Of Mice and Men in Gabon: Changes in Rodent Communities
Associated with Logging and Hunting
By
Ian Markham
Dr. John R. Poulsen
Masters project submitted in partial fulfillment of the requirements for the
Master of Environmental Management degree in
The Nicholas School of the Environment of
Duke University
Executive Summary:
Worldwide tropical rainforests are under increasing pressure from timber extraction
and bushmeat hunting. Hunting and logging have been linked to long-term reductions in
carbon storage potential, loss of floristic diversity, and diminished regeneration of valued
timber species. Many studies have focused on the consequences of hunting on medium
and large bodied mammals and how shifts in their population affect forest dynamics. Far
less work has been carried out on how small mammal communities may be indirectly
affected by hunting and logging despite indications that their communities are likely altered
by anthropogenic disturbance. Because of their important role as seed predators, changes
in rodent populations could substantially alter long-term trajectories of vegetation
communities. In this study, I investigate whether rodent communities and seed predation in
the forests of Northeastern Gabon are altered by hunting and logging as well as changes
in forest structure potentially caused by these disturbances. I hypothesized that I would
find elevated abundance, biomass, and diversity of rodents as well as higher rates of
rodent seed predation in hunted and logged sites compared to protected sites. Moreover, I
hypothesized that changes in forest structure associated with disturbance, such as dense
understories and high densities of lianas, would accompany these shifts in the small
mammal community. Employing rodent trapping and seed predation trials at sites in and
around the Ivindo National Park and surrounding villages, I found no change in the
number, total biomass, or level of seed predation of rodents associated with human
impact. However, I detected a significant shift in rodent species composition from smallbodied species dominating protected sites to large-bodied species dominating disturbed
sites with hunting and logging. This change in the rodent community was associated with
decreased understory openness, increased downed wood basal area, and increased
numbers of lianas. This first documentation of changes in Central African rodent
communities associated with hunting and logging lays an important foundation to future
work determining the role of small mammals in long-term alterations in forest structure with
implications for both conservation and timber management.
Introduction:
Rising human populations and demand for natural resources place tropical rainforests
under increasing pressure from timber extraction and bushmeat hunting (Gardner et al.
2009; Laurance et al. 2012; Abernethy et al. 2013; Malhi et al. 2013; Rosin 2014). Though
selective logging can potentially extend the “conservation estate” while supporting
economic development (Johns 1985; Clark et al. 2009), the opening of once remote
locations to hunters can have severe ecological repercussions (Wright 2003; Laurance et
al. 2006; Harrison et al. 2013). “Defaunation”—the removal of animals through hunting—
has been linked to long-term reductions in plant biodiversity (Muller-landau 2007; Wilkie et
al. 2011; Galetti & Dirzo 2013; Kurten 2013), carbon storage potential (Brodie & Gibbs
2009b; Jansen et al. 2010; Poulsen et al. 2013), and the regeneration of valued timber
species (Fredericksen & Mostacedo 2000; Grogan 2006; Rosin 2014). However, the direct
and indirect drivers of these changes as well as their relative importance remain poorly
understood, particularly in Central Africa (Muller-Landau 2007; Vanthomme et al. 2010;
Rosin 2014).
Most studies of defaunation have focused on changes in processes such as
herbivory (Dirzo & Miranda 1991), seed predation (e.g Beckman & Muller-landau 2007), or
dispersal (e.g. Forget & Jansen 2007) caused by the removal of medium and large-bodied
mammals targeted by hunters (Abernethy et al. 2013). Changes in the small mammal
community as a result of hunting and logging could also modify ecological processes, but
have been greatly understudied (Kurten 2013). Release from competition or predation by
hunted mammals can lead to compensatory increases in rodent populations (Happold
1995; Terborgh et al. 2001; Wright 2003; Dirzo et al. 2007). Rodents have been shown to
increase in abundance and diversity in areas of dense regrowth associated with canopy
gaps and logging roads (Isabirye-Basuta & Kasenene 1987; Malcolm & Ray 2000). A
number of authors have suggested that the rodent community plays a role in seedling
recruitment equal to or greater than that of larger mammals through seed predation on the
forest floor (Terborgh et al. 1993; DeMattia et al. 2004; Paine & Beck 2007). Therefore,
changes in rodent populations generated by hunting and timber extraction could have
significant impacts on the long-term trajectories of plant communities particularly in forests
regenerating from selective logging (Rosin 2014).
Studies investigating the ecological consequences of altered rodent communities in
disturbed forests primarily in the Neotropics and Southeast Asia have shown mixed
results. It has been generally suggested that defaunation results in increased abundances
of rodents accompanied by elevated rates of seed predation for small-seeded species
(Dirzo et al. 2007; Blate et al. 2013). However, some studies have found lower rates of
seed predation in defaunated sites and no relationship between rodent seed predation and
seed size (Beckman & Muller-Landau 2007), while others have found a preference by
rodents for relatively large-seeded species (Paine & Beck 2007). Furthermore, some work
has suggested that rodent populations may reduce the overall seedling diversity in
defaunated forests by preferentially consuming seeds with certain traits such as small size
(Effiom et al. 2013; Galetti & Dirzo 2013). Meanwhile, others have indicated that rodents
play a critical role in maintaining or increasing seedling diversity by preferentially
consuming the most abundant species regardless of seed traits (Paine & Beck 2007).
Despite the concomitant pressure from bushmeat hunting and timber extraction on
African forests (Poulsen et al. 2011), even less work has been done to clarify the role of
small mammals in these systems (Kurten 2013). Studies in Kibale forest, Uganda initially
found higher abundances of rodents and elevated rates of seed predation in selectively
logged forest as compared with mature forests (Kasenene 1984; Isabirye-Basuta &
Kasenene 1987). Yet a decade later, a repeated study at the same site found the
relationship reversed with more rodents and higher rates of seed predation in the mature
forests (Lwanga 1994). Malcolm and Ray found both higher abundances and diversity of
rodents immediately adjacent to primary logging roads compared with intact forest, but no
significant differences associated with secondary roads or skid trails (2000). To my
knowledge, no study to date has examined explicitly the effects of both hunting and
logging on small mammal communities and seed predation in Central Africa.
In this study, I sought to quantify the effects of human disturbance on the
composition and abundance of small mammal communities as well as rates of seed
predation. Specifically, I ask: (a) do the structure of the small mammal community and
rates of seed predation vary across sites differentially impacted by hunting and logging?;
and, (b) what vegetative characteristics are associated with such changes? To answer
these questions, I trapped rodents, conducted seed predation trials, and measured
environmental variables in sites within and surrounding the Ivindo National Park in
northeastern Gabon. I hypothesized initially that areas that are heavily disturbed by human
activities outside of the park would have greater abundance, diversity, and biomass of
rodents compared with protected sites within the park. I further hypothesized that sites with
high rodent abundance would have higher rates of seed predation than sites with low
abundance. Lastly, I hypothesized that increases in rodent populations and seed predation
would be associated with vegetative characteristics indicative of human disturbance such
as increased densities of seedlings, lianas, and downed wood.
Methods:
I conducted this study between June 16 and August 19, 2014 in the Makokou-Ivindo
region of northeastern Gabon (0.5667°, 12.8667°). Dominated by lowland rainforest, the
area is comprised of the Ivindo National Park, the regional capitol of Makokou and
numerous small villages, as well as several timber concessions. Average annual rainfall is
approximately 1700 mm, with two wet seasons from September to December and March
to May (Hladik 1978). A concurrent research project established 25 transects for surveying
medium to large-bodied mammals. The transects were established to capture the
perceived range of hunting pressure, with one-third of the transects within six kilometers of
a village, one-third of the transect located between seven and twelve kilometers from a
village, and one-third on the transects located in the national park. From these, I selected
four transects within the park and four outside of the park within logging concessions that
ranged from 3 to 30 km from villages.
Rodent Trapping
At each site, I deployed fifty Sherman live traps (22.9 x 8.9 x 7.9 cm) for four nights,
representing a total trapping effort of two hundred trap nights per site. Traps were
distributed along five parallel transects radiating out from a central access trail with 250 m
between each transect and 20 m between each trap (Appendix, Figure 1). I baited the
traps from 3-4pm with two shelled peanuts, approximately a teaspoon of dry oatmeal, and
an African oil palm nut (Elaeis guineensis). I selected these baits after experimenting with
several possibilities and determining that these resulted in high rates of capture. Traps
were checked every morning between 10-11 am. I weighed all rodents captured in the
traps and took measurements of the total body length, hind foot, and tail. I also
photographed each individual to aid in species identification. Additionally the ear of each
captured rodent was marked with a spot of colored nail polish to distinguish recaptured
rodents from first-caught rodents. After measurements, rodents were released at their
point of capture.
To analyze the rodent capture data I compared the average number, total biomass,
average individual mass, and species richness of rodents captured at the logged and
hunted sites with protected sites using two-tailed, unpaired T-tests. I also conducted linear
regressions of the total biomass and average individual mass of captured rodents with
distance to the nearest village as a proxy for the intensity of hunting pressure. I conducted
a step-down non-metric multidimensional scaling (NMDS) of the data on species
composition and relative abundance at each site to examine differences in the rodent
community. I selected the number of dimensions for NMDS based on a natural break in the
reduction of stress levels. I then correlated the scores from the ordination with the lowest
stress level with the average values for the environmental variables collected at each trap
aggregated to the site level to examine which environmental variables might effect rodent
species composition. Lastly I used logistic regressions with binomial distributions to
determine which environmental variables best predicted success in rodent capture. The
best-fit model was selected based on reduction in AIC and likelihood ratio tests of nested
models.
Environmental Variables
To determine the forest characteristics associated with changes in the rodent
community, I collected data in a 10 m radius around each trap on forest structure, using a
methodology adapted from Lambert et al. (2006). At each trap, I collected environmental
data along a 10 m sampling line centered on the trap and perpendicular to the trap line. I
measured understory openness, sapling basal area, number of woody stems, number of
herbaceous stems, basal area of woody debris, canopy cover, large tree basal area, and
number of lianas. By holding a 2.5-m pole banded in 10 cm segments at the end of the
sampling line and counting the number of bands unobstructed by vegetation I generated
an understory openness score between 0 and 15 where 0 represented a relatively dense,
closed understory and 15 represented a relatively open understory. To estimate sapling
basal area, I measured the diameter at breast height (DBH) of all saplings (stems < 5 cm
DBH) within 1.25m of the sampling line. Numbers of woody understory stems (woody
stems <1 m tall) and herbaceous stems were estimated as the number of plants whose
leaves crossed the sampling line. To assess downed wood basal area, I measured the
diameter of all branches and stems >5cm diameter at the point of intersection with the
sampling line. Additionally, I measured the DBH for all trees >5cm DBH within a 10-m
radius of each trap station and counted the number of lianas coming in contact with each
tree.
I conducted a step-down NMDS of the environmental variables collected at each
trap aggregated to site level averages to examine potential separation between logged,
hunted sites and protected sites. I selected the number of dimensions for NMDS based on
a natural break in the reduction of stress levels with increasing dimensions. Additionally I
conducted two-tailed unpaired T-tests of the average scores for the measured
environmental variables aggregated to site level between protected sites and those with
logging and hunting. Lastly I conducted linear regressions of the average site level values
of the environmental variables with distance to the nearest village.
Seed Predation Trials
To examine differences between sites in seed predation attributable to insects,
rodents, and medium to large bodied mammals, I conducted exclosure experiments. I
established eight stations placed 30 m from the terminus of four of the trap lines, and
conducted seed predation trials for two nights at each site (Appendix, Figure 1). Each
feeding station consisted of three separate experimental treatments: a complete cage to
allow insect access only, a partial cage with openings (60 x 10 cm) cut in all four sides to
allow access by only rodents and insects, and an open treatment allowing unrestricted
access to all seed predators. I constructed cages (75 x 75 x 15 cm) with metal hardware
cloth and lawn staples. Each day between 3-4 pm, I placed thirty peanuts in the center of
each caging treatment in an area cleared of leaf litter. Each morning between 11 am-12pm
I counted the number of remaining seeds in the cages. I assumed that seeds missing from
the cage and its immediate vicinity (i.e. within 1m) were consumed by seed predators.
Additionally, I deployed 2 Bushnell HD 8MP Camera traps to record video at 2 different
stations for a total of 6 nights to examine the effectiveness of the exclosures in controlling
access to the different cage treatments.
To analyze the seed predation experiment I used logistic regressions with a
binomial distribution to compare differences in proportions of seed removed for each
combination of site type and cage type individually. I also used logistic regression models
with binomial distributions to determine which environmental variables best predicted
proportions of seed removed. The best-fit model was selected based on reduction in AIC
and likelihood ratio tests of the nested models.
Results:
Rodent Trapping—From the 1,600 total trap nights (200 trap nights at eight sites), I
captured a total of 98 rodents of 13 different species. The site within the Ivindo National
park closest to human habitation (referred to herein as “Ipassa”) yielded substantially
different results from all other transects in terms of rodent abundance and total biomass.
The capture rate of rodents at Ipassa was 366% higher than the mean capture rate for the
other sites, and this site had a significantly higher capture rate (one-sample t-test: t =-26.9,
df = 6, p < 0.001). Similarly, the total rodent biomass was 253% higher and significantly
greater than the other sites (t = -10.6, df = 6, p < 0.001). Moreover, this site was the only
location within the park to have shotgun shells found on regularly walked transects at a
rate equivalent to sites outside the park (Poulsen unpublished data). Standardizing by the
total distance walked on repeated visits to the 2.5-km transects at each site, shotgun shells
were encountered at a rate of 0.3 shells km-1 at Ipassa compared with an average of 0.23
shells km-1 at the four sites outside the park and no shells encountered at the three other
sites within the park. Therefore, Ipassa was neither protected like the other park sites, nor
logged like the four sites outside the national park. Thus, I removed this transect from the
following comparison of protected sites versus hunted, logged sites.
In the comparison of protected and hunted,logged sites, I found no significant
difference in the number (two-tailed unpaired t-test: t=0.041, df=3, p=0.969), total biomass
(t=-1.93, df=3, p=0.111), or species richness (t=-0.378, df=3, p=0.721) of captured rodents.
However, the total rodent biomass was negatively correlated with distance to the nearest
village (Pearson’s correlation: r =-0.796, df=5, p<0.05; Appendix, Figure 2). Moreover, the
average individual mass of rodents captured in logged, hunted sites was significantly
greater than those in protected sites, with rodents weighing on average 173% more than in
sites within the park (t=-4.38, df=3, p=0.007; Appendix, Figure 3). Likewise, the average
individual mass of rodents was negatively correlated with the distance to the nearest
village (r=-0.85, p= 0.015; Appendix, Figure 4). The step-down NMDS of the rodent
species and abundances led to the selection of two axes R2 = 0.816; Appendix, Figure 5).
The first axis had an R2 value of 0.12 and produced no separation in the rodent
communities in the disturbed sites from those of the protected sites. The second axis had
an R2 value of 0.69 and strongly separated the rodent communities in the disturbed sites
from those of the protected sites. The first NMS axis was correlated with a number of
common rodent species while the second was most strongly correlated with two species
that appeared frequently in hunted, logged sites. NMS scores were also significantly
correlated with site level averages for understory openness (r= 0.89, df = 5, p<0.05) and
lianas (r=-0.90, df = 5, p<0.05).
Environmental Data—The NMDS plot of the environmental variables averaged
across traps for each site illustrated some separation, but no clear clustering, of the
protected and disturbed sites (Appendix, Figure 6). The first principal component was
most correlated with understory openness (r= -0.477, p<0.05), canopy cover (r=-0.428,
p<0.05), and sapling basal area (r=-0.416, p<0.05), while the second was most correlated
with woody stem count (r=-0.611, p<0.05) and downed wood basal area (r=0.543, p<0.05).
Treated individually, hunted and logged sites had significantly lower openness scores
(t=3.97, df=3, p=0.011) and higher downed wood basal area (t=-2.51, df=3 p=0.05) than
protected sites; but the sites did not differ significantly in other of the other environmental
variables. Distance to nearest village was likewise correlated with average understory
openness score (r=0.848, df = 5, p=0.016) and inversely correlated with the average
number of lianas (r=-0.787, df = 5, p=0.035).
Rodent capture at the trap level was best predicted by woody understory stem
count and sapling basal area (Table 1). The odds of capturing a rodent increased by
approximately 4% with each additional woody understory seedling within 5 meters of the
trap. On the other hand, each additional sapling (woody stems with a DBH between .5-5
cm) within 5 meters of the trap decreased the odds of capturing a rodent by approximately
3%.
Table 1: Logistic regression model of environmental variables predicting rodent
capture
eβ
β
SE
Z
p
(Odds ratio)
Intercept
-3.66
0.35
-10.44
< 0.001
NA
Sapling basal area
-0.03
0.01
-2.34
0.02
0.97
Understory woody stems
0.04
0.01
3.88
<.0001
1.04
Residual Deviance: 473.5 on 1397 degrees of freedom
Seed predation trials— Using camera traps, several unidentifiable small rodents
were observed removing seeds from the partial cages and open treatments. Additionally,
an African giant pouched rat (Cricetomys gambianus) was seen removing seeds from the
open treatment, but did not attempt to enter the partial cages. The camera traps did not
capture any other medium to large-bodied mammals. While checking the experiment, I
observed ants (family Formicidae) and seed bugs (family Coreidae) removing seeds from
the complete cages on several occasions. Rates of seed removal across all three
treatments were approximately three times higher at Ipassa than any other site (Appendix,
Figure 7). For all other sites, seed removal rates were 7.9 seeds per night from open plots,
5.8 seed per night from partial cages, and 0.5 seeds per night from complete cages. There
was no significant difference in rates of seed removal between protected sites and
disturbed sites in the complete cages (residual deviance: 43.73, df=54, p=0.218) or partial
cages (residual deviance: 578.78, df=54, p=0.675). However, seed removal rates in open
plots were significantly higher in the hunted, logged sites compared to protected sites
(residual deviance 622.67, df=54,p<0.001) or with partial cages in protected (residual
deviance: 725.98, df=54, p<0.001) or with partial cages in hunted and logged sites
(residual deviance: 840.52, df=62, p<0.001).
For all open plots and partial cages, rates of seed removal were best predicted by
average understory openness, sapling basal area, canopy cover, downed wood basal
area, and liana counts for the five traps closest to the seed predation trial (Table 2). An
increase of understory openness score of one point decreases the odds of a seed being
removed by approximately 25%.
Table 2: Logistic regression model of environmental variables predicting proportion
of seeds removed from seed predation trials
eβ
β
SE
Z
p
(Odds ratio)
Intercept
-1.02
0.56
-1.81
0.07
NA
Understory Openness
-0.30
0.03
-9.472
<0.0001
0.74
Sapling basal area
-0.02
0.005
-3.65
<0.001
0.98
Canopy Cover
0.02
0.007
2.03
0.04
1.02
-0.0006
0.0001
-5.29
<0.0001
0.999
-0.02
0.003
-7.24
<0.0001
0.98
Downed Wood Basal Area
Lianas
Residual Deviance: 1565.3 on 163 degrees of freedom
Discussion:
In this first study of the effects of logging and hunting on rodent communities in
Central Africa, I found that disturbance likely shifts species composition from small-bodied
species in intact forest to large-bodied species in disturbed forest. Previous studies in the
Neotropics and East Africa found significant increases in the abundance and diversity of
rodents associated with defaunation (Asquith et al. 1997; Dirzo et al. 2007) and selective
logging (Kasenene 1984; Isabirye-Basuta & Kasenene 1987). By contrast, I found no
difference in the number of individuals or species richness in protected and disturbed sites.
However, I did find greater biomasses of rodents with greater levels of human disturbance,
with the mass of rodents decreasing with distance from villages (Appendix, Figure 2).
Indeed, using proximity to villages as a proxy for the degree of human influence, my
results suggest that the greater the intensity of hunting and logging the more the species
composition shifts towards large-bodied species (Appendix, Figure 4). Because the
sampling sites were at least 3 km from the nearest village, these changes are unlikely to
be driven by rodents using the villages as habitat and food sources, but instead by the
indirect effects of hunting and selective logging that are likely more severe near human
inhabitations.
Interestingly, Ipassa, the only site with significant hunting but no logging, did not
have a rodent community intermediate in the spectrum in terms of species composition
and rodent biomass between the relatively pristine sites in the park and the heavily
impacted sites outside the park. Rather this site appears to have a hyper-abundance of
small bodied rodents with none of the larger rat species found particularly at the hunted,
logged sites, suggesting that hunting alone may produce quite different effects than the
combination of hunting and logging. Disruption of the forest structure associated with
logging and forest clearing likely creates an environment favorable to large-bodied
species. By contrast, hunting alone may result in higher densities of rodents without a
change in species composition. Work on medium to large bodied mammals in Central
Africa has suggested that the decoupled effects of hunting and logging can differ
substantially from their combined effect for various animal guilds (Poulsen et al. 2011). It
may be that hunting alone releases rodents from competition for food resources or
predation from larger mammals causing increases in the relative abundance of the rodent
community (Dirzo et al. 2007); whereas logging might substantially change the forest
structure, thus shifting the species composition of the small mammal community to have a
larger proportion of large-bodied rats. Comparison of selectively logged sites with intact
mature forest in Uganda have shown long-term shifts in rodent species composition
associated with disturbance (Isabirye-Basuta & Kasenene 1987; Lwanga 1994). Moreover,
study on the impact of logging roads in Gabon documented changes in rodent species
composition beside primary logging roads that were not detected within intact forests
(Malcolm & Ray 2000). However, these differences in rodent communities were not
detected along secondary logging routes or skid trails, whereas my study documented
significant changes in species composition hundreds of meters and even kilometers from
primary logging roads. Future work should attempt to separate the effect of hunting and
logging on small mammal communities with greater replication of hunted sites without
logging, and though often difficult to find, sites with logging but no hunting. Such research
may prove vital for understanding the relative importance of the factors driving long-term
losses of forest biodiversity, carbon storage potential, and the regeneration of timber
species (Brodie 2009; Poulsen et al. 2013; Rosin 2014).
The distribution of sites within the study area, with hunted and logged sites
predominately to the north and the protected sites to the south, limits the inferences that
can be drawn from this study. However, examination of the results from the environmental
sampling suggests that the observed differences in the rodent community are more likely
linked to human disturbance than environmental variation related to geography. The lack
of clustering in the NMDS suggests that protected and logged, hunted sites do not
separate along environmental axes suggesting latitudinal differences alone are unlikely to
be driving the observed differences in the rodent community (Appendix, Figure 6). Those
few environmental variables that were different between the two forest types tended to be
associated with human disturbance. For example, the logged, hunted sites had dense,
closed understories as well as large numbers of lianas and fallen logs. Selective logging
can lead to an increase in the density of lianas as well as high concentrations of downed
wood, resulting in dense closed understories (Schnitzer & Bongers 2002). Moreover,
defaunation has been linked to increased liana abundance by reducing competition
between the many animal-dispersed tree species and wind-dispersed lianas (Stoner et al.
2007; Wright et al. 2007). Interestingly, I did not specifically detect increases in seedlings
or saplings associated with hunting and logging, though a number of authors have
suggested this may result either from opportunistic growth of plants in gaps opened by
logging or through reduction of herbivores and seed predators from hunting (Galetti &
Dirzo 2013; Kurten 2013). However, the significantly lower understory openness scores
found in logged, hunted sites may have captured some of the differences in seedling and
sapling density along with differences in the density of lianas.
Rodent seed predation may play an important role in limiting plant recruitment in
these forests (Appendix, Figure 7). My finding that rates of seed removal in partial cages
were 72% of the rates in open plots suggests that rodents are responsible for the majority
of seeds removed in this experiment. Camera trap observations provide further, albeit
limited, support of this conclusion. Studies elsewhere have similarly found that small
mammals are the primary agents of seed predation on the forest floor, and therefore likely
play a major role in determining the vegetative characteristics of the forest (DeMattias et al
2004, Terborgh 1993, Paine and Beck 1997).
Although small mammals preyed on a high proportion of seeds, I found no direct
evidence that logging and hunting modified the rates of seed predation by small rodents
(Appendix, Figure 7). The similar number of peanuts removed in partial cages between
protected and disturbed sites suggests that small mammals remove generally palatable
seeds at similar rates between these sites. However, it should be noted that peanuts were
chosen for these assays for their attractiveness to seed predators as a comparatively
large, energetically rich food source without chemical defense (following Lambert et al.
2006). Changes in the species composition of the rodent community without an
accompanying shift in abundance or biomass would seem unlikely to produce a substantial
difference in removal rates for a highly apparent and widely appealing seed. However,
rodent species have been shown to vary considerably in their seed preferences when
presented seed options ranging in size, nutritional content, and structural or chemical
defense (Vieira et al. 2003, 2006; Blate et al. 2013). The observed differences in the
rodent species composition between protected sites and logged, hunted sites may well
drive differential rates of seed predation when a wider range of seeds are available.
Indeed changes in rodent species composition through time without significant changes in
overall abundance or biomass have been linked to significant differences in seed predation
when comparing multiple species of seeds (Kasenene 1984; DeMattia et al. 2004).
Moreover, DeMattia et al. (2004) observed that as rodent communities shifted in size from
small-bodied to large-bodied rodents, seed predation of some species decreased while
scatter-hoarding increased.
The substantially higher rates of seed removal in open plots within hunted and
logged sites, though consistent with hypotheses on the increased seed predation
associated with disturbance, merit further investigation. Increases in seed predation in
sites with high levels of human impact have been found by a number of other studies but
are typically attributed to rodents (Isabirye-Basuta & Kasenene 1987; Dirzo et al. 2007).
The impacts of hunting and logging either independently or concurrently have been shown
to have complex effects on animal communities in African forests, causing some species
to decline while others increase in abundance, even those targeted directly by hunters
(Poulsen et al. 2011; Effiom et al. 2013). It remains possible that species such as squirrels
or frugivorous birds, which have been shown to increase at times under the conditions
brought about by logging and hunting, are responsible for these increases in rates of
observed seed predation (Poulsen et al. 2011). However, large rodents such as the brushtailed porcupine (Atherurus africanus) or the African giant pouched rat (Cricetomys
gambianus), which have been known to have higher abundance in disturbed areas despite
being targeted by hunters, may also be responsible for the observed increases in seed
predation (Effiom et al. 2013, Laurence et al. 2008). Because of their large size, full-grown
adults of either the brush-tailed porcupine or the African giant pouched rat could not be
captured by my Sherman traps, nor would they likely be able to enter the partial cages.
Indeed, the single African giant pouched rat observed on the camera traps consumed all of
the peanuts at the open plot and approached, but did not enter, the partial cage. If these
species were more abundant at disturbed sites, as was observed by Effiom et al (2013) in
Nigerian forests and Laurence et al (2008) in Southern Gabon, they could well contribute
to the difference in seed predation observed in the open plots at sites outside the park.
However, I captured only a single juvenile of the African pouched rat, which already was
the largest of any of the captured rodents. Additional rodent trapping in this region should
include larger traps to capture these potentially important large rodent seed predators.
Lastly, the anomalous results from Ipassa, the single hunted site not affected by
logging, highlights the need for further disentangling hunting from logging. Ipassa had
rodent abundances three times higher, rodent biomass two times higher, and seed
removal rates three times higher than the other sites (Appendix, Figure 7). Interestingly,
the species composition at Ipassa more closely resembled that of the protected sites
(Appendix, Figure 5). These results suggest that hunting pressure may produce
substantially different consequences for the small mammal community than the
combination of hunting and logging. However, without additional hunted-only sites, it
remains difficult to separate the impacts of hunting and logging.
The shift in rodent species composition from small-bodied rodents in protected sites
to larger-bodied rodents in sites with hunting and logging documented in this study
represents an important step in understanding anthropogenic changes to Central African
forests. Given the tendency for small mammal populations to fluctuate, further confirmation
of this phenomenon should be carried out with trapping over a longer duration of time
ideally spanning multiple seasons. Nevertheless this initial finding indicates a greater need
to investigate the extent to which changes in forest structure caused by hunting and
logging may be altering small mammal communities and the extent to which small
mammal communities may be contributing to long-term changes in forest diversity, carbon
storage, and the regeneration of timber species.
Acknowledgements:
I would like to thank Dr. John Poulsen for his support and mentorship on this
project, and Cooper Rosin for providing valuable guidance. This work was made possible
by the generous support of the Nicholas School International Internship Fund, the
Kuzmier-Lee-Nikitine Endowment, and the Frank H. And Eva B.Buck Foundation.
Fieldwork was made possible thanks to the Agence Nationale des Parcs Natiounaux
(ANPN) of Gabon, particularly the staff and eco guards of the Ipassa Field Station in the
Ivindo National Park. I would also like to give special thanks to my guide, Roger Koue, for
his hard work and dedication.
200m
Appendix
1km
Figure 1: Diagram of the study design, depicting the configuration of rodent traps and seed exclosure experiments at
each site. Filled squares represent rodent traps. Unfilled squares represent closed cages, dotted squares represent
partial cages and collections of four spots represent open treatments. Diagram not to scale. Distances correspond
with dotted lines.
Figure 1: Total rodent biomass captured at each site regressed against distance to the nearest village (R2=0.58,
df=5, p=0.031). Red circles represent logged and hunted sites, green circles represent protected sites, and the
unfilled circle represents Ipassa, the site with hunting but no logging.
Figure 2: The average individual body size of rodents in protected sites was significantly lower than the logged
hunted sites (t=-4.38, df=3, p=0.007). The unfilled circle represents the value for Ipassa.
Figure 3: Average individual rodent mass at each site regressed against distance to the nearest village
(R2=.72, df=5, p=0.032). Red circles represent logged and hunted sites, green circles represent protected
sites, and the unfilled circle represents Ipassa, the site with hunting but no logging
Figure 4: Biplot of NMDS ordination of rodent species and relative abundance at each site. Red circles
represent logged and hunted sites, green circles represent protected sites, and the unfilled circle represents
Ipassa, the site with hunting but no logging. Arrows depict environmental variables with a significant
correlation (p<0.05) with the ordination scores. Ovals have been added to highlight separation into distinct
rodent communities within the park (green) and logged and hunted sites (red)
Figure 6: Biplot of NMDS ordination of average values of environmental variables collected at the traps at each
site. Red circles represent logged and hunted sites, green circles represent protected sites, and the unfilled circle
represents Ipassa, the site with hunting but no logging. NMDS axis 1 is most correlated with understory openness,
canopy cover, and sapling basal area. NMDS axis 2 is most correlated with woody stem counts and downed wood
basal area. No clear clustering occurs by site type.
**
*
*
*
Figure 7: Average number of peanuts removed from seed predation experimental treatments at protected sites
(green) and sites with hunting and logging (red). Complete, closed cages give access only to insects. Partial cages give
access to insects and rodents. Open treatments give access to insects, rodents and larger animals. Error bars are
standard error. Significant differences are shown with asterisks (GLMs binomial distribution p<0.001)
Works Cited
1. Abernethy, K., Coad, L., Taylor, G., Lee, M. & Maisels, F. (2013). Extent and ecological
consequences of hunting in Central African rainforests in the twenty-first century. … R. ….
2. Asquith, N.M., Wright, S.J. & Clauss, M.J. (1997). Does mammal community
composition control recruitment in neotropical forests? Evidence from Panama. Ecology,
78, 941–946.
3. Beckman, N.G. & Muller-landau, H.C. (2007). Differential Effects of Hunting on PreDispersal Seed Predation and Primary and Secondary Seed Removal of Two Neotropical
Tree Species, 39, 328–339.
4. Beckman, N.G. & Muller-Landau, H.C. (2007). Differential effects of hunting on pre
dispersal seed predation and primary and secondary seed removal of two neotropical tree
species. Biotropica, 39, 328–339.
5. Blate, G.M., Peart, D.R., Leighton, M. & Blate, M. (2013). Post-dispersal predation on
isolated seeds : a comparative study of 40 tree species in a Southeast Asian rainforest, 82,
522–538.
6. Brodie, J. & Gibbs, H. (2009a). Bushmeat hunting as climate threat. Sci. (New York,
NY), 326, 364.
7. Brodie, J.F. & Gibbs, H.K. (2009b). Bushmeat hunting as climate threat. Science.
8. Clark, C.J., Poulsen, J.R., Malonga, R. & Elkan, P.W. (2009). Logging concessions can
extend the conservation estate for Central African tropical forests. Conserv. Biol., 23,
1281–93.
9. DeMattia, E.A., Curran, L.M., Rathcke, B.J., Biology, E. & Arbor, A. (2004). Effects of
small rodents and large mammals on Neotropical seeds. Ecology, 85, 2161–2170.
10. Dirzo, R., Mendoza, E. & Ort, P. (2007). Size-Related Differential Seed Predation in a
Heavily Defaunated Neotropical Rain Forest, 39, 355–362.
11. Effiom, E.O., Nuñez-Iturri, G., Smith, H.G., Ottosson, U. & Olsson, O. (2013).
Bushmeat hunting changes regeneration of African rainforests. Proc. Biol. Sci., 280,
20130246.
12. Forget, P.-M. & Jansen, P. a. (2007). Hunting Increases Dispersal Limitation in the
Tree Carapa procera, a Nontimber Forest Product. Conserv. Biol., 21, 106–113.
13. Fredericksen, T.S. & Mostacedo, B. (2000). Regeneration of timber species following
selection logging in a Bolivian tropical dry forest, 131, 47–55.
14. Galetti, M. & Dirzo, R. (2013). Ecological and evolutionary consequences of living in a
defaunated world. Biol. Conserv., 163, 1–6.
15. Gardner, T. a., Barlow, J., Chazdon, R., Ewers, R.M., Harvey, C. a., Peres, C. a., et al.
(2009). Prospects for tropical forest biodiversity in a human-modified world. Ecol. Lett., 12,
561–582.
16. Grogan, J. (2006). Factors Limiting Post-logging Seedling Regeneration by Big-leaf
Mahogany ( Swietenia macrophylla ) in Southeastern Amazonia , Brazil , and Implications
for Sustainable Management 1, 38, 219–228.
17. Happold, D.C.D. (1995). The interactions between humans and mammals in Africa in
relation to conservation: a review. Biodivers. Conserv.
18. Harrison, R.D., Tan, S., Plotkin, J.B., Slik, F., Detto, M., Brenes, T., et al. (2013).
Consequences of defaunation for a tropical tree community. Ecol. Lett., 16, 687–94.
19. Hladik, A. (1978). Phenology of Leaf Production in Rain Forest of Gabon: Distribution
and Composition of Food for Folivores. Ecol. Arboreal Folivores, 51–71.
20. Isabirye-Basuta, G. & Kasenene, J. (1987). Small Rodent Populations in Selectively
Felled and Mature Tracts of Kibale Forest, Uganda. Biotropica, 19, 260–266.
21.Jansen, P.A., Muller-Landau, H.C. & Wright, S.J. (2010). Bushmeat hunting and
climate: an indirect link. Science.
22. Johns, A. (1985). Selective Logging and Wildlife Conservation in Tropical Rain-Forest :
Problems and Recommendations. Biol. Conserv., 31, 355–375.
23. Kasenene, J. (1984). The influence of selective logging on rodent populations and the
regeneration of selected tree species in the Kibale Forest, Uganda. Trop. Ecol.
24. Kurten, E.L. (2013). Cascading effects of contemporaneous defaunation on tropical
forest communities. Biol. Conserv., 163, 22–32.
25. Lambert, T., Malcolm, J. & Zimmerman, Bl. pd. (2006). Amazonian small mammal
abundances in relation to habitat structure and resource abundance. J. Mammal., 87, 766–
776.
26. Laurance, W.F., Alonso, A., Lee, M.E. & Campbell, P. (2006). Challenges for forest
conservation in Gabon, Central Africa. Futures, 38, 454–470.
27. Laurance, W.F., Useche, D.C., Rendeiro, J., Kalka, M., Bradshaw, C.J. a, Sloan, S.P.,
et al. (2012). Averting biodiversity collapse in tropical forest protected areas. Nature, 489,
290–4.
28. Lwanga, J.S. (1994). The role of seed and seedling predators, and browsers on the
regeneration of two forest canopy species (Mimusops bagshawei and Strombosia
scheffleri in Kibale Forest Reserve, Uganda).
29. Malcolm, J. & Ray, J. (2000). Influence of Timber Extraction Routes on Central African
Small-Mammal Communities, Forest Structure, and Tree Diversity. Conserv. Biol., 14,
1623–1638.
30. Malhi, Y., Adu-Bredu, S., Asare, R. a, Lewis, S.L. & Mayaux, P. (2013). African
rainforests: past, present and future. Philos. Trans. R. Soc. Lond. B. Biol. Sci., 368,
20120312.
31. Muller-landau, H.C. (2007). Predicting the Long-Term Effects of Hunting on Plant
Species Composition and Diversity in Tropical Forests, 39, 372–384.
32. Muller-Landau, H.C. (2007). Predicting the Long-Term Effects of Hunting on Plant
Species Composition and Diversity in Tropical Forests. Biotropica, 39, 372–384.
33. Paine, C.E.T. & Beck, H. (2007). Seed predation by neotropical rain forest mammals
increases diversity in seedling recruitment. Ecology, 88, 3076–3087.
34. Poulsen, J.R. (2009). Logging and hunting alter patterns of seed dispersal and
seedling recruitment in an afrotropical forest.
35. Poulsen, J.R., Clark, C.J. & Bolker, B.M. (2011). Decoupling the effects of logging and
hunting on an afrotropical animal community. Ecol. Appl., 21, 1819–36.
36. Poulsen, J.R., Clark, C.J. & Palmer, T.M. (2013). Ecological erosion of an Afrotropical
forest and potential consequences for tree recruitment and forest biomass. Biol. Conserv.,
163, 122–130.
37. Rosin, C. (2014). Does hunting threaten timber regeneration in selectively logged
tropical forests ? For. Ecol. Manage., 331, 153–164.
38. Schnitzer, S. & Bongers, F. (2002). The ecology of lianas and their role in forests.
Trends Ecol. Evol., 17.
39. Stoner, K.E., Vulinec, K., Wright, S.J. & Peres, C. a. (2007). Hunting and Plant
Community Dynamics in Tropical Forests: A Synthesis and Future Directions. Biotropica,
39, 385–392.
40. Terborgh, J., Lopez, L., Nuñez, P., Rao, M., Shahabuddin, G., Orihuela, G., et al.
(2001). Ecological meltdown in predator-free forest fragments. Science, 294, 1923–6.
41. Terborgh, J., Losos, E., Riley, M. & Riley, M. (1993). Predation by vertebrates and
invertebrates on the seeds of five canopy tree species of an Amazonian forest. Frugivory
seed dispersal …, 107, 375–386.
42. Vanthomme, H., Bellé, B. & Forget, P. (2010). Bushmeat hunting alters recruitment of
large-seeded plant species in Central Africa. Biotropica, 42, 672–679.
43. Vieira, E.M., Pizo, M.A. & Izar, P. (2003). Fruit and seed exploitation by small rodents
of the Brazilian Atlantic forest. Methods, 67, 1–7.
44. Vieira, M., Paise, G. & Machado, P.H.D. (2006). Feeding of small ro dents on seeds
and fruits : a com par a tive anal y sis of three spe cies of ro dents of the Araucaria for est ,
south ern Brazil, 51, 311–318.
45. Wilkie, D.S., Bennett, E.L., Peres, C. a & Cunningham, A. a. (2011). The empty forest
revisited. Ann. N. Y. Acad. Sci., 1223, 120–8.
46. Wright, S.J. (2003). The myriad consequences of hunting for vertebrates and plants in
tropical forests. Perspect. Plant Ecol. Evol. Syst., 6, 73–86.
47. Wright, S.J., Hernandéz, A. & Condit, R. (2007). The Bushmeat Harvest Alters
Seedling Banks by Favoring Lianas, Large Seeds, and Seeds Dispersed by Bats, Birds,
and Wind. Biotropica, 39, 363–371.