the role of zooplankton in the transmission of …life cycles of derogenes varicus, the most common...

Reviews in Fish Biology and Fisheries, 5,336-371 (1995)

The role of zooplankton in the transmission of helminth parasites to fish

D A V I D J . M A R C O G L I E S E

Department of Fisheries and Oceans, Maurice Lamontagne Institute, PO Box 1000, Mont-Joli, Quebec, Canada G5H 3Z4

Introduction Parasite life history patterns

Terminology Trematodes Cestodes Nematodes Acanthocephalans

The marine environment Trematodes of marine fish Cestodes of marine fish Nematodes of marine fish Acanthocephalans of marine fish

The freshwater environment Trematodes of freshwater fish Cestodes of freshwater fish Nematodes of freshwater fish Acanthoeephalans of freshwater fish

Ecology of transmission Rates of natural infections Dynamics of transmission Ecosystem effects

Summary and conclusions Marine-freshwater comparisons The future

Acknowledgements References

Contents

page 336 337

339

348

356

362

364 364

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 parasite 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 zooplankton-fish interaction, and free-living stages of parasites are not depicted.

T E R M I N O L O G Y

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.

T R E M A T O D E S

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 cercariae) 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.

C E S T O D E S

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 plerocercoid 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.

N E M A T O D E S

Unlike trematodes and cestodes, nematodes, or roundworms (Phylum Nematoda), are not exclusively parasitic. Nematode life cycles do not involve the complex metamorphoses 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.

A C A N T H O C E P H A L A N S

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


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 important implications for transmission of parasites up the food chain. Zooplankton communities 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 their chances of being ingested by a suitable fish host, and at the same time maximize the duration of the infective pool of parasites within the zooplankton.

T R E M A T O D E S O F M A R I N E F I S H

Metacercariae of three principal groups of trematodes infecting fish have been found in zooplankton. These include representatives of the Hemiuroidea, Lepocreadioidea and Didymozooidae. Species belonging to all three taxa infect a variety of zooplankters.

The hemiuroids include members of the Hemiuridae, Derogenidae and Lecisthaster- idae, among others, adults of which are usually found in the stomachs of marine teleosts. Dollfus (1923b) reviewed records of trematode infections in zooplankton from the 19th and early part of the 20th centuries. Hemiuroids infect calanoid copepods, chaetognaths, coelenterates, ctenophores and polychaetes (Table 1). Many data on infection of trematodes in chaetongnaths, coelenterates and ctenophores are also summarized in reviews by Dollfus (1960, 1963). Chaetognaths probably acquire trematode metacercariae by consuming infected copepods (Dollfus, 1960). Representative life cycles of Derogenes varicus, the most common trematode of marine fishes, with a cosmopolitan distribution in cold waters and over 100 known hosts, and Hemiurus luehei, parasitic in clupeids and salmonids, are depicted in Figs 1 and 2.

Adult hemiuroids of the Family Accacoeliidae infect the intestine or occasionally the gills of marine teleosts, especially sunfish. They have been reported from chaetognaths (Table 1). Euphausiids are reported as hosts for other hemiuroids, such as syncoelids, which inhabit the mouth or branchial cavity of fish.

Adult lepocreadioids typically inhabit the intestine or pyloric caeca of teleosts. Coelenterates and ctenophores are well-documented hosts, with occasional records of metacercariae in euphausiids and chaetognaths (Table 1). The cercariae of Opechona baciUaris, a common parasite of Atlantic mackerel (Scomber scombrus, Scombridae), penetrate the macrozooplankters directly (Fig. 3) and do not rely on ingestion of copepods for transfer (K~aie, 1975).

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Fig. 1. Life cycle of Derogenes varicus. (A) Eggs are ingested by the first intermediate host, Natica spp. (B) Free-living cercariae are ingested by calanoid copepods. (C) The infected copepod is ingested by a fish definitive host. (D) Alternatively, the copepod is ingested by a chaetognath, Sagitta spp., which is then consumed by a fish. (E and F) The parasite may be transmitted between fish through predatory interactions. Only the pelagic component of the life cycle is shown. This parasite may also be transmitted from the snail to benthic invertebrates and demersal fish. For all figures, broken lines indicate transmission via a free-living stage, which is either passively ingested or actively penetrates the host. Solid lines indicate that transmission occurs through predatory interactions. (Modified after K0ie, 1979.)

Didymozooids, whose adults are found in the muscles, skin, or lining of the pharynx, lining of the eoelom, or other visceral organs of fish, are commonly reported from chaetognaths, but also infect copepods, coelenterates, ctenophores and polychaetes (Table 1). Fellodistomids and allocreadids, intestinal parasites of fishes, have been found in chaetognaths, ctenophores and euphausiids (Table 1).

In general, natural rates of infection are very low, and larval trematodes are difficult to identify, thus hindering clarification of life cycles. To demonstrate definitively a parasite's life cycle, transmission must be observed directly, a difficult task in the field, and sometimes just as difficult in the laboratory, where a number of hosts (e.g. snails, crustaceans, fish) must be maintained in captivity. K¢ie (1975, 1979, 1989, 1990, 1991, 1992), in a series of laboratory studies, successfully determined the life cycles of a number of marine trematodes.

CESTODES OF MARINE FISH

Generally, larvae of cestodes belonging to the Trypanorhyncha and Tetraphyllidea are commonly found in zooplankton in the marine environment. These larvae are in various stages of development, and are often impossible to identify to species or even


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Fig. 2. Life cycle of Hemiurus luehei. (A) Eggs are ingested by the first intermediate host, the opisthobranch Philine denticulata. (B) Free-living cereariae are released and ingested by calanoid copepods. (C) The infected copepod is ingested by the definitive host fish, a clupeid or salmonid. (D) Alternatively, the infected copepod is ingested by a chaetognath, which is then eaten by the fish. (E) The parasite may be transmitted between fish through predation. (Modified after Koie, 1990.)

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Fig. 3. Life cycle of Opechona bacillarb. (A) Eggs are ingested by the first intermediate host, the prosohranch Nassarius pygmaeus. (B) Free-living cercariae penetrate the next intermodiate host, ctenophores, coelenterates, chaetognaths or polychaetes. (C) The infected second intermediate host is ingested by the mackerel definitive host. (Modified after K¢ie, I975.)

346 Marcogliese

genus. Adults are generally restricted to elasmobranchs. Procercoids and plerocercoids of pseudophyllideans also occur, but documentation is rare.

Experimental evidence suggests that calanoid and harpacticoid copepods, but not other invertebrates, can be infected directly with trypanorhynch coracidia (Ruszkowski, 1934; Riser, 1956; Mudry and Dailey, 1971). Larvae have also been found in euphausiids (Table 1).

Two possible life cycles are proposed for trypanorhynchs (Mudry and Dailey, 1971). In the first, a procercoid develops in a copepod. This is infective to a teleost intermediate host, where a plerocercoid infective to the elasmobranch definitive host develops. In the second, a plerocercus directly infective to the elasmobranch develops in the copepod. The second lifestyle occurs in cestodes of non-piscivorous elasmobranchs. The only experimental demonstration of a complete trypanorhynch life cycle was by Sakanari and Moser (1989), who infected harpacticoid copepods and mosquitofish (Gambusia affinis, Poeciliidae) with Lacistorhynchus dollfusi, a parasite of the leopard shark (Triakis semifasciata, Carcharhinidae) (Fig. 4). Plerocercoids of Lacisto- rhynchus spp. occur in over 40 teleosts in the Atlantic and Pacific Oceans.

Early records of larval cestode infections in zooplankton are reviewed in Dollfus (1923a,c, 1931, 1964, 1974, 1976). Indistinguishable larvae of tetraphyllideans, whether in fish or invertebrates, are generally referred to as Scolex polymorphus or Scolex pleuronectis. Larval tetraphyllideans occur in at least 11 chaetognaths from both the Pacific and Atlantic Oceans (Table 1). Only copepods have been infected experimentally (Riser, 1956; Boyce, 1969; Mudry and Dailey, 1971).

Pseudophyllidean life cycles are poorly understood in the marine environment. Species of Bothriocephalus, including the common tapeworm B. scorpii, are infective to calanoid copepods, though the copepods may display differential susceptibilities (St. Markowski, 1935; Robert and Gabrion, 1991).

NEMATODES OF MARINE FISH

Almost all records of nematodes in marine zooplankton are those of ascaridoids, which as adults are digestive tract parasites of fish, marine mammals or piscivorous birds. In

Fig. 4. Life cycle of Lacistorhynchus dollfusi. (A) Eggs hatch and free-swimming coracidia are ingested by harpacticoid copepods. (B) The infected copepod is ingested by a teleost. (C) The teleost is eaten by an elasmobranch. (Modified after Sakanari and Moser, 1989.)


all cases infective third-stage larvae may occur in the viscera or flesh of fish. Several of these nematodes are commercially or medically very important. The whaleworm, Anisakis simplex, matures in the stomachs of whales, and its infective larvae can be found in the viscera and occasionally the flesh of over 70 species of fish in the North Atlantic. This species is highly pathogenic to man and is a problem wherever raw, marinated or undercooked fish are consumed. Euphausiids are considered the most important intermediate host of whaleworm (Oshima et al., 1969). They may transmit Anisakis directly to baleen whales which feed on them extensively. However, fish are probably most important in transmitting the nematode to toothed whales (Fig. 5) (Smith, 1983b).

The most numerous records of nematodes in marine zooplankton are those of Hysterothylacium spp. and/or Contracaecum spp.. Nematodes of the genus Contra- caecum mature in birds or seals, while those of Hysterothylacium mature in fish. Larvae of both genera can be found in the viscera of fish. However, the two taxa are morphologically very similar and many older records of Contracaecum are actually those of Hysterothylacium. A wide variety of zooplankton may serve as intermediate hosts of Hysterothylacium aduncum (Table 1), one of the most common nematodes of marine fishes (Fig. 6). Other nematodes occur in euphausiids and chaetognaths (Table 1).

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Fig. 5. Life cycle of Anisakis simplex. (A) Hatched larvae are eaten by euphausiids. (B) The infected euphausiid is ingested by a baleen whale. (C) Alternatively, the euphausiid is eaten by a fish. (D) The fish is preyed upon by a toothed whale, or by (E) a piseivorous fish, which in turn is consumed (F) by the toothed whale. (Modified after Smith, 1983b.)

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Fig. 6. Life cycle of Hysterothylacium aduncum. Eggs are ingested by (A) calanoid copepods, or (B) other crustaceans. (C) The infected copepod, or (D) other crustacean, may be consumed by the definitive host. Or, (E) the copepod may be ingested by non-crustacean invertebrates. (F) The copepod, (G) other crustacean, or (H) other invertebrate may be eaten by a fish intermediate or paratenic host. (I) The infected fish may be prayed upon by the definitive host, or by (J) another paratenic host which is in turn eaten by the definitive host. Only the pelagic component of the life cycle is shown. This parasite may also be transmitted to benthic invertebrates and demersal fish. (Modified after K¢ie, 1993.)

ACANTHOCEPHALANS OF MARINE FISH

Most acanthocephalans use amphipods or ostracods as intermediate hosts. Thus, their life cycles usually have a benthic component, and reports of larval acanthocephalans in zooplankton are rare. Among zooplankton, they have only been found in euphausiids (Table 1).

The freshwater environment

Freshwater zooplankton communities differ fundamentally from their marine counter- parts in both structure and composition. Large zooplankters that feed extensively on the smaller forms occur only to a limited extent in freshwater systems. The reduction in trophic levels within the zooplankton has important consequences for the cycling of parasites within the food web. Lakes are dominated by copepods and cladocerans. Among copepods, both cyclopoids and calanoids occur in abundance. Cladocerans rarely act as intermediate hosts for helminth parasites. However, the preponderance of


predaceous and omnivorous cyclopoid copepods in freshwater compared with marine systems greatly affects the capacity for transmission as well as the evolution of parasite life cycles.

TREMATODES OF FRESHWATER FISH

The most common trematodes of marine fish and zooplankton, the hemiuroids, lepocreadioids and didymozooids, are far less abundant in freshwater systems. Many of the most abundant trematodes in freshwater fish possess cercariae which directly penetrate the fish host, or use larval insects as intermediate hosts. Thus, while zooplankters are important in transmitting trematodes to fish in marine systems, their role in the life cycles of freshwater parasites is much reduced, and few life cycles involving zooplankton are known. Cyclopoid copepods and cladocerans act as intermediate hosts for allocreadids (Table 2).

CESTODES OF FRESHWATER FISH

Life cycles of cestodes of freshwater fish are well studied, because a large number of the cestodes are economically or medically important. Bothriocephalus acheilognathi, Schistocephalus spp. and Ligula spp. can all cause mortality and/or serious pathology in fish populations. Triaenophorus spp. larvae infect the flesh of commercial and sport fish, causing economic losses. Some species of Diphyllobothrium can infect man.

A fundamental cause of differences between cestodes in marine and freshwater environments is the rarity of elasmobranchs in the latter. Thus, trypanorhynchs and tetraphyllideans are uncommon in fresh waters. The most common cestodes of freshwater fish include those of the Order Pseudophyllidea. These tapeworms use copepods as intermediate hosts and fish, birds or mammals as definitive hosts. A fish intermediate host may also be involved in the life cycle, especially if a bird or mammal is the final host. Another very important group, the Proteocephalidea, infects copepods and fish, and may include piscine intermediate and paratenic hosts.

The simplest pseudophyUidean life cycle, exhibited by Eubothrium and Bothrio- cephalus spp., consists of two hosts, a copepod and a fish definitive host (Fig. 7). Members of the circumboreal genus Triaenophorus possess a copepod first intermediate host, a piscine second intermediate host, and a piscine definitive host (Fig. 8). Members of the Ligulidae are parasitic in piscivorous birds as adults, and infect fish as plerocercoids. Ligula intestinalis uses a cyprinid as a second intermediate host, and the two species of Schistocephalus use sticklebacks (Fig. 9). Parasites of this group increase the susceptibility of the fish host to predation. Adults of the Diphyllobothriidae infect either birds or mammals, including man. Plerocercoid larvae may occur in the viscera or muscles of various fish (Fig. 10).

All these pseudophyllideans use cyclopoid copepods as intermediate hosts (Table 2). Certain calanoids may also serve as hosts for Triaenophorus, Ligula, Schistocephalus, and especially Diphyllobothrium spp. (Table 2). Susceptibility of copepods may vary with species and age (Michajlow, 1932; Watson and Price, 1960; Halvorsen, 1966; Kuperman, 1981; Dupont and Gabrion, 1987; Nie and Kennedy, 1993). However, within each parasite genus, the same species tend to be susceptible to the same extent (Watson and Price, 1960; Halvorsen, 1966; Kuperman, 1981). This relationship holds to a certain degree across cestode families, and those copepods which are good hosts are typically planktonic (Dubinina, 1980). Infections appear to depend on physiological

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Fig. 8. Life cycle of Triaenophorus crassus. (A) Hatched free-swimming coracidia are eaten by cyclopoid copepods (e.g. Diacyclops thomasi). (B) Infected copepods are ingested by whitefish (Coregonus spp.). (C) The infected whitefish is eaten by the definitive host pike. (Modified after Kuperman, 1981.)

compatibility, ecological conditions, and the geographic origin of host and parasite (Guttowa, 1961; Kuperman, 1981).

Another very common group of cestodes parasitic in freshwater fish is the Proteo- cephalidea. Their life cycles normally consist of a copepod intermediate host (Table 2) and a fish definitive host. Intermediate and paratenic fish hosts also may be involved (Fig. 11). As with pseudophyllideans, certain cyclopoids tend to be more susceptible than others (Wagner, 1954; Jarecka and Doby, 1965; Doby and Jarecka, 1966).

354 Marcogliese

Fig. 9. Life cycle of Schistocephalus solidus. (A) Hatched free-swimming coracidia are eaten by cyclopoid copepods. (B) Infected copepods are preyed upon by threespine sticklebacks. (C) Infected sticklebacks are ingested by piscivorous birds, such as gulls. (Modified after Dubinina, 1980.)

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Fig. 10. Life cycle of Diphyllobothrium latum. (A) Hatched free-swimming coracidia are ingested by calanoid copepods. (B) Infected copepods are consumed by fish such as pike or perch. (C) Infected fish are eaten by carnivores, such as bears, foxes or man. (Modified after Olsen, 1974.)


Fig. 11. Life cycle of Proteocephalus ambloplitis. (A) Hatched free-swimming coraeidia are eaten by cyclopoid copepods. (B) Infected copepods are ingested by a fish intermediate host, a bass. (C) The infected fish is preyed upon by the definitive bass host. (D) Alternatively, the intermediate fish host is consumed by a paratenic fish host, which is then eaten by the definitive host. (Modified after Olsen, 1974.)

NEMATODES OF FRESHWATER FISH

In lakes and rivers, nematodes may have fish, bird or mammal definitive hosts. Life cycles can be very flexible, and can involve numerous paratenic hosts. When fish are not the final host, they usually act as paratenic rather than intermediate hosts.

AnguiUicollid, philometrid and camallanid nematodes are members of the Order Spirurida which mature in fish. Anguillicola crassus resides in the swim bladder, and can cause mortality in European eel Anguilla anguilla (Anguillidae). Members of the genera Philonema, Philometra and Philometroides are found in the cheek pouches, fins, gill arteries, swim bladder, kidney, body cavity and under the skin of various fishes (Fig. 12). Camallanids inhabit the digestive tract. Copepods act as intermediate hosts for all these nematodes (Table 2). Specificity for the copepod host appears low (Table 2), though it may depend on host age (Ko and Adams, 1969; Moravec, 1969).

Anisakid nematodes also infect freshwater fish. Members of the genus Contracaecum use copepods and fish as paratenic or intermediate hosts, en route to infecting their avian definitive hosts (Table 2).

ACANTHOCEPHALANS OF FRESHWATER FISH

Most acanthocephalans in the aquatic environment infect amphJpods or ostracods as intermediate hosts. Life cycles involving zooplankton are rare (Table 2). However, those acanthocephalans belonging to more primitive classes, such as the Eoaeantho- cephala, infect copepods (de Buron and Golvan, 1986).

356 Marcogliese

/

J

Fig. 12. Life cycle of Philometroides nodulosa. (A) Free-living larvae are eaten by cyclopoid copepods. (B) The infected copepod is ingested by the definitive host, the white sucker. (Modified after Anderson, 1992.)

Ecology of transmission

RATES OF NATURAL INFECTIONS

Generally, rates of infections of both marine and freshwater zooplankters with helminths are extremely low. Copepods, which are important intermediate hosts for many parasites in both environments, tend to be infected at rates between 0.01% and 1.0%, though much lower rates have been observed (Table 3). Similar ranges of infection were observed for parasites in chaetognaths, though examples of much higher rates exist (Table 3). In contrast, euphausiids are often infected at even lower rates still, whereas coelenterates and ctenophores are more heavily infected (Table 3). Individual coelenterates and ctenophores may carry relatively heavy infections (Yip, 1984; Girola et aL, 1992). Densities of infected zooplankton are rarely calculated, but appear much greater for fresh waters than for marine systems (Table 4).

DYNAMICS OF TRANSMISSION

Very little is known about the dynamics of transmission of parasites to fish hosts via zooplankton. Estimates of transmission efficiency are rare. Hanzelov~ et al. (1989) estimated 67% of proceroids of Proteocephalus neglectus are transmitted to fish. In contrast, only 3-4% of procercoids of Bothriocephalus rarus in Macrocyclops ater are transmitted to red-spotted newts (Jarroll, 1980).

Spatial and temporal variation of infections in both freshwater and marine fish are well documented, but are poorly understood in zooplankton intermediate hosts. The extremely low rates of infection of helminths in zooplankton (Table 3) together with the high prevalences and abundances of the same helminths in fish hosts creates an interesting paradox. Fish may simply consume such immense quantities of zooplankton that they accumulate lots of parasites. Alternatively, seasonal and temporal variation in zooplankton parasitism may create loci of infections which enhance transmission, or parasites may alter the behaviour of the intermediate host such that it is rendered more susceptible to predation.


Spatial variations in infections of trematodes, cestodes and nematodes are apparent in zooplankton from the North-east Atlantic and the North Sea (van Banning, 1967; Reimer et al., 1971; Smith, 1983a). Euphausiids and chaetognaths display inshore-off- shore differences in infections of both trematodes and nematodes (Komaki, 1970; Smith, 1983a; Jarling and Kapp, 1985; Mazzoni, 1986). Variations with depth occur, with accacoelids infecting chaetognaths only in the upper 100 m (Elian, 1960; Jarling and Kapp, 1985), and Anisakis being most common in euphausiids between 100 and 200 m (Smith, 1983a). In a survey of 200000 invertebrates from the tropical Pacific Ocean, Slankis and Shevchenko (1974) note that helminths are most diverse and abundant in the upper 100 m. The same parasites occur to a lesser extent between 200 and 500 m, mainly in vertical migrants such as euphausiids. Parasites are much more limited in abyssal depths.

Seasonal variations in infections are known for marine trematodes and cestodes in chaetognaths and ctenophores (Fraser, 1970; Kulachkova, 1972; Weinstein, 1972; Pearre, 1976; Yip, 1984; Jarling and Kapp, 1985). No doubt seasonality of many parasites in zooplankton, especially those which reproduce in poikilotherms, is in part temperature dependent.

Cestodes of freshwater fishes fluctuate seasonally in their cyclopoid hosts (Sysoev, 1985; Hanzelov~ et al., 1989; Pronin, 1990). The highest rates of infection in Koljush- kovoe Lake, Russia, are in the pelagium (Sysoev, 1985); whereas infected crustaceans are distributed evenly in Dobsina Dam reservoir (Hanzelov~ et al., 1989). In contrast, many other parasites are most abundant in the littoral zone, often in synchrony with the presence of the definitive host. The temporal and spatial overlap of parasites, intermediate hosts, and definitive hosts often occurs in the spring, when pelagic fish move inshore to spawn. Waters warm up more rapidly in the littoral shallows, permitting acceleration of zooplankton reproduction, in addition to the embryonic development and hatching of parasite eggs (Dubinina, 1980). Many of the zooplankters which are the most suitable intermediate hosts for helminths are very common in shallow waters during the spring (Kuperman, 1981). A prime example of this synchrony is exhibited by Triaenophorus crassus and its hosts. Tapeworm eggs are released by spawning pike in shallow water. Concentrations of the first intermediate host, Cyclops strenuus, occur inshore at this time (Halvorsen, 1968). In North America, the copepod Diacyclops thomasi is most heavily infected within 6 m of shore (Watson and Lawler, 1965). Aggregation of infected copepods may enhance transmission to fish. Maximum densities of cyclopoid intermediate hosts often occur synchronously with eestode and nematode reproduction in fishes (Stromberg and Crites, 1975a; Riggs and Esch, 1987).

Because many zooplankters are only present seasonally, the ability to overwinter on the part of the parasite may be crucial for its transmission. D. thomasi infected with Philonema oncorhynchi survive 8 months at 4 °C; thus, the parasite can over~vinter in the first intermediate host and become available to the next generation of fry which pick it up in May (Ko and Adams, 1969). Similarly, the mackerel parasite Lecistho- cladium excisum may overwinter in its copepod host (KOie, 1991). It is conceivable that procercoids of Triaenophorus, Bothriocephalus and Proteocephalus may survive diapause in copepods (Watson and Lawler, 1965; Riggs and Esch, 1987; Morandi and Ponton, 1989). In northern latitudes, CV and adult D. thomasi disappear after July, and the CIV enters diapause to overwinter. In southern latitudes, D. thomasi under- goes diapause during the summer, and emerges in the fall, coinciding with an epizooitic

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of B. acheilognathi (Riggs and Esch, 1987). The reversal in population dynamics experienced by P. ambloplitis in bass from Canada and from the southern United States may be explained by the availability of infected D. thomasi, which emerge from diapause in the fall in the south and in the spring in the north (Riggs and Esch, 1987).

Parasites are known to alter the behaviour of their intermediate hosts in such a way that renders them more susceptible to predation (Holmes and Bethel, 1972; Moore, 1984). Modifications are most cormnonly noted for acanthocephalans in amphipods, ostracods and isopods. Such behavioural changes are proposed for infected chaetognaths and copepods (Boyce, 1974; Jarroll, 1980; Mazzoni, 1986). Altered respiration occurs in Eudiaptomus gracilis infected with Diphyllobothrium latum (Klekowski and Guttowa, 1968). Chaetognaths infected with hemiurids are closer to the surface, and tend to be larger and thus more conspicuous, than uninfected ones (Pearre, 1979). Triaenophorus-infected D. thomasi are more sluggish than uninfected individuals (Miller, 1943). Octospinieroides chandleri is an acanthocephalan found in the mosquitofish (Gambusia affinis, Poeciliidae), a surface feeder. Intermediate hosts are the ostracods Cypridopsis vidua and Physocypria pustulosa. The ostracods, normally photophobic, develop a positive response to light when infected and move up in the water column (DeMont and Corkum, 1982). Parasitized ostracods occur in 38.5% of surface samples, but only 1.3% of bottom samples (DeMont and Corkum, 1982). In an elegant study, Poulin et al. (1992) demonstrated that Cyclops vernalis swims more actively when infected with 2-3-week-old procercoids of Eubothrium salvelini, coinciding with infectivity to fish. Infected individuals were more likely to be captured by marauding brook charr (Salvelinus fontinalis, Salmonidae) than uninfected copepods. The authors hypothesize the altered behaviour may be the result of selection on the parasite to increase transmission.

ECOSYSTEM EFFECTS

Modifications of ecosystems, whether artificial or natural, can have drastic effects on the transmission of parasites to fish. Typically, after reservoir formation, rheophilic zooplankton species are replaced by limnophilic ones after 3-4 years. Parasites, particularly some of the cestodes and nematodes mentioned herein, experience a population decline followed by a rise, coinciding with the spread of limnophilic copepods (Izyumova, 1987).

Curtis (1988) reviewed the dynamics of Triaenophorus transmission to Coregonus in Swedish lakes and reservoirs. In natural lakes, Coregonus with the highest number of gill rakers tend to have more Triaenophorus, which is transmitted by cyclopoids. However, the correlation disappears in reserviors, due to the destruction of the littoral zone. The whitefish subsequently shift their diet and even those with fewer g~l rakers feed more on copepods and acquire parasites (Petersson, 1971). In some Swedish reservoirs, Mysis relicta was added to augment forage for fish. The mysids, however, compete with pelagic fish for preferred prey such as cladocerans. Thus, the whiteftsh again feed more on copepods and increase their infections of Triaenophorus and Diphyllobothrium. In Belews Lake, a cooling reservoir in North Carolina, transmission of the Asian fish tapeworm Bothriocephalus acheilognathi to mosquitofish was influ- enced by alterations in zooplankton community structure resulting from the introduction and proliferation of red shiners (Cyprinella lutrensis, Cyprinidae), a voracious planktivore (Marcogliese and Esch, 1989b). The smaller cyclopoid copepods became

362 Marcogliese

more abundant, and the larger ones less, due to size-selective predation by the shiners. The end result was a reduction in transmission of the tapeworm to fish, and a lower abundance of parasites. In addition, transmission was lower in unpolluted areas of the reservoir compared with selenium-polluted areas. The reduction is attributed to the restriction of host fish to the littoral zone by piscivores in the unpolluted area. The host fish were free to feed limnetically in the polluted areas, because the piscivores were eliminated through accumulation of selenium up the food chain. The copepod intermediate hosts are primarily limnetic, and transmission rates are higher therein (Riggs and Esch, 1987). Prevalence of Camallanus oxycephaIus increased between 1957 and 1972 in numerous fishes in Lake Erie. The increase is attributed to the rise in numbers of gizzard shad (Dorosema cepedianum, Clupeidae). The planktivorous shad concentrate high numbers of the nematode by feeding extensively on the zooplankton, and pass them on to the piscivorous fish which prey on them (Stromberg and Crites, 1975b).

Whole parasite assemblages can be affected by environmental changes. American eels (Anguilla rostrata, Anguillidae) from acidified streams possess fewer parasite species and fewer multiple infections than those from limed streams (Cone et al., 1993). Differences are attributed to differential susceptibility of the free-living stages or the intermediate hosts of the parasites to acidification. Thus, parasite communities may be useful environmental indicators, as the various species rely on different components of the food web for transmission.

Summary and conclusions

MARINE-FRESHWATER COMPARISONS

Patterns of transmission of helminths via zooplankton to fish differ substantially between marine and freshwater systems. Zooplankton act most frequently as intermediate hosts for digeneans, cestodes and nematodes in marine habitats, whereas digeneans infecting freshwater zooplankton are rare. In fresh waters, the most common helminths in zooplankton are larvae of pseudophyUidean and proteocephalid cestodes, the most important tapeworms of freshwater fish. In contrast, trypanorhynchs and tetraphyllideans, parasites of elasmobranchs, abound in salt water, and their larvae compose the most common cestodes. In fresh water, trematodes of fish rely mainly on active penetration. Such a mode of transmission would be inefficient in the open oceans, and is usually confined to inshore areas. Rather, the trematodes employ intermediate hosts, and possess the ability to be transmitted between invertebrates and between fish. Anisakid nematodes are very common in marine waters, especially due to the presence of whales and seals, which are rare in freshwater systems. These nematodes, too, may be transmitted from host to host along the food chain.

The diversity of helminths using zooplankton as intermediate hosts is higher in the oceans, primarily because of the large numbers of hemiuroid, lepocreadioid and didymozooid trematodes which are less frequent in fresh water. There is also a greater diversity of invertebrates to exploit as intermediate hosts, and consequently, a greater diversity of pathways to follow within a food web, leading to the definitive host. Thus, a diverse array of helminths infects a diverse array of zooplankters in marine waters. The helminths in marine systems also appear better adapted to transfer from host to host as they are passed along the food chain en route to the definitive host. Not only can they transfer from fish to fish, as in many freshwater parasites, they often can be

Zooplankton and transmission o f helminth parasites 363

passed from a zooplankter to its invertebrate predator, thus reflecting the more complex nature of marine food webs. In addition, there appears to be very little specificity for zooplankton intermediate hosts in the marine environment. This low specificity parallels that observed for helminths of marine fish (Polyanski, 1961; Holmes, 1990), which has been interpreted as spreading out the risk of failure to complete their life cycles (Bush, 1990). The capacity to undergo multiple transfers together with low specificity may be adaptations to maintain the availability of infective stages in the environment for prolonged periods, and to funnel the parasite towards the definitive host, increasing the probability of completing its life cycle. This funnelling may allow the parasite to compensate for the extremely low rates of infection of helminths in the smaller zooplankters that are observed in the extremely dilute marine habitat. In comparison, freshwater systems are characterized by simple food webs, lacking in abundant invertebrate predators. The pathways to reach the fish host are more direct. In addition, the closed nature of freshwater systems may help concentrate the parasites and create foci of infections, thus enhancing transmission. Specificity for zooplankton intermediate hosts tends to be much greater in fresh water, with parasites usually infective to a family of hosts, but rarely across orders or class, and certainly never across phyla.

In the oceans, calanoid copepods are among the most predominant of small zooplankton, and are known hosts primarily for trematodes (Slankis and Shevchenko, 1974), but also nematodes and cestodes (Zander et al., 1993). The role of large predaceous zooplankters such as chaetognaths, coelenterates and ctenophores is unclear, but they are generally infected with larval trematodes, such as the hemiurids, lepocreadids and accacoelids (Rebecq, 1965). Trypanorhynchs and nematodes usually infect euphausiids (Slankis and Shevchenko, 1974), but tetraphyllideans are often found in chaetognaths. All these zooplankters with the exception of calanoids are rare or non-existent in fresh water. In general, cyclopoid copepods are not involved to any great extent in the life cycles of helminths in the marine environment (Zander et al., 1993). Cyclopoid copepods assume a much more predominant role among freshwater zooplankton, as do cladocerans. The herbivorous cladocerans are almost never infected. However, the carnivorous nature of cyclopoids permits them to acquire larval helminths more so than the more herbivorous calanoids. The cyclopoid copepods tend to be the most important intermediate hosts among zooplankton for helminths of freshwater fish.

T H E F U T U R E

Much work remains to elucidate the basic life cycles of parasites, especially in the marine environment, where many are not fully understood. In addition, little is known of the capacity of larval helminths to be transferred from host to host. The relative roles of different intermediate hosts remain unclear, especially among marine species.

Rarely are populations of parasites studied among all hosts within a life cycle, certainly among those involving zooplankton, and never in the oceans. Indeed, much of the parasitology of the seas has not advanced beyond the survey stage. Innovative methods are required quickly to screen vast quantities of invertebrates for infection and reliably identify the larval parasites within. Application of immunological or molecular techniques such as ELISA or species-specific probes could very quickly yield a wealth of quantitative information.

364 Marcogliese

A paradox to be resolved is to determine how parasites accumulate in high numbers in fish hosts when the rates of infection in invertebrates are low. Virtually no studies exist describing modification of marine zooplankton behaviour by larval helminths, with very little on freshwater zooplankton, and most of that anecdotal. Moreover, there is a distinct lack of quantitative information on temporal and spatial variation in rates of infection, and few measurements of parasite transmission to fish. Predictive models of parasite-host population dynamics, to develop and test biological hypotheses, are limited to infections with bacteria, viruses and protozoa, or helminths with very simple but unrepresentative life cycles and lifestyles. Laboratory mesocosms appear to be a productive route for future investigations, to investigate experimentally altered behaviour, quantify dynamics of transmission, and finally provide some answers to 'the paradox of infected plankton'.

These questions are relevant to fisheries because parasites transmitted by zooplankton may severely affect the population dynamics of commercial fish species. Larval herring (Clupea harengus, Clupeidae) suffer mortalities due to infections of Hystero- thylacium sp. and Scolex pleuronectis (Rosenthal, 1967), and reduce feeding when infected with the latter (Heath and Nicoll, 1991). Mortalities have also been associated with infections of zooplankton-transmitted parasites among commercially important freshwater fishes (Liao and Shih, 1956; Kuperman, 1981). Thus, it is necessary to comprehend better the contribution of these infections to natural fish mortality among commercial species (Munro et al., 1983). Proper estimations of the impact of these parasites on fish populations demand a better understanding of transmission dynamics, which in turn requires more knowledge on the biology of these parasites in their intermediate hosts.

Acknowledgements

I am very grateful to Drs Richard Arthur, Ian McLaren and AI Shostak for critically reading the manuscript and providing many helpful suggestions. Mr Lionel Corriveau drew the figures, and Claudette Gosselin kindly assisted with the tables.

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Accepted 3 June 1994

the role of zooplankton in the transmission of …life cycles of derogenes varicus, the most common...

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