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8
Biology and Ecology of
Perch Parasites
Jasminca Behrmann-Godel
1,
* and Alexander Brinker
2
ABSTRACT
The European perch Perca fl uviatilis (L.) and the yellow perch Perca fl avescens
(M.) are generalist feeders occupying a number of different habitats during their
life stages and are exposed to infection by a variety of ecto- and endoparasites.
We provide a short general overview of parasite ecology and introduce major
macroparasite groups including examples of relevant species infecting European
perch and yellow perch in their respective distribution ranges. We describe the
ways in which specifi c perch parasites impair host fi tness by measures like
growth, fecundity or mortality. Effects of parasites on adult and juvenile perch
are discussed separately and accompanied with specifi c examples from fi eld data
and laboratory experiments. The important role of both perch species as model
systems is discussed especially for the research areas of parasite host ecology and
evolution. Thereby we incorporate basic studies on both the European and yellow
perch although almost no comparative studies for both species exist which could
be a major aim for future research. We also review some long-term studies on
the European perch populations of Lake Constance as an instructive case study.
Keywords: European perch, yellow perch, parasite host co-evolution, parasite
life cycles, parasite community ecology, trophic linkage, fi tness constraints,
bioindicators, Perca fl uviatilis, Perca fl avescens
1
Limnological Institute, University of Konstanz, Mainaustrasse 252, 78457 Konstanz, Germany.
2
Fisheries Research Station Baden-Württemberg, Argenweg 50/1, 88085 Langenargen, Germany.
E-mail: Alexander.Brinker@lazbw.bwl.de
* Corresponding author: Jasminca.Behrmann@uni-konstanz.de
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194 Biology of Perch
8.1 Introduction
Almost every major group of organisms including viruses, bacteria, protists, higher
metazoans, fungi, plants and mammals has parasitic members and there are indications
that species with at least one parasitic phase in their life history may actually outnumber
non-parasites. Some parasites develop directly on or in their host, while others have
extremely complex life cycles involving a sequence of obligate hosts infected at
different stages of development. For a glossary of important parasitological terms
used in this chapter, see the Infobox. From a parasite’s point of view, the host can
be seen as its environment, providing a number of distinct habitats for colonization
(Bush et al. 1977). The many different ways in which parasites infect their hosts are
mostly specifi c to parasite species and/or life cycle stage. Infection may be direct as
in most trematode cercariae, which penetrate the host’s skin. However parasites can
also be transmitted actively by vectors or indirectly via the food chain—for example
Infobox: Parasitological terminology
Defi nition of Parasitism:
Parasites are organisms that benefi t at the expense of another organism belonging to another species,
called the host, mostly by trophic exploitation.
Life strategies of parasites:
Endoparasites live inside the body of the host, ectoparasites on the surface. Microparasites are
unicellular organisms such as bacteria and protozoa. Viruses may also be called microparasites.
Macroparasites are eumetazoa including fl atworms, nematodes, arthropods and several others.
Parasites that depend on a host for development are called obligate parasites. In contrast, a facultative
parasite can complete its life cycle without infecting a host. Organisms that are not typically parasitic
but can become so under certain specifi c conditions (e.g., immune defi ciency of the host) are called
opportunistic parasites.
Parasite life cycles:
A direct (monoxenous) life cycle can be found in parasites that exploit only one host for development.
An indirect or complex (heteroxenous) life cycle is realized when parasites depend on several hosts
for development. Sexual maturity and reproduction is always realized in the defi nitive (fi nal, primary)
host. One or several intermediate (secondary) hosts are needed for preceding stages of development,
which may involve asexual reproduction or metamorphosis to the next developmental stage. If the
intermediate or defi nitive host is used as a carrier to the next host it is typically called a vector. In
terrestrial systems most vectors are blood-feeding arthropods, for example insects such as mosquitoes.
They transmit the parasite (e.g., Plasmodium spp., which causes malaria) to the next host of the parasite´s
life cycle. Typical vectors in the aquatic environment (especially for fi sh) are blood-feeding arthropods
or annelids such as leeches. Some parasites may infect a host but do not undergo development. These
so-called paratenic (transport) hosts can be used for dispersal or to reach the next trophic level, which
often raises the parasite´s chance of being transmitted to the next host in the life cycle.
Population and community concepts (after, Bush et al. 1997):
All parasites of a given species in a single host individual are defi ned as the infrapopulation. All
infrapopulations of a given parasite species in a given host species in an ecosystem comprise the
component population. Finally, all component populations of a given parasite species in different host
species of its life cycle make up the supra population. Similarly, the sum of the infrapopulations of all
parasite species within a single host individual is known as the infracommunity. All infracommunities
of all parasite species in a given host species in an ecosystem make up the component community.
Finally the sum of all component communities in all life cycle hosts comprises the supra community.
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Biology and Ecology of Perch Parasites 195
as a result of predation on the infective stage of the parasite itself or when a predatory
host consumes an infected prey organism.
The major benefi ts of parasitism compared with a free-living lifestyle are shelter,
access to resources, the relatively stable environment provided by the host, energy
savings though not having to forage and the ease of transportation to new areas
(Combes 2001). However there are also disadvantages for parasites, most notably
the challenge of fi nding and successfully infecting host organisms (Combes 2001).
Many parasites have developed fascinating adaptations to overcome this problem,
for example manipulating host behavior or increasing host conspicuousness in order
to improve the likelihood of successful transmission to the next host (Moore 2002).
A further challenge is presented by the immune responses mounted by hosts in an
effort to repel parasitic invaders (Combes 2001). However, the strength and effi cacy
of the host immune response can be highly stage dependent. Generally, parasites tend
to provoke stronger immune responses in an intermediate host than in the defi nitive
host (Ewald 1995). Immune responses are often dependent on the feeding strategy
of the parasite and its exact location in or on the host’s body (Jones 2001; Alvarez-
Pellitero 2008). For example, skin-penetrating cercariae generally provoke a strong
host reaction whereas the immune response to parasites residing in the gut, such as
most adult tapeworms, is often rather weak (Woo 1992). Several parasite species are
able to manipulate host immunity, for example by down-regulating the strength of
the immune response (Goater et al. 2014).
Despite the localized pathology that can be infl icted on individual hosts even in
established parasite-host systems, the typically aggregate nature of parasite distribution
within a host population usually means that only a fraction of hosts are severely
affected. Negative effects such as reduced fecundity or survival tend to be observed
only in individual hosts where infection intensity is unusually high, and not, as a rule,
at the population level.
During recent decades, anthropogenic environmental change, in particular rises
in temperature, environmental pollution and introductions of new species, have been
shown to trigger negative changes in parasite-host interactions. Even small changes
may be deleterious, and the cumulative effect of multiple environmental stresses can
result in a signifi cant negative impact on immune function and animal health. For
example, a rise in temperature can prolong the period of parasite transmission and affect
the abundance and virulence of particular pathogens and parasites (Vidal-Martínez et
al. 2010; Marcogliese and Pietrock 2011). Increased pathogenicity of opportunistic
parasites mediated by increased virulence or a prolonged season can result in a serious
threat to fi sh populations. Furthermore, rising temperatures may also favor incursions
by alien parasites, which either enter the system directly as soon as temperature
limitation disappears or arrive via co-introduction with non-native intermediate hosts
(Marcogliese 2001; Poulin 2006; Paull and Johnson 2011). Introduced parasites may
cause epizootic outbreaks in naïve host populations, which lack adaptations to reduce
pathogenicity or to defend against the invaders (Marcogliese 2001; Britton et al. 2011;
Behrmann-Godel et al. 2014).
The extensive distribution of European and yellow perch and the wide range
of habitat and food sources utilized mean the number of described parasites for
these two species is correspondingly high. Information regarding Balkhash perch
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196 Biology of Perch
(Perca schrenkii) parasites is provided in Chapter 3 (Section 3.6). Therefore, the
information given in the following section is restricted to European (Perca fl uviatilis)
and yellow perch (Perca fl avescens). Several parasite species lists for European and
yellow perch exist in the literature (e.g., Craig 2000; Morozinska-Gogol 2008). From
these it can be seen that the biodiversity of perch parasites including myxozoan,
protozoan and metazoan parasites described today includes about 160 species for
yellow perch and 147 for European perch, 19 of which are shared by both species (Craig
2000). An additional high species number of parasitic bacteria and viruses affecting
perch can be assumed. Instead of repeating these lists, we aim to provide specifi c
information about the biology and ecology of the major parasite groups, illustrated
with specifi c examples of parasite species infecting perch and their impact on host fi sh
population. Throughout the chapter we will concentrate on protozoans, myxozoans and
macroparasites (hereafter called parasites) and exclude viruses, bacteria and fungi. We
will begin with general information about the broad spectrum of parasites and illustrate
the ways in which ecological factors enhance and limit the number of parasite species
infecting host species in general and perch specifi cally. We will follow by focusing on
some specifi c parasite species and illustrate their negative impacts on adult and larval
European perch. Finally we review the role of perch parasites in providing insights
into the ecology and evolution of host-parasite interactions.
8.2 Parasites—The Hidden Biodiversity On and Within Perch
The defi nition of ecology as the relationship between an organism and its biotic and
abiotic environment means parasitism has to be seen as an ecological concept (Goater
et al. 2014). In addition to the wider environmental factors also faced by free-living
organisms, parasites must also deal with challenges arising from their habitat being
another organism. Environmental factors infl uencing the host’s ecology impact
simultaneously on the parasite, which also has to deal with factors such as continuous
attack from the host immune system (Buchmann et al. 2012; Dezfuli et al. 2014). As
with free-living organisms, parasites have basic needs for space, nutrition and shelter
and requirements for reproduction and survival, which combine to form a specifi c
niche, and restrict the parasite to particular habitats on or within the host organism.
Likewise, the distribution ranges of both free-living and parasitic organisms are
limited by factors such as dispersal ability, tolerance to environmental variability and
interaction with other species. For parasites, these factors translate to the availability
of suitable life cycle hosts, the geographical limitations on transmission, an ability
to adapt to host immune reactions and interspecifi c competition with other parasites
attempting to exploit the same host individual. These requirements and limitations
have a number of observable consequences: (1) the geographic occurrence of parasites
is highly variable, (2) parasites tend to be specialists, with evolutionary adaptations
that allow them to explore a single or very restricted range of host species, and (3) the
behavioral, morphological and physiological adaptations of parasites also restrict them
to specifi c sites, tissues or organs on or within hosts (see Poulin 1998; Goater et al.
2014). This last point is especially helpful for parasitologists, fi sh farmers and aquarium
hobbyists, in taking advantage to locate and identify particular parasite species on
or in an infected host. Figure 1 shows such a typical “distribution map” for parasite
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Biology and Ecology of Perch Parasites 197
Fig. 1. Component parasite community from European perch in Lake Constance, Germany, indicating the site specifi city on or in their host. Each parasite species occupies
a specifi c and predictable habitat (organ or tissue).
Gills
Myxospora
Oodinium
Piscicola geometra
Gyrodactylus sp.
Argulus
foliaceus
Kidney
Cotylurs pileatus
Ichthyocotylurus
variegatus
Mesenteries (peritoneum, swim bladder wall)
Cotylurs pileatus Ichthyocotylurus
variegatus
Intestine
Bunodera luciopercae
Acanthocephalus
lucii
Pomphorhynchus
laevis
Hysteromorpha triloba
Proteocephalus percae
Ancyrocephalus
percae (adult)
Triaenophorus
nodulosus
Ancyrocephalus percae
(postoncomiracidium)
Diplostomum
baeri
Thylodelphis
clavata
Ergasilus sieboldi
Eye
Liver
Isthmus
Body surface, fi ns
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198 Biology of Perch
species occurring in a parasite component community (see Infobox for defi nition) of
European perch from Lake Constance in Germany. However, only a subset of these
species will contribute to the infracommunity (see Infobox for defi nition) present in
an individual host.
Goater et al. (2014) describe parasite community composition and species richness
in terms of supply and screens (after Combes 2001). ‘Supply’ refers to the availability
of parasite species from a global pool, the contents of which determine which species
are theoretically available at a regional level. ‘Screens’ are biotic and abiotic factors
that restrict or exclude specifi c parasites from particular localities and thereby control
the composition of the local pool and ultimately the composition of the component-
and infracommunities within the local pool (Fig. 2). Abiotic factors acting as screens
may include pH, salinity, drought, acid rain or host extinctions. Biotic features might
be the feeding habits of hosts, host immunology, species interactions or phylogeny,
including recent and contemporary coevolution between parasites and hosts and host
specifi city. Thus the parasite species found in any infra- or component community
are usually only a subset of those available within the local parasite pool, and these
are in turn always only a subset of a theoretical maximum of parasites available in
the global parasite pool.
Thus parasite species richness and abundance vary greatly, not only between host
species but also among host populations of the same species in different habitats or
geographic locations (Johnson et al. 2004). Additional factors infl uencing parasite
species richness for a particular host are its physical size (body length or mass),
geographical range and population density. Increases in host size, geographical range
or density have been shown to correlate positively with parasite species richness
Fig. 2. The relationship between parasites present in the global pool and two different local pools. Letters
represent individual parasite species available in the different pools. Supply dictates which species are
available in the two different regional pools I and II, while screens determine which are available in the
local pools. Light grey ellipses within the local pools represent component communities of parasites (see
text for a more detailed explanation). Figure was redrawn from Goater et al. (2014).
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Biology and Ecology of Perch Parasites 199
(Poulin and Morand 2004). However the commonality of these rules cannot be taken
for granted, given the lack of information concerning most parasite host systems and
a number of confounding results (Goater et al. 2014).
Both European and yellow perch are distributed in a broad geographic range
including fresh, brackish and salt-water habitats. Both species are generalist feeders,
taking many different food taxa from a variety of trophic levels (including algae,
zooplankton, benthic invertebrates and fi sh), and shift between habitats (pelagic to
littoral zones) during ontogenetic development (Coles 1981; Wang and Eckmann 1994;
Wang and Appenzeller 1998; Craig 2000). Furthermore, both species can occur in
very dense populations, in particular during spawning migrations (Craig 2000). Thus
despite potential uncertainties, we would expect parasite species richness for European
and yellow perch to be high on a global as well as a local scale. Additionally, we
would expect to fi nd them hosting parasites with a broad range of infection strategies
including direct infection and indirect routes such as predator-prey interactions and
transmission by consumption of intermediate hosts from a range of trophic levels.
These expectations have been borne out in many investigations, documenting species
rich parasite component communities for each perch species (Andrews 1979; Carney
and Dick 1999, 2000a; Morozinska-Gogol 2008) as shown in Fig. 1 and Table 1.
Besides a few very common parasite species that appear in almost all component
communities of yellow and European perch (Carney and Dick 1999), the precise
composition of the local parasite pool available at a particular sampling location within
a given ecosystem remains highly unpredictable. Thus the parasite communities of
perch have been found to vary considerably between ecosystems in close geographical
proximity to one another, between sampling years at the same location (Poulin and
Valtonen 2002; Johnson et al. 2004) and between contemporary host populations
within the same ecosystem (Fig. 3).
Parasite identifi cation is not a trivial task and specialists are often required for
accurate species determination. The taxonomic determination of non-model organisms
can prove especially diffi cult and time-consuming, increasingly so when working with
the early developmental stages of host fi sh. The study of parasite infections in fi sh fry
presents particular challenges. The young age of the hosts mean that any infection
observed must be very recent, and the parasites themselves are therefore in early
stages of development (Kuchta et al. 2009) and may lack important morphological
characteristics required for identifi cation. Classically, this problem has been addressed
with life-cycle studies including experimental infections. However, such studies are
laborious and usually limited to small numbers of congeneric parasites. Molecular
identifi cation techniques based on sequences of nuclear genes such as ribosomal rRNA
and the mitochondrial cytochrome oxidase gene can be helpful in otherwise tricky
species diagnoses (Zehnder and Mariaux 1999; Scholz et al. 2007; Sonnenberg et al.
2007; Locke et al. 2010a,b). A combination of classical morphological analysis and
genetic surveys of various parasite life-cycle stages sampled from a range of hosts
has proved helpful in identifying early developmental stages of parasites in perch fry
and in elucidating the typical parasite succession during perch ontogeny (Behrmann-
Godel 2013) (Table 2). In addition, genetic surveys have provided new insights into
parasite transmission pathways between several fi sh species and their parasites within
the study area (Behrmann-Godel 2013).
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200 Biology of Perch
Table 1. Examples of component communities of macroparasites for European perch Perca fl uviatilis sampled in Lake Constance, Germany (oligotrophic lake, surface area
536 m
2
, mean depth 90 m) and yellow perch Perca fl avescens from Dauphin Lake, Manitoba (eutrophic to mesotrophic lake, surface area approximately 520 m
2
, mean depth
3.5 m) (Data from Carney and Dick 2000a). Prev = prevalence (percent of infected fi sh); Mean int. = mean intensity (mean number of parasites per infected host individual).
Perca fl uviatilis Lake Constance 2008 (n = 255) Perca fl avescens, Dauphin Lake 1993 (n = 102)
Parasite Route of infection Site of
infection
Prev
[%]
Mean
int.
Parasite Route of
infection
Site of
infection
Prev
[%]
Mean
int.
Monogenea
Ancyrocephalus percae*
Direct Gills, isthmus 67 23
Urocleidus adspectus
Direct Gills 26 8
Gyrodactylus gasterostei
Direct Body surface 7 6
Digenea/Trematoda
Bunodera luciopercae
Cladoceran/
amphipod
ingestion
Intestine 99 155
Crepidostomum cooperi
Benthic insect
larv. ingestion
Intestine 37 54
Cotylurus pileatus
Cercarial
penetration
Mesenteries 92 33
Centrovarium lobotes
Fish ingestion Intestine 9 6
Ichthyocotylurus variegatus
Cercarial
penetration
Mesenteries 79 48
Clinostomum spp.
Cercarial
penetration
Flesh 2 2
Hysteromorpha triloba
Cercarial
penetration
Mesenteries 30 4
Apophallus spp.
Cercarial
penetration
Flesch and fi ns 33 5
Diplostomum spp.
Cercarial
penetration
Eye 99 31
Diplostomum spp.
Cercarial
penetration
Eye 22 4
Tylodelphys
clavata
Cercarial
penetration
Vitreous
humor
100 193
Neochasmus spp.
Cercarial
penetration
Eye and fl esh 25 3
Phyllodistomum pseudofolium
Cercarial
penetration
Urinary
bladder
1 3
Cestoda
Triaenophorus nodulosus
Copepod
ingestion
Liver
93
5
Triaenophorus nodulosus
Copepod
ingestion
Liver 9 1
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Biology and Ecology of Perch Parasites 201
Proteocephalus percae
Copepod
ingestion
Intestine 88 18
Proteocephalus
pearsi
Copepod
ingestion
Intestine 24 26
Eubothrium crassum
Copepod
ingestion
Intestine 29 4
Bothriocephalus cuspidatus
Copepod
ingestion
Intestine 12 21
Ligula
intestinalis
Copepod
ingestion
Body cavity 1 1
Acanthocephala
Pomphorhynchus laevis
Amphipod
ingestion
Intestine 1 3
Pomphorhynchus
bulbocolli
Amphipod
ingestion
Intestine 4 2
Acanthocephalus lucii
Amphipod
ingestion
Intestine 7 9
Acanthocephalus anguillae
Amphipod
ingestion
Intestine 0.4 5
Nematoda
Raphidascaris
acus
Insect larvae, fi sh
ingest.
Liver and
mesentery
1 1
Raphidascaris
acus
Insect larvae fi sh
ingest.
Liver mesen-
tery
66 13
Angullicoloides crassus
Copepod
ingestion
Swim bladder 0.4 1
Spinitectus
gracilis
Insect larvae
ingestion
Intestine 27 4
Hirudinea
Piscicola
geometra
Direct Body surface 1 1
Myzobdella
moorei
Direct Fins and body
surface
25 3
Arthropoda/Crustacea
Ergasilus
sieboldi
Direct Gills 13 3
Ergasilus
luciopercarum
Direct Gills 14 3
Argulus
foliaceus
Direct Body surface 7 2
*A. percae is an invasive parasite fi rst documented in Lake Constance in 2012 in a study of examining n = 539 adult European perch (data from Behrmann-Godel et al. 2014).
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202 Biology of Perch
8.3 Parasites of Perch
8.3.1 Protozoa
The protozoan parasites of fi sh include both ecto- and endoparasites. Among the
endoparasitic species, the blood fl agellates of the genera Trypanosoma, Cryptobia
and Trypanoplasma spp. are of special importance. Most have a complex life cycle
including transmission by a vector. In the case of protozoan fi sh parasites this is
typically a leech, for example Piscicola geometra for European perch (Markevich
1963; Goater et al. 2014).
The ectoparasitic protozoa fall into three categories: First, there are opportunists
with limited persistence as parasites. These are typically secondary infectors that
mainly parasitize stressed or immune-depressed fi sh, for example ciliates of the
genera Ophryoglena, Tetrahymena, Hemiophrys and Glaucoma. A second category
includes ubiquitous parasites lacking host or site preference, for example the fl agellate
Ichthyobodo necator (formerly Costia necatrix), ciliates of the genus Chilodonella
spp., Ichthyophtirius multifi lis (commonly called “white spot”, “ick” or “ich”), and
several ubiquitous species of Trichodina and Tripartiella infecting the skin and
dinofl agellates of the genus Oodinium (or Piscinoodinium) (Fig. 1). The third group
are specialized parasites exhibiting restricted host specifi city but with a pronounced
Fig. 3. Two-dimensional nonmetric multidimensional scaling (nMDS) plot calculated using Bray-Curtis
ordination of parasite abundance data for adult European perch from 10 localities (different symbols) around
Lake Constance sampled in 2008 (n = 199). Based on an analysis of similarity (ANOSIM) the parasite
communities were signifi cantly different (R ≥ 0.30; p < 0.05). The difference is shown for two localities,
RM and MS, encircling the 95% confi dence area occupied by Bray-Curtis similarity data of individual fi sh.
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Biology and Ecology of Perch Parasites 203
Table 2. Species, prevalence and mean infection intensity of parasites infesting European perch sampled from Lake Constance at different ages (wph = weeks post hatch).
First three columns (2, 4 and 7 weeks post hatch (wph), grey box) represent the pelagic, the other two (8 and 12 wph) the littoral samples. Proteocephalus spp. includes P.
percae and P. longicollis. Additional information is provided concerning invertebrate hosts (1.IH = fi rst, 2.IH = second intermediate host), species names given in brackets
where known, for Lake Constance from own observations (from Behrmann-Godel 2013).
Age of perch wph (n analysed)
2(51) 4 (85) 7(52) 8(60) 12(60)
Parasite Prevalence (mean intensities) Invertebrate host
Cestoda
Triaenophorus nodulosus*
0(0) 0(0) 56(1.3) 40(2.0) 50(2.0)
Triaenophorus nodulosus**
0(0) 0(0) 38(1.9) 10(1.0) 4(1.0)
1.IH: Copepods (Cyclops spp.)
Proteocephalus spp.
0(0) 12(1.1) 71(4.8) 40(2.5) 15(2.0)
1.IH: Copepods (Cyclops spp.)
Eubothrium crassum
0(0) 70(3.0) 63(3.5) 87(6.0) 45(3.0) Copepods
Trematoda
Bunodera luciopercae
0(0) 6(1.2) 63(2.7) 85(3.0) 95(12.5) 1.IH: Bivalves; 2.IH: Copepods, cladocerans, ostracods,
amphipods, ephemeroptera
Diplostomum baeri
0(0) 0(0) 0(0) 15(4.0) 70(3.0) 1.IH: Snails
Tylodelphys clavata
0(0) 0(0) 0(0) 55(2.5) 100(70)
1.IH: Snails (Radix auricularia, Radix labiata)
Ichthyocotylurus variegatus
0(0) 0(0) 0(0) 0(0) 20(2.5)
1.IH: Snails (Valvata piscinalis)
Cotylurus pileatus
0(0) 0(0) 0(0) 8(1.0) 50(5.0) 1.IH: Snails
Hysteromorpha triloba
0(0) 0(0) 0(0) 26(2.5) 26(2.0) 1.IH: Snails
Bucephalus polymorphus
0(0) 0(0) 0(0) 5(2.0) 0(0) 1.IH: Snails
Nematoda
Raphidascaris acus
0(0) 0(0) 0(0) 1(1.0) 0(0) -
Maxillopoda
Ergasilus sieboldi
0(0) 0(0) 0(0) 0(0) 1(1.0) -
Argulus foliaceus
0(0) 0(0) 0(0) 5(2.0) 5(2.0) -
* = plerocercoids; ** = procercoids
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204 Biology of Perch
preference for a specifi c infection site, for example the highly specialized trichodines
and several species of Tripartiella, all of which parasitize the gills of fi sh (Paperna
1991; Goater et al. 2014).
8.3.2 Myxozoa
The myxozoans are spore-forming parasites of freshwater and marine fi shes. Previously
they were classifi ed as protozoans but recent molecular analyses, studies on specifi c
functional specializations and the description of multicellular stages have led to their
reclassifi cation as a new phylum of metazoans with more than 2,100 species described
to date (Yokoyama et al. 2012). Most myxozoans are not harmful to fi sh but certain
members, especially ones that belong to the Class Myxosporea, can be highly fi sh-
pathogenic.
A typical myxosporean life cycle includes two obligate hosts, an annelid
(oligochaetes in freshwater and polychaetes in marine water) and a vertebrate, typically
a fi sh (Fig. 4). In the fi sh host myxosporean spores develop by sporogony and are
released into the water. If ingested by an annelid host, mature actinospores are formed
via sporogony and released into the water where they can infect fi sh by skin, fi n or gill
contact. Subsequent invasion of the sporoplast allows the life cycle to be completed.
The best known fi sh pathogenic myxosporean species is Myxobulus cerebralis,
which causes cranial lesions and spinal deformities symptomatic of “whirling disease”
in rainbow trout (Halliday 1976). Myxobulus sandrae (Lom et al. 1991) and Triangula
percae spp. nov. (Langdon 1987) have been identifi ed as causative agents of rare
localized lesions in the spinal cord, vertebral collapse and marked curvature of the
Fig. 4. Typical myxosporean life cycle (Myxobulus cerebralis) with alternating fi sh and annelid hosts,
modifi ed with permission after Yokoyama et al. (2012).
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Biology and Ecology of Perch Parasites 205
vertebral column in European perch. In yellow perch, Myxobolus neurophilus and
M. aureatus have been found to infect the brain and may cause neurological symptoms
in this species (Khoo et al. 2010).
More commonly, perch are found to be infected by a number of myxosporean
taxa that form whitish, spore-containing nodes on the gills or skin, or in the muscle
tissue. Henneguya psorospermica is one such species associated with European perch
(Schäperclaus 1979) (Fig. 1) while H. doori infects yellow perch (Cone 1994).
8.3.3 Platyhelminthes
The Platyhelminthes are a species-rich group with three parasitic classes, the
Trematoda, the Monogenea and the Cestoda.
8.3.3.1 Trematoda
Most digenean trematodes have a complex life cycle including several obligate hosts.
The trematodes are also known as fl ukes, and categorized further as eye, blood, liver
or lung fl ukes according to the infection site in the intermediate vertebrate host. In
most species, the defi nitive host is a vertebrate such as a fi sh-eating bird like a gull or
a cormorant. Within the defi nitive host, the trematodes usually inhabit the intestine.
Here they reach maturity and reproduce sexually, laying eggs that are expelled into the
environment along with the feces of the host. From the eggs hatch free-living motile
miracidia that infect the fi rst intermediate host by penetration of the body surface.
For the majority of trematode species, the fi rst intermediate host is an aquatic snail
within which a redia or sporocyst will develop and reproduce asexually to yield large
numbers of the next infective stage, the cercaria. Cercariae are released continually
at a rate of several hundred to several thousand per day and shed from the snail via a
special “birth pore” over an extended period of up to several months. The cercariae
of most species are motile and actively search for the next host, which they again
usually infect by penetration of the body surface. This next life cycle host might be
a second intermediate host within which metacercariae are formed that are infective
for the next host, or in some cases it might be the fi nal host within which the adult
worm develops. The number of obligate intermediate hosts within the life cycle of
different trematode species varies from one to four (Goater et al. 2014). In Fig. 5 the
life cycle of Diplostomum spathaceum is shown as an example.
Members of the Diplostomum species complex are eye fl ukes, infecting European
perch and yellow perch as well as other fi sh species. They include several of the
most common species of trematode infecting European and yellow perch, along with
Bunodera spp. (Carney and Dick 2000a; Morozinska-Gogol 2008) (Table 1).
8.3.3.2 Monogenea
The Monogenea constitute a very diverse group almost exclusively parasitic on
freshwater and marine fi sh species and highly host-specifi c. H owever under the dense
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206 Biology of Perch
rearing conditions found in aquaculture or the aquaria used in the ornamental fi sh trade
for example, members of the monogenean orders Dactylogyridea and Gyrodactylidea
in particular can cause mass mortalities (Thoney and Hargis 1991). In contrast to the
trematodes, most monogeneans have a direct life cycle, spending their entire life on a
single host individual. They are either oviparous, like members of the Dactylogyridea,
mainly infecting the gills of their hosts, or viviparous like the Gyrodactylidea, which
infect the skin of their host fi sh (Chubb 1977). Several species of monogenea have
been recorded parasitizing European perch and yellow perch, the most prominent
being Urocleidus adspectus on yellow perch (Cone 1980; Cone and Burt 1985) and
Ancyrocephalus percae and Gyrodactylus gasterostei for European perch (Morozinska-
Gogol 2008) (Table 1). Figure 6 shows an exemplary life cycle for Ancyrocephalus
percae infecting European perch.
8.3.3.3 Cestoda
The cestodes, or tapeworms, constitute a diverse group of approximately 3,400
parasitic species with vertebrate hosts (including 800 known species infecting
teleosts). Adult cestodes may be the parasites that cause the most revulsion in non-
parasitologists because of their large size (some species grow to several meters in
Fig. 5. Life cycle of Diplostomum spathaceum.
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Biology and Ecology of Perch Parasites 207
length) and conspicuousness, and infestations are generally perceived by farmers,
anglers and fi shermen as detrimental to fi sh. In reality however, adult cestodes tend
to be located exclusively within the intestine of their hosts, where they function like
a “second gut”, using suckers, hooks or other holdfast organs to anchor themselves
and absorb nutrients directly from the gut content via their own skin. Thus besides
a mostly marginal reduction in food or vitamin uptake for the host, low numbers of
adult cestodes are of little inconvenience and maybe even be imperceptible to the host.
However larval cestodes, which reside in the host’s fl esh, can be harmful, reducing
the desirability, and hence profi tability, of fi shery produce, or even rendering stock
unsuitable for human consumption.
Generally, cestodes have a complex life cycle including invertebrate intermediate
hosts and vertebrate defi nitive hosts. The eggs are released from adult worms resident
in the intestine of the defi nitive host. From these eggs, free-swimming oncomiracidia
hatch and are consumed by the intermediate host, often a copepod. Depending on the
species, the copepod can be ingested by a second intermediate host in which the parasite
develops into a plerocercoid that is infective for the defi nitive host or it can be directly
ingested by a defi nitive host where the adult worm develops in the intestine and the life
cycle is completed. As an example, the life cycle of the pike tapeworm Triaenophorus
nodulosus, which uses European and yellow perch as second intermediate host species
(Kuperman 1973) is shown in Fig. 7.
The most commonly encountered cestodes of European and yellow perch
are members of the Proteocephalus spp. species complex, Eubothrium crassum,
Bothriocephalus cuspidatus and Triaenophorus nodulosus (Carney and Dick 2000a;
Morozinska-Gogol 2008) (Table 1).
Fig. 6. Life cycle of Ancyrocephalus percae. Adult worms lay eggs that are shed into open water. Ciliated
oncomiracidia hatch, seek a new host, infest the gills as postoncomiracidia and develop into adults.
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208 Biology of Perch
8.3.3.4 Acanthocephala
The acanthocephalans (thorny-headed worms) are a relatively small group of parasites
with about 1,100 species (Goater et al. 2014). They live as adults in the intestines of
fi sh, amphibians, reptiles, birds and mammals and have a worldwide distribution. They
employ a unique thorny structure, the proboscis (Fig. 8), to anchor themselves in the
intestinal wall of their host, sometimes leading to an infl ammatory reaction in heavily
infected individuals (Schäperclaus 1979). Similar to the cestodes, the acanthocephalans
absorb nutrients directly from the intestine of their host and lack both mouth and
digestive tract. They vary in length from 1 mm to more than 60 cm. Acanthocephalans
Fig. 7. Life cycle of Triaenophorus nodulosus (from Brinker and Hamers 2005).
Fig. 8. Proboscis of Acanthocephalus lucii (adult worm).
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Biology and Ecology of Perch Parasites 209
are dioecious and often sexually dimorphic, with the females growing larger than the
males. The life cycle is complex, and includes an arthropod intermediate host and a
vertebrate defi nitive host. In some species, additional paratenic hosts may be included.
The most common acanthocephalans recorded in yellow and European perch are
members of the Pomphorhynchus spp. and Acanthocephalus spp. complexes (Carney
and Dick 2000a; Morozinska-Gogol 2008) (Table 1).
8.3.3.5 Nematoda
The nematodes (roundworms) comprise one of the most abundant phyla in the animal
kingdom. Current estimates hover around 20,000 species, but the vast majority is
as yet undescribed (Goater et al. 2014). Most nematode species are free-living, but
there are a number of parasitic species, almost exclusively endoparasites of various
animal and plant hosts. The nematodes are typically dioecious and often exhibit sexual
dimorphism. They vary from 1 mm to more than 1 m in length, with the longest
nematode described so far being Placentonema gigantissima, found in the placenta
of sperm whales Physeter catodon where the females grow up to 8 m long and 2.5 cm
in diameter. Goater et al. (2014) writes of the nematodes that “perhaps no single group
of related organisms on earth possess greater life history variability.” The broad
range of possible nematode parasite life cycle strategies often involves free-living
larval stages with behavioral adaptations to attract hosts and facilitate transmission.
Common nematodes of European and yellow perch are members of Camallanus spp.
and Raphidascarus acus (Moravec 1994; Goater et al. 2014). Camallanus lacustris
typically resides in the intestine, specifi cally the pyloric cæca of European perch, but
also in other hosts such as pike Esox lucius. Gravid female nematodes shed larvae
that enter the water with the host’s feces. These larvae are ingested by an invertebrate
intermediate host, typically Cyclops spp. or Asellus aquaticus. When the intermediate
host is predated by the defi nitive host, the nematode larvae can complete their
development into adults. Planktivorous fi sh species such as sticklebacks can also be
incorporated into the life cycle as paratenic hosts, which facilitate transmission to a
piscivorous defi nitive host. Camallanus lacustris feeds on host blood, and has a very
unique color, appearing red or pinkish with a conspicuous yellow oral capsule (Fig. 9).
Fig. 9. Camallanus lacustris from European perch. The worms have a typical red or pinkish color (a)
with a yellow oral capsule (b). Photos were kindly provided by Martin Kalbe, Max Planck Institute for
Evolutionary Biology, Ploen, Germany.
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210 Biology of Perch
8.3.4 Crustacea
The Crustacea are an extremely diverse group of arthropods comprising over 38,000
species. Crustaceans are primarily an aquatic group and a large number have a parasitic
association with fi sh. The majority of fi sh parasitic crustaceans are ectoparasites
that feed on host blood, mucus or skin cells. Many also parasitize the fi sh’s gills,
and mechanical disruption of the epidermis at the attachment and feeding sites may
result in osmoregulatory or respiratory problems or create opportunities for secondary
infectors including pathogenic fungi and bacteria to invade the host. One of the
best-known crustacean parasites of freshwater fi shes is Argulus foliaceus (Fig. 1),
commonly known as the “carp louse.” The pathogenicity of the carp louse lies not
only in the mechanical damage to the fi sh’s skin but also in irritation of the epidermis
by digestive secretions. Additionally it has been shown that A. foliaceus can act as a
vector for other pathogens, such as Rhabdovirus carpio which causes spring viremia
of carp (SVC) (Ahne et al. 2002). Argulus foliaceus has a direct life cycle, in which
adult females leave the host after copulation and deposit up to 500 eggs in a gelatinous
string on any suitable submerged surface such as stones. They may then return to
the same host individual or attach to another until ready to deposit the next clutch of
eggs. Time to hatching is dependent on water temperature (within 8 days at 26ºC),
then newly hatched parasitic metanauplii set out to search for a host fi sh (Hoole et al.
2011). After attachment, nine larval moults follow in rapid succession until the adult
stage is reached. In optimal conditions, the whole life cycle may be completed in less
than 40 days, and thus as many as four generations can be realized in a single summer.
The most common crustacean parasites of yellow and European perch are Argulus
foliaceus and members of the genus Ergasilus, which parasitize the gills (Carney and
Dick 2000a; Morozinska-Gogol 2008) (Table 1).
8.4 Impacts of Parasites on Growth, Fitness and Survival of
Perch
Perch show extensive plasticity in growth rates and age at maturity with variation in
abiotic and biotic factors. In general, individuals grow more slowly in the northern
hemisphere and at high latitudes, where temperature seems to be the most important
abiotic factor affecting growth (reviewed in Craig 2000). Differences between the
sexes are also apparent, with females growing faster and attaining much larger sizes
than males. However males typically reach maturity one year earlier than females.
In Lake Constance for example, most male European perch fi rst spawn in their
second year of life, while females mature in their third year (Eckmann and Schleuter
2013). Factors that infl uence perch growth have been studied intensively by many
authors and include latitude (Heibo et al. 2005), prey type (Boisclair and Leggett
1989) and availability (Hjelm et al. 2000), lake productivity (Hayward and Margraf
1987; Abbey and Mackay 1991), duration and severity of winter (Johnson and Evans
1991), presence of competing species (Bergman and Greenberg 1994) and presence of
predators (Magnhagen and Heibo 2004). Heibo and Magnhagen (2005) demonstrated
that the same broad range of factors also affects age at maturity. The effect of parasites
on perch growth, survival and reproductive potential in natural populations is less
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Biology and Ecology of Perch Parasites 211
well studied, although it has been shown that distinct parasite species can impact
negatively on perch growth (Johnson and Dick 2001; Cloutier et al. 2012) and can
increase perch mortality (Deufel 1975), especially of young age classes (Szalai and
Dick 1991; Szalai et al. 1992).
It is very diffi cult to link parasite infection with possible effects on viability,
fertility and growth of fi sh populations in the fi eld (Kennedy 1984; Lester 1984;
Sindermann 1986). Predation and scavenging of moribund or dead animals by other
fauna hinder attempts to assess the extent of an epidemic and observable non-lethal
aspects of infection such as pathological alterations, behavioral changes, reduced
reproductive success or increased contaminant load are very diffi cult to quantify
(Lester 1984; Sindermann 1986). Causal links between parasite infection and target
organ disorders can be diffi cult to separate from other factors, especially when the
time elapsed since initial infection of the active pathogen is not known. However,
parasites take nutrients from their hosts, and provoke reaction by their mere presence,
by infl icting lesions or by actively destroying host tissue (Goater et al. 2014). In
intermediate or paratenic hosts, parasites might even benefi t from altering the host’s
behavior or weakening it such that the chances of transmission to the next host are
improved (fi sh examples reviewed in Barber et al. 2000). Further possible effects
include reduced fertility and fi tness, in extreme cases resulting in castration of hosts
(e.g., trematodes in water snails or Schistocephalus in sticklebacks) (Heins and Baker
2008; Baudoin 1975). In the laboratory, controlled experiments can be conducted in
order to investigate single aspects of infection, though it usually remains unclear how
well these trials refl ect real life. However using the seminal work of Anderson and
Gordon (1982) and Crofton (1971) increasingly sophisticated statistical tools, applied
with appropriate data sets, might offer insights into even non-observable traits like
parasite-induced mortality in the fi eld.
8.4.1 Parasite Impacts on Adult Perch
As shown earlier in this chapter, a large number of macroparasite species target
European and yellow perch as intermediate, paratenic or defi nitive hosts. For the
majority of these parasites, little or no information is available regarding impacts
on their host, but most probably, the effect of the majority is minimal as long as no
epidemic outbreak occurs. The host is a resource that is exploited by the parasite to
maximize its own fi tness. The manner of exploitation (and thus the potential for harm
to the host) depends on how the interests of the parasite are best served for maximizing
fi tness (Poulin 1998). Parasite species that use perch as defi nitive hosts usually do not
benefi t from a weakened or moribund host, because their own reproduction is optimal
in a well fed, healthy, normally behaving individual. In contrast, parasite species that
use perch as intermediate or transport host, may profi t from weakening the host or by
inducing behavior that renders the host vulnerable to predation by the parasite’s next
life cycle host. An excellent example of such manipulation of host behavior concerns
the eye fl uke Diplostomum spathaceum and its intermediate fi sh host, the rainbow
trout Oncorhynchus mykiss. Diplostomum spathaceum has a complex life cycle
(Fig. 5), including three obligate host species. Fish are used as second intermediate
hosts, wherein D. spathaceum locates itself in the lens of the eye. Experiments with
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212 Biology of Perch
infected rainbow trout have shown that D. spathaceum metacercariae in the eye can
induce cateract formation on the lens, which impairs the host’s escape response and
predisposes it to predation by birds, thereby improving the chances of transmission to
the defi nitive host (Shariff et al. 1980; Seppälä et al. 2011). Although no comparable
experiments have been done with perch, both European and yellow perch are among
the wide range of fi sh taxa parasitized by members of the highly speciose Diplostomum
species complex and a similar mechanism of behavioral manipulation can be assumed
at least for the lens-infecting Diplostomum species. Between 1960 and 1971, regular
lethal outbreaks of Diplostomum spp. where recorded in Lake Constance. Not only
European perch but also pike, burbot Lota lota and cyprinids including bream Abramis
brama were killed by massive infections in spring and early summer (Deufel 1975). In
these fi sh kills, mortality was caused by penetration of the skin by excessive numbers
of Diplostomum cercariae, a disease known as diplostomosis or cercariosis (Majoros
1999; Larsen et al. 2005). Diplostomosis is a recognised threat to fi sh in lake farms
and in natural waters, and tends to be especially devastating to fi sh larvae and juveniles
(Molnár 1974; Larsen et al. 2005).
Negative impacts on perch health have also been shown for the pike tapeworm
Triaenophorus nodulosus, which infects both perch species as a second intermediate
host. T. nodulosus has a complex life cycle (see Fig. 7) including three obligate hosts.
Adult worms live in the intestine of pike, from where eggs are shed along with the
host’s feces and hatch into motile coracidia. These coracidia are ingested, mainly
by copepods of the genus Cyclops, within which each coracidium develops into a
fi sh-infective procercoid. Several fi sh species, but principally European and yellow
perch, serve as the second intermediate host (Kuperman 1973) after ingesting infected
copepods. The procercoids migrate to the liver of the intermediate fi sh host where they
become encapsulated by a host tissue response and develop into plerocercoids (Fig. 10).
Plerocercoids are only rarely found in other organs (Kuperman 1973). Burrowing
activity of the plerocercoid and the resulting lysis of host cell membranes causes
pathological symptoms such as inflammation, atrophy, necrosis, hyperæmia,
hæmorrhage and edema (Rosen 1918; Scheuring 1922; Kuperman 1973; Schäperclaus
Fig. 10. Heavily infected adult European perch from Lake Constance. Several encapsulated pike tapeworms
Tri aenophorus nodulosus can be seen in the liver (arrows).
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Biology and Ecology of Perch Parasites 213
1979; Hoffmann et al. 1986). Further damage may result from pressure on surrounding
tissues as large larvae are encapsulated (Scheuring 1922) and from osmotic and
toxic stress (Read and Simmons 1963; Schäperclaus 1979). Predation on infected
intermediate hosts by the pike completes the life cycle. Brinker and Hamers (2007)
compared the growth of European perch with different intensities of T. nodulosus
plerocercoid infection (varying from no infection, to normal infection with 1–3
plerocercoids and severe infection with >3 plerocercoids). Increasing infection
intensity correlated with a reduction in perch growth (Fig. 11) amounting to a loss of
~10% potential mass for normal infection and ~16% for severe infection at legal gill
net catch size—an effect large enough to be commercially signifi cant. Furthermore,
Brinker and Hamers (2007) and Molzen (2006) both reported a clear correlation
between levels of pathological liver alteration and infection level, with knock-on
negative effects on fertility, i.e., the gonadosomatic index was reduced by 20% or more
(Molzen 2006). However, recent research in the fi eld has shown that the prevalence
of T. nodulosus in perch drops from ~90% to ~70% when co-infecting with the gill
worm Ancyrocephalus percae (Roch unpublished results) indicating a subsequent
increase in parasite-induced mortality.
Triaenophorus nodulosus shows a highly aggregated distribution in perch. Such
distribution patterns are common in almost all parasite communities including passive
parasite-intermediate host systems (Crofton 1971; Anderson and Gordon 1982; Lester
1984; Pacala and Dobson 1988) and are assumed to benefi t the parasite in two ways:
(1) a small proportion of the intermediate host population carries the bulk of parasites
and suffers the negative impacts, but the host population as a whole is not endangered;
(2) heavily infected second intermediate hosts are probably weakened and therefore
become relatively easy prey for the defi nitive host (Kennedy 1984; Balling and
Fig. 11. Growth curves of European perch from Lake Constance. The three lines represent growth regressions
for different infection categories: Solid line—no infection; dotted line—low infection; hatched line—heavy
infection (for details see text). Modifi ed with permission from Brinker et al. (2007).
Fish age [days]
0 500 1000 1500 2000 2500
Total length (cm)
30
25
20
15
10
5
0
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214 Biology of Perch
Pfeiffer 1997). A consequence of aggregated distribution is thus that the probability
of transmission increases (Sindermann 1986; Zander 1998).
Infection with T. nodulosus increases the relative risk of mortality in the host,
as can be seen in spring in Lake Constance, when severely infected fi sh suffer from
increased mortality following spawning stress (Brinker et al. 2007). This is further
supported by recursive fi tting of data for 1307 Lake Constance perch (Brinker
unpublished data) to the negative binomial distribution, revealing parameter k larger
than 1, which indicates parasite-induced mortality associated with high-intensity
infection (Crofton 1971).
In the yellow perch, the nematode Raphidascaris acus also infects the liver and
causes signifi cant and quantifi able negative effects. The parasite has a complex life
cycle, including aquatic invertebrates as paratenic hosts, fi sh as intermediate hosts and
piscivorous fi sh as defi nitive hosts. In North America, Perca fl avescens is the main
intermediate host, and infection is mainly via ingestion of chironomid prey (Johnson
and Dick 2001). The parasite causes extensive liver pathology and wider intensity-
dependent symptoms. For example, if infestation exceeds 100 cysts per gram of liver
tissue the yellow perch suffer from signifi cant growth reduction (Johnson and Dick
2001). Especially striking however, are further age-related effects. Infection intensity
tends to peak just before the host reaches sexual maturity and the combined pressure of
parasite infection and the physiological demands of vitellogenesis and spermatogenesis
lead to increased host mortality and reduced growth (Szalai 1991). It is even possible
that the generally observed pattern of bimodal weight distribution in female yellow
perch following vitellogenesis may be caused by the parasite. The signifi cance of
R. acus for yellow perch is convincingly demonstrated by observations from Dauphin
Lake in Manitoba, where in the absence of the parasite natural mortality was reduced
by about 50% (Szalai 1991). Thus it seems that tissue-invading parasites may play
a signifi cant role in the regulation of perch populations in both North America and
Europe.
Another macroparasite that was shown to have a dramatic negative impact on
the health of European perch from Lake Constance is the monogenean gill parasite
Ancy rocephalus percae. These oviparous fl atworms have a direct lifecycle (see also
Fig. 6) and are hermaphroditic (Chubb 1977). Eggs are laid into the open water,
followed by hatching of oncomiracidia that are able to directly infest a new host.
Ancyrocephalus percae is distributed widely all over Europe, but infects only the gills
of European perch (e.g., Andrews 1979; Bylund and Pugachev 1989; Morozinska-
Gogol 2008). Little information about this parasite is available in the scientifi c
literature, most likely because it appears not to cause severe problems for European
perch outside Lake Constance.
At some point after the year 2008, A. percae was introduced into Lake Constance
(Behrmann-Godel et al. 2014). The route into the lake is unknown, but having arrived,
the parasite became highly invasive. It infects Lake Constance perch at the isthmus
near the gills and causes oval-shaped wounds in the tissue (Fig. 12a), a behavior never
described for this parasite before. All age classes of perch are affected, especially
young fi sh. The wounds occurring on the isthmus of the hosts’ gills can be dramatic.
In extreme cases, high intensity infections can sever the isthmus, leading to partial
decapitation (Fig. 12b).
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Biology and Ecology of Perch Parasites 215
Clear differences in the prevalence of A. percae infection can be found between
two genotypes/morphotypes of European perch in Lake Constance distinguishable
by fi n color. While the majority of perch have yellow fi ns, there are increasingly
regular catches of red-fi nned perch in certain areas of the lake. Red-fi nned perch
occur alongside yellow-fi nned fi sh but are signifi cantly less affected by A. percae,
indicating a greater resilience to this parasite (Roch et al. 2015). Immunity plays a
crucial role in parasite defence (Buchmann and Lindenstrom 2002), and the resilience
of red-fi nned perch in Lake Constance is most likely due to a more effective immune
response. Additionally there are occasional catches of adult yellow-fi nned perch with
red areas on their fi ns. This unusual color pattern is not related to disease or bacterial
infection, and it is likely that these mixed color morphotypes are hybrids between
yellow- and red-fi nned types (Roch et al. 2015). Studies on prevalence of the gill
worm A. paradoxus show that the mixed color types are signifi cantly less affected by
the parasite than yellow-fi nned relatives, but more so than the pure red-fi nned ones
(Fig. 13). It seems that fi n color is concomitant with some other trait that infl uences
A. percae parasite burden. Early studies into the phenomenon have sought evidence
Fig. 12. European perch from Lake Constance infected with the gill worm Ancyrocephalus percae. (a)
Aggregation of parasites in a wound at the isthmus. The operculum and distal part of the gills have been
removed for a better view. (b) Heavily infected fi sh (isthmus is detached from lower jaw), operculum and
parasites removed for better view. (c) Light microscopic view of an adult A. percae from perch showing
morphological characters. (d) Scanning electron micrograph (Foto by V. Burkhardt-Gebauer) of ventral
body of an adult A. percae showing morphological characters. Reprinted with permission from Behrmann-
Godel et al. (2014).
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216 Biology of Perch
of a cellular immune response to the parasite. In chemotaxis assays, perch leukocytes
showed a positive chemotactic reaction to A. percae exposure. Young of the year
red-fi nned perch are also infested by A. percae, but seem to gain a resistance to the
gill parasite within their fi rst year. The yellow-fi nned morphotype does not develop a
successful immune defence, resulting in infestation of all age classes (Fig. 13).
Measurements of post mortem muscle pH in yellow-fi nned perch showed that
infection with A. percae has a negative effect on energy reserves in the muscle of
infested individuals. Following death, energy-rich compounds like glucose are
metabolized by bacteria in an anaerobic process producing lactate (Binke 2004),
which subsequently lowers pH. This process has been shown to be faster when fi sh
are stressed (Thomas et al. 1999) and the magnitude of pH loss is dependent on the
stored amount of energy-rich compounds in muscle tissue (Unger et al. 2008). As
uninfected perch show a comparable pH development during 24 h post mortem but
higher pH drop than infected ones, this indicates energy depletion in muscle tissue
of infected fi sh. Interestingly, one year old perch infected by T. nodulosus suffered a
signifi cantly lower incidence of A. percae infection, suggesting a possible immune
priming effect whereby the presence of the pike tapeworm activates the perch immune
system, which is then better able to react against A. percae. However the observation
could also be explained by an increased death rate associated with infection by two
harmful macroparasites. Follow up experiments will show whether red-fi nned perch
in Lake Constance really do have an immune advantage that allows them to throw
off infection better than yellow-fi nned perch.
8.4.2 Impact of Parasite Infection on Perch Larvae and Early Juveniles
The high levels of mortality suffered by larval and juvenile fi sh are due mainly to
predation, but starvation, disease and parasitism also take a signifi cant toll (Wootten
1974). It is easy to imagine that any debilitation or deviation from normal fi sh behavior
will increase their risk of predation and hence increase larval and juvenile mortality.
Fig. 13. Infection of three morphotypes of European perch from Lake Constance (yellow-fi nned, red-fi nned
and mixed color) with the monogenean gill parasite Ancyrocephalus percae. Shown is the prevalence in
three different age classes: young of the year (0+), one year old (1+) and older perch (>2+). Sample size is
indicated in the bars, signifi cant differences are indicated by asterisks (Fisher’s exact test).
yellow-fi nned
0+
red-fi nned
0+
yellow-fi nned
1+
red-fi nned
1+
yellow-fi nned
≥ 2+
mixed color
≥ 2+
red-fi nned
≥ 2++
100
75
50
25
0
Prevalence [%]
Fin color/age [years]
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Biology and Ecology of Perch Parasites 217
An increasing number of studies show that the early developmental stages of fi sh are
targeted by several species of endo- and ectoparasites (Balbuena et al. 2000; King and
Cone 2009; Kuchta et al. 2009; Pracheil and Muzzall 2009; Skovgaard et al. 2009a;
Behrmann-Godel 2013). Parasitic infections may be detrimental to fi sh fry by inducing
malformations and increasing mortality (Johnson and Dick 2001; Skovgaard et al.
2009b; Grutter et al. 2010; Kelly et al. 2010; Nendick et al. 2011). However the costs
of parasitism in terms of various life history parameters are far from well understood
and the consequences of parasite infection of fi sh larvae and juveniles for population
recruitment might be especially severe for threatened species (e.g., see Collyer and
Stockwell 2004).
The timings of parasite succession relative to fi rst parasite encounter are almost
unstudied in perch (but see Kuchta et al. 2009). Behrmann-Godel (2013) recently
observed that European perch fry were infected with a succession of 13 different
parasite species during the fi rst three months of development (Table 2). First infections
have already occurred by the time perch larvae in the pelagic zone of Lake Constance
start feeding on zooplankton including infected copepods, four weeks after hatching.
Distinct changes in parasite community composition and abundance were found to
be associated with perch fry age and with the ontogenetic habitat shift from pelagic
to littoral nursery areas (Behrmann-Godel 2013).
Trophically transmitted parasites such as the pike tapeworm T. nodulosus, which
is consumed along with infected prey, have the potential to reduce growth of adult
perch, as described in the previous paragraph. In perch larvae (age: 42–152 days post
hatch (dph)) however, experimental infections had no effect on growth, but did result
in increased mortality of heavily infected larvae and juveniles. Infection intensity
was higher in fi sh that died during the experiment than in the survivors (Fig. 14). For
juvenile yellow perch, between 3–24 months of age (90–1550 dph) investigated from
four Canadian Shield lakes, Johnson and Dick (2001) found negative effects of two
parasite species on both, growth and survival of perch. The myxosporidian Glugea
spp. and the trematode Apophallus brevis increased mortality and reduced the growth
of YOY fi sh when occurring in high intensities (>100 parasites for Glugea spp.) and
high densities (>50 and again with >100 cysts/g fi let weight for A. brevis).
Interestingly, the youngest European perch larvae investigated in Lake Constance
appeared not to be infected by skin penetrating trematode cercariae from snail
intermediate hosts (2 weeks post hatch (wph), Table 2). Perch spawn early in spring
(between April and June depending on latitude) in shallow littoral areas. The larvae
hatch after 6–14 days, depending on water temperature and are soon transported to
the pelagic zone (Wang and Eckmann 1994). As snail intermediate hosts in the littoral
zone already shed cercaria by the time perch larvae developed and hatched (Deufel
1975; Behrmann-Godel 2013), perch larvae might be expected to be at risk of infection
during their fi rst days post hatching. The complete lack of skin-penetrating trematode
cercariae in young sampled fi sh could indicate two possible scenarios. First, larval perch
may not be recognized as potential hosts by the skin-penetrating trematode cercariae
and thus not infected, or second, cercarial infection of fi sh larvae takes place but is
rapidly fatal. Experimental infection of perch larvae with skin-penetrating cercariae
of Diplostomum spathaceum, Cyatocotylidea sp. and Tylodelphys clavata led to death
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218 Biology of Perch
from cercariosis within 24 hours (Behrmann-Godel unpublished). Thus during the fi rst
days after hatching, even very low doses of cercariae infection by skin penetration
may result in high mortality rates of perch larvae (Fig. 15). With increasing age of
perch however, dose dependent mortality decreased and by 19 days old, mortality
rates among perch infected with the mild doses used in the experiments (max. 10
cercariae) were very low (Fig. 15f).
Fig. 14. Laboratory infection of larval and juvenile European perch with Triaenophorus nodulosus. (a) In
some fi sh, the plerocercoids where not encysted (perch age: 48 dph (days post hatch)). Plerocercoid has
been squeezed out of the liver to show burrows created by the worm. (b) In other host fi sh the plerocercoids
were encysted by a host tissue reaction (perch age: 75 dph) (photos: Michael Donner). (c) Boxplots of
T. nodulosus intensity during the infection experiment (Median, box = 50% percentiles, whiskers = 95%
percentiles, dots = outliers). The density of T. nodulosus plerocercoids in host tissues was signifi cantly
lower in infected survivors than in infected fi sh that died during the experiment (n = 162 survivors, 77 dead
fi sh, age: 42–125 dph; Welch ANOVA, F = 4.38, p = 0.038).
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Biology and Ecology of Perch Parasites 219
Fig. 15. Cercariosis caused by skin-penetrating trematode cercaria in European perch larvae and juveniles.
Diplostomum spathaceum cercariae caused spinal cord malformations and death of infected three dph (days
post hatch) perch larvae (b, c), while uninfected control larvae survived (a). In laboratory experiments perch
larvae were individually infected with different doses of trematode cercariae (d–f, every dot represents
perch mortality within 24 hours calculated from six (d) or seven (e, f) infection experiments with individual
larvae). Skin penetration by Tylodelphys clavata (d) and Cyatocotylidea sp. (e, f) resulted in dose dependent
mortality of perch larvae. Mortality rates decreased with perch age and were almost negligible at 19 dph (f).
2 dph (n = 36)
19 dph (n = 49)
Infection dosis (no. cercariae)
Infection dosis (no. cercariae)
0 2 4 6 8 10
0 1 2 3 4 5
1.0
0.8
0.6
0.4
0.2
0
Mortality
Mortality
Mortality
1.0
0.8
0.6
0.4
0.2
0.0
1.0
0.8
0.6
0.4
0.2
0.0
0 2 4 6 8 10
Infection dosis (no. cercariae)
14 dph (n = 48)
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220 Biology of Perch
Cercarial shedding from infected intermediate host snails is highly temperature
dependent. It has been shown that with a slight increase of water temperature in spring,
the number of cercariae shed by snails increases exponentially (Lyholt and Buchmann
1996 and personal observations). Lymnaea stagnalis snails infected with the trematode
Diplostomum spathaceum started shedding cercariae at water temperatures of 4–6ºC.
At 10ºC, cercariae were shed at a rate of 10,000 per snail per day, rising to 58,000
cercariae per snail per day at 20ºC (Lyholt and Buchmann 1996). A slight increase in
spring water temperatures as a result of global warming may therefore be expected to
result in an increased shedding of trematode cercariae in spring. Rising spring water
temperatures have already been shown for several lakes including Lake Constance
(Stich and Brinker 2010; Straile et al. 2012), and it might be speculated that increasing
numbers of cercariae in the littoral zone will negatively impact newly hatched perch
larvae and result in high mortality rates.
8.5 Ecology and Evolution of Host-parasite Interactions
Parasite studies are increasingly incorporated into ecosystem research, and especially
into investigations of aquatic ecosystems. Incorporating parasites into “classical” food
webs from which they were previously excluded greatly increases the complexity
of the models, but improves understanding by increasing apparent species richness,
trophic chain lengths and connectivity (Marcogliese and Cone 1997; Lafferty et al.
2006, 2008).
Furthermore, parasites have long been overlooked as prey in their own right
(Johnson et al. 2010). They may be consumed along with a host organism or via direct
predation of free-living stages (Lafferty et al. 2006, 2008). Incorporating parasites into
a food web for the Carpinteria salt marsh in California doubled trophic connectivity
and quadrupled the number of links (Lafferty et al. 2006). Thus future ecosystem-
level investigations of trophic interactions should consider parasites as a matter of
course from the outset.
Community ecology is a central theme in parasitology but has yet to be extensively
studied in fi sh (Bush et al. 1990; Kennedy 1990). Indeed, there is considerable
uncertainty as to whether the freshwater fi sh parasite communities are stochastic in
nature or follow ecological patterns (Kirk 1990). The topic in all its facets is beyond
the scope of this chapter, but yellow perch are among the few fi sh in which this
complex matter has been successfully addressed, we will briefl y review the work
and its important ecological implications. Carney and Dick (2000) and Johnson et al.
(2004) provide evidence that certain aspects of parasite assemblages are predictable
and follow decisive ecological patterns. For example, the coevolution of parasite and
host provides some phylogenetic predictability in terms of host specifi city (important
parasite species being Urocleidus adspectus, Bunodera sacculata and Proteocephalus
pearsei) (Johnson et al. 2004). However ecological predictability also occurs, as a
result of stable infracommunity processes (Carney and Dick 2000). Parasites that
are transmitted trophically via predation on intermediate host species can be used as
natural indicators of trophic linkage within ecosystems (reviewed in Marcogliese and
Cone 1997). Analysis of parasite communities associated with yellow perch in several
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Biology and Ecology of Perch Parasites 221
Canadian Lakes of differing trophic status, size and invertebrate abundance showed that
the parasite infracommunities were non-random, highly nested associations of species
that were predictive in several ecologically important ways, providing an extensive
insight into host feeding habits and dietary preferences and indicative of the richness
of the invertebrate community of the habitat (Carney and Dick 2000). Similar results
from Jonson et al. (2004) suggested parasite fauna to be good indicators of the trophic
status of yellow perch in the Canadian Shield lakes. Interesting in this context is the
observation that parasite assemblages are generally richer in waters with complex
invertebrate communities, whereas the complexity of fi sh communities seems to have
no infl uence on parasite richness (Johnson and Dick 2000). This observation has yet
to be fully explained, but as rule of thumb, schooling host and exploiting exclusive
trophic categories tend to homogenize parasite infracommunities, while overlap with
other species tends to increase parasite richness. Thus the data for yellow perch,
though at odds with Kennedy’s (1990) assessment that local compound communities
of freshwater fi sh are stochastic, suggest that stable infracommunity processes do
act in the complex environment of fi sh communities and therefore could be valuable
tools in ecological research.
In the light of anthropogenic environmental change, several parasite species
have been shown to accumulate trace metals, making them interesting candidates
for environmental pollution indicators (Sures 2003; Vidal-Martinínez 2010).
Acanthocephalans, for example, have been shown to accumulate toxic metals such as
arsenic, cadmium and lead at concentrations hundreds to a thousand times greater than
in the tissue of their host fi sh (Sures et al. 1999; Sures 2001). The trace metal load of
parasites may be therefore useful in identifying anthropogenic pollution in the host
environment at levels that are otherwise undetectable (Nachev 2013). Interestingly
however, fi sh infected by some parasites, including acanthocephalans, have lower trace
metal concentrations in their tissue than unparasitized fi sh from the same polluted area
(Sures 2008; Vidal-Martínez 2010). This raises the possibility that some endoparasites
may act as “metal sinks,” effectively cleansing the host tissues of trace metals and
eventually benefi ting the overall health status of the host fi sh.
All these studies strongly suggest that environmental change and anthropogenic
environmental pollution in particular, can impact considerably on parasite-host
interactions. Any detrimental effect of parasites can be exacerbated when the host is
stressed by pollutants in the environment. Marcogliese et al. (2005, 2010) studied the
combined effects of parasites and pollution on yellow perch sampled at sites in the St.
Lawrence River, Quebec, Canada that differed in the degree of pollution (mainly by
trace metals). The results of that study show that perch in more heavily polluted sites
generally expressed higher levels of oxidative stress biomarkers (lipid peroxidation)
than perch from non-polluted waters (Marcogliese et al. 2005). Within the same
polluted site, parasitized perch were in a worse state of health than non-parasitized
fi sh, with higher levels of oxidative stress biomarkers. Further study (Marcogliese
et al. 2010) indicated that, despite comparable numbers of parasites in yellow perch
from contaminated and uncontaminated sites, the pathogenicity of single parasite
species was enhanced under polluted conditions. Thus while environmental pollution
may not affect resistance to specifi c parasite species, tolerance is likely to be reduced
under polluted conditions.
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222 Biology of Perch
A comparison of both the phylogenetic and biogeographic data of perch and
their associated parasites was used to understand historic ecological parasite-host
interactions and host switches, and to test different hypotheses of the phylogeographic
origin of the yellow perch in North America. Carney and Dick (2000b) have used
phylogenetic and biogeographic information of both yellow perch and three of their
associated parasites Crepidostomum cooperi, Proteocephalus pearsei and Urocleidus
adspectus to investigate whether the parasite-host associations are solely based on
ecology or on co-speciation between the partners. They could show for all three
investigated parasite-host interactions that they are not based on parasite-host co-
speciation but have all arisen by a host switch and must have had a North American
ancestor. Crepidostomum cooperi forms a monophyletic clade with C. ictaluri and
C. cornutum, two parasites of endemic North American Centrarchidae and Ictaluridae.
Urocleidus adspectus was found in a clade with uncertain relationships that is a
sister clade to the Ligictalurids, a group of parasites of the North American ictalurid
catfi shes. Finally P. pearsei form yellow perch and P. percae from European and
yellow perch were not found to be sister taxa based on the Proteocephalid phylogeny,
suggesting no co-speciation to have occurred between these two parasite species but
also a host switch of P. pearsei to yellow perch from another North American endemic
host species. These fi ndings of Carney and Dick (2000b) together with a study on
Bunodera spp. biogeography from yellow perch and North American sticklebacks
(Choudhurs and Règagnon 2005) strongly support the hypothesis of a Laurasian
origin for the Percidae as fi rst proposed by Wiley (1992) (see also Chapter 2 of this
book for molecular-level corroboration). This hypothesis predicts the existence of a
North American-European ancestor for both the yellow and the European perch that
dispersed into both continents. Divergence between the two species happened later
during vicariance due to the separation of both continents after the opening of the
North Atlantic during the Miocene (20 Myr BP).
8.6 Conclusions and Future Perspectives
The parasite fauna of perch, including European and yellow perch, is highly diverse,
with numerous representative species of a variety of genera. The diversity of the
parasite community of perch refl ects the variable autecology of the host fi sh species,
their widespread distribution, broad habitat preferences (including streams, rivers,
lakes, estuaries and low salinity marine areas such as the Baltic Sea) and concomitant
nonselective feeding behavior. At the perch host individual level, the variability of the
parasite infracommunity is also high because individual fi sh tend to migrate between
habitats and consume food from different sources and trophic levels during ontogenetic
development and in later life. Meanwhile, many associations between perch and their
parasites are quite well studied and a diverse array of analytical tools is now available
for eco-parasitological investigations. Immunological techniques recently developed
for measuring physiological reactions to parasite infection in perch include the analysis
of oxidative stress biomarkers (Marcogliese et al. 2005, 2010), measurements of post
mortem muscle pH and chemotaxis assays with perch leukocytes (see 3.1 above). All
these new techniques and methods are yielding intriguing new insights and answers
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Biology and Ecology of Perch Parasites 223
to eco-parasitological questions. Perch and their parasites are thus an increasingly
valuable model system for research areas including facilitation phenomena in parasite
infrapopulations, cost-benefi t analyses and the study of parasite-host co-evolutionary
processes.
The scope of parasitological study, once an almost exclusively descriptive
biological discipline, has widened considerably in recent decades into a variety
of new and intriguing areas, not least evolutionary biology, where parasite-host
interactions allow unique insights and opportunities for study. Fish and their parasites
are particularly promising in this respect, given the relative ease of culture, fecundity
and short generation time relative to other vertebrate hosts and the extensive reservoir
of biological background knowledge.
One of the most prominent fi sh model organisms studied in this context is the
three-spined stickleback Gasterosteus aculeatus, whose natural parasites include the
tapeworm Schistocephalus solidus and the monogenean Gyrodactylus gasterostei
(Barber 2013). Several aspects of parasite-host co-evolution have been investigated
using these model systems, including infection dynamics (Kalbe and Kurtz 2006;
Raeymaekers et al. 2011) and parasite-host co-adaptation, mainly including the study
of genes of the major histocompatibility complex (MHC) (Eizaguirre et al. 2009,
2011; Lenz et al. 2013). The expanding range of model parasite-host systems will
further benefi t our understanding of co-evolutionary processes. Recently a similar
methodology was developed to study genes of the MHC in European perch (Michel
et al. 2009; Oppelt and Behrmann-Godel 2012). Major histocompatibility complex
receptors (especially class II receptor genes) present antigens derived from extracellular
pathogens such as parasites to helper T cells of the immune system, and induce an
adaptive immune response to parasitic invaders (Janeway et al. 2005). This means
that the specifi c MHC setting of an individual directly determines its ability to resist
or defend against parasitic infections and as such is expected to be a major target
trait of antagonistic parasite-host co-evolution. Björklund et al. (2015) were able to
compare MHC variability in two perch populations exposed to different temperature
conditions over 35 years. One population, living in the vicinity of a nuclear power
station, was isolated and exposed to artifi cially warm water used as a coolant, while
the other nearby population served as an unmanipulated control. They concluded that
isolation and heating has led to a change in the selection regime imposed by parasites.
It resulted in observable changes in MHC allele variability and cycling patterns. These
observations were supported by the fi nding that the current parasite communities of
the two perch populations now differ signifi cantly from each other (Marian Schmid,
M.Sc. Thesis, University of Konstanz).
Despite recent advances, major defi cits remain in some important scientifi c aspects
of perch knowledge, including: (1) the lack of comparative studies for European and
yellow perch concerning parasite-host interactions and the impact of parasites on host
fi tness, (2) understanding of perch immunity, in particular specifi c immune reactions
against parasitic invaders, (3) the physiological consequences of parasitic infections for
perch, and especially of multiple infections with a diverse range of parasitic species, or
of invasive parasite species new to the ecosystem, and (4) the variable susceptibility to
infection of different perch genotypes. This last fi eld in particular will benefi t greatly
from the development and widening availability of new genetic techniques, such as
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224 Biology of Perch
whole genome sequencing. The rapid development of new molecular techniques has
revolutionized many fi elds of biology, including parasitology, where it promises to
facilitate and support urgently needed taxonomic approaches, such as the identifi cation
of “new” parasites and pathogens or the description of cryptic species. Such methods
may also help to clarify the origins of diseases and infer transmission routes of
pathogens. Additionally, it may elucidate host ecology, as recently demonstrated by
Criscione et al. (2006), who showed that the source of a population of steelhead trout
could be evaluated more precisely using the mitochondrial genotypes of its trematode
parasites (Plagioporus shawi) than those of the trout itself.
It is fi tting to end this chapter by highlighting the importance of multidisciplinary
approaches. The development of synergistic scientifi c projects combining interesting
new and “classic” fi elds of biology including ecology, parasitology, immunology and
molecular genetics, is likely to be key in driving forward understanding of parasite-
host interactions in complex ecosystems.
8.7 Acknowledgements
We thank Patrice Couture and Gregory Pyle for inviting us to contribute to this volume.
We thank students Daniela Harrer (PhD), Michael Donner (PhD), Samuel Roch (MS),
Martina Knaur (MS), Marian Schmid (MS), Melody Reithmann (BS) and Dennis
Rosskothen (BS) for supplying results from their graduate and undergraduate degree
work in the Fish Ecology Group at the University of Konstanz and the Fisheries
Research Station at Langenargen. Warm thanks to Amy-Jane Beer for reviewing the
manuscript and for English correction. We thank three unknown reviewers for their
fruitful contributions. JBG is thankful to Reiner Eckmann for his kind support. Funding
came from the German science foundation (DFG) within the CRC 454 “littoral of Lake
Constance” as well as from the Stiftung für Umwelt und Wohnen and the University
of Konstanz.
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