Diverse effects of parasites in ecosystems: linking interdependent processes

Author(s): Melanie J Hatcher, Jaimie TA Dick and Alison M Dunn

Source: Frontiers in Ecology and the Environment, Vol. 10, No. 4 (May 2012), pp. 186-194
Published by: Wiley on behalf of the Ecological Society of America
Stable URL: http://www.jstor.org/stable/41480051
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 -REVIEWS REVIEWS REVIEWS

Diverse
linkin
Melanie J Hatch

positve f ects within ecosy tems. Howev r, par sites - us aly regarde in terms of their detrimental ef ects on
the indivduals they infect - can also have positve impacts on other species in the com unity. We now recog-
nize that par sites influence species coexistence and extirpation by altering competi on, prdation, and her-
bivory, and that hes ef ects can, in turn, influence cosy tem properties. Par sites and pathogens act as ecosy -
tem engine rs, alter en rgy budgets and nutrient cycling, and influence biodiversity. Equaly, because cosy tem
properties - such as biodiversity - af ect par site po ulations, ther is the potential for fe dback betwe n par -
sitsm and ecosy tem sta es. Using examples from animal and plant sy tems, we xamine this potential bidrec-
tional interdep ndence and chalenge the conventional wisdom that par sites have only negative or inconse-
quential impacts on ecol gical com unites.
I positve bivory, the properties Com unity tem nize tional sitsm quential indivduals engine rs, that and interdep ndence and ef ects impacts par sites - ecosy tem that such ecol gist alter within they thes on as influence nergy biodiversity ecol gical infect sta es. ef ects ecosy tems. gen raly and - budgets Using chalenge can can, species com unites. - also in recognize af ect examples Howev r, and turn, coexistence have the nutrient par site influence conventional positve the from par sites importance cycling, po ulations, and animal impacts ecosy tem - extirpation us aly wisdom and and on of influence plant her properties. regarde other species that by sy tems, is altering species the par sites biodiversity. - in such Par sites potential terms in we competi on, as the have xamine of polinators and com unity. their for Equaly, only pathogens fe dback detrimental this negative prdation, because - potential that We betwe n act or now have cosy tem ef ects as and inconse- bidrec- ecosy - recog- par - clear her- on
Front Ecol Environ 2012; 10(4): 186-194, doi: 10.1890/1 0 16 (published online 29 Mar 2012)

protists, viruses, bacteria, and fungi; and parasitoids.

ativetheimpacts
Say ative impactsonword
the "parasite"
health of onindividuals unlucky
the and health most people of individuals think of the unlucky neg- The potential for parasites to influence community struc-
enough to be infected. This is not surprising, given that ture can be seen in relatively simple, three-species interac-
stealing resources from a host lies at the heart of the various tions, which show the positive and negative effects of para-
definitions of parasitism. However, parasites can have both sites on non-host species (Figure 1). For example, parasites
positive and negative effects on populations of non-host shared by two species can cause apparent competition, even
species, with consequences that ripple throughout ecologi- if the hosts do not interact directly (Holt and Pickering
cal communities (Thomas et al 2005; Hatcher and Dunn 1985). This can lead to species exclusion, as one host acts as
2011). Indeed, because of their potential influence on a reservoir of disease for the other (Figure la). Alternatively,
ecosystem functioning and resilience, it has even been pro- parasites can enhance the coexistence of two species, by *
posed that a diversity of parasites can be a sign of ecosystem ameliorating the deleterious effects of one host on another.
health (Hudson et al . 2006). Here, we review the effects of Parasites can play this keystone role when a dominant com-
parasites on ecological communities as well as the influence petitor (Figure lb) or consumer (Figure lc) is more strongly
of community structure on the spread of parasites. We use regulated by the parasite (Hatcher et al . 2006, 2008).
the term "parasite" to include macroparasites such as Parasites mediate interactions between hosts at all
helminths, fleas, and parasitic plants; microparasites such as trophic levels, modifying competitive and consumer-
resource interactions. These indirect effects of parasitism
In a nutshell: may be population-density mediated. There is also
increasing realization regarding the importance of para-
Parasites can have positive effects on other species within site- induced changes in host behavior (termed trait-
communities, despite the negative impacts on their hosts
mediated, indirect interactions; Werner and Peacor
Parasites affect the complexity of food webs and can influence
how community composition responds to local species 1993), and such keystone effects may also influence com-
extinctions munity structure (Hatcher and Dunn 2011). For
Parasites also contribute to ecosystem energy budgets and instance,
can parasites may mediate biological invasions, such
alter the physical and chemical properties of ecosystems as one in the UK in which a key processor of basal
Understanding the complex relationship between host and
resources (the crustacean Gammarus duebeni celticus) is
parasite diversity is important for conservation management
and public health challenged by invasive species (Gammarus pulex ,
Gammarus tigrinus) that differ in their functional roles
(Figure 2; MacNeil et al 2003a; Dick et al 2010). This is
School of Biological Sciences, University of Bristol, Bristol, UK one of many recently documented systems in which para-
* (mel.hatcher@bristoiac.uk) ; 2 Institute of Integrative and Com- sites appear to play an important structuring role. Here,
parative Biobgy, University of Leeds, Leeds, UK; 3 School of Biology we review this developing field, which is challenging the
and Biochemistry, Medical Biology Centre, The Queen's University conventional wisdom that parasites only have either neg-
of Belfast, Belfast, Northern Ireland, UK ative or inconsequential impacts on ecological communi-
Beyond the Frontier: Listen to Melanie Hatcher discussing this re- ties. We discuss how parasites influence food-web struc-
search on Frontiers' monthly podcast, at www.frontiersinecology.org. ture and stability, and their effects on ecosystem function

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MJ Hatcher et al. Parasites and ecosystem processes

Figure 1. Keystone effects of parasitism. Arrows depict positive (+) and ne

population density resulting from the impact of a consumer or resource species)
arrows indicate key interactions , leading to the following patterns: (a) apparent co
higher parasite population densities , which have a greater detrimental effect on h
B. (b) Parasite-mediated coexistence: regulation of a superior competitor A by a
persist, (c) Parasite-mediated trophic cascade: regulation of herbivore (or pr
cascade, releasing the immediately lower trophic level from herbivory or prdat

(for instance, by altering nutrient

also interact
cycling
with their
orhosts'
by prey,
engineer-
predators, and other
ing the physical characteristics of ecosystems).
parasites. We
In addition, many parasites can then
infect multiple
host species, some biodiversity,
examine how parasites might influence as more or less generalistandconsumers,
how biodiversity could affect parasite
others as populations.
specialists on different host species at different
Further research is required stages of their life cycles.
to establish how In a groundbreaking
common study,
these diverse effects of parasites
Laffertyon et al ecosystems (andtoof
(2006) used network analysis examine a
food
ecosystems on parasites) are, but theweb involving
results parasites, based on over
are likely to20 years of
have important implications for data collected
parasite from and
the Carpintera
ecosystem Salt Marsh in
management in a variety ofCalifornia.
conservation
Including parasitesandalmost public
doubled connectiv-
health settings. ity (the proportion of possible links realized) and quadru-
pled nestedness (a measure of web structure; well-nested
Food-web studies: putting webs
thehave a parasites
strong core of generalist
back species that interact
with each other; specialists interact with subsets of
The potential importance of parasites
these). When properly
in ecosystems
accounted for, over 78% is of all
becoming clear from studies of linksfood
in the foodwebsweb involved
that parasites,
include with para-
parasites as part of an ecological community
site-predator (Table
links (which had been missing 1).
from earlier
Food webs describe ecological studies)
communities as afood-
dramatically enhancing network
web connectivity.
of trophic relationships; despiteIt their
is unclear long
whether history
this study is representative
of use, of the
effectscentury,
prior to the beginning of the 21st of parasites in other
fewecosystems;
of these however, other
networks included parasites. Thislake andis surprising;
river systems show similaralthough
(albeit less dramatic)
parasites are often inconspicuouseffects and
(Table 1).may be missed in
ecological studies, parasitism is regarded by many as the
most common consumer strategy Parasites of allstability
and the (Lafferty
of ecologicalet al
networks
2008). However, we now know that, despite their gener-
ally small size, the impact of parasites on are
Ecological communities ecological
regarded as stablenet-
if they pos-
works can be considerable. The well-studied food webs of sess three properties: population dynamic stability
estuarine communities and herbivorous insects can con- (rapidly reaching and returning to equilibrium, or with
tain just as many parasites as free-living species; parasites only mild fluctuations); robustness to secondary extinc-
therefore increase web complexity by increasing species tion (if one species is removed, few others go extinct as a
richness and food-chain length. result); and resilience (if the community is perturbed, it
quickly returns to its former state). Network studies sug-
Parasites enhance food-web connectivity gest that the properties we might expect to be associated
with parasitism will generally increase stability (reviewed
More recent studies indicate that parasites can influence in Poulin 2010). One reason for this is that interactions
other structural properties in ecological networks (Figure between hosts and parasites are often weak (compared to,
3). Not only do parasites interact with their hosts, they for instance, predatory interactions), as effects on indi-

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Parasites and ecosystem processes MJ Hatcher et al.

Figure 2 Simplified food <web for the native and

invasive Gammarus system. In Northern Ireland ,
UK, the native amphipod Gammarus duebeni
celticus is challenged by three non-native invasive
species . Parasites modify competition and intra -
guild prdation (prdation between species that
potentially compete) between natives and invaders,
as well as increasing the predatory impact of the
invasive Gammarus pulex (Dunn 2009; Dick
et al. 2010). Arrows show energy flow. All five
Crustacea are detritivores, with four also
predating smaller invertebrates. The three Gam-
marus species are arranged in an intraguild
prdation hierarchy (N: native G duebeni celti-
cus; II: invader G pulex; 12: invader Gam-
marus tigrinus); they also compete for smaller
invertebrate prey. Parasites (shaded boxes) influ-
ence interactions at all trophic levels. Infection of
the native amphipod with Pleistophora mulleri
(a microsporidian) reduces prdation by the native G duebeni celticus on A
predator on the invading G tigrinus, facilitating continued native-invader c
the invasive G pulex by the acanthocephalan parasite Echinorynchus truttae
host for E truttae) but also increases the predatory impact of G pulex on s
exclusion of the native G duebeni celticus by this invader (Dick et al. 2
amphipods are also predated by the white-clawed crayfish (Austropotamob
astaci) can reduce crayfish densities, thereby reducing prdation pressu
conte jeani reduces the ability of the crayfish to catch its amphipod prey (H

Table 1. Food-web studies including parasites

# of free-living # of
Community species parasites Effects of including parasites Reference

Ythan Estuary, Scotland 94 4 1 *Chain length increased; linkage density and Huxham et al. ( 1 995)
connectivity increased or decreased slightly;
% omnivory increased

Loch Leven Estuary, Scotland 22 30 Chain length increased; linkage density Huxham et al. (1 995)
slightly increased; % omnivory increased

Scotch broom (Cytisus scoparium ), 85 69 Predators, parasitoids, and pathogens Memmott et al. (2000)
Silwood Park, England contribute to connectivity, but predators
(the most generalist) have greatest impact

Company Bay intertidal mudflat, 67 9 *Greatly increased food-chain length; linkage Tho
New Zealand density increased slightly; connectivity
reduced slightly

Muskingum Brook, Pinelands, 28 I0 increased linkage density, decreased Hernandez and

New Jersey nestedness; slight increase in connectivity Sukhdeo (2008a)
Carpintera Salt Marsh, California 87 47 Strongly increased linkage density, nestedness Lafferty et al. (2006)
(439%), and connectivity (93%), when all
logically possible parasite links included;
Muskingum, Company Bay, and Ythan, when
re-examined, showed similar patterns

Takvtan Lake pelagic zone, 37 1 3 Increased food-chain length, linkage density, Amundsen et al. (2009)
Norway connectivity, and omnivory; more
connected host species supported more
trophically transmitted parasite species

Notes: Inclusion of parasites inevitably increases species richness and average food-chain length. Orig
some studies (marked with an asterisk), when re-examined to take into account missing data on par
increases linkage density and connectivity. Re-analyses (see Lafferty et al. 2006) were based on the
on web metrics were strongest.

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MJ Hatcher et al. Parasites and ecosystem processes

Figure 3 Effects of parasites on network structure . (a) Connectivity measures the

the food <web . Adding parasites to the web can boost connectivity substant
parasite-predator , and host-parasite links) are included. In this example, includin
links in a simple network, even though parasite species number only half those o
herbivores: blue ; predators: black). Provided these interactions are generally weak, i
by increasing dynamic stability, (b) Nestedness describes how consumer-reso
communities have a core of strongly interacting species (shaded) around which o
consumers use strongly and weakly connected resources, and specialists tend to cons
Well-nested webs tend to be less vulnerable to secondary extinction, and food webs in

vidual hosts are usually sublethal (Hatcher

exposing et al 2006;
the cockles to prdation by thei
Hatcher and Dunn 2011). The addition ( of
tercatcher many such
Haematopus ostralegus finsch
sitic manipulation
weak interactions offsets the destabilizing effects of of cockle behavior
fewer
hard structure
strong interactions, enhancing the and decreases sediment
community's disturbance with
dynamic
stability. Hence, at the ecosystem
community-wide
level, we effects.
might
Here, therefore,
predictparasitism has a
that parasites may counteract positive
the effect
strong feedback
on the diversity rela-
and abundance of benthic
tionships between predators and and
invertebrates prey,
a negative enhancing
effect on primary production
resilience and robustness to secondary
(Mouritsen extinction.
and Poulin 2010).
However, this concept has yet toParasitic
be put plantsto
alsodirect
influence the chemical and physi-
empiri-
cal structure
cal testing, and there is evidence of communitiesmay
that parasites through their effects on
cause
- or may themselves be more water vulnerable
relations and hostto - secondary
growth. Witchweed ( Striga her -
monthica , a major
extinction, counteracting any stabilizing parasite of
effect (decereal crops) can increase
Castro
and Bolker 2005; Lafferty andtranspiration
Kuris 2009). rates among Nevertheless,
host plants, leading to a reduc-
recent food-web analyses attest tion
tointheleaf temperature
importance of up to 7Cofand para-
thereby poten-
sites in food-web topology. For tially
instance, the non-random
affecting surrounding soil-water and nutrient rela-
tionsfood
distribution of parasites within (Phoenix and Press
webs 2005). Many
suggests mistletoes
that
parasites exploit - and alter - food-web
engineer topology.
the physical structure of the environment
Trophically transmitted parasites
(Figure 4).
(parasites
Dwarf mistletoesthat(Arceuthobium
infect spp) induce
both predators and their preythe andgrowthareof dense, twiggy masses (witches'
transmitted when brooms),
the definitive host preys upon which
anareinfected
used by birds and
intermediate
mammals for concealment,
host) are more likely to exploit highly
shelter, connected
or nesting. Mistletoe host
is now recognized in wildlife
conservation policy
species and are more often generalists thatfor iconic species such
exploit manyas the north-
host species (Chen et ai 2008; ern
Amundsen et ai 2009).
spotted owl ( Strix occidentalis caurina), and for biodi-
versity in general (Aukema 2003). However, the use of
dwarf mistletoe in conservation requires careful manage-
Parasites as ecosystem engineers
ment, as severe infestation results in substantial eco-
nomic
Parasites can alter the physical losses and increases
properties of the likelihood of dangerous
ecosystems
forest crown fires (Mathiasen
through direct effects on the environment, or by et al influ-
2008).
encing their hosts; as such, they can be regarded as
ecosystem engineers. In New Zealand,
Parasites the cockle
and energy budgets
(A ustrovenus stutchburyi ) plays a role in sediment biotur-
bation (releasing nutrients and
Parasites
exposing
themselves can
algae
contribute
to substantially
light). to the
energy budget
This effect is reduced by trematodes of theof ecosystems (Johnson et
Curtuteria al 2010).
aus - They
may be consumed
trails species complex, which induce incidentally when
surfacing an infected host is
behavior,

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Parasites and ecosystem processes MJ Hatcher et al.

Figure 4 Mistletoe in winter . The European mistletoe - Viscum album

orchards - can also use a broad range of other tree species as hosts (here
clumps of leafy shoots throughout the year , providing food and shelter f
distribution ([a] and inset) , the result of uneven seed dispersal by birds fee
high biomass of this parasitic plant in parts of Europe and the US. Althoug
releasing nutrients that were previously locked away in the long-lived host tre
specialist insect herbivores in the UK, with a greater diversity in its core rang

dation upon
eaten, or they may be actively preyed by the definitive
(for example, bird host
the exploitation of external parasites
1996). Manipulation
during grooming
of host behavi
behavior). In Carpintera Salt flow
Marsh, parasitic
both to and trema-
from the infect
G of
todes have a biomass equal to that duebeni
birds, celticus (Figure 2; a fre
fish, burrow-
ing shrimp, and worms combined infected(Kuris
by theet al 2008).
acanthocephalan Echi
Trematodes in the California horn more active
snail than uninfected
Cerithidea califor- individ
nica - the dominant invertebrate seeking
grazer shade,
in thisthey
ecosystem
move toward lig
- represent, on average, 22% of the target
easier soft-tissue weight
for trout of
predators - the
parasite
infected snails, denoting a sizeable resource(MacNeil et al 2003b). Such
for predators.
In addition, annual productionincrease
of the free-living
energy flow stages
to predators; in
produced by these trematodes can be
active, three times
infected the had a 30%
individuals
tion on stage
standing stock biomass of the parasitic smaller andprey
up to(Dick
ten et al 2010
times the standing stock biomass Some parasitic
of birds, plants
the top alter energy f
preda-
tors in this system. Many of theseecosystems
free-living via their
stages effects
fail to on nu
reach the next host but become food for
parasites are planktivorous
often short-lived or ha
turnover,
species. Similarly, many parasitic whereas abun-
plants produce their hosts, of
dant berries and seeds that provide food
sequester for both
resources verte-
for long periods,
brates and invertebrates (Figurecult4;toAukema 2003).
obtain by mostTheconsumers
tropical mistletoes (Loranthaceae
eucalypt
spp) have
forests
evolved
in Australia,
in tre
close association with particular bird species;
mistletoe (A mymany have
ema miquelii) contr
much litter
elaborate flower-opening mechanisms biomass
and offer as uninfect
large
understory
quantities of sugar-rich nectar in exchange forplant biomass (Marc
pollination
services (Mathiasen et al 2008). Rattles ( Rhinanthus spp) and velvet
Trophically transmitted parasites often
enhance change
nitrogen theirby releasi
cycling,
host's behavior, increasing their enable colonization
chances of beingby other plant
eaten
(reviewed in Lefevre et al . 2008); this will also
environments influence
(Quested 2008). In c
energy budgets in food webs.also Forreduce
example,
ratestrematode
of energy flow; for
of detritus
(Euhaplorchis californiensis ) - induced - the
changes basal energy res
in killifish
(F undulus parvipinnis) behavior stream
make the host
- by themore
isopodcon-
Caecidotea co
bya more
spicuous to predators, resulting in than
30-fold 40% as
increase inapr-
result of inf

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M] Hatcher et al Parasites and ecosystem processes

cephalan parasite A canthocephalus

these patterns will not tahlequahensis
necessarily be repeated across all
(Hernandez and Sukhdeo 2008b).
ecosystems, and parasites may respond to environmental
A recent study has provided quantitative
change evidence
at different rates than their hosts. that
parasitic manipulation can alter energy flow within and
between ecosystems. The nematomorph parasite
Biodiversity affects parasites Gordionus
spp causes its terrestrial cricket hosts to jump into water,
where the free-living stage Theofrelationship
the worm between biodiversity
exits the and the
hostpreva-
and swims away to seek a mate.
lence This
of generalist provides
parasites is complicatednovel
and depends
on many
opportunities for prdation of these factors, including the relative
terrestrial insects frequency
by of
fish, a subsidy amounting species
to 60%that canof the
amplify andannual
transmit theenergy
parasite effec-
tively (knownleucomaenis
intake of Japanese trout (Salvelinus as competent hosts)japonicus;
and the transmission
Sato et al 2011). mode of the parasites (Keesing et al 2010). Parasite estab-
lishment is predicted to be enhanced with increasing bio-
diversity if transmission success is strictly host-density
Parasites and biodiversity
dependent (Dobson 2004)* However, if parasite transmis-
sion depends on host
The relationship between parasitism andfrequency, parasite prevalence
biodiversity is will
complex (Hatcher and Dunn be determined
2011). by the relative frequency
Although parasitesof competent
themselves are a substantial hosts,
elementwhich may
of increase, decrease, or bethey
biodiversity, unrelated to
biodiversity. In some
may be more vulnerable to extinction diseaseare
than systems, more diverse com-
free-living
munities contain
species, an important consideration fora higher frequency of less
conservation pol-competent
icy (Dobson et al . 2008). Specialist parasites
hosts, to some extent are
buffering the particu-
more sensitive species
larly vulnerable to secondary
against extinction
infection (reviewed following the
in Keesing et al . 2010). Such
demise of their host; for instance,
"dilution effects"the California
of biodiversity horn
can be caused by several
snail (C caHfornica), host to at least
different 17
processes, specialist
including trema-
transmission mode, reduc-
tion of host density inby
todes, is under threat of replacement morethe
diverseinvasive
communities, and
"wasted
Japanese mudsnail or Japanese falsebites"cerith
of vectors( on non-competent
Batillaria hosts. A
ama-
mentaria) >, host to only one growing list of examples
trematode show evidence
(Lafferty andthat Kuris
reduced bio-
2009). Epidemiological models predict
diversity that
is associated with many
increased para-
disease risk, includ-
sites require a threshold ing
host population
Lyme disease, West Nile virus,size, below
hantavirus, and foliar
which the parasite will inevitably become
fungal pathogens (reviewed extinct.
in Keesing et al 2010). For
highly
Thresholds for establishment virulent on
depend parasites that regulate hostand
transmission populations,
virulence characteristics variation
and in can be quite
the relationship betweenhigh; for
diversity and trans-
instance, measles and other modern
mission might, under"crowd" diseases
some circumstances, set up alterna-
tive patterns of feedback
were unknown before the Agricultural between parasitism
Revolution, when and biodi-
human populations reached versity (Figurenumbers.
critical 5). Moreover, some of the life-history
characteristics that improve species* resilience to ecosys-
Parasites as bioindicators tem change (eg high reproductive output, low immune
investment) may also make these species competent
In some systems, it may be easier to monitor parasites
hosts (Keesing et al . 2010); such a relationship would per-
petuate
than hosts; hence, parasites might be used as indicators of feedback between biodiversity and parasitism.
ecosystem state. Helminths, for example, accumulate However, the dilution effect is not directly related to bio-
heavy metals at higher rates than their hosts, and diversity;
may it depends on whether biodiversity increases
the relative abundance of non-competent hosts. The lit-
therefore have a role as pollution sentinels or chemical
buffers for ecosystems (Dobson et al 2008). For specialist
erature commonly conflates these issues, giving the mis-
parasites, the more host species that are present in taken
a com-impression that biodiversity per se decreases infec-
tious disease.
munity, the more parasite species should also be present;
consequently, these parasites could be used as biodiversity
indicators. For instance, parasitoid diversity is correlated
Parasites affect biodiversity
with that of arthropods in Irish farmland, so the former
Parasites can enhance biodiversity when a dominant con-
might be used as bioindicators of the effects of farming
practices (Anderson et al 2011). Huspeni and Lafferty
sumer or competitor is the more vulnerable host (Figure
1). Diversity, spatial heterogeneity, and succession in a
(2004) used the trematode parasites of the snail califor-
wide
nica to assess the success of a salt-marsh restoration range of plant communities are maintained in part by
pro-
ject in boosting avian (the final host) biodiversity and soil-borne pathogens; these processes may even
specialist
underlie
found that trematode abundance and species richness global patterns in diversity (Kulmatiski et al .
increased as a result of restoration efforts. Research into Some parasitic plants, such as yellow rattle
2008).
parasites as biological indicators is still in its infancy;
(R hinanthus minor), can enhance plant species richness in

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Parasites and ecosystem processes MJ Hatcher et al.

detritivores (Finkes et al 20
influencing mammalian herbi
community composition (
2007). Generalist pathogens a
to cause species extirpation
host is present at a suitable
instance, rabies and canine
regarded as extinction th
Ethiopian wolf ( Canis simensi
wild dog ( Lycaon pictus ); fer
tions, which have increased in
act as reservoirs for thes
(Haydon relationships
Figure 5 A conceptual model of biodiversity-disease et al 2006).for
An in
para
number of
of multiple host species . (a) If parasite transmission is feral dogs
density in parts (
dependent
has been
success depends on the product of infectious attributedhost
and susceptible to the e
dens
withand
bwering host biodiversity reduces transmission increased mortality
lowers parasite leadi
prevalen
this case , the most vulnerable host species solution. of human
may increase familydens
in population uni
sequent abandonment
the parasite regulates host numbers), and parasitism will not feed of dome
back on
and
diversity, (b) If transmission is frequency Rupprecht
dependent 2007). This
(it depends a
only o
cade
density of infectious hosts or their vectors) , aeffect illustrates
reduction in host another
diversit
parasites
potentially increase total parasite transmission can interact
and prevalence with
in the commu
This process is contingent upon reduced drive extinction
host diversity risk.
resulting in a h
frequency of competent hosts, a relationship found in some ecosystems bu
necessarily predicted in general (white arrow). The most of
Introduction vulnerable h
parasites
population would then decline with increasing
extinctionparasite
risk prevalence, maki
more vulnerable to extinction . This could potentially set up a cycle of pos
feedback, with successive extinctions of Themore
introduction
vulnerable
of novel parasites
hosts.
or their This
t
vectors is regarded asis
scenario is more likely to occur when (1) transmission a major factor in thedepend
frequency
both within and between species; (2) the decline or extinction
parasite regulatesof many birds,popul
host
density and is highly deleterious to some amphibians,
species but and reptiles (eg Plowright
is widely et al
transmitted
2008). For instance,
others, allowing the required relationship between extinction or endan-'
host diversity and comm
competence (white arrow) to occur. germent of unique Galapagos avian and
reptilian fauna is a distinct possibility if
meadowlands, and this parasite has been piloted as a tool West Nile virus were accidentally imported to the archi-
for grassland restoration in the UK (Pywell et al 2004). pelago; the ability of native mosquito species to act as
Parasites can also influence biodiversity by inducingvectors for this virus further raises the risks (Eastwood et
trophic cascades; effects can propagate to varying degreesal 2011). This scenario may, however, be the exception
through food webs and can be found in a range of ecosys- rather than the rule, as disease has been cited as a
causative factor in only a few cases among the
tems. For instance, reductions in the rabbit populations of
Europe, following the introduction of myxomatosis, led to International Union for Conservation of Nature's red-
conversion of grassland to scrub and woodland in parts oflisted species (<4% of extinctions and <8% of critical
endangerments; Smith et al 2006). However, the same
southern England (Dobson and Crawley 1994), and also
underlie the endangerment of two specialist predators, the survey shows that disease is implicated as an additional
Iberian lynx (Lynx pardinus) and the Spanish imperial factor, operating in concert with other ecological drivers
eagle (Aquila adaberti; Ferrer and Negro 2004). The intro-more frequently than would be expected by chance.
duction of rinderpest to Africa in the 1890s caused wilde-Populations that are declining as a result of other factors
beest (Connochaetes spp) and African buffalo (Syncerus (eg habitat loss, invasive species) may be more prone to
caffer) population crashes and influenced plant commu- disease-induced extinction risk (de Castro and Bolker
2005; Tompkins et al 2011).
nity structure in parts of East Africa; its eradication in the
1960s led to equally strong effects on several herbivoreParasites (introduced or native) can influence
species and their predators and has caused a shift in the native-invasive interactions in several ways (Dunn 2009;
ecosystem regime, making the modern Serengeti a net car-
Tompkins et al 2011). In the UK, the invasive gray squir-
bon sink (Holdo et al . 2009). Endophyte infection rel
of (Sciurus carolinensis) is a reservoir for squirrel pox
virus, and this disease (which is usually fatal to the native
grasses is associated with reduced herbivory, while lab and
field experiments have demonstrated effects on popula- red squirrel Sciurus vulgaris , but largely benign in grays)
tion densities and species richness among aphids and theirhas caused a 25 -fold increase in the speed of invasion by
parasitoids (Omacini et al 2001), predatory spiders, and grays in England, where the virus is present (Rushton et

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al 2006). Non-native invaders may also act as reservoirs and could contribute valuable information for decisio
for the spillback of native parasites, amplifying their inci- making in a variety of conservation, animal, and public
dence in the more vulnerable native species (Kelly et al health settings.
2009). For example, the invasive crayfish Pacifastacus
leniusculus is an asymptomatic host to both the intro- Acknowledgements
duced fungus A phanomyces astaci (crayfish plague) and
the native microsporidian Thelohania contejeani , both of The authors acknowledge* support from the Natural
which are lethal to the endangered native white-clawed Environment Research Council (NERC NE/G015201/1).
crayfish A ustropotamobius pallipes (Dunn 2009; Dunn et
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