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The Role of Zooplankton in the Transmission of Helminth Parasites to Fish

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The Role of Zooplankton in the Transmission of Helminth Parasites to Fish Reviews in Fish Biology and Fisheries, 5,336-371 (1995) The role of zooplankton in the transmission of helminth parasites to fish DAVID J. MARCOGLIESE Department of Fisheries and Oceans, Maurice Lamontagne Institute, PO Box 1000, Mont-Joli, Quebec, Canada G5H 3Z4 Contents Introduction page 336 Parasite life history patterns 337 Terminology Trematodes Cestodes Nematodes Acanthocephalans The marine environment 339 Trematodes of marine fish Cestodes of marine fish Nematodes of marine fish Acanthocephalans of marine fish The freshwater environment 348 Trematodes of freshwater fish Cestodes of freshwater fish Nematodes of freshwater fish Acanthoeephalans of freshwater fish Ecology of transmission 356 Rates of natural infections Dynamics of transmission Ecosystem effects Summary and conclusions 362 Marine-freshwater comparisons The future Acknowledgements 364 References 364 Introduction Parasites are an important, but often neglected, component of any ecosystem. By their very nature, they siphon off energy at virtually every trophic level within a food web. Their effects on hosts are diverse. In fish alone, they are known to affect behaviour, lower body condition, reduce fecundity and even cause mortality. Indeed, mathemat- ical models suggest that parasite populations regulate populations of their hosts. Thus, 0960-3166 © 1995 Chapman & Hall Zooplankton and transmission of helminth parasites 337 given the potential of parasites significantly to affect fish host populations, fish biologists should know how parasites are transmitted to their fish hosts. This paper is not an exhaustive review of all records of zooplankton as intermediate hosts for fish parasites. Rather, the various patterns of life cycles of parasites utilizing zooplankton and fish are summarized. It will become evident that these life cycles are wonderfully diverse and complex. Examples will be provided for numerous parasites within each of the various helminth groups, and prevalent trends within these groups highlighted for both marine and freshwater systems. There are fundamental differences between the two environments; this disparity is in part a reflection of the differences in zooplankton diversity and species composition. Lastly, the ecological aspects of para- site transmission from zooplankton to fish are discussed. Parasite life history patterns Many parasites, especially metazoan worms, or helminths, possess complex life cycles. Complex life cycles normally involve ontogenetic changes that result in metamorphoses and habitat and niche shifts, or, in the case of nematodes, moults. The parasitic helminths display complexity to an extreme. Metamorphoses and moults can occur several times within a single life cycle that can include both free-living and parasitic stages, often with two or more parasitic phases infecting invertebrates and vertebrates. Those metazoan fish parasites that can infect zooplankton during their life cycles are limited to the helminths: trematodes, cestodes, nematodes and acanthocephalans. Thus, discussion of parasite life history patterns will be confined to those groups, though the reader should be aware that a variety of other lifestyles and transmission patterns exist among fish parasites. Parasites transmitted to fish via ingestion of, penetration and/or attachment by, free-living stages are not considered in this review, as it is intended to focus on the interaction between zooplankton and fishes in parasite transmission. Furthermore, life cycle diagrams are simplified to emphasize this zoo- plankton-fish interaction, and free-living stages of parasites are not depicted. TERMINOLOGY For all groups, the term definitive host refers to that host where parasite maturity and sexual reproduction occurs. An intermediate host is one that is required to complete the life cycle. Such requirement may be developmental; the host is necessary for parasite metamorphosis, or development to the subsequent stage, or both. Alternatively, the requirement may be ecological, in that the intermediate host is a necessary link in the transmission of the parasite to the next host. Paratenic hosts are optional hosts which may be involved in the life cycle, but are not required for its completion. Accidental hosts are those which may acquire infection, but are not involved in transmission and reproduction of the parasite. These hosts constitute dead ends for the parasite, yet infection may have grave consequences for such hosts. For almost all helminths, definitive hosts are vertebrates, while intermediate hosts may be invertebrates, or vertebrates, or both. TREMATODES Trematodes, or flukes, are flatworms of the phylum Platyhelminthes (Class Trematoda: subclass Digenea), and they possess very characteristic and complex life cycles. Adults 338 Marcogliese are found in vertebrates, and are usually site-specific within the host. They can be found associated with the alimentary tract, the hepatic system, the circulatory system, the respiratory system and the urinary system, among others. Larvae in molluscs (known as sporocysts and rediae) asexually produce infective stages (known as cer- cariae) that are released. Free-living cercariae either penetrate or are ingested by the next host. If a second intermediate host is involved, the trematode develops into a metacercaria, which may or may not encyst. The metacercaria is infective to the definitive host, which acquires the parasite by ingesting infected intermediate hosts. The metacercaria is the phase of the life cycle which occurs in zooplankton. However, it is crucial that readers be aware that when zooplankton participate in these life cycles, they are intermediary between the compulsory mollusc and the definitive host. CESTODES Cestodes, or tapeworms, are also flatworms (Class Cestoidea) that are typically intestinal parasites of vertebrates when adults. Depending on the type of cestode, variations occur in the larval and juvenile stages and the type of hosts used. Those which use zooplankton as intermediate hosts and infect fishes belong to the orders Trypanorhyncha, TetraphyUidea, Pseudophyllidea and Proteocephalidea. Life cycles within these groups are similar. Eggs passed into the water are ingested, or hatch into free-swimming coracidia, which are ingested by invertebrates, where they develop into larvae or procercoids. In some cases, the intermediate host is ingested by a second intermediate host, where the cestode develops further, often into a worm-like plerocer- coid that is infective to the definitive host. In others, the plerocercoid stage as well as the adult occur in the definitive host. The procercoid stage is typically associated with zooplankton. Fish may be intermediate hosts and carry plerocercoids, or definitive hosts and carry adult cestodes. NEMATODES Unlike trematodes and cestodes, nematodes, or roundworms (Phylum Nematoda), are not exclusively parasitic. Nematode life cycles do not involve the complex metamorph- oses observed in platyhelminthes; rather, they typically possess five developmental stages separated by moults. The fifth stage is the adult, and among parasites this is usually associated with vertebrates. Like trematodes, adult nematodes are site-specific and reproduction may occur in any one of a variety of organs. The eggs or larvae are passed externally and ingested by invertebrate intermediate hosts, where one or two moults may occur. Life cycles of nematodes may involve a number of intermediate and/or paratenic hosts that pass the roundworm to the definitive host when ingested. In most cases, the third larval stage is infective to the definitive host. Early larval stages infect zooplankton intermediate hosts, and fish may carry third- and fourth-stage larvae as intermediate and/or paratenic hosts, or adults as definitive hosts. ACANTHOCEPHALANS Adults of this group, also known as thorny-headed worms (Phylum Acanthocephala), like cestodes, are parasitic only in the intestine of vertebrates. Eggs must be eaten by an invertebrate host to hatch. An acanthor hatches, and develops through an acanthella stage into a cystacanth which is infective to the vertebrate definitive host. Alternatively, the cystacanth and its intermediate host may be ingested by a paratenic host. The Zooplankton and transmission of helminth parasites 339 definitive host acquires the parasite by feeding on infected intermediate and/or paratenic hosts. Among the Acanthocephala, there are no motile, free-living stages. Both zooplankton and fish may carry cystacanths as intermediate and paratenic hosts, respectively, and fish may serve as definitive hosts. The marine environment Zooplankton in the marine environment are characterized not only by a high diversity of species, but also a varied assortment of higher taxonomic groups. Usually calanoid copepods predominate, but other crustaceans include euphausiids, cyclopoid copepods and hyperiid amphipods. Soft-bodied zooplankters are also important, and most commonly represented by chaetognaths, coelenterates and ctenophores. The community structure of zooplankton within the marine environment has impor- tant implications for transmission of parasites up the food chain. Zooplankton commu- nities include a number of trophic levels. Many marine fish parasites using zooplankton as intermediate hosts are characterized by a low specificity for the planktonic host, and an ability to transfer hosts through predatory interactions within the zooplankton assemblage en route to the fish host. These life history traits permit parasites of pelagic fishes to maximize
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