Internarionnl Joournolfor Primed in Great Britain

Porasirology

Vol. 20, No. 4. pp. 565-575.

1990

002&7519/90$3.00 + 0.00 Pergamon Press p/c Society/or Parmilology

Ausrralim

MARINE PARASITES: AN AUSTRALIAN

PERSPECTIVE

K. ROHDE Department of Zoology, University of New England, Armidale, N.S.W. 2351, Australia K. 1990. Marine parasites: an Australian perspective. International Journal for A review is given of major studies in marine parasitology in Australia. Aspects discussed include: geographical distribution of parasites in Australian coastal waters and their affinities to parasites of other zoogeographical regions; species diversity in Australian coastal surface and deep waters; use of marine parasites for stock discrimination; use of marine parasites as ecological models; ultrastructural and phylogenetic studies of marine parasites; and effects of marine parasites on their hosts. Abstiaet-R~~~~

Parasitology 20: 565-575.

INDEX KEY WORDS: Marine parasites; Australia; zoogeography; ecology; Monogenea; Trematoda; Cestoda; Nematoda; Copepoda; Protozoa; ultrastructure; phylogeny.

THIS paper

established (Rohde, 1976b, 1977a, 1978c,d, 1980b, 1982, 1984b, 1985a, 1986b), are an increased species richness of fish helminths towards low latitudes, a greater relative species richness (number of parasite species per all host species examined) of gill Monogenea of teleost fish at low latitudes, a greater species richness of digenean trematodes and monogeneans of fish in the Indo-Pacific than the Atlantic Oceans and as a consequence of this, greater endemicity in the IndoPacific (Lebedev, see Rohde, 1984b), a similarly narrow host specificity of trematodes and gill Monogenea at all latitudes (using the host specificity index proposed by Rohde, 198Oc), an increased host range of trematodes at high latitudes, and a greater parasite endemicity of fish trematodes of oceanic islands in the Pacific and South Atlantic than in the North Atlantic (Manter, see Rohde, 1982) (likely to apply also to Monogenea, although studies of monogeneans of oceanic islands in the North Atlantic have yet to lx made). Rohde (1985a) showed that there is a marked increase in the proportion of the viviparous Gyrodactylidae compared with other, egg-laying Monogenea towards high latitudes particularly in the Northern Hemisphere (Thorson’s rule). Rohde (1988a) showed that relative species richness of gill Monogenea is approximately five times greater in surface than in deep waters of southeastern Australia, and that the composition of the fauna of deep-sea Monogenea differs markedly from that of the surface. The former consists to a large degree of Diclidophoroidea (for taxonomy see Rohde & Williams, 1987), the latter of Microcotylidae, Dactylogyridae Ancyrocephalinae and Capsaloidea. A similar paucity and composition of the monogenean fauna have also been found from other deep-sea surveys, in the northwestern Pacific and northwestern Atlantic (for authors and details see Rohde, 1988a). The patterns found permit a characterization of the Australian fauna of marine parasites. Firstly, the

INTRODUCTION aims to give a concise review of major

marine parasitological studies in Australia, including a discussion of the geographical distribution of parasites in Australian coastal waters and their affinities with parasites of other zoogeographical regions, and of diversity of parasites in coastal surface water and in deep water. Also discussed will be some recent studies on marine parasites as indicators of host migrations and segregation of host populations, studies using marine parasites as ecological models, and ultrastructural and phylogenetic studies of marine parasites. Finally, effects ofparasites on their hosts will be reviewed. The literature review does not aim to be complete, and does not include papers concerned with aquaculture or bacteria and viruses. It aims to lead into the more important research programmes on marine parasitology in Australia. For earlier references, the reader ig referred to Beumer, Ashbumer, Burbury, Jette & Latham (1982) who compiled a checklist of parasites of Australian fish for the period 1861-1979, although the list of references is by no means complete (see also references in JettC E., unpublished M.Sc. thesis, James Cook University, 1977). Publications found in the checklist are included here only if necessary for understanding the discussion. Lester & Sewell (1989) published a checklist of parasites from Heron Island, Great Barrier Reef, with many relevant references. Rohde (1976a, 1981d, 1986a) briefly reviewed aspects of marine parasitology in Australia. ZOOGEOGRAPHY Earlier reviews of zoogeographical aspects of marine parasites are by Rohde (1982, 1984b, see also 1985b). Here, I only summarize those findings necessary to give a zoogeographical characterization of marine parasites in Australian coastal waters. Major trends in parasite distribution, earlier 565

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K.

waters around the Australian continent, as part of the Jndo-Pacific region and located largely in a warm environment, have a comparatively rich fauna of Monogenea and Digenea (for Monogenea of Western Australia see Williams, A., unpublished Ph.D. thesis, Murdoch University. W.A., 1988). Other groups of marine parasites are likely to exhibit similar diversity, as recently shown by Molnar & Rohde (1988) for Coccidia of marine fishes. The authors found eight species in 130 fish of 15species on the coast of northern New South Wales. Considering the small sample size and the fact that all fish were collected from a single locality in a single season, it does not seem unlikely that, on average, each fish species has about one species of Coccidia. Secondly, both trematodes and monogeneans in Australian waters show a high degree of host specificity. Thirdly, Gyrodactylidae are very scarce. Fourthly, gill Monogenea of deep-water teleosts, represented mainly by the Diclidophoroidea, are about five times less diverse than Monogenea of surface fish. Concerning the distribution of marine parasites in the various Australian zoogeographical regions, and affinities with other regions, two studies permit important conclusions. The first, by Byrnes (Byrnes, T., unpublished Ph.D. thesis. University of New England, Armidale, 1985) deals with 48 species of ectoparasites on the four species of bream, Acanthopugrus spp., occurring in the Australian regions, the second, by Kruse, G.O.W. (unpublished Ph.D. thesis, University of Nebraska State Museum, Lincoln, NE, 1981) deals with the digenean trematodes of marine teleosts in the South Australian Sea. Data on the ectoparasites of bream already published (Byrnes, 1985a, 1986a,b,c, 1987) show that the distribution of the parasites does not correspond to the Australian regions. as established on the basis of studies of marine benthic invertebrates. Of the species found more than once, most occur in several regions. Kruse concluded that the South Australian region has a strong endemic digenean fauna, dependent on the endemicity of the final (fish) and intermediate (molluscan) hosts, and that his findings support the concept of the Flindersian biogeographical province. Furthermore, South Australian Digenea belong to groups known to have wide and disjunct distributions. and their presence in southern Australia indicates that the major families of marine Digenea had evolved by the end of the Jurassic period. Kruse also concluded that the “Tethys Sea served as a major dispersal route for a fauna1 complex involving marine digeneans as indicated by the close affinity of the southern Australian fauna with the Caribbean fauna”, and “the affinity between South Australia and faunas in northern latitudes suggests the presence of a fragment of Gondwanaland” filling most of the Tethyan Bay, creating two major channels used for dispersal. Kruse’s data on Digenea are of great value and his zoogeographical interpretation deserves consideration. However, other Australian coastal regions need

ROHIE

to be studied before conclusions concerning the validity of the various regions for parasites can be drawn. and high percentages of genera shared between South Australia and the Caribbean, Japan and Hawaii may be somewhat misleading for zoogeographical conclusions because all these are warm water regions with a high species richness which have been well studied, and a relatively high proportion of shared genera could therefore be expected. Other regions. for example the Kerguelens, have cold water and therefore few species, and others again are incompletely known. Thus, few shared genera can be expected. SPECIES

DIVERSITY

Species richness of some groups, which are sufficiently known to permit certain zoogeographical conclusions, has been discussed in the previous section. However, studies of most other groups of marine parasites around Australia are too incomplete for generalizations on species richness and host specificity. Nevertheless, valuable contributions to our knowledge of various groups have been made. Thus, Lester, Blair & Heald (1980) recorded the ascaridoid nematode Sulcascaris sulcata and the gnathostome nematode Echinocephalus sp. from saucer scallops, Amusium balloti, in Shark Bay, Western Australia. The ascaridoid made some of the catch unsuitable for export. The same authors reported adult S. sulcata, larval Echinocephalus and two other nematodes from loggerhead turtles, Caretta caretta in the same area, and Cannon (1977) three nematodes including Anisakis simplex and a larval cestode from the melonheaded whale, Peponocephala electra stranded on Moreton Island, southern Queensland. Ascarid nematodes of scallops in Queensland were studied by Cannon (1978a), and the complete life cycle of Sulcascaris sulcata was worked out by Berry & Cannon (1981). Two moults occur in the eggs, the third stage larva hatches spontaneously and develops in marine bivalves and gastropods. After 34 months of steady growth to about 5 mm length, larvae moult again. In experimentally infected loggerhead turtles, Caretta caretta, the fourth stage larvae attached themselves to the oesophago-gastric junction and moulted to adults in 7-21 days. Substantial contributions to an understanding of ascarid nematodes of fishes have recently been made by Bruce & Cannon (I 989) Sprent (1990) Bruce (in press a,b) and Bruce & Cannon (in press). Bruce (1982, 1986, 1987a,b,c) made valuable studies of the taxonomy of parasitic isopods in Australian waters. In his monograph on the genus Mothocya he increased the number of recognized species from foureight to 25. This completely changed the concept of both host specificity and parasite distribution in this genus, from very broad to very narrow. The genera and species of externally attached cymothoids (Anilocrinae) in the Australian Museum collection were revised, leading to a substantial increase in the

Marine parasitology in Australia number of species known from Australia. According to Bruce (personal communication), isopods of Australian and adjacent waters are too poorly known to permit definitive biogeographical conclusions. In general, isopods on pelagic and semi-pelagic hosts are widely distributed, those on demersal hosts less so. Hooper (1983) recorded two species of cestodes, nine nematodes, five acanthocephalans, seven digeneans, two isopods and one copepod from approximately 200 fish of seven species of flathead (Platycephalidae) from northern New South Wales. The survey did not include Monogenea and most other ectoparasites. Byrnes (f985a,b, t986a,b,c, 1987) and Byrnes & Cressey (1986) described 15 species of Monogenea, two Branchiura, and 16 Copepoda from Acan&pugrus spp. from around Australia, and Bahrudin, AS. (unpublished MSc. thesis, University of New England, Armidale, N.S.W., 1985) examined 449 Acanthopagrus austro~~sfrom northern New South Wales and recorded 11 species of Digenea, five larval Cestoda, four larval and eight adult Nematoda and four Acanthocephala. Sedlak-Weinstein (in press) recorded five cyamids (Amphipoda) from cetaceans in Australian waters. Beveridge (1985) re-described Echinocephalus uncin~tus and E. spinos~s~~ from elasmobranchs in the Black Sea and Indian Ocean, respectively, and Beveridge (1987) reported E. overstreeti from elasmobranchs (including chimaeriform fishes) and molluscs in southern Australia. Andrews, Beveridge, Adams & Baverstock (1988) used allozyme electrophoresis to demonstrate that larvae of this species from molluscs and adults from an elasmobranch were indeed different life cycle stages of the same species. Studies by Campbell & Beveridge (1987a,b, 1988), Beveridge & Campbell (1987, 1988a,b), and Beveridge & Sakanari (1987) have enhanced our taxonomic understanding of trypanorhynch cestodes from Australian elasmobranchs and teleosts. Blair (1987) revised the digenean subfamily Octangiinae from marine turtles, Bray & Cribb (1989) described some digeneans of the family Opecoelidae from the southern Great Barrier Reef, and Rohde (1977~. 1978a) described bird schistosomes from the Great Barrier Reef, potential agents of schistosome dermatitis. Of particular interest is the observation that pelagic heteropod molluscs contain trematode larvae, the first such record since Leuckart’s, 135 years ago (Lester & Newman, 1986). Larval trematodes of two snail species and some aspects of the ecology of the hosts and parasites were described by Cannon (1978b, 1979) and Rohde (1981~). Several studies of marine Monogenea have been published. Williams (1988, thesis cited above) and Williams (1986, 1988) described Monogenea of fish from Western Australian coastal and estuarine waters, and Rohde (1976c, 1977d, 1978e,f, 1987a, 1989b), Rohde, Roubal & Hewitt (1980) Rohde & Watson (1985a,b), Rohde & Williams (1987) and Williams & Beverley-Burton (1989) Monogenea from various

567

Australian, New Zealand and New Caledonian localities. Extensive monographs of ectoparasites, including the Monogenea, of bream, Acanthopagrus australis and snapper, Chrysophrys auratus are by Roubal(l981) and Roubal, Armitage & Rohde (1983), respectively. Of particular importance for taxonomic studies of Monogenea is the demonstration of a high degree of geographical variation in this group (Rohde &Watson, 1985a,b; Rohde, 1987b, 1989b). Owens (1987) published a checklist of metazoan parasites of Crustacea Natantia (excluding crustacean parasites of the Caridea). Owens & Glazebrook (1985) cornrn~~t~ some interesting observations on sex determination of bopyrid isopods infecting penaeid prawns, suggesting that in the Bopyridae there are at least two types of sex determination, i.e. epigenetic determination by host substrate and genetic determination at fertilization. The same authors (Owens & Glazebrook, 1988) found two species of microsporidians, Ameson sp. and The~oh~n~~sp. in several species of Penaeus on the Great Barrier Reef. Prevalence of infection was low (c 0.1%) in both species. Lester (1982) described a new species of Unicapsula (Myxozoa) from Seriola lalaudi on the Great Barrier Reef. Valuable studies on a group containing some interesting marine parasites but not usually considered in parasitological surveys, i.e. the Turbellaria, were made by Cannon, who published an illustrated guide to the families and genera of Turbellaria (Cannon, 1986b), and descriptions of species from various echinoderms (Cannon, 1978c, 1982, 1986a, 1987, in press), fish (Cannon L Lester, 1988) and a tridacnid clam (Goggin & Cannon, 1989). Observations on the nutritional physiology and the respiratory pigment of some species were also made (Jennings & Cannon 1985, 1987). Cannon & Jennings (1988) described a new aseptate gregarine, a hyperparasite of a turbellarian infecting the Crown-of-Thorns starfish on the Great Barrier Reef. The first record of a fecampiid turbellarian from New Zealand was published by Blair & Williams (1987) (see also Blair, 1984). The species, Kronborgia isopodicola lives in the haemocoel of the intertidal isopod Exosphaeroma obtusum. The mature female emerges from the host, secretes a cocoon around herself, and is joined by a male. Numerous egg capsules are laid, each with two embryos. USE OF PARASITE3 FOR STOCK DISCRIMINATION

Several authors have used parasites for stock discrimination. Owens (1985) used the lecanicephalid cestode Polypocephalus as a biological marker for banana prawns, Penaeus merguiensis in the Gulf of Carpentaria. Parasite loads were low and constant at salinities from 14 to 34 ppm, and frequency distribution was best described by a non-truncated negative binomial distribution, indicating lack of parasite-induced mortality. Parasite loads formed two natural groupings, one in the south-east comer of the Gulf and one in the Keerweer-Mitchell River area.

56X

K. ROHDE

Parasite loads did not suggest that there are extensive migrations of adolescent prawns away from their nursery estuaries. Earlier, Owens (198I, 1983) had also examined the possible use of the trypanorhynch cestode Parachr~stianeZ~a monomegacantha and the bopyrid isopod ~pipenaeon ingens, respectively as biological markers of banana prawns, but found them to be of much less use. Speare (1988) conducted a ‘preliminary survey’ of parasites of Pacific sailfish, Istiophorus platypterus, from coastal waters of northeastern Australia during 1987/!988. Infection leveis with six (out of IO) parasite species were signi~cantIy different between two fishing grounds (Cape Bowling Green and Cape Moreton), and thus potentially useful for stock discrimination. In particular, the digenean trematode Cardicola sp. was prevalent in fish from the first but almost absent from the second locality, and a didymozoid trematode in the body cavity, ,~ematobothr~um, was found only at the second locality. However, only IO fish from the first and 11 from the second locality were examined. Almost all studies on stock discrimination use endoparasites. Rohde (1987b) suggested that differences in sclerite size of Monogenea of the same species from different localities may be useful as we!! According to the method described by him, monogeneans are left in a drop of 45% acetic acid on a microscope slide for a few minutes, squashed under a cover slip to spread the sclerites in one plane, and measured under a microscope. Permanent mounts can be made by dehydrating the sclerites and mounting them in eupara! or some other mounting medium. He showed that populations of Kuhnia scombri from Scomber australa&us in New Zealand and New South Wales and from S. japonicus in Japan and Ecuador have hamuli of different lengths. Subsequent studies (unpublished) on larger samples showed significant differences in hamulus length between populations of K. scombri in Western Australia, New South Wales and New Zealand, but not between those ofTasmania and New South Wales. Studies on the life span of Kuhn~a, and on possible effects of host size on the hamulus length of the worms, are under way. A knowledge of the life span is important to establish on what time scale the method can be used. Lester, Barnes & Habib (1985) recovered 26 parasite ‘types’ from 878 skipjack tuna, Katsuwonus ~e~arn~s from Australia, New Zealand, Papua New Guinea, several other regions in the Indo-Pacific Ocean, and Puerto Rico. Data from the 22 most reliable parasites gave no evidence of discrete stocks of the fish, either when analyzed singly or when using combinations of parasites in multivariate analyses. Analysis of the numbers of parasites from particular schools suggested that schools stayed together for several weeks but not for life. The orange roughy, Hoplostethus atlanticus has become an important fish trawled in deep water of Australia and New Zealand. Lester, Sewell, Barnes & Evans (1988). in order to develop a feasible tag for the

species, examined 125 1 fish collected from eight areas off southern Australia and three areas off New Zealand between 1983 and 1986. Fish from each area were divided into three length groups, and a canonical multivariate analysis performed on larval nematodes and cestodes discriminated five Australian and three New Zealand stocks. The authors concluded that N. atlanticus “is a sedentary species with little movement between fish-management zones” (see Sewe!l& Lester. 1988 for data of the survey). A!! these studies indicate how useful parasites can be for discriminating stocks of fish and other marine animals. However, there are limits to the method. The timespan over which a parasite can be used depends on its longevity. and dispersal of eggs or larvae before infection occurs may restrict the usefulness of the method to distinguishing older populations: fish stocks with different parasites may still be genetically identical. For example, the fact that Smith (1986) found little genetic separation between samples of orange roughy from several sites in New Zealand. whereas Lester et al. (1988) distinguished separate stocks in the same waters using parasites, may be due to early dispersal of eggs or larvae, although Lester et al. (1988) drew attention to other explanations: recently isolated fish populations may not have developed sufficient genetic differences, and a small amount of gene flow will make it difficult to recognize semi-isolated stocks. It may often be impossible and unnecessary, but ideally the life cycle and life span of a parasite, and where and when infection occurs, should be known in studies using the parasite for stock discrimination. In many cases, several methods may be useful, such as isoenzyme and parasite studies. MARINE PARASITES AS ECOLOGICAL MODELS Rohde (1976a,c, !977b,d. 1978b,c. 1979a. 1980a, 1981b, 1982; Rohde & Hobbs, 1986) has used supposedly simple ecological systems, i.e. the gills of marine fish, to investigate certain ecological patterns. A recent review of the work was given by Rohde (1989a). Gills may vary in a number of parameters, such as size, numbers of individuals and species of ectoparasites infecting them, and latitude where collected. A!! but one or a few of these variables can be kept constant in ‘natural experiments’, at least to a degree reasonably to be expected in biological ‘experiments’. The following conclusions were reached: (I) Many potential niches are empty, i.e. species have not yet evolved for them, since fish of similar size and habits in the same locality, or at different latitudes, or at different depths, contain different numbers of parasite species, and since only some parasite species harbour hy~rparasites. (2) Microhabitat restriction may be stabilized or enhanced in order to facilitate mating of parasites. (3) Much of the evidence for the evolutionary significance of interspecific competition is doubtful, but whereas there is little or no evidence that interspecific competition has been an important evolutionary force

Marine parasitology in Australia leading to niche segregation, there is much evidence for the significance of mechanisms leading to reproductive isolation. (4) By ruling out the effects of climatic stability, climatic predictability, spatial heterogeneity, productivity, stability of primary production, com~tition, rarefaction, predation and ecological time, it is concluded that only an evolutionary time hypothesis can give a general explanation for latitudinal gradients in species diversity, although the other factors may have local effects or secondarily enhance the gradients. (5) Longer ‘effective’ evolutionary time at low latitudes is likely to be due to accelerated evolution as the result of faster selection and possibly faster mutation rates. (6) A greater proportion of small species of marine teleost fish with their smaller microhabitats in tropical Pacific than in cool Atlantic waters indicates a possible reduction in niche width of tropical animals, however, there is no evidence for greater specialization and greater species packing of parasites in warm environments. (7) No evidence was found that area per se is a primary force determining species diversity, an important factor determining species diversity of ectoparasites of marine fish, at least in some cases, is diversity of the host group. (8) Thorson’s rule, that non-pelagic development of marine benthic invertebrates increases with latitude, is shown to apply to a group of marine parasites, the Monogenea: the only explanation for the phenomenon consistent with characteristics of the Monogenea is suggested to be an effective method of getting to a host. Rohde (1989a) stressed that conclusions based on the study of simple systems cannot be automatically applied to more complex> ones, but simple systems must be understood if complex systems are to be understood. Some suggestions for future studies were outlined. ULTRASTRU~RE AND PHYLOGENY OF MARINE PARASITES Studies conducted over recent years at the University of New England had several aims. Firstly, comparative ultrastructural studies of free-living and parasitic Platyhelminthes, particularly of their protonephridia, sperm, s~~atogenesis, epidermal cilia and sense receptors, aimed to contribute to a phylogenetic system of the Platyhelminthes (papers on marine parasites only: Rohde & Watson, 1988; Rohde, Watson & Cannon, 1988; Rohde, Watson & Roubal, 1989b; Rohde, Justine & Watson, 1989); secondly, detailed ultrastructural studies of Aspidogastrea aimed to characterize this archaic group which is likely to be at the very root of parasitic PlatyheIminthes; thirdly, electron-microscopic studies of Monogenea aimed to extend our morphological knowledge of the group (Rohde, 1979b, 1980d, 1981a, 1986c; Rohde, Justine & Watson, 1989; Rohde, Watson & Roubal, 1989b). Concerning the first point, a recent review of

569

the major findings (Rohde, 1988b) showed that all groups of parasitic flatworms are closely related, as already suggested by Rohde (1980d) on the basis of studies of the protonephridia, and supported in detail by Ehlers (1985), who established the phylum Neodermata for the parasitic groups. Among the Neodermata, two major lineages can be distinguished. One, the Trematoda (Aspidogastrea, Digenea) and Monogenea have a septate junction along the flame bulb and protonephridial capillaries; the other, the Cestoda including the Gyrocotylidea, Amphilinidea and Cestoidea, are without a septate junction. In the first group, the surface area of the protoneph~dial capillaries is increased by lamellae and/or reticula, in the second group, it is increased by short microvilli. Udonellu is clearly characterized as a neodermatan by the ultrastructure of sense receptors, tegument, sperm and protonephridia. it differs from all the Monogenea Polyopisthocotylea and Monopisthocotylea as well as the Trematoda examined in the lack of a septate junction in the protonephridia, resembling the cestodes in this feature. It differs from the latter in the presence of numerous ‘desmosome-like’ connections between the flame bulbs and adjacent cytoplasm (Rohde, Watson & Roubal, 1989a). Ultrast~ctural studies of umagillid tur~lla~ans symbiotic in Echin~e~ata clearly indicate that these forms are not close relatives of the Neodermata, although a tendency towards loss of the vertical rootlet of epidermal cilia, also characteristic of the Neodermata, was demonstrated in the Umagillidae (Rohde et al., 1988; Rohde & Watson, 1988). Concerning the second point, studies of the marine aspidogastrean Lob~tostomu manteri revealed an amazing variety and number of sense receptors, far in excess of anything found in parasitic stages of other platyhelminths or in free-living species. Rohde (1989c) and Rohde & Watson (1989a) suggested that the most likely explanation for the presence of a large variety and large numbers of sensilla is avoidance of damage to the mollusc host, prosobranch snails on the Great Barrier Reef. Importantly, the parasite has no freeliving stages. The final host, a teleost fish, becomes infected by eating infected snails, snails become infected by eating eggs containing infective larvae shed in the faeces (Rohde, 1973, 1975; Rohde & Sandland, 1973). Ultrast~ctural studies of other organ systems of Lobatostoma confirmed previous studies of aspidogastreans indicating the close relationship of the group with digenean trematodes and Monogenea (Rohde, 1989d; Rohde & Watson, 1989b). Beveridge & Smith (1988) made a transmission electron microscope study of the rhyncheal system of the trypanorhynch cestode Tr~rn~crac~t~us aetobatidis. Blair & Williams (1987) and Williams (1988a,b) examined the fine structure of the fecampiid turbellarian Kronborgia isopodicolu, the last paper using transmission electron microscopy. As in the Neodetmata, sperm has two 9+ ‘1’ axonemes incorporated in the sperm body.

570 EFFECTS OF MARINE

K. PARASITES

ON THEIR HOSTS

Rohde (1982, 1984a) gave brief reviews on effects of marine parasites on their hosts. Rohde (1984~) discussed various pathological effects of helminths of marine fishes in greater detail, and several Australian studies on specific effects of marine parasites have been published. One aspect which has recently received much attention is the effect parasites have on host populations. Lester (1984) discussed six methods for detecting mortality due to parasitic infections in natural fish populations, i.e. (1) autopsies, (2) determination of the frequency of infections known to be eventually lethal, (3) observation of decreases in prevalence of long-lived parasites or permanent scars due to parasites with host age, (4) observation of decreases in the variance/mean ratio for parasites with host age, (5) comparison of observed frequency of a combination of two independent events with the calculated probability of their occurrence, and (6) comparison of observed frequency distribution of a parasite with a projected frequency based on data from lightly infected fish. In the last method, which received a good deal of attention, negative binomial distributions are fitted to the data and truncated at various points. Some earlier authors had already pointed out that aggregation of parasites within their host population (as indicated by negative binomials) can be a result of the heterogeneity of hosts, the distribution of infective stages and/or of chance, and that not only parasite-induced host mortality, but also immune responses can reduce the degree of aggregation (as indicated by truncation of the negative binomials). Rohde & Hobbs (1988) showed that simulation of even a minor Allee-effect (a deleterious effect on individuals, in this case parasites, due to their very low densities) by shifting a few individuals from the ‘0’ to the ‘l’class (i.e. hosts with no parasites or one parasite) has the same result on negative binomial frequency distributions, as has mortality. The authors stressed that this was no ‘proof’ of an Allee-effect, but suggested that truncation of frequency distributions alone, in the absence of strong corroborative evidence like direct observation of death or pathological data, does not imply mortality. Lester (1980) examined the pathology of the flathead fish, PlatycephaIus fiscus, infected with the didymozoid trematode Neometadidymozoon helicis, and Sharahom & Lester (1982) that of the Spanish mackerel, Scomberomorus commerson, infected with the trypanorhynch Grillotia branchi. Roubal(1986a,b,c,d, 1987b, 1989a,b) made thorough studies of pathological effects of gill and other ectoparasites (Monogenea, Copepoda and Hirudinea) of the Australian bream, Acanthopagrus australis, using light microscopy and scanning as well as transmission electron microscopy. As a basis for pathological studies, the gill surface of this fish species was also examined (Roubal, 1987a,b). Some interesting observations on the effects of the

ROHDE

rhizocephalan parasite Sacculina granijtira on an invertebrate, the sand crab Portunus pelagicus, were communicated by Phillips & Cannon (1978) and Bishop & Cannon (1979). According to the former authors, an increased prevalence of barnacles on the carapace of infected crabs indicates that the parasite inhibits moulting, and distribution of infected crabs in Moreton Bay, Queensland, suggests that the parasite preferentially attacks young crabs as they move inshore and then induces crabs to behave like eggbearing females by moving seaward as they grow. Infected female crabs show little morphological change, whereas the chelae of infected males become more similar to those of females. Infected crabs are sterile, the hepatopancreas appears green rather than tan. and they groom their ‘externae’ (parts of the parasite on the abdomen) as egg-laying females groom their egg masses. Behaviour changes due to Sacculina are described in more detail by Bishop & Cannon (1979). Roubal, Masel & Lester (1989, see also Roubal & Lester, 1987) used an indirect fluorescent antibody test to detect Marteilia sydneyi (Ascetospora), the agent of QX disease, in the digestive gland of the Sydney rock oyster, Saccostrea commercialis. Large numbers of sporonts were shed by infected oysters before death, but lightly infected oysters were apparently able to shed all their parasites and recover. Lester, Goggin & Sewell (in press) pointed out that Perkinsus spp. (Apicomplexa) are widespread in Australian molluscs and have been associated with mortalities of greenlip abalone, Haliotes laevigata, in South Australia, and of giant clams, Tridacna gigas, in Queensland. Although the number of species of the genus present in Australia is not known, infection experiments indicate that some species can infect many species of molluscs (Goggin, Sewell & Lester. 1989). Twenty-two of 32 H. laevigata and four of 15 of the small, non-commercial abalone H. cyclobates sampled in the Gulf of St. Vincent, South Australia, were infected with P. olseni (see Lester, 1986) and 160 individuals of 30 species (out of a total of 644 individuals) of 84 species of bivalves on the Great Barrier Reef were infected (Goggin & Lester, 1987). CONCLUSIONS

This review has shown that marine parasites of many groups in Australian waters are being actively studied. It is very likely that parasites of various kinds represent the majority of all marine animals, but all groups are incompletely known. Marine parasites are useful for zoogeographical studies, for stock discrimination, and as ecological models. Ultrastructural studies of marine parasites can make important contributions to establishing a phylogenetic system of invertebrates, and marine parasites can have significant pathological effects on their hosts, and cause mortality. In Australia, programmes in marine parasitology are being conducted at the Department of Parasitology, University of Queensland (taxonomy

Marine parasitology in Australia

of trematodes, amoebic gill disease, community ecology of crab parasites, morphology and biology of Monogenea, effects of isopod parasites on host populations, protozoan pathogens of molluscs, parasites as indicators of fish movements, parasites as indicators of water quality, phylogeny of cetacean parasites); at the Department of Zoology, University of New England (taxonomy and zoogeography of Monogenea, other helminths and Copepoda, ultrastructure and phylogeny of Platyhelminthes, use of parasites in stock discrimination, pathology due to parasites, parasites of parasite as ecological models, seasonality infections); at the Queensland Museum (Turbellaria, Isopoda, fish nematodes); at the James Cook University and the Australian Institute of Marine Science, Queensland (parasites for stock discrimination and biological control); and in several other universities and research institutions. Acknowledgements-I wish to thank the following colleagues for making reprints, proofs and preprints of their work available to me: Dr R. J. G. Lester and Dr F. R. Roubal, Department of Parasitology, University of Queensland, St. Lucia; Dr J. B. Williams, Department of Zoology, University of Canterbury, Christchurch, New Zealand; Dr I. Beveridge, School of Veterinary Science, The University of Melbourne; Dr G. D. W. Kruse, Harold W. Manter Laboratory, University of Nebraska State Museum, Lincoln, NE, U.S.A.; Dr L. R. G. Cannon, Queensland Museum, Brisbane; Dr L. Owens and Dr J. S. Glazebrook, Graduate School of Tropical Veterinary Science, James Cook University, Queensland; Dr N. Bruce, Editorial Office, Ausfralian Journal of Scien@c Research, East Melbourne; P. Speare, Department of Marine Biology, James Cook University and Australian Institute of Marine Science, Townsville, Queensland. Dr N. Watson critically read the manuscript and Mrs V. Watt and Mrs S. Higgins typed the manuscript.

ANDREWS R. H., BEVERIDGE I., ADAMSM. & BAVERSTOCK P. R. 1988. Identification of life cycle stages of the nematode Echinocephalus overstreeri by allozyme electrophoresis. Journal of Helminthology 62: 153-157.

BERRYG. N. & CANNONL. R. G. 1981. The life history of Sulcascaris sulcata (Nematoda: Ascaridoidea), a parasite of marine molluscs and turtles. International Journal for Parasitology 11:43-54.

BEUMER J. P., ASHBURNER L. D., BURBURY M. E., JETTYE. & LATHAMD. J. 1982. A Checklist of the Parasites of Fishes Australia and its Adjacent Antarctic

redescriptions of T. aetobatidis (Robinson, 1959) comb. nov. and T. binuncus (Linton, 1909) comb. nov. Transactions of the Royal Society of South Australia 111: 163171. BEVERIDGE I. & SAKANARI J. A. 1987. Lacistorhynchus dolljiii

sp. nov. (Cestoda: Trypanorhyncha)

in elasmobranch fishes from Australian and North American coastal waters. Transactions of the Royal Socieiy of South Australia 111: 147-154.

BEVERIDGE I. & CAMPBELL R. A. 1988a. A review of the Tetrarhynchobothriidae Dollfus, 1969 (Cestoda: Trypanorhyncha) with descriptions of two new genera, Didymorhynchus and Zygorhynchus. Systematic Parasitology 12: 3-29.

BEVERIDGE I. & CAMPBELL R. A. 1988b. Ceforhinicolu n. g., Shirleyrhynchus n. g. and Stragulorhynchus n. g., three new genera of trypanorhynch cestodes from elasmobranchs in Australian waters. Systematic Parasitology 12: 47-60. BEVERIDGE I. & SMITH K. 1988. Ultrastructure of the rhyncheal system of Trimacrucanthus aetobafidis (Cestoda: Trypanorhyncha). International Journal for Parasitology 18: 623432.

BISHOPR. K. & CANNON L. R. G. 1979. Morbid behaviour of the commercial sand crab, Portunus pelagicus (L.), parasitized by Sacculina granifera Boschma, 1973 (Cirripedia; Rhizocephala). Journal of Fish Diseases 2: 131-144. BLAIRD. 1984. An unusual turbellarian parasite in intertidal isopods. New Zealand Journal of Zoology 11: 102. BLAIRD. 1987. A revision of the subfamily Octangiinae (Platyhelminthes: Digenea: Microscaphidiidae) parasitic in marine turtles (Reptilia: Chelonia). Australian Journal of Zoology 35: 75-92.

BLAIRD. & WILLIAMSJ. B. 1987. A new fecampiid of the genus Kronborgiu (Platyhelminthes: Turbellaria: Neorhabdocoela) parasitic in the intertidal isopod Exosphaeroma obtusum (Dana) from New Zealand. Journal of Natural History 21: 1155-l 172. BRAYR. A. & CRIBBT. G. 1989. Digeneans of the family Opecoelidae Ozaki, 1925 from the southern Great Barrier Reef, including a new genus and three new species. Journal of Natural History 23: 429473.

REFERENCES

from

571

Territories.

Technical Communication No. 48 of the Commonwealth Institute of Parasitology. Commonwealth Agricultural Bureaux, Farnham Royal, Slough. BEVERIDGEI. 1985. A redescription of Echinocephalus uncinarus Molin, 1858 (Nematoda, Gnathostomatoidea) from European rays, Dusyatispastinaca (Linnaeus, 1758). Bulletin du Museum Naiional d’Hisfoire NaturelIe (Paris, 4 series) 7: 78 l-790.

BEVERIDGE I. 1987. Echinocephalus overstreeti Deardorff & Ko, 1983 (Nematoda: Gnathostomatoidea) from elasmobranchs and molluscs in South Australia. Transactions of the Royal Society of South Australia 111:79-92.

BEVERIDGE I. & CAMPBELL R. A. 1987. Trimacracanthus gen. nov. (Cestoda: Trypanorhyncha: Eutetrarhynchidae), with

BRUCEN. L. 1982. Species of Argathona Stebbing, 1905 (Isopoda, Corrallanidae) new to Australia, with description of two new species. Crustaceana 42: 12-25. BRUCEN. L. 1986. Revision of the isopod crustacean genus Mothocya Costa in Hope, c851 (Cymothiidae: Flabellifera), parasitic on marine fishes. Journal of Natural History 20: ‘1689-l 192.

BRUCEN. L. 1987a. Australian Pleopodias Richardson, 1910 and Anilocra Leach, 1818 (Isopoda: Cymothoidae), crustacean parasites of marine fishes. Records of the Australian Museum 39: 85-130.

BRUCE N. L. 1987b. Australian Renocila Miers, 1880 (Isopoda, Cymothoidae), crustacean parasites of marine fishes. Records of the Australian Museum 39: 169-182. BRUCEN. L. 1987~. Australian species of Nerocila Leach, 1818, and Creniolu n. gen. (Isopoda, Cymothoidae), crustacean parasites of marine fishes. Records of the Australian Museum 39: 355412.

BRUCEN. L. & CANNONL. R. G. 1989. Hysterothylacium, Iheringascaris and Maricostula new genus, nematodes (Ascaridoidea) from Australian pelagic marine fishes. Journal of Natural History 23: 1397-1441. BRUCEN. L. (in press a) Redescription of the ascaridoid nematode Hysterothylacium scomberomori (Yamaguti) from Australian Spanish mackerel Scomberomorus commerson (La&p&de). Memoirs of the Queensland Museum.

512

K. R~HIX

BRUCE N. L. (in press b) Hysterothylacium Ward & Hagath. 1917 and Ichthyascaris Wu. 1949, ascaridoid nematodes, from Australian demersal fishes. Memoirs qf the Queensland Museum. BRUCE N. L. & CANNON L. R. G. (in press) Ascaridoid nematodes from sharks from Australia and the Solomon Islands, Southwestern Pacific. Invertebrate Taxonomy. BYRNEST. 1985a. Four species of Pol.vlabroides (Monogenea: Polyopisthocotylea: Microcotylidae) on Australian bream, Acanthopagrus spp. Australian Journal of Zoology 33: 129142. BYRNES T. 1985b. Two new Argulus species (Branchiura: Argulidae) found on Australian bream (Acanthopagrus spp.). Australian Zoologist 21: 579-586. BYRNEST. 1986a. Six species of Lamellodiscus (Monogenea: Diplectanidae) collected from Australian bream (Acanthopagrus spp.). Publications of the Seto Marine Biological Laboratory 31: 169-I 90. BYRNES T. 1986b. Some ergasilids (Copepoda) parasitic on four species of Australian bream, Acanthopagrus spp. Australian Journal of Marine and Freshwater Research 37: 8 l-93. BYRNEST. 1986c. Five species of Monogenea from Australian bream, Acanthopagrus spp. Australian Journal of Zoology 34: 65-86. BYRNES T. & CRESSEY R. 1986. A redescription of Colobomatus mylionus Fukui from Australian bream, Acanthopagrus (Sparidae) (Crustacea: Copepoda: Philichthyidae). Proceedings of the Biological Society of Washington 99 388-391. BYRNES T. 1987. Caligids (Copepoda: Caligidae) found on the bream (Acanthopagrus spp.) of Australia. Journal of Natural History 21: 363404. CAMPBELLR. A. & BEVER~DGE I. 1987a. Florieepsminacanthus sp. nov. (Cestoda: Trypanorhyncha) from Australian fishes. Transactions of the Royal Society of South Australia 111: 189-194. CAMPBELL R. A. & BEVERIDGE I. 1987b. Hornelliella macropora (Shipley & Hornell. 1906) comb. nov. (Cestoda: Trypanorhyncha) from Australian elasmobranch fishes and a re-assessment of the family Hornelliellidae. Transactions of the Royal Society of South Australia 111: 195200. CAMPBELLR. A. & BEVERIDGEI. 1988. Mustelicola antarcticus sp. nov. (Cestoda: Trypanorhyncha) from Australian elasmobranchs, and a re-assessment of the family Mustelicolidae Dollfus, 1969. Transactions of the Royal Society of South Australia 112: 153-I 61. CANNON L. R. G. 1977. Some aspects of the biology of Peponocephala electra (Cetacea: Delphinidae). II. Parasites. Australian Journal of Marine and Freshwater Research 28: 711-722. CANNON L. R. G. 1978a. A larval ascaridoid nematode from Queensland scallops. International Journal for Parasitolog) 8: 75-80. CANNON L. R. G. 1978b. Marine cercariae from the gastropod Cerithium moniliferum Kiener at Heron Island. Great Barrier Reef. Proceedings of the Royal Society of Queensland 89: 45-57. CANNON L. R. G. 1978~. Pterastericola vivipara n. sp., a parasitic turbellarian (Rhabdocoela: Pterastericolidae) from the Crown-of-Thorns starfish, Acanthaster planci. Memoirs of the Queensland Museum 18:179-183. CANNONL. R. G. 1979. Ecological observations on Cerithium moni&rum Kiener (Gastropoda: Cerithiidae) and its trematode parasites at Heron Island, Great Barrier Reef.

Austrulian Journul sf Marine and Frrshwatrr Reseurch 30: 365-374. CANNON L. R. G. 1982. Endosymbiotic umagillids (Turbellaria) from holothurians of the Great Barrier Reef. Zoologica Scripta 11: 173- 188. CANNON L. R. G. 1986a. The Pterastericolidae: parasitic turbellarians from starfish. In: Parasite Lives-Pupers on Parasites, their Hosts and their Associations to Honour J. F. A. Sprent (Edited by CREMIN M., DOBSONC. & M~~RHOVS~D. E.), pp. 15-32. University of Queensland Press, St. Lucia. CANNON L. R. G. 1986b. Turbellaria of the World-a Guide to Families and Genera. Queensland h;luseum. Brisbane. CANNON L. R. G. 1987. Two new rhabdocoel turbellarians. Umagilla pa&a sp. n. and U. karlingi sp. n. (Umagillidae), endosymbiotic with holothurians (Echinodermata) from the Great Barrier Reef, and a discussion of the sclerotic structures in the female system of the Umagillidae. Zoologicu Scripta 16: 297-303. CANNON L. R. G. & JENNINGS J. B. 1988. Monocystella epibatis n. sp., a new aseptate gregarine hyperparasite of rhabdocoel turbellarians parasitic in the Crown-of Thorns starfish, Acanthaster planci Linnaeus, from the Great Barrier Reef. Zeitschriftftir Parasitenkunde 136: 261-212. CANNON L. R. G. & LESTER R. J. G. 1988. On two turbellarians parasitic in fish. Diseases of Aquatic Organisms 5: 12-22. CANNON L. R. G. (in press) Anoplodium (Umagillidae: Rhabdocoela: Platyhelminthes) endosymbiotes from sea cucumbers from Australia and New Zealand. Zoologica Scriptu. EHLERS U. 1985. Das phylogenetische System der Plathelminthes. Gustav Fischer, Jena. G~GGIN C. L. & LESTER R. J. G. 1987. The occurrence of Perkinsus species (Protozoa: Apicomplexa) in bivalves on the Great Barrier Reef. Diseases of Aquatic Organisms 3: 113-117. GOGG~N C. L. & CANNON L. R. G. 1989. Occurrence of a turbellarian from Australian tridacnid clams. International Journalfor Parasitology 19: 345-346. GOGGIN C. L.. SEWELLK. B. & LESTER R. J. G. 1989. Cross infection experiments with Australian Perkinsus species. Diseases of Aquatic Organisms 7: 55-59. HWPER J. N. A. 1983. Parasites of estuarine and oceanic flathead fishes (Familv PlatvceDhahdae) from Northern New South Wales. -Austr&n Journal of Zoology, Supplementary Series 90: I-69. JENNINGSJ. B. & CANNON L. R. G. 1985. Observation of the occurrence, nutritional physiology and respiratory pigment of three species of flatworms (Rhabdocoela: Pterastericolidae) entosymbiotic in starfish from temperate & tropical waters. Opheliu 24: 199-215. JENNINGSJ. B. & CANNON L. R. G. 1987. The occurrence, spectral properties and probable role of haemoglobins in four species of entosymbiotic turbellarians (Rhabdocoela: Umagillidae). Ophelia 27: 143-154. LESTER R. J. G. 1980. Host-parasite relations in some didymozoid trematodes. Journal of Parasitology 66: 527531. LESTERR. J. G., BLAIR D. & HEALD D. 1980. Nematodes from scallops and turtles from Shark Bay, Western Australia. Australian Journal of Marine and Freshwater Research 31: 713-717. LESTERR. J. G. 1982. Unicapsulaseriolae n. sp. (Myxosporea, Multivalvulida) from Australian yellowtail kingfish Seriola lalaudi. Journal of Protozoology 29:584-587.

573

Marine parasitology in Australia LESTERR. J. G. 1984. A review of methods for estimating

mortality

due to parasites

in wild fish populations.

Helgoliinder Meeresuntersuchungen

37: 53-64.

LESTERR. J. G., BARNESA. & HABIBG. 1985. Parasites of skipjack tuna, Katsuwonus pelamis: fishery implications. Fishery Bulletin 831 343-356. LESTERR. J. G. 1986. Abalone die-back caused by protozoan infection? Australian Fisheries 45(6): 26-27.

LESTERR. J. G. & NEWMANL. J. 1986. First rediae and cercariae to be described from heteropods. Journal of Parasitology

12: 195-197.

LESTERR. J. G., SEWELL K. B., BARNES A. & EVANSK. 1988. Stock discrimination of orange roughy, Hoplostethus atlanticus, by parasite analysis. Marine Biology 99: 137143.

LESTERR. J. G. & SEWELL K. B. 1989. Checklist of parasites from Heron Island, Great Barrier Reef. Australian Journal ofzoology

Zeitschrift fiir Parasitenkunde

37: 101-128.

LESTERR. J. G., G~GG~NC. L. & SEWELLK. B. (in press) Perkinsus in Australia. In: Pathology in Marine Aquaculture (Edited by CHENGT. C. &PERKINSF. 0.). Academic Press, London. MOLNARK. & ROHDEK. 1988. Seven new coccidian species from marine fishes in Australia. Systematic Parasitology 11: 19-29. OWENSL. 1981. Relationships between some environmental parameters and trypanorhynch cestode loads in banana prawns (Penaeus merguiensis de Man). Australian Journal of Marine and Freshwater Research 32: 469-474. OWENSL. 1983. Bopyrid parasite Epipenaeon ingens Nobili as a biological marker for the banana prawn, Penaeus merguiensis de Man. Australian Journal of Marine and Freshwater Research 34: 47748 1. OWENS L. 1985. Polypocephalus sp. (Cestoda: Lecani-

cephalidae) as a biological marker for banana prawns, Penaeus merguiensis de Man, in the Gulf of Carpentaria. Australian Journal of Marine and Freshwater Research 36: 29 l-299. OWENSL. & GLAZEBR~CIK J. S. 1985. Sex determination in the Bopyridae. Journal of Parasitology 71: 134-135. OWENS L. 1987. A checklist of metazoan parasites from

Natantia (excluding the crustacean parasites of the Caridea). Journal of Shellfish Research 6: 117-124. OWENSL. & GLAZEBR~~K J. S. 1988. Microsporidiosis in prawns from northern Australia. Australian Journal of Marine and Freshwater Research 39: 301-305.

PHILLIPSW. J. & CANNONL. R. G. 1978. Ecological observations on the commercial sand crab, Portunus pelagicus (L.), and its parasite Sacculina granifera Boschma, 1973 (Cirripedia: Rhizocephala). Journal of Fish Diseases 1: 137-149. ROHDEK. 1973. Structure and development of Lobatostoma manteri sp. nov. (Trematoda, Aspidogastrea) from the Great Barrier Reef, Australia. Parasitology 66: 63-83. ROHDEK. & SANDLAND R. 1973. Host-parasite relations in Lobatostoma manteri Rohde (Trematoda, Aspidogastrea). Zeitschrifr ftir Parasitenkunde 41: 115-136. ROHDEK. 1975. Early development and pathogenesis of Lobatostoma manteri Rohde (Trematoda: Aspidogastrea). International Journalfor

the Australian east coast. Zeitschriftfir Parasitenkunde 51: 49-69. ROHDE K. 1977a. Species diversity of monogenean gill parasites of fish on the Great Barrier Reef. Proceedings of the Third International Coral Reef Symposium, Rosenstiel School of Marine and Atmospheric Science, University of Miami, pp. 585-591. ROHDEK. 1977b. A non-competitive mechanism responsible for restricting niches. Zoologischer Anzeiger 1991164172. ROHDE K. 1977~. The bird schistosome Austrobilharzia terrigalensis from the Great Barrier Reef, Australia. Zeitschrift ftir Parasitenkunde 52: 39-5 1. ROHDEK. 1977d. Habitat partitioning in Monogenea of marine fishes. Heteromicrocotyla australiensis, sp. nov. and Heteromicrocotyloides mirabilis, gen. and sp. nov. (Heteromicrocotylidae) on the gills of Carangoides emburyi (Carangidae) on the Great Barrier Reef, Australia.

Parasitology

5: 597-607.

ROHDEK. 1976a. Marine parasitology in Australia. Search 7: 477-482.

ROHDEK. 1976b. Species diversity of parasites on the Great Barrier Reef. Zeitschrift ftir Parasitenkunde SO: 93-94. ROHDE K. 1976c. Monogenean gill parasites of Scomberomorus commersoni La&p&de and other mackerel on

53: 171-182.

ROHDEK. 1978a. The bird schistosome Gigantobilharzia sp. in the silver gull, Larus novaehollandiae, a potential agent of schistosome dermatitis in Australia. Search 9: 4&42. ROHDEK. 1978b. Latitudinal differences in species diversity and their causes. I. A review of the hypotheses explaining the gradients. Biologisches Zentralblatt 97: 393403. ROHDEK. 1978~. Latitudinal gradients in species diversity and their causes. II. Marine parasitological evidence for a time hypothesis. Biologisches Zentralblatt 971405-418. ROHDEK. 1978d. Latitudinal differences in host specificity of marine Monogenea and Digenea. Marine Biology 47: 125134. ROHDEK. 1978e. Monogenea of Australian marine fishes. The genera Dionchus, Sibitrema and Hexostoma. Publications of the Seto Marine Biological Laboratory

24: 349-367.

ROHDEK. 1978f. Monogenean gill parasites of the kingfish, Seriola grandis Castlenau (Carangidae) from the Great Barrier Reef. Publications of the Seto Marine Biological Laboratory 24: 369-376. ROHDE K. 1979a. A critical evaluation

of intrinsic and extrinsic factors responsible for niche restriction in parasites. American Naturalist 114: 648-671. ROHDEK. 1979b. The buccal organ of some Monogenea Polyopisthocotylea. Zoologica Scripta 8: 161-170. ROHDEK. 1980a. Warum sind ijkologische Nischen begrenzt? Zwischenartlicher Antagonismus oder innerartlicher Zusammenhalt? Naturwissenschaftliche Rundschau 33: 98102.

ROHDEK. 1980b. Diversity gradients of marine Monogenea in the Atlantic and Pacific Oceans. Experientia 36: 13681369. ROHDEK. 198Oc. Host specificity indices of parasites and their application. Experientia 36: 1369-l 37 1. ROHDEK. 1980d. Some aspects of the ultrastructure of Gotocotyla secunda (Tripathi, 1954) (Monogenea: Gotocotylidae) and Hexostoma euthynni Meserve, 1938 (Monogenea: Hexostomatidae). Angewandte Parasitologie 21: 3248.

ROHDEK., ROUBALF. & HEWITTG. C. 1980. Ectoparasitic Monogenea, Digenea and Copepoda from the gills of some fishes of New Caledonia and New Zealand. New Zealand Journal of Marine and Freshwater Research 14: I-13. ROHDEK. 198la. Ultrastructure of the buccal organs and associated structures of Zeuxapta seriolae (Meserve, 1938) Price, 1962, and Paramicrocotyloides reticularis Rohde, 1978 (Monogenea, Polyopisthocotylea). Zoologischer Anzeiger 206: 279-291.

ROHDEK. 1981b. Niche width of parasites in species-rich and

574

K. ROHDE

species-poor communities. E.\-peri~ntia 37: 359-361. ROHDE K. 1981~. Population dynamics of two snail species, Plana.xis sulcatus and Cerithium monil$wm, and their trematode species at Heron Island. Great Barrier Reef. Oecologia 49: 344-352. ROHDE K. 198ld. Marine parasitology research at New England University. Australian Fisheries 40(2): 3 I. ROHDE K. 1982. Ecology of Marine Parasites. University of Queensland Press, St. Lucia. ROHDE K. 1984a. Ecology of marine parasites. Helgoliinder Meeresuntersuchungen 37: 5-33. ROHDE K. 1984b. Zoogeography of marine parasites. Helgo&tier Meeresuntersuchungen 37: 35-52. ROHDE K. 1984~. Helminth diseases of marine fishes. In Diseases of Marine Animals 4 (Edited by KINNE 0.). pp. 193-320, 435-501. Biologische Anstalt Helgoland, Hamburg. ROHDE K. 1985a. Increased viviparity of marine parasites at high latitudes. Hydrobiologia 127: 197-201. ROHDE K. 1985b. Some aspects of the zoogeography of marine parasites. New Zealand Journal of Zoology 13: 446. ROHDE K. & WATSON N. 1985a. Morphology and geographical variation of Pseudokuhnia minor n. g., n. comb. (Monogenea Polyopisthocotylea). International Journal ,for Parasitology 15: 557-567. ROHDE K. &WATSON N. 1985b. Morphology, microhabitats and geographical variation of Kuhnia spp. (Monogenea Polyopisthocotylea). International Journal for Parasitology 15: 569-586. ROHDE K. 1986a. Differences in species diversity of Monogenea between the Pacific and Atlantic Oceans. HJadrobiologia 137: 21-28. ROHDE K. 1986b. Marine parasitology in Australia. Purasitology Today 2: 520. ROHDE K. 1986c. Ultrastructure of the pharynx and some parenchyma cells of Zeuxapta seriolae and Paramicrocotyloides reticularis (Monogenea, Polyopisthocotylea. Microcotylidae). Australian Journal of Zoology 34: 47348 1. ROHDE K. & HOBBS R. P. 1986. Species segregation: competition or reinforcement of reproductive barriers? In: Parasite Lives-Papers on Parasites, their Hosts and their Associations to Honour J. F. A. Sprent (Edited by CREMIN M., DOBSON C. & MOORHOUSE D. E.). pp. 189-199. University of Queensland Press, St. Lucia. ROHDE K. 1987a. Grubea australis n. sp. (Monogenea. Polyopisthocotylea) from Scomber australasicus in southeastern Australia, and Gruhea cochlear Diesing, 1858 from S. scombrus and S. japonicus in the Mediterranean and western Atlantic. Systematic Parasitology 9: 29-38. ROHDE K. 1987b. Different populations of Scomber australasicus in New Zealand and southeastern Australia, demonstrated by a simple method using monogenean sclerites. Journal of Fish Biology 30: 65 l-657. ROHDE K. & WILLIAMSA. 1987. Taxonomy of monogeneans of deep sea fishes in southeastern Australia. Systematic Parasitology 10: 45-7 I. ROHDE K. 1988a. Gill Monogenea of deepwater and surface fish in southeastern Australia. Hydrobiologia 16: 271-283. ROHDE K. 1988b. Phylogenetic relationship of free-living and parasitic Platyhelminthes on the basis of ultrastructural evidence. Fortschritte der Zoologie (Progress in Zoology) 36: 353-357. ROHDE K. & HOBBS R. 1988. Rarity in marine Monogenea. Does an Allee-effect or parasite-induced mortality explain truncated frequency distributions? Biologisches Zentralblatt 107: 327-338.

ROHDE K. & WATSON N. 1988. Ultrastructure of epidermis and sperm of Swdis~rinx punicea (Hickman, 1956) (Rhabdocoela, Umaglllidae). Australian Journal q/ Zoology 36: 131-139. ROHDE K.. WATSON N. & CANNON L. R. G. 1988. Comparative ultrastructural studies of the epidermis, sperm and nerve fibres of Cleistogamia longicirrus and Seritia stichopi (Rhabdocoela, Umagillidae). Zoologica Scripta 17: 337345. ROHDE K. 1989a. Simple ecological systems, simple solutions to complex problems? Evolutionary Theory 8: 305-350. ROHDE K. 1989b. Kuhnia sprostonae Price, 1961 and K. scombercolias Nasir & Fuentes Zambrano, 1983 (Monogenea: Mazocraeidae) and their microhabitats on the gills of Scomber australasicus (Teleostei: Scombridae), and the geographical distribution of seven species of gill Monogenea of Scomher spp. Systematic Parasitology 14: 93-100. ROHDE K. 1989~. At least eight types of sense receptors in an endoparasitic flatworm: a counter-trend to sacculinization. Naturwissenschafien 76: 383-385. ROHDE K. 1989d. Ultrastructure of the protonephridial system of Lobatostoma manteri(Trematoda, Aspidogastrea). Journal of Submicroscopic Cytology and Pathology 21: 599-610. ROHDE K., JUSTINEJ.-L. &WATSON N. 1989. Ultrastructure of the flame bulbs of the monopisthocotylean Monogenea Loimosina wilsoni(Loimoidea) and Calceostoma herculanea (Calceostomatidae). Annales de Parasitologic Humaine et ComparPe 64: 433442. ROHDE K. & WATSON N. 1989a. Sense receptors in Lobatostoma manteri (Trematoda, Aspidogastrea). International Journal,for Parasitology 19: 847-858. ROHDE K. & WATSON N. 1989b. Ultrastructure of the marginal glands of Lohatostoma manteri (Trematoda. Aspidogastrea). Zoologischer Anzeiger 223: 301-3 10. ROHDE K.. WATSON N. and ROULIALF. 1989a. Ultrastructure of flame bulbs, sense receptors, tegument and sperm of Udonella (Platyhelminthes) and the phylogenetic position of the genus. Zoologischer Anzeiger 222: 143-157. ROHDE K., WATSONN. & ROVEAL F. 1989b. Ultrastructure of the protonephridial system of Dactylogyrus sp. and an unidentified ancyrocephaline (Monogenea. Dactylogyridae). International Journalfor Parasitology 19: 859-864. ROUBAL F. R. 198 I. The taxonomy and site specificity of the metazoan ectoparasites on the black bream. Acanthopagrus australis (Giinther), in northern New South Wales. Australian Journal of Zoology (Supplementary Series) 84: I-100. ROUBAL F. R.. ARMI~AGEJ. & ROHDE K. 1983. Taxonomy of metazoan ectoparasites of snapper, Chrysophrys auratus (Family Sparidae), from southern Australia, eastern Australia and New Zealand. Australian Journal of Zoology (Supplementary Series) 94: l-68. ROUBALF. R. 1986a. Studies on monogeneans and copepods parasitizing the gills of a sparid (Acanthopagrus ausfralis (Giinther)) in northern New South Wales. Canadian Journal of Zoology 64: 841-849. ROUBALF. R. 1986b. Blood and other possible inflammatory cells in the sparid, Acanthopugrus australis (Giinther). Journal of Fish Biology 28: 573-593. ROUBAL F. R. 1986~. Histopathology of the leech, Austrobdella bilobota, on the yellowfin bream. Acanthopagrus australis (family Sparidae) in northern New South Wales. Journal of Fish Diseases 9: 2 13-223. ROUBAL F. R. 1986d. The histopathology of the copepod. Ergasilus lizae Kroyer. on the pseudobranchs ofthe teleost.

515

Marine parasitology in Australia Acanchopugrus australis (Gunther) Zoologischer Anzeiger 211: 65-14.

(family Sparidae).

ROULIALF.

R. 1987a. Gill surface area and its components in the yellowfin bream Acanthopagrus australis (Gunther) (Pisces: Sparidae). Australian JournalofZoology35: 25-34. ROLIBALF. R. 1987b. Comparison of ectoparasite pathology on the gills of Acanthopagrus australis (Gunther) (Pisces: Sparidae): a surface area approach. Australian Journal of

and observations on Grillotia brunchi n. sp., a larval trypanorhynch from the Spanish mackerel Scomberomorus commerson. Systematic

Parasitology

4: l-6.

J. G. 1989. Studies on

SMITHP. J. 1986. Genetic similarity between samples of the orange roughy Hoplostethus atlanticus from the Tasman Sea, South-west Pacific Ocean and North-east Atlantic Ocean. Marine Biology 91: 173-180. SPEAREP. 1988. Parasites of the pacific sailfish, Zstiophorus plucypterus: a preliminary investigation of their usefulness in stock discrimination. Proceedings of the International Billfish Symposium II, Hawaii. SPRENTJ. F. A. 1990. Some ascaridoid nematodes of fishes: Paranisakis and Mawsonascaris ng. Systematic Parasitology 15:41-63. WILLIAMS A. 1986. Taxonomy of two new species of Heterobothrium (Monogenea: Diclidophoridae) from Torquigener pleurogramma (Pisces: Tetradontidae) from Western Australia. Australian Journal of Zoology 34: 707-7 15. WILLIAMS A. 1988. Three new species of monogeneans of the family Mazocraeidae from clupeiform fishes in the Swan River estuary, Western Australia. Systematic Parasitology

Marteilia sydneyi, agent of QX disease in the Sydney rock oyster Saccostrea commercialis, with implications for its life cycle. Australian Journal of Marine and Freshwater Research 40: 155-167.

WILLIAMS A. & BEVERLEY-BURTON M. 1989. Redescription of three species of the genus Encotyllabe (Capsalidae: Monogenea) from fishes of the east coast of Australia.

Zoology 35: 93-100. ROUBAL F.

R. & LESTERR. J. G. 1987. New test developed for QX parasite in oysters. Australian Fisheries 46(10): 38. ROUBALF. R. 1989a. Comparative pathology of some monogenean and copepod ectoparasites on the gills of Acanthopagrus australis (family Sparidae). Journal of Fish Biology 34: 503-514.

ROUBALF. R. 1989b. Pathological changes in the gill filaments of Acanthopugrus australis (family Sparidae) associated with post-settlement growth of a lernaeopodid copepod, Alella macrotrachelus. Journal of Fish Biology 34: 333-342.

ROUBALF. R.,

MASEL J. & LESTERR.

SEDLAK-WEINSTEINE.

(in press) Three new records ofcyamids from Australian cetaceans. Crustaceuno. SEWELLK. B. & LESTERR. J. G. 1988. The Numbers of Selected Parasites in Australian and New Zealand Samples of Orange Roughy, Hoplostethus atlanticus, 1983-1986.

Technical Report 26, Department of Sea Fisheries, Tasmania Marine Laboratories, Crayfish Point, Taroona, Australia. SHAHAROMF. M. & LESTERR. J. G. 1982. Description of Note added in proof

After this review was sent to Press the author received a Special Issue of the Australian Journal of Zoology containing fourteen papers on Marine Parasites from the southern Great Barrier Reef. REFERENCE Australian Journal of Zoology 31: l-142 (1989).

12: 93-104.

Austrahan Journal of Zoology 31: 45-53.

WILLIAMS J. B. 1988a. Ultrastructural studies on Kronborgia (Platyhelminthes: Neoophora): the spermatozoon. In&= national Journalfor

Parasitology

18: 477-483.

WILLIAMS J. B. 1988b. Further observations on Kronborgia isopodicola, with notes on the systematics of the Fecampiidae (Turbellaria: Rhabdocoela). New) Zealand Journal of Zoology 15: 2 1l-22 1.