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Parasites as prey
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Anouk Goedknegt, Jennifer Welsh, David W Thieltges
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NIOZ Royal Netherlands Institute for Sea Research, Texel, The Netherlands
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For: Encyclopedia of Life Sciences
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Article ID: A23604
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Level
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undergraduates, graduate students, postgraduates, and researchers reading
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Abstract
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Parasites are usually considered to use their hosts as a resource for energy.
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However, there is increasing awareness that parasites can also become a
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resource themselves and serve as prey for other organisms. Here we describe the
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various forms of predation on parasites and discuss their relevance for parasite
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and host populations as well the benifist that parasite predators may gain.
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Article Contents
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
Introduction
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
Predation and transmission
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Concomitant predation
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Predation on free-living stages
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Predation on ectoparasites
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Parasites as consumers of parasites
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Summary
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Introduction
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In ecological studies, parasites are usually not considered to serve as prey or a
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resource for other organisms. Instead, by definition, they use other organisms as
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a resource themselves. However, recent studies on food webs including parasites
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have shown that parasites are involved in 75% of the trophic links between
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species, including many links where they serve as a resource themselves
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(Lafferty, 2006). There are several different ways in which parasites can be
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involved in trophic links in food webs. First of all, many parasites depend on the
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predation of their hosts for successful transmission to the succeeding down-
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stream host , thus hitch-hiking on predation links (trophic transmission).
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However, not all predators of infected organisms are suitable down-stream hosts
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and parasites may thus be “accidentally” and indirectly consumed by predators
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and therefore, not result in a successful transmission. Parasites may also directly
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become prey during free-living stages of thei complex life cycle. Many species of
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parasites need multiple hosts to complete their life cycle and include free-living
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stages to get from one host to the next. In this free-living stage, parasites are
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extremely vulnerable to predation by non-host predators. Another type of direct
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predation on parasites involves parasites that attach themselves to the outside of
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their hosts (ectoparasites). Ectoparasites may also be vulnerable and can be
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consumed by other animals. Finally, parasites can also serve as prey or host
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resources for other parasites. In the following, we explain the different cases
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where parasites become prey and discuss the ecological effects of predation on
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parasites for the parasites, their hosts and the predators.
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See also: Here we should add links to other articles in the encyclopedia (at least
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they asked for it last time). Maybe you can just enter a few links now and leave
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the rest for later. We will have to revise the draft after the review process anyway
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and then there will be a good opportunity. These “see also” links could also be
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added later in the text, e.g. always at the end of a chapter to not mess up the
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text too much.
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Predation and transmission
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Trophic transmission
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By definition, parasites are always dependent on the presence of their hosts as all
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parasites have to transmit from one host to another at some point in their lives.
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They do so by an infective stage, which is often free-living, whereby the parsite
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isreleased from a host into the environment., If the parasite has a direct life
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cycle, the infective stage can infect conspecific hosts or, in the case of parasites
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with complex life cycles, other hosts. The latter types of parasites often include
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more than one free-living stage in their life cycle by which the parasites goes
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through a specific sequence of parasitic stages in hosts and free-living stages.
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This is illustrated by the typical three-host life cycle of digenan trematodes, a
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type of parasitic flat worm which are often referred to as ‘flukes’ (Fig. 1). In these
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trematodes, infection of the next hosts in the life cycle (down-stream hosts) not
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only occurs via free-living infective stages (definitive host to first intermediate
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host and first to second intermediate hosts) but also via predation of infected
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hosts (second intermediate host to definitive hosts). The second intermediate
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host (up-stream host; a bivalve in Fig. 1) needs to be consumed by the definitive
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host (the downstream host; a bird in Fig. 1) before the parasite can develop into
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its adult stage and reproduce. In this life cycle stage, predation of its up-stream
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host is the only way for the parasite to successfully complete its life cycle. Almost
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all parasites with complex life cycles follow predator-prey links and depend on
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trophic transmission at some point in their lives; thus predation and transmission
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are intricately linked for many parasites (Lafferty et al., 2008). The importance of
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trophic transmission for parasites is illustrated in a food web from a saltmarsh in
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California, where a third of the parasite species consumed by predators via their
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prey use the predator as host (Lafferty et al., 2006). Is this figure really correct?
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“Concomitant predation” is ONLY predation by non-hosts!
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Parasites manipulate hosts to increase transmission
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[The reviewers might suggest to cut this paragraph as it has nothing really to do
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with parasites as prey, although it is a nice story. For now, I would leave it in and
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just wait what they say.]
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As predation by down-stream hosts is often crucial for the successful transmission
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of parasites, many parasite species have developed strategies to increase their
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chances to become transmitted via manipulating the behaviour of their hosts. For
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example, one trematode species encysts itself in the brain of killifish, an
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important prey item for birds in the estuaries of California. When a killifish
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becomes infected, it exhibits behaviours that make it more conspicuous (e.g.
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surfacing or flashing), making the fish 10-30 times more vulnerable for predation
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by birds, the definitive host of the parasite (Lafferty and Morris, 1996). Another
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example is that of the so-called ‘zombie snails’. These snails are infected by a
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trematode that uses birds as definitive host (Lewis, 1977). When a snail is
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infected by a parasite egg, the egg transforms/develops into a sporocyst, which
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contain hundreds of parasitic clones (also called ‘brood-sacs’), which
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subsequently invade the snail’s tentacles. As the tentacles become more swollen
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and colourful they start to mimic the appearance of a caterpillar. This alteration to
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the host caused by the parasite lures birds to eat the tentacles of the snail host
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and can result in the parasite infecting the bird. The parasite also has another
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tactic to increase the likelihood of predation by the bird. The infection of the
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parasite in the tentacles reduces the ability of the snail to react to light intensity.
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As a result, the snail may no longer hide in the shadow as it would do normally
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and, therefore, it is more visible for predators.Furthermore, the brood-sacs in the
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tentacles start to pulsate in response to light intensity (Wesenburg-Lund, 1931),
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making the resemblance to a caterpillar even more likely. These examples
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illustrate that parasites can mediate overall predation rates and predator prey
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choice, depending on the infection levels in a host population. By doing so, they
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can also affect the flow of energy through a food web.
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Concomitant predation
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Trophic transmission gone wrong
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Predation of infected hosts does not always lead to a successful transmission. In
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most cases, the predator will actually be an unsuitable host for the parasite. In
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this case, the potential (but unsuitable) host acts as a predator, leading to
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consumption rather than transmission of the parasite (Johnson et al., 2010). In
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the example of the trematode life cycles (Fig. 1), first or second intermediate
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hosts as well as the definitive hosts may be preyed on by non-host predators,
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consuming the parasites together with their prey without becoming infected. This
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type of accidental predation has been termed concomitant predation (Johnson et
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al. 2010; black arrows in Fig. 1). For trophically transmitted parasites, this seems
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like an unavoidable side effect of being dependent on predation links for
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transmission: whilst predation will sometimes ensure transmission it will probably
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more often lead to ending up in the wrong host. Interestingly, concomitant
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predation does not need to lead to the total consumption of the host. For
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example, one trematode species prevents New Zealand cockles (Austrovenus
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stutchburyi) from burying in the sediment (via encysting in the cockle’s foot and
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interfering with the musculature) so that they lay on the sediment surface where
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they are more vulnerable to predation by birds than their un-infected conspecifics
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buried in the sediment (Mouritsen and Poulin, 2003). This is usually interpreted
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as a case of parasite manipulation as the parasite’s down-stream definitive hosts
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are birds. However, infected cockles on the sediment surface are often not
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completely eaten by birds (suitable hosts) but partially consumed by benthic
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fishes (unsuitable hosts): fishes feed on the highly infected tip of the cockles’
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feet, a behaviour that is referred to as foot cropping. In manipulative
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experiments, the scientists found that this partial foot cropping by fish occurs to
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such an extent that it exceeds total predation by birds. As a result, only 2.5% of
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the parasites are actually transferred to their down-stream hosts, while 17.1%
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are lost to the fish (Mouritsen and Poulin, 2003; Fig. 2).
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Increased parasite mortality and changes in prey quality
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The cockle example illustrates how concomitant predation can significantly
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contribute to parasite mortality. Food web studies that include parasites suggest
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that about 63% of the links, where a predator consumes infected hosts, lead to
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concomitant predation because the predator is an unsuitable host but only about
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37% of these links result in the transmission of parasites (Lafferty et al 2006,
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Collinge book chapter). However, to date, little is known on the actual magnitude
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of concomitant predation on parasite population dynamics.
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For a predator, concomitant predation may result in a food resource with higher
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nutritional value, specifically when the host is highly infected. However, again, to
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date there are no studies regarding the potential energy gain that predators get
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from consuming parasites alongside their actual prey. In contrast, more is known
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on the effects of parasites on the general energetic value of their hosts. Infected
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prey may have a reduced or increased quality as a resource for predators,
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depending on the parasite-host system. For example, brine shrimps which are
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infected by tapeworm larvae have a higher energy content compared to
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uninfected conspecifics (Sánchez et al. 2009). In contrast, fungal infections of
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Daphnia reduce the energetic value of infected hosts for their juvenile fish
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predators (Forshay et al. 2008).
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Besides directly affecting the energetic value of their hosts, parasites may also
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have indirect effects on predation rates of predators. Similar to the host
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manipulation in trophically transmitted parasites discussed above, parasites may
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influence predator-prey interactions in non-host predators. They can do so by
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making their hosts more vulnerable to predation. For example, Daphnia water
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fleas are more likely to be predated on by fish predators when they are infected
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by a fungi, but the fish do not serve as down-stream hosts (Johnson et al., 2006).
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As a consequence of the infection, the body cavity of Daphnia is filled with
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thousands of dark sporangia, reducing its transparency and making it more
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visible for fish predators. Another example of how parasites can influence
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predator-prey interactions is the case of the shell-boring polychaete Polydora
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ciliata. This worm weakens the shell of the marine periwinkle Littorina littorea,
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making infected snails more vulnerable to predators. Interestingly, shore crabs
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make use of this weakness, preferring infected snails over uninfected snails
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(Buschbaum et al., 2007).
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Predation on free-living stages
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Vulnerable life cycle stage
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As discussed above, some parasites have life cycle stages which occur in a host
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and other stages whereby the parasite is living freely in the environment (Fig. 1).
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Once outside the protection of a host, these free-living stages are vulnerable to
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various abiotic and biotic factors (for abiotic examples: Pietrock & Marcogliese;
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Thieltges et al., 2008). For example, surrounding organisms can prey upon the
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free-living stages, thereby reducing them in numbers. Some predators prey
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actively on these free-living stages such as juvenile crab and shrimp, while others
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predate in a more passive way such as filter feeders. As a result, the infection
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levels in the down-stream hosts decrease. This process is called the ‘dilution
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effect’ and has been reported in many different parasite-host systems (Thieltges
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et al., 2008a; Johnson & Thieltges 2010). Instead of direct predation, free-living
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parasites can also be ingested together with a totally different food source. For
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instance, dung beetles and earth worms frequently ingest eggs and larvae of
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parasitic nematodes when feeding on faeces of other organisms (English 1979;
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Waghorn et al., 2002).
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Effects on parasites and application in pest control
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Many studies suggest that the various forms of predation on free-living stages are
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an important mortality factor for parasites. Predators can, therefore, be very
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effective in reducing numbers of free-living stages of parasites. For example,
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copepods can reduce the number of juvenile nematodes [I do not have the paper,
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is it nematode eggs or larvae and where do they occur?]by 70-100%, depending
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on the species of copepod and their density (Archinelly et al., 2003). There are
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many other organisms that have been reported to significantly reduce infective
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stages of nematodes, either directly or indirectly via ingestion with other food
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(see Fig. 3 for examples). Similarly, many bivalves like oysters and mussels have
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been shown to be effective diluters, reducing the number of free-living stages of
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trematodes by almost 80% (Thieltges et al., 2008b).
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Such strong reductions in the numbers of infective parasite stages have important
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implications for pest control in agriculture and live stock farming. One example is
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the reduction of eggs of parasitic nematodes by a nematophagous fungi in the
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intestines of swines (Ferreira et al., 2011). Normally, the nematodes cause liver
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damage to the swine (“milk spots” caused by larvae), but the addition of a special
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fungi to the feed reduced the numbers of eggs by more than 50%. This is
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because the fungi excreted with the faeces reduce the numbers of eggs on the
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pasture (Fig. 3). [I am only guessing that this is the mechanism, if not the
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please correct. The fungi need to consume free-living stages at some point to
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qualify for this type of parasite predation. If you just give it to the swines like a
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drug it is not really parasite predation.]
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As free-living stages are usually produced in high numbers, they may also
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constitute an energy resource for predators preying on them. For example, the
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production of trematode cercariae in coastal marine systems exceeds the
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standing stock of birds (Kuris et al. 2008). Many organisms are known to prey on
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cercariae, suggesting that cercariae may be a significant energy source for some
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predators (Thieltges et al. 2008). However, actual data of the relevance of
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cercariae in the diet of non-hosts are restricted to juvenile fish in a Californian
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estuary where predation of cercariae was calculated to comprise approximately 2-
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3 % of the fishes’ energetic requirements (Kaplan et al. 2009).
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Predation on ectoparasites
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Grooming and cleaning
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Another case where parasites become prey is predation on ectoparasites, which
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are parasites that attach themselves to the outside of the body of a host. A
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classic example of predation on ectoparasites is grooming by monkeys. In this
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type of intraspecific interaction, one individual releases a second individual from
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fleas and other ectoparasites. This is beneficial for the monkey that is groomed,
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but it also strengthens the social bounding between both individuals. Similar
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examples are known from interspecific interactions, e.g. from oxpeckers which
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free mammals on the African savannahs of ticks (Grutter, 1999) and from cleaner
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shrimps and fishes which pick ectoparasites from fish hosts (Fry et al., 2000).
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Effects on parasites, hosts and predators
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For parasites, grooming and cleaning are probably often significant sources of
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mortality, with negative effects on parasite population dynamics. In contrast,
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grooming and cleaning are beneficial for both, the host and the predator: one
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species profits from the energy resource and the other species is released from its
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parasite pressure. Hence, this type of interaction can be considered to be
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mutualistic. The benefit for hosts can be illustrated in the case of cleaner fish that
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that feed on ectoparasites attached to the body of their clients. When these
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cleaner fish are absent over a longer period the hosts are negatively influenced by
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the ectoparasites. In a study over a 8.5 year period, Grutter et al. (2011a) found
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significantly smaller hosts in an area where no cleaner fish were present,
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suggesting that these hosts had to investigate their energy in their immune
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system rather than into growth (Grutter et al., 2011a). In addition, in the
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absence of cleaner fish, a reduction of 65% in visiting juvenile hosts was
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observed. The juveniles suffer from the absence of cleaner fish, as the
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ectoparasites have a negative influence in their performance as measured by
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swimming and oxygen consumption (Grutter et al., 2011b). The cleaning
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symbiosis is also very beneficial for the cleaners as ectoparasites may constitute
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a large part of their diet (Grutter 1996).
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Cleaner fish in aquaculture
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Ectoparasites can be a significant problem in aquaculture, where high stocking
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densities often provide ideal habitats for the parasites. A prominent example is
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ectoparasitic salmon lice (a copepod), which feed on the fish tissue and can cause
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morbidity and mortality (Pike and Wasworth, 1999; Fig. 4a). When a population
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of lice settles in thesea cages, where the salmon are raised (Fig. 4b), the
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parasites can spread easily due to a free-living life stage and the high densities in
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which the fish are kept, resulting in declines of salmon stocks in the cages
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[correct addition?] (Conners et al., 2010). Even more worrying is the fact that the
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free-living stages of the parasite can also spillover and infect wild populations of
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salmon, (Costello, 2009). This spill-over can cause up over 80% mortality in
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many runs of wild pink salmon, which frequently pass salmon farms on their way
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to the open ocean (Krkošek et al., 2007). Since salmon lice are such a problem,
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various treatments have been tested; however these compounds often have
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undesired effects on the fish or the environment (Roth et al., 1993). As an
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alternative, it has been suggested to add cleaner fish or shrimp into the net pens
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to reduce ectoparasite burden of the fish (Figure 4c). For example, scientists
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introduced two species of cleaner fish on two Irish salmon farms (Deady et al.,
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1995). By using a ratio of one cleaner fish to 250 salmon, the lice levels were
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kept below five lice per fish. In addition, the salmon were less stressed by this
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type of pest control than conventional chemical treatments. Furthermore, there
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are two species of cleaner shrimps that inhabit North-Atlantic shallow waters and
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remove ectoparasites from plaice (Östlund-Nilssen et al., 2005). These results
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suggest that cleaner shrimps and cleaner fish could be suitable as biological
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control agents for sea lice infections on salmon and other fish in aquaculture
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settings.
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Parasites as consumers of parasites
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Hyperparasitism and intraguild predation
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Finally, parasites can serve as a resource for other parasites, either by being
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parasitized by other parasites (hyperparasitism) or by being preyed by other
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parasites (intraguild predation). The first happens when a parasite infects another
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parasite. This is particularly well demonstrated within an order of Hymenoptera
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insects . These so-called hyperparasitoids often infect a primary parasitoid, which
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in turn infects a herbivorous or scavenger host (Sullivan and Völkl, 1999). The
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second happens when parasites kill and consume other parasites, often in order
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to get rid of potential competitors. For example, trematodes infecting snails as
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first intermediate host can be preyed on by other species of trematodes. Some of
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these predating species develop a special cast of small ‘soldier morphs’ with large
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mouths for this purpose. These ‘warrior’ worms attack other parasites trying to
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invade the snail host. Another morph of large worms acts as reproductive cast
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worms (Hechinger et al., 2011). Both morphotypes (?) are genetically identical as
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they are clones derived from a single miracidium infecting the host snail. Hence,
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this shows an analogy to the social organisation in colonies of ants or bees.
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Hyperparasitism and pest control
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The significant effect of hyperparasites on their hosts is illustrated by the effective
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use of insect hyperparasitoids as biological control agents against pest insects in
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agriculture. Here, they can be very efficient in controlling pest populations.
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However, there are also cases where hyperparasites can infect the ‘good’ parasite
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that was initially introduced for pest control. For example, a non-indigenous wasp
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of the order Hymenoptera is used to protect cassave plants from the South
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American mealybug in Africa (Herren and Neuenschwander, 1991; Fig. 5). The
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original infection success of the wasp was so high that even the defence
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mechanisms of the mealybugdid not stop the biological control (Sullivan and
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Neuenschwander, 1988). However, the presence of the new wasp got attention
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from at least ten native species of hyperparasitoids. They infect the introduced
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control agent in occasional but very high levels despite, on average, having no
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detrimental effect on the control efficiency (Neuenschwander, 1996).
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Summary
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The examples above demonstrate that there are numerous ways of how parasites
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can act as prey for other organisms: via predation of non-hosts on infected hosts
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(concomitant predation) or predation of free-living stages, via predation on
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ectoparasites in form of grooming or cleaning or by serving as prey (or host) for
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other parasites. In many cases, these types of predation significantly reduce the
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numbers of parasites and thus affect parasite population dynamics. In contrast,
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predation on parasites is often beneficial for the hosts as they are released from
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parasite burden. Finally, when parasites act as prey they may contribute to the
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non-host predator’s diet, in some cases constituting a significant proportion of the
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diet. Integrating the different types of predation on parasite as trophic links in
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food webs indicates that such predation is very common. Studying the strength of
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these links in future studies will increase our understanding of disease dynamics
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as well as the topology and functioning of food webs.
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References
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Add complete reference list here
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Check that references in the text match the references in the reference section
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Make sure formatting is uniform
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Check ELS Author Guidelines for their formatting requirements
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Sánchez, M.I. et al. (2009) Neurological and physiology disorders in
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Artemia harboring manipulative cestodes. J. Parasitol. 95, 20–24
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Grutter, A.S. (1996) Parasite removal rates by the cleaner wrasse
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Labroides dimidiatus. Mar. Ecol. Prog. Ser. 130, 61–70
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Forshay, K.J. et al. (2008) Festering food: chytridiomycete pathogen
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reduces quality of Daphnia host as a food resource. Ecology 89, 2692–
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2699
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Kaplan, A.T. et al. (2009) Small estuarine fishes feed on large
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trematode cercariae: lab and field observations. J. Parasitol. 95,
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477–480
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Further reading
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Any other ideas?
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Johnson, P.T.J., Dobson, A., Lafferty, K.D., Marcogliese, D., Memmott, J.,
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Orlofske, S.A., Poulin, R., Thieltges, D.W. (2010) When parasites become prey:
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Ecological and epidemiological significance of eating parasites. Trends in Ecology
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and Evolution 25: 362-371
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Johnson, P.T.J., Thieltges, D.W. (2010) Diversity, decoys and the dilution effect:
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how ecological communities affect disease risk. Journal of Experimental Biology
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213: 961-970
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Thieltges, D.W., Jensen, K.T, Poulin, R. (2008) The role of biotic factors in the
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transmission of free-living endohelminth stages. Parasitology 135: 407–426
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[Some figures still need a little fine-tuning, so these are not the final version. I
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will explain to Anouk in detail what needs to be changed]
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[Match the final colour in the figure with the one mentioned in legend]
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Figure 1: Example of a typical three-host life cycle of a trematode, showing the sequence
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of different hosts and free-living stages involved (thin arrows) and illustrating the different
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types of predation on them (thick arrows). In this case, the definitive host is a bird, from
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which the parasites release free-living eggs into the water together with the bird’s faeces.
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The eggs infect a first intermediate host (a gastropod), in which the parasite reproduces
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asexually in so-called sporocysts or rediae and releases a second free-ling stage into the
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water (cercariae). These cercariae infect a second intermediate host (a cockle) in which
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the parasites encyst (metacercariae). Finally, when the second intermediate host is
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consumed by the definitive host the life cycle of the parasite is completed. Parasites can
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become prey either when infected hosts are consumed by non-hosts (concomitant
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predation; grey thick arrows) or when their free-living stages are consumed (white thick
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arrows). Note that parasite consumption is also an essential part of the parasite’s life cycle
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when the infected second intermediate host is eaten by the definitive host.
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[Do you need copyrights for the little drawings?]
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Figure 2: Partial predation on infected hosts by a non-host predator. A
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trematode species infecting the New Zealand cockle impairs its burying ability so
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that cockles are exposed on the sediment, resulting in an increased predation by
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the definitive host compared to uninfected conspecifics . However, fish also
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partially prey on exposed infected cockles by nipping off the tip of the cockles’
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foot. Most parasites are concentrated in the foot tip and, since the fishes do not
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serve as down-stream hosts, a significant proportion of the parasites are lost via
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this concomitant predation.
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[Are my additions below correct?]
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Figure 3: Examples of the levels of reduction of infective free-living stages of parasitic
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nematodes by various organisms from different systems: earth worms (Grønvold, 1987;
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Waghorn et al., 2002) and dung beetles (English, 1979) preying on nematode eggs and
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larvae in dung, copepods preying on [what and where?] (Archinelly et al., 2003), mites
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[what and where?] (Karagoz et al., 2007) and nematophagous funghi on nematode larvae
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on livestock pasture (Ferreira et al., 2011).
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Figure 4: Typical ectoparasites of salmon in aquaculture and their consumption by cleaner
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fishes: a) salmon lice (parasitic copepods, the brown ectoparasites) infect salmon and
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cause damage to the skin, often leading to secondary infections (Copyright of Colin
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Kirkpatrick), b) salmon farm, where the high stocking densities are ideal habitats for the
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transmission of the copepods (with a direct life cycle) from one host to another (Copyright
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of The Atlantic Salmon Trust) an c) a cod with a cleaner fish, preying on ectoparasites like
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copepods (Copyright of A. Grutter).
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Figure 5: Example of a parasitoid, introduced to control a plant pest, which then became
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host to native parasitoids, thus becoming hyperparasitoids. The cassava plant is defoliated
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by the South American mealybug, an unwanted herbivore. As a control for this pest, a
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parasitoid from the order Hymenoptera was introduced. This parasitoid, in turn, was
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exploited by 10 native species of parasitoids.
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