EFFECTS OF BIOTIC INTERACTIONS ON SPATIAL BEHAVIOR OF SMALL MAMMALS IN A SEMIARID COMMUNITY IN NORTH-CENTRAL CHILE EFECTOS DE LAS INTERACCIONES BIÓTICAS SOBRE EL COMPORTAMIENTO ESPACIAL DE PEQUEÑOS MAMÍFEROS EN UNA COMUNIDAD SEMIÁRIDA EN EL NORTE-CENTRAL DE CHILE John A. Yunger, Peter L. Meserve, and Julio R. Gutiérrez ABSTRACT We examined live-trap data of 4 small mammal species for evidence of behavioral responses to predator and/or competitor exclusions in a semiarid thorn scrub community in north-central Chile. The species included an herbivorous hystricognath rodent, Octodon degus, a granivorous/herbivorous sigmodontine rodent, Phyllotis darwini, and 2 omnivorous/insectivorous sigmodontines, Abrothrix olivaceus and Abrothrix longipilis. Significant numerical effects of predation on O. degus were present during the study; although none were detected on P. darwini, previous analyses showed significant but small magnitude effects of predation. Both species had significant effects of predation on survival. We examined effects of biotic interactions on mean distance between successive captures (MDBSC) for consecutive 6-month seasons during a 36- month period during and following an El Niño (ENSO) event in 1991-1994. Time and density were included with predation and competition in 4-way analyses of variance for each species. There was a significant inverse relationship between density and MDBSC for P. darwini; this relationship was most pronounced in predator exclusions. There also were inverse relationships between density and MDBSC for O. degus and A. olivaceus, but only female O. degus showed any response to predator exclusion. The mechanisms supporting these movement-density relationships may include sociality for O. degus, predation risk for P. darwini, and intraspecific agonistic encounters for A. olivaceus. A. longipilis evidently operates at a different spatio-temporal scale than the other 3 species, and its movements evidently were not affected by density or predator exclusion. Key words: Abrothrix longipilis, Abrothrix olivaceus, Chaparral, Density Dependence, El Niño, Movement, Octodon degus, Phyllotis darwini, Predator Exclusion, Rodents RESUMEN Examinamos los datos de trampeo vivo de 4 especies de micromamíferos buscando evidencia de respuestas conductuales a exclusión de depredadores y/o competidores en una comunidad arbustiva espinosa semiárida del norte-centro de Chile. Las especies incluyeron un roedor histricognato herbívoro, el degu (Octodon degus), un roedor sigmodontino granívoro/herbívoro, la laucha orejuda de Darwin (Phyllotis darwini), y dos sigmodontinos omnívoros/insectívoros, la laucha oliva de pastizal (Abrothrix
Transcript
EffEcts of Biotic intEractions on spatial BEhavior of small mammals in a sEmiarid community in north-cEntral chilE
EfEctos dE las intEraccionEs Bióticas soBrE El comportamiEnto Espacial dE pEquEños mamífEros En una
comunidad sEmiárida En El nortE-cEntral dE chilE
John A. Yunger, Peter L. Meserve, and Julio R. Gutiérrez
ABSTRACT
We examined live-trap data of 4 small mammal species for evidence of behavioral responses to predator and/or competitor exclusions in a semiarid thorn scrub community in north-central Chile. The species included an herbivorous hystricognath rodent, Octodon degus, a granivorous/herbivorous sigmodontine rodent, Phyllotis darwini, and 2 omnivorous/insectivorous sigmodontines, Abrothrix olivaceus and Abrothrix longipilis. Significant numerical effects of predation on O. degus were present during the study; although none were detected on P. darwini, previous analyses showed significant but small magnitude effects of predation. Both species had significant effects of predation on survival. We examined effects of biotic interactions on mean distance between successive captures (MDBSC) for consecutive 6-month seasons during a 36-month period during and following an El Niño (ENSO) event in 1991-1994. Time and density were included with predation and competition in 4-way analyses of variance for each species. There was a significant inverse relationship between density and MDBSC for P. darwini; this relationship was most pronounced in predator exclusions. There also were inverse relationships between density and MDBSC for O. degus and A. olivaceus, but only female O. degus showed any response to predator exclusion. The mechanisms supporting these movement-density relationships may include sociality for O. degus, predation risk for P. darwini, and intraspecific agonistic encounters for A. olivaceus. A. longipilis evidently operates at a different spatio-temporal scale than the other 3 species, and its movements evidently were not affected by density or predator exclusion.
Key words: Abrothrix longipilis, Abrothrix olivaceus, Chaparral, Density Dependence, El Niño, Movement, Octodon degus, Phyllotis darwini, Predator Exclusion, Rodents
RESUMEN
Examinamos los datos de trampeo vivo de 4 especies de micromamíferos buscando evidencia de respuestas conductuales a exclusión de depredadores y/o competidores en una comunidad arbustiva espinosa semiárida del norte-centro de Chile. Las especies incluyeron un roedor histricognato herbívoro, el degu (Octodon degus), un roedor sigmodontino granívoro/herbívoro, la laucha orejuda de Darwin (Phyllotis darwini), y dos sigmodontinos omnívoros/insectívoros, la laucha oliva de pastizal (Abrothrix
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olivaceus), y la laucha de pelo largo de pastizal (Abrothrix longipilis). Efectos numéricos de depredación sobre O. degus estuvieron presente durante el estudio; aunque ninguno fue detectado sobre P. darwini, análisis previos mostraron efectos significativos de depredación pero de magnitud pequeña. Ambas especies tuvieron efectos significativos de depredación sobre la sobrevivencia. Se examinaron los efectos de interacciones bióticas en la distancia promedio entre capturas sucesivas (MDBSC) para estaciones sucesivas de 6 meses durante un período de 36 meses y después de un evento El Niño (ENSO) en 1991-1994. El tiempo y la densidad se incluyeron con depredación y competencia en un análisis de varianza de 4 vías para cada especie. Hubo una relación inversa significativa entre densidad y MDBSC para P. darwini; esta relación fue más pronunciada en la exclusión de depredadores. Hubo también una relación inversa entre densidad y MDBSC para O. degus y A. olivaceus, pero sólo las hembras de O. degus mostraron alguna respuesta a la exclusión de depredadores. Los mecanismos que sustentan esta relación de densidad-movimiento pueden incluir sociabilidad para O. degus, riesgo de depredación para P. darwini, y encuentros agonísticos intraespecíficos para A. olivaceus. A. longipilis opera evidentemente a una escala espacio-temporal diferente a las otras 3 especies, y sus movimientos evidentemente no fueron afectados por la densidad o exclusión de depredadores.
Palabras claves: Abrothrix longipilis, Abrothrix olivaceus, Matorral, Dependencia de la Densidad, El Niño, Exclusión de Depredadores, Movimiento, Octodon degus, Phyllotis darwini, Roedores
INTRODUCTION
In addition to affecting small mammal numbers and survival, predation can have important behavioral effects (e.g., Kotler, 1984a, 1984b, 1984c; Brown, 1988, 1989, 1992; Brown et al., 1988, 1992; Desy et al., 1990; Lima and Dill, 1990; Kotler et al., 1992; Lima, 1992; Lagos et al., 1995a; Yunger et al., 2002; Yunger, 2004). Perceived predation risk may decrease the area used by prey and the distances moved. Conversely, within a patchy environment, prey using specific microhabitats that provide concentrated resources and/or refuges from predators may increase mobility and areas used with increasing predator risk. In the first case, there is assumed to be a direct relationship between the probability of being detected (and subsequently consumed) by a predator, and prey mobility and foraging behavior. In the second, the advantages of exploiting a patchy resource for food and/or refuge outweigh potential disadvantages of greater movement and/or exposure. When studying such behavior in the field, investigators typically assume that prey can rapidly assess risk vs. energetic gains through proximal cues such as vegetation density, proportion of open habitat, and the relative richness of potential foraging microhabitats.
These foraging strategies are not mutually exclusive. Environmental conditions can play an important role in altering prey responses to their habitat and the presence of predators. This environmental variation can result in 2 broad manifestations that influence foraging; (1) changes in resource availability and (2) fluctuations in population density. Early models of resource availability predicted an inverse relationship between movement and the abundance of food (Cody, 1974; Schoener, 1983), but Ebersole (1980) pointed out that there can be selective pressure not only
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to obtain necessary energy but also to maximize energy intake. The energy obtained beyond the requirements for basic body maintenance, growth, and reproduction can be directed to reduced intervals between reproductive bouts, increased litter/clutch size, increased growth rates leading to earlier reproductive maturity, and/or large body size favoring the probability of obtaining a mate(s). There are limitations, however, to the area an individual can exploit for procuring resources. As the area used increases, so too does the probability of intra- and interspecific agonistic encounters, and, if the area is a defended territory, the probability of intrusion.
Although most studies have reported an inverse relationship between population density and measures of spatial variation, this pattern is far from universal. The presence or absence of this inverse relationship appears to be independent of the spatial measure used (e.g., home range area, maximum distance across area used, movement between captures). The preponderance of this work is Holarctic and focuses on Microtus spp. There have been at least 8 studies on the relationship between density and spatial patterns in Microtus; 5 reported an inverse relationship between home range or movement and density (Getz, 1961; Van Vleck, 1969; Krebs, 1970; Abramsky and Tracy, 1980; Ostfeld and Canham, 1995) while 3 did not (Batzli, 1968; Arai and Shiraishi, 1982; Gaines and Johnson, 1982). The inverse relationship between spatial measures and density has also been found for Peromyscus leucopus in prairie habitat (Yunger, 2004) and 3 species of heteromyid rodents in a southwestern U.S. desert (Maza et al., 1973), while no relationship was found for Tamias in oak woodlands (Mares et al., 1980). Gaines and Johnson (1982) concluded that the lack of a constant inverse relationship may be due to differences in gender and age. Seasonal fluctuations in environmental variables and changes in density among interspecific competitors can also alter spatial-density patterns (Yunger, 2004) or potentially mask intraspecific spatial-density relationships. These patterns need to be tested in other biogeographic regions and with other lineages of mammals.
Several studies have examined behavioral responses of small mammals to varying conditions simulating increased predation risk under semi-natural settings. These have involved introduction of predators into enclosures (e.g., Brown et al., 1988; Kotler et al., 1988), altering light levels as a surrogate for increased actual or perceived predation risk (e.g., Kotler, 1984a, 1984b, 1984c; Vásquez, 1996), and manipulating food levels and distribution to assess relative foraging intensity in different “risk” environments (e.g., Brown, 1988, 1989; Lima and Valone, 1985; Kotler et al., 1992). However, few studies have examined small mammal behavioral responses in natural situations where predators have been excluded. Exceptions include Desy et al. (1990) and Yunger (2004) who analyzed behavioral responses of voles (Microtus ochrogaster) and mice (Peromyscus) to predator-exclusions, Lagos et al. (1995a, 1995b) who measured changes in microhabitat use by a large caviomorph rodent, Octodon degus, in vertebrate predator-exclusions, and Yunger et al. (2002) and Kelt et al. (2004) who utilized foraging experiments and “giving up densities” (GUD’s; the level at which small mammals cease to remove a particular resource; sensu Brown, 1988, 1989) as indicators of the influence of predators and/or competitors. All of these studies found some effect of predators on home range, movements, or foraging sites of small mammal prey. This included changes in density of 1 species, which reduced movements of a second species (Yunger, 2004), individuals traveling in more direct routes through open sites in the absences of predators (Lagos, 1995a), reduced predator suppression on movements (Desy at al., 1990), and shifts in microhabitat foraging site (Yunger et al., 2002; Kelt et
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al., 2004). However, there was extensive heterogeneity among these results. Within a given study there were differential responses among species to predator exclusion, with some species exhibiting no effect. One study that included a seasonal component found responses varied over time (Kelt et al., 2004).
A current challenge in mammalian ecology is integration of behavioral responses, territorial defense, movements, and foraging behavior with multiple constraints, such as intra- and interspecific competition, temporal fluctuations in resource availability, and predation risk. In this study we use movement to assess how predation risk, intraspecific variation in density, and interspecific competition act individually and interact collectively on small mammal behavior. This investigation was part of a long-term study of mammalian ecology in north-central Chile (Meserve et al., 1995, 1996, 2003; Yunger et al., 2002; Kelt et al., 2004). The study has provided information on temporal changes in individual small mammal movements at both a long temporal and large spatial scale while experimentally excluding the dominant small mammal competitor and excluding mammalian and avian predators. This semi-arid coastal region of Chile is strongly influenced by El Niño Southern Oscillation (ENSO) events. ENSO events trigger dramatic increases in small mammal densities (Meserve et al., 1995, 1996, 1999, 2003), affording the opportunity to examine the previous experimental manipulations under population fluctuations reaching 1 order of magnitude. This lead to 4 predictions: (1) there would be an inverse relationship between movement and population density of small mammals; (2) prey movements would increase in the absence of predators; (3) smaller, competitively subordinate species would reduce movements in response to increased densities of a large, competitively dominate species; and (4) peak densities resulting from ENSO events would mask any predator or competitor effects.
MATERIALS AND METHODS
Descriptions of the study area were given previously (Meserve et al., 1995, 1996, 1999, 2003). It is located in a relatively homogeneous thorn scrub community (“Quebrada de las Vacas”, 240 m elev.) in Parque Nacional Bosque Fray Jorge (71°40’W, 30°38’S) in the IV Region [Coquimbo] ca. 85 km S La Serena and 350 km N Santiago, Chile near the coast (Fig. 1). The flora of the lower elevation scrub zone includes spiny drought-deciduous and evergreen shrubs and understory herbs on a predominantly sandy substrate, and is termed the Porlieria chilensis-Proustia pungens-Adesmia bedwelli association (Muñoz and Pisano, 1947; Muñoz, 1985; Hoffmann, 1989; Gutiérrez et al., 1993). The area has been protected from grazing and disturbance since 1941. The climate is semiarid Mediterranean with 90% of the mean 110 mm annual precipitation falling in winter months (May-October); summer months are warm and dry. During 1989-1990 and 1993-1994, rainfall was average to below average (range = 32-89 mm); an ENSO event in 1991-1992 resulted in high rainfall (233 mm, and 229 mm respectively).
Small mammals found in the thorn scrub assemblage include year-around resident “core” species such Octodon degus (Octodontidae), and Phyllotis darwini (Cricetidae: Sigmodontinae) and a “quasi-core” species (Abrothrix olivaceus; Cricetidae: Sigmodontinae) which, although usually resident, undergoes large demographic fluctuations in the thorn scrub. “Opportunistic” species such as Abrothrix longipilis (Cricetidae: Sigmodontinae) disappear for varying lengths of time during dry years
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(Meserve et al., 1999; Milstead, 2000). O. degus is strongly herbivorous, P. darwini is granivorous/herbivorous, and A. olivaceus and A. longipilis are omnivorous and insectivorous, respectively (Meserve, 1981a). Other species such as Oligoryzomys longicaudatus (Cricetidae: Sigmodontinae), Thylamys elegans (Didelphidae), and Abrocoma bennetti (Abrocomidae) are sporadic and/or maintain generally low numbers in the thorn scrub (Meserve and Le Boulengé, 1987; Meserve et al., 1995). Predator numbers are particularly high within park boundaries and include the owls Tyto alba, Bubo magellanicus, Speotyto cunicularia, and Glaucidium nanum [sporadic]), and the culpeo fox (Pseudalopex culpaeus; Fulk, 1976a; Jaksic et al., 1997; Meserve et al., 1987).
A series of 16 - 75 m x 75 m (0.56 ha) grids have been live-trapped since March 1989 for 4 nights per month with 2 large Sherman-type traps/station (5 x 5 stations, 15 m interval). Animals are marked with ear tags or leg bands, and data taken on tag number, species, sex, weight, reproductive condition, and capture location during handling. Data are analyzed with the CMR (capture-mark-recapture) programs of Le Boulengé (1985; see also Meserve and Le Boulengé, 1987; Meserve et al., 1995). Monthly
Figure 1. Map of the IV Region (Coquimbo) in north-central Chile showing the location of Parque Nacional Bosque Fray Jorge.
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trappabilities (the mean percentage of the known population that was captured each month).for the first 5 species listed above (except O. degus) has exceeded 90% (that for degus averaged 65.3 ± 1.6 (SEM)%). We use minimum number known alive (MNKA) estimates per grid for analyses of population trends.
The experiment is a 2 x 2 factorial design with treatments being competition (presence/absence of degu) and predation (presence/ absence; see Meserve et al., 1993a, 1993b, 1995, 1996) and 4 grids randomly assigned to each treatment. For convenience, we term these treatments +D+P (degu and predators present), +D-P (degu present, predators absent), -D+P (degu absent, predators present), and -D-P (degu and predators absent; see Fig. 2).
Differences in density among treatments and temporal changes in density were analyzed with repeated measures analysis of variance (rmANOVA; SAS, 1990) yielding a 2 x 2 within-subjects factorial design. Months were the repeated measures and random
Figure 2. Location of treatments and grids in Quebrada de las Vacas, Parque Nacional Bosque Fray Jorge; symbols and codes as in text. Heavy and lighter shaded lines running among grids indicate locations of access roads and trails among grids, respectively.
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variables. Fixed effects were our biotic treatments (degu present/absent and predator present/absent), and density was the independent variable. Inference was based on Type III sum-of-squares. Exclusions began after the May 1989 census; during the pre-test period (March-May), there were no significant differences observed between treatments with respect to densities of Octodon degus (rmANOVAs F = 0.23, d.f. = 1,6, p = 0.65) or other principal species (all F ≤ 2.36, d.f. = 1,12, all p ≥ 0.15; Meserve et al., 1996). We examined pooled spatial results from live-trapping on the grids for successive 6-month time blocks corresponding to principal dry and wet seasons (November-April, and May-October, respectively) from late 1991 through late 1994 (N = 36 months). This period was chosen as it spanned a time of high small mammal captures during and following the 1991-1992 El Niño, thereby facilitating 6 consecutive seasons for comparisons. Mean distance between successive captures (MDBSC, in m, obtained from Program CMR; Le Boulengé, 1985) was used as a measure of movement. As a 6-month season yielded a maximum of ca. 18 (nocturnal) to 24 (diurnal) opportunities for capture, MDBSC was calculated using 10-24 captures per individual.
Treatment effects (competition and predation) were analyzed for each of the first 4 species listed. To avoid pseudoreplication (Hurlbert, 1984), we used mean values per grid because grids are our replicate. Effects of treatment on spatial measures were tested with analysis of covariance (ANCOVA; SAS PROC GLM, SAS, 1990); density and time were included as covariates yielding a 4-way ANCOVA (Table 1). Residuals were inspected for departures from normality using box-plots and normal probability plots (Tukey, 1977). All statistical inferences were based on Type III sum-of-squares with α = 0.05.
RESULTS
During the first 32 months of the study (through October 1991) we recorded 8773 captures of 2120 individuals of 8 species. Thereafter, during the focal period of this study (November 1991 through October 1994, N = 36 mo.), we documented 103,637 additional captures of 13,294 individuals of 9 species. Captures of the 4 species considered here (i.e., O. degus, P. darwini, A. olivaceus, A. longipilis) comprised 94.4% of all small mammals captured during the focal period.
Numbers of Octodon degus were significantly higher in predator-exclusion grids (Fig. 3; rmANOVA’s, F = 7.53, d.f. = 1, 6, p = 0.034). However, trends converged in early 1994 suggesting that predation effects were less pervasive when small mammal (and predator) numbers were declining. Predation effects on Phyllotis darwini density were not significant (Fig. 3; F = 0.19, d.f. = 1, 12, p = 0.670) although there was a strong trend towards a time x predation interaction (F = 1.80, d.f. = 1, 35, p = 0.058); competition effects (of O. degus) also were not significant (F = 0.04, d.f. = 1, 12, p = 0.854). No significant main treatment effects of competition or predation were found on numbers of Abrothrix olivaceus (Fig. 3; predation: F = 1.00, d.f. = 1, 12, p = 0.337; competition: F = 0.79, d.f. = 1,12, p = 0.392). However, a trend towards a time x competition interaction (F = 1.94, d.f. = 1, 35, p = 0.065) suggested that degu effects changed over time. Similar to A. olivaceus, Abrothrix longipilis exhibited no significant treatment effects (Fig. 3; predation: F = 1.95, d.f. = 1, 12, p = 0.188; competition: F = 1.65, d.f. = 1, 12, p = 0.223). A significant time x predator interaction (F = 1.98, d.f. = 1, 35, p = 0.043), and a trend towards a time x competitor interaction (F = 1.67, d.f. = 1, 35, p = 0.097) suggest differing
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effects of interactions over time. These trends generally are similar to those of longer-term analyses (Meserve et al., 1996, 1999, 2003); perhaps the most notable difference was a significant predation effect and significant time x predator interactions for P. darwini during longer-time periods (i.e., June 1989 through mid-1996; Meserve et al., 1999). There also were strong trends towards statistically significant time x competitor interactions (Meserve et al., 1996, 1999). For A. olivaceus and A. longipilis, we detected strong trends to statistically significant interactions between time x competition and time x predation (Meserve et al., 1996, 1999).
For O. degus MDBSC changed significantly over time and with density (Table 2). These significant density, time, and density x time interactions were the result of an inverse relationship between MDBSC and density (Fig. 4). Predators interacted with both time and density to influence the movements of female O. degus (Table 2). When predators were excluded, there was little change in MDBSC; when predators were present and densities increased, MDBSC declined (Fig 4). This effect occurred at the end of the time series when densities were low.
Phyllotis darwini males showed a significant effect of predation on their MDBSC
Table 1. Covariate model used for the analysis of small mammal mean distance be-tween successive captures (MDBSC). The predator and competitor exclusions were treated as categorical variables, whereas time and density were continuous covari-ates.
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Figure 3. Population trends for Octodon degus, Phyllotis darwini, Abrothrix olivaceus, and Abrothrix longipilis from November 1991 through October 1994. Symbols denote treatments (see text for explanation).
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with higher values in predator-exclusion plots (Table 2; Fig. 5). For all 3 groups MDBSC changed inversely with density over time; this difference was most pronounced in predator exclusion treatments (Table 2). Thus, P. darwini movements were greater under conditions of low density when predators were absent. The exclusion of O.
Octodon degus Phyllotis darwini Male Female Total Male Female Total
Table 2.— Summary of 4-way analysis of covariance (ANCOVA) of treatment effects (predation, competition) with density and time included as covariates. Presented are the F and p-values (in parentheses) associated with each response variable and interaction; degrees of freedom can be found in Table 1. For Abrothrix longipilis all values of p > 0.10.
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degus had no effect on P. darwini movements (Table 2). For A. olivaceus there were no significant effects of predation or competition on
MDBSC. In all cases MDBSC changed significantly over time (Table 2; Fig. 6). There was a significant effect of density on MDBSC for males (Table 2) but not for females
Abrothrix olivaceusMale Female Total
Predator 0.01 (0.978)
0.03 (0.858)
0.01 (0.929)
Competitor 0.18 (0.668)
0.44 (0.511)
1.33 (0.253)
Time 20.16 (0.001)
10.48 (0.002)
18.08 (0.001)
Density 4.11 (0.046)
0.83 (0.372)
1.92 (0.169)
Predator*Competitor 0.22 (0.639)
0.74 (0.393)
0.37 (0.544)
Time*Predator 0.02 (0.881)
0.01 (0.932)
0.16 (0.689)
Density*Predator 0.01 (0.916)
0.02 (0.891)
0.04 (0.835)
Time*Competitor 0.33 (0.569)
0.96 (0.329)
2.35 (0.129)
Density*Competitor 0.12 (0.731)
0.26 (0.610)
1.17 (0.283)
Time*Density 14.52 (0.001)
4.73 (0.032)
11.34 (0.001)
Time*Predator*Competitor 0.35 (0.555)
0.89 (0.349)
0.48 (0.492)
Density*Predator*Competitor 0.38 (0.550)
0.59 (0.445)
0.28 (0.598)
Time*Density*Competitor 0.27 (0.602)
0.45 (0.503)
1.94 (0.168)
Time*Density*Predator 0.01 (0.917)
0.03 (0.857)
0.07 (0.794)
Time*Density*Predator*Competitor 0.38 (0.541)
0.50 (0.480)
0.18 (0.671)
Table 2 (continued).
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(Table 2). However, all 3 A. olivaceus time x density interactions were significant (Table 2); this was a result of MDBSC increasing over time while density decreased (Fig. 6).
For A. longipilis, there no significant effects of predation or competition on MDBSC (all F ≤ 0.65, d.f. = 1, 79, p ≥ 0.42; Fig. 7). Additionally, there were no significant effects of either time or density on any spatial measure (all F ≤ 0.65, d.f. = 1, 79, p ≥ 0.42; Fig. 7).
MDBSC estimates for O. degus were ca. 16-32% of linear grid measurements (e.g., widths/lengths, both = 75 m). P. darwini had MDBSC estimates that were ca. 16-43% of linear grid measurements. A. olivaceus had mean seasonal MDBSC of 15-37% of grid widths/length which tended to increase over time and with declining density. A. longipilis had the highest mean seasonal MDBSC estimates of the 4 species ranging from 21 to 37% of the linear grid widths/lengths; there was little change in these measures over time or with density.
Figure 4. Minimum distance between successive captures (± 1SE, MDBSC) for Octodon degus females, males, and all individuals for 6-month periods between November 1991 and October 1994.
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DISCUSSION
There were no effects of competitor exclusion on movements among the 3 species that are smaller than the diurnal O. degus. This was not surprising for P. darwini, which is nocturnal; these 2 species rarely come into direct contact. Although Yunger et al. (2002) found no effect of O. degus exclusion on P. darwini foraging, Kelt et al. (2004) recorded significant increases in foraging by P. darwini in the absence of degus. This difference may be attributed to temporal scale of these studies; the latter had a
Figure 5. Minimum distance between successive captures (± 1SE, MDBSC) for Phyllotis darwini females, males, and all individuals for 6-month periods between November 1991 and October 1994.
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longer duration and potentially greater sensitivity to variation in foraging. Additional work is required to determine the spatio-temporal scale of competition between these 2 species. Based on their natural history, this investigation, and the 2 studies cited above, it appears that interference competition and the direct influence on movements does not occur, but that scramble competition or resource depletion may be occurring. Although there have been no notable numerical effects of O. degus exclusion on A. olivaceus (Meserve et al., 1996), previous work on foraging behavior has shown that the former species can reduce the giving up densities (GUD) of the latter (Kelt et al.,
Figure 6. Minimum distance between successive captures (± 1SE, MDBSC) for Abrothrix olivaceus females, males, and all individuals for 6-month periods between November 1991 and October 1994.
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2004; Yunger et al., 2002). As with P. darwini, future work on behavioral interactions between these 2 species needs to resolve the spatio-temporal scale at which significant behavioral interactions occur: is this only when the 2 species come in direct contact over a potential food source, or is A. olivaceus moving in such a way as to avoid O. degus but not necessarily alter its average distance moved? The opportunistic A. longipilis functions at a spatial scale different than O. degus. There are periods during which A. longipilis is not captured at the study site for several months; during ENSO periods it
Figure 7. Minimum distance between successive captures (± 1SE, MDBSC) for Abrothrix longipilis females, males, and all individuals for 6-month periods between November 1991 and October 1994.
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is regularly captured at the site, reflecting this species’ long-term sporadic occurrence (Meserve et al., 2003). A. longipilis movements at both short and long temporal scales and movements between grids are significantly greater than O. degus (Yunger et al., 2002). Thus, it appears these differences in spatial scale result in no direct effect of O. degus on A. longipilis movements.
Among the 4 small mammal species in this study, there was extensive temporal variation in movements associated with predator exclusion and changes in densities. Responses to predator exclusion ranged from strong, pervasive effects on both male and female P. darwini, to interactions of predation with time and density affecting female O. degus movement, to no detectable effects of predators on A. olivaceus or A. longipilis. Both male and female O. degus MDBSC showed a significant inverse relationship with density over time. The same was true for P. darwini, although the response was more pronounced on predator exclusion plots. Movements of both male and female A. olivaceus changed significantly over time in a density-dependent manner. Similar to the predator exclusion response, A. longipilis movements did not change significantly over time, irrespective of density. These graded responses are readily explained by life history characteristics of these species.
O. degus tend to be distributed in areas of high bare ground cover associated with patches of shrubs under which their burrows are located (Meserve, 1981b). Within these areas, MDBSC declined as density increased following the ENSO. Degus are highly social and colonial, and concentrate activity around clusters of burrows and related groups of individuals (Fulk, 1976b; Meserve et al., 1984; Vásquez, 1998). Affinity for other members of the social group or the burrow system itself may prevent degus from making extensive movements away from the family site. As densities increase and space becomes limited, individuals likely reduce overall movements due to aggressive encounters with members of adjacent family groups. A caveat is that food resources remain adequate within this limited area as densities increase. The change in herbaceous plant cover from near zero to 90% following ENSOs (Meserve et al. 2003) suggests this may be the case. Future work should examine changes in O. degus spatial patterns following the factorial manipulation of food and density.
Under low densities, female degus had significantly lower MDBSC on predator exclusion plots than predator access plots. Lagos et al. (1995a) found that degus in predator access plots (i.e., +P+D) used open areas less (assessed with smoked tracking plates), had increased daily activity ranges (assessed with fluorescent tracking), and made shorter, more direct movements between shrub patches. Similarly, Yunger et al. (2002) found greater foraging and a trend towards use of open microhabitats by degus in predator exclusion grids (as determined by GUD’s). Whereas daily activity ranges and foraging experiments could reflect more subtle patterns of spatial usage than detected by live-trapping, Lagos et al. (1995a) also pooled data over nearly a year; therefore, we expected more similarity between their results and those presented here, which were based on mark-recapture. There also are important energetic and thermoregulatory considerations. Degus limit activity to areas beneath shrubs in summer months regardless of treatment (Lagos et al., 1995b); use of continuous periods would have obscured seasonal differences. Therefore, special attention must be paid to temporal and spatial scales of measurement, and the extent to which individual spatial measures reflect population- vs. individual-level responses to experimental manipulations of biotic interactions.
In the absence of predators, both female and male P. darwini showed a strong
Yunger et al. - Behavior of Small Mammals in Semiarid Chile 17
inverse relationship between movement and density. In view of this significant but small magnitude numerical response to predation, and effects of predation on survival rates (Meserve et al., 1995, 1999), changes in spatial behavior may reflect consequences of increased predation risk. For example, snowshoe hares alter their habitat use due to predation risk, foraging in areas of reduced food availability (Krebs et al., 1995). The increased MDBSC suggested increased spatial usage in the absence of predation. A similar response was reported for prairie voles (Microtus ochrogaster) in predator-exclusion plots (Desy et al., 1990). Foraging experiments conducted in summer 1991 showed that P. darwini foraged more intensively in predator-exclusion grids (Yunger et al., 2002); Kelt et al. (2004) reported a similar trend in 1999-2001. This species performed more evasive maneuvers to an avian predator model under conditions of a full (vs. new) moon, and that they have significantly higher GUD’s (i.e., lower foraging intensity) under artificial full moon light levels (Vásquez, 1994). Yunger et al. (2002) and Kelt et al. (2004) reported a similar effect of moonlight, but only the former reported an effect of cover on P. darwini foraging intensity. Increased foraging under shrubs and during a new moon have been inferred as responses to predation risk for gerbils in both the Negev (Kotler, 1984b, Kotler et al., 1991) and Namib Deserts (Hughes et al., 1994), and for heteromyid rodents in the Sonoran Desert (Price et al., 1984). Aviary experiments with owls and Gerbillus spp. (Kotler et al., 1991) and field experiments with lanterns and Dipodomys spp. (Kotler, 1984c) have confirmed that light levels influence foraging sites and movements between patches. P. darwini evidently shares with these other species a variety of behavioral responses to perceived predation risk.
Exclusion of predators had no effect on movement by A. olivaceus, and earlier work demonstrated a lack of numerical effects of predation on them (Meserve et al., 1996, 1999). A. olivaceus are only occasional prey items for diurnal raptors and foxes (Fulk, 1976a; Meserve et al., 1987; Jaksic et al., 1997). There was a clear and pronounced inverse relationship between movements and density. The inverse correlation between density and MDBSC for A. olivaceus may be attributed to a reduction in intraspecific agonistic encounters as reported for Microtus ochrogaster (Abramsky and Tracy, 1980).
Changes in density and predator exclusion had no effect on movements by A. longipilis. There have also been no numerical effects of predator or competitor exclusion on this species. As with competition, the absence of any response may be attributed to differences in spatial scales. It has also been suggested that A. longipilis may travel long distances and “skim” sporadically distributed numerous patches of abundant food (Yunger et al., 2002). Similar results have been found for gerbils in the Negev Desert (Brown et al., 1994) and Ammospermophilus harrisii in the Sonoran Desert (Brown, 1989). Associated with the high MDBSC are large long-distance movements for A. longipilis at this field site (Yunger et al., 2002). This species also has large home range area in southern temperate rainforests (Rau et al., 1981; Meserve et al., 1991). This lends further support to its characterization as an opportunistic species that persists in more mesic areas such as river bottoms and fog forest habitats during droughts and invades upland thorn scrub after El Niño events (Meserve et al., 1999; Milstead, 2000). Further, its insectivorous diet would predict a larger spatial scale of habitat usage (McNab, 1963; Kelt and Van Vuren, 2001).
Although results for relationships between population density and home range/movement-density relationships are conflicting (Batzli, 1968; Contreras, 1972; Mares et al., 1980; Arai and Shiraishi, 1982), this study lends support to the general trend of an inverse relationship among a diversity of small mammals (Getz, 1961; Van Vleck,
University of California Publications in Zoology18
1969; Krebs, 1970; Maza et al., 1973; Gaines and Johnson, 1982). Three of the 4 species investigated at Fray Jorge conform to this relationship. However, the mechanisms underlying this relationship do not appear to be consistent among the 3 species, and range from sociality for O. degus, to intraspecific agonistic encounters for A. olivaceus, and predation risk for P. darwini.
ACKNOWLEDGEMENTS
We thank the following people who have helped in various aspects of the fieldwork: M. Gooding, A. Levicán, V. Salvatori, G. Vaglio, V. Valverde, and H. Vásquez. Also, we appreciate the assistance of various Earthwatch volunteers in 1993. We are grateful to the Corporación Nacional Forestal, Coquimbo (IV) Region, and in particular to W. Canto, for permitting us to carry out this project in Parque Nacional Bosque Fray Jorge. We also appreciate the cooperation of park personnel there. Support for this project came from the Graduate School, Northern Illinois University, the U.S. National Science Foundation (BSR-8806639, DEB-9020047, and DEB-0319966), and the Fondo Nacional de Investigación Científica y Tecnológica (FONDECYT 90-0930 and 1000041), Chile. Two anonymous reviews helped to improve this paper.
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