1 International Journal for Parasitology 35 (2005) 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 public s 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 host s 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.: C ; fax: C address: 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 /$30.00 Crown Copyright q 2005 Published by Elsevier Ltd. on behalf of Australian Society for Parasitology Inc. All rights reserved. doi: /j.ijpara
2 706 D.J. Marcogliese / International Journal for Parasitology 35 (2005) 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 party s 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 Karr s 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 host s 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.
3 D.J. Marcogliese / International Journal for Parasitology 35 (2005) 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 Host parasite system Ecosystem and trophic relationships Reference Long-term feeding interactions Ontogenetic changes Feeding specializations Niche shifts Predators Seasonal or temporary migrants Resolve inconsistencies in diet Absence of predators Presence of other organisms Resource partitioning Test food web models Arctic charr (Salvelinus alpinus) and Cystidicola farionis (Nematoda) Coryphaenoides armatus and helminths Arctic charr (S. alpinus) and helminths Brook charr (Salvelinus fontinalis) and helminths 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 Lake, northern Norway: occurrence of adult parasite indicates long-term feeding on the amphipod (Gammarus lacustris) 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 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 Knudsen et al. (2004) Campbell et al. (1980) Knudsen et al. (2004) Dubois et al. (1996) Zander et al. (1993) Marcogliese and Scholz (1999) Kennedy et al. (1992) Pascual et al. (1996) Overstreet (1997) George-Nascimento (1987) Huxham et al. (1995) 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 webstructureandfunctionthatresultfromthemyriad 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). 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
4 708 D.J. Marcogliese / International Journal for Parasitology 35 (2005) 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
5 D.J. Marcogliese / International Journal for Parasitology 35 (2005) A Mean species richness B 20 Species richness < >5.4 ph 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 * 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 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
6 710 D.J. Marcogliese / International Journal for Parasitology 35 (2005) 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 Group of conspecific organisms infecting a given host species in a given space in time Populations can be further subdivided into infra-, component and suprapopulations (Bush et al., 1997). (Suprapopulations include all species of hosts.) Selected higher taxa Family, order, etc. Common phylogenetic lineages May overlap and be identical to guilds and/or suites. Parasite guilds Functionally similar Species that share common resources May overlap and be identical to higher taxa and/or suites. parasite species (e.g. nutrition, habitat) Host guilds (sensu Functionally similar Host species that share common This is a host-based category distinct from a parasite guild. Zander, 2001) host species resources (e.g. nutrition, habitat) Suites Life histories Species that share intermediate hosts and/ May overlap and be identical to higher taxa and/or guilds. or follow common transmission pathways Autogenic/allogenic Life histories Species that use fish (autogenic) or birds and mammals as definitive hosts This concept was originally designed to apply to parasites of fish. % Autogenic larvae Life histories Species whose larval stages occur in fish and that use piscivorous fish as definitive hosts Planktonic/benthic Life histories Species that use planktonic or benthic intermediate hosts Community Multiple species Group of organisms infecting a given host species in a given space in time Higher taxa Species within a community are combined into a higher taxonomic level (e.g. family, order) for analysis This includes metacercariae, plerocercoids, cystacanths, and L 3 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.) 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
7 D.J. Marcogliese / International Journal for Parasitology 35 (2005) A 100 Prevalence (%) B Infracommunity richness % infected Coliforms Dorval Boucherville Vert Beauregard St. Ours 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 Parasite populations Locality Infracommunity richness Coliforms Dorval Boucherville Vert Beauregard St. Ours Locality Numerous investigators have examined the effects of environmental stress on single species of parasites in aquatic 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). 0 Fecal coliforms/100 ml Fecal coliforms/100 ml 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 parasite s intermediate host or a negative impact on infected intermediate hosts (Poulin, 1992). Increases will be seen if the host s resistance is somehow compromised under stressful conditions, or if environmental perturbations result in a proliferation of the parasite s intermediate host. In addition, the stress may alter the host s 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 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 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
8 712 D.J. Marcogliese / International Journal for Parasitology 35 (2005) A B Anoxic Parasites Anoxic Parasites mayflies mayflies sphaerid clams 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 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 malformations as a result of its trophic impact on nearby water bodies Other categories of parasite assemblages 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 Wiśniewski (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
9 D.J. Marcogliese / International Journal for Parasitology 35 (2005) 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. 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 Parasites Location Variables Reference Fish Ariopsis assimilis (Mayan catfish) Metazoans Chetumal Bay, Mexico Immunological (lysozymes, leucocytes, phagocytosis, ROS a ) Vidal-Martínez et al. (2003) Bairdiella chrysura Protozoans and Estuaries, Florida Histopathological, condition indices, abiotic Landsberg et al. (1998) (silver perch) metazoans parameters, contaminants in host tissues Oncorhynchus Nanophyetus Laboratory Immunological (kidney and spleen Jacobson et al. (2003) tshawytscha (Chinook salmon) salmonicida plaque-forming assay) Perca flavescens (yellow perch) Apophallis brevis, Raphidascaris acus St Lawrence River, Quebec Ecotoxicological (oxidative stress) Marcogliese et al. (2005) Platichthys flesus (European flounder) Pleuronectes americanus (winter flounder) Siganus rivulatus (rabbitfish) Tautogolabrus adspersus (cunner) Amphibians Rana pipiens (leopard frog) Rana sylvatica (wood frog) Protozoans and metazoans Protozoans and metazoans Protozoans and metazoans Protozoans and metazoans Protozoans and metazoans Acanthocephalans North Sea German Bight, North Sea Southwest Newfoundland Western Newfoundland Mediterranean Sea, Red Sea Western Newfoundland Immunological and ecotoxicological (lysozyme stability, EROD b ), contaminants in host tissues Immunological (lysozymes, leucocytes, phagocytosis, respiratory burst, ROS a ), abiotic parameters Histopathological, condition indices, immunological (lymphocytes) Histopathological, condition indices, ecotoxicological (MFO c, acetylcholinesterase) Immunological and ecotoxicological (lysozyme stability, EROD b ) Histopathological, condition indices, toxicological (EROD b ) Rhabdias ranae Laboratory Immunological (cellarity, phagocytosis, lymphocyte proliferation) Ribeiroia sp., Telorchis sp. Field mesocosms and laboratory a ROS, reactive oxygen species. b EROD, CYP1A-dependent monooxygenase ethoxyresorufin-o-deethylase. c MFO, mixed function oxygenases. 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) Immunological (eosinophils) Kiesecker (2002)
10 714 D.J. Marcogliese / International Journal for Parasitology 35 (2005) 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-Martínez 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., Population biology of infectious diseases: part I. Nature 280, Barker, D.E., Khan, R.A., Hooper, R., Bioindicators of stress in winter flounder, Pleuronectes americanus, captured adjacent to a pulp and paper mill in St George s Bay, Newfoundland. Can. J. Fish. Aquat. Sci. 51, Billiard, S.M., Khan, R.A., Chronic stress in cunner Tautogolabrus adspersus, exposed to municipal and industrial effluents. Ecotox. Environ. Safety 55, Blaustein, A.R., Johnson, P.T.J., Explaining frog deformities. Sci. Am. 288, Boulton, A.J., An overview of river health assessment: philososphies, practice, problems and prognosis. Freshw. Biol. 41, Broeg, K., Zander, S., Diamant, A., Körting, W., Krüner, G., Paperna, I., Westernhagen, H.v., The use of fish metabolic, pathological and parasitological indices in pollution monitoring. I. North Sea. Helgol. Mar. Res. 53, Bush, A.O., Holmes, J.C., Intestinal helminths of lesser scaup ducks: patterns of association. Can. J. Zool. 64, Bush, A.O., Lafferty, K.D., Lotz, J.M., Shostak, A.W., Parasitology meets ecology on its own terms: Margolis et al. revisited. J. Parasitol. 83, Campbell, R.A., Haedrich, R.L., Munroe, T.A., Parasitism and ecological relationships among deep-sea benthic fishes. Mar. Biol. 57, Christin, M.S., Gendron, A.D., Brousseau, P., Ménard, L., Marcogliese, D.J., Cyr, D., Ruby, S., Fournier, M., Effects of agricultural pesticides on the immune system of Rana pipiens and on its resistance to parasitic infection. Environ. Toxicol. Chem. 22, Cone, D.K., Marcogliese, D.J., Watt, W.D., Metazoan parasite communities of yellow eels (Anguilla rostrata) in acidic and limed rivers of Nova Scotia. Can. J. Zool. 71, Costanza, R., 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 Coyner, D.F., Spalding, M.G., Forrester, D.J., Epizootiology of Eustrongylides ignotus in Florida: distribution, density, and natural infections in intermediate hosts. J. Wildl. Dis. 38, Coyner, D.F., Spalding, M.G., Forrester, D.J., Influence of treated sewage on infections of Eustrongylides ignotus (Nematoda: Dioctophymatoidea) in eastern mosquitofish (Gambusia holbrooki) in an urban watershed. Comp. Parasitol. 70, Diamant, A., Banet, A., Paperna, I., Westernhagen, H.v., Broeg, K., Kruener, G., Koerting, W., Zander, S., The use of fish metabolic, pathological and parasitological indices in pollution monitoring. II. The Red Sea and Mediterranean. Helgol. Mar. Res. 53, Dobson, A., Hudson, P.J., Parasites, disease and the structure of ecological communities. Trends Ecol. Evol. 1, Dubois, N., Marcogliese, D.J., Magnan, P., Effect of the introduction of white sucker, Catostomus commersoni, on the parasite fauna of brook trout, Salvelinus fontinalis. Can. J. Zool. 74, Esch, G.W., Impact of ecological succession on the parasite fauna in centrarchids from oligotrophic and eutrophic ecosystems. Am. Midl. Nat. 86, Esch, G.W., Fernandez, J.C., A Functional Biology of Parasitism. Chapman and Hall, London. Esch, G.W., Hazen, T.C., Marcogliese, D.J., Goater, T.M., Crews, A.E., A long-term study on the population biology of Crepidostomum cooperi (Trematoda: Allocreadidae) in the burrowing mayfly, Hexagenia limbata (Ephemeroptera). Am. Midl. Nat. 116, Esch, G.W., Kennedy, C.R., Bush, A.O., Aho, J.M., Patterns in helminth colonization in freshwater fish in Great Britain: alternative strategies for colonization. Parasitology 96, Gayraud, S., Statzner, B., Bady, P., Haybachp, A., Schöll, F., Usseglio- Polatera, P., Bacchi, M., Invertebrate traits for the biomonitoring of large European rivers: an initial assessment of alternative metrics. Freshw. Biol. 48, Gendron, A.D., Marcogliese, D.J., Barbeau, S., Christin, M.-S., Brousseau, P., Ruby, S., Cyr, D., Fournier, M., Exposure of leopard frogs to a pesticide mixture affects life history characteristics of the lungworm Rhabdias ranae. Oecologia 135, George-Nascimento, M.A., 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, Halmetoja, A., Valtonen, E.T., Koskenniemi, E., Perch (Perca fluviatilis L.) parasites reflect ecosystem conditions: a comparison of a natural lake and two acidic reservoirs in Finland. Int. J. Parasitol. 30, Huspeni, T.C., Lafferty, K.D., Using larval trematodes that parasitze snails to evaluate a saltmarsh restoration project. Ecol. Appl. 14,
11 D.J. Marcogliese / International Journal for Parasitology 35 (2005) Huxham, M., Raffaelli, D., Pike, A., Parasites and food web patterns. J. Anim. Ecol. 64, Jacobson, K.C., Arkoosh, M.R., Kagley, A.N., Clemons, E.R., Collier, T.K., Casillas, E., Cumulative effects of natural and anthropogenic stress on immune function and disease resistance in juvenile Chinook salmon. J. Aquat. Anim. Health 15, Johnson, P.T., Chase, J.M., Parasites in the food web: linking amphibian malformations and aquatic eutrophication. Ecol. Lett. 7, Johnson, P.T.K., Sutherland, D.R., Amphibian deformities and Ribeiroia infection: an emerging helminthiasis. Trends Parasitol. 19, Karr, J.T., Defining and measuring river health. Freshw. Biol. 41, Kennedy, C.R., Freshwater fish parasites and environmental quality: an overview and caution. Parassitologia 39, Kennedy, C.R., Nie, P., Kaspers, J., Paulisse, J., Are eels (Anguilla anguilla L.) planktonic feeders? Evidence from parasite communities. J. Fish Biol. 41, Khan, R.A., Payne, J.F., A multidisciplinary approach using several biomarkers, including a parasite, as indicators of pollution: a case history from a paper mill in Newfoundland. Parassitologia 39, Khan, R.A., Thulin, J., Influence of pollution on parasites of aquatic animals. Adv. Parasitol. 30, Kiesecker, J., Synergism between trematode infection and pesticide exposure: a link to amphibian limb deformities in nature? Proc. Nat. Acad. Sci. 99, Knudsen, R., Curtis, M.A., Kristoffersen, R., Aggregation of helminths: the role of feeding behavior of fish hosts. J. Parasitol. 90, 1 7. Koskivaara, M., Environmental factors affecting monogeneans parasitic on freshwater fish. Parasitol. Today 8, Lafferty, K.D., Environmental parasitology: What can parasites tell us about human impacts on the environment?. Parasitol. Today 13, Lafferty, K.D., Is disease increasing or decreasing, and does it impact or maintain biodiversity?. J. Parasitol. 89, S101 S105. Landsberg, J.H., Blakesley, B.A., Reese, R.O., McRae, G., Forstchen, P.R., Parasites of fish as indicators of environmental stress. Environ. Monitor. Assess. 51, MacKenzie, K., Parasites as pollution indicators in marine ecosystems: a proposed early warning system. Mar. Pol. Bull. 38, MacKenzie, K., Abaunza, P., Parasites as biological tags for stock discrimination of marine fish: a guide to procedures and methods. Fish. Res. 38, Mackenzie, K., Williams, H.H., Williams, B., McVicar, A.H., Siddall, R., Parasites as indicators of water quality and the potential use of helminth transmission in marine pollution studies. Adv. Parasitol. 35, Marcogliese, D.J., The role of zooplankton in the transmission of helminth parasites to fish. Rev. Fish Biol. Fish. 5, Marcogliese, D.J., Implications of climate change for parasitism of animals in the aquatic environment. Can. J. Zool. 79, Marcogliese, D.J., Food webs and the transmission of parasites to marine fish. Parasitology 124, S83 S99. Marcogliese, D.J., Food webs and biodiversity: are parasites the missing link? J. Parasitol. 89, S106 S113. Marcogliese, D.J., Parasites: small players with crucial roles in the ecological theatre. EcoHealth 1, Marcogliese, D.J., Cone, D.K., On the distribution and abundance of eel parasites in Nova Scotia: influence of ph. J. Parasitol. 82, Marcogliese, D.J., Cone, D.K., 1997a. Food webs: a plea for parasites. Trends Ecol. Evol. 12, Marcogliese, D.J., Cone, D.K., 1997b. Parasite communities as indicators of ecosystem stress. Parassitologia 39, Marcogliese, D.J., Cone, D.K., Myxozoan communities parasitizing Notropis hudsonius (Cyprinidae) at selected localities on the St. Lawrence River, Quebec: possible effects of urban effluents. J. Parasitol. 87, Marcogliese, D.J., Scholz, T., Recent visitations by eels to Sable Island, Canada, confirmed by parasites. J. Fish Biol. 54, Marcogliese, D.J., Goater, T.M., Esch, G.W., Crepidostomum cooperi (Allocreadidae) in the burrowing mayfly, Hexagenia limbata (Ephemeroptera) related to trophic status of a lake. Am. Midl. Nat. 124, Marcogliese, D.J., Brambilla, L.G., Gagné, F., Gendron, A.D., Joint effects of parasitism and pollution on biomarkers of oxidative stress in yellow perch (Perca flavescens). Dis. Aquat. Org. 63, May, R.M., Anderson, R.M., Population biology of infectious diseases: part II. Nature 280, McCallum, H., Dobson, A., Detecting disease and parasite threats to endangered species and ecosystems. Trends Ecol. Evol. 10, Meyer, J.L., Stream health: incorporating the human dimension to advance stream ecology. J. N. Am. Benthol. Soc. 16, Minchella, D.J., Scott, M.E., Parasitism: a cryptic determinant of animal community structure. Trends Ecol. Evol. 6, Morley, N.J., Irwin, S.W.B., Lewis, J.W., Pollution toxicity to the transmission of larval digeneans through their molluscan hosts. Parasitology 126, S5 S26. Ouellet, M., Bonin, J., Rodrigue, J., DesGranges, J.-L., Lair, S., Hindlimb deformities (ectromelia, ectrodactyly) in free-living anurans from agricultural habitats. J. Wildl. Dis. 33, Overstreet, R.M., 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 Overstreet, R.M., Parasitological data as monitors of environmental health. Parassitologia 39, Pascual, S., Gonzales, A., Arias, C., Guerra, A., Biotic relationships of Illex condetii and Todaropsis eblanae (Cephalopoda, Ommastrephidae) in the Northeast Atlantic: evidence from parasites. Sarsia 81, Pietrock, M., Marcogliese, D.J., Free-living endohelminth stages: at the mercy of environmental conditions. Trends Parasitol. 19, Poulin, R., Toxic pollution and parasitism in freshwater fish. Parasitol. Today 8, Price, P.W., Evolutionary Biology of Parasites. Princeton University Press, Princeton. Schmidt, V., Zander, S., Körting, W., Steinhagen, D., Parasites of the flounder Platichthys flesus (L.) from the German Bight North Sea, and their potential use in ecosystem monitoring. Helgol. Mar. Res. 57, 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, Skouras, A., Schmidt, V., Körting, 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, Somerfield, P.J., Clarke, K.R., Taxonomic levels, in marine community studies, revisted. Mar. Ecol. Prog. Ser. 127, Spalding, M.G., Bancroft, G.T., Forrester, D.J., The epizootiology of eustrongylidosis in wading birds (Ciconiiformes) in Florida. J. Wildl. Dis. 29, Steedman, R.J., Ecosystem health as a management goal. J.N. Am. Benthol. Soc. 13, Sures, B., The use of fish parasites as bioindicators of heavy metals in aquatic ecosystems: a review. Aquat. Ecol. 35, Sures, B., Accumulation of heavy metals by intestinal helminths in fish: an overview and perspective. Parasitology 126, S53 S60.
12 716 D.J. Marcogliese / International Journal for Parasitology 35 (2005) Sures, B., Environmental parasitology: relevancy of parasites in monitoring environmental pollution. Trends Parasitol. 20, Sures, B., Siddall, R., Taraschewski, H., Parasites as accumulation indicators of heavy metal pollution. Parasitol. Today 15, Suter II., G.W., A critique of ecosystem health concepts and indexes. Environ. Toxicol. Chem. 12, Valtonen, E.T., Holmes, J.C., Aronen, J., Rautalahti, I., Parasite communities as indicators of recovery from pollution: parasites of roach (Rutilus rutilus) amd perch (Perca fluviatilis) in central Finland. Parasitology 126, S43 S52. Vidal-Martínez, V.M., Aguirre-Mecedo, M.L., Noreña-Barroso, E., Gold- Bouchot, G., Caballaro-Pinzón, P.I., Potential interactions between metazoan parasites of the Mayan catfish Ariopsis assimilis and chemical pollution in Chetumal Bay, Mexico. J. Helminthol. 77, Waite, I.R., Herlihy, A.T., Larsen, D.P., Urquhart, N.S., Klemm, D.J., The effects of macroinvertebrate taxonomic resolution in large landscape bioassessments: an example from the Mid-Atlantic Highlands, USA. Freshw. Biol. 49, Warwick, R.M., Analysis of community attributes of the macrobenthos of Frierfjord/Langesundfjord at taxonomic levels higher than species. Mar. Ecol. Prog. Ser. 46, Williams, H.H., MacKenzie, K., Marine parasites as pollution indicators: an update. Parasitology 126, S27 S41. Williams, H.H., MacKenzie, K., McCarthy, A.M., Parasites as biological indicators of the population biology, migrations, diet, and phylogenetics of fish. Rev. Fish Biol. Fish. 2, Wiśniewski, W.L., Characterization of the parasitofauna of an eutrophic lake. Acta Parasitol. Pol. 6, Yeomans, W.E., Chubb, J.C., Sweeting, R.A., Use of protozoan communities for pollution monitoring. Parassitologia 39, Zander, C.D., Ecology of host parasite relationships in the Baltic Sea. Naturwissens. 85, Zander, C.D., The guild as a concept and a means in ecological parasitology. Parasitol. Res. 87, Zander, C.D., Reimer, L.W., Parasitism at the ecosystem level in the Baltic Sea. Parasitology 124, S119 S135. Zander, C.D., Strohbach, U., Groenewold, S., The importance of gobies (Gobiidae, Teleostei) as hosts and transmitters of parasites in the SW Baltic. Helgoländer Meeresunters. 47,