Symbionts of Marine Copepoda: an Overview

BULLETIN OF MARINE SCIENCE, 37(2): 586-598,1985

SYMBIONTS OF MARINE COPEPODA: AN OVERVIEW

Ju-shey Ho and Penny S. Perkins

ABSTRACT Symbionts of marine free-living Copepoda are reviewed according to their occurrence on the host's body (including appendages) and internally. No virus, rickettsia, or blue-green alga has been reported from marine Copepoda. Fungi, diatoms, ellobiopsids, ciliates (apostomes and suctorians) and larvae of epicaridean isopods are known as ectosymbionts. Bacteria are known from the body surface and gut. Endosymbionts include dinoflagellates (Blastodinium) and gregarines occurring inside the gut; dinoflagellates (Syndinium and Paradinium), haplosporidians and larvae of digeneans (metacercaria), cestodes (procercus, procercoid and plerocercoid), and nematodes (second and third stage larvae) inhabit the hemocoel. Distri- bution records indicate that symbionts of cope pods are unknown in many regions of the world's oceans; therefore, numerous species of symbionts are yet to be discovered and described. Information on the symbiont's life history and effects to the host is particularly wanting. Knowledge of symbiosis is indispensable to a complete understanding of the host's biology.

In terms of biomass, species diversity, niche exploitation and distribution, the Copepoda constitute one ofthe most prevalent assemblages of marine organisms. Consequently, copepods would be expected to host all conceivable forms of symbionts. However, most of the literature on marine copepod symbionts is concerned with protozoans and metazoans, there are few accounts of bacteria and fungi and, thus far, no virus or rickettsia has been reported. Although a species of blue-green alga (Lyngbya kuetzingii) was found on two species of freshwater copepods (Mar- galef, 1953), no comparable symbiont has been reported from marine copepods. In our opinion, this sparse and disproportionate documentation of copepod symbionts does not reflect the true phenomenon in nature. Although the first marine pelagic copepod, "Monoculus finmarchicus Gunne- rus" (=Calanus finmarchicus), was reported by the Bishop Gunnerus of Trond- heim, Norway in 1770, its symbionts remained unknown for nearly 100 years. In 1848 the Danish zoologist, Henrik Kr0yer, mentioned seeing "egg masses" of parasites attached to the mouth parts, as well as the backs and ventral surfaces of "Calanus spitsbergensis Kr." (=Calanus finmarchicus). A century later, Mar- shall and Orr (1955) suggested that the egg masses on the mouth parts of C. finmarchicus were cysts (phoronts) of ciliates and we suspect the masses on the backs and sides of the copepod are spores of Syndinium sp., a dinoflagellate. The first comprehensive documentation of symbionts of marine pelagic copepods was attempted by Apstein (1911). He examined the calanoids occurring in the North Sea and Kattegat, and recorded 23 kinds ofsymbionts from the following genera: Acartia, Calanus, Centropages, Euchaeta, Metridia, Paracalanus, Pseu- docalanus, and Temora. Although Apstein did not identify the symbionts, Jepps (1937a) reviewed Apstein's report and was able to identify most of the recorded symbionts. These included: Blastodinium, Ellobiopsis, gregarines, Ichthyospo- ridium, Jeppsia (=Chattonella), Paradinium, and trematode, cestode, and nematode larvae. Later, Sewell (1951) reported 19 kinds ofsymbionts (mainly protozoans) from pelagic copepods collected in the Red Sea and Indian Ocean during the John Murray Expedition. Sewell also investigated the effects of the symbionts on the host copepods. In their popular book on the biology of Calanus finmarchicus, Marshall and 586 HO AND PERKINS: MARINE COPEPOD SYMBIONTS 587

Orr (1955) devoted a chapter to the parasites of C. finmarchicus occurring in European waters. Because many early accounts on marine copepod symbionts were not included and especially since additional reports have appeared after 1955, we believe that it is timely to summarize our present knowledge and discuss problems and perspectives in the studies of copepod symbionts. In general, copepod symbionts inhabit the body surface (including the appendages), the gut and hemocoel. Those inhabiting the body surface are referred to herein as ectosymbionts, whereas those existing internally are called endosymbionts.

ECTOSYMBIONTS In this section we are chiefly concerned with symbionts inhabiting the body surface of pelagic copepods. However, it is necessary to consider those symbionts which occur on the surface of floating calanoid eggs, since this association may have a dramatic impact on copepod standing stock. For example, Redfield and Vincent (1979) reported that a Lagenidium-like fungus was a virulent parasite to the eggs of Diaptomus novamexicanus; they estimated that in 1976, the potential copepod recruitment in an alpine lake in California was reduced by 48.8% due to this fungus. In addition to fungi, other organisms infect copepod eggs. Cachon and Cachon (1968) found three species of the marine dinoflagellate, Chytriodi- nium, attached to calanoid eggs by a stalk; however, impact on copepod recruitment was not examined. Dissodinium is another genus of marine dinoflagellates containing two species that are found exclusively on eggs of planktonic copepods (Drebes, 1969; 1978; Elbrachter and Drebes, 1978). Certain protistans, such as Syndinium and Paradinium (dinoflagellates) appear on the copepod's body surface after a certain period oflatent growth internally. These symbionts will be discussed in the subsequent section under ENDOSYMBIONTS. Bacteria. -Souchard et al. (1979) have succeeded in isolating bacteria from the wild copepods (Acartia tonsa. Centropages furcatus, Labidocera aestiva, Pleuro- mamma sp. and Pontel/opsis regalis; collected from marine and estuarine envi- ronments) and healthy, laboratory-reared Acartia tonsa. They discovered that a greater proportion of bacteria was associated with the copepods than found free- living in the water column. The microorganisms identified were species of Vibrio, Pseudomonas, and Cyatophaga. Whereas Vibrio spp. were the most abundant bacteria associated with free-living copepods, Pseudomonas spp. were most prevalent in laboratory-reared copepods. Diatoms. -Some members of two families of diatoms, Diatomaceae and Proto- raphidaceae, are known to occur as epizoic organisms of marine Copepoda. They attach to the copepod with a mucilaginous substance or by stalks. Although poecilostomatoid copepods of the genera Corycaeus and Farranula are the most commonly reported hosts, some calanoids and harpacticoids have recently been added to the host list (Gibson, 1979; Hiromi and Takano, 1983). Pseudohiman- tidium pacificum is the most widely distributed epizoic diatom on Copepoda; it has been reported from the Adriatic Sea (Jurilj, 1957), the East and South China Seas (Voigt, 1959), the Gulf of Guinea and the Persian Gulf (Simonsen, 1970), Puget Sound, Washington (Russell and Norris, 1971), the Indian Ocean (Simon- sen, 1974), the Florida Current (Gibson, 1978), and off Izu Shimoda, Japan (Hiromi and Takano, 1983). Russell and Norris (1971) noted that the occurrence of P. pacificum on Corycaeus affinis in Puget Sound could reach as high as 82% and they speculated, based on the differential distribution of symbionts on the 588 BULLETIN OF MARINE SCIENCE, VOL. 37, NO.2, 1985

host body, that the diatoms were transferred to other copepods through copulatory and/or noncopulatory clasping.

Fungi. - In his review of the literature of fungal diseases of Crustacea, Unestam (1973) noted that bacteria infected mainly vertebrates, and fungi preferably at- tacked invertebrates. His review included a report of a saprolegnid fungus, Lep- tolegnia baltica, responsible for Euretemora hirundoides mortality in the Baltic Sea (Vallin, 1951; Hohnk and Vallin, 1953), and an ascosporous yeast, Metschni- kowia sp., that infected Calanus plunchrus in the Strait of Georgia, Canada (Seki and Fulton, 1969), but killed Euretemora vedox off the French coast (Fize et aI., 1970). Apstein's (1911) synopsis of copepod symbionts included observations on the relative pathogenicities of several fungi on Calanus finmarchicus. Jepps (1937b) identified the fungi as Leptolegnia, Metschnikowia and Ichthyosporidium. How- ever, Ichthyosporidium is no longer considered a fungus. In fact, its taxonomic status has long been disputed and remains controversial. Currently, Ichthyospo- ridium is included with either the Haplosporea or Microsporea. It should also be noted that Marshall and Orr (1955) used Jepps' original diagnosis and referred to Ichthyosporidium as a fungus. In any case, Apstein (1911) noted that Ich- thyosporidium infecting C. finmarchicus in the North Sea and Kattegat was less pathogenic than either Leptolegnia or Metschikowia; he remarked that Calanus infected with Ichthyosporidium could still swim actively. Similarly, Jepps (1937b) observed that although the ovary of infected Calanus was small, the eggs were not visibly degenerated.

Ellobiopsidae. - The ellobiopsids are protistans with unknown affinity (Johnson, 1983). Although they have questionably been included among the dinoflagellates (Caullery, 1910; Chatton, 1920; Sournia et aI., 1975), an affiliation with fungi has also been suggested (Jepps, 1937b). Boschma (1949; 1959) considered the ellobiopsids as a heterogenous assemblage of protistans with diverse affinities. Cur- rently, the family consists of about 20 species, most of them belonging to the genus Thalassomyces, symbionts of pelagic crustaceans, such as mysids, euphau- siids, amphipods, and caridean shrimps. Only three species of ellobiopsids are presently known to occur on marine copepods. Ellobiopsis chattoni is widely distributed; it has been reported from various species of calanoids in the North Sea (Caullery, 1910; Jepps, 1937b), Adriatic Sea (Hoenigman, 1958), Black Sea (Elian and Petran, 1971), Arabian Sea (Sewell, 1951), Indian Ocean (Krishnaswamy, 1950; Wickstead, 1963; Santhakumari and Saraswathy, 1979), and northeastern Pacific Ocean (Hoffman and Yancey, 1966). Ellobiopsis elongata is known to occur on Ctenocalanus vanus in the South At- lantic (Steuer, 1932) and Mediterranean (Hoenigman, 1958), but EllobiopsisJagei is so far confined to Clausocalanus arcuicornis in the Mediterranean (Hovasse, 1952). The ellobiopsids are found almost invariably attached to the antennae and the oral region of their copepod hosts. They first appear as a small knob of about 3- 70 SLm, then develop an oval or club-shaped test with a stalk which pierces the host's body. At maturity, the symbiont is divided into two segments, a proximal trophomere and a distal gonomere. The size and shape of these structures are species specific. Eventually, sporulation occurs within the gonomere producing numerous small buds (about 30 SLm) on the free surface. Each bud undergoes a series of divisions to form spores. According to Hovasse (1952), spores were released in small masses and no flagellawere present at this stage. After completion HO AND PERKINS: MARINE COPEPOD SYMBIONTS 589

of sporulation, it is speculated that a new gonomere is divided off and the process is repeated.

Ciliates. - Two groups of ciliates, apostomes (Order Apostomatida) and suctorians (Order Suctorida), are known to occur on marine copepods. The apostomes have a complex life history; it includes vegetative trophonts, dividing tomonts, free- swimming tomites, and encysting phoronts. Several types of cysts described by Chatton and Lwoff (1935), Jepps (1937b) and Sewell (1951) are attributable to phoronts of certain apostome ciliates. The cysts vary from 10 to 50 ~m in length and attach to various locations on the body, including the setae on the appendages. Since the morphology of the trophont is essential for species identification, most of the cysts are unnamed. Vampyrophrya pelagica is an apostome ciliate that encysts on planktonic copepods in the Atlantic Ocean. According to Grimes (1980), it has a peculiar mode offeeding on its host's tissue. The trophont emerges from its cyst when the copepod is mangled or crushed by a predator or other mechanical means. The freed trophont enters a fissure in the exoskeleton and feeds on the copepod's tissue. Several species ofsuctorians associate with marine copepods. Interestingly, they not only attach to free-living copepods, but also to symbiotic copepods normally living on octocorals (Humes and Ho, 1968). According to Bowman (1977), the suctorian ciliate, Dendrosomides lucicutiae occurring on calanoid copepods off the east coast of North America, initially appears on the copepod as a vermiform individual (measuring 260-280 ~m) attached by a basal sucker. After developing a stalk the ciliate grows, buds off arms, elaborates tentacles, and becomes a dendritic individual. Subsequently, a bud evaginates from the body just proximal to the arms. The bud grows eventually forming an elongate individual which sep- arates from the dendritic parent, and becomes established as a new vermiform individual.

Epicaridea. - Epicaridean isopods are parasites of marine crustaceans. The females of most species are so highly transformed that little or no resemblance to free-living isopods is apparent. However, the morphology of epicaridean males and larvae is less drastically altered and clearly reveals their isopod affiliation. Although numerous species of epicaridean isopods have been reported, life cycles are known for very few. Probopyrus pandalicola, occurring off the coast of North Carolina, is one species for which a complete life history is known. According to Anderson (1975), the adult isopods are found in the branchial chamber of the grass shrimp (Palae- monetes pugio). The epicaridean larvae develop in marsupial plates of the isopod and are liberated when the host molts. Once released the larvae swim toward the light in order to locate a copepod host. While the epicaridia are attaching to the host, they develop into a microniscus. This stage grows rapidly and molts to form the cryptoniscus. The cryptoniscus larva leaves the copepod and descends to locate the benthic decapod host. During their investigations on the larvae of three species of Probopyrus, Dale and Anderson (1982) found that the epicaridia of all species readily infested Acartia tonsa, but did not infest the other (possibly six) species of copepods present in their cultures. The attachment process of isopod larvae to the copepod host was first docu- mented by Marshall and Orr (1955). They reported that the larvae first grasp the appendages, then gradually migrate up onto the body where they settle for further development. Larvae that failed to reach the host's body were soon rejected. 590 BULLETIN OF MARINE SCIENCE, VOL. 37, NO.2, 1985

ENDOSYMBIONTS The endosymbionts of marine copepods are found either in the digestive tract or in the hemocoel. However, regardless of site preference in the host, they appear to gain entrance through the mouth. Although 22 species of Microsporidea were listed as endosymbionts of fresh- watercopepods by Sprague (1977), this group ofcnidosporans is yet to be reported from marine copepods. However, it should be noted that Oithona rigida in Indian waters is known to harbor in its hemocoel a haplosporidian parasite, Coelospo- ridium oithonae. Haplosporidians are sporozoans with strong affinity to the Mi- crosporidea. According to Narasimhamurti and Kalavati (1976), the infected copepods could be easily identified by their "bluish black colour and sluggish movements. " In the following, we shall discuss the endosymbionts of marine copepods according to their location within the host.

Gut Symbionts Bacteria. -Souchard et al. (1979) obtained fewer bacteria from the gut than from the body surface of pelagic copepods. Although Vibrio spp. were most abundant on the body surface of the pelagic copepods, Pseudomonas spp. predominated in the gut (P. j/uorescens comprised the largest proportion). On the other hand, the gut flora oflaboratory-reared copepods uniquely consisted of Vibrio spp. Souchard et al. (1979) speculated that the differences in the gut flora of otherwise similar copepods were attributable to differences in the host's feeding habits. Dinoj/agellates. -About 10 species of Blastodinium have been reported from the gut of marine pelagic copepods (Sewell, 1951). When mature, Blastodinium spp. reside within the midgut (stomach) occupying nearly the entire lumen. Therefore, infected copepods usually harbor only one symbiont. Since Blastodinium spp. retain plastids and pyrenoids while within the copepod's gut, it is speculated that photosynthesis may supplement nutrients gained from the host (Couch, 1983). Authorities (Chatton, 1920; Sewell, 1951) speculated that the symbiont begins its life within the copepod as a spore. An ingested spore germinates in the host's midgut forming a trophocyte. After a period of growth, the trophocyte divides producing a secondary trophocyte and a gonocyte. The gonocyte divides repeatedly producing numerous sporocytes which partially or completely surround the secondary trophocyte forming a mono blastic individual. In some species, after a period of rest, the secondary trophocyte may divide again producing a tertiary trophocyte and another gonocyte. The gonocyte undergoes repeated division forming a second layer of sporocytes inside the first. The resulting double layered individual is referred to as diblastic. During its existence within the host, the symbiont is enclosed within a cuticle. However, upon completion of sporocyte formation, the cuticle ruptures releasing sporocytes into the host's alimentary canal. It is suspected that spore maturation does not occur until the sporocyte is ejected out of the host through the anus. The liberated sporocyte then divides forming two dinospores. Although viruses have not been reported from copepods, some virus-like par- ticles were discovered by Soyer (1978) in the nucleus of a species of Blastodinium infesting copepods recovered from the Mediterranean off the French coast. Sporozoa. -Gregarines are intestinal parasites that require only one host to complete their life cycles. Although trophozoites of several gregarines have been reported from the midgut of marine copepods (Apstein, 1911; Krishnaswamy, 1950; HO AND PERKINS: MARINE COPEPOD SYMBIONTS 591

Marshall and Orr, 1955; Gobillard, 1963; Soyer, 1965), most of them are unidentified because their life cycles are incompletely known. The trophozoite rep- resents one of many stages in the gregarine life cycle, The only two named species of gregarines are Monocystis copiliae reported by Rose (1933) from Copilia vitrea off the coast of Algeria and Cephaloidophora petiti by Gobillard (1964) from two species of Candacia off the Mediterranean coast of France.

Coelomic Symbionts Dinoflagellates. -Syndinium is a genus of symbiotic dinoflagellates which occurs primarily in radiolarians. One or two species of Syndinium have also been reported from the hemocoel of marine copepods. The parasite is initially discernible as a plasmodium embedded in the connective tissue. Next it develops into a flattened mass that spreads throughout the hemocoel along the surface of the viscera. Eventually sporulation occurs resulting in numerous spores (dinospores, zoo- spores) visible inside the hemocoel. The spores are complete, they possess a girdle, sulcus, and two flagella, and are probably released into the sea upon rupture of the host's exoskeleton. Syndinium turbo has been reported from calanoids occurring off the French coast (Chatton, 1920) and in the Black Sea (Elian, 1970). An unidentified species of Syndinium has been reported from the North Sea (Jepps, 1937b) and Red Sea (Sewell, 1951). Interestingly, studies on the ultrastructure, chemistry, and nuclear division of Syndinium indicate that it differs fundamentally from free-living dinoflagellates (Soyer, 1974; Ris and Kubai, 1974). Three species of Paradinium (P. poucheti, P. caulleryi, and P. mesniti) parasitize copepods in the Mediterranean (Chatton and Soyer, 1973). Jepps (1937b) made observations on an unidentified species of Paradinium infecting copepods from the North Sea. According to Jepps, plasmodia in the copepod's hemocoel are capable of amoeboid movement. After a certain period of growth, the plasmodia move posteriorly, penetrate the hind gut, and emerge from the anus. Sporulation occurs while the plasmodium (which appears as an orange mass) is attached to the host's urosome. In an hour or so after emerging, the entire mass divides into a swarm of spores, each possessing two flagella. Although Paradinium is placed with the dinoflagellates, their affinity is still unclear. Ultrastructural studies on the plasmodium and spore of Paradinium poucheti have indicated a relationship with the mycetozoans (mixomycetes) (Ca- chon et al., 1968; Chatton and Soyer, 1973). Digeneans. -Digenetic trematodes have a complex life cycle involving two intermediate hosts. Copepods and many other zooplanktors, such as cnidarians, ctenophores, and chaetognaths, serve as the second intermediate hosts and harbor the metacercaria. Although numerous metacercariae have been recovered from marine plankton, few were from copepods (Dollfus, 1923a; Rebecq, 1965). Fur- thermore, almost all the metacercariae found in the hemocoel of marine copepods belong to a single family, Hemiuridae, a large family parasitic as adults in the esophagus and stomach offish. Some nonhemiurid metacercariae include Moni/i- caecum sp. in Paracalanus aculeatus, reported from the Bay of Bengal by Madhavi (1968), and Syncoelium sp. on Candacia pachydactyla, found near the mouth of the Amazon River by Overstreet (1970). According to Steuer (1929), the occurrence of metacercaria in copepods was first discovered in 1863 by the renowned German copepodologist, Carl Claus, from Paracalanus parvus in Helgoland Bay. Nevertheless, complete life histories are known for only two species of marine hemiurids. 592 BULLETIN OF MARINE SCIENCE, VOL. 37, NO.2, 1985

Derogenes varicus is perhaps the most widely distributed digenean, It has been recorded from more than one hundred species of fish (such as cod, flounder, sole, halibut, sculpin, perch, salmon, mackerel, etc.) in temperate waters worldwide. Based on K0ie's (1979) experiment, the calanoid copepods (Acartia sp., Calanus finmarchicus, Centropages hamatus, Paracalanus parvus, Pseudocalanus elongatus, and Temora longicornis) actively caught the free-swimming cystophorous cercariae that had been released from the snail (the first intermediate host). The pressure from seizure by the copepod's oral appendages caused the delivery tube in the caudal vesicle of the cercaria to evert and inject the cercarial body into the copepod's hemocoel. The injected cercarial body develops into a metacercaria within the copepod. As many as 132 metacercariae were found from a single experimentally infected copepod. The life cycle of another species ofhemiurid, Lecithaster confusus, is also known. The copepod, Acartia sp., was experimentally infected with the cercariae obtained from the gastropod intermediate host. Two weeks later, the infected copepods were fed to sticklebacks and the adult parasite eventually developed in the fish host. Hunninen and Cable (1943) and Ching (1960) also succeeded in infecting the harpacticoid copepod, Tigriopus californicus, with cercariae. However, the adult fluke failed to develop in fishes that were fed infected copepods. Since a nearly mature Lecithaster sp. (possibly L. salmonis) was recovered from a cyclopoid copepod collected in a plankton haul, it was suspected that Ching's failure to obtain the adult parasite was due to utilizing an improper experimental host. Progenesis is known in many species of digeneans parasitic in marine animals. For example, Bunocotyle cingulata, a parasite of perch, develops progenetically in the hemocoel of the copepod, Popella guernei (Chabaud and Biquet, 1954). An interesting discovery was made by Dollfus (1954); he found a progenetic metacercaria of Derogenes sp. in a parasitic copepod, Lernaeocera lusci, that was attached to the gill arch of a cod.

Cestodes.-Dollfus, in a series of reports (1923b; 1964; 1974; 1976) on the occurrence of cestode larvae in marine plankton and invertebrates, indicated that copepods hosted the larval stages oftetraphyllideans and tetrarhynchs. In the life cycle of these cestodes, the egg or coracidium is eaten by the copepod, the on- cosphere is released and penetrates the gut wall becoming lodged in the hemocoel where it develops into a procercoid or procercus (Ruszkowski, 1934; Riser, 1956; Euzet, 1959; Murdy and Dailey, 1971). After the infected copepod is eaten by an appropriate second intermediate host (usually a fish), the larva develops into a plerocercoid (Markowski, 1935; Overstreet, 1978). Some cestodes seem to have a rather strict host specificity with respect to intermediate hosts. For instance, in their work on the life cycle of Callotetra- rhynchus sp., a tetrarhynch existing as a plerocercoid in the muscle of cultured yellowtail, Nakajima and Egusa (1972) failed to experimentally infect seven species of copepods. Furthermore, out of 9,066 wild copepods (in 15 genera) that were collected from the water in which the fish culture was conducted, not a single procercus was recovered. Host specificity is further exemplified by the work of Kamo et al. (1973) on the life cycle of Diplogonoporus grandis, a pseudophyllidean parasitic in whales. They exposed the coracidia of this parasite to 33 species (in 19 genera and 17 families) of copepods, but only succeeded in obtaining procer- coids from a cyclopoid (Oithona nana) and a calanoid (Labidocera japonica). Similarly, host specificity in cestodes was demonstrated by another species of pseudophyllidean parasite of whales, Diphyllobothrium macroovatum. Hatsushika et al. (1981) found that the coracidia of this cestode experimentally infected 75% HO AND PERKINS: MARINE COPEPOD SYMBIONTS 593 of Acartia clausi, but failed to infect any of the other seven species of copepods tested. Nematodes. - Many species of ascaridoid nematodes are parasitic as adults in the digestive tract of marine fishes, birds, and mammals. However, as is true with other helminth parasites, larval stages and complete life histories are unknown for most species. Based on the available fragmentary information, it seems that nematodes require either one or two intermediate hosts which are various invertebrates. In their review on the occurrence of the larvae of Hysterothylacium, an ascaridoid genus found as adults in the digestive tract of fishes, Norris and Ov- erstreet (1976) listed seven phyla of invertebrates which serve as intermediate hosts. These are: Cnidaria (hydrozoans and scyphozoans), Ctenophora, Mollusca (gastropods and cephalopods), Annelida (polychetes), Arthropoda (crustaceans), Echinodermata (asteroids), and Chaetognatha. In general, nematode life cycles include four larval stages. Most marine ascari- doids hatch at the second stage larva (L2), which is eaten by a small crustacean, such as a copepod. Copepods are believed to serve as either a transfer host or a true intermediate host (Overstreet, 1983). In a transfer host, an ingested L2 ex- sheaths, but remains as L2 in the host's hemocoel. On the other hand, in a true intermediate host, the second stage larva develops into the third stage larva (L3), which is infective to the second intermediate host or the final host (in the case of a life cycle with a single intermediate host). McClelland (1982) experimentally determined that the anisakinae larva of Pho- canema decipens (living as adults in the intestine of harbor and grey seals) failed to infect calanoids (Euretemora and Pseudocalanus), but successfully infected 12 species ofharpacticoids and one species of cyclopoid (Paracyclopina sp.). Huizinga (1966) found that the second stage larva of Contracaecum spiculigerium, an intestinal parasite of marine piscivorous birds, is readily infective to both freshwater (Cyclops vernalis) and marine (Tigriopus californicus) copepods. Nematodes of the Order Spiurida also utilize copepods as their primary intermediate hosts. Whereas complete life histories are known for several species of freshwater spiurids, a single entire life history has yet to be worked out for a marine form. The larvae of marine spiurids parasitic in fish appear to be fairly host specific. In their study on the life history of Philometroides seriolae parasitic in yellowtail, Nakajima and Egusa (1970) found that only 4 of the 11 species of copepods tested in their experiments ingested the offered nematode larvae, but none of the larvae succeeded in penetrating the host's gut wall. One specimen of Acartia bifilosa ingested 17 larvae, but died; however, the larvae lived for 2 more days while in the midgut of the dead host.

PERSPECTIVES AND CONCLUSIONS We believe that numerous forms of symbionts of marine copepods are yet to be discovered and described. Aside from the North Sea and Mediterranean Sea, few oceanic regions have been thoroughly investigated. For example, symbionts of marine Copepoda have only been sporadically reported from the waters of North America, Japan, and India, and are virtually unknown from the remainder of the world's vast oceans. Frequently, the discovery of symbiont(s) is purely by chance. Therefore, collaboration between planktonologists and specialists of marine symbioses would greatly facilitate our knowledge of copepod symbionts. Presently, our nascent understanding of symbionts of marine copepods is attributable to several factors. First, complete life histories are known for very few 594 BULLETIN OF MARINE SCIENCE, VOL. 37, NO.2, 1985 symbiotic species. This is due, in part, to inherent difficulties in maintaining planktonic hosts in the laboratory and to restricted host specificities ofsymbionts precluding utilization of sUlTogatehosts in many experimental studies. Because knowledge of life histories is indispensable for understanding host-symbiont relationships, this void cannot be neglected; at least one complete life history should be worked out for each family of symbionts. One form of symbiosis is parasitism, and Anderson (1978) and May (1983) have discussed at length the role of parasites in regulating host populations. Although predation and competition are the two biotic factors receiving attention from population biologists, the effect of parasitism cannot be ignored. For example, Weinstein (1973) reported that the population of Calanus finmarchicus living in the Gulf of St. Lawrence was frequently infected with metacercariae of Derogenes varicus. The copepods were infected beginning at the fourth copepodid stage, 84.4% of infected copepods were in the fifth copepodid stage, 11.8% were adult females, and no infected adult male copepods were reported. Do these data suggest a high mortality of the fifth copepodid, and were males more susceptible? One might argue that Calanus finmarchicus is so abundant that impact of parasitism may not attain drastic reduction of the copepod population; but, not all planktonic copepods are as abundant as C. finmarchicus and when infection rate of this magnitude occurs on less common species, the damage it inflicts on the larval recruitment can be substantial. Certain parasites modify the behavior of their intermediate hosts lending them more susceptible to predation. For instance, some cystacanths (the final larval stage of Acanthocephala) are capable of altering the pigmentation and phototactic behavior of isopod (Muzzall and Rabalais, 1975; Camp and Huizinga, 1979) and amphipod (Bethel and Holmes, 1977; Kennedy et aI., 1978) intermediate hosts. The infected crustaceans were more conspicuous and, therefore, more vulnerable to predation by the final hosts (fishes and waterfowl). Although similar behavioral changes in response to parasitism have not been reported for marine Copepoda, the necessity for a parasite to complete its life cycle at the expense of the intermediate hosts is undoubtedly an underlying principle common to many parasitic species including those utilizing copepods as hosts. Some parasites are known to cause various morphological changes to the hosts. Sewell (1951) noticed that alterations in the body length, genital segment (first two segments of the urosome failed to fuse into a genital segment in female copepodid), and swimming legs (particularly the fifth pair in calanoids) were induced by parasitic infection. Cattley (1948) attributed sexual reversal observed in the fifth legs of Pseudocalanus elongatus to infection with Blastodinium. Sewell (1951), while concurring with Cattley's assertion on the influence of parasitism, considered that those transformed males of P. elongatus were actually females bearing a pair of fifth legs of the male type. Information on morphological alterations as a result of parasitism is particularly important to copepod taxonomists, especially when structures used for species identification, such as the swimming legs, are modified. Finally, knowledge of symbiosis can be utilized as a means of acquiring information on the host's biology. Noble (1972) reviewed investigations on the use of parasites of marine plankton as a tool for detecting feeding habits and distribution of fishes that prey on infected plankton. Additionally, symbionts can be used in fisheries management as "tags" to identify stock and trace migrations (Overstreet, 1983). Presently, it is not possible to apply these techniques to the study of marine Copepoda because too little information is available on their symbionts. HO AND PERKINS: MARINE COPEPOD SYMBIONTS 595

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DATEACCEPTED: March 25, 1985.

ADDRESSES:(l.S.H.) Department of Biology. California State University, Long Beach, California. 90840; (P.S.P.) Department of Anatomy, School of Medicine, University of California, Los Angeles, California 90024.