Harry W. Palm

The life cycle of Anisakis simplex in the Norwegian Deep (northern North Sea)

Copepoda (Calanus finmarchicus n=1,722, Paraeuchaeta norvegica n=1,955), Hyperiidae (n=3,019), Euphausiacea (Meganyctiphanes norvegica n=4,780), and the fishes Maurolicus muelleri (n=500) and Pollachius virens (n=33) were collected in the Norwegian Deep (northern North Sea) during summer 2001 to examine the importance of pelagic invertebrates and vertebrates as hosts of Anisakis simplex and their roles in the transfer of this nematode to its final hosts (Cetaceans). Third stage larvae (L3) of A. simplex were found in P. norvegica, M. muelleri and P. virens. The prevalence of A. simplex in dissected P. norvegica was 0.26%, with an intensity of 1. Prevalences in M. muelleri and P. virens were 49.6% and 100.0%, with mean intensities of 1.1–2.6 (total fish length ≥6.0–7.2) and 193.6, respectively. All specimens of C. finmarchicus and M. norvegica examined were free of anisakid nematode species and no other parasites were detected. P. norvegica, which harboured the third stage larvae, is the obligatory first intermediate host of A. simplex in the investigated area. Though there was no apparent development of larvae in M. muelleri, this fish can be considered as the obligatory second intermediate host of A. simplex in the Norwegian Deep. However, it is unlikely that the larva from P. norvegica can be successfully transmitted into the cetacean or pinniped final hosts, where they reach the adult stage. An additional growth phase and a second intermediate host is the next phase in the life cycle. Larger predators such as P. virens serve as paratenic hosts, accumulating the already infective stage from M. muelleri. The oceanic life cycle of A. simplex in the Norwegian Deep is very different in terms of hosts and proposed life cycle patterns of A. simplex from other regions, involving only a few intermediate hosts. In contrast to earlier suggestions, euphausiids have no importance at all for the successful transmission of A. simplex in the Norwegian Deep. This demonstrates that this nematode is able to select definite host species depending on the locality, apparently having a very low level of host specificity. This could explain the wide range of different hosts that have been recorded for this species, and can be seen as the reason for the success of this parasite in reaching its marine mammal final hosts in an oceanic environment.

Evolution of the trypanorhynch tapeworms: Parasite phylogeny supports independent lineages of sharks and rays

Trypanorhynch tapeworms (Platyhelminthes: Cestoda) are among the most diverse and abundant groups of metazoan parasites of elasmobranchs and are a ubiquitous part of the marine food webs that include these apex predators. Here we present a comprehensive analysis of their phylogeny, character evolution and host associations based on 10years of sampling effort, including representatives of 12 of 15 and 44 of 66 currently recognized trypanorhynch families and genera, respectively. Using a combination of ssrDNA and lsrDNA (Domains 1-3) for 79 and 80 taxa, respectively, we maintain one-to-one correspondence between molecules and morphology by scoring 45 characters from the same specimens used for sequencing, and provide museum vouchers for this material. Host associations are examined through likelihood-based ancestral character state reconstructions (ACSRs) and by estimating dates of divergence using strict and relaxed molecular clock models in a Bayesian context. Maximum parsimony and Bayesian inference analyses of rDNA produced well-resolved and strongly supported trees in which the trypanorhynchs formed two primary lineages and were monophyletic with respect to the diphyllidean outgroup taxa. These lineages showed marked differences in their rates of divergence which in turn resulted in differing support and stability characteristics within the lineages. Mapping of morphological characters onto the tree resulting from combined analysis of rDNA showed most traits to be highly plastic, including some previously considered of key taxonomic importance such as underlying symmetries in tentacular armature. The resulting tree was found to be congruent with the most recent morphologically based superfamily designations in the order, providing support for four proposed superfamilies, but not for the Tentacularioidea and Eutetrarhynchoidea. ACSRs based on the combined analysis of rDNA estimated the original hosts of the two primary parasite lineages to be alternatively rajiform batoids and carcharhiniform sharks. This fundamental split provides independent support for rejecting the notion that rays are derived sharks, and thus supports the most recent molecular phylogenies of the Neoselachii. Beyond the basal split between shark- and ray-inhabiting lineages, no pattern was found to suggest that the trypanorhynchs have closely tracked the evolutionary histories of these host lineages, but instead, it appears that host-switching has been common and that the subsequent evolution of the parasites has been ecologically driven primarily through overlap in the niches of their shark and ray hosts. Using a relaxed molecular clock model calibrated by means of host fossil data, the ray-inhabiting lineage is estimated to have diversified around the Jurassic-Cretaceous boundary, whereas the shark-inhabiting lineage is estimated to have diversified later, in the Middle Cretaceous. Although the large error associated with the estimated divergence dates prevents robust conclusions from being drawn, the dates are nevertheless found to be consistent in a relative sense with the origins of their major hosts groups. The erection and definition of the suborders Trypanobatoida and Trypanoselachoida, for the major clades of trypanorhynchs parasitizing primarily rays and sharks, respectively, is proposed for the two primary lineages recovered here.

Ecology of Pseudoterranova decipiens (Krabbe, 1878) (Nematoda: Anisakidae) from Antarctic waters

Abstract The present study provides further data on the occurrence of Pseudoterranova decipiens in fish from two different sampling sites in the Antarctic. A total of 690 fish belonging to 33 species from the eastern Weddell Sea and 322 fish belonging to 12 species from the South Shetland Islands were examined. Altogether, 23 fish species were found to be infested and 11 new host records could be established. P. decipiens occurred at a water depth of between 80 and 820 m. Chaenocephalus aceratus and Notothenia coriiceps from the South Shetland Islands were the species with the highest prevalence (95%) and intensity (2–194 and 1–121, respectively) of infestation. Both are transport hosts, which mainly feed on benthic nototheniid fish species and accumulate the nematodes. Bathypelagic, pelagic, or mainly euphausid feeding fish species were only lightly infested, if at all. This demonstrates the benthic life cycle of P. decipiens in the Antarctic. The preferred site of infestation was the body cavity and the liver; no specimen could be isolated from the fish musculature. This might be explained by the low water temperatures. The infestation of fish from the Weddell Sea was distinctly lower than that of fish around the South Shetland Islands. Besides possible differences in final host populations at the two localities studied, the loss of eggs and larvae under the eastern Weddell Sea shelf ice and over the continental slope and differences in the availability of the first intermediate and macroinvertebrate hosts led to a lower level of infestation. Another role, although nondecisive, may be played by the reduced time of development and infectivity of eggs and larvae, respectively, in the extremely cold waters of the Weddell Sea. P. decipiens is not a rare but, rather a well-established parasite of the Antarctic fauna, which demonstrates the ability of this cosmopolitan species to complete its life cycle even under conditions of subzero temperatures.

Seasonal dynamics of Trichodina spp. on whiting (Merlangius merlangus) in relation to organic pollution on the eastern Black Sea coast of Turkey

It was determined that there is a relationship between prevalence and mean densities of Trichodina spp. on Merlangius merlangus and organic pollution, measured as levels of nitrite, nitrate and phosphate in the surrounding environment. Monthly, two left anterior gill arcs of 60 M. merlangus (unless otherwise stated) captured with hook and line were fixed in 10% formalin. The number of Trichodina spp. was determined by counting all of the cells with a grid slide. The two right anterior gill arcs were used to prepare dry smears to picture the morphology of the trichodinids and to determine species composition. High levels of prevalence and densities of the protozoan were observed during the late fall, winter and early spring months. Then, prevalence decreased to lower levels but never below 60%, an indication of the important role of M. merlangus for Trichodina spp. in the studied region. A multivariate analysis revealed that the magnitude of prevalence was related to the level of all three parameters: nitrite, nitrate and phosphate (r2=0.59). However, a much stronger relationship between prevalence and nitrate, phosphate, oxygen and temperature (r2=0.89) was detected. Consequently, the seasonal parasite prevalence and density were affected by organic pollution. The timing for a high prevalence and mean densities of this parasite also suggests that primary production may be responsible for the observed seasonal variation in prevalence and mean densities. By using the model describing the relationship between the water quality parameters and the prevalence data of Trichodina spp. recalculated values and observed field data corresponded closely.

Preliminary cladistic analysis of genera of the cestode order Trypanorhyncha Diesing, 1863

A preliminary cladistic analysis was carried out on the 49 currently recognised genera of the order Trypanorhyncha. Forty-four characters were analysed; a functional outgroup was used for scolex and strobilar characters, while Nybelinia was utilised to polarise characters related to the rhyncheal system. Eight well-resolved clades were evident in the resultant cladogram, which is compared with existing phenetic classifications. An analysis of families resulted in a similar clustering of taxa to that observed in the case of the genera. The results suggest that two key characters used in existing classifications, namely the presence of sensory fossettes on the bothridia and the development of atypical heteroacanth and poeciloacanth armatures from typical heteroacanth armatures, have occurred on several occasions. Some clades provide support for the arrangements used in current classifications. Suggestions are made for future avenues of research which might provide more robust phylogenetic data for the Trypanorhyncha.

Anisakid Nematode (Ascaridoidea) Life Cycles and Distribution: Increasing Zoonotic Potential in the Time of Climate Change?

Parasitic nematodes are known as important pathogens that cause problems for human and animal health. Some of them naturally inhabit the marine environment, where they are widespread and can be found in a variety of different hosts. Food-borne zoonoses via aquatic animals are most often linked to anisakid nematodes of the genera Anisakis Dujardin, 1845, Contracaecum Railliet and Henry, 1912, and Pseudoterranova Mozgovoi, 1951. These are commonly found in the digestive tract of marine mammals, and infect aquatic invertebrates and vertebrates as intermediate hosts. The most widely distributed whale worms Anisakis spp. involve cetaceans as final and planktonic copepods, euphausiids, squids and teleosts as intermediate or paratenic hosts. Painful infections of the digestive tract in humans originate through consumption of raw or semi-raw fisheries products, for example fish and squid. Recent molecular studies revealed the existence of morphologically similar but genetically different cryptic species (‘sibling species’) within the anisakids. Among these, A. simplex (s.s.) is responsible for the highest number of recorded human infections. Molecular studies of Anisakis larvae from various parts of the world Oceans demonstrate an uneven species distribution, with A. simplex (s.s.) being limited to the northern hemisphere. Another species, A. typica, has not yet been connected to this disease, and seems to be restricted to the tropical regions. This chapter presents the present state of knowledge about this widespread group of fish parasites, including the importance as human pathogens, their life cycle biology, biogeography and phylogeny. The distribution of the currently recognized Anisakis species is summarized and combined with the number of known cases of human anisakiasis. We suggest that pathogenicity for humans is different among the Anisakis siblings, providing a possible explanation for uneven disease records worldwide. The possibility of a changing risk of anisakidosis in the time of climate change is discussed.

Occurrence of trichodinid ciliates (Peritricha : Urceolariidae) in the Kiel Fjord, Baltic Sea, and its possible use as a biological indicator.

Abstract Investigations on the occurrence of trichodinid ciliates from fish caught in the Kiel Bight and Kiel Fjord (western Baltic Sea) were carried out between September 1996 and March 1997. Smears of the gills, fins, and skin of 120 Gadus morhua and 92 Platichthys flesus caught by fish traps and trammel nets revealed the presence of trichodinid ciliates. According to the fish species and locality, different prevalences and densities of trichodinid ciliates were found. Fish caught in the Kiel Bight revealed a lower prevalence of trichodinid ciliates on their gills (P. flesus 74.2%, G. morhua 3.8%) in comparison with fish of the same species and size caught in the Kiel Fjord (P. flesus 75.0%, G. morhua 26.2%). In both areas, P. flesus was more heavily infested than G. morhua. Seasonal changes in the prevalence of infestation of P. flesus between autumn and winter in the Kiel Fjord are proposed to be linked to an increase in bacterial biomass during winter. The fish ecology in combination with the total number of bacteria in the fish environment is discussed as an important factor influencing the abundance of trichodinid ciliates. The present data suggest the use of trichodinid ciliates as an indicator for eutrophication in brackish-water environments.

The role of the rock cod Notothenia coriiceps Richardson, 1844 in the life-cycle of Antarctic parasites

Abstract Fifty specimens of Notothenia coriiceps caught in Potter Cove, King George Island, were examined for ecto- and endoparasites. Of the 22 parasite species found, 18 were helminths, 2 were hirudineans and 2 were crustaceans. The isopod Aega antarctica and an unidentified hirudinean are reported for the first time from this fish host. Dominant parasites were the adults of Aspersentis megarhynchus, the invasive stage of Corynosoma spp. (cystacanth) and the adults of Macvicaria pennelli, with respective prevalences of infestation of 94, 76 and 74%. The preferred sites of infestation were the pylorus and intestine, where five different larval (nematodes and cestodes) and eight adult (digeneans and acanthocephalans) parasite species were found. No adult nematodes and cestodes were found and no parasites could be isolated from the musculature. The results of the present study are related to previous findings on the parasite fauna of N. coriiceps. The comparison implies a high parasite diversity in this benthic Antarctic fish species. Most parasites found appear to have a wide range of distribution within Antarctic waters together with a low host specificity. Besides its role as final host for several species of trematodes and acanthocephalans, N. coriiceps serves as transmitter of parasite larvae to piscivorous birds and seals. It is concluded that the parasite fauna in Antarctic fish species provides important insights into the different habitat use and trophic relationship of their fish hosts.

A new approach to visualize ecosystem health by using parasites

A new approach is chosen to visualize ecosystem health by using parasite bioindicators in Segara Anakan Lagoon, a brackish water ecosystem at the southern Java coast, Indonesia. Three fish species (Mugil cephalus, Scatophagus argus, Epinephelus coioides) were collected in two different years and sampling sites and studied for ecto- and endoparasites. Additional data were taken for E. coioides from two further sites in Lampung Bay, Sumatra, and for E. fucoguttatus out of floating cages from a mariculture facility in the Thousand Islands, Jakarta Bay, North Java. The parasite fauna of fishes inside the lagoon was characterized by a high number of ecto- and a low number of endoparasites, the endoparasite diversity was relatively low and the prevalence of ectocommensalistic trichodinid ciliates was high. These parameters were chosen to indicate the biological conditions inside the lagoon. In E. coioides during rainy season, the prevalence of trichodinid ciliates was highest inside the lagoon (55%) compared with 27% in an open-net-cage mariculture and 5.7% in free-living specimens in Lampung Bay. The endoparasite diversity (Shannon-Wiener) was lowest in fish from Segara Anakan lagoon (0.66) compared with fish from an open-net-cage mariculture (0.71) and free-living specimens (1.39). Results for E. fuscoguttatus from the mariculture site in the Thousand Islands, a relatively undisturbed marine environment, demonstrated high parasite diversity (1.58) in the cultivated fish, a high number of endoparasites, and no trichodinids. A star graph is used to visualize the parasite composition for the different fishes, sampling sites, and conditions, using (1) the prevalence of trichodinid ciliates, (2) the ecto/endoparasite ratio and (3) the endoparasite diversity as bioindicators. The application of the star graph is suggested to be a suitable tool to visualize and monitor environmental health under high parasite biodiversity conditions within tropical ecosystems. It can also support a better communication to stake holders and decision makers in order to monitor environmental impact and change.

Crustacean fish parasites from Segara Anakan Lagoon, Java, Indonesia

The present study is the first investigation on ectoparasites of commercial important fish from Segara Anakan, a brackish water lagoon located at the southern coast of Java, Indonesia. Eight economically important marine fish species (Mugil cephalus, Siganus javus, Scatophagus argus, Caranx sexfasciatus, Lutjanus johnii, Eleutheronema tetradactylum, Johnius coitor, and Epinephelus coioides) were examined for crustacean parasites. Prevalence and intensity data for each parasite species are given, together with an analysis of the origin and possible transmission pathways. A highly divers copepod fauna consisting of 23 different species and two isopods was found. All fish species were at least infested with two copepod species, with the exception of L. johnii, S. argus, and M. cephalus. With seven and six species, respectively, they harboured the most species-rich ectoparasite fauna. The copepods Ergasilus sp. 3 and Caligus acanthopagri on S. argus showed the highest prevalence (78.6) and intensity [17.8 (1–233) and 5.3 (1–22)] of infestation. The recorded parasite fauna is represented by marine, brackish water, and probably also freshwater components. The brackish water environment of Segara Anakan does not prevent disease outbreaks due to parasitic copepods by preventing pathogenic marine or freshwater species to enter the lagoon. This might cause fish health problems if the Segara Anakan Lagoon would be developed for finfish mariculture in future.