OIKOS 106: 27
/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.
/ Oikos 106: 27
/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
/ HB also at Center for Tropical Conservation, Duke
Univ., 3705-C Erwin Rd, Durham, NC 27705, USA (harald@duke.edu).
/ 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-Granér 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 structu-
rally heterogeneous patches within the undisturbed

Accepted 7 November 2003

Copyright # OIKOS 2004
ISSN 0030-1299

OIKOS 106:1 (2004) 27

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 regenerat-
ing 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, Piñero et al. 1984,
Sarukhán 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) exam-
ined 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 under-
storey. 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 asso-
ciated 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 avail-
ability in gaps than in the understorey (Bullock 1980,
Piñero et al. 1984, Sarukhán et al. 1984, Denslow et al.
1986, Levey 1988, 1990), we predict that resource
densities should drive habitat-specific population dy-
namics of the two most common species of small
terrestrial mammals, the rice rat (Oryzomys megacepha-
lus, Fischer 1814) and the spiny rat (Proechimys spp.,
Allen 1899). Because spatio-temporal variation in re-
source availability can lead to different carrying capa-
cities 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 Em-
mons 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 immigra-
tion 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
/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
OIKOS 106:1 (2004)
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
/May, Sept
/May) than in
the dry seasons (Jun
/Aug,
Jun
/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 (/X/981 m29/73.6 SE)
and 7 small (/X/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.

OIKOS 106:1 (2004) 29

grid dimensions from each gap for its respective under-
storey control-trapping grid. The mean area of the small
gaps was 295 m2 (n /79/62.71 SE), and on average we
used 41 traps (range: 39
/54) for each individual trapping
grid. Large gaps had a mean of 981 m2 (n /49/73.68
SE), with a mean of 73 traps (range: 60
/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.
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 gap-
understorey 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 collec-
tions or invasive procedures. Neither is allowed within
the Manu Park nor is desirable in an ecological study.
30
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).
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 popula-
tion (no additions via immigration or birth and no
deletions through death or emigration) using the pro-
gram 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
(pi), abundance (/N̂i ) 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 time-
dependent) model for survival (fi) and capture prob-
ability (pi). The full model for each of the four species-
habitat 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 Re-
lease version 3.0 (Burnham et al. 1987) with data from
each habitat. Our data fit the general model for
Oryzomys in gaps: x20.05(30) /9.634, P/ 0.999; in the
understorey: x20.05(21) /7.689, P / 0.996, and for Pro-
OIKOS 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 indepen-
dent, (r) resource density used as a covariate.
Model No. of parameters DAICc
question and the model with the lowest AICc) values
calculated for each model. We estimated monthly
abundance (/N̂i ) for a given time period (t) by dividing
the count statistic, the number of animals caught during
periods (ni), by the corresponding estimate (/p̂i ) of the
capture probability (Seber 1982): N̂i ni =p̂i :

a) Oryzomys in gaps
f(g/r) p(g/r) 8 0.00
f(g) p(g/t) 24 13.73 Fitness parameter estimation
f( ×/) p(×/) 2 16.39
f(g/t) p(g/t) 42 36.51 Because we were not able to measure fitness directly in
b) Oryzomys in understorey
the field, we used monthly survival probability estimated
f(g/r) p(t/r) 6 0.00 from capture-recapture models (obtained from the
f(g) p(g/t) 24 10.08 model selection procedure by Program MARK) and
f(g/t) p(g/t) 39 14.95
f( ×/) p(×/) 2 27.67 per capita recruitment as fitness surrogates. Because the
complements of survival probability estimates (1 /f)
c) Proechimys in gaps from capture-recapture models include permanent emi-
f( ×/) p(×/) 2 0.00
f(g/r) p(g/r) 4 0.40 gration (Pollock et al. 1990), these estimates are not ideal
f(g/t) p(t) 27 32.12 metrics reflecting fitness.
f(g/t) p(g/t) 32 41.93 We also estimated number of recruits per female.
d) Proechimys in understorey Given our intensive trapping within each habitat, we
f( ×/) p(×/) 2 0.00 assumed that all new recruits were born within the
f(t/r) p(g/r) 6 1.62
f(g/t) p(t) 28 46.47 habitat in which we caught them. We considered
f(g/t) p(g/t) 31 50.87 Oryzomys individuals with a body mass 5/28 g (max-
imum 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
echimys in gaps: x20.05(13) /5.460, P/ 0.963, in the differences in per capita recruitment across habitats, size
understorey: x20.05(21) /7.689, P / 0.996. classes and seasons, we compared the mean number of
We derived additional, parsimonious models by con- recruits trapped for the first time divided by the capture
straining the number of parameters and their time probability (/p̂i ) to estimate the abundance of recruits and
dependency (Table 1). For example, in the model divided that number by the estimated abundance of
f(×/)p( ×/), survival (f) and capture probability (p) were females in reproductive condition trapped during that
constant (×/) with respect to time, hence only two given month. To examine whether habitats, size classes
parameters were estimated. In the model f(g /t) p( ×/), and/or seasons had an effect on the fitness of each
survival was estimated separately for each month (t) and rodent species, we tested for differences between the two
size class (g) separately, whereas (p) was constant over monthly fitness surrogates combined into seasons.
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
Movement into habitats
fewest parameters. AIC is an information
/theoretical
approach that treats model selection as an optimisation We estimated the number of monthly new immigrants
problem rather than as a hypothesis-testing problem (Pollock et al. 1990) into a given habitat (animals not
(Burnham and Anderson 1998). Additional models in present in the habitat at time t but immigrating onto it
the set tested whether survival and capture probability between t and t/1 and still present at t/1) by first
varied with consumed resource density. We specified the estimating the abundance of adult individuals for month
monthly means of resource density as a covariate for the t/1. We defined an adult as an individual of a body
survival and capture probabilities within several models. mass equal to or greater than the body mass of
Many individuals survived the transition periods individuals reaching sexual maturity for each species.
between rainy and dry seasons (May
/June, and From adult abundance, we subtracted the estimated
November
/December when no trapping occurred) and number of surviving adults and juveniles (that survived
were captured in the following season. Thus, we used the and grew up to be adults) from the previous period
mean resource density over these transition periods as a computed as the product of the estimated abundance in
covariate for survivorship. We followed Anderson et al. month t and estimated survival probability between t
(1994) and selected the most parsimonious models based and t/1. Within each season, we then compared the
on the DAICc (difference between AICc for the model in mean number of immigrants to gaps from the under-

OIKOS 106:1 (2004) 31

storey, as well as the number of immigrants to the
understory area.
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 re-
source density-, and feeding experiment data, and
square-root arcsine transformed survival data. Homo-
geneity 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).
Results
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 /
0.107, P/0.746) between gaps (/X/7.0 g/m29/1.20) and
understorey (/X/9.2 g/m29/1.46) or between size classes
(F1,33 /0.125, P/0.726, Fig. 1). However, more re-
sources were available during the rainy season (/X/11.4
g/m29/1.46) than during the dry season (/X/5.4 g/m29/
1.17; F1,33 /22.625, PB/0.0001, Fig. 1).
32
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 /0.001, P/0.978)
or size classes (F1,33 /2.884, P/0.099). However,
Oryzomys consumed more fruits during the rainy season
than the dry seasons (F1,33 /10.965, P/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 /0.083, P/0.775)
or size classes (F1,33 /0.000, P/0.986). However,
Proechimys consumed more fruits during the rainy
season than the dry season (F1,33 /18.989, P B/0.0001).
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
/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 peri-
meter to area ratio in small grids. In contrast, in the
understorey, capture probability varied among month
but not by size classes. Both models included linear-
logistic 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 per-
mitted 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 prob-
ability, 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 under-
storey the slope was 1.019/0.93 SE. Again, both slopes
OIKOS 106:1 (2004)
indicate a positive relationship between survival and
mean consumed resource.
Abundance estimates
In large gaps, Oryzomys had a higher monthly abun-
dance during the rainy season (/X/19.199/6.7) than the
dry season (/X/8.679/1.9, F1,7 /5.221, P /0.056,
Fig. 3a). In contrast, in small gaps, there was no seasonal
difference (F1,13 /1.168, P/0.299). In large under-
storey, Oryzomys had a higher abundance during the
dry season (/X/15.329/2.3) than the rainy season (/X/
6.059/2.3, F1,7 /21.406, P/0.002). Similarly, in small
understorey, Oryzomys had a higher abundance during
the dry season (/X/9.629/1.6) than during the rainy
season (/X/3.599/0.6, F1,13 /18.364, P/0.001, Fig.
3a). During the rainy season, Oryzomys was more
abundant in gaps (/X/10.739/2.8) than in the under-
storey (/X/4.499/0.6, F1,18 /10.086, P/0.005, Fig.
3a). During the dry season, however, there were no
differences between habitats (F1,18 /2.908, P /0.105) or
size classes (F1,18 /2.101, P /0.164, Fig. 3a).
Fig. 3. Mean (9/1 SE) seasonal abundance in large (n/4) and
small (n/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.
OIKOS 106:1 (2004)
Proechimys abundance did not differ seasonally
(F1,40 /1.369, P /0.249); however, it was higher in
both large (/X/9.329/1.5) and small (/X/6.49/2.36)
gaps than in the large (/X/4.09/1.13) and small (/X/
1.449/0.37) understorey (F1,40 /18.794, PB/0.0001, Fig.
3b).
Fitness parameters
Survival
During the rainy seasons, there was no difference in
Oryzomys survival by habitat (F1,8 /2.371, P/0.162)
or size class (F1,8 /3.123, P/0.115). However, during
the dry seasons, Oryzomys had a higher survival in the
understorey than in gaps (F1,8 /166.981, PB/0.0001,
Fig. 4a), and was higher in large system than small ones
(F1,8 /449.290, P B/0.0001).
Proechimys had a higher survival (F1,10 /7.055, P/
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 /1.107, P / 0.333).
Fig. 4. Mean (9/1 SE) seasonal survival probability in large
(n/4) and small (n/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.
33
Per capita recruitment
There was no difference in Oryzomys per capita recruit-
ment between seasons (F1,20 /0.052, P/0.823), or size
classes (F1,20 /1.100, P /0.307). However, Oryzomys
had a higher seasonal per capita recruitment (F1,20 /
6.993, P /0.016, Fig. 5a) in the understorey (/X/
3.179/0.48) than in gaps (/X/1.679/0.48).
For Proechimys there was no difference in per capita
recruitment between seasons (F1,19 /0.007, P/0.936),
or size classes (F1,19 /0.074, P /0.789). However,
Proechimys had a higher seasonal recruitment rate
(F1,19 /12.932, P/0.002, Fig. 5b) in gaps (/X/7.89/
0.59) than in the understorey (/X/3.89/0.51).
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.
Fig. 5. Mean (9/1 SE) per capita recruitment in large (n /4)
and small (n/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.
34
There was no difference in the number of Oryzomys
immigrants by season (F1,41 /0.071, P /0.791) or by
size class (F1,41 /3.475, P /0.069). But more indivi-
duals immigrated into gaps than into the understorey
(F1,41 /8.884, P/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
/Whitney U-
test. More individuals immigrated into the understorey
than into the gaps (U/91.00, P/0.003, Fig. 6b).
Discussion
Resource density
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. 6. Mean (9/1 SE) number of immigrants in large (n/4)
and small (n/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.
OIKOS 106:1 (2004)
studies (Piñero et al. 1984, Sarukhán et al. 1984,
Denslow et al. 1986, Levey 1988, 1990).
The salient question is whether different methodolo-
gical approaches used among studies to measure re-
source 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 produc-
tion 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 (Alvarez-
Buylla and Martinez-Ramos 1990). The continuously
higher resource availability in gaps compared to under-
storey 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 simulta-
neously 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
OIKOS 106:1 (2004)
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 vesicular-
arbuscular 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 avail-
ability 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 wide-
spread 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 pre-
ferred 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 X/545 m2, 9/95 SE, range 173
/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 density-
dependent 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 new-
borns 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 (n/20) than in the understorey
(n /4, x20.05 (1) /9.481, P/ 0.01). Similarly, Adams et
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. Habitat-
specific 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 pre-
dation 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 under-
storey 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
/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
/ 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. Nuńez, 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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