Download Consumers indirectly increase infection risk in grassland food webs

Consumers indirectly increase infection risk in
grassland food webs
Elizabeth T. Borera,1, Charles E. Mitchellb, Alison G. Powerc, and Eric W. Seablooma
aDepartment
of Zoology, Oregon State University, Corvallis, OR 97331; bDepartment of Biology, University of North Carolina, Chapel Hill, NC 27599;
and cDepartment of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY 14853
Most pathogens exist within complicated food webs of interacting hosts, vectors, competitors, and predators. Although
theory has demonstrated a variety of mechanisms by which
predation and competition in food webs can indirectly control
infection risk in hosts, there have until now been no experimental tests of this theory. We sampled the effect of long-term
exclusion of large vertebrate herbivores on the prevalence of
infection by a group of aphid-vectored viruses that infect
grasses (barley and cereal yellow dwarf viruses) in an oak
savannah in central California. We found that pathogen prevalence was ⬇4-fold higher in the presence of consumers than in
areas where they were excluded. Vertebrate consumers did not
directly alter infection rates by this aphid-vectored pathogen
group, but rather increased infection risk by increasing the
relative abundance of highly-competent hosts in the grassland
community. This large-scale experiment, measuring changes in
host abundance and infection risk in response to altered consumption rates, confirms theoretical predictions that consumers
can indirectly increase infection risk by altering the composition
of whole communities. Most importantly, these results demonstrate that, even in complex natural communities, alterations to
food web composition such as consumer invasion or extinction
can lead to significant impacts that cascade throughout entire
communities, including changes in infection risk.
apparent competition 兩 dilution effect 兩 disease ecology 兩 grazing 兩
healthy herds
H
uman activities worldwide are redistributing predators
and other consumers via selective removal and deliberate
or accidental introduction (1–3). Although altered consumer
communities are known to impact biodiversity, ecosystem
productivity, and stability and facilitate further biological
invasions (4, 5), there is mounting concern about the effects of
these food web alterations on host–vector–pathogen dynamics
(6 –9). Theory predicts that direct predation on a host population generally reduces pathogen prevalence regardless of
whether predators preferentially target infected hosts or susceptible hosts or show no preference for either host type
(9 –11). In addition, the effect of predators and herbivores on
infection prevalence in their prey may be mediated by impacts
on other aspects of the community such as the abundance of
either highly-competent host species or nonhosts or the search
efficiency of a vector, leading to either increased or decreased
infection risk (7, 12). For example, selective removal of
nonhosts or hosts minimally viable for a pathogen may increase
communitywide infection risk, whereas removal of highly
competent ‘‘spillover’’ host species generally leads to reduced
infection by generalist pathogens (7, 13). Predators or herbivores also may alter host diversity, generally leading to enhanced infection with reduced host diversity (7).
Although the theoretical exploration of the direct and indirect
role of predators in altering disease risk has focused on directlytransmitted diseases in which transmission is a function of
infected host density, theory demonstrates that the results are
typically robust to transmission formulations (7, 9). These the-
www.pnas.org兾cgi兾doi兾10.1073兾pnas.0808778106
oretical predictions about the role of predators in altering
disease risk have been explored by using comparative studies and
extensive observations in systems with directly- and vectortransmitted pathogens (e.g., refs. 9, 14, and 15). However,
despite repeated calls for replicated, experimental assessments
of the effects of consumers on host community composition and
infection rates, none yet exist (7, 11). Here, we present results
from a long-term experiment quantifying the effect of vertebrate
consumers on the prevalence of a globally-distributed, economically-important vector-borne group of pathogens, the barley and
cereal yellow dwarf viruses (B/CYDV).
B/CYDV, a group of generalist pathogens of grasses, infects
well over 100 crop and noncrop species (16) and is among the
most prevalent groups of all viral pathogens globally (17). This
RNA virus complex, obligately transmitted by aphids, reduces
longevity, growth, and seed production in infected hosts (16, 18).
B/CYDV infection can cause extreme yield reductions in crops
(16), and recently has been implicated in shifting the competitive
balance between native and invasive grasses to allow the invasion
and domination of ⬎9 million ha of California’s native perennial
grassland by Mediterranean annual grasses (19, 20). Thus, this
pathogen group has relevance for both global cereal crop
production and conservation of the world’s remaining grasslands. In contrast to most human and wildlife diseases, plant–
pathogen interactions, such as those between the B/CYDV
group and their hosts, also provide excellent model systems for
testing theoretical predictions about the effects of consumers as
the drivers of host community composition on pathogen spread,
because consumer, host, vector, and pathogen populations can
be experimentally manipulated at relevant spatial scales in the
field (12).
Host life history appears to play an important role in disease
transmission in West Coast grasslands; aphid vectors prefer and
perform better on annual grasses compared with perennials, and
some annuals cause substantially elevated transmission (i.e.,
‘‘spillover’’) throughout grassland communities (12, 19). In this
system, nonhosts (i.e., forbs) do not support either aphid vectors
or B/CYDV, but they compete with host species for shared soil
and light resources. Perennial grasses are, as a group, low-quality
hosts that serve as between-season pathogen reservoirs but
sustain lower aphid populations and have relatively low reservoir
competence, whereas annual grasses are high-quality hosts that
support elevated aphid populations and have relatively high
reservoir competence (19–21). Because B/CYDV require an
aphid vector for transmission and cannot be directly or vertically
transmitted, vertebrate herbivores cannot serve as a mode of
Author contributions: E.T.B. and E.W.S. designed research; E.T.B., C.E.M., A.G.P., and E.W.S.
performed research; E.T.B. and E.W.S. analyzed data; and E.T.B., C.E.M., A.G.P., and E.W.S.
wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
1To
whom correspondence should be addressed. E-mail: [email protected].
This article contains supporting information online at www.pnas.org/cgi/content/full/
0808778106/DCSupplemental.
© 2009 by The National Academy of Sciences of the USA
PNAS 兩 January 13, 2009 兩 vol. 106 兩 no. 2 兩 503–506
ECOLOGY
Edited by Harold A. Mooney, Stanford University, Stanford, CA, and approved November 25, 2008 (received for review September 4, 2008)
Results and Discussion
Our results confirm theoretical predictions that consumers can
indirectly control pathogen prevalence: B/CYDV-infection rates
increased 3.6-fold, from 5% inside of exclosures to 18% in the
presence of large vertebrate herbivores (P ⫽ 0.04; Fig. 1).
Although this effect of consumers on infection is striking, it is not
concordant with the healthy herds hypothesis, i.e., direct regulation of infected hosts leads to lower infection in the presence
of consumers (11). These results are unlikely to arise from direct
consumer control of pathogen prevalence because the direct
pathway nearly always results in a reduction in prevalence in the
presence of consumers (9, 11).
Theory predicts that changes in the species diversity or
composition of hosts and nonhosts can control infection risk (7,
13). Although theoretical predictions suggest that reduced species richness can alter the prevalence of infectious disease (7),
here, vertebrate consumers did not change host species richness,
evenness, or Shannon diversity (P ⬎ 0.05). Thus, our results are
not consistent with the dilution effect hypothesis (7).
Consumer alteration of the relative abundance of nonhosts,
low-quality hosts, and high-quality hosts does appear to control infection in this community. Vertebrate consumers increased the total cover of high-quality hosts (P ⫽ 0.006; Fig.
2A), and these high-quality annual grasses comprised 80%
(12/15) of the host species that increased outside of exclosure
fences. In contrast, the cover of nonhosts (Fig. 2B) and
504 兩 www.pnas.org兾cgi兾doi兾10.1073兾pnas.0808778106
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1. Do consumers decrease host infection in this community (i.e.,
healthy herds hypothesis; ref. 11)?
2. Do consumers alter host community diversity leading to
increased infection rates in low diversity communities (i.e.,
dilution effect, ref. 7;, i.e., dilution effect, ref. 13)?
3. Do consumers control the composition of the host community (i.e., abundance of high-quality hosts, low-quality hosts,
or nonhosts), leading to increased infection in communities
dominated by high-quality hosts (e.g., refs. 7 and 12)?
C
6
pathogen transmission. However, vertebrate herbivore diet preferences can control grassland plant composition (e.g., selective
removal of forbs) (22, 23), and plant regrowth stimulated by
grazing can increase aphid colonization (24).
In a replicated, long-term experimental exclusion of large
vertebrate herbivores, we examined whether and how vertebrate
consumers indirectly control B/CYDV prevalence. Specifically,
we examine the following questions:
B
4
Annual Host Abundance (% Cover)
Fig. 1. In concordance with theory, the presence of consumers increases
infection risk. Vertebrate herbivores caused a 12.9% increase in infection of an
annual grass host by a group of aphid-vectored grass pathogens, the B/CYDV,
compared with paired plots with no large vertebrate access.
Non−host Abundance (% Cover)
Unfenced
Perennial Host Abundance (% Cover)
25
20
15
10
5
Viral Prevalence (% Infected)
Fenced
A
Fenced
Unfenced
Fig. 2. Large vertebrate consumers increase the relative abundance of
highly-competent hosts. (A) The long-term removal of large vertebrate
herbivores shifted grassland plant composition, strongly reducing the
cover of high-quality hosts (i.e., 13% reduction of annual grass cover). (B
and C) In contrast, removal of large herbivores did not alter the cover of
nonhosts (i.e., forbs) (B) or low-quality hosts (i.e., perennial grasses) (C).
Cover estimates were independent for each species (i.e., do not sum to
100%). Here, we present means and 2 SE for the summed cover of each host
and nonhost type.
low-quality hosts (Fig. 2C) remained constant across fence
lines (P ⫽ 0.51). The relative frequency of host types in a
community (proportional abundance) can be as important as
absolute frequency (total abundance) for pathogen transmission, especially for vectored pathogens in which transmission
may either be independent of host density or (more realistically) vary nonmonotonically with host density (10, 25). Because high-quality host cover increased, whereas the cover of
nonhosts and low-quality hosts was unchanged by consumers,
high-quality hosts were also relatively more abundant outside
of exclosure fences (P ⫽ 0.03). Thus, large vertebrate consumers shifted the community context to enhance a group of
hosts known to increase B/CYDV prevalence (12, 19), providing support for the host quality hypothesis (7).
The fact that consumers increased both abundances of
high-quality hosts and pathogen prevalence suggests that host
compositional shifts caused by consumers are the most likely
Borer et al.
Borer et al.
hosts and decreased the relative abundances of nonhosts and
low-quality hosts, indirectly increasing communitywide infection risk. These results provide an experimental demonstration
that infection risk in natural communities can critically depend
on the community context of hosts, which can be, in turn,
dynamically controlled by consumers. In addition, these results
extend the implications of theoretical predictions from general
models motivated by predation (11) and host composition (7)
to a broader variety of consumers. Specifically, we have
experimentally demonstrated the presence of an indirect pathway in which consumers indirectly alter pathogen prevalence
by increasing the abundance of highly competent hosts (12).
This indirect pathway is relevant for multihost pathogens in
which hosts differ in competence, a scenario common across
many vectored pathogens (7, 12, 30). Thus, anthropogenic
addition or removal of predator or herbivore consumers is
likely to cause far-reaching effects throughout entire communities, including dramatic changes in infection risk.
Methods
To assess the direct and indirect influence of consumers on host composition and infection risk in natural communities, we sampled soils and plants
from each side of fenced herbivore exclusion areas at Hastings Natural
History Reservation (Carmel Valley, CA, 36.39° N 121.55° W) that had
excluded large vertebrate herbivores for an average of 28 years from areas
averaging 1,338 m2 (Table S2). Large vertebrate herbivores at the site
included mule deer (Odocoileus hemionus) and European wild boar (Sus
scrofa), both of which have catholic diets that include both grasses and
forbs. All fences were intact and effectively reduced access for many
vertebrate consumers; 10/11 fenced areas had fences high enough to
substantially deter access by mule deer. The abundance and richness of
small and medium mammals were also lower inside of exclosure fences
intended to exclude them (Table S2), and wild boars were completely
excluded; boar disturbance was never present inside of fenced areas (31).
Thus, fences effectively reduced consumption by mammals, consistently
removing mule deer and wild boars; however, for simplicity, we refer to the
areas inside and outside of each fence as ‘‘grazed’’ and ‘‘ungrazed.’’
We collected 20 individuals of a common and widespread annual grass
host, Bromus hordeaceus, from each of the paired grazed and ungrazed areas
in May 2006, for a total of 440 host individuals. We assayed each host
individual for infection by any 1 of the 5 major B/CYDV species via ELISA
(antibodies from Agdia). In each grazed and ungrazed replicate, we quantified plant biomass by clipping, drying, and weighing 2 10-cm ⫻ 1-m strips,
visually estimated the cover of each plant species in 2 1⁄2-m ⫻ 1-m quadrats and
collected 3 10-cm soil cores that were analyzed for 13 different soil characteristics (Table S1). Soil assays were performed at A & L Western Agricultural
Laboratories, Modesto, CA.
Pathogen prevalence and host-community responses to long-term experimental manipulation of large vertebrate consumers were analyzed by using
a mixed-effects regression model in which each of the 11 grazed– ungrazed
pairs was treated as a random effect (lme package in R, version 2.5.1).
Treatment (fenced or unfenced) was included as a fixed effect to test for
overall effects of consumers (P values reported in Results and Discussion).
Exclosure type (large vertebrate, burrowing vertebrate, climbing vertebrate;
Table S2), exclosure age, and four soil variables (phosphorous, nitrate nitrogen, sand percentage, and clay percentage; Table S1) also were included as
covariates. The effect of consumer removal on infection did not depend on the
exclosure age, soils, or suite of consumers excluded by each fence (P ⬎ 0.05; see
Table S2). Thus, our results point to consistent compositional shifts and
elevated infection caused by reduced consumer access, particularly implicating mule deer and wild boars, the most common large vertebrates excluded
from virtually all fenced areas. Data used in this paper are available on the
Knowledge Network for Biocomplexity (KNB) at http://knb.ecoinformatics.org/
by searching on keywords seabloom and bydv.
ACKNOWLEDGMENTS. We thank B. Martin and A. Brandt for assistance in
field collection; A. Blaustein, A. Dobson, M. Hixon, K. Dickinson, and 3 anonymous reviewers for helpful comments on an earlier version of this manuscript; and M. Stromberg and the Hastings Natural History Reservation for
invaluable support of this research. This work was supported by National
Science Foundation/National Institutes of Health Ecology of Infectious Diseases Grants 05-25666 (to E.T.B. and E.W.S.), 05-25641 (to C.E.M.), and 0525669 to A.G.P., and the California Integrated Hardwood and Range Management Program (E.T.B. and E.W.S.).
PNAS 兩 January 13, 2009 兩 vol. 106 兩 no. 2 兩 505
ECOLOGY
drivers of change in disease risk in this system. To determine
whether the change in host composition caused by consumers
was the driver of increased B/CYDV prevalence, we included
annual grass cover as a covariate in our regression model. The
inclusion of annual grass cover in this model of infection
removed the significance of the exclosure treatment as a factor
(P ⫽ 0.62), suggesting that there is no additional, independent
effect of vertebrate exclusion after accounting for host context.
This finding supports the conclusion that increased abundance
of high-competence hosts is the mechanism linking consumption by vertebrate herbivores and increased virus prevalence.
In addition to testing these three hypotheses based on general
theory, we tested whether several factors more specific to our
study system might provide alternative explanations of our
results. Experimentally simulated herbivory of infected individuals can increase survivorship in some B/CYDV-infected perennial grasses (26), providing one potential mechanism by
which consumers could directly increase virus prevalence (11).
However, half of the perennial species (4/8) were never found
outside of exclosures, perennial host cover did not differ across
fence lines (P ⫽ 0.60), and change in infection prevalence in our
focal annual grass host was unrelated to the intensity of recent
herbivory (difference in plant biomass inside and outside of each
exclosure fence; P ⫽ 0.23). In addition, perennial grasses can
serve as among-season pathogen reservoirs; however, our data
do not support this mechanism for controlling the increased
B/CYDV prevalence: perennial cover was not higher outside of
exclosures (Fig. 2C). Alternatively, aphids can exhibit strong
population responses to increased soil fertility, which can increase pathogen transmission rates (27, 28). Here, soil resource
pools did not differ across fence lines (P ⬎ 0.05), despite high
studywide variation in several resources (Table S1). Thus, infection risk was increased by consumers, but was not associated
with removal of uninfected hosts or changes in plant biomass (11,
26), nor was infection risk associated with differences in soil
fertility (29).
Our results experimentally confirm the theoretical prediction
that consumers can dramatically alter infection risk in a complex
natural community, but do not support the theoretical prediction
that consumption should generally reduce infection prevalence
(11). Using theory to inform our interpretation, these results
suggest two likely mechanisms by which consumers may substantially increase infection risk in this host community. First,
consumers may enhance the abundance of hosts that maximize
virus replication and/or vector reproduction, thereby enhancing
the average transmission competence, and hence infection risk,
across the host community (7). Second, by shifting the community to reduce the relative abundance of nonhosts and poorquality hosts, consumers may improve the probability that a
searching vector will encounter a high-quality host plant, thereby
elevating encounter rates between vectors and susceptible hosts
(7, 12).
Models of vectored pathogen transmission often assume that
transmission depends only on the proportion of infected individuals in the population (i.e., ratio- or frequency-dependent
transmission) (10). However, pure frequency dependence is
unlikely for most vectored pathogens, because the host-finding
behavior of most vectors will be affected by host density and
vector mobility (25). Our results suggest that elevated relative
abundance of nonhosts and poor hosts may reduce the search
efficiency of aphid vectors, reducing the encounter probability
with susceptible hosts. However, these results point most
strongly to the enhancement of high-quality hosts by consumers,
leading to elevated virus and/or aphid reproduction and infection risk (7, 19).
This long-term, replicated field experiment demonstrates
that consumers can indirectly control pathogen prevalence:
consumers increased the absolute abundance of high-quality
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Supporting Information
Borer et al. 10.1073/pnas.0808778106
Table S1. Variation in soil characteristics in response to grazing treatments
Total variation
Characteristic
NO3, ppm
P, ppm
K, ppm
SO4, ppm
Mg, ppm
Ca, ppm
Na, ppm
pH
Organic matter, %
Cation exchange capacity, meq/100 g
Sand, %
Silt, %
Clay, %
Minimum
Maximum
Effect of grazing, P value
2
10
53
2
65
595
11
6.2
1
4.1
50
6
6
15
82
287
17
224
2,833
34
7
5.6
19.3
88
26
28
0.4497
0.5277
0.7683
0.7654
0.3019
0.5144
0.2470
0.6446
0.2979
0.5192
1.0000
0.4316
0.4933
Whereas variation in some soil characteristics was quite high across the entire study area, variation in soil characteristics across individual fences never differed
from 0 (based on a mixed model with block considered a random effect).
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Table S2. Fence exclosure size, location, age, and major consumers excluded
Exclosure
Area, m2
Universal
Transverse
Mercator
Northing
2GRIFFA
3GRIFFA
4GRIFFA
5GRIFFA
6MUICK
7MUICK
8MUICK
11GRIFFC
12BOUC
13MENK
14KNOP
2000
2000
2000
500
45
45
45
25
60
1500
6500
629738
629666
629570
629975
629818
630299
630264
629235
629605
628744
628716
Universal
Transverse
Mercator
Easting
Year
built
Large
vertebrate
access
Climber
access
Burrower
access
Source
4027224
4027004
4027066
4028209
4027937
4027435
4026864
4027411
4027668
4026416
4026359
1965
1965
1965
1965
1987
1987
1987
1982
1980
1985
1992
Restricted
Restricted
Restricted
Restricted
Restricted
Restricted
Restricted
Accessible
Restricted
Restricted
Restricted
Accessible
Accessible
Accessible
Accessible
Restricted
Restricted
Restricted
Accessible
Accessible
Accessible
Accessible
Accessible
Accessible
Accessible
Accessible
Restricted
Restricted
Restricted
Restricted
Restricted
Accessible
Accessible
1
1
1
1
2
2
2
3
4
J.W. Menke, University of California, Davis
5
Grass hosts, soils, and plant community data were collected by using the same techniques from inside each exclosure and in an adjacent paired area outside
of each exclosure of equal size and geometry. Fences restricting large vertebrate access had wire mesh (15 cm) fencing to at least 1.25 m and barbed wire to at
least 2 m. Burrower access was restricted by fences with 1-cm fine mesh buried into the ground, and extending at least 1 m above the ground. Climbers were
restricted by fences with wire mesh (15 cm) to at least 1.25 m, metal flashing from 1–1.5 m from the ground, and fine mesh (1 cm) extending from the soil (or
below) to 1 m. The type of consumer excluded was never a significant term in any model (P ⬎ 0.05), demonstrating the primary importance of reduced herbivory,
particularly from large vertebrates; infection rates did not differ across the one fence line that permitted access by large vertebrate consumers (11GRIFFC).
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