Small-Mammal Foraging Behavior: Mechanisms for Coexistence and Implication for Population Dynamics

Ecological Monographs, 72(4), 2002, pp. 561–577 ᭧ 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 2Departamento de Biologia, Universidad de La Serena, Casilla 599, La Serena, Chile

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 ϫ 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 fa- vorable 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 lating biotic interactions, it may be possible to elucidate mechanisms of community composition and dynamics. General background Brown (1989) studied foraging behavior and coex- To understand how species coexist within a com- istence of four rodent species in the Sonoran Desert. munity and the temporal dynamics of a system, it is Seasonal rotation in foraging efficiency was the mech- necessary to integrate across ecological levels and anism permitting coexistence among three of the spe- scales (Bissonette 1997). For example, individuals for- cies (Brown 1989). Spatial variation in resource abun- age to procure energy for growth, maintenance, and dance was presumed to be responsible for coexistence reproduction. However, interference from competitors, of a fourth species in the small-mammal assemblage. risk of predation, and physiological constraints all can Selection of open vs. bush microhabitat and temporal influence the resource level at which an individual will variation in resource abundance appeared to be of rel- abandon, or choose not to forage in, a patch. By in- atively little importance. In the Israeli Negev Desert, corporating environmental heterogeneity, while simul- live-trapping at large spatial scales (macrohabitat) taneously measuring foraging behavior and manipu- showed that two species of gerbils occurred most fre- quently in semi-stabilized dune habitats, although un- Manuscript received 9 February 2001; revised 16 January der high densities, secondary habitat preferences di- 2002; accepted 28 January 2002. verged between stabilized and unstabilized dunes (Ro- 3 Present address: Environmental Biology Program, Gov- ernors State University, University Park, Illinois 60466 USA. senzweig and Abramsky 1986, Abramsky et al. 1990). E-mail: [email protected] Both gerbils foraged more under low levels of lunar 561 562 JOHN A. YUNGER ET AL. Ecological Monographs Vol. 72, No. 4 light intensity (Kotler 1984a) and beneath shrubs as degus, 140.9 Ϯ 20.9 g, X¯ Ϯ 1 SE), which is diurnal opposed to open areas (microhabitat; Kotler et al. (Meserve and Le Boulenge´ 1987, Wilson and Reeder 1991). Such foraging behaviors are putative modes of 1993). All three species feed largely or exclusively on reducing predation risk. In the Namib Desert, Hughes plant material, including seeds. Seed utilization of the et al. (1994) studied the foraging behavior of the noc- three species in decreasing order is Phyllotis, Akodon, turnal dune hairy-footed gerbil (Gerbillurus tytonis)in and Octodon (Meserve 1981a, b). three microhabitats: open, grass, and brush. This gerbil foraged the most in brush, followed by grass and then Hypotheses open areas. The authors attributed the pattern to re- Predation risk.—Analysis of vertebrate predator di- duced predation risk in brush and grass microhabitats. ets showed that Octodon were consumed more than In all three microhabitats, G. tytonis foraged more un- would be predicted based on total prey availability, der a new moon than a full moon. Effects of a putative followed by Phyllotis, with Akodon representing a com- competitor were unclear, given no patterns in micro- paratively low proportion of the predator diets (Jaksic habitat shifts as a result of the removal. et al. 1993, 1997). From these results, two alternative Because predators were never directly manipulated, predation risk hypotheses can be suggested. First, Oc- these studies provide limited insight into the influence todon should show a clear pattern of foraging more of predation. Although Hughes et al. (1994:1397) pur- under shrubs, followed by Phyllotis, with Akodon ex- ported to ‘‘provide direct experimental evidence on the hibiting the least microhabitat preference. Alternative- role of predation risk...,’’lunar light levels were used ly, Akodon may be under moderate or high predation as a surrogate. This approach has commonly been em- intensity, but are least observed in predator diets be- ployed when investigating small-mammal foraging cause they are good at avoiding depredation, e.g., by (e.g., Lockard and Owings 1974, Kotler 1984b, c, Price staying under shrubs. At the same time, the high dep- et al. 1984, Bowers 1988). Although it provides useful redation rate of Octodon could be the result of indi- information, alternative explanations, such as ther- viduals spending a proportionately greater amount of moregulatory constraints (Goodfriend et al. 1991, La- time in the open. Two lines of evidence support the gos et al. 1995a) or intraspecific competition, may at former hypothesis. First, preliminary field observations least partially explain the foraging regimes observed suggest that Akodon spent more time in the open than under different lunar light levels (Reichman and Price did Octodon. Because the vast majority of the predator 1993). Under low levels of lunar light intensity, ver- assemblage includes species that have been observed tebrate predators may still be present and may forage to feed more in the open than in or under shrubs, Ako- successfully (Dice 1945). In addition, lunar light in- don may not be under high predation intensity. Second, tensity is irrelevant for diurnal prey species. Octodon has exhibited a significant numerical response In this study, predator and competitor exclosures to predator exclusion, whereas Akodon has not (Mes- were used to test four spatial and three temporal hy- erve et al. 1999). potheses on small-mammal coexistence. These hy- Acceptance of the first alternative hypothesis leads potheses, which are not mutually exclusive, were tested to three predictions. First, Octodon GUD should be using natural variation in cover and light intensity. In significantly lower under shrubs than in the open, the context of these manipulations and variation, the whereas there should be no significant difference in foraging patterns of small mammals were examined Akodon GUD between the two microhabitats. Second, using giving-up densities (GUD), the level at which an Octodon should show significantly lower GUD in the individual ceases to use a particular resource (Brown absence of predators than in their presence, followed 1988, Kotler et al. 1991, Brown et al. 1992); similar by Phyllotis and then Akodon. Third, Octodon should methods have been used elsewhere (e.g., Bowers et al. show the greatest shift toward foraging in the open as 1993, Bowers and Breland 1996). Most often the re- a result of predator exclusion, followed by Phyllotis, source is some type of food mixed with a matrix ma- with little or no significant response by Akodon. terial (e.g., sand), resulting in a diminishing rate of Physiological constraints.—Diurnal species in warm return as the food is consumed. Two or more predic- deserts must avoid hyperthermia while foraging in open tions pertaining to foraging supported by marginally areas exposed to direct sun and in contact with sand significant treatment effects would suggest that indi- that can be heated to relatively high temperatures. In viduals are ‘‘balancing’’ multiple constraints. Finally, turn, lower GUD under shrubs could be incorrectly as part of a long-term study, it was possible to relate interpreted as foraging to reduce predation risk. For a the GUD work to population and community dynamics. species that preferentially forages under shrubs, no We present results on the foraging behavior of three change in microhabitat selection when predators are small-mammal species in semiarid north-central Chile: removed may indicate microhabitat selection resulting the olivaceous field mouse (Akodon olivaceus, 32.3 Ϯ from thermoregulatory constraints. 5.3 g, X¯ Ϯ 1 SE), which is continuously active, Darwin’s Competition.—Large body size implies competitive leaf-eared mouse (Phyllotis darwini, 58.2 Ϯ 13.7 g, X¯ superiority in many taxa, including small mammals Ϯ 1 SE), which is nocturnal, and the degu rat (Octodon (Bowers et al. 1987). Thus, in our system, Akodon November 2002 SMALL-MAMMAL FORAGING BEHAVIOR 563 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 Oc- todon. 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 Reich- man 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. Fol- lowing 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 Ako- don is that decreased Phyllotis foraging during a full moon would result in competitive release and increased FIG. 1. Map of the IV Region (Coquimbo) in north-central Akodon foraging. Chile showing the location of Parque Nacional Fray Jorge. 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 con- from ESNOs may permit coexistence within the sys- tribute to the coexistence of small-mammal species. A tem. We hypothesized that a species showing a rapid species that shows a rapid numerical response to the numerical response as a result of the ENSO could sub- initial seed pulse would be a relatively inefficient for- sequently depress resource levels. A second species, ager (high GUD overall); rapid growth and reproduc- showing a more delayed numerical response, should be tion would be supported by feeding on rich patches of a more efficient forager, further depressing resource food. Because this would reduce the initial pulse of availability. This should, in turn, be followed by a cor- food, a species showing a more protracted response responding decrease in the numbers of the first species. should be a relatively efficient forager (low GUD over- That is, a trade-off exists between reproductive poten- all), having to obtain food from already foraged patch- tial and foraging efficiency. es. METHODS ENSO.—El Ninõ–Southern Oscillations (ENSO), which generally last about one year, occur every four Field site years on average (range: 2–10 yr; Cane 1983). In many The study area is located in Parque Nacional Bosque areas of coastal Chile, ENSO events result in increased Fray Jorge (71Њ40Ј W, 3 0 Њ38Ј S; IV Region) ϳ100 km levels of precipitation followed by increased seed pro- south of La Serena and 350 km north of Santiago, Chile duction (Gutie´rrez et al. 1997). Rapid increases in near the coast (Fig. 1). This 10 000-ha park contains small-mammal density of one to two orders of mag- semiarid thorn scrub vegetation and isolated fog forests nitude have been recorded following the seed pulse on coastal mountain ridges, which have been protected (Pearson 1975, Fuentes and Campusano 1985, Meserve from grazing and disturbance since 1941. The study et al. 1995). The high densities can be maintained site is located in a valley (‘‘Quebrada de las Vacas’’) throughout the ENSO year, followed by declines of one at an elevation of 240 m. Shrub coverage at the site, to two orders of magnitude that may occur over several dominated by Porlieria chilensis, Proustia pungens, years (Jimeńez et al. 1992). Thus, the magnitude and and Adesmia bedwellii, averages ϳ50% (Gutie´rrez et temporal patterns of population dynamics resulting al. 1997). The climate is semiarid, with mild (ϳ21ЊC) 564 JOHN A. YUNGER ET AL. Ecological Monographs Vol. 72, No. 4 winter months (May–October) and warm (ϳ25ЊC) dry uary–February 1993); and (3) a means of relating for- summers. In 1991 and 1992, there was an ENSO event aging results to the longer time scale of population resulting in heavy rainfall. Rainfall was normal in 1989 dynamics. (89 mm), and 1990 was a dry year (32 mm), but in The investigation used a 2 ϫ 2 factorial design, with 1991 and 1992, rainfall increased to 233 and 229 mm, the factors being predation and competition by the larg- respectively. Rainfall was close to average in 1993 (77 est small mammal (Octodon). The four treatments were mm), whereas 1994 was relatively dry (35 mm). located in a homogenous habitat and were assigned In addition to the three principal year-round members using a stratified random design, evenly divided among of the small-mammal assemblage already noted, four 16 plots: ϩD ϩP (access to degus and predators), ϩD species are rare or sporadic in occurrence (Meserve et ϪP (predator exclusion), ϪD ϩP (degu exclusion), and al. 1995). The co-occurrence of Thylamys elegans ϪD ϪP (degu and predator exclusion; Meserve et al. (mouse opossum) with the other small-mammal species 1995). Terrestrial predators were excluded with 1.8 m may be attributed to its insectivorous diet (Meserve high fencing (with a 1-m overhang) buried 40 cm deep. 1981a, b). The occurrence of Oligoryzomys longicau- Avian predators were excluded by suspending poly- datus (long-tailed rice rat) is highly sporadic. When ethylene netting (15 cm diameter mesh) over the grids. coupled with its reproductive biology, the population Predator-accessible plots had similar fencing only 1 m dynamics and spatial distribution of O. longicaudatus high. All species other than degus could freely pass suggest that this species is nomadic (Meserve et al. through the 2.5-cm mesh fencing; ϳ5.0 cm diameter 1996, 1999). Consequently, T. elegans and O. longi- holes allowed degu entry on degu-accessible plots. caudatus were not considered further in this study. Foraging experiments.—Within each plot (experi- Abrothrix longipilis (long-haired field mouse), which mental unit), four foraging stations were established in is insectivorous/herbivorous, and Abrocoma bennetti January 1993. Two hardware cloth cages were placed (Bennett’s chinchilla rat), which is primarily herbivo- at each station, one under shrubs (cover) and one ϳ2– rous, are also present at the site, but will only briefly 3 m away from the cover of the nearest shrub (open). be considered because of their rarity. The cages were divided into two compartments. One In addition to the previously noted small mammals, side of the cage had relatively small holes (1.5 ϫ 1.5 there are several numerically common vertebrate pred- cm) through which only Akodon could pass. The op- ators, including owls (Speotyto cunicularia, Tyto alba, posing side had large holes (5.0 ϫ 5.0 cm) through Bubo virginianus) and the culpeo fox (Pseudalopex cul- which individuals of the three common species (Ako- paeus). Most are important small-mammal predators don, Phyllotis, and Octodon) could pass. Hole size was (Fulk 1976, Jaksic et al. 1992, 1993, 1997, Meserve et determined by trials in which individuals were placed al. 1987). Concentrations of these predators within park in hardware cloth cages with holes of different dimen- boundaries are particularly high because the park has sions. The holes were too small and close to the ground one of the only significant areas of undisturbed semi- for birds to enter (J. Yunger and P. Meserve, personal arid scrub community in north-central Chile. Two spe- observation). During the foraging experiments, a can cies of snakes occur at the site (Tachymenis chilensis containing 250 g of sifted sand from the site, mixed and Philodryas chamissonis), although neither is con- with 10 g of oat (Avena) seeds, was placed in each sidered an important small-mammal predator (Jaksic compartment of the cage. This resulted in seed densities 1998). similar to those occurring naturally (Gutie´rrez et al. 1997), although the oats were somewhat larger than Experimental design natural seeds. The cages prevented birds from feeding Following initial surveys in late 1988, 16 75 ϫ 75 on the seeds and partitioned foraging among small- m (0.56-ha) plots were established in the valley during mammal species. Differentiation based on tracks was January–March 1989 (see Meserve et al. 1996), and unreliable because of the coarse sand. Ants were rel- monthly small-mammal trapping was initiated. Since atively rare at the site and were not considered im- March 1989, live-trap small-mammal censuses have portant seed predators. been conducted for four nights per month on each of Foraging Experiment 1 (predation).—The first ex- the 16 plots (5 ϫ 5 array, 15-m interval, 25 stations, periment, conducted during a new moon, was designed two traps per station). Animals were marked with ear to test the effects of predators on both nocturnal and tags or leg bands, and data were taken on tag number, diurnal small mammals, using the predator exclusion species, sex, body mass, reproductive condition, and (ϩD ϪP) and predator access plots (ϩD ϩP). Cans capture location. Data were analyzed with the Capture– containing sand and preweighed seeds were placed in Mark–Recapture programs of Le Boulenge´ (1985). the cages at dawn. Contents were collected and re- Minimum number known alive (MNKA) estimates per placed at dusk and then again the following dawn. This plot were used for analyses of population trends (Seber protocol was repeated for a second consecutive 24-h 1982). These monthly censuses provided data on: (1) period to determine the repeatability of the results. The small-mammal movements; (2) small-mammal density two 24-h periods were treated as blocks. By collecting and species composition during foraging studies (Jan- the seeds at dusk and dawn, it was possible to examine November 2002 SMALL-MAMMAL FORAGING BEHAVIOR 565

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 Ϯ 1 SE) Main effect Akodon Phyllotis df tP No predator 6.706 Ϯ 0.492 2.386 Ϯ 0.098 47 8.462 Ͻ0.0001 With predator 3.862 Ϯ 0.325 2.792 Ϯ 0.135 47 3.331 0.0011 Open 5.014 Ϯ 0.459 2.266 Ϯ 0.122 47 4.786 Ͻ0.0001 Cover 5.455 Ϯ 0.452 2.712 Ϯ 0.158 47 6.816 Ͻ0.0001

differences between nocturnal and diurnal foraging by Octodon exclusion plots (t ϭ 1.87, df ϭ 126, P ϭ 0.12), Akodon, using the Akodon-only side of the cage. The providing additional support that the GUDs of the two side with the large holes was used to determine the larger species were not masked by that of Akodon. nocturnal foraging by Phyllotis and diurnal foraging Demographics and movements.—We analyzed the by Octodon. Because Akodon had access to both sides population data on two temporal scales, short and long of the cage, the GUD of the two larger species could term. The short-term scale (January–March 1993) in- potentially be obscured if Akodon had a lower GUD. cluded censuses conducted prior to, between, and fol- However, a comparison of the GUD of the two sides lowing the foraging experiments, and was analyzed to of the cage for all main effects (including those of determine if predator or competitor exclusions had a Experiments 2 and 3) showed that the means were con- numerical effect on any of the three principal species sistently and highly significantly lower on the all-spe- during the foraging study. The long-term scale included cies access side (Tables 1 and 2). This indicates that data collected between March 1989 and October 1994. Phyllotis and Octodon had lower rates of diminishing This range of dates provided a time series representing return than Akodon and that the all-species access side two years of non-ENSO dynamics, numerical responses of the cage can be used to measure the GUD of the during an ENSO event, and the decline following an two larger species. ENSO. Because Octodon is diurnal and Phyllotis is Foraging Experiment 2 (lunar light).—The second nocturnal, we did not conduct a foraging experiment foraging experiment tested the effects of predators and on competitive interactions between these two species. lunar light levels on the nocturnal species, using the Accordingly, unlike the studies of Meserve et al. (1995, ϩD ϩP and ϩD ϪP plots. The nocturnal data collected 1996, 1999) that provide more complete analyses of during the first night of Experiment 1 were used as the the population dynamics, the Phyllotis density analysis new moon treatment. Fourteen days later, the design reported here does not include the competitor exclusion followed in Experiment 1 was repeated with a full moon under a clear, cloudless sky. plots. Foraging Experiment 3 (competition).—The third The percentage of reproductively active individuals experiment examined the effects of interspecific com- on control plots was used to compare differences in petition on foraging behavior, using the ϩD ϩP and reproductive patterns among the three principal spe- ϪD ϩP plots. Because Octodon are strictly diurnal, the cies. Males were classified as reproductively active if experiment was conducted only during the day. Con- their testes were descended (vs. abdominal); females sequently, only data on Akodon GUD were collected. were classified as reproductively active if they were The protocol was the same as in Experiment 1: four perforate, lactating, or visibly pregnant. Only the pe- stations, two cages per station, one in the open and one riod September 1991–October 1994 was used for com- under a shrub. For consistency, the GUD from the Ako- parisons of reproductive activity, due to limited sample don-only side of the cages was used. However, there size. Within plots, capture records from the four con- was no significant difference between GUD on the Ako- trols were used to calculate the mean distance between don-only (7.72 Ϯ 0.42 g; X¯ Ϯ 1 SE) and all-species successive captures (MDBSC) for both the short- and sides of the cages (6.85 Ϯ 0.74 g; X¯ Ϯ 1 SE)onthe long-term scales. Between plots, the percentage of in-

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 Ϯ 1 SE) Main effect Akodon Octodon df tP No predator 8.793 Ϯ 0.195 3.120 Ϯ 0.306 47 15.075 Ͻ0.0001 With predator 8.019 Ϯ 0.286 3.788 Ϯ 0.318 47 10.127 Ͻ0.0001 Open 8.073 Ϯ 0.207 4.659 Ϯ 0.357 47 9.810 Ͻ0.0001 Cover 8.109 Ϯ 0.281 2.350 Ϯ 0.163 47 17.738 Ͻ0.0001 566 JOHN A. YUNGER ET AL. Ecological Monographs Vol. 72, No. 4

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 Akodon olivaceus Source of variation df Error Source of variation df Error Pred 1 Pred ϫ Block Pred 1 Pred ϫ Block Plot(Pred) 6 Error Plot (Pred) 6 Error Station(Plot ϫ Pred) 24 Error Station (Plot ϫ Pred) 24 Error Cover 1 Cover ϫ Block Cover 1 Cover ϫ Block Block 1 Pred ϫ Block ϩ Cover Time 1 Time ϫ Block ϫ Block Ϫ Pred ϫ Block 1 Pred ϫ Block ϩ Cover Cover ϫ Block ϫ Block ϩ Time ϫ Block Ϫ 2 ϫ Error Pred ϫ Cover 1 Pred ϫ Cover ϫ Block Pred ϫ Cover 1 Error Pred ϫ Block 1 Pred ϫ Cover ϫ Block Pred ϫ Time 1 Error Cover ϫ Block 1 Pred ϫ Cover ϫ Block Cover ϫ Time 1 Error Pred ϫ Cover ϫ Block 1 Error Pred ϫ Block 1 Error Error 90 Cover ϫ Block 1 Error Time ϫ Block 1 Error Pred ϫ Cover ϫ Time 1 Error Error 214 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 RANDOM (SAS Institute 1990a) option, and follows was calculated at the long time scale. Littell et al. (1991). All other models used the global error term. Statistical analysis One-way ANOVA was used to test for significant The three foraging experiments were analyzed as hi- differences between MDBSC; Rayn’s Q test was used erarchical split-plots, with plots nested within treat- for post hoc multiple comparisons (Day and Quinn ments and stations nested within plots ϫ treatments, 1989, SAS Institute 1990a). Chi-square goodness of fit using SAS PROC GLM (SAS Institute 1990a). Plots was used to test for significant differences between the were treated as the experimental unit to avoid pseu- percentages of individuals moving between plots. The doreplication (Hurlbert 1984). Tables 3 and 4 outline short-term demographic data were analyzed by MAN- all main effects (sources of variation), nested levels, OVA using SAS PROC GLM (SAS Institute 1990a). and interactions. For brevity, only significant results Time (3 mo) was used as the response variable. For from these models are presented in text. In all cases, the reproductive patterns and long-term population inference was based on Type III sum-of-squares. With trends, a univariate repeated-measures ANOVA the exception of the block term in Experiment 1, all (rmANOVA) was used (SAS PROC GLM; SAS Insti- sources of variation were treated as fixed. The block tute 1990a, Winer et al. 1991, von Ende 1993). All term was treated as random to generalize the repeat- within-subject inferences were based on Huynh-Feldt ability of the experiment, resulting in a mixed model. adjusted P values (Huynh and Feldt 1970). To help Selection of the appropriate error terms for the mixed partition within- and between-year effects, we used a models was accomplished using the SAS PROC GLM doubly-within-subjects design (Winer et al. 1991) for

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

Experiment 2 Experiment 3 Source of variation df Source of variation df Pred 1 Competitor 1 Plot (Pred) 6 Plot (Competitor) 6 Station (Plot ϫ Pred) 24 Station (Plot ϫ Competitor) 24 Moon 1 Cover 1 Cover 1 Competitor ϫ Cover 1 Pred ϫ Cover 1 Error 63 Pred ϫ Moon 1 Moon ϫ Cover 1 Pred ϫ Moon ϫ Cover 1 Error 90 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. November 2002 SMALL-MAMMAL FORAGING BEHAVIOR 567

TABLE 5. Doubly-within-subject repeated-measures ANO- VA 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 Akodon olivaceus Source of Source of variation df variation df Between subject: Between subject: Predation (Pred) 1 Predation (Pred) 1 Error 6 Competition (Comp) 1 Pred ϫ Comp 1 Error 12 Within subject: Within subject: Year 4 Year 4 Year ϫ Pred 4 Year ϫ Pred 4 Error (Year) 24 Year ϫ Comp 4 Year ϫ Pred ϫ Comp 4 Error (Year) 48 Month 5 Month 5 Month ϫ Pred 5 Month ϫ Pred 5 Error (Month) 30 Month ϫ Comp 5 Month ϫ Pred ϫ 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 Shapiro- Wilks 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. Ho- mogeneity of cell variances (precluding within-subject FIG. 2. Significant giving-up densities (GUD) of the degu, analyses) were tested using an F-max test. Octodon degus, for Experiment 1: (a) foraging on predator- excluded vs. predator-accessible plots and (b) under shrub RESULTS cover vs. in the open. Panel (c) depicts the predation ϫ cover interaction. GUD is given as grams of seeds (mean Ϯ 1 SE). Foraging Experiment 1 (predation).—For all three species, the predation foraging experiments had no significant block term and only one significant interaction more under shrubs as opposed to in the open (F ϭ involving the block term, indicating that the results are 11 978.01, P ϭ 0.005; Fig. 2b). This supports the pre- at least reasonably repeatable. The significant Akodon diction that Octodon responds behaviorally to preda- time ϫ block interaction (F ϭ 8.244, P ϭ 0.004; refer tion risk. However, the predator ϫ cover interaction to Table 3 for all Experiment 1 df values) indicated was not significant (F ϭ 4.810, P ϭ 0.272), indicating that there was increased foraging during the second that Octodon did not respond to a reduction in predation night, a possible associative learning effect. risk by foraging more in the open, although there was Octodon foraged significantly more when predators a trend toward increased foraging in the open on pred- were excluded (F ϭ 2166.52, P ϭ 0.012; Fig. 2a) and ator exclusion plots (Fig. 2c). These results support the 568 JOHN A. YUNGER ET AL. Ecological Monographs Vol. 72, No. 4

FIG. 3. Significant giving-up densities (GUD) of Darwin’s FIG. 4. Significant giving-up densities (GUD) of the ol- leaf-eared mouse, Phyllotis darwini, for Experiment 1: (a) ivaceous field mouse, Akodon olivaceus, for Experiment 1: foraging on predator-excluded vs. predator-accessible plots (a) foraging on predator-excluded vs. predator-accessible and (b) under shrub cover vs. in the open. GUD is given as plots and (b) during both the day and the night. GUD is given grams of seeds (mean Ϯ 1 SE). as grams of seeds (mean Ϯ 1 SE). physiological constraints hypothesis that thermoregu- would suggest that Phyllotis was primarily responsible latory constraints limit the time Octodon can spend for the decrease in Akodon foraging when predators foraging in the open (Lagos et al. 1995a). The only were excluded. significant treatment effect on Phyllotis foraging in Ex- Foraging Experiment 2 (lunar light).—Phyllotis for- periment 1 was predator exclusion (F ϭ 453.67, P ϭ aged more under a new moon than a full moon (F ϭ 0.009). As predicted, Phyllotis foraged more in the ab- 3.90, P ϭ 0.051; Fig. 5a), suggesting the importance sence of predators (Fig. 3a). There was a marginally of reduced predation risk (refer to Table 4 for all ex- significant trend toward lower Phyllotis GUD in the periment 2 df values). However, the predator ϫ moon open vs. under cover of shrubs (F ϭ 2166.50, P ϭ interaction was not significant, indicating that Phyllotis 0.012; Fig. 3b). did not respond behaviorally to the exclusion of pred- There was a marginally significant effect of predator ators, and that lunar light levels play only a weak role exclusion on Akodon foraging (F ϭ 129.57, P ϭ 0.052; in determining how Phyllotis perceives predation risk. Fig. 4a). The increase in Phyllotis and Octodon for- Contrary to the prediction, Phyllotis foraged more in aging on predator exclusion plots was the probable the open than under shrubs (F ϭ 21.85, P Ͻ 0.001; cause for the reduction in Akodon foraging. Akodon Fig. 5b). However, the lack of a significant predator ϫ also had a significant predator ϫ time interaction (F cover interaction indicated that Phyllotis did not re- ϭ 13.20, P Ͻ 0.001), with higher GUD during the night spond behaviorally to the predator exclusions, or that on predator exclusion plots than on controls; during predation risk is of secondary importance to alternative the day, GUDs on the predator access plots were similar foraging constraints. to, but somewhat lower than, those on predator exclu- Akodon had significantly lower GUD on predator sion plots (Fig. 4b). Because Octodon is diurnal, this access plots (F ϭ 8.30, P ϭ 0.005; Fig. 6a). As in November 2002 SMALL-MAMMAL FORAGING BEHAVIOR 569

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 Ϯ 1 SE).

Experiment 1, this may be the result of interspecific competition. There was a significant predator ϫ moon interaction (F ϭ 8.12, P ϭ 0.005) and a marginally significant moon ϫ cover interaction (F ϭ 3.60, P ϭ 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 FIG. 6. Significant giving-up densities (GUD) of Akodon foraging on predator exclusion plots. Akodon GUDs olivaceus for Experiment 2: (a) foraging on predator-excluded under shrubs were relatively similar for both the new vs. predator-accessible plots; interactions involving predation moon and full moon treatments. However, there was a (b) during a full moon vs. new moon and (c) under shrub shift toward increased foraging in the open under a cover vs. in the open. GUD is given as grams of seeds (mean Ϯ 1 SE). new moon (Fig. 6c). Although Phyllotis foraged more during a new moon, this was not followed by a cor- responding increase in Akodon foraging during a full clusion plots (F ϭ 20.29, P ϭϽ0.001; Fig. 7). This moon. Thus, the alternative lunar light cycle hypothesis provides direct experimental support for the competi- is refuted. tion hypothesis: in the absence of Octodon, the smaller Foraging Experiment 3 (competition).—Akodon oli- Akodon foraged more. There was no significant com- vaceus had significantly lower GUD on competitor ex- petitor ϫ cover interaction, suggesting that diurnal in- 570 JOHN A. YUNGER ET AL. Ecological Monographs Vol. 72, No. 4

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 Ϯ 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 ϭ 12.7, df ϭ 1, 6, P ϭ 0.021; Fig. 8a). Phyllotis densities were significantly lower on the predator exclusion plots (F ϭ 14.8, df ϭ 1, 6, P ϭ 0.007; Fig. 8b), whereas the number of Ako- don did not differ significantly between the control, competitor exclusion, and predator exclusion plots (F ϭ 2.41, df ϭ 1, 2, P ϭ 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 ϭ 12.20, P Ͻ 0.001) and dry (F ϭ 15.08, P Ͻ 0.001) season and Phyllotis (F ϭ 15.76, P Ͻ 0.001) and Akodon (F ϭ 74.45, P Ͻ 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 (ϳApril– 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 FIG. 8. Small-mammal densities (minimum number of the wet season, followed by a decline in numbers known alive, mean Ϯ 1 SE) during the foraging experiments: between seasons (Fig. 9b). Significant month effects (a) Octodon degus, (b) Phyllotis darwini, (c) Akodon oliva- for Akodon were primarily the result of increased num- ceus. Abbreviations are: ϪD, Octodon excluded; ϩD, Oc- Ϫ ϩ bers during the ENSO. There were no clear seasonal todon present; P, predators excluded; and P, predator access. patterns. Prior to the ENSO, Akodon were relatively rare (Fig. 9c; Meserve et al. 1995). The relatively syn- chronous seasonal population dynamics of Octodon ϭ 111.80, P Ͻ 0.001; Phyllotis, F ϭ 60.14, P Ͻ 0.001; and Phyllotis and the rarity of Akodon provide little or Akodon, F ϭ 81.22, P Ͻ 0.001) seasons. As a result no support for the seasonal coexistence hypothesis. of the ENSO, Akodon and Phyllotis numbers increased All three species showed highly significant numer- synchronously starting in November 1991, although the ical year effects during both the wet (Octodon, F ϭ rate of increase in Akodon quickly exceeded that of 88.17, P Ͻ 0.001; Phyllotis, F ϭ 191.58, P Ͻ 0.001; Phyllotis (Fig. 9b, c). Akodon reached a peak in January Akodon, F ϭ 365.46, P Ͻ 0.001) and dry (Octodon, F 1992, followed by a gradual 8-mo decline. They November 2002 SMALL-MAMMAL FORAGING BEHAVIOR 571

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

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 TABLE 6. Repeated-measures ANOVA of the percentage of in November 1991, Phyllotis reached a high in January reproductively active Octodon degus, Phyllotis darwini, 1992, after which numbers remained relatively constant and Akodon olivaceus during the period of high densities resulting from the ENSO, September 1991–October 1993. for the duration of the ENSO. They then declined pre- cipitously in November 1993. Octodon did not begin Source of to increase substantially in density until September variation df MS FP1992, 10 mo after the other two species (Fig. 9a), which Between subjects: reached peak densities around January–May 1993. Fol- Species 2 26 946.48 22.06 Ͻ0.001 lowing a gradual decline, Octodon densities remained Error 9 1221.29 relatively stable until May 1994, when they declined Within subject: rapidly. Time 37 4592.64 17.83 Ͻ0.001 There was a signiﬁcant difference in the percentage Time ϫ Species 74 1539.04 5.97 Ͻ0.001 of reproductively active individuals among Octodon, Error 33 257.62 Phyllotis, and Akodon (Table 6). Both within-subject 572 JOHN A. YUNGER ET AL. Ecological Monographs Vol. 72, No. 4

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 ϫ species, were significant (Table Fig. 9a). The only significant effect of predator removal 6), indicating that the percentage of reproductively ac- on Phyllotis was a month ϫ predator interaction during tive individuals fluctuated differently among the three the wet season (F ϭ 15.76, P Ͻ 0.001), the result of species. The onset of reproduction was similar between numbers on the treatment plots being greater than on Akodon and Phyllotis during the spring 1991 (Fig. 10). the controls at the start of the season and converging Consequently, it is unlikely that differences in the tim- by the end of the season (Fig. 9b). There was no sig- ing of reproduction contributed to the more rapid in- nificant overall effect of predator or competitor exclu- crease of Akodon as compared to Phyllotis. The most sion on Akodon numbers. There was a significant year notable difference in reproductive timing between the ϫ predator interaction for Akodon during the dry sea- three species was a protracted response by Octodon, son (F ϭ 7.38, P ϭ 0.006) and a significant month ϫ which may be attributed to its reproductive biology. competitor interaction in the wet season (F ϭ 2.79, P Octodontids are caviomorph rodents that have long ϭ 0.025; Fig. 9c). gestation periods compared to other rodents (Weir At the long time scale, the principal three species, 1974, Meserve et al. 1995). This resulted in a 10-mo plus Abrothrix and Abrocoma, differed significantly in lag before the percentage of reproductively active in- MDBSC (F ϭ 5.81, df ϭ 4, 15, P ϭ 0.0102). There dividuals of Octodon reached levels approaching Ako- was also a significant difference in MDBSC at the short don and Phyllotis (Fig. 10). time scale, although Abrocoma was not included be- The numerical and reproductive responses to the cause of small sample size (F ϭ 10.44, df ϭ 3, 12, P ENSO provide support for the ENSO hypothesis. Prior ϭ 0.0012). A multiple comparison showed that Abroth- to the ENSO, Akodon was generally less common than rix, at both time scales, and Abrocoma, at the long time either Phyllotis or Octodon. It was also the least effi- scale, had significantly greater MDBSC than did the cient forager (i.e., it had the highest GUD overall; Ta- three principal species (Table 7). For the three principal bles 1 and 2), and showed the most rapid increase and decrease in numbers. Its decrease preceded that of the species, Abrothrix, and Abrocoma, there was a signif- two more efficient foragers, Phyllotis and Octodon,by icant difference in the percentage of individuals mov- ␹2 ϭ 10 and 17 mo, respectively. ing between plots at the long time scale ( 24.610, ϭ ϭϽ Predator exclusion had an overall (between-subject) df 4, P 0.001). Abrothrix had significantly great- effect on Octodon numbers during the dry season (F er between-plot movement (42.8% of the individuals) ϭ 6.16, P ϭ 0.047; Fig. 9a). A significant year ϫ than did any of the other species, whereas Abrocoma predator interaction (F ϭ 6.16, P ϭ 0.047) was the had significantly fewer (1.75%); there was no signifi- result of Octodon increasing at greater rates on the cant difference among the three principal species. Al- predator exclusion plots than on the controls. A sig- though GUD data are not available for Abrothrix, its nificant month ϫ predator interaction reflected an in- significantly greater rates of both within- and between- crease in numbers on predator exclusion plots during plot movements provide inferential support for the the wet season (F ϭ 12.20, P Ͻ 0.001); during the dry within- vs. between-patch foraging efficiency hypoth- season, this trend was reversed (F ϭ 15.08, P Ͻ 0.001; esis. November 2002 SMALL-MAMMAL FORAGING BEHAVIOR 573

TABLE 7. Distances moved (mean Ϯ 1 SE) between successive captures at the short- and long-term time scales for ﬁve small-mammal species.

Time period Akodon olivaceus Octodon degus Phyllotis darwini Abrothrix longipilis Abrocoma bennetti Short term 11.78 Ϯ 0.390 13.25 Ϯ 0.346 13.32 Ϯ 0.174 22.25 Ϯ 1.18 NA

------Long term 14.82 Ϯ 0.166 14.82 Ϯ 0.336 16.57 Ϯ 0.315 22.08 Ϯ 0.515 20.40 Ϯ 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 (␣ϭ0.05).

DISCUSSION food. Overheating, however, precludes spending more Small-mammal foraging in Chile than a few minutes foraging on all but the richest patches in the open, producing relatively high GUD. This As predicted, Octodon foraged more in the absence supports the physiological hypothesis. A second pos- of predators, although the data on GUD are confounded sible physiological constraint is water loss, although it by the numerical response that occurred at the time of is unlikely that this applies to Octodon degus. Corte´s the foraging study. This leads to a circular dilemma: et al. (1994) has shown this species to have a highly does increased foraging (i.e., lower GUD as a result of developed recapture rate of water through the nares, decreased predation risk) lead to increased densities, and a relatively low overall rate of water loss. Thus, or do increased densities, due to decreased mortality for Octodon, a single-factor explanation is not ade- resulting from predator exclusion, lead to increased quate. As discussed previously, two or more predictions foraging? Three lines of evidence suggest that the in- supported by significant or marginally significant treat- creased foraging was a behavioral response to reduced ment effects would suggest that individuals are ‘‘bal- predation risk. First, Phyllotis densities were lower on ancing’’ multiple constraints. predator exclusion plots and they had lower GUD. Predators clearly influenced Phyllotis foraging. Dur- Thus, when the Phyllotis and Octodon foraging and ing Experiment 1, Phyllotis had significantly lower demography results are viewed jointly, GUD were low- GUD on the exclusion plots, and in Experiment 2, it er in areas of reduced predation risk, irrespective of foraged more during a new moon than a full moon, rodent densities. Second, predator exclusion does alter suggesting a partial role of lunar light levels in influ- Octodon behavior. Lagos et al. (1995b) showed that encing predation risk. This was as predicted; Phyllotis individuals moved in a more linear fashion on exclu- appears under moderate predation intensity. The field sion plots as compared to controls. These linear move- experiments support laboratory studies of foraging by ments were the result of individuals traversing open areas as opposed to traveling more circuitous routes Phyllotis (Va´squez 1994). When exposed to artificial beneath shrubs. Finally, Mitchell et al. (1990) provide light levels similar to that of a full moon, Phyllotis had both theoretical and empirical support that increased significantly more evasive reactions to an avian pred- competition resulting from increased densities should ator model than at light levels comparable to a new reduce foraging effort. moon. Similarly, individuals significantly increased If predation risk did result in decreased Octodon for- their GUD under artificial full-moon light levels (Va´s- aging in the open, this should have been reflected as a quez 1994). significant predator ϫ cover interaction, which was not We also predicted that to reduce predation risk, Phyl- detected (although there was a trend toward foraging lotis would forage more under shrubs: the opposite was more in the open). If Octodon responded behaviorally found. During both Experiments 1 and 2, Phyllotis had to predator exclusion, why did they not forage signif- lower GUD in the open than under shrubs. There are icantly more in the open? We believe that this was due two possible explanations. The first is competition with to thermoregulatory constraints because Octodon is Octodon. As discussed previously, seed renewal does stenothermic (Rosenmann 1977). Lagos et al. (1995a) not occur on a daily basis. If Octodon feeds under found that Octodon body temperatures can quickly rise shrubs due to physiological constraints, thereby de- to hyperthermic levels in open locations as opposed to pleting resource levels, this could force Phyllotis to under shrubs. All individuals experiencing hyperther- feed more in the open. The second explanation, which my at air temperature Ͼ30ЊC were located in open ar- is commonly applied to heteromyids (Reichman and eas, never under shrubs. Foraging experiments were Price 1993), is based on morphology. Species that are also conducted in the warmest months. Thus, in the adapted to detecting and escaping predators (i.e., hav- absence of predators, there is little or no selective pres- ing inflated auditory bulla, large outer ears, and sal- sure to avoid crossing open areas or spending short torial locomotion) may forage in areas with increased periods of time feeding on particularly rich patches of predation risk, but also with reduced competition for 574 JOHN A. YUNGER ET AL. Ecological Monographs Vol. 72, No. 4 food. Phyllotis has large eyes, large pinna (J. Yunger role in determining coexistence at our site; competition and P. Meserve, personal observation), and slightly in- appears to play the predominant role influencing Ako- flated auditory bulla (Steppan 1995), all of which aid don foraging. in detecting predators. It also has a bounding gate (as opposed to the diagonal sequence gait of Octodon and Relation to population dynamics Akodon; J. Yunger and P. Meserve, personal obser- Together, the data on population dynamics and GUD vation) and comparatively elongated feet and hind provide support for the ENSO hypothesis. Akodon, the limbs that would aid in escaping predators. Although least efficient forager, showed the strongest and most Phyllotis does not have nearly as highly specialized rapid response to the ENSO. This response can be at- morphological adaptations as Dipodomys or Microdi- tributed to differences in reproductive biology. Mean podops, its morphology does suggest that it would have litter size for the three principal species is similar (Mes- a selective advantage over Octodon or Akodon when erve and Le Boulenge´ 1987). However, Phyllotis and foraging in the open. Akodon can reach sexual maturity in ϳ2 mo, whereas Based on the monthly trap censuses, it is clear that Octodon, a caviomorph, takes ϳ10 mo (Meserve and Akodon had greater nocturnal than diurnal activity. Le Boulenge´ 1987). Also, the gestation period of Oc- What the trap data cannot elucidate are potential mech- todon (ϳ90 d; Weir 1974) is substantially longer than anisms to explain this. Three alternative hypotheses can that of Phyllotis or Akodon (Meserve and Le Boulenge´ account for the Akodon activity, based on trapping: (1) 1987). The difference between Phyllotis and Akodon is increased interspecific competition during the day; (2) less clear. Both species responded at about the same physiological constraints (e.g., temperature and water); time to the ENSO, yet Akodon continued to increase and (3) decreased predation intensity at night. Hy- rapidly, resulting in densities nearly three times greater pothesis (3) is unlikely because Akodon is not under than Phyllotis. There is evidence that immigration may high predation intensity and, when recorded in predator be partially responsible for the large, rapid increase in diets, most often occurs in pellets of nocturnal owls Akodon numbers (Meserve et al. 1999). This species (Jaksic et al. 1993, 1997). In addition, there have been began to decline at about the same time that Octodon no main effects of predator exclusion on Akodon num- reached its peak density. Presumably, the decline was bers, and Akodon had lower GUD on predator access precipitated when the two more efficient foragers de- plots during both Experiments 1 and 2. The answer to pleted abundant patches of food. Whether Akodon hypothesis two remains unclear and requires further would disappear entirely from the small-mammal as- investigation. However, because there was virtually no semblage if not for periodic ENSO events is difficult difference in diurnal Akodon GUD in the open as com- to ascertain. Current work on metapopulation structure pared to under shrubs, it is unlikely that thermoregu- may shed light on the spatiotemporal dynamics of the latory constraints are important. This also is supported species and determine the importance of refuges and by work on water dependency. Although Akodon could recolonization. forage more at night to reduce water loss, they can The limited effect of predator exclusion on Akodon survive for 3–4 wk without free water (Meserve 1978), foraging behavior is corroborated at the population lev- suggesting that it is relatively unimportant as a phys- el. The only detectable numerical effect of predator iological constraint. There is direct experimental sup- exclusion on Akodon numbers was a year ϫ predator port for the first hypothesis: in the absence of Octodon, interaction during the dry season. This provides further Akodon have significantly lower GUD. However, com- evidence that predators play only a limited role in the petition from Octodon must also be balanced with com- overall behavioral and demographic dynamics of Ako- petition from Phyllotis and potential owl predation. don. The effects of competitor exclusion on Akodon Competition between Phyllotis and Akodon was not foraging behavior can be seen at the population level tested experimentally, although a competitive effect is by the significant month ϫ competitor interactions dur- suggested by the inverse relationships between Phyl- ing both seasons. Octodon exclusion had a strong effect lotis and Akodon GUD. on Akodon foraging, which translates into significant There also is evidence that owl predation affects Ako- seasonal fluctuations in Akodon numbers. Phyllotis, don GUD, albeit in a limited way. During a full moon, which showed limited changes in foraging behavior due Akodon must ‘‘balance’’ competition with Phyllotis and to predator exclusion, had only weak numerical re- predation risk. If predation risk is reduced under low sponses to the exclusion of predators. Similarly, Oc- lunar light levels and Phyllotis foraging is greater on todon, which showed an increase in foraging as a result predator exclusion plots, then Akodon should forage of predator exclusion, had strong and pervasive nu- more on predator-accessible plots under relatively low merical responses in the absence of predators. lunar light levels. This is supported by the significant predator ϫ moon interaction. Second, during a new Comparisons with other systems moon, Akodon shift foraging toward open sites. Al- Microhabitat partitioning (i.e., open vs. covered though owl predation may have some influence on Ako- sites) has been widely implicated as a mechanism for don foraging behavior, it is unlikely to play a major coexistence among desert rodents (Kotler and Brown November 2002 SMALL-MAMMAL FORAGING BEHAVIOR 575

1988). Spatial variation appears to be one mechanism it is apparent how seven species of small mammals can responsible for the coexistence of Phyllotis and, in par- coexist in coastal north-central Chile. ticular, Akodon, with Octodon. For several deserts In conclusion, there are numerous possible mecha- around the world, predation risk has been suggested as nisms for the coexistence of desert rodents that are the selective force resulting in microhabitat partition- common throughout the world. It should also be rec- ing (Rosenzweig 1973, Thompson 1982a, b, Price ognized, though, that phylogenetic constraints, histor- 1984, Kotler and Brown 1988, Kotler et al. 1988, ical artifacts, and different selective pressures have re- Hughes et al. 1994, Va´squez 1994). Although predation sulted in some distinct differences (Kelt et al. 1996). risk may be partially responsible for the observed open This is exemplified by our Chilean site. The strong, vs. cover foraging behavior of Octodon, physiological periodic effects of ENSOs and geographic isolation on constraints are also important at our site in Chile. For the west side of the Andes (Meserve and Glanz 1978, Akodon, interspecific competition appears to be more Meserve and Kelt 1990) have resulted in a system that important than predation risk in determining micro- has evolved a set of special, unique characteristics. habitat partitioning. In addition, rodents in numerous arid regions of the ACKNOWLEDGMENTS world have evolved morphological adaptations to aid We thank the following people who have served as tech- in predator detection and avoidance (Kotler and Brown nicians on the project: Kenneth L. Cramer, Sergio Herrera, V. O. Lagos, Brian K. Lang, Bryan Milstead, Sergio S. Silva, 1988, Mares 1993). Large pinna and inflated auditory Elier Tabilo, and Miguel-Angel Torrealba. Also, we appre- bullae that aid in hearing are particularly pronounced ciate the assistance of various Earthwatch volunteers in 1993. among Dipodomys, Microdipodops, Jaculus, and Al- We are grateful to the Corporacioń Nacional Forestal, IV lactaga. Bipedal locomotion, also common among the Region, and, in particular, to Waldo Canto and Juan Cerda four previous genera, aids in predator avoidance. South for permitting the realization of this project in Parque Na- cional Fray Jorge. We also appreciate the cooperation of park America has no extant morphological equivalents to personnel there. Burt Kotler, Barry Fox, Lynda Randa, and the bipedal heteromyids and dipodids (Mares 1993). an anonymous reviewer offered valuable comments that There is evidence that Phyllotis is better adapted at helped to improve the manuscript. The Northern Illinois Uni- escaping and detecting predators than are other small versity Institutional Animal Care and Use Committee ap- proved all work. Support for this project has come from the mammals in the assemblage, which may partially ac- Graduate School, Northern Illinois University, the U.S. Na- count for their level of foraging in the open. However, tional Science Foundation (BSR-8806639 and DEB- it is unlikely that unique morphological adaptations for 9020047), and the Fondo Nacional de Investigacioń Cientifica utilizing open microhabitats play an overriding role as y Tecnolo´gica (FONDECYT 90-0930, 191-1150, and 100- a mechanism for resource partitioning at our site. 0041), Chile.

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