Ken MacKenzie

Parasites as Pollution Indicators in Marine Ecosystems: a Proposed Early Warning System

Abstract There are good reasons for focusing on parasites in the search for indicators to monitor the effects of pollutants on marine organisms. Firstly, there are more parasitic than free-living species. Secondly, in parasites with complex life cycles, the different stages have widely differing requirements, so that each stage must be assessed separately, thereby greatly increasing the number of potential indicators. Thirdly, many parasites have delicate free-living transmission stages which are highly sensitive to environmental change. A reduction in their levels of infection will serve as an early warning that changes are occurring. Conversely, other parasites are highly resistant to environmental change and will respond by increased levels of infection. As a general rule, infections with endoparasitic helminths tend to decrease, while infections with ectoparasites tend to increase, with increasing levels of pollution.

Spatial and temporal variations in parasite prevalence and infracommunity structure in herring ( Clupea harengus L.) caught to the west of the British Isles and in the North and Baltic Seas: implications for fisheries science

Herring Clupea harengus L. viscera were examined for endoparasitic infections as part of a multidisciplinary stock identification project (WESTHER, EU Contract no. Q5RS-2002-01 056) which applied a range of stock discrimination techniques to the same individual fishes to obtain comparable results for multivariate analysis. Spawning and non-spawning adults, and juvenile herring were caught, over 3 years, by commercial and research vessels from numerous locations to the west of the UK and Ireland, along with control samples of spawning fish from the eastern Baltic Sea, and juveniles from sites in the eastern and western North Sea, and the north of Norway. The metacercariae of two renicolid digeneans (Cercaria pythionike and Cercaria doricha), one larval nematode (Anisakis simplex s.s.) and one larval cestode (Lacistorhynchus tenuis) were selected as tag species. Results were compared with those from herring collected between 1973 and 1982, which suggested remarkable stability in the parasite fauna of herring in the study area. These species were used to compare the parasite infracommunities of spawning herring. A significant variation in infracommunity structure was observed between different spawning grounds. These results suggest that the parasite fauna of herring are spatially variable but remain temporally stable in both the short and long term. Significant differences in prevalence and abundance of infections and comparisons of parasite infracommunity enabled the separation of putative herring stocks west of the British Isles. Distinctive patterns of parasite infection in two different spawning groups off the north coast of Scotland suggest that this area is occupied by two spawning populations, one recruiting from the west of Scotland, the other from outside this area, and most likely from the eastern North Sea. The distribution patterns of L. tenuis, C. doricha and C. pythionike suggest the potential for fish that spawn in three distinct International Council for the Exploration of the Seas (ICES) management units to be present in mixed aggregations found over the Malin Shelf, with significant implications for management in this area.

Parasites of the Patagonian toothfish, Dissostichus eleginoides Smitt 1898, in different parts of the Subantarctic

The parasite faunas of the Patagonian toothfish Dissostichus eleginoides from six locations around the Southern Ocean were studied and compared. Thirty-two parasite taxa were found. Ten parasite species are reported from D. eleginoides for the first time and some other previously reported species were new locality records. Sample size at Shag Rocks was sufficient to examine the effect of intrinsic host factors, including sex and length, on the parasite fauna and these results are discussed here. Some parasite species were found only in certain areas. Sørensen’s similarity index indicated that the parasite faunas at Heard, Maquarie and Prince Edward Islands were the most similar, while those from the Ross Sea was the most dissimilar. There may be a gradual decrease in parasite diversity the further east the samples were collected around the Southern Ocean.

The occurrence of some metazoan parasites of Atlantic cod, Gadus morhua L., in relation to age and sex of the host in Balsfjord (70°N), North Norway

Abstract Age and sex differences in the occurrence of some metazoan parasites were investigated in 243 cod (Gadus morhua L.) from Balsfjord, a subarctic fjord in northern Norway. Thirteen species of parasite were studied, comprising seven nematodes, three parasitic copepods, one acanthocephalan, one cestode and one digenean. The nematode Anisakis simplex showed significant increases in both prevalence and mean abundance with host age, while the digenean Hemiurus levinseni showed a significant increase in mean abundance with age. The increases probably result from a long parasite life-span for A. simplex and changes in the feeding pattern of cod with age for H. levinseni. Prevalence of the nematode Contracaecum sp. and mean abundance of the acanthocephalan Echinorhynchus gadi were significantly higher in male than in female cod, whereas mean abundance of H. levinseni was significantly higher in female cod. These results suggest that there may be differences in feeding behaviour between male and female cod in Balsfjord.

The genera Ceratomyxa Thélohan, 1892, Leptotheca Thélohan, 1895 and Sphaeromyxa Thélohan, 1892 (Myxosporea: Bivalvulida) in gadid fish of the Northeast Atlantic

The gall-bladders of four species of gadid fish from the North Sea and Norwegian waters were examined for myxosporeans. The host species were cod Gadus morhua L. (350 examined), haddock Melanogrammus aeglefinus (L.) (592 examined), saithe Pollachius virens (L.) (205 examined) and whiting Merlangius merlangus (L.) (368 examined). Four species of myxosporeans are redescribed from these fish. Ceratomyxa arcuata Thélohan, 1892 was the most common species and was found in whiting (42.8%) and cod (0.6%). Leptotheca informis Auerbach, 1910 was found only in whiting (6.5%). L. longipes Auerbach, 1910 was found only in haddock (6.2%). Sphaeromyxa hellandi Auerbach, 1909 was found in haddock (9.1%) and whiting (0.3%). None of the saithe examined, and no cod or haddock from Norwegian waters, was infected with these myxosporeans. All four species appear to have distributions limited to the Northeast Atlantic, with S. hellandi having a more northern distribution than the other three. The validity of reports of C. arcuata, L. informis and L. longipes from outside this area is discussed.

Parasites as biological tags for Eleginops maclovinus (Teleostei: Eleginopidae) around the Falkland Islands

This is the first study of the parasite fauna of Eleginops maclovinus in the Falkland Islands. It was undertaken to catalogue the parasite fauna of E. maclovinus in order to provide a baseline for future studies and to determine whether parasites might be used as biological tags. Between 21 January and 17 March 2002 samples were taken from three stations, Teal Creek (30 fish), Port Louis (30 fish) and Camilla Creek (10 fish), all in East Falkland, and examined for protozoan and metazoan parasites. Twenty-four parasite taxa were recorded, of which three were possible new species, two new host records and five new geographical records. Because of the small number of fish in the Camilla Creek sample it was excluded from further analyses. E. maclovinus is a protandrous hermaphrodite and all fish greater than 53 cm total length were found to be female, so these too were excluded from further analyses. The parasite data from the remaining fish were analysed by an agglomerative hierarchical cluster analysis using an average linkage and a Jaccard measure of similarity, followed by a linear discriminant function analysis (LDA). Both analyses misclassified only one fish from Port Louis as being from Teal Creek, with the LDA giving an overall correct classification of 97.5% (39/40). The results support mechanical tagging data in suggesting that smaller male E. maclovinus are resident in the creeks in which they are caught, and that at this stage of their lives they tend not to migrate over long distances.

Aponurus laguncula Looss, 1907 (Digenea: Lecithasteridae): a report from herring, Clupea harengus L., in the eastern English Channel and a review of its biology.

The digenean Aponurus laguncula is reported for the first time from the herring, Clupea harengus, and for the first time from the north-eastern Atlantic Ocean. These specimens from the English Channel are described and differ from previous descriptions only in their greater egg-size, the mean of which is 38 × 18 μm. Their occurrence in the new host and locality is discussed. Comparison with other described species of Aponurus suggests that several may be synonymous with A. laguncula. A. laguncula is euryxenic, with no dominant host-group, but the most frequently recorded host-family is the Carangidae.

VARIATIONS IN THE PARASITE FAUNA OF THE PATAGONIAN TOOTHFISH (DISSOSTICHUS ELEGINOIDES SMITT, 1898), WITH LENGTH, SEASON, AND DEPTH OF HABITAT AROUND THE FALKLAND ISLANDS

The parasite fauna of Dissostichus eleginoides was examined from locations around the Falkland Islands. In total, of 11,362 individual parasites of 27 taxa were recovered from 105 fish. Two species, Ceratomyxa dissostichi and Sphaerospora dissostichi, represent new host records. The nematode Ascarophis nototheniae and the larval acanothocephalan Corynosoma bullosum were found to be new locality records and add to the knowledge of the biogeography and host specificity of parasites on the Patagonian Shelf. There were no significant differences in the mean abundance and prevalence of parasites recovered between sexes. Therefore, sex was not considered in further analysis and the data were pooled. Cysts of unknown etiology (CUE), the monogenean Neopavlovskioides georgianus, the larval acanthocephalan Corynosoma bullosum, and the digenean Neolepidapedon magnatestis had significant positive correlations with increasing host length. The larval Trypanorhynch cestode Grillotia erinaceus and the digenean Elytrophalloides oatesi showed significant negative correlations with increasing host length. CUEs, N. georgianus, the digenean Gonocerca physidis and E. oatesi showed statistically significant prevalence between summer, winter, and spring. The effect of depth on parasite communities was also examined, initially using a linear discriminant function analysis. The prevalence of individual parasites was then compared between depth strata using the chi-square test. The parasite communities on the shelf and deep water (>1,000 m) were found to be different, whereas those caught at intermediate depths on the shelf slope were found to have parasite communities that were intermediate, containing a mixture of shelf and deeper-water parasites. The causes of the variations in parasite faunas in association with these intrinsic and extrinsic factors are discussed.

Two species of myxozoan parasites (Myxosporea: Bivalvulida), including a new genus, fromPatagonotothen sima (Richardson, 1845) (Pisces: Teleostei) in the southwest Atlantic

A new genus and species of myxozoan parasite,Renispora simae, is described from the gall-bladder of the nototheniid fishPatagonotothen sima (Richardson). Four of 12 fish caught in Stanley harbour in the Falkland Islands in May, 1993 were infected. The new genus is placed in the family Alatosporidae and differs from other genera in this family by the shape of the spore body and the shape and site of adhesion of the membranous extensions to the spore valves. To accommodate the new genus, we propose an amendment to the definition of the family Alatosporidae to include forms with reniform spores.Myxidium baueri Kovaleva & Gaevskaya, 1982 is reported fromP. sima for the first time. It was found in the gall-bladder of one of the same 12 fish caught in Stanley harbour.

Macroparasites of allis shad (Alosa alosa) and twaite shad (Alosa fallax) of the Western Iberian Peninsula Rivers: ecological, phylogenetic and zoonotic insights

Samples of anadromous Alosa alosa (Clupeidae) (n = 163) and Alosa fallax (Clupeidae) (n = 223), caught in Western Iberian Peninsula Rivers from 2008 to 2013, were examined for buccal, branchial and internal macroparasites, which were identified using morphological and molecular methods. Alosa alosa were infected with Anisakis simplex s.s., Anisakis pegreffii, Hysterothylacium aduncum, Rhadinorhynchus pristis, Mazocraes alosae, Hemiurus appendiculatus, Ceratothoa italica and an unidentified ergasilid copepod. Ceratothoa italica represents a new host record for A. alosa. Alosa fallax were infected with A. simplex s.s., A. pegreffii, H. aduncum, H. appendiculatus, Clavellisa emarginata and an unidentified cymothoid isopod. This is the first report of C. italica, C. emarginata and M. alosae in the Iberian Peninsula. The phylogenetic positions of M. alosae, H. appendiculatus and C. emarginata were assessed using 18S and 28S ribosomal RNA (rRNA); our contributions provide a better understanding of the phylogenetic relationships within their groups. Qualitative and quantitative differences in the parasite faunas of these two shad species are consistent with different feeding strategies. The results provide information about host migration behaviour and transmission pathways through diet during the marine trophic phase of the shad’s life cycle and their roles as paratenic or final hosts and transporters of parasites between seawater and freshwater environments. The zoonotic parasites A. simplex s.s. and A. pegreffii pose a risk for consumers or riverine mammals (e.g. European otter). The use of parasites as biological tags for shad stocks in Western Iberian Rivers could be a useful approach in multidisciplinary studies concerning fish stock delimitation and characterization.