive, mean ⫾ 1 SE) between March 1989 and October 1994: (a) Octodon degus, (b) Phyllotis darwini, (c) Akodon olivaceus. Abbreviations are: ⫺D, Octodon excluded; ⫹D, Octodon present; ⫺P, predators excluded; and ⫹P, predator access. The gray area denotes the ENSO period.

TABLE 6. Repeated-measures ANOVA of the percentage of reproductively active Octodon degus, Phyllotis darwini, and Akodon olivaceus during the period of high densities resulting from the ENSO, September 1991–October 1993. Source of variation

df

Between subjects: Species Error Within subject: Time Time ⫻ Species Error

MS

F

P

2 9

26 946.48 1221.29

22.06

⬍0.001

37 74 33

4592.64 1539.04 257.62

17.83 5.97

⬍0.001 ⬍0.001

reached their highest peak in December 1992, and then began a continuous decline to pre-ENSO numbers by spring 1994 (Fig. 9c). Following their initial increase in November 1991, Phyllotis reached a high in January 1992, after which numbers remained relatively constant for the duration of the ENSO. They then declined precipitously in November 1993. Octodon did not begin to increase substantially in density until September 1992, 10 mo after the other two species (Fig. 9a), which reached peak densities around January–May 1993. Following a gradual decline, Octodon densities remained relatively stable until May 1994, when they declined rapidly. There was a significant difference in the percentage of reproductively active individuals among Octodon, Phyllotis, and Akodon (Table 6). Both within-subject

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FIG. 10. Percentage of reproductively active individuals during the period of high densities resulting from the ENSO, September 1991–October 1994. Data are based on trap records from the control plots only.

terms, time, and time ⫻ species, were significant (Table 6), indicating that the percentage of reproductively active individuals fluctuated differently among the three species. The onset of reproduction was similar between Akodon and Phyllotis during the spring 1991 (Fig. 10). Consequently, it is unlikely that differences in the timing of reproduction contributed to the more rapid increase of Akodon as compared to Phyllotis. The most notable difference in reproductive timing between the three species was a protracted response by Octodon, which may be attributed to its reproductive biology. Octodontids are caviomorph rodents that have long gestation periods compared to other rodents (Weir 1974, Meserve et al. 1995). This resulted in a 10-mo lag before the percentage of reproductively active individuals of Octodon reached levels approaching Akodon and Phyllotis (Fig. 10). The numerical and reproductive responses to the ENSO provide support for the ENSO hypothesis. Prior to the ENSO, Akodon was generally less common than either Phyllotis or Octodon. It was also the least efficient forager (i.e., it had the highest GUD overall; Tables 1 and 2), and showed the most rapid increase and decrease in numbers. Its decrease preceded that of the two more efficient foragers, Phyllotis and Octodon, by 10 and 17 mo, respectively. Predator exclusion had an overall (between-subject) effect on Octodon numbers during the dry season (F ⫽ 6.16, P ⫽ 0.047; Fig. 9a). A significant year ⫻ predator interaction (F ⫽ 6.16, P ⫽ 0.047) was the result of Octodon increasing at greater rates on the predator exclusion plots than on the controls. A significant month ⫻ predator interaction reflected an increase in numbers on predator exclusion plots during the wet season (F ⫽ 12.20, P ⬍ 0.001); during the dry season, this trend was reversed (F ⫽ 15.08, P ⬍ 0.001;

Fig. 9a). The only significant effect of predator removal on Phyllotis was a month ⫻ predator interaction during the wet season (F ⫽ 15.76, P ⬍ 0.001), the result of numbers on the treatment plots being greater than on the controls at the start of the season and converging by the end of the season (Fig. 9b). There was no significant overall effect of predator or competitor exclusion on Akodon numbers. There was a significant year ⫻ predator interaction for Akodon during the dry season (F ⫽ 7.38, P ⫽ 0.006) and a significant month ⫻ competitor interaction in the wet season (F ⫽ 2.79, P ⫽ 0.025; Fig. 9c). At the long time scale, the principal three species, plus Abrothrix and Abrocoma, differed significantly in MDBSC (F ⫽ 5.81, df ⫽ 4, 15, P ⫽ 0.0102). There was also a significant difference in MDBSC at the short time scale, although Abrocoma was not included because of small sample size (F ⫽ 10.44, df ⫽ 3, 12, P ⫽ 0.0012). A multiple comparison showed that Abrothrix, at both time scales, and Abrocoma, at the long time scale, had significantly greater MDBSC than did the three principal species (Table 7). For the three principal species, Abrothrix, and Abrocoma, there was a significant difference in the percentage of individuals moving between plots at the long time scale (␹2 ⫽ 24.610, df ⫽ 4, P ⫽ ⬍0.001). Abrothrix had significantly greater between-plot movement (42.8% of the individuals) than did any of the other species, whereas Abrocoma had significantly fewer (1.75%); there was no significant difference among the three principal species. Although GUD data are not available for Abrothrix, its significantly greater rates of both within- and betweenplot movements provide inferential support for the within- vs. between-patch foraging efficiency hypothesis.


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TABLE 7. Distances moved (mean ⫾ 1 small-mammal species.

SE )

573

between successive captures at the short- and long-term time scales for five

Time period

Akodon olivaceus

Octodon degus

Phyllotis darwini

Abrothrix longipilis

Abrocoma bennetti

Short term

11.78 ⫾ 0.390

13.25 ⫾ 0.346

13.32 ⫾ 0.174

22.25 ⫾ 1.18

NA

Long term

14.82 ⫾ 0.166

14.82 ⫾ 0.336

16.57 ⫾ 0.315

--------------------------------

22.08 ⫾ 0.515

20.40 ⫾ 1.325

----------------------------------------------------------------------------------------------------

Notes: Means with the same underline type are not significantly different using Ryan’s Q test. ‘‘NA’’ indicates that the sample size was not adequate for statistical analysis (␣ ⫽ 0.05).

DISCUSSION

Small-mammal foraging in Chile As predicted, Octodon foraged more in the absence of predators, although the data on GUD are confounded by the numerical response that occurred at the time of the foraging study. This leads to a circular dilemma: does increased foraging (i.e., lower GUD as a result of decreased predation risk) lead to increased densities, or do increased densities, due to decreased mortality resulting from predator exclusion, lead to increased foraging? Three lines of evidence suggest that the increased foraging was a behavioral response to reduced predation risk. First, Phyllotis densities were lower on predator exclusion plots and they had lower GUD. Thus, when the Phyllotis and Octodon foraging and demography results are viewed jointly, GUD were lower in areas of reduced predation risk, irrespective of rodent densities. Second, predator exclusion does alter Octodon behavior. Lagos et al. (1995b) showed that individuals moved in a more linear fashion on exclusion plots as compared to controls. These linear movements were the result of individuals traversing open areas as opposed to traveling more circuitous routes beneath shrubs. Finally, Mitchell et al. (1990) provide both theoretical and empirical support that increased competition resulting from increased densities should reduce foraging effort. If predation risk did result in decreased Octodon foraging in the open, this should have been reflected as a significant predator ⫻ cover interaction, which was not detected (although there was a trend toward foraging more in the open). If Octodon responded behaviorally to predator exclusion, why did they not forage significantly more in the open? We believe that this was due to thermoregulatory constraints because Octodon is stenothermic (Rosenmann 1977). Lagos et al. (1995a) found that Octodon body temperatures can quickly rise to hyperthermic levels in open locations as opposed to under shrubs. All individuals experiencing hyperthermy at air temperature ⬎30⬚C were located in open areas, never under shrubs. Foraging experiments were also conducted in the warmest months. Thus, in the absence of predators, there is little or no selective pressure to avoid crossing open areas or spending short periods of time feeding on particularly rich patches of

food. Overheating, however, precludes spending more than a few minutes foraging on all but the richest patches in the open, producing relatively high GUD. This supports the physiological hypothesis. A second possible physiological constraint is water loss, although it is unlikely that this applies to Octodon degus. Corte´s et al. (1994) has shown this species to have a highly developed recapture rate of water through the nares, and a relatively low overall rate of water loss. Thus, for Octodon, a single-factor explanation is not adequate. As discussed previously, two or more predictions supported by significant or marginally significant treatment effects would suggest that individuals are ‘‘balancing’’ multiple constraints. Predators clearly influenced Phyllotis foraging. During Experiment 1, Phyllotis had significantly lower GUD on the exclusion plots, and in Experiment 2, it foraged more during a new moon than a full moon, suggesting a partial role of lunar light levels in influencing predation risk. This was as predicted; Phyllotis appears under moderate predation intensity. The field experiments support laboratory studies of foraging by Phyllotis (Va´squez 1994). When exposed to artificial light levels similar to that of a full moon, Phyllotis had significantly more evasive reactions to an avian predator model than at light levels comparable to a new moon. Similarly, individuals significantly increased their GUD under artificial full-moon light levels (Va´ squez 1994). We also predicted that to reduce predation risk, Phyllotis would forage more under shrubs: the opposite was found. During both Experiments 1 and 2, Phyllotis had lower GUD in the open than under shrubs. There are two possible explanations. The first is competition with Octodon. As discussed previously, seed renewal does not occur on a daily basis. If Octodon feeds under shrubs due to physiological constraints, thereby depleting resource levels, this could force Phyllotis to feed more in the open. The second explanation, which is commonly applied to heteromyids (Reichman and Price 1993), is based on morphology. Species that are adapted to detecting and escaping predators (i.e., having inflated auditory bulla, large outer ears, and saltorial locomotion) may forage in areas with increased predation risk, but also with reduced competition for

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food. Phyllotis has large eyes, large pinna (J. Yunger and P. Meserve, personal observation), and slightly inflated auditory bulla (Steppan 1995), all of which aid in detecting predators. It also has a bounding gate (as opposed to the diagonal sequence gait of Octodon and Akodon; J. Yunger and P. Meserve, personal observation) and comparatively elongated feet and hind limbs that would aid in escaping predators. Although Phyllotis does not have nearly as highly specialized morphological adaptations as Dipodomys or Microdipodops, its morphology does suggest that it would have a selective advantage over Octodon or Akodon when foraging in the open. Based on the monthly trap censuses, it is clear that Akodon had greater nocturnal than diurnal activity. What the trap data cannot elucidate are potential mechanisms to explain this. Three alternative hypotheses can account for the Akodon activity, based on trapping: (1) increased interspecific competition during the day; (2) physiological constraints (e.g., temperature and water); and (3) decreased predation intensity at night. Hypothesis (3) is unlikely because Akodon is not under high predation intensity and, when recorded in predator diets, most often occurs in pellets of nocturnal owls (Jaksic et al. 1993, 1997). In addition, there have been no main effects of predator exclusion on Akodon numbers, and Akodon had lower GUD on predator access plots during both Experiments 1 and 2. The answer to hypothesis two remains unclear and requires further investigation. However, because there was virtually no difference in diurnal Akodon GUD in the open as compared to under shrubs, it is unlikely that thermoregulatory constraints are important. This also is supported by work on water dependency. Although Akodon could forage more at night to reduce water loss, they can survive for 3–4 wk without free water (Meserve 1978), suggesting that it is relatively unimportant as a physiological constraint. There is direct experimental support for the first hypothesis: in the absence of Octodon, Akodon have significantly lower GUD. However, competition from Octodon must also be balanced with competition from Phyllotis and potential owl predation. Competition between Phyllotis and Akodon was not tested experimentally, although a competitive effect is suggested by the inverse relationships between Phyllotis and Akodon GUD. There also is evidence that owl predation affects Akodon GUD, albeit in a limited way. During a full moon, Akodon must ‘‘balance’’ competition with Phyllotis and predation risk. If predation risk is reduced under low lunar light levels and Phyllotis foraging is greater on predator exclusion plots, then Akodon should forage more on predator-accessible plots under relatively low lunar light levels. This is supported by the significant predator ⫻ moon interaction. Second, during a new moon, Akodon shift foraging toward open sites. Although owl predation may have some influence on Akodon foraging behavior, it is unlikely to play a major


role in determining coexistence at our site; competition appears to play the predominant role influencing Akodon foraging.

Relation to population dynamics Together, the data on population dynamics and GUD provide support for the ENSO hypothesis. Akodon, the least efficient forager, showed the strongest and most rapid response to the ENSO. This response can be attributed to differences in reproductive biology. Mean litter size for the three principal species is similar (Meserve and Le Boulenge´ 1987). However, Phyllotis and Akodon can reach sexual maturity in ⬃2 mo, whereas Octodon, a caviomorph, takes ⬃10 mo (Meserve and Le Boulenge´ 1987). Also, the gestation period of Octodon (⬃90 d; Weir 1974) is substantially longer than that of Phyllotis or Akodon (Meserve and Le Boulenge´ 1987). The difference between Phyllotis and Akodon is less clear. Both species responded at about the same time to the ENSO, yet Akodon continued to increase rapidly, resulting in densities nearly three times greater than Phyllotis. There is evidence that immigration may be partially responsible for the large, rapid increase in Akodon numbers (Meserve et al. 1999). This species began to decline at about the same time that Octodon reached its peak density. Presumably, the decline was precipitated when the two more efficient foragers depleted abundant patches of food. Whether Akodon would disappear entirely from the small-mammal assemblage if not for periodic ENSO events is difficult to ascertain. Current work on metapopulation structure may shed light on the spatiotemporal dynamics of the species and determine the importance of refuges and recolonization. The limited effect of predator exclusion on Akodon foraging behavior is corroborated at the population level. The only detectable numerical effect of predator exclusion on Akodon numbers was a year ⫻ predator interaction during the dry season. This provides further evidence that predators play only a limited role in the overall behavioral and demographic dynamics of Akodon. The effects of competitor exclusion on Akodon foraging behavior can be seen at the population level by the significant month ⫻ competitor interactions during both seasons. Octodon exclusion had a strong effect on Akodon foraging, which translates into significant seasonal fluctuations in Akodon numbers. Phyllotis, which showed limited changes in foraging behavior due to predator exclusion, had only weak numerical responses to the exclusion of predators. Similarly, Octodon, which showed an increase in foraging as a result of predator exclusion, had strong and pervasive numerical responses in the absence of predators.

Comparisons with other systems Microhabitat partitioning (i.e., open vs. covered sites) has been widely implicated as a mechanism for coexistence among desert rodents (Kotler and Brown

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1988). Spatial variation appears to be one mechanism responsible for the coexistence of Phyllotis and, in particular, Akodon, with Octodon. For several deserts around the world, predation risk has been suggested as the selective force resulting in microhabitat partitioning (Rosenzweig 1973, Thompson 1982a, b, Price 1984, Kotler and Brown 1988, Kotler et al. 1988, Hughes et al. 1994, Va´squez 1994). Although predation risk may be partially responsible for the observed open vs. cover foraging behavior of Octodon, physiological constraints are also important at our site in Chile. For Akodon, interspecific competition appears to be more important than predation risk in determining microhabitat partitioning. In addition, rodents in numerous arid regions of the world have evolved morphological adaptations to aid in predator detection and avoidance (Kotler and Brown 1988, Mares 1993). Large pinna and inflated auditory bullae that aid in hearing are particularly pronounced among Dipodomys, Microdipodops, Jaculus, and Allactaga. Bipedal locomotion, also common among the four previous genera, aids in predator avoidance. South America has no extant morphological equivalents to the bipedal heteromyids and dipodids (Mares 1993). There is evidence that Phyllotis is better adapted at escaping and detecting predators than are other small mammals in the assemblage, which may partially account for their level of foraging in the open. However, it is unlikely that unique morphological adaptations for utilizing open microhabitats play an overriding role as a mechanism for resource partitioning at our site. Similar to findings in the Sonoran (Brown 1989) and Negev (Ziv et al. 1993, Brown et al. 1994) Deserts, temporal partitioning is an important mechanism for small-mammal coexistence in north-central Chile. However, the temporal scales among the three deserts vary greatly. In the Negev, diel redistribution of seeds results in partitioning between early- and late-night foragers (Brown et al. 1994). In the Sonoran, foraging efficiencies vary on a seasonal basis, permitting coexistence due to annual fluctuations (Brown 1989). In north-central coastal Chile, long-term (⬃4–7 yr) fluctuations in rainfall resulting from ENSO events appear to be the primary mechanism supporting Akodon coexistence. In the Sonoran Desert, Brown (1989) concluded that one species coexisted by traveling long distances and ‘‘skimming’’ numerous patches of abundant food. This may also be the mechanism for coexistence of Abrothrix, although further investigations are necessary to confirm this. Finally, it must be remembered that resource axes other than space and time may be potential mechanisms for coexistence. All three principal species and Abrothrix in our study readily feed on seeds, although there are also some distinct differences in their diets (Meserve 1981a, b). When coupled with spatial differences in microhabitat use, temporal differences in demography, and possible metapopulation dynamics,

575

it is apparent how seven species of small mammals can coexist in coastal north-central Chile. In conclusion, there are numerous possible mechanisms for the coexistence of desert rodents that are common throughout the world. It should also be recognized, though, that phylogenetic constraints, historical artifacts, and different selective pressures have resulted in some distinct differences (Kelt et al. 1996). This is exemplified by our Chilean site. The strong, periodic effects of ENSOs and geographic isolation on the west side of the Andes (Meserve and Glanz 1978, Meserve and Kelt 1990) have resulted in a system that has evolved a set of special, unique characteristics. ACKNOWLEDGMENTS We thank the following people who have served as technicians on the project: Kenneth L. Cramer, Sergio Herrera, V. O. Lagos, Brian K. Lang, Bryan Milstead, Sergio S. Silva, Elier Tabilo, and Miguel-Angel Torrealba. Also, we appreciate the assistance of various Earthwatch volunteers in 1993. We are grateful to the Corporacioń Nacional Forestal, IV Region, and, in particular, to Waldo Canto and Juan Cerda for permitting the realization of this project in Parque Nacional Fray Jorge. We also appreciate the cooperation of park personnel there. Burt Kotler, Barry Fox, Lynda Randa, and an anonymous reviewer offered valuable comments that helped to improve the manuscript. The Northern Illinois University Institutional Animal Care and Use Committee approved all work. Support for this project has come from the Graduate School, Northern Illinois University, the U.S. National Science Foundation (BSR-8806639 and DEB9020047), and the Fondo Nacional de Investigacioń Cientifica y Tecnolo´gica (FONDECYT 90-0930, 191-1150, and 1000041), Chile. LITERATURE CITED Abramsky, Z., M. L. Rosenzweig, B. Pinshow, J. S. Brown, B. P. Kotler, and W. A. Mitchell. 1990. Habitat selection: an experimental field test with two gerbil species. Ecology 71:2358–2369. Bissonette, J. A. 1997. Wildlife and landscape ecology: effects of pattern and scale. Springer-Verlag, New York, New York, USA. Bowers, M. A. 1988. Seed removal experiments on desert rodents: field evidence for resource partitioning. Journal of Mammalogy 69:201–204. Bowers, M. A., and B. Breland. 1996. Foraging of gray squirrels on an urban–rural gradient: use of the GUD to assess anthropogenic impact. Ecological Applications 6:1135– 1142. Bowers, M. A., J. L. Jefferson, and M. G. Kuebler. 1993. Variation in giving-up densities of foraging chipmunks (Tamias striatus) and squirrels (Sciurus carolinensis). Oikos 66:229–236. Bowers, M. A., D. B. Thompson, and J. H. Brown. 1987. The spatial organization of a desert rodent community: food addition and species removal. Oecologia 72:77–82. 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. 1989. Desert rodent community structure: a test of four mechanisms of coexistence. Ecological Monographs 59:1–20. Brown, J. S., B. P. Kotler, and W. A. Mitchell. 1994. Foraging theory, patch use, and the structure of a Negev Desert granivore community. Ecology 75:2286–2300. Brown, J. S., A. Morgan, B. D. Dow. 1992. Patch use under

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