Craig J. Hayward

Aspects of the ecology of metazoan ectoparasites of marine fishes

Numerous (3947) individuals of 102 marine fish species from Papua New Guinea, New Zealand, the North Sea, Antarctica, the deepsea and coast of southeastern Australia, Pacific Canada, Brazil, Argentina and the Great Barrier Reef were examined for metazoan ectoparasites. Of the 102 fish species, 86 harboured at least 1 parasite species, and only in Antarctica and the deepsea were large proportions of fish species found to be free of ectoparasites. The mean prevalence of infection was 30.1%, the average of abundances was 6.7 parasites per fish, due to very heavy intensities of some parasite species (mean median abundance 4.31). Most parasite species exhibited a clustered distribution in the host populations, as measured by variance to mean ratios, i.e. some fish were more, and others less, heavily infected than if infection were random. Core and satellite species cannot be distinguished unambiguously, because numbers of parasites on almost all hosts are too small for any bimodality to become apparent. On average, the most dominant species represented 90% of all parasite individuals of a particular fish; different parasite species were often dominant on different fish individuals of a particular host species. Both abundances and maximum intensities of infection were positively correlated with prevalence of infection. Community richness varies greatly at and between localities, with the lowest richness found in Antarctic and deepsea fish and the highest richness in tropical fish. Species richness, abundance and prevalence of infection in many fish groups (with different ecological characteristics) are strongly correlated with temperature. If fish from all localities were pooled, pelagic fish had fewer intensities and (jointly with benthopelagic fishes) fewer species than benthic fish, and planktivorous fish had lower abundances and prevalences of infection than predatory and omnivorous fish. Prevalences of infection, abundance and parasite species richness were significantly correlated with host length. Fifteen positive and 1 negative associations among species were found. This and the generally low prevalences and abundances of infection indicate that competitive interactions are probably scarce. Overall, the findings indicate that most (if not all) metazoan ectoparasite communities of marine fish live in non-saturated, little-ordered assemblages.

The life cycle of Cardicola forsteri (Trematoda: Aporocotylidae), a pathogen of ranched southern bluefin tuna, Thunnus maccoyi

Aporocotylids (fish blood flukes) are emerging as pathogens of fishes in both marine and freshwater aquaculture. Efforts to control these parasites are hampered by a lack of life cycle information. Here we report on the life cycle of Cardicola forsteri, which is considered a significant pathogen in southern bluefin tuna, Thunnus maccoyi, ranched in South Australia. We surveyed polychaetes, bivalves and gastropods from sites close to tuna pontoons. Infections consistent with the Aporocotylidae were found in terebellid polychaetes, a single Longicarpus modestus and five individuals of Reterebella aloba. All infections were comprised of hundreds of sporocysts in the body cavity of the host, each filled with developing and mature cercariae. Sequences of ITS-2 and lsrDNA from the infection from L. modestus were a perfect match with those of adult C. forsteri from T. maccoyi. This life cycle link is considered confirmed but it is possible that additional terebellid species are infected in South Australia; equally, other species of intermediate host are likely to be involved in other parts of the range of this cosmopolitan trematode. Sequences of the species from R. aloba did not match a known adult but phylogenetic analysis of lsrDNA suggests that it is also a species of Cardicola Short, 1953. These findings show that terebellid polychaetes are a major host group for marine aporocotylids, especially given that Cardicola is the largest marine aporocotylid genus. The two cercarial types are among the smallest known for the family and are unusual, but not unique, in having short, simple tails. We speculate that the form of the tail means that these cercariae are not active swimmers and are thus heavily dependent on currents for dispersal. Control of this parasite might be effected by moving the tuna pontoons appropriate distances to avoid encounter with current-dispersed cercariae, or by increasing the separation of the nets from the sea floor, either by raising the nets or moving to deeper water.

A tropical assemblage of ectoparasites: Gill and head parasites of Lethrinus miniatus (Teleostei, Lethrinidae)

Aspects of the community ecology of metazoan ectoparasites of Lethrinus miniatus (Teleostei. Lethrinidae) from 3 localities on the Great Barrier Reef were examined. Twelve species of Monogenea, 6 of Copepoda, 2 species of adult and several larval Isopoda and 1 leech were found. Total parasite numbers reach 3500 per host, and prevalence of infection with a particular parasite species reached 100% in some species. Numbers of parasite species per fish varied from 5 to 11. Four parasite species were most dominant on different fish if intensities of infection were used to calculate dominance, one species representing about 80% of all parasite individuals on a particular fish at 2 localities and about 50% at the third locality. Ten parasite species were most dominant on different fish, if volume (biomass) was used for calculating dominance, one species representing about 55% at one and 80% of total parasite volume at 2 localities. Parasites included at least 12 congeneric species of 4 or more genera, and those (of 2 genera) occurring on the gills showed much overlap in their distribution. Congeneric Monogenea of the families Dactylogyridae and Diplectanidae occurring in the same sites differ markedly in the size and structure of their copulatory sclerites. Positive associations between species were much more common than negative ones. The bony parts of the gills (gill arches) were never found to be infected, indicating the availability of empty niches.

Global spread of the eel parasite Gyrodactylus anguillae (Monogenea)

Gyrodactylus anguillae is known from four continents, and intraspecific variation in the morphology of specimens from each continent is negligible. However, morphological characters alone may not always be adequate for recognizing populations that have been isolated geographically over evolutionary time. We were unable to obtain specimens from Northeast Asia, but G. anguillae collected from North America, Europe and Australia had identical ribosomal DNA sequences (ITS1-5.8SrRNA-ITS2 region). This lack of even minor genetic variation in populations from three remote continents leads us to conclude that they share a contemporary common ancestor. This is one of at least five pests of eels to have invaded new continents as a result of the eel trade in the last four decades; these other known eel pests include Pseudodactylogyrus spp. (Monogenea) and Anguillicola spp. (Nematoda). Their dispersal has probably been secondarily augmented by longshore migration of infected eels, and perhaps also by transportation in ballast waters. The only other known gyrodactylid from eel gills, G. nipponensis from Japanese eel, is not closely related to G. anguillae, because the ITS1 region of the former is short (370 bases) and that of the latter long (685 bases). G. anguillae probably originated in Europe, because it was recorded there over 40 years ago, before the development of the international eel trade. We predict that the worm has a high potential to invade eel populations in East Africa, Southeast Asia, and New Zealand.

Nematode worm infections (Camallanus cotti, Camallanidae) in guppies (Poecilia reticulata) imported to Korea

Abstract Camallanus cotti [Jpn. J. Zool. 1(1927) 169] is a common intestinal nematode parasite of guppies. It was first reported from several kinds of freshwater fishes in Japan in 1927, and is thought to be native to continental Asia, from Japan westwards, perhaps extending as far as the Nile delta. Because of the worldwide trade in aquarium fishes, it is now found in many fishes in several continents. Guppies are one of the most popular tropical pet fishes in Korea. Here we report C. cotti infection of cultured guppies in Korea, originally imported from Indonesia, for the first time. In a tropical fish farm, mortality reached up to 30% and most guppies did not show any clinical signs except in heavily infected fish, in which worms were extruded from the anus. Prevalence of infection was 71% (59/83 fish), and there was no preference for host sex (34 of 45 female fish and 25 of 38 male fish). Although we found C. cotti in dead guppies, we could not conclude that C. cotti infection was the cause of death, because some fish died without C. cotti infection. In addition, we detected high numbers of the histophagous ciliate, Tetrahymena corlissi (Thompson, 1955) in these fish. We suspect that both C. cotti and T. corlissi infections contributed to death, but more detailed studies are required.

Assemblages of ectoparasites of a pelagic fish, slimy mackerel (Scomber australasicus), from south-eastern Australia

Four-hundred and fifty-three Scomber australasicus, ranging in length from 14.1 to 46.5 cm and taken in 12 samples over 5 years from a single locality in south-eastern Australia, were examined. Ten species of ectoparasites were recorded: six monogeneans, three copepods and one isopod. The maximum number of parasite species in any one fish reached five, and the maximum total parasite intensity reached 39. Host size is an important determinant of the structure of ectoparasite assemblages of slimy mackerel: the average number of species per host peaked at 2.2 in fishes between 20 and 25 cm in length, then declined in larger fish; the abundance of all parasites on each fish similarly peaked in fishes 20-25 cm (mean of 9.9). The monogenean Pseudokuhnia minor had the highest prevalence and abundance of all parasites, infecting almost 80% of fish < 25 cm long. Over half of the total number of parasites belonged to this species, and it was dominant in intensity in just over half of the fish in which it occurred. When approximate volume was considered, assemblages were dominated by Kuhnia scombercolias in fish < 20 cm, by Kuhnia scombri in fish 20-34.9 cm, and by P. minor in fish larger than 35 cm long. The intensities of these three monogeneans were very strongly and positively correlated with each other, as were the intensities of P. minor and Grubea australis; the intensities of only one pair of species were associated negatively (K. scombercolias and the isopod Ceratothoa imbricata). A nested subset analysis indicates that the ectoparasite assemblages are random. This and the low prevalences and abundances of infection, as well as low species richness per fish, indicate that infra-assemblages are isolationist.

Order in ectoparasite communities of marine fish is explained by epidemiological processes.

Two kinds of community structure referred to, nestedness and bimodal distribution, have been observed or were searched for in parasite communities. We investigate here the relation between these two kinds of organisation, using marine fishes as a model, in order to show that parasite population dynamics may parsimoniously explain the patterns of ectoparasite species distribution and abundance. Thirty six assemblages of metazoan ectoparasites on the gills and heads of marine fish showed the following patterns: a positive relationship between abundance and the variance of abundance; a positive relationship between abundance and prevalence of infection; a bimodal pattern of the frequency distribution of prevalence of infection; nestedness as indicated by Atmar and Pattersons thermodynamic measure (a mean of 7.9 degrees C); a unimodal distribution of prevalence in parasite assemblages with a temperature lower than the mean, and a bimodal distribution in assemblages with a temperature higher than the mean. We conclude that patterns are the result of characteristics of the parasite species themselves and that interspecific competition is not necessary to explain them. We emphasize that a holistic approach, taking all evidence jointly into account, is necessary to explain patterns of community structure. Ectoparasite assemblages of marine fish are among the animal groups that have been most thoroughly examined using many different methods, and all evidence supports the view that these animals live under non-equilibrium conditions, in largely non-saturated niche space in which interspecific competition occurs but is of little evolutionary importance.

Effects of immunostimulants on ranched southern bluefin tuna Thunnus maccoyii : immune response, health and performance

Ranched southern bluefin tuna Thunnus maccoyii were fed baitfishes supplemented with vitamins (predominantly E and C) or vitamins and immunostimulants, nucleotides and β-glucans, over 12 weeks after transfer and monitored for enhancement in immune response, health and performance through their 19 week grow-out period. Fish from two different tows were sampled separately at three different sampling points: at transfer to grow-out pontoons, at 8 weeks post-transfer and at harvest, 19 weeks post-transfer. Lysozyme activity was enhanced during vitamin supplementation compared to control fish. Performance (i.e. survival, condition index and crude fat), health (i.e. blood plasma variables including pH, osmolality, cortisol, lactate and glucose) and alternative complement activity were not commonly improved through diet supplementation. There were some tow-specific improvements in performance through vitamin supplementation including survival, selected parasite prevalence and intensity, and alternative complement activity. Immunostimulant supplementation also showed a tow-specific improvement in plasma cortisol level. Tow-specific responses may suggest that life history, previous health condition and husbandry can affect the success of vitamin and immunostimulant enhancement of immune response, health and performance of ranched T. maccoyii.

Oceanic barriers as indicated by scombrid fishes and their parasites

Four genera of scombrid fishes (26 species) and their copepod (32 species) and monogenean ectoparasites (25 species) were used to test the hypothesis that the East Pacific Barrier is responsible for the most pronounced break in the circum-tropical warm water fauna of the continental shelves, and not the New World Barrier. Analysis at the species level showed that there is a primary centre of diversity in the West Pacific, and a secondary centre in the West Atlantic. The former, almost entirely, shares its species of the largely coastal Scomberomorus and Grammatorcynus and their parasites with seas located to the west. Only four parasites (all copepods) are shared by the East and West Pacific, and they are circum-tropical. In contrast, the West Pacific shares species of the more pelagic Scomber and their parasites with seas both to the east and west, although at the genus level, only two circum-tropical monogenean genera are shared by the E and W Pacific. We conclude that the East Pacific Barrier has been a 100% or almost 100% effective barrier to dispersal of species of Scomberomorus, Grammatorcynus and their parasites, whereas for species of Scomber and their parasites, the East Pacific has been a less effective barrier.

Epizootics of metazoan gill parasites did not threaten feasibility of farming southern bluefin tuna ( Thunnus maccoyii ) in a trial extending over summer months

Tuna farming off Port Lincoln, Australia, involves catching wild 2-4-year-old southern bluefin tuna in summer and then fattening for periods of 2-8 months. As fresh product is not available year-round, the feasibility of maintaining tuna for longer periods was trialled, including over a summer season, when temperatures may exceed 24 degrees C. As the rates of growth and reproduction in ectoparasites of fishes are usually most rapid during warm temperatures, parasite epizootics at this time may adversely affect the health of tuna. We collected epidemiological data on burdens of metazoans on the gills of tuna from the time of stocking in April 2005 through to final harvest in August 2006 (N=220). We document an epizootic of the copepod Pseudocycnus appendiculatus, characterised by a significant increase in both prevalence and mean intensity in the first winter, followed by a decline in these parameters over the next 12 months. This epizootic pattern appears to be independent of seasonal changes in temperature. For two other species, a second copepod (Euryphorus brachypterus) and a polyopisthocotylean flatworm (Hexostoma thynni), there were no clearly discernible trends in infections. As the high water temperatures over the summer period did not lead to increased infections of any species of gill parasites, we conclude that they do not threaten the feasibility of farming of Thunnus maccoyii.