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OIKOS 106: 27 Á/38, 2004

Comparative dynamics of small mammal populations in treefall gaps and surrounding understorey within Amazonian rainforest
Harald Beck, Michael S. Gaines, James E. Hines and James D. Nichols

Beck, H., Gaines, M. S., Hines, J. E. and Nichols, J. D. 2004. Comparative dynamics of small mammal populations in treefall gaps and surrounding understorey within Amazonian rainforest. Á/ Oikos 106: 27 Á/38. Variation in food resource availability can have profound effects on habitat selection and dynamics of populations. Previous studies reported higher food resource availability and fruit removal in treefall gaps than in the understorey. Therefore, gaps have been considered ‘‘keystone habitat’’ for Neotropical frugivore birds. Here we test if this prediction would also hold for terrestrial small mammals. In the Amazon, we quantified food resource availability in eleven treefall gaps and paired understorey habitats and used feeding experiments to test if two common terrestrial rodents (Oryzomys megacephalus and Proechimys spp.) would perceive differences between habitats. We live-trapped small mammals in eleven gaps and understorey sites for two years, and compared abundance, fitness components (survival and per capita recruitment) and dispersal of these two rodent species across gaps and understorey and seasons (rainy and dry). Our data indicated no differences in resource availability and consumption rate between habitats. Treefall gaps may represent a sink habitat for Oryzomys where individuals had lower fitness, apparently because of habitat-specific ant predation on early life stages, than in the understorey, the source habitat. Conversely, gaps may be source habitat for Proechimys where individuals had higher fitness, than in the understorey, the sink habitat. Our results suggest the presence of source-sink dynamics in a tropical gap-understorey landscape, where two rodent species perceive habitats differently. This may be a mechanism for their coexistence in a heterogeneous and species-diverse system. H. Beck and M. S. Gaines, Dept of Biology, Univ. of Miami, P. O. Box 249118, Coral Gables, FL 33124-0421, USA Á/ HB also at Center for Tropical Conservation, Duke Univ., 3705-C Erwin Rd, Durham, NC 27705, USA ( Á/ J. E. Hines, and J. D. Nichols, USGS Patuxent Wildlife Research Center, 11510 American Holly Dr. 201, Laurel, MD 20708-4017, USA.

One of the main challenges in ecology is to understand the spatial and temporal distribution of individuals in heterogeneous landscapes (Pusenius et al. 2000, Lin and Batzli 2001, Calsson-Graner and Thrall 2002). The ´ concept of habitat selection (MacArthur and Pianka 1966) has stimulated an increasing body of theoretical and empirical research. Both habitat selection models and optimal foraging theories assume that an individual attempts to maximize its survival, reproductive success, and the net rate of energy intake (McPeek and Holt

1992, Abrams 2000, Delibes et al. 2001). Habitat selection and dispersal patterns of tropical animals are largely unknown. MacArthur et al. (1966) suggested that because of higher structural heterogeneity in tropical forests than in the temperate areas, tropical individuals should have higher habitat specificity than individuals in the temperate zone. Treefall gaps are the most frequently occurring perturbation in tropical forests and represent structurally heterogeneous patches within the undisturbed

Accepted 7 November 2003 Copyright # OIKOS 2004 ISSN 0030-1299
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understorey matrix (Denslow 1995, Molino and Sabatier 2001, Beck 2002, 2003). In general, a given forest consists of gaps or patches at different stages of a cycle that includes new treefall openings, as well as regenerating and closed-canopy phases (Hubbell et al. 1999, Molino and Sabatier 2001). An extensive body of literature has demonstrated abiotic differences between undisturbed forest and treefall gaps (Lee 1978, Chazdon and Fetcher 1984). Other differences include higher rates of seed predation (Alvarez-Buylla and Martinez-Ramos 1990), herbivory (Swaine 1996), and fruit removal (Murray 1987) in gaps than in understorey. Additionally, many plants in gaps produce more fruits than when in the understorey (Bullock 1980, Pinero et al. 1984, ˜ Sarukhan et al. 1984, Denslow et al. 1986, Clark and ´ Clark 1987, De Steven et al. 1987, Marquis 1988, Martinez-Ramos et al. 1988, Levey 1990). Although many ecological studies have been concerned with the flora of gaps, their fauna remains largely ignored. Schemske and Brokaw (1981) found that the species richness of insectivorous birds was higher in gaps than in the understorey. Similar results were reported in other studies (Hoppes 1987, Levey 1988). Levey (1988) examined the distribution and abundance of fruiting plants and birds in gaps and the understorey. He found a distinct gap community of frugivorous birds. Because of the continuously higher resource availability in gaps compared to understorey, Levey (1990) categorized gaps as keystone habitats for frugivores. Crome and Richards (1988) studied insectivorous bats and found that certain species selected gap habitats in preference to the understorey. The above studies found that volant species select gaps as foraging sites. Within tropical rainforests the area of treefall gaps depends primarily on the number of trees that were knocked down. For example, in Costa Rica, Sanford et al. (1986) found that 25% of 394 treefall gaps were larger than 200 m2. Previous studies on small mammals in treefall gaps did not provide data on gap size or age, but found species-specific responses. In Vietnam, Adler et al. (1999) trapped small mammals in different forest habitats including treefall gaps. They found one species mainly in gaps, and suggested that this species is a gap specialist. In Africa, Lwanga (1994) and Struhsaker (1998) found that several terrestrial rodent species had higher densities in gaps while others had higher densities in the understorey. They suggested that dense groundcover provided ideal habitat for many rodents. In Panama, Lambert and Adler (2000) found that Proechimys semispinosus was significantly associated with treefall gap habitats. In Cocha Cashu, Peru, several small mammal species such as the Neacomys spinosus were almost exclusively found in gaps (Beck 2002, 2003). At the same study site, Emmons (1982) radio tracked three Proechimys species and reported that individuals preferred treefall gaps to the understorey. 28

Because previous studies found higher recourse availability in gaps than in the understorey (Bullock 1980, Pinero et al. 1984, Sarukhan et al. 1984, Denslow et al. ´ ˜ 1986, Levey 1988, 1990), we predict that resource densities should drive habitat-specific population dynamics of the two most common species of small terrestrial mammals, the rice rat (Oryzomys megacephalus, Fischer 1814) and the spiny rat (Proechimys spp., Allen 1899). Because spatio-temporal variation in resource availability can lead to different carrying capacities between habitats, we first tested for differences in resource availability and consumption by both rodent species across habitats. Based on the work of Levey (1988, 1990) we predicted higher resource availability in gaps than understorey. We also predicted higher resource availability during the rainy season than during the dry season (Foster 1985a,b, Levey 1988, Janson and Emmons 1990, Lugo and Frangi 1993). We then quantified how variation in resource availability in gaps and understorey affect population dynamics by comparing abundance, fitness (survival and per capita recruitment) and dispersal patterns of both rodent species across habitats and seasons. We predicted greater abundance, survival, per capita recruitment and immigration in the habitat with greater resource availability. Similarly, we expected abundance, survival, recruitment and immigration to show a positive relationship with seasonal variation in resource availability. Finally, we discuss results in terms of ecological theory, including the source-sink model.

Material and methods
Study area and trapping regime
We conducted this study at Cocha Cashu Biological Station (CC), which is located within the 1.8 million hectare World Biosphere Park Manu in Peru, (118 54? S, 718 22? W). CC is one of the few research sites within the Neotropics, which offers a completely undisturbed ecosystem with a full complement of both top predators and their prey (Terborgh 1990). Average annual rainfall during the two-year study period was 2,424 mm, with 81% occurring during the rainy season (November to May, Fig. 1). Mean annual temperature for the same time period was 22.98C (range 98C Á/348C, Beck 2002). In September 1994, a storm created hundreds of treefall gaps within Manu, and more than 40 gaps within the 12 km2 study area of CC (Foster and Terborgh 1998). All gaps were permanently marked and are part of a long-term study on forest dynamics (Beck, unpubl.). This storm event provided a unique opportunity for research because it offered many similar sized gaps of the same age and successional status. Gaps of comparable age and size are similar in abiotic factors such as light and temperature (Chazdon and Fetcher 1984) and biotic
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Fig. 1. Monthly rainfall and mean (9/1 SE) resource density based on 138 seed traps (41.5m2) in nine gaps and understorey sites in CC, Peru. There was no difference between habitats, but both had a significant higher resource density in the rainy seasons (Jan Á/May, Sept Á/May) than in the dry seasons (Jun Á/Aug, Jun Á/Oct).

factors such as plant communities and species richness (Hubbell et al. 1999). In July 1998, we measured the area of 40 gaps following Brokaw (1982). We selected the four largest treefall gaps and randomly selected seven small gaps for permanent trapping grids. We randomly selected distance and compass direction from each gap to determine the location for a same-sized control trapping grid in the understorey (Fig. 2). The maximum and mean distance between the experimental gaps was

4.7 km, and 427 m9/104 SE, respectively. In gaps, trap lines began 1 to 5 m behind the root ball of the fallen tree where disturbance was obvious and continued towards the fallen crown until the entire gap area was covered. Trap lines and stations were spaced 10 m apart, with each station comprising one Sherman trap (10 )/12 )/38 cm), one Tomahawk trap (13 )/13 )/30 cm) at the ground, and one arboreal Tomahawk trap, attached onto the vegetation up to 3 m high. We used the trapping

Fig. 2. Spatial configuration of 4 large (/X0/981 m29/73.6 SE) and 7 small (/X0/295 m29/62.7 SE) treefall gaps and understorey trapping locations within the lowland rain forest of CC, Peru. The maximum and mean distance between the gaps was 4.7 km, and 427 m9/ 104 SE, respectively. Size classes of gaps and understorey are indicated by different ellipse sizes. The CC study area encompasses 12 km2, and is served by over 50 km of trails. An approximately 40 to 150 meter wide meander belt of the white-water Manu River borders the study area to the South and West, while continuous lowland and upland forest extends to the North and East.

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grid dimensions from each gap for its respective understorey control-trapping grid. The mean area of the small gaps was 295 m2 (n 0/79/62.71 SE), and on average we used 41 traps (range: 39 Á/54) for each individual trapping grid. Large gaps had a mean of 981 m2 (n 0/49/73.68 SE), with a mean of 73 traps (range: 60 Á/84) for each individual grid. Each primary trapping period consisted of a five-week period in which all eleven gaps and understorey systems were sampled for seven consecutive days. This sampling schedule was repeated three more times during each rainy season (January to April) and dry season (July to October) for two years. Traps were baited every morning with a mixture of rice, peanut butter and vanilla extract, and checked the following morning. We recorded the following data from captured animals: species, gender, trap location, ear tag number (if previously captured), and reproductive condition.

Thus, we limited identification of Proechimys to the genus level. For the feeding experiments, we trapped rodents in the forest near the CC field station. Individuals of both species were kept temporarily in 50)/15 )/15 cm cages with free access to water and food. During daily trials each animal was provided with an excess random sample of at least four different fruit species. On the following day, animals were removed from the cage and the fruit samples were examined. We recorded whether seeds and fruit were consumed. Utilization was defined as a sample being partially or completely consumed. For statistical comparisons of utilized resource density across habitats, size classes and seasons, we included only data from the overall resource densities (obtained from the seed traps) for those plant species that were consumed by the rodent species. Furthermore, we used the monthly mean weights of the utilized plants as covariates in models to estimate rodent capture and survivor probabilities (below).

Resource density and feeding experiments
We used seed traps to quantify seasonal differences in resource availability between gaps and undisturbed understorey. From the eleven gaps and understorey trapping grids, we randomly selected three large gaps, their understorey controls, and six additional small gapunderstorey systems for seed traps. Depending on the total area of each gap-understorey system, we set up 7 to 12 seed traps at random locations. Each plastic seed trap had a collecting area of 0.3 m2, a depth of 0.4 m and was suspended approximately 0.5 m above the ground. In the nine gaps and understorey systems, we installed a total of 138 seed traps with a total collecting area of approximately 41.5 m2. We collected seed samples at weekly intervals from January 1999 through October 2000. Samples were identified to genus or species level, then air-dried for 24 hours and weighed to the nearest 0.1 gram. We estimated the monthly mean resource availability in grams per square meter for each gap and understorey system for comparisons across habitats, size classes and seasons. Although seed traps allow the quantification of overall resource density, not every fruit species is utilized equally by every consumer species. Therefore, we performed feeding experiments throughout the two-year study period with individuals of both Oryzomys megacephalus and Proechimys spp. and fruit samples obtained from the seed traps. At least four different Proechimys species occur sympatrically in the lowland forest of Manu Park (Voss and Emmons 1996). Because these species exhibit overlapping morphological characteristics (Weksler et al. 2001), species identification requires extensive collections or invasive procedures. Neither is allowed within the Manu Park nor is desirable in an ecological study. 30

Model selection for capture and survival probabilities
Before estimating quantities of interest for each species, we tested if the trap data within each seven-day sampling period would meet the assumptions of a closed population (no additions via immigration or birth and no deletions through death or emigration) using the program CAPTURE (Rexstad and Burnham 1991). We had initially hoped to use the robust design (Pollock et al. 1990) approach to estimation, taking advantage of the flexible modelling capability to estimate abundance using closed population models (Otis et al. 1978). Because the test results indicated our data violated the closure assumptions, we employed the open population Jolly-Seber (JS) model to estimate capture probability ˆ (pi), abundance (/Ni ) and survival probabilities (fi) utilizing Program MARK version 1.8 (White 2001). We thus pooled captures within each 7-day period to develop capture histories that simply reflected whether or not an animal was caught at least once in the period. We used the capture histories for each species by habitat (i.e., combining all sample locations within each habitat by size class) and ran the most general (full timedependent) model for survival (fi) and capture probability (pi). The full model for each of the four specieshabitat combinations was thus a 2-group JS model with parameters dependent on both time (t) and plot size (g); f(g )/t) p(g )/t). Following Lebreton et al. (1992), we tested whether or not this general model fit the data by conducting goodness-of-fit-tests using the program Release version 3.0 (Burnham et al. 1987) with data from each habitat. Our data fit the general model for Oryzomys in gaps: x2 0.05(30) 0/9.634, P0/ 0.999; in the understorey: x2 0.05(21) 0/7.689, P 0/ 0.996, and for ProOIKOS 106:1 (2004)

Table 1. Comparison between the most parsimonious (AICc) and several other models to estimate survival (fi) and capture probabilities (pi) for Oryzomys megacephalus and Proechimys spp. in gap and understorey habitats. Subscripts indicate how both parameters (fi and pi) were estimated: (g) size classes were not combined, (t) monthly time dependency, (×/) time independent, (r) resource density used as a covariate. Model a) Oryzomys in gaps f(g)/r) p(g)/r) f(g) p(g)/t) f( ×/) p(×/) f(g)/t) p(g)/t) No. of parameters 8 24 2 42 DAICc 0.00 13.73 16.39 36.51 0.00 10.08 14.95 27.67 0.00 0.40 32.12 41.93 0.00 1.62 46.47 50.87

question and the model with the lowest AICc) values calculated for each model. We estimated monthly ˆ abundance (/Ni ) for a given time period (t) by dividing the count statistic, the number of animals caught during periods (ni), by the corresponding estimate (/pi ) of the ˆ ˆ capture probability (Seber 1982): Ni 0ni =pi : ˆ

Fitness parameter estimation
Because we were not able to measure fitness directly in the field, we used monthly survival probability estimated from capture-recapture models (obtained from the model selection procedure by Program MARK) and per capita recruitment as fitness surrogates. Because the complements of survival probability estimates (1 (/f) from capture-recapture models include permanent emigration (Pollock et al. 1990), these estimates are not ideal metrics reflecting fitness. We also estimated number of recruits per female. Given our intensive trapping within each habitat, we assumed that all new recruits were born within the habitat in which we caught them. We considered Oryzomys individuals with a body mass 5/28 g (maximum adult weight was 120 g), and all new Proechimys individuals with a body mass 5/160 g (maximum adult weight was 537 g) to be recent recruits. To test for differences in per capita recruitment across habitats, size classes and seasons, we compared the mean number of recruits trapped for the first time divided by the capture probability (/pi ) to estimate the abundance of recruits and ˆ divided that number by the estimated abundance of females in reproductive condition trapped during that given month. To examine whether habitats, size classes and/or seasons had an effect on the fitness of each rodent species, we tested for differences between the two monthly fitness surrogates combined into seasons.

b) Oryzomys in understorey 6 f(g)/r) p(t)/r) f(g) p(g)/t) 24 39 f(g)/t) p(g)/t) 2 f( ×/) p(×/) c) Proechimys in gaps f( ×/) p(×/) f(g)/r) p(g)/r) f(g)/t) p(t) f(g)/t) p(g)/t) 2 4 27 32

d) Proechimys in understorey 2 f( ×/) p(×/) f(t)/r) p(g)/r) 6 28 f(g)/t) p(t) f(g)/t) p(g)/t) 31

echimys in gaps: x2 0.05(13) 0/5.460, P0/ 0.963, in the understorey: x2 0.05(21) 0/7.689, P 0/ 0.996. We derived additional, parsimonious models by constraining the number of parameters and their time dependency (Table 1). For example, in the model f(×/)p( ×/), survival (f) and capture probability (p) were constant (×/) with respect to time, hence only two parameters were estimated. In the model f(g )/t) p( ×/), survival was estimated separately for each month (t) and size class (g) separately, whereas (p) was constant over time and size class. We used the AICc (Akaike’s information criterion) values to determine which model best explained the variation in the data while using the fewest parameters. AIC is an information Á/theoretical approach that treats model selection as an optimisation problem rather than as a hypothesis-testing problem (Burnham and Anderson 1998). Additional models in the set tested whether survival and capture probability varied with consumed resource density. We specified the monthly means of resource density as a covariate for the survival and capture probabilities within several models. Many individuals survived the transition periods between rainy and dry seasons (May Á/June, and November Á/December when no trapping occurred) and were captured in the following season. Thus, we used the mean resource density over these transition periods as a covariate for survivorship. We followed Anderson et al. (1994) and selected the most parsimonious models based on the DAICc (difference between AICc for the model in
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Movement into habitats
We estimated the number of monthly new immigrants (Pollock et al. 1990) into a given habitat (animals not present in the habitat at time t but immigrating onto it between t and t'/1 and still present at t'/1) by first estimating the abundance of adult individuals for month t'/1. We defined an adult as an individual of a body mass equal to or greater than the body mass of individuals reaching sexual maturity for each species. From adult abundance, we subtracted the estimated number of surviving adults and juveniles (that survived and grew up to be adults) from the previous period computed as the product of the estimated abundance in month t and estimated survival probability between t and t'/1. Within each season, we then compared the mean number of immigrants to gaps from the under31

storey, as well as the number of immigrants to the understory area.

Feeding experiments
Overall, we tested 53 individual Oryzomys in the feeding experiments using 32 identified plant species. Oryzomys consumed 83.3% fruit biomass of the identified plants obtained from gaps and 84.3% from the understorey. There was no difference in fruit consumption by Oryzomys between habitats (F1,33 0/0.001, P0/0.978) or size classes (F1,33 0/2.884, P0/0.099). However, Oryzomys consumed more fruits during the rainy season than the dry seasons (F1,33 0/10.965, P0/0.002). We tested 59 individual Proechimys and 39 identified plant species during the feeding experiments. Proechimys consumed 95.6% fruit biomass of the identified plants obtained from gaps and 96.1% from the understorey. There was no difference in fruit consumption by Proechimys between habitats (F1,33 0/0.083, P0/0.775) or size classes (F1,33 0/0.000, P0/0.986). However, Proechimys consumed more fruits during the rainy season than the dry season (F1,33 0/18.989, P B/0.0001).

Statistical analyses
We analyzed the data using two-way repeated-measures analyses of variance (rm ANOVAs: Type III sums of squares, Zar 1996). We specified the two-way rm ANOVAs with habitat (gaps and understorey) and size class (large and small) as between-subject factors and season (rainy and dry) as a within-subject factor. If a two-way rm ANOVA revealed a significant interaction, we used one-way rm ANOVAs to test for simple effects (Stevens 1996). We compared survival for Oryzomys across habitats and size classes within each season using two-way rm ANOVAs. Here season (e.g. dry season of 1999 and dry season 2000) was the within-subject factor. Because MARK indicated no difference in survival across size classes, we compared survival of Proechimys only across habitats within each season using a one-way rm ANOVA. Prior to any rm ANOVA, we tested whether the data met the assumption of normality using the Shapiro-Wilk statistic. We log10 (x'/1)-transformed resource density-, and feeding experiment data, and square-root arcsine transformed survival data. Homogeneity of variance was tested by Levene’s test. Equality of sphericity, which is used to assess the circularity of a variance-covariance matrix (Ende 2001), was estimated using Mauchly’s test. If the assumption of sphericity was violated, we used the Greenhouse-Geisser correction to adjust the degrees of freedom (Zar 1996). All analyses were performed using SPSS version 10.1.0 (SPSS 2000).

Model selection for capture and survival probabilities
For Oryzomys the low-AICc model for gap habitats included variation in survival and capture probability among months and also between large and small gaps. Therefore, both survival and capture probability varied by size class. Because the capture Á/recapture survival probability estimates include permanent emigration, our result of a lower survival in small understorey is expected because there is a higher probability of emigration of individuals from small than large understorey grids. This expectation is a simple consequence of the large perimeter to area ratio in small grids. In contrast, in the understorey, capture probability varied among month but not by size classes. Both models included linearlogistic models for both parameters as functions of the monthly mean consumed resource from each habitat as covariates (Table 1a, b). For gaps the slope (beta estimate) of the linear-logistic model was 0.119/0.06 SE, while for the understorey the slope was 1.279/0.25 SE. Both slopes are positive indicating a positive relationship between survival and mean consumed resource. For Proechimys in gaps, the low-AICc model permitted variation in survival and capture probability monthly but contained no variation across size classes. The best model for the understorey permitted monthly variation as a function of the monthly mean of consumed resource for both survival and capture probability, but the latter parameter was kept constant across size classes (Table 1c, d). The slope of the linear-logistic model for gaps was 0.099/0.08 SE, and for the understorey the slope was 1.019/0.93 SE. Again, both slopes
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Resource densities
Over the course of 22 months, we collected a total of 6,176 g (dry mass) of fruits and seeds from the seed traps installed in nine gaps. We were able to identify 39 plant species. For the understorey, we obtained a total of 8,963 g and identified 31 plant species. The 39 species from the gaps represented 55.2% of the overall seed weight, and the 31 species from the understorey represented 58.7% of the total. We attempted to test all identified plant species in feeding experiments, depending on the availability of the rodent species (below). There was no difference in resource density (F1,33 0/ 0.107, P0/0.746) between gaps (/X0/7.0 g/m29/1.20) and understorey (/X0/9.2 g/m29/1.46) or between size classes (F1,33 0/0.125, P0/0.726, Fig. 1). However, more resources were available during the rainy season (/X0/11.4 g/m29/1.46) than during the dry season (/X0/5.4 g/m29/ 1.17; F1,33 0/22.625, PB/0.0001, Fig. 1). 32

indicate a positive relationship between survival and mean consumed resource.

Abundance estimates
In large gaps, Oryzomys had a higher monthly abundance during the rainy season (/X0/19.199/6.7) than the dry season (/X0/8.679/1.9, F1,7 0/5.221, P 0/0.056, Fig. 3a). In contrast, in small gaps, there was no seasonal difference (F1,13 0/1.168, P0/0.299). In large understorey, Oryzomys had a higher abundance during the dry season (/X0/15.329/2.3) than the rainy season (/X0/ 6.059/2.3, F1,7 0/21.406, P0/0.002). Similarly, in small understorey, Oryzomys had a higher abundance during the dry season (/X0/9.629/1.6) than during the rainy season (/X0/3.599/0.6, F1,13 0/18.364, P0/0.001, Fig. 3a). During the rainy season, Oryzomys was more abundant in gaps (/X0/10.739/2.8) than in the understorey (/X0/4.499/0.6, F1,18 0/10.086, P0/0.005, Fig. 3a). During the dry season, however, there were no differences between habitats (F1,18 0/2.908, P 0/0.105) or size classes (F1,18 0/2.101, P 0/0.164, Fig. 3a).

Proechimys abundance did not differ seasonally (F1,40 0/1.369, P 0/0.249); however, it was higher in both large (/X0/9.329/1.5) and small (/X0/6.49/2.36) gaps than in the large (/X0/4.09/1.13) and small (/X0/ 1.449/0.37) understorey (F1,40 0/18.794, PB/0.0001, Fig. 3b).

Fitness parameters
During the rainy seasons, there was no difference in Oryzomys survival by habitat (F1,8 0/2.371, P0/0.162) or size class (F1,8 0/3.123, P0/0.115). However, during the dry seasons, Oryzomys had a higher survival in the understorey than in gaps (F1,8 0/166.981, PB/0.0001, Fig. 4a), and was higher in large system than small ones (F1,8 0/449.290, P B/0.0001). Proechimys had a higher survival (F1,10 0/7.055, P0/ 0.024, Fig. 4b) in gaps than in the understorey during the rainy seasons. However, there was no difference in survival during the dry seasons between habitats (F1,6 0/1.107, P 0/ 0.333).

Fig. 3. Mean (9/1 SE) seasonal abundance in large (n0/4) and small (n0/7) gaps and understorey habitats based on two years of trapping in CC, Peru. (a) Oryzomys had a significantly higher abundance during the rainy season in gaps than in understorey. There was no difference in abundance during the dry season between habitats or size classes. (b) Proechimys abundance did not differ seasonally, but was significantly higher in both large and small gaps than in the large and small understorey.
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Fig. 4. Mean (9/1 SE) seasonal survival probability in large (n0/4) and small (n0/7) gaps and understorey habitats based on two years of trapping in CC, Peru. (a) During the dry season, Oryzomys had a significant higher survival in the understorey than in gaps. (b) During the rainy season, Proechimys had a significant higher survival in gaps than in understorey.


Per capita recruitment
There was no difference in Oryzomys per capita recruitment between seasons (F1,20 0/0.052, P0/0.823), or size classes (F1,20 0/1.100, P 0/0.307). However, Oryzomys had a higher seasonal per capita recruitment (F1,20 0/ 6.993, P 0/0.016, Fig. 5a) in the understorey (/X0/ 3.179/0.48) than in gaps (/X0/1.679/0.48). For Proechimys there was no difference in per capita recruitment between seasons (F1,19 0/0.007, P0/0.936), or size classes (F1,19 0/0.074, P 0/0.789). However, Proechimys had a higher seasonal recruitment rate (F1,19 0/12.932, P0/0.002, Fig. 5b) in gaps (/X0/7.89/ 0.59) than in the understorey (/X0/3.89/0.51).

There was no difference in the number of Oryzomys immigrants by season (F1,41 0/0.071, P 0/0.791) or by size class (F1,41 0/3.475, P 0/0.069). But more individuals immigrated into gaps than into the understorey (F1,41 0/8.884, P0/0.005, Fig. 6a). Because of low sample size for Proechimys, we pooled the data across seasons and size class and tested for differences between habitats using a Mann Á/Whitney Utest. More individuals immigrated into the understorey than into the gaps (U0/91.00, P0/0.003, Fig. 6b).

Resource density Movement into habitats
We never encountered an individual that was captured in the same habitat type at different locations. Therefore, the distance between individual gaps or understorey plots was large enough for the plots to be considered independent sampling units. The higher resource availability in the understorey during the rainy season than during the dry season was consistent with previous studies (Foster 1985a,b, Levey 1988, Janson and Emmons 1990, Lugo and Frangi 1993). However, the similarity in resource availability between the two habitats is inconsistent with previous

Fig. 5. Mean (9/1 SE) per capita recruitment in large (n 0/4) and small (n0/7) gaps and understorey habitats based on two years of trapping in CC, Peru. (a) Oryzomys had a significant higher seasonal per capita recruitment in the understorey than in gaps. There was no difference between size class and season. (b) Proechimys had a significant higher per capita recruitment in gaps than in the understorey. There was no difference between size class and season.

Fig. 6. Mean (9/1 SE) number of immigrants in large (n0/4) and small (n0/7) gaps and understorey habitats based on two years of trapping in CC, Peru. (a) Significantly more Oryzomys immigrated into gaps than into the understorey, but there was no difference between size class and season. (b) Because of low sample size for Proechimys data were pooled across seasons and size classes. Significantly more individuals immigrated into the understorey than into gap habitats.
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studies (Pinero et al. 1984, Sarukhan et al. 1984, ´ ˜ Denslow et al. 1986, Levey 1988, 1990). The salient question is whether different methodological approaches used among studies to measure resource availability led to different conclusions. Blake et al. (1990) evaluated different methods of quantifying resource availability. They pointed out several potential biases when using seed traps. For example, fruits might not fall to the ground and therefore, are not available for terrestrial animals. However, they can be harvested by arboreal frugivores. If the objective is to quantify resource availability for terrestrial animals, as in this study, however, then seed traps are an appropriate and effective method. This assumes that traps are regularly checked and maintained to minimize biases (e.g. due to decay processes). Most studies have quantified fruit phenology using either direct counts of fruits on plants or area-based sample approaches. For example, Levey (1988, 1990) assessed resource availability monthly along transects by recording all fruiting plants and their fruit abundance. He found that fruiting plants were more abundant in gaps and carried more fruits over a longer time period than conspecifics in the understorey. Additionally, Levey (1990) found a lower seasonal variance in fruit production in gaps than in the understorey. The higher resource availability in the canopy of gaps led to a higher abundance of frugivorous birds and consequently higher fruit removal rates than in the understorey (AlvarezBuylla and Martinez-Ramos 1990). The continuously higher resource availability in gaps compared to understorey led Levey (1990) to categorize gaps as keystone habitats for frugivores. We are aware of only two other studies that employed seed traps to quantify resource availability simultaneously in treefall gaps and understorey. Augspurger and Franson (1988) quantified the number of seeds dispersing into 43 treefall gaps and understorey during an 11-week period in the dry season in Panama. They found that more wind-dispersed seeds arrived in gaps than in the understorey, whereas a higher number of non-wind-dispersed seeds arrived in the understorey than in gaps. For total seeds, however, there was no significant difference between habitats. Loiselle et al. (1996) established seed traps directly at ground level in five treefall gaps and understorey locations in Costa Rica. They concluded that there was no difference in resource availability between gaps and understorey. The results of these two studies agree with our findings on resource availability. Although it is possible that gaps are ‘‘keystone habitat’’ for arboreal frugivores as suggested by Levey (1990), our data suggest that this is not the case for terrestrial species including terrestrial arthropods and mammals (Beck 2002). Food resources (Foster 1985b, Terborgh 1986, Milton 1990) and/or cover as refuge from predation (Peles and
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Barrett 1996, Struhsaker 1998, Batzli et al. 1999, Beck 2002) are two major limiting factors for mammals. Numerous studies suggest that many frugivorous and herbivorous mammals are controlled in a bottom-up fashion by seasonal shortages in food resources (Foster 1985b, Janson and Emmons 1990, Milton 1990). Furthermore, Terborgh (1986) suggested that food shortages during the dry season cause frugivorous mammals in Cocha Cashu to turn to alternative food resources that include insects and leaves. Despite our data indicating low resource availability in both habitats during the dry seasons, one cannot necessarily conclude that animals experience famine. For example, Janos et al. (1995) quantified the consumption of vesiculararbuscular mycorrhizal fungi by measuring spores in faecal samples of Oryzomys and Proechimys at Cocha Cashu. They found that faecal samples from Proechimys contained a significantly higher number of Glomus spores during the dry season than during the rainy season. Based on our findings of comparable resource availability in gaps and understorey and similar consumption rate of both rodent species, we conclude that resource availability is not driving habitat-specific population dynamics. We specified the monthly means of resource density as covariates for modelling survival. As indicated by the positive slopes of the linear-logistic models, survival was a function of resource availability. Despite the widespread belief that animal population dynamics are closely tied to resource abundance, evidence of a relationship between resources and survival is relatively rare and represents an important result of this study.

Population dynamics
A question is whether non-volant mammal species could maintain a local population within gaps. How small in area can a habitat patch be to encompass all ecological requirements needed to maintain a local terrestrial population? In Panama, Lambert and Adler (2000) found that Proechimy s preferred gap habitats to the understorey. In CC, Emmons (1982) radio tracked three Proechimys species and reported that individuals preferred treefall gaps to the understorey. Their daily home range ranged from 0.023 to 0.174 ha. Taking together, these studies demonstrate that local populations can persist and reproduce within habitat patches or home ranges that are smaller than the gaps used in this study (overall X0/545 m2, 9/95 SE, range 173 Á/1143 m2). Within a heterogeneous landscape where individuals are distributed among patches of different qualities, alternative models have been proposed to describe population dynamics and dispersal. For example, based on different assumptions, authors have suggested 35

a variety of source-sink models (Shmida and Ellner 1984, Holt 1985, Pulliam 1988, Pulliam and Danielson 1991). Per capita reproductive recruitment exceeds mortality for population in source habitats, with densitydependent dispersal. In the absence of movement, populations in sink habitats experience an average growth rate of less than one. Sink populations are only able to persist because of continuous net immigration from a source population. Oryzomys in the understorey had higher survival and per capita recruitment than in gaps. Furthermore, more individuals immigrated from the understorey into gap than into understorey habitat. Given the absence of resource differences between gaps and understorey, one reason why Oryzomys apparently had fewer recruits in gaps than in the understorey could be the frequent ant attacks in gaps. In both habitats, ants attacked trapped individuals. Free-ranging individuals undoubtedly are able to avoid potential attacks. However, Oryzomys produce altricial young; their eyes open after a week (Eisenberg and Redford 1999). These immobile newborns are vulnerable to ant attacks (Janzen and Wilson 1983). If we assume that ant attacks on trapped individuals reflect ant foraging activity in each habitat, we can test if predation pressure by ants differs between habitats by comparing the frequency of individuals attacked in traps. We found that two species of ants (Camponotus sericeiventris and C. femoratus ) attacked more individuals in gaps (n0/20) than in the understorey (n 0/4, x2 (1) 0/9.481, P0/ 0.01). Similarly, Adams et 0.05 al. (2001), Murphy (2001) and Rosenheim (2001) found that predation on early life stages of several taxa led to a significant decline in reproduction and population density and resulted in source-sink dynamics. Habitatspecific predation may reduce the fitness of Oryzomys in gaps. Therefore, gaps may represent sink habitats for Oryzomys, and their populations may be maintained by immigration from the understorey source habitat. Proechimys in gaps had higher survival and per capita recruitment than in the understorey. A lower predation rate, possibly because of greater structural heterogeneity in gaps (Beck 2002, 2003), could be one mechanism explaining why survival may be higher in gaps than in understorey. Peles and Barrett (1996) also reported that greater structural heterogeneity led to decrease in predation rates. Unlike Oryzomys, Proechimys has precocial newborn; therefore, ant attacks should not affect their survival. Ants attacked only one trapped individual in a gap. Abundance in gaps was higher than in the understorey throughout the year. These results are consistent with those of Emmons (1982), who radio-tracked several Proechimys spp. in Cocha Cashu and reported that they primarily utilized gap habitats. Similarly, in Panama, Lambert and Adler (2000) reported that Proechimy s preferred gaps and areas with high densities of logs and lianas within the forest. Treefall gaps have higher 36

structural heterogeneity (i.e. more ground cover, more vines and lianas) than the understorey (Beck 2002, 2003). For Proechimys gaps may represent source habitats where individuals have higher fitness compared to individuals in the understorey. In conclusion, our seed trap data clearly demonstrated that treefall gaps did not receive greater resource input than the understorey, and both habitats exhibited seasonal variation in resource availability. Therefore, gaps are not superior habitats for terrestrial frugivore taxa compared to the understorey with respect to fruit and seed resource availability or consumption rate. However, species-specific predation pressure by ants may lead to unequal fitness across habitats. Gaps may represent a sink habitat for Oryzomys populations, whereas the understorey may be a source habitat. Conversely, gaps may represent a source habitat for Proechimys, whereas, the understorey may be a sink habitat. Our findings of potential reciprocal source Á/sink dynamics for two rodent species may shed light on the community structure of mammals and provide a possible mechanism for local co-existence within a species diverse Amazonian rainforest.
Acknowledgements Á/ We thanks the Peruvian Ministry of Agriculture, Directorate of Forestry and Fauna, for permission to work in the Manu National Park. For their help in identifying innumerable seeds and fruits we thank J. Terborgh, P. Nunez, M. Foster, R. King, and F. Bossuyt. D. ´ Davidson identified the ant species. M. Rosenzweig provided stimulating discussions. For assistance in the field we thank D. O’Dell, A. Helm, A. Hudson, A. Sorenson, G. Wells, P. Alvarez and N. v. Vliet. Financial support to HB was provided by a NSF Dissertation Improvement Grant (DEB-9901993), Sigma Xi Grant-in-Aid, Tropical Fellowship through the University of Miami, Biology Department, and GAFAC grants from the University of Miami. For review of the manuscript we thank D. DeAngelis, T. Fleming, L. Hansson, C. Horvitz, D. Janos and D. Wilson.

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