International Journal for Parasitology 35 (2005) 705716

www.parasitology-online.com

Invited review

Parasites of the superorganism: Are they indicators of ecosystem health?

David J. Marcogliese*
St Lawrence Centre, Environment Canada, 105 McGill, 7th Floor, Montreal, Que., Canada H2Y 2E7
Received 8 December 2004; received in revised form 19 January 2005; accepted 19 January 2005

Abstract
The concept of ecosystem health is derived from analogies with human health, which subsequently leads to the implication that the
ecosystem has organismal properties, a superorganism in the Clementsian sense. Its application and usefulness has been the subject of a
contentious debate; yet, the term ecosystem health has captured the publics imagination and woven its way into the current lexicon, even
incorporated into public policy. However, the application of parasites as bioindicators of ecosystem health poses a curious conundrum.
Perceptions of parasites range from mild distaste to sheer disgust among the general public, the media, environmental managers and nonparasitologists in the scientific community. Nevertheless, the biological nature of parasitism incorporates natural characteristics that are
informative and useful for environmental management. The helminths in particular have evolved elegant means to ensure their transmission,
often relying on complex life cycle interactions that include a variety of invertebrate and vertebrate hosts. The assemblage of these diverse
parasites within a host organism potentially reflect that hosts trophic position within the food web as well as the presence in the ecosystem of
any other organisms that participate in the various parasite life cycles. Perturbations in ecosystem structure and function that affect food web
topology will also impact upon parasite transmission, thus affecting parasite species abundance and composition. As such, parasite
populations and communities are useful indicators of environmental stress, food web structure and biodiversity. In addition, there may be
useful other means to utilise parasitic organisms based on their biology and life histories such as suites or guilds that may be effective
bioindicators of particular forms of environmental degradation. The challenge for parasitology is to convince resource managers and fellow
scientists that parasites are a natural part of all ecosystems, each species being a potentially useful information unit, and that healthy
ecosystems have healthy parasites.
Crown Copyright q 2005 Published by Elsevier Ltd. on behalf of Australian Society for Parasitology Inc. All rights reserved.
Keywords: Parasites; Ecosystem health; Pollution; Indicators; Environmental stress; Community

1. Introduction
The concept of ecosystem health has permeated
environmental management, the public domain, and even
our contemporary scientific and legislative lexicon. As a
current paradigm in environmental science, however, it is
not accepted without some degree of controversy.
Ecosystem health encompasses both ecological integrity
and the human dimension. Whereas integrity refers to that
condition of an ecosystem free from human interference
(Karr, 1999), most ecosystems are not only impacted
by human activities, but they are also managed,
harvested and otherwise used to provide goods and services.

* Tel.: C1 514 283 6499; fax: C1 514 496 7398.

E-mail address: david.marcogliese@ec.gc.ca

Thus, the concept of ecosystem health implies recognition

of the human impact rooted in societal needs and values
(Steedman, 1994; Meyer, 1997; Boulton, 1999).
However, the idea and use of ecosystem health as a
management tool has been roundly criticised on numerous
fronts, primarily because it is considered ambiguous and
unquantifiable. Indeed, there is no doubt that ecosystem
health cannot be measured directly (Steedman, 1994), and
serves more as a metaphor for a currently desired
environmental state (Suter, 1993; Steedman, 1994). Adoption of the concept does not permit the critical assessment of
environmental conditions, the determination of cause and
effect, or the testing of scientific hypotheses (Suter, 1993).
The concept is basically analogous with human health
(Costanza, 1992; Suter, 1993). This leads to the extrapolation of qualities important to the understanding of human
health to the environment. Thus, by implication, ecosystems

0020-7519/$30.00 Crown Copyright q 2005 Published by Elsevier Ltd. on behalf of Australian Society for Parasitology Inc. All rights reserved.
doi:10.1016/j.ijpara.2005.01.015

706

D.J. Marcogliese / International Journal for Parasitology 35 (2005) 705716

may be considered superorganisms in the Clementsian

sense, with organismal properties such as predetermined
development, homeostasis, and distinct and consistent
integration of its components (Suter, 1993). (Frederick
Clements was an American botanist who pioneered the
concept early in the 20th century that succession in
ecosystems proceeds via growth and maturation to a
dominant, predetermined climax formation with the
capacity for self-healing and self-regulation; hence, a
superorganism). Yet, in reality, it is not possible to state
whether an ecosystem is in poor health or in good health as
the criteria are ambiguous and the definition will vary
according to a particular partys interests. However, the
concept has been successful in raising the profile of
environmental concerns by communicating useful generalisations to resource managers, generating public interest,
capturing the attention of legislators, and consequently
securing funds for scientific activities (Steedman, 1994).
While our scientific colleagues jump on the ecosystem
health bandwagon and the concept continually gains
acceptance in society at large, where does that leave
parasitologists and their parasites? Typically, parasites
are considered with some disdain, if not complete
disgust, by resource managers, some biologists and
scientists, the media, and the general public. This attitude
in part derives from the fact that some parasites are
indeed capable of causing serious disease and are
considered economic and social problems on a global
scale. However, this perception also stems from a lack of
understanding of the complex biology of these elegant
creatures and a lack of awareness of their important role
in ecosystems (Marcogliese, 2004).
One conceptual definition of ecosystem health is the
absence of disease, as disease is considered a stress on
the environment (e.g. contaminants) (Costanza, 1992;
Meyer, 1997), again conveying organismal properties on
an ecosystem. In fact, environmental indices that
incorporate certain parasites and pathogens, such as
Karrs Index of Biotic Integrity, are reduced at higher
frequencies of disease (Suter, 1993). To many, parasites
are organisms of no value to contemporary society that
simply should be eradicated. In the case of deleterious
diseases of humans and their biological resources, that
will no doubt be desirable, but where does that leave the
vast majority of parasites that occur in nature and the
scientists who study them? Parasites are indeed important
components of any ecosystem that not only play key
roles in population dynamics and community structure,
but that can provide important information on environmental stress, food web structure and function, and
biodiversity (Marcogliese, 2003, 2004) that are relevant
to societal needs. Indeed, in theory, the absence of
disease under certain circumstances may reduce biodiversity and promote the expansion of introduced species
(Lafferty, 2003).

2. Why consider parasites?

Virtually all free-living organisms are hosts to parasites
and parasitism, in its broadest sense, is considered to be the
most common lifestyle on earth (Price, 1980). With that in
mind, healthy ecosystems can hardly be considered disease
free. Furthermore, the impact of parasitism on hosts and
their populations is significant. Parasites may affect host
biology in numerous ways, be it behaviourally, physiologically, morphologically, or reproductively (Marcogliese,
2004). Indeed, parasite-host epidemiology relies in part on
the fact that parasites can cause host mortality leading to
regulation of the host population (Anderson and May, 1979;
May and Anderson, 1979). The impact of parasitism extends
beyond the individual host or its population, as mounting
evidence suggests that parasites play an important role in
structuring ecological communities (Dobson and Hudson,
1986; Minchella and Scott, 1991; McCallum and Dobson,
1995; Marcogliese and Cone, 1997a; Marcogliese, 2002,
2004).
Parasites are ubiquitous. They occur in virtually all food
webs at all trophic levels. Often possessing complex life
cycles that rely on trophic interactions for transmission,
parasites can be used to elucidate the role of their hosts in
the food web, that is, to help determine food web structure
(Marcogliese and Cone, 1997a,b; Marcogliese, 2002, 2003,
2004). The concepts discussed herein apply to all ecosystems, but the emphasis and examples pertain to parasites of
aquatic organisms, given that they are the focus of the
majority of environmental studies in parasitology.
The fact that many parasites are trophically transmitted enables them to furnish important ecological
information about the host and its interactions in the
ecosystem (Marcogliese and Cone, 1997a; Overstreet,
1997; Marcogliese, 2003). In addition to highlighting
direct trophic links between their host and other
organisms in the environment, parasites may provide
long-term feeding information, help clarify uncertainties,
and indicate ontogenetic changes in host diet (Table 1).
Hosts may undergo niche shifts, or individuals within
populations may display feeding specialisations illustrated
via the hosts parasite fauna. The presence of predators
or seasonal migrants may be evident from the parasites
occurring in a host. Theoretically, parasites have been
incorporated to help resolve inconsistencies in food web
theory and to test food web models. George-Nascimento
(1987) proposed that parasites were useful indicators of
persistent ecological interactions because their life cycles
are adapted to repetitive seasonal patterns and co-evolved
predator-prey relationships. Indeed, as such, parasites
may be useful indicators of ecosystem stability
(Marcogliese and Cone, 1997a).
Taken together, a study of parasites in a given host
population clearly will generate much information on the
trophic biology of the host and its place in the food
web, in addition to knowledge of food web structure.

D.J. Marcogliese / International Journal for Parasitology 35 (2005) 705716

707

Table 1
Examples of studies that have used parasites as indicators of trophic relationships between fish hosts and other organisms in an aquatic ecosystem
Trophic effect

Hostparasite system

Ecosystem and trophic relationships

Reference

Long-term feeding
interactions

Arctic charr (Salvelinus

alpinus) and
Cystidicola farionis
(Nematoda)
Coryphaenoides
armatus and helminths
Arctic charr (S. alpinus)
and helminths

Lake, northern Norway: occurrence of adult parasite indicates long-term

feeding on the amphipod (Gammarus lacustris)

Knudsen et al. (2004)

Deep sea, New York Bight: change in parasite fauna with size reflects
change in diet
Lake, northern Norway: occurrence of various parasites demonstrate
feeding specializations on either copepods or amphipods by individual
fish
Lakes, Quebec, Canada: change in parasite fauna from those transmitted
by benthic intermediate hosts to those transmitted by zooplankton
reflects niche shift due to competition from introduced white sucker
(Catostomus commersonii)
SW Baltic Sea: parasite fauna demonstrates importance of fish species as
prey for piscivorous fish, seabirds and pinnipeds
Sable Island, Nova Scotia, Canada: presence of parasite in fish indicates
occurrence of American eels (Anguilla rostrata) in ponds

Campbell et al. (1980)

Rivers, marshes, lakes, UK: occurrence of parasites transmitted by

copepods indicates eels feed on zooplankton
NE Atlantic: absence of didymozoid trematodes indicates absence of
swordfish (Xiphias gladius) in ecosystem
Freshwater and brackish water habitats, Mississippi, USA: presence of
parasites indicates occurrence of other intermediate and final hosts in
ecosystems
Pacific coast, Chile: differences in prevalence and intensity of various
parasites reflect food and habitat partitioning
Ythan estuary and Loch Leven; Scotland: incorporation of parasites into
food webs alters basic properties of webs

Kennedy et al. (1992)

Ontogenetic changes
Feeding specializations

Niche shifts

Brook charr (Salvelinus

fontinalis) and
helminths

Predators

Five species of goby

and helminths
Four species of fish and
Proteocephalus
macrocephalus
(Cestoda)
European eels (Anguilla
anguilla) and helminths
Two species of squid
and digeneans
Western mosquitofish
(Gambusia affinis) and
parasites
Cusk eels (Genypterus
spp.) and parasites
Various species of
invertebrates, fish, birds
and helminths

Seasonal or temporary
migrants

Resolve inconsistencies
in diet
Absence of predators
Presence of other
organisms
Resource partitioning
Test food web models

Each parasite species reflects the presence of different

organisms that participate in its life cycle; together, all
the parasite species in a host reflect the presence of a
plethora of host organisms and trophic interactions in the
environment. Thus, parasites potentially may be used as
surrogate indicators of species diversity and ecosystem
diversity, two of the three important levels of biodiversity cited in the Rio Convention on Biological Diversity
(Marcogliese, 2003). Given that pollution and other
stressors may have impacts on populations and communities of organisms, and thus on food web structure,
parasites may be used as natural biological tags of
ecosystem health.
Similarly, parasites may be indicators of climate
change, which is expected to affect the structure and
species composition of entire ecosystems. Examination
of parasite assemblages may reflect alterations in food
web structure and function that result from the myriad
of ecological disturbances to host distributions, water
levels, eutrophication, stratification, ice cover, acidification, oceanic currents, ultraviolet radiation, extreme
weather, and resulting human interference that are
predicted to accompany climatic change (Marcogliese,
2001).

Knudsen et al. (2004)

Dubois et al. (1996)

Zander et al. (1993)

Marcogliese and Scholz
(1999)

Pascual et al. (1996)

Overstreet (1997)

George-Nascimento
(1987)
Huxham et al. (1995)

3. Ecosystem stress and parasites

Numerous studies have examined effects of anthropogenic-induced environmental perturbations on parasitic
organisms at both the population and the community
level. The subject has been extensively and thoroughly
reviewed by Khan and Thulin (1991), Overstreet (1993) and
Mackenzie et al. (1995) among others. Types of stressors
include domestic and industrial sewage, eutrophication,
acidification, pulp mill effluents, pesticides, thermal stress,
hydrological changes, urban development and ultraviolet
light. Recent summaries of pollution studies appear
in Lafferty (1997), Williams and MacKenzie (2003),
Marcogliese (2004) and Sures (2004). In general, responses
of hosts and communities vary depending on the type and
intensity of the stressor, the parasite life cycle and exposure
time (Marcogliese, 2004). However, pollution and stress are
often associated with a reduction in species richness of
parasites (Marcogliese, 2004), contrary to the organismal
notion of ecosystem health meaning the absence of disease.
Diversity of endoparasites may decrease because free-living
stages may be directly affected or certain intermediate hosts
may be reduced, thus hindering parasite transmission
(MacKenzie, 1999). Concurrently, populations of parasite

708

D.J. Marcogliese / International Journal for Parasitology 35 (2005) 705716

species with direct life cycles, usually protozoans and

monogeneans, may increase, an effect usually attributed to a
compromised immune response by the host (Mackenzie
et al., 1995; MacKenzie, 1999). Other parasite populations
may also increase or decrease as a result of direct toxic
effects on themselves or their hosts or indirect environmental effects on intermediate host populations (Poulin, 1992;
Overstreet, 1997).
Free-living infective stages of parasites are considered
fragile and sensitive and, thus, potentially good indicators of
polluted conditions (Overstreet, 1993; MacKenzie, 1999).
Conceivably, if effects on these susceptible stages are
clearly elucidated, then populations of the parasites in an
appropriate host could be monitored (MacKenzie, 1999).
Alternatively, the free-living stages themselves can be used
in standardised toxicity tests (Morley et al., 2003; Pietrock
and Marcogliese, 2003). The effects of different types of
toxic substances on free-living stages of helminths recently
have been reviewed elsewhere (Morley et al., 2003; Pietrock
and Marcogliese, 2003).
Certain parasites, most notably intestinal acanthocephalans and cestodes, have the capacity to accumulate heavy
metals to a degree many times that of their vertebrate hosts
(Sures et al., 1999; Sures, 2001, 2003). These organisms
also hold promise as environmental monitoring tools for
specific pollution problems.
Lafferty (1997), Kennedy (1997) and Overstreet (1997)
discuss the various attributes and limitations of parasites as
environmental indicators. One major drawback is that, with
some exceptions, the direct effects of contaminants on freeliving and parasitic stages of parasites are often unknown
because the lethal and sublethal toxic effects have not been
investigated in controlled laboratory studies. A major
problem in evaluating the pollution work on parasite
populations and communities in situ is that field studies
have employed a variety of experimental designs, in many
cases inadequate or difficult to interpret. Simple designs
involving single impacted and reference sites suffer from
pseudoreplication (Poulin, 1992), and those with upstream
downstream sites are further complicated by riverine effects.
It is important to account for spatial and temporal
heterogeneity in sampling, and this can be done using
before-after-control-impact (BACI) sampling protocols to
incorporate temporal and spatial replication (Lafferty, 1997;
Marcogliese and Cone, 1997b). Other appropriate designs
may involve sampling along gradients when the strength of
the impact varies in space or over a time series if looking for
recovery from an impact (Lafferty, 1997). Another major
sampling concern is host distribution and movement. When
samples come from two or more sites within a system, the
investigator must verify that one is indeed sampling from
different populations of hosts. For example, when collecting
fish from different sites in a river system or coastal
embayment, one may simply be sampling from a highly
vagile host population whose members are exposed to both
impacted and reference conditions (Kennedy, 1997).

In addition, certain populations of parasite species may

respond positively to anthropogenic impacts while others
may respond negatively; thus, it becomes difficult to predict
the effects on the parasite community as a whole (Lafferty,
1997; Kennedy, 1997; Overstreet, 1997).

4. Hierarchical scales of analysis

4.1. Parasite communities
Despite the fact that it is difficult to predict the direction
of effects of anthropogenic impacts on parasite communities, numerous studies have been undertaken to examine
exactly that question. Many of these are summarised in
Mackenzie et al. (1995), Williams and MacKenzie (2003),
Marcogliese (2004) and Sures (2004). Most studies
document changes in some aspect of the parasite fauna
and it is clear that pollution has effects on parasite
populations and communities (Kennedy, 1997). Among
the various anthropogenic impacts that have been examined
for effects on parasite communities, acidification is among
the most profound. A general finding resulting from an
examination of parasite communities in fish from aquatic
ecosystems experiencing acidification is the reduction in
species richness of the parasite component community
(Marcogliese, 2004). Species richness decreased in the
component community of perch (Perca fluviatilis) from
acidified reservoirs in Finland (Halmetoja et al., 2000) and
in American eels (Anguilla rostrata) from acidified streams
in Nova Scotia, Canada (Cone et al., 1993; Marcogliese and
Cone, 1996; Marcogliese and Cone, 1997b) (Fig. 1). In both
systems, these results were primarily due to the loss of
digeneans, which use acid-sensitive molluscs as obligate
intermediate hosts. Marcogliese and Cone (1996, 1997b)
noted that the change in diversity of the parasite community
occurred at the same level of acidity (pH) where species
richness of fish and invertebrates declines; thus, parasite
community diversity mirrors that of the free-living community on which parasites depend for transmission.
Furthermore, by using an artificially limed system to restore
the pH to normal levels, Cone et al. (1993) demonstrated
that the parasite community can recover, again similar to
free-living systems (Marcogliese and Cone, 1997b).
Limited recovery of parasite communities after reduction
of chemical and nutrient loading was also found in Finnish
lakes (Valtonen et al., 2003).
The larval digeneans that occur in snails are often
considered a community. Using a BACI approach, Huspeni
and Lafferty (2004) examined the consequences of saltmarsh restoration on the digenean fauna of the California
horn snail (Cerithidea californica). Prevalence of infection
and species richness increased at restored sites, a result
attributed to an increased bird presence in those
habitats. The digenean assemblage provided an indication
of changes in food web structure associated with

D.J. Marcogliese / International Journal for Parasitology 35 (2005) 705716

A 5

Mean species richness

*
4

and indirect effects on the parasites mediated via impacts

on intermediate hosts. However, as stated previously,
different types of parasites (and their hosts) may respond
either positively or negatively to various contaminants and
environmental stressors.

4.2. Guilds, taxa and suites

Whereas overall community analyses may often be

informative, in many cases specific subsets of the parasite
assemblage may provide a more robust evaluation of
environmental stress. Given that parasite communities are
composed of many species belonging to different phylogenetic lineages with varied life histories, its members may
not respond in the same way to environmental perturbations,
thus confounding interpretation (Lafferty, 1997). In these
cases, it may be best to examine specific taxa, guilds or
suites of parasites within the host population. The choice
should be based on knowledge of the biology of the
parasite and the potential stressors acting on the ecosystem
(Overstreet, 1997). If acidification is the concern, look at the
digeneans. If eutrophication is the problem, examine hosts
for parasites transmitted by oligochaetes or other invertebrates whose populations are either enhanced or decreased
by the nutrient stress (see Zander, 1998; Zander and Reimer,
2002). Based on a synopsis of published literature, Lafferty
(1997) predicted that ciliates and nematodes are sensitive
indicators of eutrophication and thermal effluents, while
digeneans and acanthocephalans are sensitive to heavy
metals and unspecified human disturbance.
Using selected taxa, guilds or suites are analogous to
macroinvertebrate biomonitoring programs that employ the
EPT technique that evaluates the abundance of Ephemeroptera, Plecoptera and Trichoptera in rivers. Guilds, suites
and higher taxa are not necessarily mutually exclusive.
There may be considerable overlap between them and in
some cases they may be identical. A summary of these and
the other categories discussed herein is provided in Table 2.
A novel approach that has been adopted in free-living
aquatic systems is to evaluate communities based on higher
taxa without proceeding to the species level in identification. This has the economical advantage that it is much
less labour-intensive than species-based analyses and
requires less training and expertise. Indeed, higher-level
taxonomic resolution (family, phylum) has proven successful in delineating environmental effects for marine benthic
invertebrates (Warwick, 1988; Somerfield and Clarke,
1995). Many studies of pollution in rivers find that
identification to the family level is sufficient to determine
effects on benthic macrofauna (Gayraud et al., 2003; Waite
et al., 2004). This approach has not been attempted with
parasites, but it would be interesting to see if it yields useful
results. However, caution must be expressed, because the
diversity of parasites in a single species of fish will be much
less than that of marine or riverine macroinvertebrates

0
< 4.7

4.7-5.0

5.1-5.4

>5.4

pH
B 20

15

Species richness

709

10

Lake

R1

R2

Locality
Fig. 1. Parasite species richness in habitats of differing acidity (pH).
(A) Mean species richness of metazoan parasites in American eels
(Anguilla rostrata) from streams in Nova Scotia, characterised by pH.
Data from Marcogliese and Cone (1996). *, Significant difference.
(B) Species richness of protozoan and metazoan parasites in perch (Perca
fluviatilis) from a lake and reservoirs of different pH in Finland. Lake pH
6.4; R1Z5.9; R2Z5.3. Data from Halmetoja et al. (2000).

the restoration activities. In this case, as in numerous others,

improved ecosystem health is reflected by an increase in
parasite occurrence.
In other instances, the use of species richness or diversity
of parasite communities may be somewhat less informative.
Our own data demonstrate only subtle changes in parasite
community structure in spotail shiners (Notropis hudsonius)
exposed to urban effluents in the St Lawrence River
(Marcogliese, unpublished data). However, the contamination levels in the St Lawrence River have declined
dramatically since pollution controls were implemented
during the last two decades. When dealing with only
moderate levels of contaminants, parasite communities may
be less informative as pollution indicators. In this situation,
it may be more prudent to rely on a specific subset of the
parasite community to search for anthropogenic impacts.
It is not surprising that parasite communities may
respond more subtly to less potent environmental impacts.
Parasite communities integrate the direct effects resulting
from impacts of toxicants on each parasite species

710

D.J. Marcogliese / International Journal for Parasitology 35 (2005) 705716

Table 2
Biological and ecological categories of parasites that may be used as indicators of environmental conditions and stress in aquatic ecosystems
Category

Biological basis

Definition

Additional comments and caveats

Populations

Single species

Selected higher taxa

Parasite guilds

Populations can be further subdivided into infra-, component

and suprapopulations (Bush et al., 1997). (Suprapopulations
include all species of hosts.)
May overlap and be identical to guilds and/or suites.
May overlap and be identical to higher taxa and/or suites.

Host guilds (sensu

Zander, 2001)
Suites

Family, order, etc.

Functionally similar
parasite species
Functionally similar
host species
Life histories

Autogenic/allogenic

Life histories

% Autogenic larvae

Life histories

Planktonic/benthic

Life histories

Community

Multiple species

Group of conspecific organisms infecting

a given host species in a given space in
time
Common phylogenetic lineages
Species that share common resources
(e.g. nutrition, habitat)
Host species that share common
resources (e.g. nutrition, habitat)
Species that share intermediate hosts and/
or follow common transmission pathways
Species that use fish (autogenic) or birds
and mammals as definitive hosts
Species whose larval stages occur in fish
and that use piscivorous fish as definitive
hosts
Species that use planktonic or benthic
intermediate hosts
Group of organisms infecting a given host
species in a given space in time

Higher taxa

This is a host-based category distinct from a parasite guild.

May overlap and be identical to higher taxa and/or guilds.
This concept was originally designed to apply to parasites
of fish.
This includes metacercariae, plerocercoids, cystacanths, and
L3 larvae.

Communities can be further subdivided into infra-, component

and supracommunities (Bush et al., 1997). (Supracommunities
include all species of hosts and life cycle stages.)

Species within a community are combined into a higher taxonomic level

(e.g. family, order) for analysis

and higher-level resolution of data may lead to an

unacceptable loss of information.
Guilds of parasites consist of functionally similar species
within a community, or species that share common
resources such as nutrients or habitat (Esch and Fernandez,
1993; Bush et al., 1997). Bush et al. (1997) warn that
membership in a guild should not be defined by taxonomy,
nor should it be based exclusively on occurrence in a
common habitat, as this habitat may be further partitioned
based on resource use. Parasites that inhabit the same tissue
or organ, such as skin, gills or intestine may be considered a
guild. On a finer scale, parasites may partition resources
within a habitat, for example absorbers in the intestine that
occupy either the mucosa or the lumen may be considered as
separate guilds. As used here, guild as originally defined in
parasitology (Esch and Fernandez, 1993) is a parasite-based
concept, distinct from the host-based concept adopted by
Zander (2001), who interprets guild to refer to parasites in a
suite of ecologically similar hosts.
A clear application already discussed where guilds or
higher taxa may be used as indicators of environmental
stress is that of acidification. In acidified streams, intestinal
digeneans are absent or rare in American eels (Cone et al.,
1993; Marcogliese and Cone, 1996). Digeneans herein are
not only a taxonomic group, but they may be considered a
guild in the sense that they share the same habitat in the fish
host. It is the intermediate host, and not the parasite, that is
sensitive to the environmental stress. Note also that
acidification affects all digeneans, not only the intestinal

ones, so that a particular taxonomic group may also be used

as an indicator. Thus, acidification affects parasite communities as a whole but also impacts most strongly on
populations of digeneans.
Apart from communities, the most common groups of
parasites examined to date in response to environmental
stress are ectoparasites (see summaries in Mackenzie et al.,
1995; Williams and MacKenzie, 2003; Sures, 2004),
including trichodinids (Yeomans et al., 1997) and monogeneans (Koskivaara, 1992). These parasites are transmitted
directly and reproduce rapidly. Generally, their
populations proliferate under conditions stressful to their
hosts (MacKenzie, 1999), a response that is more in line
with the concept of ecosystem health equalling the absence
of disease.
In the case of parasites, a suite consists of those species
with similar life-history characteristics or that share
common intermediate hosts (sensu Bush and Holmes,
1986). Given that parasites of a given taxon usually possess
similar life histories, suites of parasites often are taxonomically related as well. The fact that parasites share life
histories implies that they have similar modes of transmission and thus would be jointly affected by any
environmental perturbation affecting the transmission
process. Thus, in some situations, certain suites of higher
parasite taxa may provide information on a specific form of
environmental stress. Marcogliese and Cone (2001) studied
myxozoan communities in spottail shiners in the
St Lawrence River in relation to urban effluents from

D.J. Marcogliese / International Journal for Parasitology 35 (2005) 705716

100

% infected
Coliforms

6000
5000

Prevalence (%)

80

4000
60

3000
40

2000
20

1000

Fecal coliforms/100 ml

Dorval Boucherville

Vert

Beauregard St. Ours

Locality

1.6

Infracommunity richness

6000

Coliforms
1.4

5000

Infracommunity richness

1.2

4000

3000

0.8
0.6

2000

0.4

Fecal coliforms/100 ml

1000

0.2

Dorval Boucherville

Vert

Beauregard St. Ours

Locality
Fig. 2. Occurrence of myxozoan parasites in spottail shiners (Notropis
hudsonius) collected in the St Lawrence River upstream and downstream of
the urban effluent outfall from the island of Montreal. Density of fecal
coliforms per 100 ml water are presented in each graph as a line. The
vertical arrow indicated the relative location of the urban effluent outfall.
(A) Prevalence of myxozoan infections. (B) Mean infracommunity species
richness of myxozoan parasites. Data from Marcogliese and Cone (2001).

the city of Montreal. They found that the component

community species richness, the mean infracommunity
species richness and the prevalence increased downstream
of the effluents compared to upstream (Fig. 2). These results
were attributed to organic input into the sediments downstream that resulted in enhanced populations of the
oligochaete alternate hosts. While they viewed the myxozoan assemblage as a community and measured traditional
community parameters to characterise it, the myxozoans as
a taxonomic group share similar life histories and equally
may be considered a suite, despite the fact that they do not
necessarily share the same resources of their fish host. In
this case, it is the alternate hosts that are directly affected by
the environmental perturbation, thus altering the population
dynamics of the various myxozoan species.
4.3. Parasite populations
Numerous investigators have examined the effects of
environmental stress on single species of parasites in aquatic

711

systems. These studies are summarised in the reviews of

Khan and Thulin (1991), Overstreet (1993), Mackenzie
et al. (1995), Williams and MacKenzie (2003), Marcogliese
(2004) and Sures (2004). Populations of individual parasite
species may increase or decrease when exposed to
environmental stress. Decreases will be observed if the
parasite is in some way negatively affected by direct
exposure to the stress, or if it has a negative impact on the
parasites intermediate host or a negative impact on infected
intermediate hosts (Poulin, 1992). Increases will be seen if
the hosts resistance is somehow compromised under
stressful conditions, or if environmental perturbations result
in a proliferation of the parasites intermediate host. In
addition, the stress may alter the hosts behaviour, leading to
unpredictable changes in encounter rates with free-living
infective stages or those in intermediate hosts (Poulin,
1992).
As with communities and other groupings of parasites, it
is important to relate the biology of the parasite in question
to the system under study, in order to arrive at a meaningful
interpretation of results (Overstreet, 1997). Esch and his
students (Esch et al., 1986; Marcogliese et al., 1990)
measured the abundance and prevalence of the digenean
Crepidostomum cooperi in its mayfly intermediate host
(Hexagenia limbata) in Gull Lake, Michigan between 1969
and 1989. This parasite infects sphaeriid clams as its first
intermediate host, the mayfly as its second, and centrarchid
fish as the definitive host. Prevalence of this parasite in the
mayflies for the most part remained above 80% in males and
90% in females from 1969 to 1984. Then from 1984 to
1989, prevalence dropped to less than 40% (Esch et al.,
1986; Marcogliese et al., 1990). Sampling along a depth
gradient, it was found that prevalence and intensity were
highest in the littoral zone, when mayflies spatially
overlapped with sphaeriid clams. However, mayflies
typically prefer deeper water and normally do not overlap
greatly with sphaeriid clams. During the initial years of the
monitoring program, the perimeter of Gull Lake was
increasingly developed and the lake became eutrophic due
to excessive nutrient input. The sediments in the hypolimnion became anoxic, causing mayflies to shift to a shallower
distribution, overlapping the sphaeriid clams and enhancing
transmission of C. cooperi. Eutrophication was reversed
with the construction of a sewer system around the lake. As
a result, the mayflies reverted to their former distribution in
the deeper waters, thus spatially reducing the transmission
window for the parasite and causing infection levels in the
mayflies to decline (Fig. 3).
There are two other excellent examples of increases in
parasite populations as a result of eutrophication, both with
devastating ecological consequences. The epizootiology of
the nematode Eustrongylides ignotus in wading birds and
the fish intermediate hosts was related to nutrient input and
human activities in Florida (Spalding et al., 1993; Coyner
et al., 2002). The parasite caused 80% mortality of nestling
herons and egrets at one colony alone. The enhanced

712

D.J. Marcogliese / International Journal for Parasitology 35 (2005) 705716

malformations as a result of its trophic impact on nearby

water bodies.

1969-84

Parasites
mayflies
Anoxic

4.4. Other categories of parasite assemblages

sphaerid
clams

1984-89

Parasites

Anoxic

mayflies
sphaerid
clams

Fig. 3. Schematic diagram representing the sequence of events that

occurred in Gull Lake, Michigan as a result of eutrophication and its
subsequent reversal, and the consequences for infection levels of
metacercariae of the digenean Crepidostomum cooperi in the burrowing
mayfly, Hexagenia limbata. (A) Abundance and prevalence of the parasite
was high between 1969 and 1984 because eutrophication, a result of
shoreline development, caused the deeper waters to become anoxic, thus
forcing the mayflies to inhabit less-preferred shallower depths and overlap
with sphaeriid clams, the first intermediate host of C. cooperi.
(B) Construction of a sewage system led to a reversal in eutrophication.
Mayflies returned to their preferred depths, reducing the opportunity for
transmission and causing abundance and prevalence of the parasite to
decline after 1984. Based on information in Esch et al. (1986) and
Marcogliese et al. (1990). Reprinted with slight modifications from
Marcogliese (2001) with permission.

infections were attributed to eutrophication, which led to

increased densities of oligochaetes, the first intermediate
host. Furthermore, discharge of treated sewage was halted in
one watershed, leading to a reduction in prevalence in the
eastern mosquitofish (Coyner et al., 2003), further implicating nutrient input as the ultimate cause of high E. ignotus
infection.
Another environmental problem of global concern is the
rise in deformities in frogs. While originally attributed to a
number of causes including pesticides and UV radiation, it
has been clearly demonstrated that the infection with
digenean Ribeiroia ondatrae can cause limb deformities
(Blaustein and Johnson, 2003; Johnson and Sutherland,
2003). Furthermore, in an experimental field study,
pesticides alone did not cause malformations in wood
frogs (Rana sylvatica), but exposure to the parasite did.
Moreover, parasites and pesticides together acted synergistically, leading to a greater occurrence of deformities
(Kiesecker, 2002). High malformation rates have previously
been linked to agricultural activities (Ouellet et al., 1997),
which many then attributed to pesticides. However, the
cause may be ecological and not toxicological. Biomass of
the first intermediate host (planorbid snails: Planorbella
spp.) is directly correlated to nutrient input, and parasite
abundance is correlated with snail biomass (Johnson and
Chase, 2004). In addition, the frequency of malformations is
directly correlated with abundance of R. ondatrae. Thus,
agriculture appears to be a major culprit in the rise of frog

Parasitologists have characterised their study organisms

in numerous different ways. One particular dichotomy that
has spurred much discussion is the breakdown of parasitic
helminth communities of fish into autogenic and allogenic
species (Esch et al., 1988), based on their life histories and
dispersal capabilities. Allogenic species are those that use
vertebrates other than fish, usually birds or mammals, as
definitive hosts. These parasites are capable of relatively
rapid dissemination from one locality to another via the
movement of their definitive hosts. Other species that
mature in fish are referred to as autogenic parasites.
Basically these latter species must complete their life
cycle within the same aquatic habitat.
This categorisation has been used extensively by others,
mostly in the context of parasite community structure and its
determinants. However, there is excellent potential for its
application to environmental studies. In a landmark paper
published more than three decades ago, Esch (1971),
following upon the work of Wisniewski (1958), described
fundamental differences between the parasite fauna of fish
inhabiting oligotrophic and eutrophic lakes. In oligotrophic
systems, fish were infected primarily with adult parasites
(autotrophic), whereas larval forms (allogenic) that matured
in birds were more common in fish from eutrophic lakes.
A further potentially useful characterisation of the
parasite fauna of fish according to their life histories is the
proportion of larval autogenic forms. These include larval
stages of autogenic parasites that occur in fish, such as
digenean metacercariae, cestode plerocercoids, nematode
larvae, and acanthocephalan cystacanths whose adults occur
in other piscivorous fish. The proportion of larval autogenic
parasites may reflect the predation pressure by piscivorous
fish in the ecosystem and, thus, the complexity of the local
food web. Examination of the distribution of larval
autogenic parasites in spottail shiners among sites in the
St Lawrence River is currently underway (Marcogliese,
unpublished data).
Another means of characterising parasites, also based on
life histories, that can be applied to environmental studies is
to divide them into groups based on whether they have
planktonic or benthic intermediate hosts (for reviews, see
Marcogliese, 1995, 2002). For example, after intitial
eutrophication in the Baltic Sea, herbivore and detritivore
populations increased (e.g. the snail Hydrobia spp.), as did
their parasites. However, as eutrophication proceeded the
bottom waters and sediments became anoxic, and parasites
that use benthic intermediate hosts were eliminated (Zander,
1998; Zander and Reimer, 2002).
Indeed, there may be other divisions of the parasite fauna
not yet considered. It is essential that these categories be
based on biological realism and that they reflect the ecology

D.J. Marcogliese / International Journal for Parasitology 35 (2005) 705716

of the ecosystem under study, and not artificial constructs. It

is noteworthy that some of the most useful concepts to date
are based on parasite transmission and life histories.
Landsberg et al. (1998) developed a preliminary parasite
index for silver perch (Bairdiella chrysura) in Floridian
estuaries as a bioindicator of pollution stress. Parasites were
separated into groups based on the type of life cycle, the life
cycle stage residing in the fish, the number and type of hosts
participating in the life cycle and their habitats, and the
mode of transmission. Their conclusion was that the
parasites were more sensitive indicators to environmental
degradation than their fish hosts. As remarked elsewhere,
the fact that parasites possess complex life cycles makes
them extremely valuable information units about environmental conditions, because their presence/absence tells us a
great deal about not only their host ecology but food web
interactions,
biodiversity,
and
environmental
stress (Marcogliese and Cone, 1997a; Overstreet, 1997;
Marcogliese, 2002, 2003, 2004). Combining different
species based on shared patterns of transmission provides
a potentially more powerful indicator of environmental
conditions.

713

5. Conclusions
The incorporation of parasitology into environmental
assessments and any biotic inventories should be encouraged strongly. The study of parasitology has already
contributed much to the discrimination of commercial fish
stocks, movement, and recruitment. The use of parasites to
discriminate among host populations inhabiting sites of
different environmental quality is conceptually similar. Just
as there are criteria for the selection of appropriate parasites
for analysis of fish stocks (Williams et al., 1992; MacKenzie
and Abaunza, 1998), criteria and guidelines also exist for
selecting hosts and parasites as indicators of pollution and
other stresses (Mackenzie et al., 1995; Overstreet, 1997). In
the case of proper fisheries management, managers do not
rely on a single technique, but on at least two, be they
morphological, genetic, biochemical or parasitological, to
obtain the required information. Similarly, resource
managers interested in environmental quality should consult
the expertise available in their ecosystem assessments, and
that means using parasitology along with other traditional
other disciplines.

Table 3
Selected examples of multidisciplinary investigations incorporating parasitology into effects of pollution and environmental stress on vertebrates in aquatic
ecosystems
Host
Fish
Ariopsis assimilis
(Mayan catfish)
Bairdiella chrysura
(silver perch)
Oncorhynchus
tshawytscha (Chinook
salmon)
Perca flavescens
(yellow perch)
Platichthys flesus
(European flounder)

Pleuronectes
americanus (winter
flounder)
Siganus rivulatus
(rabbitfish)
Tautogolabrus
adspersus (cunner)
Amphibians
Rana pipiens
(leopard frog)
Rana sylvatica (wood
frog)
a
b
c

Parasites

Location

Variables

Reference

Metazoans

Chetumal Bay, Mexico

Protozoans and
metazoans
Nanophyetus
salmonicida

Estuaries, Florida

Immunological (lysozymes, leucocytes,

phagocytosis, ROSa)
Histopathological, condition indices, abiotic
parameters, contaminants in host tissues
Immunological (kidney and spleen
plaque-forming assay)

Vidal-Martnez et al.
(2003)
Landsberg et al. (1998)

Laboratory

Apophallis brevis,
Raphidascaris acus
Protozoans and
metazoans

St Lawrence River,
Quebec
North Sea

Protozoans and
metazoans

German Bight, North

Sea

Protozoans and
metazoans
Protozoans and
metazoans
Protozoans and
metazoans
Acanthocephalans

Southwest Newfoundland
Western Newfoundland
Mediterranean Sea,
Red Sea
Western Newfoundland

Rhabdias ranae

Laboratory

Immunological (cellarity, phagocytosis,

lymphocyte proliferation)

Ribeiroia sp.,
Telorchis sp.

Field mesocosms and

laboratory

Immunological (eosinophils)

ROS, reactive oxygen species.

EROD, CYP1A-dependent monooxygenase ethoxyresorufin-O-deethylase.
MFO, mixed function oxygenases.

Ecotoxicological (oxidative stress)

Immunological and ecotoxicological
(lysozyme stability, ERODb), contaminants in
host tissues
Immunological (lysozymes, leucocytes,
phagocytosis, respiratory burst, ROSa), abiotic
parameters
Histopathological, condition indices,
immunological (lymphocytes)
Histopathological, condition indices,
ecotoxicological (MFOc, acetylcholinesterase)
Immunological and ecotoxicological
(lysozyme stability, ERODb)
Histopathological, condition indices,
toxicological (ERODb)

Jacobson et al. (2003)

Marcogliese et al.
(2005)
Broeg et al. (1999)

Schmidt et al. (2003)

and Skouras et al.
(2003a,b)
Barker et al. (1994)
Khan and Payne (1997)
Diamant et al. (1999)
Billiard and Khan
(2003)
Christin et al. (2003)
and Gendron et al.
(2003)
Kiesecker (2002)

714

D.J. Marcogliese / International Journal for Parasitology 35 (2005) 705716

Proper interpretation of parasitological results depends

primarily on knowledge of the organisms under study, both
parasites and their hosts and their relationship to the
environment (Overstreet, 1997). Moreover, results from
applied parasitology should be corroborated using other
techniques (Overstreet, 1997). There is a pressing need for
multidisciplinary studies (Table 3) that incorporate ecology,
ecotoxicology, parasitology, immunology, and other disciplines as seen in some recent initiatives in the North Sea,
the Red Sea, coastal Mexico and the southeastern United
States (Landsberg et al., 1998; Broeg et al., 1999; Diamant
et al., 1999; Vidal-Martnez et al., 2003).
Traditionally, parasites have only been considered in
environmental models if they cause disease to humans or to
valuable resources. There is an incredibly diverse array of
parasites that do not necessarily cause economic damage to
their hosts and that may appear relatively benign. In fact, the
species composition of parasite communities is clearly
impacted by environmental stress and species richness tends
to decrease under degraded conditions. Rather than be
considered villains causing disease in a superorganism,
parasites are in reality ubiquitous and integral components
of all ecosystems that by their very nature are incredibly
valuable information units. Healthy ecosystems have
healthy parasite communities and assemblages, and sick
superorganisms do not!

Acknowledgements
I thank Alan Lymbery for the invitation to participate in
the symposium entitled Parasites and Ecosystem Health at
the 46th Annual Meeting of the Australian Society of
Parasitology Inc. (ASP) in Freemantle, Western Australia.
A travel fellowship from the ASP is gratefully acknowledged. Comments on the manuscript by Drs Jane Cook,
Alan Lymbery and Dave Spratt are greatly appreciated.

References
Anderson, R.M., May, R.M., 1979. Population biology of infectious
diseases: part I. Nature 280, 361367.
Barker, D.E., Khan, R.A., Hooper, R., 1994. Bioindicators of stress in
winter flounder, Pleuronectes americanus, captured adjacent to a pulp
and paper mill in St Georges Bay, Newfoundland. Can. J. Fish. Aquat.
Sci. 51, 22032209.
Billiard, S.M., Khan, R.A., 2003. Chronic stress in cunner Tautogolabrus
adspersus, exposed to municipal and industrial effluents. Ecotox.
Environ. Safety 55, 918.
Blaustein, A.R., Johnson, P.T.J., 2003. Explaining frog deformities. Sci.
Am. 288, 6065.
Boulton, A.J., 1999. An overview of river health assessment: philososphies,
practice, problems and prognosis. Freshw. Biol. 41, 469479.
Broeg, K., Zander, S., Diamant, A., Korting, W., Kruner, G., Paperna, I.,
Westernhagen, H.v., 1999. The use of fish metabolic, pathological and
parasitological indices in pollution monitoring. I. North Sea. Helgol.
Mar. Res. 53, 171194.

Bush, A.O., Holmes, J.C., 1986. Intestinal helminths of lesser scaup ducks:
patterns of association. Can. J. Zool. 64, 132141.
Bush, A.O., Lafferty, K.D., Lotz, J.M., Shostak, A.W., 1997. Parasitology
meets ecology on its own terms: Margolis et al. revisited. J. Parasitol.
83, 575583.
Campbell, R.A., Haedrich, R.L., Munroe, T.A., 1980. Parasitism and
ecological relationships among deep-sea benthic fishes. Mar. Biol. 57,
301313.
Christin, M.S., Gendron, A.D., Brousseau, P., Menard, L.,
Marcogliese, D.J., Cyr, D., Ruby, S., Fournier, M., 2003. Effects of
agricultural pesticides on the immune system of Rana pipiens and on its
resistance to parasitic infection. Environ. Toxicol. Chem. 22,
11271133.
Cone, D.K., Marcogliese, D.J., Watt, W.D., 1993. Metazoan parasite
communities of yellow eels (Anguilla rostrata) in acidic and limed
rivers of Nova Scotia. Can. J. Zool. 71, 177184.
Costanza, R., 1992. Toward an operational definition of ecosystem health.
In: Costanza, R., Norton, B., Haskell, B. (Eds.), Ecosystem Health: New
Goals for Environmental Management. Island Press, Washington, DC,
pp. 239256.
Coyner, D.F., Spalding, M.G., Forrester, D.J., 2002. Epizootiology of
Eustrongylides ignotus in Florida: distribution, density, and natural
infections in intermediate hosts. J. Wildl. Dis. 38, 483499.
Coyner, D.F., Spalding, M.G., Forrester, D.J., 2003. Influence of treated
sewage on infections of Eustrongylides ignotus (Nematoda: Dioctophymatoidea) in eastern mosquitofish (Gambusia holbrooki) in an
urban watershed. Comp. Parasitol. 70, 205210.
Diamant, A., Banet, A., Paperna, I., Westernhagen, H.v., Broeg, K.,
Kruener, G., Koerting, W., Zander, S., 1999. The use of fish metabolic,
pathological and parasitological indices in pollution monitoring. II. The
Red Sea and Mediterranean. Helgol. Mar. Res. 53, 195208.
Dobson, A., Hudson, P.J., 1986. Parasites, disease and the structure of
ecological communities. Trends Ecol. Evol. 1, 1115.
Dubois, N., Marcogliese, D.J., Magnan, P., 1996. Effect of the introduction
of white sucker, Catostomus commersoni, on the parasite fauna of brook
trout, Salvelinus fontinalis. Can. J. Zool. 74, 13041312.
Esch, G.W., 1971. Impact of ecological succession on the parasite fauna in
centrarchids from oligotrophic and eutrophic ecosystems. Am. Midl.
Nat. 86, 160168.
Esch, G.W., Fernandez, J.C., 1993. A Functional Biology of Parasitism.
Chapman and Hall, London.
Esch, G.W., Hazen, T.C., Marcogliese, D.J., Goater, T.M., Crews, A.E.,
1986. A long-term study on the population biology of Crepidostomum
cooperi (Trematoda: Allocreadidae) in the burrowing mayfly, Hexagenia limbata (Ephemeroptera). Am. Midl. Nat. 116, 304314.
Esch, G.W., Kennedy, C.R., Bush, A.O., Aho, J.M., 1988. Patterns in
helminth colonization in freshwater fish in Great Britain: alternative
strategies for colonization. Parasitology 96, 519532.
Gayraud, S., Statzner, B., Bady, P., Haybachp, A., Scholl, F., UsseglioPolatera, P., Bacchi, M., 2003. Invertebrate traits for the biomonitoring
of large European rivers: an initial assessment of alternative metrics.
Freshw. Biol. 48, 20452064.
Gendron, A.D., Marcogliese, D.J., Barbeau, S., Christin, M.-S.,
Brousseau, P., Ruby, S., Cyr, D., Fournier, M., 2003. Exposure of
leopard frogs to a pesticide mixture affects life history characteristics of
the lungworm Rhabdias ranae. Oecologia 135, 469476.
George-Nascimento, M.A., 1987. Ecological helminthology of wildlife
animal hosts from South America: a literature review and a search for
patterns in marine food webs. Rev. Chil. Hist. Nat. 60, 181202.
Halmetoja, A., Valtonen, E.T., Koskenniemi, E., 2000. Perch (Perca
fluviatilis L.) parasites reflect ecosystem conditions: a comparison of
a natural lake and two acidic reservoirs in Finland. Int. J. Parasitol. 30,
14371444.
Huspeni, T.C., Lafferty, K.D., 2004. Using larval trematodes that parasitze
snails to evaluate a saltmarsh restoration project. Ecol. Appl. 14,
795804.

D.J. Marcogliese / International Journal for Parasitology 35 (2005) 705716

Huxham, M., Raffaelli, D., Pike, A., 1995. Parasites and food web patterns.
J. Anim. Ecol. 64, 168176.
Jacobson, K.C., Arkoosh, M.R., Kagley, A.N., Clemons, E.R.,
Collier, T.K., Casillas, E., 2003. Cumulative effects of natural and
anthropogenic stress on immune function and disease resistance in
juvenile Chinook salmon. J. Aquat. Anim. Health 15, 112.
Johnson, P.T., Chase, J.M., 2004. Parasites in the food web: linking
amphibian malformations and aquatic eutrophication. Ecol. Lett. 7,
521526.
Johnson, P.T.K., Sutherland, D.R., 2003. Amphibian deformities and
Ribeiroia infection: an emerging helminthiasis. Trends Parasitol. 19,
332335.
Karr, J.T., 1999. Defining and measuring river health. Freshw. Biol. 41,
221234.
Kennedy, C.R., 1997. Freshwater fish parasites and environmental quality:
an overview and caution. Parassitologia 39, 249254.
Kennedy, C.R., Nie, P., Kaspers, J., Paulisse, J., 1992. Are eels (Anguilla
anguilla L.) planktonic feeders? Evidence from parasite communities.
J. Fish Biol. 41, 567580.
Khan, R.A., Payne, J.F., 1997. A multidisciplinary approach using several
biomarkers, including a parasite, as indicators of pollution: a case
history from a paper mill in Newfoundland. Parassitologia 39, 183188.
Khan, R.A., Thulin, J., 1991. Influence of pollution on parasites of aquatic
animals. Adv. Parasitol. 30, 201238.
Kiesecker, J., 2002. Synergism between trematode infection and pesticide
exposure: a link to amphibian limb deformities in nature? Proc. Nat.
Acad. Sci. 99, 99009904.
Knudsen, R., Curtis, M.A., Kristoffersen, R., 2004. Aggregation of
helminths: the role of feeding behavior of fish hosts. J. Parasitol. 90,
17.
Koskivaara, M., 1992. Environmental factors affecting monogeneans
parasitic on freshwater fish. Parasitol. Today 8, 339342.
Lafferty, K.D., 1997. Environmental parasitology: What can parasites tell
us about human impacts on the environment?. Parasitol. Today 13,
251255.
Lafferty, K.D., 2003. Is disease increasing or decreasing, and does it impact
or maintain biodiversity?. J. Parasitol. 89, S101S105.
Landsberg, J.H., Blakesley, B.A., Reese, R.O., McRae, G., Forstchen, P.R.,
1998. Parasites of fish as indicators of environmental stress. Environ.
Monitor. Assess. 51, 211232.
MacKenzie, K., 1999. Parasites as pollution indicators in marine
ecosystems: a proposed early warning system. Mar. Pol. Bull. 38,
955959.
MacKenzie, K., Abaunza, P., 1998. Parasites as biological tags for stock
discrimination of marine fish: a guide to procedures and methods. Fish.
Res. 38, 4556.
Mackenzie, K., Williams, H.H., Williams, B., McVicar, A.H., Siddall, R.,
1995. Parasites as indicators of water quality and the potential use of
helminth transmission in marine pollution studies. Adv. Parasitol. 35,
85144.
Marcogliese, D.J., 1995. The role of zooplankton in the transmission of
helminth parasites to fish. Rev. Fish Biol. Fish. 5, 336371.
Marcogliese, D.J., 2001. Implications of climate change for parasitism of
animals in the aquatic environment. Can. J. Zool. 79, 13311352.
Marcogliese, D.J., 2002. Food webs and the transmission of parasites to
marine fish. Parasitology 124, S83S99.
Marcogliese, D.J., 2003. Food webs and biodiversity: are parasites the
missing link? J. Parasitol. 89, S106S113.
Marcogliese, D.J., 2004. Parasites: small players with crucial roles in the
ecological theatre. EcoHealth 1, 151164.
Marcogliese, D.J., Cone, D.K., 1996. On the distribution and abundance of
eel parasites in Nova Scotia: influence of pH. J. Parasitol. 82, 389399.
Marcogliese, D.J., Cone, D.K., 1997a. Food webs: a plea for parasites.
Trends Ecol. Evol. 12, 320325.
Marcogliese, D.J., Cone, D.K., 1997b. Parasite communities as indicators
of ecosystem stress. Parassitologia 39, 227232.

715

Marcogliese, D.J., Cone, D.K., 2001. Myxozoan communities parasitizing

Notropis hudsonius (Cyprinidae) at selected localities on the St.
Lawrence River, Quebec: possible effects of urban effluents.
J. Parasitol. 87, 951956.
Marcogliese, D.J., Scholz, T., 1999. Recent visitations by eels to Sable
Island, Canada, confirmed by parasites. J. Fish Biol. 54, 685687.
Marcogliese, D.J., Goater, T.M., Esch, G.W., 1990. Crepidostomum
cooperi (Allocreadidae) in the burrowing mayfly, Hexagenia limbata
(Ephemeroptera) related to trophic status of a lake. Am. Midl. Nat. 124,
309317.
Marcogliese, D.J., Brambilla, L.G., Gagne, F., Gendron, A.D., 2005. Joint
effects of parasitism and pollution on biomarkers of oxidative stress in
yellow perch (Perca flavescens). Dis. Aquat. Org. 63, 7784.
May, R.M., Anderson, R.M., 1979. Population biology of infectious
diseases: part II. Nature 280, 455461.
McCallum, H., Dobson, A., 1995. Detecting disease and parasite threats to
endangered species and ecosystems. Trends Ecol. Evol. 10, 190194.
Meyer, J.L., 1997. Stream health: incorporating the human dimension to
advance stream ecology. J. N. Am. Benthol. Soc. 16, 439447.
Minchella, D.J., Scott, M.E., 1991. Parasitism: a cryptic determinant of
animal community structure. Trends Ecol. Evol. 6, 250254.
Morley, N.J., Irwin, S.W.B., Lewis, J.W., 2003. Pollution toxicity to the
transmission of larval digeneans through their molluscan hosts.
Parasitology 126, S5S26.
Ouellet, M., Bonin, J., Rodrigue, J., DesGranges, J.-L., Lair, S., 1997.
Hindlimb deformities (ectromelia, ectrodactyly) in free-living anurans
from agricultural habitats. J. Wildl. Dis. 33, 95104.
Overstreet, R.M., 1993. Parasitic diseases of fishes and their relationship
with toxicants and other environmental factors. In: Couch, J.A.,
Fournie, J.W. (Eds.), Pathobiology of Marine and Estuarine Organisms.
CRC Press, Boca Raton, FL, pp. 111156.
Overstreet, R.M., 1997. Parasitological data as monitors of environmental
health. Parassitologia 39, 169175.
Pascual, S., Gonzales, A., Arias, C., Guerra, A., 1996. Biotic relationships
of Illex condetii and Todaropsis eblanae (Cephalopoda, Ommastrephidae) in the Northeast Atlantic: evidence from parasites. Sarsia 81,
265274.
Pietrock, M., Marcogliese, D.J., 2003. Free-living endohelminth stages: at
the mercy of environmental conditions. Trends Parasitol. 19, 293299.
Poulin, R., 1992. Toxic pollution and parasitism in freshwater fish.
Parasitol. Today 8, 5861.
Price, P.W., 1980. Evolutionary Biology of Parasites. Princeton University
Press, Princeton.
Schmidt, V., Zander, S., Korting, W., Steinhagen, D., 2003. Parasites of the
flounder Platichthys flesus (L.) from the German Bight North Sea, and
their potential use in ecosystem monitoring. Helgol. Mar. Res. 57,
236251.
Skouras, A., Broeg, K., Dizer, H., Westernhagen, H.v., Hansen, P.-D.,
Steinhagen, D., 2003a. The use of innate immune responses as
biomarkers in a programme of integrated biological effects monitoring
on flounder (Platichthys flesus) from the southern North Sea. Helgol.
Mar. Res. 57, 190198.
Skouras, A., Schmidt, V., Korting, W., Steinhagen, D., 2003b. Note: the
effect of parasite infection on the innate immune response of European
flounder (Platichthys flesus L.) in the southern North Sea. Helgol. Mar.
Res. 57, 176180.
Somerfield, P.J., Clarke, K.R., 1995. Taxonomic levels, in marine
community studies, revisted. Mar. Ecol. Prog. Ser. 127, 113119.
Spalding, M.G., Bancroft, G.T., Forrester, D.J., 1993. The epizootiology of
eustrongylidosis in wading birds (Ciconiiformes) in Florida. J. Wildl.
Dis. 29, 237249.
Steedman, R.J., 1994. Ecosystem health as a management goal. J.N. Am.
Benthol. Soc. 13, 605610.
Sures, B., 2001. The use of fish parasites as bioindicators of heavy metals in
aquatic ecosystems: a review. Aquat. Ecol. 35, 245255.
Sures, B., 2003. Accumulation of heavy metals by intestinal helminths in
fish: an overview and perspective. Parasitology 126, S53S60.

716

D.J. Marcogliese / International Journal for Parasitology 35 (2005) 705716

Sures, B., 2004. Environmental parasitology: relevancy of parasites

in monitoring environmental pollution. Trends Parasitol. 20,
170177.
Sures, B., Siddall, R., Taraschewski, H., 1999. Parasites as accumulation indicators of heavy metal pollution. Parasitol. Today 15,
1621.
Suter II., G.W., 1993. A critique of ecosystem health concepts and indexes.
Environ. Toxicol. Chem. 12, 15331539.
Valtonen, E.T., Holmes, J.C., Aronen, J., Rautalahti, I., 2003. Parasite
communities as indicators of recovery from pollution: parasites of roach
(Rutilus rutilus) amd perch (Perca fluviatilis) in central Finland.
Parasitology 126, S43S52.
Vidal-Martnez, V.M., Aguirre-Mecedo, M.L., Norena-Barroso, E., GoldBouchot, G., Caballaro-Pinzon, P.I., 2003. Potential interactions
between metazoan parasites of the Mayan catfish Ariopsis assimilis
and chemical pollution in Chetumal Bay, Mexico. J. Helminthol. 77,
173184.
Waite, I.R., Herlihy, A.T., Larsen, D.P., Urquhart, N.S., Klemm, D.J., 2004.
The effects of macroinvertebrate taxonomic resolution in large
landscape bioassessments: an example from the Mid-Atlantic Highlands, USA. Freshw. Biol. 49, 474489.

Warwick, R.M., 1988. Analysis of community attributes of the macrobenthos of Frierfjord/Langesundfjord at taxonomic levels higher than
species. Mar. Ecol. Prog. Ser. 46, 167170.
Williams, H.H., MacKenzie, K., 2003. Marine parasites as pollution
indicators: an update. Parasitology 126, S27S41.
Williams, H.H., MacKenzie, K., McCarthy, A.M., 1992. Parasites as
biological indicators of the population biology, migrations, diet, and
phylogenetics of fish. Rev. Fish Biol. Fish. 2, 144176.
Wisniewski, W.L., 1958. Characterization of the parasitofauna of an
eutrophic lake. Acta Parasitol. Pol. 6, 164.
Yeomans, W.E., Chubb, J.C., Sweeting, R.A., 1997. Use of protozoan
communities for pollution monitoring. Parassitologia 39, 201212.
Zander, C.D., 1998. Ecology of host parasite relationships in the Baltic Sea.
Naturwissens. 85, 426436.
Zander, C.D., 2001. The guild as a concept and a means in ecological
parasitology. Parasitol. Res. 87, 484488.
Zander, C.D., Reimer, L.W., 2002. Parasitism at the ecosystem level in the
Baltic Sea. Parasitology 124, S119S135.
Zander, C.D., Strohbach, U., Groenewold, S., 1993. The importance of
gobies (Gobiidae, Teleostei) as hosts and transmitters of parasites in the
SW Baltic. Helgolander Meeresunters. 47, 81111.