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Parasites as Prey
Anouk Goedknegt,
NIOZ Royal Netherlands Institute for Sea Research, Texel,
The Netherlands
Jennifer Welsh,
NIOZ Royal Netherlands Institute for Sea Research, Texel, The Netherlands
David W Thieltges,
NIOZ Royal Netherlands Institute for Sea Research, Texel,
The Netherlands
Parasites are usually considered to use their hosts as a
resource for energy. However, there is increasing aware-
ness that parasites can also become a resource themselves
and serve as prey for other organisms. Here we describe
various types of predation in which parasites act as prey
for other organisms: (1) predation of nonhosts on
infected hosts (concomitant predation), (2) predation on
free-living parasite life cycle stages, (3) predation on
ectoparasites in form of grooming or cleaning and (4)
predation or hyperparasitism by other parasites. In many
cases, these types of predation significantly reduce the
numbers of parasites and thus affect parasite population
dynamics. In contrast, predation on parasites is often
beneficial for the hosts as they are released from parasite
burden. Finally, when parasites act as prey they may con-
tribute to the nonhost predator’s diet, in some cases
constituting a significant proportion of energy intake.
Introduction
In ecological studies, parasites are usually not considered
to serve as prey or a resource for other organisms. Instead,
by definition, they use other organisms as a resource
themselves. However, recent studies on food webs includ-
ing parasites have shown that parasites are involved in 75%
of the trophic links between species in a food web, including
many links where they are a resource for other organisms
(Lafferty et al., 2006a). There are several different ways in
which parasites can be involved in trophic links in food
webs. First of all, many parasites depend on the predation
of their hosts for successful transmission to the succeeding
down-stream host during some part of their complex life
cycles, thus hitch-hiking on predation links (a transmission
type called trophic transmission). However, not all preda-
tors of infected organisms are suitable down-stream hosts
and parasites may thus be ‘accidentally’ and indirectly
consumed by predators and, therefore, not result in suc-
cessful transmission. Parasites may also directly become
prey during their free-living life cycle stages. Most parasites
include free-living stages to get from one host to the next. In
this free-living stage, parasites are extremely vulnerable to
predation by nonhost predators. Another type of direct
predation on parasites involves parasites that attach
themselves to the outside of their hosts (ectoparasites).
Ectoparasites may also be vulnerable and can be consumed
by other animals. Finally, parasites can also serve as prey or
host resources for other parasites. In the following, we
explain the different cases where parasites become prey and
discuss the ecological effects of predation on parasites for
the parasites, their hosts and the predators. See also:Food
Webs;Parasites and Pathogens: Avoidance;Parasitism:
Life Cycles and Host Defences against Parasites;Parasit-
ism: the Variety of Parasites;Parasitoids
Predation and Transmission
Trophic transmission
By definition, parasites are always dependant on the pres-
ence of their hosts. However, all parasites have to transmit
from one host to another at some point in their lives. They
do so by an infective life cycle stage, whereby the parasite is
one free living and released into the environment. If the
parasite has a direct life cycle, the infective stage can infect
conspecific hosts or, in the case of parasites with complex
life cycles, other hosts. The latter types of parasites often
include more than one free-living stage in their life cycle by
which the parasites go through a specific sequence of
parasitic stages in hosts and free-living stages. This is
illustrated by the typical three-host life cycle of digenan
trematodes, a type of parasitic flat worm which are often
referred to as ‘flukes’ (
Figure 1
). In these trematodes,
Advanced article
Article Contents
.
Introduction
.
Predation and Transmission
.
Concomitant Predation
.
Predation on Free-Living Stages
.
Predation on Ectoparasites
.
Parasites as Consumers of Parasites
.
Conclusion
Online posting date: 17
th
September 2012
eLS subject area: Ecology
How to cite:
Goedknegt, Anouk; Welsh, Jennifer; and Thieltges, David W
(September 2012) Parasites as Prey. In: eLS. John Wiley & Sons, Ltd:
Chichester.
DOI: 10.1002/9780470015902.a0023604
eLS &2012, John Wiley & Sons, Ltd. www.els.net
1
infection of the next hosts in the life cycle (down-stream
hosts) not only occurs via free-living infective stages but
also via predation of infected hosts (
Figure 1
). The second
intermediate host (up-stream host; a bivalve in
Figure 1
)
needs to be consumed by the definitive host (the down-
stream host; a bird in
Figure 1
) before the parasite can
develop into its adult stage and sexually reproduce. In this
life cycle stage, predation of its up-stream host is the only
way for the parasite to successfully complete its life cycle.
Almost all parasites with complex life cycles follow
predator–prey links and depend on trophic transmission at
some point in their lives; thus predation and transmission
are intricately linked for many parasites (Lafferty et al.,
2008). The importance of trophic transmission for
parasites is illustrated in a food web from a saltmarsh in
California, where a third of the parasite species consumed
by predators via their prey use the predator as host
(Lafferty et al., 2006b).
Parasites manipulate hosts to increase
transmission
As predation by down-stream hosts is often crucial for the
successful transmission of parasites, many parasite species
have developed strategies to increase their chances to
become transmitted via manipulating the behaviour of
their hosts. For example, one trematode species encysts
itself in the brain of killifish, an important prey item for
birds in the estuaries of California. When a killifish
becomes infected, it exhibits behaviours that make it more
conspicuous (e.g. surfacing or flashing), making the fish
10–30 times more vulnerable for predation by birds, the
definitive host of the parasite (Lafferty and Morris, 1996).
Another example is that of the so-called ‘zombie snails’.
These snails are infected by a trematode that uses birds as
definitive host (Lewis, 1977). When a snail is infected by a
parasite egg, the egg develops into a sporocyst, which
contain hundreds of little parasitic clones (also called
‘brood-sacs’), which subsequently invade the snail’s ten-
tacles. As the tentacles become more swollen and colourful
they start to mimic the appearance of a caterpillar (
Figure 2
).
This alteration to the host caused by the parasite lures birds
to eat the tentacles of the snail host and can result in the
parasite infecting the bird. The parasite also has another
tactic to increase the likelihood of predation by the bird.
The infection of the parasite in the tentacles reduces the
ability of the snail to react to light intensity. As a result, the
snail may no longer hide in the shadow as it would do
normally and, therefore, it is more visible for predators.
Furthermore, the brood-sacs in the tentacles start to pul-
sate in response to light intensity (Wesenberg-Lund, 1934),
making the resemblance to a caterpillar even more likely.
These examples illustrate that parasites can mediate overall
predation rates and predator–prey choice, depending on
the infection levels in a host population. By doing so, they
can also affect the flow of energy through a food web.
Concomitant Predation
Trophic transmission gone wrong
Predation of infected hosts does not always lead to a suc-
cessful transmission. In most cases, the predator will
actually be an unsuitable host for the parasite. In this case,
Free-living
stage
Free-living
stage
Figure 1 Example of a typical three-host life cycle of a trematode,
showing the sequence of different hosts and free-living stages involved
(black arrows) and illustrating the different types of predation on them
(blue arrows). In this case, the definitive host is a bird, from which the
parasites release free-living eggs into the water together with the bird’s
faeces. The eggs infect a first intermediate host (a gastropod), in which the
parasite reproduces asexually in so-called sporocysts or rediae and releases
a second free-living stage into the water (cercariae). These cercariae infect a
second intermediate host (a cockle) in which the parasites encyst
(metacercariae). Finally, when the second intermediate host is consumed
by the definitive host, the life cycle of the parasite is completed. Parasites
can become prey either when infected hosts are consumed by nonhosts
(concomitant predation; filled blue arrows) or when their free-living stages
are consumed (open blue arrows). Note that parasite consumption is also
an essential part of the parasite’s life cycle when the infected second
intermediate host is eaten by the definitive host.
Parasites as Prey
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2
the potential (but unsuitable) host acts as a predator,
leading to consumption rather than transmission of the
parasite (Johnson et al., 2010). In the example of the tre-
matode life cycles (
Figure 1
), first or second intermediate
hosts as well as the definitive hosts may be preyed on by
nonhost predators, consuming the parasites together with
their prey without becoming infected. This type of acci-
dental predation has been termed concomitant predation
(Johnson et al., 2010; filled blue arrows in
Figure 1
). For
trophically transmitted parasites, this seems like an
unavoidable side effect of being dependent on predation
links for transmission: whilst predation will sometimes
ensure transmission, it will probably more often lead to
ending up in the wrong host. Interestingly, concomitant
predation does not need to lead to the total consumption of
the host. For example, one trematode species prevents New
Zealand cockles (Austrovenus stutchburyi) from burying in
the sediment by encysting itself in the cockle’s foot and
interfering with the musculature. As a result, the cockles lay
on the sediment surface where they are more vulnerable to
predation by birds than their uninfected conspecifics bur-
ied in the sediment (Mouritsen and Poulin, 2003). This is
usually interpreted as a case of parasite manipulation as the
parasite’s down-stream hosts are birds. However, infected
cockles on the sediment surface are often not completely
eaten by birds (suitable hosts), but partially consumed by
benthic fishes (unsuitable hosts). The fishes feed on the
highly infected tip of the cockles’ feet, a behaviour that is
referred to as foot cropping. In manipulative experiments,
the scientists found that this partial foot cropping by
fish occurs to such an extent that it exceeds total predation
by birds. As a result, only 2.5% of the parasites are
actually transferred to their down-stream hosts, whereas
17.1% are lost to the fish (Mouritsen and Poulin, 2003;
Figure 3
).
Increased parasite mortality and changes in
prey quality
The cockle example illustrates how concomitant predation
can significantly contribute to parasite mortality. Food
web studies that include parasites suggest that approxi-
mately 63% of the links where a predator consumes
infected hosts lead to concomitant predation because the
predator is an unsuitable host, but only approximately
37% of these links result in the transmission of parasites
(Lafferty et al., 2006b). However, to date, little is known on
the actual magnitude of the effect of concomitant predation
on parasite population dynamics.
For a predator, concomitant predation may result in
an additional food resource, specifically when the host is
highly infected. However, again, to date, there are no
studies regarding the potential energy gain that predators
get from consuming parasites alongside their actual prey.
In contrast, more is known on the effects of parasites on
the general energetic value of their hosts. Infected prey
may have a reduced or increased quality for predators,
depending on the parasite–host system. For example,
brine shrimps which are infected by tapeworm larvae
have a higher energy content (including the parasite)
compared to uninfected conspecifics (Sa
´nchez et al.,
2009). In contrast, fungal infections of Daphnia reduce
the energetic value of infected hosts (again including the
parasites) for their juvenile fish predators (Forshay et al.,
2008).
Besides directly affecting the energetic value of their
hosts, parasites may also have indirect effects on pre-
dation rates of predators. Similar to the host manipula-
tion in trophically transmitted parasites discussed above,
parasites may influence predator–prey interactions in
nonhost predators. They can do so by making their hosts
more vulnerable to predation. For example, Daphnia
water fleas are more likely to be predated on by fish
predators when they are infected by a fungi, but the fish
do not serve as down-stream hosts (Johnson et al., 2006).
As a consequence of the infection, the body cavity of
Daphnia is filled with thousands of dark sporangia,
reducing its transparency and making it more visible
for fish predators. Another example of how parasites
can influence predator–prey interactions is the case of
the shell-boring polychaete Polydora ciliata. This worm
weakens the shell of the marine periwinkle Littorina
littorea, making infected snails more vulnerable to
predators. Interestingly, shore crabs make use of this
weakness, preferring infected snails over uninfected snails
(Bushbaum et al., 2007).
Figure 2 A ‘zombie snail’. The snail is infected by a trematode that
invades the snail’s tentacles, leading to swollen and colourful tentacles. This
mimics the appearance of a caterpillar, which is the prey of the parasite’s
definitive bird hosts. Hence, the phenotypic changes caused by the parasite
increase its transmission. Reproduced by permission of Marek Snowarski
(www.atlas-roslin.pl).
Parasites as Prey
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3
Predation on Free-Living Stages
Vulnerable life cycle stage
As discussed above, many parasites have life cycle stages
which occur in a host and other stages whereby the parasite
is living freely in the environment (
Figure1
). Once outside the
protection of a host, these free-living stages are vulnerable
to various abiotic and biotic factors (Thieltges et al., 2008b;
for abiotic examples see: Pietrock and Marcogliese, 2003).
For example, surrounding organisms can prey upon the
free-living stages, thereby reducing them in numbers. Some
predators prey selectively on these free-living stages such as
juvenile crab and shrimp, whereas others predate in a
nonselective way such as filter feeders. As a result, the
infection levels in the down-stream hosts decrease. This
process is called the ‘dilution effect’ and has been reported
for many different parasite–host systems (Thieltges et al.,
2008a; Johnson and Thieltges, 2010). Instead of direct
predation, free-living parasites can also be ingested toge-
ther with a totally different food source. For instance, dung
beetles and earth worms frequently ingest eggs and larvae
of parasitic nematodes when feeding on faeces of other
organisms (English, 1979; Waghorn et al., 2002).
Effects on parasites and application in pest
control
Many studies suggest that the various forms of predation
on free-living stages are important mortality factors for
parasites. Predators can, therefore, be very effective in
reducing numbers of free-living stages of parasites. For
example, copepods can reduce the number of juvenile
stages of mermithid nematodes by 70– 100%, depending on
the species of copepod and their density (Achinelly et al.,
2003). There are many other organisms that have been
reported to significantly reduce infective stages of nema-
todes, either directly or indirectly via ingestion with other
food (see
Figure 4
for examples). Similarly, many bivalves
like oysters and mussels have been shown to be effective
diluters, reducing the number of free-living stages of tre-
matodes by almost 80% (Thieltges et al., 2008b).
Such strong reductions in the numbers of infective parasite
stages have important implications for pest control in agri-
culture and livestock farming. One example is the reduction
of eggs of parasitic nematodes by a nematophagous fungi in
the intestines of swines (Ferreira et al., 2011). Normally, the
nematodes cause liver damage to the swine (‘milk spots’
caused by larvae), but the addition of a special fungi to the
swines’ feed reduced the numbers of eggs by more than 50%.
This is because the fungi excreted with the faeces reduce the
numbers of infective eggs on the pasture (
Figure 4
).
As free-living stages are usually produced in high num-
bers, they may also constitute an energy resource for
predators preying on them. For example, the production of
trematode cercariae in coastal marine systems exceeds the
standing stock of birds (Kuris et al., 2008). Many organ-
isms are known to prey on cercariae, suggesting that cer-
cariae may be a significant energy source for some
predators (Thieltges et al., 2008a). However, actual data of
Infected cockles
Fish
% of infected stages eaten
Bird
Uninfected cockles
Figure 3 Partial predation on infected hosts by a nonhost predator. A trematode species infecting the New Zealand cockle impairs its burying ability so that
cockles are exposed on the sediment, resulting in an increased predation by the definitive host compared to uninfected cospecifics (a case of host
manipulation). However, fish also partially prey on exposed infected cockles by nipping off the tip of the cockles’ foot. Most parasites are concentrated in the
foot tip and, since the fishes do not serve as down-stream hosts, a significant proportion of the parasites are lost via this concomitant predation.
Parasites as Prey
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4
the relevance of cercariae in the diet of nonhosts are
restricted to juvenile fish in a California estuary where
predation of cercariae was calculated to comprise
approximately 2–3% of the fishes’ energetic requirements
(Kaplan et al., 2009).
Predation on Ectoparasites
Grooming and cleaning
Another case where parasites become prey is predation on
ectoparasites, which are parasites that attach themselves to
the outside of the body of a host. A classic example of
predation on ectoparasites is grooming by monkeys. In this
type of intraspecific interaction, one individual releases a
second individual from fleas and other ectoparasites. This
is beneficial for the monkey that is groomed, but it also
strengthens the social bounding between both individuals.
Similar examples are known from interspecific inter-
actions, for example, from oxpeckers which free mammals
on the African savannahs of ticks (Hart et al., 1990) and
from cleaner shrimps and fishes which pick ectoparasites
from fish hosts (Grutter, 1999).
Effects on parasites, hosts and predators
For parasites, grooming and cleaning are probably often
significant sources of mortality, with negative effects on
parasite population dynamics. In contrast, grooming and
cleaning are beneficial for both, the host and the predator:
one species profits from the energy resource and the other
species is released from its parasite pressure. Hence, this
type of interaction can be considered to be mutualistic. The
benefit for hosts can be illustrated in the case of cleaner fish
that that feed on ectoparasites attached to the body of their
clients. When these cleaner fish are absent over a longer
period the hosts are negatively influenced by the ecto-
parasites. In a study over a 8.5-year period, Waldie et al.
(2011) found significantly smaller hosts in an area where no
cleaner fish were present, suggesting that these hosts had to
invest their energy in their immune system rather than
into growth. In addition, in the absence of cleaner fish, a
reduction of 65% in visiting juvenile hosts was observed.
The juveniles suffer from the absence of cleaner fish, as the
ectoparasites have a negative influence in their perform-
ance as measured by swimming and oxygen consumption
(Grutter et al., 2011). The cleaning symbiosis is also very
beneficial for the cleaners as ectoparasites may constitute a
large part of their diet (Grutter, 1996).
Cleanerfishinaquaculture
Ectoparasites can be a significant problem in aquaculture,
where high stocking densities often provide ideal habitats
for the parasites. A prominent example is ectoparasitic
salmon lice (a copepod), which feed on the fish tissue and
can cause morbidity and mortality (Pike and Wadsworth,
1999;
Figure 5a
). When a population of lice settles in the
cages where the salmon are raised (
Figure 5b
), the parasites
can spread easily due to a free-living life stage and the high
densities in which the fish are kept, resulting in declines of
salmon stocks in the cages (Connors et al., 2010). Even
more worrying is the fact that the free-living stages of the
parasite can also spill-over and infect wild populations of
salmon, as the salmon farms are often built in the proximity
of their migration routes (Costello, 2009). This spill-over
can cause up over 80% mortality in many runs of wild pink
salmon, when passing salmon farms on their way to the
open ocean (Krkos
ˇek et al., 2007). Since salmon lice are
such a problem, various treatments have been tested;
however these compounds often have undesired effects on
the fish or the environment (Roth et al., 1993). As an
alternative, it has been suggested to add cleaner fish or
shrimp into the net pens to reduce ectoparasite burden of
the fish (
Figure 5c
). For example, goldsinny wrasse (Cteno-
labrus rupestris) added to salmon cages can effectively
control sea lice (1– 8 sea lice per fish compared to up to 40 in
control cages; Treasurer, 1994). Similar results were
obtained with two species of cleaner fish on two Irish sal-
mon farms (Deady et al., 1995). By using a ratio of one
cleaner fish to 250 salmon, the lice levels were kept below
five lice per fish. In addition, the salmon were less stressed
by this type of pest control than conventional chemical
treatments. Furthermore, there are two species of cleaner
shrimps that inhabit North-Atlantic shallow waters and
remove ectoparasites from plaice (O
¨stlund-Nilssen et al.,
2005). These results suggest that cleaner shrimps and
cleaner fish could be suitable as biological control agents
for sea lice infections on salmon and other fish in aqua-
culture settings.
% Reduction of free-living stages
Dung beetles
Nematodes
100
90
80
70
60
50
40
30
20
10
0
Copepods
Mites
Funghi
Figure 4 Examples of the levels of reduction of infective free-living stages
of parasitic nematodes by various organisms from different ecosystems
(indicated by different colours): earth worms (Waghorn et al., 2002) and
dung beetles (English, 1979) preying on nematode eggs and larvae in
dung, copepods preying on nematode larvae in fresh water systems
(Achinelly et al., 2003), mites preying on nematode larvae in sandy soils
(Karagoz et al., 2007) and nematophagous fungi on nematode larvae on
livestock pasture (Ferreira et al., 2011).
Parasites as Prey
eLS &2012, John Wiley & Sons, Ltd. www.els.net
5
Parasites as Consumers of Parasites
Hyperparasitism and intraguild predation
Finally, parasites can serve as a resource for other para-
sites, either by being parasitized by other parasites
(hyperparasitism) or by being preyed by other parasites
(intraguild predation). The first happens when a parasite
infects another parasite. This is particularly well demon-
strated within the insect order of Hymenoptera. These so-
called hyperparasitoids often infect a primary parasitoid,
which in turn infects a herbivorous or scavenger host
(Sullivan and Vo
¨lkl, 1999). The second happens when
parasites kill and consume other parasites, often in order to
get rid of potential competitors. For example, trematodes
infecting snails as first intermediate host can be preyed on
by other species of trematodes. Some of these predating
species develop a special cast of small ‘soldier morphs’ with
large mouths for this purpose. These ‘warrior worms’
attack other parasites trying to invade the snail host.
Another morph of large worms acts as reproductive cast
worms (Hechinger et al., 2011). Both morphotypes are
genetically identical as they are clones derived from a single
egg infecting the host snail. Hence, this shows an analogy to
the social organisation in colonies of ants or bees.
Hyperparasitism and pest control
The significant effect of hyperparasites on their hosts is
illustrated by the effective use of insect hyperparasitoids as
biological control agents against pest insects in agriculture.
Here, they can be very efficient in controlling pest popu-
lations. However, there are also cases where hyperparasites
(a)
(b)
(c)
Figure 5 Typical ectoparasites of salmon in aquaculture and their consumption by cleaner fishes: (a) salmon lice (parasitic copepods, the brown
ectoparasites) infect salmon and cause damage to the skin, often leading to secondary infections. Reproduced by permission of Bruce MacGregor Sandison.
(b) Salmon farm, where the high stocking densities are ideal habitats for the transmission of the copepods (with a direct life cycle) from one host to another.
Reproduced by permission of The Atlantic Salmon Trust. (c) A cod with a cleaner fish, preying on ectoparasites like copepods. Reproduced by permissionof
Alexandra Grutter.
Plant host
Introduced parasitoid:
Control agent
Target pest
Native hyperparasitoids
Figure 6 Example of a parasitoid, introduced to control a plant pest,
which then became host to native parasitoids, thus becoming
hyperparasitoids. The cassava plant is defoliated by the South American
mealybug, an unwanted herbivore. As a control for this pest, a parasitoid
from the order Hymenoptera was introduced. This parasitoid, in turn, was
exploited by 10 native species of parasitoids.
Parasites as Prey
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6
can infect the ‘good’ parasite that was initially introduced
for pest control. For example, a nonindigenous wasp of the
order Hymenoptera is used to protect cassave plants from
the South American mealybug in Africa (Herren and
Neuenschwander, 1991;
Figure 6
). The original infection
success of the wasp was so high that even the defence
mechanisms of the mealybug did not stop the biological
control (Sullivan and Neuenschwander, 1988). However,
the new wasp was soon itself used as a host by at least 10
native species of hyperparasitoids. The native wasps infect
the introduced control agent in occasional but very high
levels despite, on average, having no detrimental effect on
the control efficiency (Neuenschwander, 1996).
Conclusion
The examples above demonstrate that there are numerous
ways of how parasites can act as prey for other organisms.
In many cases, predation on parasites can have important
consequences for parasite population dynamics, the
infection burden of their hosts and possibly also for the
energy intake of nonhosts. The few studies that integrated
predation on parasites as trophic links in food web studies
indicate that such predation is very common. Studying the
strength of these links in future studies will increase our
understanding of disease dynamics as well as the topology
and functioning of food webs.
References
Achinelly MF, Micielli MV and Garcia JJ (2003) Pre-parasitic
juveniles of Strelkovimermis spiculatus Poinar and Camino,
1986 (Nematoda: Mermithidae) predated upon by freshwater
copepods (Crustacea: Copepoda). Nematology 5: 885–888.
Bushbaum C, Buschbaum G, Schrey I and Thieltges DW (2007)
Shell-boring polychaetes affect gastropod shell strength and
crab predation. Marine Ecology Progress Series 329: 123–130.
Connors BM, Hargreaves B, Jones SRM and Dill LM (2010)
Predation intensifies parasite exposure in a salmonid food
chain. Journal of Applied Ecology 47: 1365–1371.
Costello MJ (2009) How sea lice from salmon farms may cause
wild salmonid declines in Europe and North America and be a
threat to fishes elsewhere. Proceedings of the Royal Society –
Biological Sciences 276: 3385–3394.
Deady S, Varian S and Fives JM (1995) The use of cleaner-fish to
control sea lice on 2 Irish salmon (Salmo salar) farms with
particular reference to wrasse behavior in salmon cages.
Aquaculture 131: 73–90.
English AW (1979) The effects of dung beetles (Coleoptera-
Scarabaeinae) on the free-living stages of strongylid nematodes
of the horse. Australian Veterinary Journal 55: 315–321.
Ferreira SR, de Arau´ jo JV, Braga FR et al. (2011) Biological
control of Ascaris suum eggs by Pochonia chlamydosporia fun-
gus. Veterinary Research Communications 35: 553–558.
Forshay KJ, Johnson PTJ, Stock M, Alva CP and Dodson SI
(2008) Festering food: chytridiomycete pathogen reduces
quality of Daphnia host as a food resource. Ecology 89: 2692–
2699.
Grutter AS (1996) Parasite removal rates by the cleaner wrasse
Labroidesdimidiatus.Marine EcologyProgress Series 130:61 –70.
GrutterAS (1999) Cleaner fishreally do clean. Nature 398:672–673.
Grutter AS, Crean AJ, Curtis LM et al. (2011) Indirect effects of
an ectoparasite reduce successful establishment of a damselfish
at settlement. Functional Ecology 25: 586–594.
Hart BL, Hart LA and Mooring MS (1990) Differential foraging
of oxpeckers on impala in comparison with sympatric antelope
species. African Journal of Ecology 28: 240–249.
Hechinger RF, Wood AC and Kuris AM (2011) Social organ-
ization in a flatworm: trematode parasites from soldier and
reproductive castes. Proceedings of the Royal Society B 278:
656–665.
Herren HR and Neuenschwander P (1991) Biological control
of cassava pests in Africa. Annual Review of Entomology 36:
257–283.
Johnson PTJ, Dobson A, Lafferty KD et al. (2010) When parasites
become prey: ecological and epidemiological significance of
eating parasites. Trends in Ecology and Evolution 25: 362– 371.
Johnson PTJ, Stanton DE, Preu ER, Forshay KJ and Carpenter
SR (2006) Dining on disease: how interactions between infec-
tion and environment affect predation risk. Ecology 87: 1973–
1980.
Johnson PTJ and Thieltges DW (2010) Diversity, decoys and the
dilution effect: how ecological communities affect disease risk.
Journal of Experimental Biology 213: 961–970.
Kaplan AT, Rebhal S, Lafferty KD and Kuris AM (2009) Small
estuarine fishes feed on large trematode cercariae: lab and field
investigations. Journal of Parasitology 95: 477–480.
Karagoz M, Gulcu B, Cakmak I, Kaya HK and Hazir S (2007)
Predation of entomopathogenic nematodes by Sancassania sp.
(Acari: Acaridae). Experimental & Applied Acarology 43:
85–95.
Krkos
ˇek M, Ford JS, Morton A et al. (2007) Declining wild sal-
mon populations in relation to parasites from farm salmon.
Science 318: 1772–1775.
Kuris AM, Hechinger RF, Shaw JC et al. (2008) Ecosystem
energetic implications of parasite and free-living biomass in
three estuaries. Nature 454: 515–518.
Lafferty KD, Allesina S, Arim M et al. (2008) Parasites in food
webs: the ultimate missing links. Ecology Letters 11: 533–546.
Lafferty KD, Dobson AP and Kuris AM (2006a) Parasites
dominate food web links. Proceedings of the National Academy
of Sciences of the USA 103: 11211–11216.
Lafferty KD, Hechinger RF, Shaw JC, Whitney KL and Kuris
AM (2006b) Food webs and parasites in a salt marsh ecosys-
temCollinge S and Ray C (eds) Disease Ecology: Community
Structure and Pathogen Dynamics, pp. 119–134. Oxford:
Oxford University Press.
Lafferty KD and Morris AK (1996) Altered behavior of parasit-
ized killifish increases susceptibility to predation by bird final
hosts. Ecology 77: 1390–1397.
Lewis PD Jr. (1977) Adaptations for the transmission of species of
Leucochloridium from molluscan to avian hosts. Proceedings of
the Montana Academy of Sciences 37: 70–81.
Mouritsen KN and Poulin R (2003) Parasite-induced trophic
facilitation exploited by a non-host predator: a manipulator’s
nightmare. International Journal of Parasitology 33: 1043– 1050.
Parasites as Prey
eLS &2012, John Wiley & Sons, Ltd. www.els.net
7
Neuenschwander P (1996) Evaluating the efficiency of biological
control of three exotic homopteran pests in tropical Africa.
Entomophaga 41: 405–424.
O
¨stlund-Nilssen S, Becker JHA and Nilsson GE (2005) Shrimps
remove ectoparasites from fishes in temperate waters. Biology
Letters 1: 454–456.
Pietrock M and Marcogliese DJ (2003) Free-living endohelminth
stages: at themercy of environmental conditions. Trends in
Parasitology 19: 293–299.
Pike AW and Wadsworth SL (1999) Sealice on salmonids: their
biology and control. Advances in Parasitology 44: 233–337.
Roth M, Richards RH and Sommerville C (1993) Current prac-
tices in the chemotherapeutic control of sea lice infestations in
aquaculture: a review. Journal of Fish Diseases 16: 1–26.
Sa
´nchez MI, Thomas F, Perrot-Minnot M et al. (2009) Neuro-
logical and physiology disorders in Artemia harboring
manipulative cestodes. Journal of Parasitology 95: 20–24.
Sullivan DJ and Neuenschwander P (1988) Melanization of eggs
and larvae of the parasitoid, Epidinocarsis lopezi, (Hymen-
optera: Encyrtidae), by the cassava mealybug, Phenacoccus
manihoti Matile-Ferrero (Homoptera: Pseudococcidae). Can-
adian Entomologist 120: 63–71.
Sullivan DJ and Vo
¨lkl W (1999) Hyperparasitism: Multitrophic
Ecology and Behavior. Annual Review of Entomology 44:
291–315.
Thieltges DW, de Montaudouin X, Fredensborg B et al. (2008a)
Production of marine trematode cercariae: a potentially over-
looked path of energy flow in benthic systems. Marine Ecology
Progress Series 372: 147–155.
Thieltges DW, Jensen KT and Poulin R (2008b) The role of biotic
factors in the transmission of free-living endohelminth stages.
Parasitology 135: 407–426.
Treasurer J (1994) Prey selection and daily food consumption by a
cleaner fish, Ctenolabrus rupestris (L.), on farmed Atlantic sal-
mon, Salmo salar L. Aquaculture 122: 269–277.
Waghorn TS, Leathwick DM, Chen LY, Gray RAJ and Skipp RA
(2002) Influence of nematophagous fungi, earthworms and
dung burial on development of the free-living stages of Oster-
tagia (Teladorsagia) circumcincta in New Zealand. Veterinary
Parasitology 104: 119–129.
Waldie PA, Blomberg SP, Cheney KL, Goldizen AW and Grutter
AS (2011) Long-Term Effects of the Cleaner Fish Labroides
dimidiatus on Coral Reef Fish Communities. PLoS ONE 6:
1–7.
Wesenberg-Lund C (1934) Contributions to the development of
the trematode digenea. II. The biology of the freshwater cer-
cariae in Danish freshwater waters. Det Konglige Danske
Videnskapernes Selskabs Naturvidenskabelige og Mathematiske
Afhandlinger 9: 1–223.
Further reading
Johnson PTJ, Dobson A, Lafferty KD et al. (2010) When parasites
become prey: ecological and epidemiological significance of
eating parasites. Trends in Ecology and Evolution 25: 362– 371.
Keesing F, Belden LK, Daszak P et al. (2010) Impacts of bio-
diversity on the emergence and transmission of infectious
diseases. Nature 468: 647–2010.
Keesing F, Holt RD and Ostfeld RS (2006) Effects of species
diversity on disease risk. Ecology Letters 9: 485–498.
Thieltges DW, Jensen KT and Poulin R (2008) The role of biotic
factors in the transmission of free-living endohelminth stages.
Parasitology 135: 407–426.
Parasites as Prey
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