Loggins 2012
Annie Loggins
20 May 2012
Large Mammal Hunting Reduces Mammal Abundances and Changes the Dominant Seed
Predators of Differently-sized Seed Species in Tambopata, Peru
Abstract
Large mammal hunting, prevalent throughout the neotropics, affects long-term forest
structure and diversity through size-differential seed predation whereby it is assumed that large
seeds are no longer consumed in hunted areas due to the absence of correspondingly large
mammals. This study compared two nonhunted and recently hunted sites in the Tambopata
National Reserve in Peru, evaluating the abundance of large and small mammals in each area and
assessing the levels of seed predation of small and large seeds by differently-sized animals. It
was predicted that fewer large seeds would be consumed in hunted sites, while more small seeds
would be consumed due to increased small mammal abundances. Animal abundance and
diversity in the differing sites were assessed through periodic transect censuses and camera traps.
Significantly fewer large mammals were found in the hunted area, as expected, while similar
abundances of small animals were reported between sites, possibly due to the lack of sensitivity
in detecting very small animals under this methodology. Seed-containing quadrants were also
laid out in each site, containing both open plots and experimental plots that excluded large
mammals, and total seed predation of large and small seeds in the two treatment types was
measured after a short timeperiod. Small animals were confirmed to be the dominant seed
predators in the hunted area, as expected, with large animals playing larger roles in seed
predation in the unhunted region. Of the 4 seed trials conducted, only one supported the
hypothesis of higher small seed predation and lower large seed predation in hunted areas. All
other trials reported similar levels of large and small seed predation across sites, but differing
methods of consumption depending on the types of animals abundant in each site. Contrary to
expectation, small animals in hunted sites were found to consume several large seeded species,
presumably filling niches left vacant by hunted large mammals. These results emphasize the
complexity of size-related seed predation under hunting pressure, and suggest that closer
examination of the consequences of different seed consumption methods by different size classes
of animals may further the understanding of how forests will respond to the continued hunting of
large mammals in the neotropics.
Introduction
Forest ecosystems are under threat due to global land use change and deforestation.
While these activities are hazardous to most species in forest ecosystems, the hunting of large
vertebrates, in particular mammals, is also a concerning threat to ecosystem health, especially in
tropical systems. Large mammal hunting, termed “defaunation” by Dirzo (2001), is prevalent
and at high magnitude in many areas of the tropics. Redford (1992) estimated that 14 million
mammals are directly killed each year in the Brazilian Amazon, with many more affected
indirectly, including orphaned juveniles. Along with the devastation on mammal survival and
abundance in hunted regions, defaunation can have significant effects on plant communities that
depend upon the interactions between mammals and the rainforest (Dirzo and Miranda 1991).
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Large mammals consume plant material, defecate throughout the forest, trample any area
they travel through, and feed on seeds, often aiding in their dispersal. In Africa, seed dispersal of
a primate-dispersed plant was severely limited in defaunated regions, with few geneticallydistinct seedlings growing near the mother plant (Wang et. al. 2007). Large mammal loss has
also been correlated with changes in the density, abundance, and composition of understory
plants, leading to loss of plant diversity (Wright et. al. 2007), because large mammal hunting has
strong effects on seed dispersal and, consequently, seedling recruitment. A comparison between
the unhunted Montes Azules forest and the defaunated region of Los Tuxtlas (both sites in
Mexico) revealed a higher density and a lower diversity of seedlings in the Los Tuxtlas
understory, due to the lack of trampling, herbivory, and seed predation of the vegetation by large
mammals (Dirzo and Miranda 1991).
The importance of large mammals to seed dispersal is linked to size-differential seed
predation. Through mammal exclusion experiments, Terborgh et. al. (1993) found that seeds of
different sizes were primarily consumed by either small or large mammals, indicating sizedifferentiation. Size-differential seed predation is the cited mechanism explaining why plant
community structure is altered by an increase in large mammal hunting, though it has proved
difficult to predict how the community will respond (Stoner et. al. 2007). Dirzo et. al. (2007)
reported an increase in rodent seed predation in the defaunated Los Tuxtlas region. As small
mammals were found to prefer small seeds, large-seeded plants proliferated due to the lack of
large mammal seed predators, suggesting an eventual shift in understory composition towards
large-seeded species. Similarly, the abundance of large-seeded plant species increased in hunted
sites in Panama (Wright et. al. 2007).
However, in hunted regions in Manu National Park, Peru, Nuñez-Iturri and Howe (2007)
found an increase in the density and abundance of saplings dispersed by small mammals, leading
to proportionally higher numbers of small-seeded plants present, presumably due to low primate
species richness and abundance from hunting. Similarly, in Tambopata, Peru, Nuñez-Iturri et. al.
(2008) studied plants relying on primate seed dispersal, and reported few primate-dispersed plant
species and far more abiotically-dispersed ones present in the defaunated region compared to the
unhunted region. These studies suggest that the benefits of increased seed survival for largeseeded species in defaunated regions may not always override the importance of mammal seed
dispersal for plant fitness. If hunting persists in the long-term, plant communities may become
dominated by small-seeded species, reducing the possibility of a reversal of impact should
hunting stop, as large herbivores will be unable to survive without the requisite large-seeded
plant resources (Stoner et. al. 2007).
These two studies were conducted in the Peruvian Amazon, possibly suggesting a
difference in mammal and plant interactions between Amazonian forests and other neotropical
sites where studies have suggested that large-seeded species survive better in hunted forests. A
comprehensive study comparing the effects of all types of mammals in two very similar sites in
the western Amazon is needed to help isolate the effects of defaunation on tropical forests, given
the described variation in plant/animal relationships between different neotropical forests.
Tambopata is an ideal location to conduct these experiments, as the habitats, soil types, and
fauna composition between the two sites in question are similar. Many other seed predation
studies rely upon separate forests that differ by geographic location as well as by hunting
pressure, potentially displaying differences in forest structure (for example Dirzo and Miranda
1991). This study is the first to conduct seed predation exclusion experiments between
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geographically close hunted and nonhunted sites in the Tambopata Reserve, although seedling
composition has been studied in relation to primate-dispersal (Nuñez-Iturri et. al. 2008).
By comparing the state of the mammalian community in the formerly hunted site with
that of the intact site, evidence of size-differential hunting in the region was assessed. It was
predicted that the abundance and diversity of mammals would be highest in the unhunted region,
and furthermore that large mammals would be significantly more abundant than in the hunted
site. As studies show that the abundance of small mammals tends to increase under large
mammal hunting pressure, it was further predicted that small mammal abundance would increase
in the hunted area, although these survey methods may not directly reveal this difference, due to
the difficulty in assessing abundances of very small mammals without the use of live-trapping
and other methods.
Overall seed predation was predicted to be higher in the unhunted site, due to the
expected decreased abundance of seed predators in the hunted area. Assuming that differences in
mammal abundance and diversity between sites would be size-related, it was hypothesized that
the amount of large seeds consumed in the unhunted area would be greater than that of the
hunted area. Consequently, it was predicted that there would be a higher proportion of small seed
predation in the hunted area, given the predicted higher abundances of small mammal seed
predators in that region and the evidence suggested by Dirzo et al. (2007) and Mendoza and
Dirzo (2007). Through these observations and experiments this study aimed to improve the
understanding of the relationship between large and small mammal seed predation in defaunated
areas of the Peruvian Amazon.
Methods
Study Site
Research was conducted between 16 August and 18 October 2011 in two sites along the
Tambopata River in the Tambopata National Reserve, Madre de Dios, Peru and based in the ecolodges of Rainforest Expeditions. The unhunted site was located 8 hours from the nearest town,
Puerto Maldonado, in the vicinity of the Tambopata Research Center (hereafter referred to as
“TRC”). Forest in this region is primary and largely floodplain, with occasional areas of terra
firme and bamboo, especially near the riverbank. The site is within the boundaries of the
Tambopata National Reserve, restricting all external fauna, impacts, and extractive activities
beyond those of the lodge and related campers and kayakers. Activities at this lodge are nonimpactful, with a combination of tourism on trails with guide supervision and research within the
forest. Many trails are only utilized by observational researchers and few long-term research
structures or plots are currently in use in the forest, with the exception of tree-climbing near
macaw nesting sites.
The impacted site was located 3 hours from the town, near the El Refugio Lodge
(hereafter referred to as “Refugio”). This area was recently established in 2006 and is under a
minimal disturbance protection status on the edge of the National Preserve. Hunting, farming,
and extractive activities (with the exception of seasonal brazil nut harvesting) are not allowed
within the jurisdiction of the lodge boundaries, although all these activities occurred prior to
2006. For the purposes of this study this area is considered under hunting impacts, although the
several years of hunting prohibition may have affected some of the results on mammal
abundance and activity. Forest in this region is at a similar elevation to that of the unhunted site,
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though at a greater distance from the riverbank, rendering more of the forest terra firme. Unlike
TRC, the landscape is predominantly secondary forest with restoration areas from abandoned
farmland, several large clearings, and a floodplain region near a small lake. Refugio supports
nearly triple the quantity of tourists at TRC and sponsors a variety of activities, including nature
walks, tree-climbing, biking, and kayaking. With the exception of these tourist activities and
former hunting impacts, the two sites are considered similar enough in terms of adjacency,
habitat types, soil structure, and elevation to be compared using the following data extraction
methods.
Mammal Survey Transects
Walking transects were conducted in order to assess the abundance of diurnal wildlife in
the two contrasting sites. Three transect lines were delineated on previously existing, relatively
straight trails in each site. Transects were between 1.05 and 1.50 km in length, with every 50m
marked along the trail with flagging tape. Transects were chosen in similar forest types between
sites whenever possible in order to adjust for the differences in habitat. In TRC, Transect 1 (T1;
1.50km) lay along a researcher trail through floodplain forest away from the lodge that was
visited only by researchers. Transect 2 (T2; 1.15km) lay in a floodplain area closer to the lodge
but seldom visited by tourists, and near the location of the seed plots, but not within range of
causing disturbance. Transect 3 (T3; 1.30 km) lay along a terra firme area that overlapped with
bamboo regions and was frequented by tourist nature walks.
In Refugio, Transect 1 (R1; 1.50km) was located far from the lodge within a floodplain
area near the lake and frequented by tourists. This transect was close to the seed plots, which
were designed to match the floodplain habitat in TRC. Transect 2 (R2; 1.05km) was located
along a terra firme and bamboo tourist biking trail, though tourists were never observed using
this trail. Transect 3 (R3; 1.25 km) was located along a trail close to the lodge used by brazil nut
harvesters during the rainy season. Though several people were encountered in this area, it was
not as trafficked or disturbed as other trail possibilities. Due to the nature of the activities and the
purpose of the Refugio lodge and region, it was not possible to correlate the trails to match
perfectly with those of TRC, though every attempt was made to mitigate potential impacts from
different levels of tourist activity.
The two sites were visited on an alternating schedule of roughly 10 days at a time across
the data collecting time period in accordance with the seed plot trials (see below). Transects were
conducted in TRC from 16-Aug to 14-Oct and in Refugio from 2-Sep to 18-Oct. Transects were
surveyed every day possible, when weather permitted and when attention was not diverted to the
seed plots. Walking transects at a pace not exceeding 1.25 km/hour, every animal detected on or
near the transect line was recorded, including the group number, detection time, distance along
the transect line, and estimated perpendicular distance from the trail (following methodology in
Peres 2001). Only data on species encountered and group size was used in this analysis. All
mammals and large ground birds (tinamous, guans, curassows, trumpeters) were included in data
collection and analysis, as ground birds are also hunted, also predate upon seeds, and may also
visit seed plots.
After walking a transect to its end, 5 minutes were allowed to pass before walking was
recommenced back along the transect length. Both directions of walking were recorded as an
independent transects, though the areas at the end-point were surveyed closer together than those
at the beginning of the transect line. Because the transects took between 1 and 2 hours to
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complete (depending on transect length), the majority of the transect line was considered to be
independent from the other, and animals were assumed to redistribute themselves throughout that
time (as described in detail in Peres 2001). In the rare cases where sedentary animals (treedwelling monkeys and coatimundis) were observed a second time near the turning point, they
were ignored in order to maintain the assumed independence of the transect line as a whole. The
total distance surveyed in TRC was 74.95 km (T1: 27 km; T2: 23.40 km; T3: 23.40 km) and the
total distance surveyed in Refugio was 72.75 km (R1: 29.05 km; R2: 19.95 km; R3: 23.75 km).
During analysis of the transects and the camera trap surveys (see below), a cut-off mark
of 5kg was used to classify mammals by size. Those with average recorded masses of greater
than 5kg were “large,” those with masses lower than 5kg were “small” (estimated from Emmons
1997). Due to this distinction several animals that are not often hunted (pacas, small cats, etc) are
placed in the “large” category, and some that are typically hunted (capuchin monkeys, etc) are
placed in the “small” category. This arbitrary cut-off point was used in order to reduce bias from
hunting reports and compare the variation in the sizes of the animals within the hunted and
unhunted sites.
Camera Traps
Camera traps were placed in matched pairs in each site designed to cover maximum types
of habitats and avoid tourist activity. Cameras T-A and R-A were each placed on a walking
transect line (T1 and R3). Cameras T-B and R-B were placed at the open seed plots that allowed
all animals access (in the vicinity of T2 and R1 but not near the transect line). Due to camera
malfunctions, the Camera T-B data for TRC are limited for this seed plot pairing. Cameras T-C
and R-C were placed in sites off-trail and away from all human activity. Cameras T-D and R-D
were placed at claylicks in both sites, though this camera pairing was not used in this analysis
due to the disparity in claylick size and data between sites (detailed in Results section). The final
pair, Cameras T-E and R-E, was to be along the Tambopata riverbank, though Camera R-E in
Refugio was stolen shortly after it was set up, thus eliminating its comparison to the matching
TRC camera, though data does exist for Camera T-E.
Before several of these matched sites were established, cameras collected data in several
other locations, and these data were also used in the camera analysis. Camera T-A was set up
almost a month before the other cameras in TRC, and another camera was used at a different site
along the transect length before it was relocated to the seed plot site. Two camera trap locations
in Refugio were used during this stretch of time as well. One was in a secluded clearing far along
R3, past the ending point of the actual transect, but recorded no data. The other was along a cliffside trail near the Tambopata riverbank.
Camera traps took captures with a 10 second frequency, recording color during the
daytime and black and white after dark. Cameras T-C and R-C had flash capabilities, and
showed color photos at all times of the day. During analysis the presence of the same species of
animal was recorded every 2 minutes, regardless of how many captures were taken every 10
seconds. In the cases where more than one animal was in the photo frame, the highest number of
animals seen in one photograph was taken to be the recorded number for every 2-minute interval.
This interval reduced over-estimating the number of captures of the same animal at a given time,
while also notating the maximum number of animals caught in one capture so as to better
estimate the total number of animals present. Due to the variances in time the cameras were
active, all camera trap numerical data (numbers of animal captures and total abundances
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recorded) were adjusted to the total number of 12-hour periods each camera was recording data,
thus standardizing the data to the total amount of time the cameras were active.
Seed Plots
Seed plots were constructed in floodplain areas in TRC and Refugio (near transects T2
and R1, respectively). Three treatments were established in each site with six plots of each:
Exclusion Treatment, caged plots excluding all animals; Partial-Exclusion Treatment, caged
plots excluding large mammals but open to small; and Open Treatment, open plots excluding no
animals. After clearing the ground of leaves and debris, 0.66m x 0.66m plots were constructed
and arranged at a perpendicular distance of 10m into the forest from a walking trail. The six plots
of each treatment were arranged in a 2x3 grid, with 3m separating each. Treatments were spaced
50m apart along the trail.
Exclusion plots were encircled with 1-metre tall, ¼ inch mesh chicken wire supported by
wooden or plastic stakes and nailed into the ground at intervals to prevent any mammal from
burrowing underneath. The Partial-Exclusion plots were encircled with 1-metre tall, ½-¾ inch
mesh chicken wire supported with stakes but not nailed into the ground. In order to ensure that
small mammals were able to access the plot while still excluding large mammals, one 6x8 inch
door was cut out of the chicken wire at the base of each of the cage walls, allowing all small
mammals to enter and exit the plots through these holes. The Open plots were cleared and
measured to be the same size as the other treatment plots, with small stakes marking the edges,
but no other form of cage or impact.
Seeds were collected from the forest floor or directly from the plant (Chamaedorea and
Clarisia only; see Table 1 for seed species used) and were chosen for their predicted palatability.
Each plot replicate contained 5 seed pairs of two species in the same taxonomic family (with the
exception of Trial 4), one large and one small, and were arranged in a random, predetermined
scatter plot formation within each plot, following methodology described in Mendoza and Dirzo
(2007). In Trails 1 and 3 the small seeds were so small that multiple seeds were placed in 5
groups in each plot in order to better match the size and mass of the large seeds. In Trial 1, 10
small seeds were placed for every large seed, and in Trial 3, 3 small seeds were placed for every
large seed. The length and width of each type of seed was measured using a 50-seed sample in
order to confirm the size differences between seeds (see Appendix A for average seed sizes).
Seeds Used in Trials
Trial Family
Large Seed Genus Small Seed Genus
Iriartea
Chamaedorea
1 Arecaceae
Pourouma
2 Cecropiaceae Pourouma
Iriartea
Euterpe
3 Arecaceae
Unknown
4 Brindaceae
Moraceae
Clarisia
Table 1. Seed families used in each trial with genus listed for small and large seeds. The same
species of large seed was used in Trials 1 and 3. Trial 2 seeds were both from the same genus,
and Trial 4 seeds were from different families.
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Seed trials were run approximately every 10 days with seed collection occurring several
days before the seed plot starting dates (see Table 2). Four trials were completed, with seven
species of seeds used total (see Table 1; the same large seed was used in both Trials 1 and 3 due
to the absence of other comparable large seeds). At the end of each seed trial, seeds were
collected, the amount eaten of each seed was determined (all eaten, partially eaten, and uneaten),
and the method of seed consumption was noted, if visible. Categories ranged from Germinated,
Intact (the percentage of viable seeds remaining in each treatment), Partial (seeds that were
damaged but not entirely consumed), Shell (the cracked shell of the seed case that was left
behind though the seed itself was gone), Bits (the shell of the seed was gnawed into small
fragments though the seed itself was gone), and Unknown (the percentage of seeds lost to the site
and presumed eaten, though the method of predation is not known). Average seed predation was
calculated from the seed methods, with 100% = no seed remaining (although remnants of seed
shell, fruit, or outer coating may exist), 50% = seeds were partially consumed or damaged
(regardless of the degree of damage observed, all were standardized to 50% due to the inability
to accurately judge the percentage of seeds damaged in the field), and 0% = whole seed
remaining and undamaged, although seed shell, fruit, and/or outer coating may show some
damage. Seeds were then discarded and replaced with the seeds of the next trial.
Seed Trial Placement Dates and Durations
Trial
Date
TRC
1
2
3
4
Final
clearing of
seeds
27-Aug
31-Aug
11-Sep
12-Sep
22-Sep
23-Sep, 24Sep
5-Oct
6-Oct
15-Oct, 16Oct
Refugio
Morning
TRC Trial
Duration
16 days
REF Trial
Duration
11 days
Morning/afternoon
Morning
10 days
12 days
14 days
11 days
9 days
13 days
Morning/afternoon
Morning
Afternoon, morning
Morning
Afternoon
Afternoon,
morning
18-Oct
Morning
Table 2. Dates seeds were placed, collected, and replaced in each site. Consistent trial duration
was limited by unpredictable transportation between sites.
Exclusion and Partial Exclusion plots that were knocked over or damaged by visiting
large animals (predominantly white-lipped peccaries in TRC) were not included in the analysis
and were fortified to resist future damage (the majority of these accidents occurred during Trial
1). Data was collected on the types of animals visiting the Open plots through the use of cameras
in each site. Though ideally another camera would have been placed near the Partial Exclusion
plots, this was not possible in this study.
Results
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Transect Surveys
A) Total Number of Species Sighted
10
9
8
7
6
5
4
3
2
1
0
TRC
Refugio
Large
Small
B) Total Animal Sightings
70
60
50
40
TRC
30
Refugio
20
10
0
Large
Small
C) Total Animal Abundance Encountered
800
700
600
500
400
TRC
300
Refugio
200
100
0
Large
Small
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Figure 1. Total number of animal species encountered (A), number of separate animal sightings
(B), and total abundance of animals as summed for every estimated animal group size in the field
(C), separated into size class and compared across the two sites.
The number of species and number of sightings of all animals (including ground birds) of
both sizes was significantly higher in TRC, the intact site (using a 2-fixed-factor ANOVA
analysis with no significant interaction term, Site was significant with Species: p=.004 and
Sightings: p=.015). Large animal abundance was significantly higher in TRC, though small
animal abundance was not (Tukey’s test after a 2-fixed-factor ANOVA analysis, Large: p=0.016;
Small: p=0.713). Avian species are included in the analysis to increase sample size, as trends
including birds mirror those without birds. The difference between the two sites is greater for
large animals than for small animals in all data categories, as follows: Species (Large: 3; Small:
2), Sightings (Large: 38; Small: 15), Abundance (Large: 684; Small: 78). The Total Abundance
estimates represent the largest disparity between sites, where large animals are over 10 times
more abundant in TRC than in Refugio. As in all other cases, the difference in small animals is
much lower, in this case only 1.4 times more abundant in TRC than Refugio.
Similarity Coefficients between Hunted and Intact Sites
1
0.9
0.8
0.7
0.6
0.5
Large
0.4
Small
0.3
0.2
0.1
0
Historical Level
Species
Sitings
Total
Abundance
Figure 2. The calculated similarity coefficients for number of species, number of sightings, and
total abundance of animals between sites, separated by size class, as compared to predicted
historical levels of similarity.
Small animals remain at a constant 0.8-0.9 similarity coefficient across each category
though large animals decline in similarity as they progress from species counts, which are
relatively similar across size classes (again between 0.8 and 0.9), to number of sightings, and
finally total abundance, where large animals reach below 0.2 for similarity. This further
emphasizes the greater difference between the sites when considering large animals, particularly
in terms of estimated abundances. The number of species in each site is less dissimilar for both
size classes. Though TRC boasts greater species richness than Refugio in large and small
animals, the bulk of the species surveyed are present in both the two sites. No species was found
in Refugio that was not also found in TRC (see Appendix B).
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Species Diversity by Size Class and Site
Site
Large Animals
Small Animals
TRC
0.829719725
0.879432624
Refugio
0.770750988
0.85026738
Table 2. The calculated Simpson’s Species Diversity using the total numbers of species as
compared with the number of sightings for each site separated into size class. Reported values
are the inverse of the calculated Simpson’s Diversity Index values (1 = the highest diversity
rating).
The species diversity values for Sightings in each location separated by size class further
emphasize the higher levels of diversity in TRC for both large and small animals. Note again that
the difference in diversity between TRC and Refugio is higher for large animals than for small
ones. Small mammal diversity is almost identical between sites, though large mammal diversity
is lowest in the hunted area.
Camera Traps
The cameras at the claylicks in both sites (T-D and R-D) were eliminated from the data
set, due to the outlying data in Refugio, which contained a large volume of animal captures with
a count higher than that of any other camera found in Refugio or in TRC. The Refugio claylick is
large and periodically cleared by staff to support tourist activity in a nearby viewing blind, while
the claylick at TRC is much smaller and less defined, in a gully that is not available to tourists.
Due to the nature of the large claylick structure at Refugio, it is assumed that the majority of
these images were taken of the same animals as they visited the lick. Because these data varied
so much from the rest of the data from Refugio, and the increase in animal captures at the
claylick was not equaled at the matching claylick in TRC (claylick data was similar to that from
other cameras, likely due to the much smaller TRC claylick size and lack of clearing and
maintenance), data from both claylicks were ignored in this analysis.
A) Total Number of Species Captured by Cameras
14
12
10
8
TRC
6
Refugio
4
2
0
Large
Small
B) Total Animal Captures as Proportions of Time Active
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1.4
1.2
1
0.8
TRC
0.6
Refugio
0.4
0.2
0
Large
Small
C) Total Animal Abundance as Proportions of Time Active
1.6
1.4
1.2
1
0.8
TRC
0.6
Refugio
0.4
0.2
0
Large
Small
Figure 3. Total numbers of animal species encountered (A), number of separate animal captures
as determined by the 2-minute timing limit (B), and total abundance of animals as summed for
every estimated animal group size per photograph (C), separated into size class and compared
across the two sites. The numerical data for B) and C) was normalized into the proportion of the
total time the camera was active, standardized to 12-hour timeslots.
As in the transect surveys, TRC exceeds Refugio in all measurements of animal captures
and abundance. Though species counts are similar between sites, species overlaps are different.
All large birds, with the exception of the Spix’s Guan and the Pale-winged Trumpeter, were only
captured in TRC, as were the Brazilian Rabbit and the Brazilian Porcupine. The Short-eared
Dog, the Jaguarundi, and the Tayra were only recorded in Refugio (note that Tayras were
recorded in TRC during the transect counts, and Razor-billed Curassows were reported in
Refugio, emphasizing the importance of multiple types of observation to fully assess animal
presence and absence).
The differences in capture count and estimated abundance (adjusted as proportions of
total camera activity time) between the two sites is again of higher magnitude for the large
animals and lower for small animals: Captures (Large: 1.034; Small: 0.190), Abundance (Large:
1.057; Small: 0.179).
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Similarity Coefficients Between Sites
1
0.9
0.8
0.7
0.6
0.5
Large
0.4
Small
0.3
0.2
0.1
0
Historical Level
Species
Captures
Total
Abundance
Figure 4. The calculated similarity coefficients for number of species, number animal captures as
adjusted per 12-hour timeslot of camera activity, and total abundance of animals captured as
adjusted per 12-hour timeslot of camera activity in each site, separated by size class, as
compared to predicted historical levels of similarity.
As with the transecting surveys, the species richness of the two sites was most similar,
though more different than in the transects due to the lower species overlaps between sites. Some
animals were found only in Refugio, unlike in the transects where all animals in Refugio were
also recorded in TRC. Unlike in the transecting study, the small animal data were as dissimilar
between sites as the large animal data, and in fact are more dissimilar than large animals in every
type of data representation.
Seed Predation Plots
Species Recorded in Seed Plot Camera Traps
Animal
TRC Captures Refugio Captures
White-lipped Peccary
7 (1)
1 (3)
Total Peccaries
8 (1)
4 (2,3,4)
Brocket Deer
1 (1)
1 (4)
Green Acouchy
1 (1)
Red Squirrel
1 (1)
Rat/Small Opossum
5 (1)
Common Opossum
1 (1)
Small Tinamou
1 (1)
Large Tinamou
1 (1)
Crake
4 (1)
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Loggins 2012
9-banded Armadillo
1 (3)
Brazilian Tapir
1 (4)
Paca
2 (3)
Pale-winged Trumpeter
1 (4)
Total
31 (1)
11 (1-4)
12-hour Proportion
1.9292938
0.12442852
Table 4. All animal captures recorded on camera traps placed near seed plots. Proportions are
the data in numbers divided by the total time cameras were active (TRC: 192.82 hours; Refugio:
1060.85 hours) represented by 12-hour intervals. Numbers in parentheses indicate during which
Seed Trial the animal was detected.
Due to camera malfunctions in TRC, the seed plot camera (Camera T-B) was only active
during Trial 1 of the seed plots, while the matching camera in Refugio (Camera R-B) was active
through all four trials, though only reported animals during the last 3 Trials (see Table 4). TRC
recorded almost 3 times as many animals than Refugio, despite the much longer time active for
the Refugio camera. The animal counts converted into proportions of the cameras’ total time
active reinforce the difference between sites. Only white-lipped peccaries and brocket deer were
recorded in both seed plot sites, and the number of species recorded was higher in TRC than in
Refugio, though Refugio recorded more large animals than TRC. Brazilian Tapir, Paca, and
Pale-winged Trumpeter are all classified as “large,” and Large Tinamou was the only “large”
animal seen in TRC that was not also recorded in Refugio.
Seed Predation for Partial and Open Treatments – Trial 1
A) TRC
B) Refugio
1
1
0.8
0.8
0.6
Big
Seeds
0.4
Small
Seeds
0.2
0
Big
Seeds
0.4
Small
Seeds
0.2
0
Partial
C) TRC
0.6
Open
Partial
Open
D) Refugio
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Loggins 2012
100%
90%
80%
70%
60%
50%
40%
30%
20%
10%
0%
Big
Small
Partial
Big
Small
100%
90%
80%
70%
Germinated
60%
% remaining
50%
40%
Shell
30%
Bits
20%
10%
Unknown
0%
Germinated
% remaining
Shell
Bits
Unknown
Big
Open
Small
Partial
Big
Small
Open
Figure 5. A),B) Trial 1 (Family Arecaceae) seed predation as measured as the proportion of
seeds gone in all plot treatments separated by site and seed size. C),D) Method of seed
consumption as judged by the remaining evidence divided by site, treatment, and seed size.
Fully caged, Exclusion plots universally served their purpose of excluding all non-insect
animal activity and are ignored in this report. No significant differences were found at the site
level for Trial 1, although the interaction between site, treatment, and seed size was significant
(3-fixed-factor ANOVA, p=0.018). Seed predation of large seeds was slightly but not
significantly higher in TRC than in Refugio for Open plots. Seed predation of small seeds was
similarly high in both treatments in both sites. Significantly more large seeds were consumed in
Open plots in both sites than in Partial Exclusion plots (Tukey’s Test after 3-fixed-factor
ANOVA, TRC: p<<0.001; Refugio: p=0.001). Only Refugio reported predation of large seeds in
Partial Exclusion plots.
Because the way seeds were eaten in the plots was noted in the field, data can be shown
according to method of seed consumption and disappearance. The majority of large seeds eaten
in Refugio in Trial 1 left behind shredded residue, while all large seed predation evidence in
TRC was in the form of cracked shells. Though no seeds germinated in TRC, large seeds
germinated in both treatment types in Refugio.
Seed Predation for Partial and Open Treatments – Trial 2
A) TRC
B) Refugio
1
0.9
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
Big
Seeds
Small
Seeds
Partial
Open
1
0.9
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
Big
Seeds
Small
Seeds
Partial
Open
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Loggins 2012
C) TRC
D) Refugio
100%
90%
80%
70%
60%
50%
40%
30%
20%
10%
0%
100%
90%
80%
% remaining
70%
60%
Partial Damage
50%
Shell
40%
30%
Bits
20%
10%
Unknown
0%
Big
Small
Partial
Big
% remaining
Partial Damage
Shell
Bits
Unknown
Big
Small
Small
Partial
Open
Big
Small
Open
Figure 6. A), B) Trial 2 (Family Cecropiaceae) seed predation as measured as the proportion of
seeds gone in all plot treatments separated by site and seed size. C), D) Method of seed
consumption as judged by the remaining evidence divided by site, treatment, and seed size.
Very few small seeds were consumed in Trial 2, though large seeds were consumed in
both sites. Seed predation in Open plots was similar between sites (Tukey’s Test after 3-fixedfactor ANOVA, Large: p=1.000; Small: 1.000) and both reported significantly more predation of
large seeds than that of small in Open plots (Tukey’s Test after 3-fixed-factor ANOVA, TRC:
p<<0.001; Refugio: p<<0.001). However, significantly more large seeds were eaten in Refugio
in Partial Exclusion plots than in TRC (3-fixed-factor ANOVA, p=0.045).
The majority of large seeds attacked in Refugio in Trial 2 were only partially affected,
while fewer seeds in TRC display this impact, leaving behind a higher proportion of shells than
in Refugio.
Seed Predation for Partial and Open Treatments – Trial 3
A) TRC
B) Refugio
1
0.9
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
Big
Seeds
Small
Seeds
Partial
C) TRC
Open
1
0.9
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
Big
Seeds
Small
Seeds
Partial
Open
D) Refugio
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Loggins 2012
100%
90%
80%
70%
60%
50%
40%
30%
20%
10%
0%
100%
90%
80%
Germinated
70%
% remaining
60%
50%
Partial Damage
40%
Shell
30%
20%
Bits
10%
Unknown
0%
Big
Small
Partial
Big
Small
Open
Germinated
% remaining
Partial Damage
Shell
Bits
Big
Small
Partial
Big
Small
Unknown
Open
Figure 7. A), B) Trial 3 (Family Arecaceae) seed predation as measured as the proportion of
seeds gone in all plot treatments separated by site and seed size. C), D) Method of seed
consumption as judged by the remaining evidence divided by site, treatment, and seed size.
Though Trial 3 used the same large seed species as in Trial 1, results differed, although
the duration of seed exposure was lower in Trial 3 than in Trial 1 (see Table 2). No significant
differences were found at the site level for Trial 3, although the interaction between site,
treatment, and seed size was significant (3-factor ANOVA, p=0.018). Small seed predation was
similar across treatments in TRC (Tukey’s Test after 3-fixed-factor ANOVA, p=0.995), although
nearly significantly higher in Open plots in Refugio than in Partial Exclusion plots (Tukey’s Test
after 3-fixed-factor ANOVA, p=0.050). Conversely, large seed predation was similar across
treatments in Refugio (Tukey’s Test after 3-fixed-factor ANOVA, p=0.230), though significantly
higher in Open plots in TRC than in Partial Exclusion plots (Tukey’s Test after 3-fixed-factor
ANOVA, p<<0.001).
The most complicated of the seed trials, all sites and treatments in Trial 3 show evidence
of large seed germination, though again differing between sites. Large seeds eaten in Partial
Exclusion plots in Refugio left behind primarily seed bit remnants. More large seeds in TRC
were not found, with the method of consumption unknown. Shells of small seeds were left
behind in both sites, although as the seeds were smaller the method of consumption may be less
attributed to seed predator size than it may be for larger seeds (see Discussion).
Seed Predation for Partial and Open Treatments – Trial 4
A) TRC
B) Refugio
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Loggins 2012
1
0.9
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
Big
Seeds
Small
Seeds
Partial
1
0.9
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
Small
Seeds
Partial
Open
C) TRC
Big
Seeds
Open
D) Refugio
100%
90%
80%
70%
% remaining
60%
Partial Damage
50%
40%
Shell
30%
Bits
20%
10%
Unknown
0%
100%
90%
80%
70%
60%
50%
40%
30%
20%
10%
0%
Big
Small
Partial
Big
Small
Open
% remaining
Partial Damage
Shell
Bits
Unknown
Big
Small
Partial
Big
Small
Open
Figure 8. A), B) Trial 4 (multiple families) seed predation as measured as the proportion of seeds
gone in all plot treatments separated by site and seed size. C), D) Method of seed consumption
as judged by the remaining evidence divided by site, treatment, and seed size.
Though seeds in Trial 4 were not heavily predated upon, significantly more small seeds
were consumed in Open plots in Refugio than in TRC (Tukey’s Test after 3-fixed-factor
ANOVA, p=0.042). Large seeds did not differ in consumption levels between treatments in
Refugio (Tukey’s Test after 3-fixed-factor ANOVA, p=0.507), though significantly more large
seeds were consumed in Open plots in TRC than in Partial Exclusion plots (Tukey’s Test after 3fixed-factor ANOVA, p<<0.001).
As in Trial 1, more large seed shells were encountered in TRC than in Refugio, while
only Refugio left behind seed fragments of large seeds. More seeds of both sizes were only
partially affected in Refugio than in TRC.
Discussion
Mammal Abundance
17
Loggins 2012
From the transecting and camera trap studies it is clear that mammal abundance is indeed
lower in the formerly hunted site, Refugio. Data also show that mammals (as well as ground
birds) are absent according to their size; large animals were greatly reduced in numbers and in
species count in the hunted area. The large disparity in abundance of large mammals between
sites is specifically attributed to the high abundances and frequency of encounters of whitelipped peccaries in TRC, which travel in large herds and were common and easy to detect in
transect and camera trap surveys. In Refugio these mammals were all but absent (appearing only
once each on the transect line and in the camera traps; see Appendix B). Spider monkeys were
another significant large mammal entirely absent in Refugio, likely due to past hunting pressure
as well as human impacts in the region. Though sites are dissimilar in all data categories
(species, sighting, and abundance) they differ least in species count, indicating that the species
diversity of the sites remains similar, although the frequency of encounter of certain large species
and their overall abundance is much lower in the hunted area.
Contrary to the results of other studies and to expectation, small mammal abundance did
not seem to increase in the hunted area, according to the transecting and camera trapping studies.
However, the methods of this study were not designed to specifically target the abundance of
mammals smaller than diurnal primates and large rodents. No small rodent traps were used, and
the evidence of these creatures in the camera trap data cannot accurately represent their true
numbers, due to the difficulty in observing them within the camera trapping field of view.
Therefore although differences in small rodent abundances may indeed exist under the different
hunting pressures, this study was unable to detect them using survey methods.
Furthermore, the formerly hunted area contains larger animals than might be expected in
a currently hunted site (such as peccaries, tapirs, and large cats), which suggests that large
mammal populations have begun to recover in the five years since hunting ceased. Though still
maintaining significantly lower populations of large mammals than in intact sites, the Refugio
area may represent a more intermediate level of hunting damage, whereby the recovering
presence of large mammals may be slowly reducing the competitive advantages of small
mammals that might otherwise exist in much higher abundances in regions where large
mammals are fully absent.
The transecting and camera trap data confirm the assumption that mammals have been
differentially hunted according to size in the Tambopata region near the El Refugio Lodge, and
provide a basis for making inferences about the accompanying seed predation experiment.
Seed Predation
Due to the limits on the camera functioning in TRC, it is difficult to quantify exactly
which animals were eating the seeds in the intact site, although it is assumed that more peccaries
were detecting and consuming the seeds there than in Refugio, due both to the camera trap
evidence from the first trial when both cameras were active and because of the much higher
abundances of peccaries in TRC as measured by the transects and overall camera trapping data.
Though Refugio recorded a larger diversity of large animal species in seed plot captures, these
were gathered over the entire time period with a low number of captures per species, therefore it
is likely that an equal if not greater number of large animal species would have been captured in
TRC had the camera been active for the full duration. The camera on the TRC plots detected
almost 3 times more animals in one trial than the Refugio camera did over the whole 2-month
18
Loggins 2012
collecting period, suggesting a much higher level of seed detection and animal activity in the
intact site for animals large enough to be captured regularly on camera.
Because Trials 1 and 3 were grouped in pairs within the same taxonomic family,
Arecaceae, these trials will be compared in relation to each other, especially because both
utilized the same large palm species, of the genus Iriartea.
The total amount of seed predation in Trial 1 of large and small seeds did not differ
greatly between the sites. Large seeds were eaten in Partially-Excluded plots in Refugio, while
none were eaten in this area in TRC, possibly suggesting a higher abundance of small seed
predators in the hunted area able to crawl through the cage openings. It must be noted that caged
plots in Trial 1 experienced more destructive accidents than in any other trial. Exclusion and
Partial Exclusion treatments in TRC contained only 4 and 3 usable replicates, respectively,
instead of the usual 6. With more replication seed predation of large seeds might have been
detected in Partial Exclusion plots in TRC. Refugio plots were unharmed in this treatment, again
suggesting a low abundance of the large animals that knocked over the plots in TRC.
Though overall seed predation was similar, the manner in which the seeds were eaten
differed between sites. Seed remnants in TRC took the form of shell halves, while seeds were
shredded into small pieces in Refugio. As the camera trap data show that white-lipped peccaries
visited TRC seed plots during Trial 1, it is assumed that many large seeds were consumed by
these animals, leaving behind evidence of shells cracked by their teeth (as detailed in Beck
2006). As very few seed shells were encountered in Refugio, and the majority of seed evidence
was that of small pieces, it is assumed that smaller animals, such as rodents or opossums,
consumed the seeds through multiple gnawing attacks. The camera trap in Refugio did not record
any presence of animals at the seed plots during Trial 1, further suggesting that seed predators in
this site were predominantly small rodents, which are most difficult to capture on camera, and
reinforce the assumed lack of larger animals in the area during the trial. Thus although the
abundance of seeds consumed was the same across sites, no matter the different levels of
hunting, the way in which the large seeds were eaten revealed the animals that had detected the
seeds first: large animals in TRC, smaller ones in Refugio. This evidence supports the hypothesis
that smaller animals are responsible for more seed predation in Refugio than in TRC, due to the
reduced populations of large animals.
The same amount of small seeds was consumed in both sites in both treatments,
suggesting that small animals are consuming small seeds, as the amount of seeds eaten did not
vary between treatments that allowed all animals’ access and those that only allowed small
animals. This is expected from the literature that suggests that small animals typically consume
small seeds (Terborgh et. al. 1993, Dirzo et al. 2007, Mendoza and Dirzo 2007). Unfortunately it
is unknown at what point the small seeds were detected and consumed. Awareness of this
detection time might have determined whether smaller seeds were detected sooner in Refugio, as
would be predicted under a model where small animal abundance is higher in hunted areas and
more seed predators are foraging for small seeds.
It is unexpected that such large proportions of large seeds would be consumed in
Refugio, given the lack of large mammals and the evidence from the literature that small
mammals do not consume larger seeds. Clearly, rodents and other small mammals do gnaw
through some large seeded species. Some research has been done on small neotropical animals
caching larger seeds for later use, particularly squirrels and acouchies (Jansen et al. 2004). These
small mammals can play important roles in seed dispersal by burying seeds in caches, which they
often forget to recover, and allowing some seeds to survive. However, the evidence in this
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Loggins 2012
Tambopata study suggests that the seeds were being predated upon, rather than removed for
storage. From Trial 1 it appears that though hunting pressure may differ between sites, the actual
predation of large seeds, at least for the Iriartea species used, remains the same.
In Trial 3 significantly more large seeds were consumed in TRC in Open than in Partial
Exclusion plots, emphasizing that large animals dominate the seed predation of large seeds, as
expected. This parallels results found in Trial 1, where the difference was even greater, as no
large seeds were consumed in Partial plots at all. Though this trend was reported in both sites in
Trial 1, in Trial 3 no significant difference was found between plot treatments for large seeds in
Refugio, suggesting that the same small animals were consuming the seeds in both plots equally.
This supports the hypothesis that primarily only small mammals are predating upon seeds in
hunted sites, though again questions the assumption that small animals only consume small
seeds.
It is unexpected that though small seeds were consumed equally between plot treatments
in TRC, significantly more small seeds were consumed in Open plots in Refugio than in Partial
Exclusion plots. This could be related to random variance in the detection of small seeds by
small seed predators, though the close proximity of the seed trials (at 50 m distance apart) was
designed to limit potential differences in seed detection across the vegetation matrix. It is
possible that there was some interaction between the seed species and the preferences of the
visiting seed predators. Different seed predators with different seed preferences could have
visited each treatment by chance, resulting in lower levels of predation in Partial Exclusion plots
than expected.
According to Trials 1 and 3 together, seed predation levels may remain the same under
hunting pressure. However, the way in which the seeds were eaten could have implications for
large seeded plant species. Though seeds that were shelled or gnawed to bits were entirely
consumed by the animal, many large seeds in both sites were only partially gnawed. Depending
on the seed species, these seeds may be able to survive. A portion of the large seeds that
germinated appeared to have been partially gnawed (Loggins pers. obs.). The largest amount of
germination, which occurred in Partial Exclusion plots in TRC during Trial 3, coincides with the
highest level of partial seed consumption. This suggests that some seed species may be able to
survive a certain degree of seed predation, provided it is from an organism that only partially
consumes the seed. This could explain the lower seed germination levels reported in Refugio for
Trial 3, where more seeds were fully chewed to pieces instead of only partially consumed. It is
possible that the disturbance of the seed casing benefits some seeds by hastening their exposure
to soil nutrients. No seeds germinated in Exclusion plots in Trial 1, even though these excluded
all animals and displayed the highest level of seed survival (data not shown), which could
support the theory that these seeds benefit from partial gnawing attacks. Though some seeds did
germinate in Exclusion plots in Trial 3, the highest level of germination recorded is still that of
Partial Exclusion plots.
In the long-term, large Iriartea seeds could experience higher seed germination success
in areas where seeds are partially consumed by seed predators than in areas where seed predators
are absent. Unfortunately, it is difficult to determine the mechanism behind the higher levels of
partial seed consumption in TRC than in Refugio. It is possible that the abundance of small seed
predators in Refugio led to more seeds being fully consumed, while in TRC small animals were
more dispersed, and fewer seeds were consumed fully. Similarly, seeds may be suffering attacks
by multiple individuals in areas where small animals are in higher abundance. In areas where
smaller animals are less populous, seed predators gnaw only partially through seeds in one
20
Loggins 2012
sitting, leaving them the opportunity to germinate and proliferate if another seed predator does
not find them.
One final examination of the evidence reveals that more large seeds were marked as
“unknown” in TRC than in Refugio for both Trials 1 and 3. For the purposes of this study, any
seed not in the seed plot at the end of each seed trial was reported as consumed, although the fate
of each seed is unknown in actuality. Seeds vanishing from plots were assumed to have been
moved by animals for consumption. However, under this assumption it is still possible that some
seeds may have been taken by disperser animals such as tapirs, who excrete palm seeds intact,
allowing for the survival of consumed seeds via dispersal (as detailed in Olmos et al. 1999).
Thus although seed consumption is presumed to be similar between hunted and unhunted sites,
in fact large palm seeds may have survived better in unhunted areas, due to the abundance of
large seed dispersers such as tapirs who could have swallowed the seeds whole, leaving behind
no shell evidence. This study was unable to track the fate of the seeds in plots; therefore the
method of consumption is at times unknown. Further studies on both the animals visiting the
seed plots, and the fate of the seeds themselves are needed to confirm the levels of seed predation
assumed in this study and the specific consumers involved.
Trials 1 and 3 were most successful at gauging animal responses to two different sizes of
seeds, presumably due by chance to the palatability of the palm species selected. Unfortunately,
few small seeds were consumed in Trial 2, no matter the treatment or site, suggesting a lack of
palatability of that seed species, at least for vertebrate seed predators on the ground. In this case
only the predation of large seeds can be discussed, as an interaction between seed size and
predation level between sites is not present.
Nonetheless, evidence from Trial 2 confirms the assumption that more small seed
predators exist in Refugio than in TRC. Significantly more seeds were consumed in Partial
Exclusion plots in Refugio than in TRC, suggesting that more small seed predators are present in
Refugio. Seed predation is similar between Partial Exclusion and Open treatments in Refugio,
while more seeds were consumed in Open plots than in Partial Exclusion plots in TRC,
presumably because in Refugio the same small animals were accessing both seed plots equally;
while in TRC large seed predators were only able to consume seeds in Open plots.
The manner of seed consumption again differed between sites, even though seed
predation in Open plots was similar. More large seeds were only partially attacked in Refugio,
again suggesting smaller seed predators that focused on the fruit and gnawed only intermittently
at the underlying seed. In TRC more seed shells were left behind, suggesting more intent to
consume the whole seed from the start. It is unfortunate that the camera trap at TRC was unable
to capture animal photographs beyond the first trial, to see if this assumption is correct. Only one
animal, a peccary, was captured on camera in Refugio, emphasizing the assumption that small
animals were the predominant consumers in this site, as in Trials 1 and 3. One animal capture is
not sufficient to assume that peccaries were a significant visitor to the plots, especially
considering the tendency of peccaries to travel in large groups and trigger multiple captures.
It is unclear how the large Pourouma species in question would react in the long-term to
the difference in seed predators between sites, as overall seed predation in Open plots was high
in both sites, suggesting a similar level of seed predation no matter the level of hunting. Though
seeds from palm species like those in Trials 1 and 3 may survive being partially gnawed, it is not
predicted that this Pourouma species would have the same reaction. Germination of this species
was never noted, although its germination period may be longer than that of the palm. This
species may experience equivalent levels of seed predation and seed mortality in defaunated and
21
Loggins 2012
intact sites, suggesting that not all large seeds will experience less predation under hunting
pressure, as predicted by the literature.
In Trial 4, significantly more small seeds were consumed in Open plots in Refugio than
in TRC, again suggesting that small seed predators are more abundant in Refugio. As in Trial 2,
more seeds in Refugio were only partially-consumed, which further supports the assumed
abundance of small seed predators. Large seeds were consumed equally across treatments in
Refugio, while significantly more large seeds were consumed in Open plots than in Partial
Exclusion plots in TRC, suggesting that large seed predators play a significant role in large seed
predation, as in Trial 2.
The camera trap in Refugio reported both a brocket deer and a Brazilian tapir at the seed
plots during Trial 4, which would seem to contradict the theory that only small animals are
consuming seeds in this site. However, neither photo depicts the animals actively consuming the
seeds. The sample size is too low to confirm the abundance of large animal seed predators during
this Trial, as these animals may have been only passing through, since capture counts would
presumably be higher if they lingered to forage in the area.
For Trial 4 it appears that small seeds of this species will be more actively predated upon
in hunted areas, presumably due to the higher abundance of small animals. Conversely, large
Clarisia seeds will be more heavily consumed in unhunted areas. Trial 4 is the only trial to
support the hypothesis that small seeds are consumed more in hunted areas and large seeds
consumed more in unhunted areas, due to the differential hunting of large mammals and the
resultant increase in small mammal abundance. It must be noted that this was the only trial not to
use seeds from within the same family, so additional bias may have affected these results.
Conclusion
Large animals are clearly most abundant in unhunted sites in Tambopata, though small
animals appear to be in similar abundance, although further differences could be revealed by
using methodology that targets small mammals, such as live-trapping. These results are as
expected, given the past history of hunting in the region, and typify the size-differential hunting
present throughout neotropical rainforests.
Taken together, the seed predation trials reveal somewhat conflicting results. With the
exception of Trial 4, seed predation seems to be largely similar between sites across seed trails
for Open plots. Looking closer at the method of seed consumption reveals differences in the type
of seed predators found in hunted and unhunted sites. However, the seed trials universally
emphasize that small animals are predominantly responsible for seed predation in Refugio. This
is shown through the higher levels of small seed remnants and amount of partially-gnawed seeds
in the hunted site, as well as the similarity between Partial Exclusion and Open plots in Refugio.
By contrast, TRC seed predators left behind more shell evidence, and seed predation varied more
between treatment types, suggesting that large seed predators were responsible for much of the
seed predation. Only Trial 4 supports the original hypothesis that large and small animals
consume large and small seeds, respectively, and that seed predation of specific seed sizes will
depend on the abundance of the corresponding mammal size in the region.
Seeds that were lost entirely to the plots remain a mystery, possibly suggesting the
presence of large animals such as tapirs, which transport and disperse seeds intact, or the
abundance of scatter-hoarding rodents, which transport whole seeds to buried caches. Further
examination of the seed fate of these “lost” seeds is needed to assess the seed predation as a
22
Loggins 2012
whole and better determine the impact of hunting on the seeds in question. Functioning camera
traps placed at seed plot sites could provide evidence of seed predators, and seed tracking
methodology could be used to trace seeds to their final consumption or dispersal destination.
Predation of large-sized seeds is not necessary correlated to large-sized seed predators.
Some seeds are predated by large animals in unhunted areas, but are consumed by small animals
when the size-differential hunting of large mammals presumably reduces the competition for
seeds. Though surprising, the finding that small animals will consume large seeds can be
consistent with the findings that small animals prefer small seeds. Preference of small seeds may
be determined by ease of detection, handling, and digestion, as well as competition. Large
mammals consume larger seeds, but in their absence small animals may fill their niche and
consume both food resources, thus boosting small animal abundances in hunted areas. This
additional food resource may be what allows small animal abundances to increase after the
removal of large animals by hunting (as predicted by Dirzo 2007). Seed consumption could also
be species specific, and more cafeteria experiments with small seed predators using a broad
variety of seed species could help determine which seeds are preferred, and which seeds may be
consumed only as populations approach carrying capacities and preferred food resources become
limited.
However, even if the consumption of large seeds in hunted sites is kept at similar levels
to intact sites through the spillover effect of small animal seed predators, not all large seeds may
benefit. Many seeds may be impossible for small seed predators to consume, such as large palm
fruits and other seeds with dense external coatings. In this manner plant communities in hunted
sites may become splintered compared with unhunted sites, with some large seeds remaining
consumed at similar rates as before, but other large seeds experiencing less seed predation, and
consequently less mortality and dispersal. Even those plant species whose large seeds are
consumed at similar rates may be affected by the differing methods of seed consumption in ways
that we do not yet understand. As noticed for the large palm species Iriartea, some seeds may
resist partial attacks from gnawing rodents and germinate regardless of past seed predation,
though this may only occur in areas where shell-cracking peccaries are not the dominant seed
predators. Looking at seed predation alone may not reveal the full story. By focusing further on
the ways in which seeds are consumed in hunted as compared to unhunted areas, no matter the
similarity in predation rates, we may better understand the complex relationships that may evolve
between seeds and seed predators under size-differential hunting conditions.
Acknowledgements
I would like to acknowledge my advisor Professor Rodolfo Dirzo for his mentorship in
conceiving and planning the project both before and during the field component, as well as his
invaluable advice and support for the analysis and writing stages.
I cannot thank Professor William Durham enough for granting me the opportunity to
study at Tambopata, and for his continual support of the project even when all else seemed lost. I
also wish to thank Claire Menke for her assistance in preparation before going into the field and
her support throughout the project’s duration, as well as her persistence in attaining permits, for
which I also owe Crissel Vargas.
I am greatly indebted to James Watanabe for his assistance with statistical design,
analysis, and interpretation of statistics results.
23
Loggins 2012
I also wish to thank Darwin, Gustavo, Carlos, and Daphne for their assistance in
identifying seeds and plants in the field as well as the identification of trail routes. I would like to
acknowledge the Stanford researchers, the varying members of the Macaw Research Team at
TRC, and the Rainforest Expeditions guides, staff, and boat-drivers for their enthusiasm for the
project, occasional assistance, and overall moral support.
Finally, this would not have been possible without the support of Kurt Hulle and
Rainforest Expeditions, as well as the assistance of the lodge managers: Liz and Agosto (TRC)
and Malu and Liz (Refugio).
Literature Cited
Beck H., 2006, “A Review of Peccary-Palm Interactions and Their Ecological Ramification
across the Neotropics,” Journal of Mammalogy, Vol. 87 Issue 3, pp. 519-530.
Dirzo R., 2001, “Plant-mammal interactions: Lessons for our understanding of nature, and
implications for biodiversity conservation.” In: M. C. Press, N. J. Huntly, and S. Levin
(Eds.), Ecology: Achievement and Challenge, Blackwell Science, Oxford, UK, pp. 319–
335.
Dirzo R. et. al., 2007, “Size-Related Differential Seed Predation in a Heavily Defaunated
Neotropical Rain Forest,” Biotropica, Vol. 39 Issue 3, pp. 355–362.
Dirzo R. and Miranda A., 1991, “Altered patterns of herbivory and diversity in the forest
understory: a case study of the possible consequences of contemporary defaunation,” In:
P.W. Price, T.M. Lewinsohn, G. W. Fernandes, and W.W. Benson (Eds.), Plant Animal
Interactions, Evolutionary Ecology in Tropical and Temperate Regions, Wiley, New
York, USA, pp. 273–287.
Emmons L. H. and Feer F., 1997, Neotropical Rainforest Mammals: a Field Guide, University of
Chicago Press, Chicago, USA.
Jansen P.A. et al., 2004, “Seed Mass And Mast Seeding Enhance Dispersal By a Neotropical
Scatter-Hoarding Rodent,” Ecological Monographs, vol. 74 Issue 4, pp. 569-589.
Mendoza E. and Dirzo R., 2007, “Seed-size variation determines interspecific differential
predation by mammals in a neotropical rain forest,” Oikos, Vol. 116, pp. 1841-1852.
Nuñez-Iturri G. et. al., 2008, “Hunting reduces recruitment of primate-dispersed trees in
Amazonian Peru,” Biological Conservation, Vol 141, pp. 1536–1546.
Nuñez-Iturri G. and Howe H., 2007, “Bushmeat and the Fate of Trees with Seeds Dispersed by
Large Primates in a Lowland Rain Forest in Western Amazonia,” Biotropica, Vol. 39
Issue 3, pp. 348-354.
Olmos F. et al., 1999, “Do Tapirs Steal Food from Palm Seed Predators or Give Them a Lift?,”
Biotropica, Vol. 31 Issue 2, pp. 375-379.
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Peres C.A., 1999, “General guidelines for standardizing line-transect surveys of tropical forest
primates,” Neotropical Primates, Vol. 7 Issue 1, pp. 11–16.
Redford K. H., 1992, “The Empty Forest,” BioScience, Vol. 42 No. 6, pp. 412-422.
Stoner K.E. et. al., 2007, “Hunting and Plant Community Dynamics in Tropical Forests: A
Synthesis and Future Directions,” Biotropica, Vol. 39 Issue 3, pp. 385-392.
Terborgh J. et. al., 1993, “Predation by vertebrates and invertebrates on the seeds of five canopy
tree species of an Amazonian forest,” Plant Ecology, Vol. 107-108, No. 1, pp. 375-386.
Treves L. et. al., 2003, “Wildlife Survival Beyond Park Boundaries: the Impact of Slash-andBurn Agriculture and Hunting on Mammals in Tambopata, Peru,” Conservation Biology,
Vol. 17 No. 4, pp. 1106–1117.
Wang B. C. et. al., 2007, “Hunting of Mammals Reduces Seed Removal and Dispersal of the
Afrotropical Tree Antrocaryon klaineanum (Anacardiaceae)”, Biotropica, Vol. 39 Issue
3, pp. 340-347.
Wright S. J. et. al., 2007, “The Plight of Large Animals in Tropical Forests and the
Consequences for Plant Regeneration,” Biotropica, Vol. 39 Issue 3, pp. 289–291.
Appendix
Average Seed Sizes
Seed Genus
Length (mm) Width (mm)
Trial 1 Iriartea
24.1
23.1
Chamaedorea
6.9
6.6
Trial 2 Pourouma (lg)
26.9
16.9
Pourouma (sm)
16.9
10.0
Trial 3 Iriartea
25.6
24.3
Euterpe
10.4
9.3
Trial 4 Clarisia
22.2
20.4
Brindaceae
15.0
13.6
Appendix A. Average length, width, and estimated volume for seeds used in trials.
Measurements were taken from a random sample of 50 seeds of each species.
List of All Animals Recorded in Transects and Camera Traps
Family
Mammals
Common Name
Scientific Name
Rat/Opossum
Multiple spp.
Average
Body
Size (kg)
~0.50
Transect
Sightings
Camera
Captures
T=11
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Loggins 2012
(multiple spp.)
Agoutidae
Atelidae
Agouti paca
Ateles belzebuth
Callitrichidae
Canidae
Paca
Spider Monkey
Saddle-backed
Tamarin
Short-eared Dog
Cebidae
Brown Capuchin
Cebus apella
Cebidae
Callicebus moloch
Cebidae
Duski Titi
Red Howler
Monkey
Cebidae
Squirrel Monkey
Saimiri sciureus
Cervidae
Dasypodidae
Dasypodidae
Red Brocket Deer
9-banded
Armadillo
Giant Armadillo
Dasyproctidae
Brown Agouti
Dasyproctidae
Green Acouchy
Common
Didelphidae
Opossum
Brazilian
Erethizontidae Porcupine
Felidae
Jaguar
Felidae
Saguinus fuscicollis
Atelocynus microtis
Alouatta seniculus
Mazama americana
Dasypus
novemcinctus
Priodontes maximus
Dasyprocta
variegata
Myoprocta pratti
Didelphis
marsupialis
Coendou prehensilis
9.00
8.15 T=5
T=5
0.387 R=2
7.75
T=11
3.10 R=8
T=3
1.13 R=2
T=4
6.40 R=2
T=6
0.94 R=3
36.0
4.50
30
T=7
4.10 R=7
T=1
1.00
1.088
R=1
T=5
R=13
T=3
R=2
T=1
T=56
R=6
T=1
R=1
T=6
R=1
T=1
4.25
94.50
Jaguarundi
Panthera onca
Herpailurus
yaguarondi
Felidae
Ocelot
Leopardus pardalis
11.25
Felidae
Puma
74.50
Leporidae
Mustelidae
Rabbit
Tayra
Puma concolor
Sylvilagus
brasiliensis
Eira barbara
Procyonidae
Nasua nasua
Sciuridae
Coatimundi
Amazon Red
Squirrel
Tapirdae
Brazilian Tapir
Tapirus terrestris
Sciurus spadiceus
R=1
T=19
R=15
6.75
0.825
4.85 T=2
T=1
5.10 R=2
T=5
0.625 R=2
238.50
T=3
R=19
R=2
T=9
R=7
T=3
R=3
T=11
R=1
T=1
R=1
T=3
R=4
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Loggins 2012
Tayassuidae
Tayassuidae
Birds
Cracidae
Cracidae
Cracidae
Eurypygidae
Psophiidae
Rallidae
Tinamidae
Tinamidae
Tinamidae
Collared Peccary
White-lipped
Peccary
Pecari tajacu
Crake
Pigeon
Piping Guan
Razor-billed
Currasow
Species unknown
Species unknown
Pipile cumanensis
Spix's Guan
Sunbittern
Pale-winged
Trumpeter
Grey-Necked
Wood Rail
Penelope jacquacu
Eurypyga helias
Tayassu pecari
Mitu tuberosum
Psophia leucoptera
T=3
26.0 R=3
T= 20
35.0 R=1
T=3
R=30
T=224
R=1
T=4
R=2
T=2
T=7
R=4
T=13
R=10
T=5
R=3
T=35
T=3
R=3
R=46
T=25
R=4
T=3
Aramides cajanea
Crypturellus
obsoletus
Tinamus major
Tinamus tao
Brown Tinamou
R=1
Great Tinamou
T=2
Grey Tinamou
T=3
Small Tinamou
T=6
T=1
Tinamidae
(multiple spp.)
Crypturellus spp.
R=8
R=2
Undulated
Crypturellus
Tinamidae
Tinamou
undulates
R=1
Appendix B. List of all animals seen in transects and camera trap surveys with family, species
name, and in which site the animal was recorded (T=TRC, R=Refugio) organized by survey type
(Transect or Camera). Average body sizes were used to classify animals in Small and Large
categories for data analyses (see Methods). Listings in bold were detected only in claylick
camera trapping sites and are not included in the analysis. Evidence of animals that were
present both at the claylick and at other sites are not added to sightings totals.
27