Download Effects of resource availability and social aggregation on the species

Oikos 120: 1427–1433, 2011
doi: 10.1111/j.1600–0706.2011.19260.x
© 2011 The Authors. Oikos © 2011 Nordic Society Oikos
Subject Editor: Hamish McCallum. Accepted 3 February 2011
Effects of resource availability and social aggregation on the species
richness of raccoon endoparasite infracommunities
Ryan J. Monello and Matthew E. Gompper
R. J. Monello ([email protected]), National Park Service, Biological Resource Management Division, 1201 Oak Ridge Drive, Fort Collins,
CO 80525, USA. – M.E. Gompper, Dept of Fisheries and Wildlife Sciences, Univ. of Missouri, Columbia, MO 65203, USA.
Within populations the contact rate of hosts and infectious parasites is mediated by the interactions of resource availability,
host density, and host behavior. Fluctuations in host density can result in the loss or extinction of a parasite population as
contact rates between parasites and susceptible individuals drop below thresholds of parasite population persistence. Less
understood is how changes in resources and the behavioral ecology of host populations affect parasites. We used food provisioning to experimentally assess the effects of resource availability and of inducing host aggregation on the endoparasite
community of free-ranging raccoons. Twelve independent raccoon populations were subjected to differential resource provisioning for two years: a clumped food distribution to aggregate hosts (n ⫽ 5 populations), a dispersed food distribution
to add food without aggregating hosts (n ⫽ 3), and a no food treatment (n ⫽ 4). Remote cameras indicated that aggregation sizes were three to four times greater in aggregated versus non-aggregated populations. We considered endoparasites
with direct and indirect life cycles separately and determined the best-fit models of parasite species richness in relation to
host aggregation, food supplements, and host age and sex. Social aggregation had a negligible impact on the species richness of directly or indirectly transmitted parasites. However, food additions decreased the number of indirectly transmitted
parasite species by 35% in the oldest age classes. These results suggest that while resource availability can influence the
transmission of indirectly transmitted parasites, an examination of additional factors will be necessary to understand the
role of host contact and factors that shape the community structure of endoparasites in natural environments.
Parasite transmission within animal populations depends on
the rate at which hosts come into contact with each other or
the infectious stage of a parasite. Contact rates are mediated
by resource availability and population density (Anderson
et al. 1981), but relationships between host sociality, food
resources, and parasite burden are difficult to quantify in
free-ranging populations and are continually influenced by
a wide range of factors, including host and parasite behavior,
the ecological constraints and life history of each parasite,
host demographics, and environmental conditions (Anderson and May 1991, Møller et al. 1993, Krasnov et al. 2002,
Wilson et al. 2002). Attempts to address this complexity have
resulted in a large number of comparative studies that assess
host–parasite relationships between different host species. In
contrast, few studies have examined the role of host or ecosystem attributes on parasite species richness within species
(the parasite component community and infracommunity).
There is a need to better understand this dynamic relationship, as generalized cross-species trends do not adequately
describe and can contradict the known ecological relationships that may occur within a host population (Poulin 1997,
Poulin and Mouillot 2004). In particular, consistent patterns
of endoparasite species richness among mammal species have
been shown to depend on the scale of study and ecology of
individual hosts (Bordes and Morand 2008). Surprisingly,
few studies have employed experiments to determine the
intrinsic ecological relationships between a mammalian host
and their endoparasite species richness in a natural setting.
Comparative studies have found that host traits such as
longevity, size, social organization, density and life history
can all correlate with parasite component community richness (Gregory 1997, Morand et al. 2000, Stanko et al. 2002,
Nunn et al. 2003, Ezenwa et al. 2006). For example, among
mammals, host density is positively correlated with parasite
abundance and prevalence across a range of taxa (Arneberg
et al. 1998). This makes intuitive sense as rates of contact
frequently increase with density and result in greater parasite transmission. While such findings are important, they
primarily inform our understanding of stable host–parasite
relationships across multiple species and are limited in their
ability to predict how alterations in the behavioral ecology of
individual hosts will affect parasite communities in a particular ecosystem. For example, when examining a single host
species within a site or region, one is asking a fundamentally different question – do alterations in contact or density
within a particular species alter the parasite species richness
of a population? Furthermore, how does any such relationship compare in importance to other host characteristics that
may also influence the species richness of parasites, such as
host sex or age? Such assessments are essential to understand
1427
the predominant factors that control parasite transmission
and parasite species richness among host populations in their
natural settings.
Here we examine factors that influenced endoparasite
species richness of raccoons Procyon lotor. We considered
two measures of species richness by evaluating parasites with
direct and indirect life cycles separately. Those with direct
life cycles are transmitted directly between raccoons via close
contact or contact with feces or fomites. Some directly transmitted parasites can also be transmitted indirectly through
a different host, although this is not required. Parasites with
indirect life cycles must infect at least one additional host
(often a prey species such as an insect or gastropod) before
they can infect raccoons and complete their development and
reproduction. Previous studies have observed only endoparasites with direct life cycles to correlate with, or respond to,
changes in the behavioral ecology or density of hosts (Altizer
et al. 2003, Wright and Gompper 2005). Indirect parasites
are generally not thought to be as sensitive to alterations or
behavioral differences in host ecology because they are constrained by an additional intermediate host.
Our objective was to experimentally assess the effects of
food resources and social aggregation on endoparasite prevalence and species richness. The experimental design consisted
of a clumped food distribution to aggregate hosts, a dispersed
food distribution that added the same amount of food but
did not aggregate hosts, and a no food treatment. Food additions and aggregation were predicted to affect parasites with
direct and indirect life cycles in a different manner. Many
comparative studies have suggested that the diversity of food
intake, food resources, and differing levels of social contact
can impact the prevalence and abundance of parasites (Kuris
et al. 1980, Pacala and Dobson 1988, Poulin 1995, Gregory
1997, Morand et al. 2000, Altizer et al. 2003, Nunn et al.
2003, Ezenwa et al. 2006). We hypothesized that parasite
species richness of directly transmitted species would increase
in aggregation treatments due to higher contact between
hosts and infected feces near areas of aggregation. However,
we expected the number of indirectly transmitted species to
decline in aggregated treatments, and in food-augmented
populations, because it would decrease the need to search
for other food sources, including alternative hosts that are
necessary to obtain indirectly transmitted species.
Material and methods
Study design
Raccoons were sampled from March to November in 2006
and 2007 at 12 sites in central Missouri, USA. All sites were
located on forested state, federal, or university conservation
or research areas within 60 km of Columbia, Missouri. Sites
consisted of second growth oak Quercus spp. and hickory
Carya spp.) forest with a maple Acer spp. and cedar Juniperus
virginiana understory. Sites were considered independent of
each other; over the course of four years we marked ⬎ 700
individuals and none were recaptured at any of the other
study sites (Monello and Gompper 2010).
Sites were assigned to differential resource provisions for
two years: a clumped food pile to aggregate hosts (n ⫽ 5
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aggregated populations), a dispersed food distribution to
control for the effects of food without aggregating hosts
(n ⫽ 3 control with food), and a no food treatment (n ⫽ 4
control without food). Treatments were assigned randomly
to sites within geographically defined site subsets that were
used to assure that treatments were interspersed. The aggregated sites were maintained by placing 35 kg of dried dog
food in the same location each week. Control with food
sites were provisioned by placing food in multiple 0.25 kg
piles (∼140 week-1) that were randomly located throughout
each 4 km2 study site. All provisions were maintained from
January through September in 2006 and 2007.
Remote film cameras were used to monitor feeding
station use, rates of contact, and raccoon aggregation sizes
in treatment and control sites with and without food. One
camera was maintained from January to August at each permanent feeding station in aggregated sites. Five cameras were
maintained in control sites with and without food for 10–15
days during both the spring and summer. Cameras were
placed in front of a small pile of food (control with food)
or bait (control without food) and relocated every five days.
Aggregation size was recorded as the maximum number of
raccoons, excluding cubs, observed per night at each site. We
assigned a categorical variable for short-term contact while
at the feeding station of 0 (no contact within the ca 16m2
camera range) or 1 (contact with conspecifics within the
range) (Gompper and Wright 2005). Instantaneous contact
rates were assessed for each site by quantifying the percent of
camera days with photos that had ⬎ two raccoons, excluding cubs.
We calculated population density of each site by estimating adult population size in 2007 using closed population models in Popan-5 (Arnason and Schwarz 1999), and
divided these values by the effective trapping area (Kenward
1985). We estimated the effective trapping area by multiplying the linear length of the trapline by a buffer of ¾ of
the annual home range of raccoons (Kenward 1985) from a
subset of the sites in this study (Wehtje and Gompper 2011).
We used the residuals from a linear regression of body mass
on body size to assess the relative body condition of each
individual (Schulte-Hostedde et al. 2005), with higher values indicating better body condition.
Raccoons were trapped for ⬎10 days at each site three
times per year between March and November. Tomahawk
traps were baited with mackerel and checked daily. Raccoons
were immobilized with ketamine hydrochloride and xylazine
(Evans 2002), tagged with metal ear tags, weighed, sexed
and aged by body size, genital morphology, and tooth eruption and wear (Grau et al. 1970). Animals were categorized
into one of four age classes; I ⫽ 5–14 months, II ⫽ 15–38
months, III ⫽ 39–57 months, or IV ⫽ over 58 months. We
rarely detected endoparasites in cubs (⬍5 months; Monello
2009) and they were not included in our analyses.
Fresh feces was collected from within or below traps,
homogenized, and stored in 10% formalin. Endoparasite
ova and oocysts were identified by standard fecal floatation
procedures using sugar and zinc sulfate centrifugation techniques (Bowman 1999). Only one sample per animal was
included in this study. When multiple samples of an individual were obtained due to recapture events, one sample was
randomly selected for analysis. Although using additional
samples may give a more accurate parasite species richness
index for an animal, we did not include them because it
would have resulted in a disproportionately larger sampling
effort for animals that were recaptured. We assumed that by
using one sample per individual and sampling each area with
equal effort across seasons, the likelihood of finding parasites
in fecal samples would be equal across all individuals, sites,
and treatments.
Model selection
We used information-theoretic model selection to evaluate
the ability of treatments and host characteristics to explain
the species richness of directly and indirectly transmitted
parasites. To assess the importance of these factors on parasite infracommunities, we developed 13 candidate models
that included aggregation, food supplementation, year, and
host age and sex. The factors food and aggregation were considered separately to compare their relative importance. Year
was only included when significant model effects were found
(p ⬍ 0.05). Factor selection and a priori model formulation
for experimental sites was based on previous findings from
single parasite species and comparative studies of parasite
species richness (Wilson et al. 2002), as well as data that
indicated host age and sex to be important to the parasite
burden of free-ranging raccoons (Monello and Gompper
2007, 2009, 2010).
We used generalized linear models with a normal distribution for model selection; previous work on this data indicated
that endoparasite species richness was normally distributed
for parasites with both direct (skewness ⫽ 0.155 ⫾ 0.179;
kurtosis ⫽ –0.493 ⫾ 0.356) and indirect life cycles (skewness ⫽ 0.345 ⫾ 0.179; kurtosis ⫽ –0.029 ⫾ 0.356)
(Monello 2009). We conducted a goodness-of-fit test to
assess the ability of model factors to explain endoparasite
species richness by comparing the global model against the
intercept-only model (Franklin et al. 2000). We proceeded
with model selection procedures only if global models provided a better fit than intercept-only models (α ⫽ 0.05).
We calculated Akaike’s information criterion (corrected for
small sample size; AICc) and ranked the models based on
differences between the best approximating model and all
other models (ΔAICc) in the candidate set. Models with a
ΔAICc value ⱕ2 of the best-fitting model were considered
to have empirical support as a best-fitting model. To better
assess model structure and factors, we calculated the overdispersion parameter of the best-fit model for each ectoparasite species, model weight (i.e. the relative likelihood that a
particular model is the best-fit model) and model-averaged
estimates and odds ratios ( ⫾ 95% CI) for each variable in the
90% confidence set of models (Σmodel weights ⬎0.90;
Burnham and Anderson 2002).
Results
Aggregation size of adult raccoons was greatest in sites
with the permanent feeding stations (Kruskal–Wallis H′ ⫽ 230.948, DF ⫽ 2, p ⬍ 0.001; aggregated ⬎
control sites with food ⬎ control sites without food, all
comparisons p ⬍ 0.006 based on Mann Whitney U- test),
with up to 10 individuals simultaneously visiting the food
plots in aggregated sites (mean number of individuals per
photo ⫾95% confidence interval (CI); control without
food ⫽ 1.00 ⫾ 0.00; control with food ⫽ 1.16 ⫾ 0.06;
aggregated ⫽ 3.22 ⫾ 0.19). Instantaneous contact rates for
adults were 80% in aggregated sites (n ⫽ 358), 15% in control with food sites (n ⫽ 149), and 0% in control without
food sites (n ⫽ 43). Individual opossums Didelphis virginiana were the only other animal that consistently used the
food piles (⬎5% of camera nights), and this only occurred
in the aggregated sites.
Raccoon density did not differ among treatments
(Kruskal–Wallis H′ ⫽ 1.10, DF ⫽ 2, p ⫽ 0.576), averaging
20.0 ⫾ 4.9 (SE) in control without food sites (range 15.3 to
22.8, n ⫽ 4), 23.7 ⫾ 5.1 in control with food sites (range
19.9 to 27.1, n ⫽ 3), and 22.0 ⫾ 5.8 in aggregated sites
(range 8.8 to 31.6, n ⫽ 5). Supplemental food increased the
weight and improved the relative body condition of female
raccoons (mean body condition ⫾ 95% CI; control without
food ⫽ –0.54 ⫾ 0.21; control with food ⫽ –0.17 ⫾ 0.16;
aggregated ⫽ 0.03 ⫾ 0.15), but no differences were observed
among males (control without food ⫽ 0.26 ⫾ 0.25; control
with food ⫽ 0.40 ⫾ 0.27; aggregated ⫽ 0.35 ⫾ 0.17).
We observed 16 endoparasite species from 289 individual
raccoons sampled during 2006–2007 (Table 1). The most
common parasites were a capillarid roundworm Capillaria
procyonis (prevalence ⫽ 86–90%) and the intracellular
parasite Eimeria nutalli (prevalence ⫽ 81–91%). Five parasites detected in this study have been confirmed to reproduce
in raccoons and have direct life cycles (E. nutalli, E. procyonis,
Placoconus lotoris, Molineus barbatus and Baylisascaris procyonis). We considered these five species to be directly transmitted and all other species to be indirectly transmitted. Of the
Table 1. Prevalence (% infected) of endoparasites detected among
raccoons in control, control with food, and aggregated sites
(n ⫽ number of individual raccoons).
Parasite Species
Directly transmitted parasites
Eimeria nutalli1,2
Placoconus lotoris3
Molineus barbatus4,5
Eimeria procyonis1
Baylisascaris procyonis6
Indirectly transmitted parasites
Capillaria procyonis7
Capillaria puttori7
Eurytrema procyonis5,8
Capillaria plica7
Crenosoma spp.10
Physaloptera spp.11
Atriotaenia procyonis12
Macracanthorhynchus ingens13
Cruzia spp.14
Sarcocystis spp.15
Alaria spp.9
Control
Control w/food Aggregated
(n ⫽ 93) (n ⫽ 89) (n ⫽ 107)
81%
39%
43%
35%
9%
91%
36%
42%
55%
16%
88%
29%
31%
50%
20%
90%
51%
52%
25%
23%
15%
1%
2%
1%
0%
1%
87%
51%
21%
30%
22%
9%
1%
2%
1%
2%
0%
86%
42%
25%
23%
14%
19%
1%
3%
1%
0%
0%
1Inabnit
et al. 1972, 2Yakimoff and Matikaschwili 1933, 3Balasingam
1958, 4Gupta 1939, 5Chandler 1942, 6Kazacos 2001, 7Butterworth
and Beverley-Burton 1980, 8Denton 1942, 9Shoop and Corkum
1981, 10Dougherty 1946, 11Morgan 1941, 12Gallati 1959, 13Moore
1946, 14Bartholomew and Crites 1964, 15Stanek et al. 2002.
1429
remaining 11 endoparasites, nine are known to only have
an indirect life cycle, and two have unknown life cycles in
raccoons (C. procyonis and Cruzia spp.). We considered both
of these species to have indirect life cycles. When C. procyonis and Cruzia spp. were classified as directly transmitted,
support for the model results reported below only increased.
Thus, the classification of parasites and corresponding results
of this study should be considered conservative.
Three of five directly transmitted parasite species declined
in the presence of raccoon aggregation (Table 1; E. nutalli, P.
lotoris and M. barbatus). Among the directly transmitted parasite species that increased due to aggregation, Fisher’s exact
comparisons (with a Bonferroni correction factor) indicated
there were no significant increases in prevalence (control vs
aggregation treatments; B. procyonis p ⫽ 0.029, E. procyonis
p ⫽ 0.045). Several indirectly transmitted parasite species
exhibited declines when food was added (e.g. E. procyonis,
Crenosoma spp., C. puttori; Table 1); however, only E. procyonis
exhibited a statistically significant decline due to aggregation
and food supplementation (control vs food supplementation
or aggregation; E. procyonis p ⬍ 0.001, all other species and
treatment comparisons p ⬎ 0.140; Table 1).
Model selection
Goodness-of-fit tests that compared species richness in
global and intercept-only models found a significant
difference for parasites with a direct (likelihood ratio
χ2 ⫽ 39.217, DF ⫽ 7, p ⬍ 0.001) and indirect life cycle
(likelihood ratio χ2 ⫽ 16.550, DF ⫽ 6, p ⫽ 0.011). Year
of sample collection had significant model effects on parasites with direct (χ2 ⫽ 26.576, DF ⫽ 1, p ⬍ 0.001) but
not indirect life cycles (χ2 ⫽ 0.126, DF ⫽ 1, p ⫽ 0.72),
and was therefore only included in model selection procedures of directly transmitted parasite species (Table 2). The
mean number of directly transmitted parasite species was
greater in 2007 (mean ⫾ 95% CI; 2.52 ⫾ 0.17, n ⫽ 140)
than 2006 (1.91 ⫾ 0.16, n ⫽ 149), whereas the number
of indirectly transmitted parasite species was similar in
2006 (2.40 ⫾ 0.22, n ⫽ 149) and 2007 (2.46 ⫾ 0.20,
n ⫽ 140).
The best fit models of directly transmitted parasite species
richness (ΔAICc of 0–2) all included age (Table 2; overdispersion of best-fit model ⫽ 1.021). Model averaged estimates
and odds ratios indicated that age class III had ∼30% greater
species richness of directly transmitted parasites in the first
year of the experiment (Table 3, Fig. 1a), but this effect only
occurred in sites with food additions (Fig. 1b). When age
class III was examined by treatment in 2006, results indicate
the increase in species richness of directly transmitted parasites primarily occurred in aggregated sites (mean ⫾ 95%
CI: aggregated ⫽ 3.10 ⫾ 0.53, n ⫽ 10; control with
food ⫽ 2.30 ⫾ 0.83, n ⫽ 10; control ⫽ 2.07 ⫾ 0.67,
n ⫽ 13). These differences were not apparent in the second year of the experiment (2007), as species richness of
endoparasites with direct life cycles increased across all age
classes compared to 2006 (Fig. 1a).
The best fit models of indirectly transmitted parasite
species (ΔAICc of 0–2) included all four factors (age, sex, food,
aggregation) from the a priori model set (Table 2). The top
model was age ⫹ food, with a model weight of 0.438 and
1430
Table 2. Candidate set of models used to estimate species richness
of directly and indirectly transmitted parasites of raccoons (n ⫽ 289).
Models shown here represent the 90% confidence set (Σweight ⬎
0.90) used in model averaging procedures.
Model
log (l)
K ΔAICc Weight
Directly transmitted parasites
Age ⫹ Food ⫹ Year
Age ⫹ Year
Age ⫹ Sex ⫹ Food ⫹ Year
Age ⫹ Sex ⫹ Year
Age ⫹ Aggregation ⫹ Year
Age ⫹ Sex ⫹ Aggregation ⫹
Food ⫹ Year
Age ⫹ Sex ⫹ Aggregation ⫹ Year
–405.789 6 4.884 0.029
Indirectly transmitted parasites
Age ⫹ Food
Age ⫹ Sex ⫹ Food
Age
Age ⫹ Aggregation
Food
Age ⫹ Sex ⫹ Aggregation ⫹ Food
Sex ⫹ Food
Age ⫹ Sex
–478.339
–478.339
–481.051
–480.139
–483.386
–478.326
–483.385
–481.043
–404.405
–405.871
–404.332
–405.833
–405.835
–404.075
7
6
8
7
7
9
6
7
5
6
3
8
4
6
0.00
0.832
1.970
2.857
2.862
3.586
0.000
2.101
3.337
3.599
3.880
4.190
5.334
5.409
0.333
0.219
0.124
0.080
0.080
0.055
0.438
0.153
0.083
0.072
0.063
0.054
0.030
0.029
overdispersion parameter of 1.018. Model averaged estimates
and odds ratios indicated age class I and sites with food had
30–40% fewer indirectly transmitted parasite species (Table 3).
The role of age and food additions on indirectly transmitted species richness is best understood when considered
together. In control sites with no food additions, age classes
I and II had the lowest number of parasites and their 95%
CI overlapped little with the larger number of parasites supported by age classes III and IV (Fig. 1c). Conversely, the
number of indirectly transmitted parasite species was similar among all age classes of animals that inhabited sites with
food, while the age classes III and IV exhibited divergent
patterns in sites with versus without food (Fig. 1c). The
lower species richness among older age classes in sites with
food was primarily due to aggregated sites (mean ⫾ 95% CI
of ages III and IV combined: aggregated ⫽ 2.18 ⫾ 0.34,
n ⫽ 44; control with food ⫽ 2.57 ⫾ 0.36, n ⫽ 47;
control ⫽ 3.17 ⫾ 0.39, n ⫽ 48).
Discussion
Parasite species richness of raccoons was relatively high and
consistent across the 12 sites in this study. Photo analyses
indicated that the permanent food piles effectively increased
the co-occurrence and group size of raccoons in the
aggregated sites, and that this effect did not occur in the
control sites with and without food. Yet despite increases in
rates of contact and localized use of the permanent food piles
by hosts, aggregated populations did not exhibit any increase
in endoparasite species richness. Conversely, food supplementation decreased the richness of indirectly transmitted
endoparasites, particularly among the oldest age classes of
hosts that harbored the most parasites.
Alterations in resource availability led to a decline in the
number of indirectly transmitted parasite species per raccoon. Assessments of mean parasite species richness indicated
that animals from the aggregated category were the primary
Table 3. Model averaged estimates and odds ratios of parameters included in the 90% confidence set of models used to estimate the number
of directly and indirectly transmitted endoparasite species among raccoons in control, control with food, and aggregated sites
(2006–2007).
Parameter1
Model averaged estimate
Unconditional SE
Odds ratio
Lower 95% CI
Upper 95% CI
Directly transmitted parasites
Year (2006)
Age I (5–14 months)
Age II (15–38 months)
Age III (39–57 months)
No food
Sex (female)
No aggregation
–0.521
–0.228
–0.051
0.293
–0.113
0.011
0.002
0.115
0.165
0.144
0.156
0.085
0.035
0.023
0.570
0.781
0.946
1.392
0.807
1.046
0.968
0.454
0.551
0.698
1.003
0.633
0.831
0.763
0.716
1.108
1.282
1.932
1.031
1.317
1.228
Indirectly transmitted parasites
Age I (5–14 months)
Age II (15–38 months)
Age III (39–57 months)
No food
Sex (female)
No aggregation
–0.3627
–0.1676
0.1990
0.2803
0.0004
0.0170
0.236
0.186
0.204
0.193
0.041
0.041
0.639
0.811
1.272
1.456
0.999
1.236
0.408
0.548
0.833
1.063
0.742
0.909
1.002
1.204
1.942
1.994
1.344
1.681
1The
parameters year (2007), age (IV), sex (male), food and aggregation were redundant and set to 0 in model averaged estimates and 1 in
odds ratios.
driver of such effects. However, odds ratios from model
selection procedures indicated that the addition of food was
more important. This apparent discrepancy is due to the
moderate declines in the number of indirectly transmitted
parasite species in control with food sites (vs aggregated food
sites) and can be resolved by considering the implications of
food dispersal; aggregated food piles were large and predictable in location, whereas dispersed food piles were small and
unpredictable. Raccoons in aggregated treatments were able
to travel directly to the same spot to obtain food, while those
in control with food sites still had to search for food. Thus,
the likelihood of coming into contact with and consuming intermediate hosts that harbor infectious parasites was
lower for raccoons in aggregated versus control with food
sites. Two alternative explanations are also plausible. First,
increased nutrition can decrease susceptibility to parasitism
(Ezenwa 2004, Hines et al. 2007). We consider this unlikely
to underlie the patterns observed in this study because similar
declines in species richness were not observed among directly
transmitted parasites. Further, only female body condition
improved in sites with food additions (Monello and Gompper 2010). Second, food or social aggregations could alter
the distribution of intermediate hosts. This is also unlikely
because such effects would be localized in aggregated sites
(where the primary decline of indirectly transmitted parasite
species occurred); food plots were less than 5 m in diameter and visibly altered areas were less than 20 m in diameter
(Monello unpubl.). Thus, a decline in the diversity of diet is
the most plausible reason for the observed decline in species
richness of parasites with indirect life cycles.
Species richness of parasites with a direct life cycle was
generally not altered by treatments. The only notable difference was that animals in age class III displayed greater
species richness of directly transmitted parasites in aggregated sites during the first year of the experiment (based
on 95% CI). It is unclear why this would occur only in
age class III animals, and these results may be due a type II
error associated with a large number of comparisons. Overall, the lack of differences among the treatments do not
concur with other research that has found increases in parasite burdens in fed or aggregated populations (Wright and
Gompper 2005, Hines et al. 2007). However, the interaction between aggregation and population density has not
been well studied. Monello and Gompper (2010) found a
directly transmitted louse species responded to host aggregation by becoming less abundant due to a dilution effect
that lowered per capita infestation levels among males. In
contrast, a tick species that does not rely on host contact for
transmission became more abundant on hosts because they
can detect and seek out hosts and were more likely to drop
off after obtaining a blood meal and re-attach to raccoons
in the areas near the feeding stations. Such counterintuitive
results suggest that many parasitic species can interact in
unique ways with their hosts that are inconsistent with generally accepted expectations derived from an understanding of transmission mechanisms. Alternatively, animals
in this study may be exposed to infectious parasites at a
relatively high rate and aggregation cannot further increase
many of the parasites that are transmitted fecal-orally. Such
a conclusion is consistent with Prange et al. (2004), who
found that raccoons in high density populations do not
temporally segregate themselves from each other and
suggested that, even in the absence of social aggregation, such
populations are at risk for greater parasite transmission.
The fluke Eurytrema procyonis declined due to the addition
of food and was the only parasite that exhibited statistically
significant differences between treatments. This suggests the
intake of intermediate hosts for this parasite, which include
grasshoppers and snails, declined to a greater degree or made
up a larger part of the raccoon diet than other intermediate
hosts in this study (Carney et al. 1970). It is also noteworthy that the prevalence of B. procyonis was twice as great in
aggregated versus control populations. Although this difference was not statistically significant when a Bonferonni correction was conducted, the findings here are consistent with
previous research that found greater rates of contact or localized concentrations of raccoons may facilitate transmission
of this parasite (Gompper and Wright 2005).
1431
3
References
(a)
2
1
Direct transmission
2006 vs. 2007
Number of endoparasite species
0
4
(b)
3
2
1
Direct transmission
with and without food
0
4
(c)
3
2
1
Indirect transmission
with and without food
0
I
II
III
Age class
IV
Figure 1. Average number ( ⫾ 95% CI) of parasite species detected
per raccoon (n ⫽ 289). (a) Directly transmitted parasite species in
2006 (filled circles) and 2007 (open circles). (b) Directly transmitted parasite species at sites with food (open circles; note this includes
aggregated and control with food sites) and without food (control;
filled circles). (c) Indirectly transmitted parasite species in sites with
(open circles) and without (filled circles) food.
These results further emphasize the need to consider
parasite life cycles when infra- and component community
processes are examined. Distinct differences were apparent
in this study when parasites with direct and indirect life
cycles were considered separately. Further research is needed
to determine the effects of experimentally increased rates of
contact or social aggregation among a variety of species and
populations. The results of this study suggest the outcome
among infracommunities may largely depend on ecosystem properties that determine animal contact, such as host
spacing patterns and host feeding diet ecology.
Acknowledgements – This work was supported by National
Science Foundation grant DEB-0347609. We thank B. Cook, T.
Hamilton, D. Kuschel, K. McBride, T. McVicker, K. Mottaz,
E. O ’ Hara, S. Pennington, K. Purnell, S. Wade, M. Wehtje,
A. Wiewel and J. Wisdom for assistance in the field and
laboratory.
1432
Altizer, S. et al. 2003. Social organization and parasite risk in
mammals: integrating theory and empirical studies. – Annu.
Rev. Ecol. Syst. 34: 517–547.
Anderson, R. M. and May, R. M. 1991. Infectious diseases of
humans: dynamics and control. – Oxford Univ. Press.
Anderson, R. M. et al. 1981. Population dynamics of fox rabies in
Europe. – Nature 289: 765–771.
Arnason, A. N. and Schwarz, C. J. 1999. Using POPAN-5 to
analyse banding data. – Bird Study 46: S157-S168.
Arneberg, P. et al. 1998. Host densities as determinants of
abundance in parasite communities. – Proc. R. Soc. B 265:
1283–1289.
Balasingam, E. 1958. Studies on the life cycle and developmental
morphology of Placoconus lotoris (Schwartz, 1925) Webster,
1956 (Ancylostomidae: Nematoda). – Can. J. Zool. 42:
869–902.
Bartholomew, A. R. and Crites, J. L. 1964. On the occurrence of
the nematode, Cruzia Americana, in a raccoon, Procyon lotor
lotor. – Ohio J. Sci. 65: 219–220.
Bordes, F. and Morand, S. 2008. Helminth species diversity of
mammals: parasite species richness is a host species attribute.
– Parasitology 135: 1701–1705.
Bowman, D. D. 1999. Georgis’ parasitology for veterinarians. –
Elsevier.
Burnham K. P. and Anderson, D. R. 2002. Model selection and
multimodel inference: a practical information-theoretic
approach. – Springer.
Butterworth, E. W. and Beverley-Burton, M. 1980. The taxonomy
of Capillaria spp. (Nematoda: Trichuroidea) in carnivorous
mammals from Ontario. – Can. Syst. Parasitol. 1: 211–236.
Carney, W. P. et al. 1970. Eurytrema procyonis, a pancreatic fluke of
North American carnivores. – J. Wildlife Diseases 6: 422–429.
Chandler, A. C. 1942. The helminths of raccoons in east Texas. –
J. Parasitol. 28: 255–268.
Denton, F. 1942. Eurytrema procyonis n. sp. (Trematoda: Dicrocoelidae) from the raccoon, Procyon lotor. – Proc. Helminthol.
Soc. Wash. 9: 29–30.
Dougherty, E. 1946. A review of the genus Crenosoma Molin, 1861
(Nematoda: Trichostrongylidae); its history, taxonomy, adult
morphology, and distribution. – Proc. Helminthol. Soc. Wash.
12: 44–62.
Evans, R. H. 2002. Raccoons and relatives (Carnivora, Procyonidae). – In: Heard, D. (ed.), Zoological restraint and anesthesia.
Int. Vet. Inf. Serv. ⬍www.ivis.org/special_books/Heard/evans/
ivis.pdf⬎
Ezenwa, V. O. 2004. Interactions among host diet, nutritional
status and gastrointestinal parasite infection in wild bovids. –
Int. J. Parasitol. 34: 535–542.
Ezenwa, V. O. et al. 2006. Host traits and parasite species richness
in even and odd-toed hoofed mammals, Artiodactyla and
Perissodactyla. – Oikos 115: 526–536.
Franklin, A. B. et al. 2000. Climate, habitat quality, and fitness in
northern spotted owl populations in northwestern California.
– Ecol. Monogr. 70: 539–590.
Gallati, W. W. 1959. Life history, morphology and taxonomy of
Atriotaenia (Ershovia) procyonis (Cestoda: Linstowiidae), a
parasite of the raccoon. – J. Parasitol. 45: 363–377.
Gompper, M. E. and Wright, A. N. 2005. Increased prevalence of
raccoon roundworm, (Baylisascaris procyonis) owing to manipulated contact rates of hosts. – J. Zool. 266: 215–219.
Grau, G. A. et al. 1970. Age determination in raccoons. – J. Wildlife Manage. 34: 364–372.
Gregory, R. D. 1997. Comparative studies of host–parasite communities. – In: Clayton, D.H. and Moore, J. (eds), Host
parasite evolution: general principles and avian models. Oxford
Univ. Press, pp. 198–211.
Gupta, S. P. 1939. The life history of Molineus barbatus Chandler,
1942. – Can. J. Zool. 39: 579–587.
Hines, A. M. et al. 2007. Effects of supplemental feeding on
gastrointestinal parasite infection in elk (Cervus elaphus):
preliminary observations. – Vet. Parasitol. 148: 350–355.
Inabnit, R. et al. 1972. Eimeria procyonis sp.n., an Isospora sp., and
a redescription of E. nuttalli Yakimoff and Matikaschwili, 1932
(Protozoa: Eimeriidae) from the American raccoon (Procyon
lotor). – J. Protozool. 19: 244–247.
Kazacos, K. R. 2001. Baylisascaris procyonis and related species. –
In: Samuel, W. M. et al. (eds), Parasitic diseases of wild mammals. Iowa State Univ. Press, pp. 301–341.
Kenward, R. E. 1985. Ranging behaviour and population dynamics in grey squirrels. – In: Silby, R. M. and Smith, R. H. (eds),
Behavioural ecology. Ecological consequences of adaptive
behaviour. Blackwell, pp. 319–330.
Krasnov, B. et al. 2002. The effect of host density on ectoparasite
distribution: an example of a rodent parasitized by fleas. –
Ecology 83: 164–175.
Kuris, A. et al. 1980. Hosts as islands. – Am. Nat. 116: 570–586.
Møller, A. P. et al. 1993. Parasites and the evolution of host social
behavior. – Adv. Stud. Behav. 22: 65–102.
Monello, R. J. 2009. Experimentally assessing the influence of
resource availability and social aggregation on the parasites of
raccoons. – PhD thesis, Univ. of Missouri.
Monello, R. J. and Gompper, M. E. 2007. Biotic and abiotic predictors of tick (Dermacentor variabilis) abundance and engorgement on free-ranging raccoons (Procyon lotor). – Parasitology
134: 2053–2062.
Monello, R. J. and Gompper, M. E. 2009. Relative importance
of demographics, locale, and seasonality underlying louse and
flea parasitism of raccoons (Procyon lotor). – J. Parasitol. 95:
56–62.
Monello, R. J. and Gompper, M. E. 2010. Differential effects
of experimental increases in sociality on ectoparasites of
free-ranging raccoons. – J. Anim. Ecol. 79: 602–609.
Moore, D. V. 1946. Studies on the life history and development
of Macracanthorhynchus ingens Meyer, 1933, with a redescription of the adult worm. – J. Parasitol. 32: 387–399.
Morand, S. et al. 2000. Wormy world: comparative tests of theoretical hypotheses on parasite species richness. – In: Poulin, R.
et al. (eds), Evolutionary biology of host–parasite relationships.
Elsevier, pp. 63–79.
Morgan, B. B. 1941. A summary of the Physalopterinae (Nematoda) of North America. – Proc. Helminth. Soc. Wash. 8:
28–30.
Nunn, C. L. et al. 2003. Comparative tests of parasite species richness in primates. – Am. Nat. 162: 597–614.
Pacala, S. W. and Dobson, A. P. 1988. The relation between the
number of parasites/host and host age: population dynamic
causes and maximum likelihood estimation. – Parasitology 96:
197–210.
Poulin, R. 1995. Phylogeny, ecology, and the richness of
parasite communities in vertebrates. – Ecol. Monogr. 65:
283–302.
Poulin, R. 1997. Species richness of parasite assemblages: evolution
and patterns. – Annu. Rev. Ecol. Syst. 28: 341–358.
Poulin, R. and Mouillot, D. 2004. The evolution of taxonomic
diversity in helminth assemblages of mammalian hosts. – Evol.
Ecol. 18: 231–247.
Prange, S. et al. 2004. Influences of anthropogenic resources on
raccoon (Procyon lotor) movements and spatial distribution. –
J. Mammal. 85: 483–490.
Schulte-Hostedde, A. I. et al. 2005. Restitution of mass–size residuals: validating body condition indices. – Ecology 86:
155–163.
Shoop, W. L. and Corkum, K. C. 1981. Some trematodes of mammals in Louisiana. – Tulane Stud. Zool. Bot. 22: 109–121.
Stanek, J. F. et al. 2002. Life cycle of Sarcocystis neurona infections
in its natural intermediate host, raccoon (Procyon lotor). –
J. Parasitol. 88: 1151–1158.
Stanko, M. et al. 2002. Mammal density and patterns of ectoparasite species richness and abundance. – Oecologia 131:
289–295.
Wehtje, M. and Gompper, M. E. 2011. Effects of an experimentally clumped food resource on raccoon (Procyon lotor) home
range use. – Wildlife Biol. 17: 25–32.
Wilson, K. et al. 2002. Heterogeneities in macroparasite infections:
patterns and processes. – In: Hudson, P. J. et al. (eds), The
ecology of wildlife diseases. Oxford Univ. Press, pp. 6–44.
Wright, A. N. and Gompper, M. E. 2005. Altered parasite assemblages in raccoons in response to manipulated resource availability. – Oecologia 144: 148–156.
Yakimoff, W. L. and Matikaschwili, I. L. 1933. Coccidiosis in
raccoons: Eimeria nutalli n.sp., parasite of Procyon lotor. –
Parasitology 24: 574–575.
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