Biodiversity of parasites of coral reef fish
Open access papers available:
Justine, J.-L., Rahmouni, C., Gey, D., Schoelinck, C., & Hoberg, E. P. (2013) The monogenean which lost its clamps. PLoS ONE, 8 (11), e79155. Free PDF: doi:10.1371/journal.pone.0079155
Ectoparasites face a daily challenge: to remain attached to their hosts. Polyopisthocotylean monogeneans usually attach to the surface of fish gills using highly specialized structures, the sclerotized clamps. In the original description of the protomicrocotylid species Lethacotyle fijiensis, described 60 years ago, the clamps were considered to be absent but few specimens were available and this observation was later questioned. In addition, genera within the family Protomicrocotylidae have either clamps of the “gastrocotylid” or the “microcotylid” types; this puzzled systematists because these clamp types are characteristic of distinct, major groups. Discovery of another, new, species of the genus Lethacotyle, has allowed us to explore the nature of the attachment structures in protomicrocotylids. Lethacotyle vera n. sp. is described from the gills of the carangid Caranx papuensis off New Caledonia. It is distinguished from Lethacotyle fijiensis, the only other species of the genus, by the length of the male copulatory spines. Sequences of 28S rDNA were used to build a tree, in which Lethacotyle vera grouped with other protomicrocotylids. The identity of the host fish was confirmed with COI barcodes. We observed that protomicrocotylids have specialized structures associated with their attachment organ, such as lateral flaps and transverse striations, which are not known in other monogeneans. We thus hypothesized that the clamps in protomicrocotylids were sequentially lost during evolution, coinciding with the development of other attachment structures. To test the hypothesis, we calculated the surfaces of clamps and body in 120 species of gastrocotylinean monogeneans, based on published descriptions. The ratio of clamp surface: body surface was the lowest in protomicrocotylids. We conclude that clamps in protomicrocotylids are vestigial organs, and that occurrence of “gastrocotylid” and simpler “microcotylid” clamps within the same family are steps in an evolutionary sequence, leading to the absence of these attributes in species of Lethacotyle.
Free PDF here (PLoS ONE)
Justine J.-L., Beveridge I., Boxshall G.A., Bray R.A., Miller, T.L., Moravec F., Trilles, J.-P., Whittington I.D. (2012) An annotated list of fish parasites (Isopoda, Copepoda, Monogenea, Digenea, Cestoda, Nematoda) collected from Snappers and Bream (Lutjanidae, Nemipteridae, Caesionidae) in New Caledonia confirms high parasite biodiversity on coral reef fish. Aquatic Biosystems, 8, 22.
Coral reefs are areas of maximum biodiversity, but the parasites of coral reef fishes, and especially their species richness, are not well known. Over an 8-year period, parasites were collected from 24 species of Lutjanidae, Nemipteridae and Caesionidae off New Caledonia, South Pacific.
Host-parasite and parasite-host lists are provided, with a total of 207 host-parasite combinations and 58 parasite species identified at the species level, with 27 new host records. Results are presented for isopods, copepods, monogeneans, digeneans, cestodes and nematodes. When results are restricted to well-sampled reef fish species (sample size>30), the number of host-parasite combinations is 20-25 per fish species, and the number of parasites identified at the species level is 9-13 per fish species. Lutjanids include reef-associated fish and deeper sea fish from the outer slopes of the coral reef: fish from both milieus were compared. Surprisingly, parasite biodiversity was higher in deeper sea fish than in reef fish (host-parasite combinations: 12.50 vs 10.13, number of species per fish 3.75 vs 3.00); however, we identified four biases which diminish the validity of this comparison. Finally, these results and previously published results allow us to propose a generalization of parasite biodiversity for four major families of reef-associated fishes (Lutjanidae, Nemipteridae, Serranidae and Lethrinidae): well-sampled fish have a mean of 20 host-parasite combinations per fish species, and the number of parasites identified at the species level is 10 per fish species.
Since all precautions have been taken to minimize taxon numbers, it is safe to affirm than the number of fish parasites is at least ten times the number of fish species in coral reefs, for species of similar size or larger than the species in the four families studied; this is a major improvement to our estimate of biodiversity in coral reefs. Our results suggest that extinction of a coral reef fish species would eventually result in the coextinction of at least ten species of parasites.
PDF here (Aquatic Biosystems)
Justine J.-L., Beveridge I., Boxshall G.A., Bray R.A., Moravec F., Whittington I.D. (2010) An annotated list of fish parasites (Copepoda, Monogenea, Digenea, Cestoda and Nematoda) collected from Emperors and Emperor Bream (Lethrinidae) in New Caledonia further highlights parasite biodiversity estimates on coral reef fish. Zootaxa, 2691, 1-40.
Abstract Parasites were collected from 17 species of emperors and emperor bream (Lethrinidae) in the waters off New Caledonia, South Pacific. Host-parasite and parasite-hosts lists are provided, with a total of 188 host-parasite combinations (11 per fish species), including 81 identifications at the species level. A total of 52 parasites were identified at the species level, and 40 new host records were found. Results are presented for larval isopods, copepods (16 species), monogeneans (24), digeneans (27), cestodes (11) and nematodes (10). When results were restricted to the four best-sampled fish species for which more than 30 specimens were examined, the number of host-parasite combinations was 22.25 per fish species, and the number of parasite taxa identified at the species level was 9.5 per fish species. From these data, the total number of metazoan parasite species predicted from all lethrinid species of New Caledonia, based on a classification of fish sizes using length in three categories, is 340, i.e. 13 per fish species. A biogeographical comparison with Heron Island on the Great Barrier Reef (Queensland, Australia) was possible only for a single fish species, Lethrinus miniatus: in a total of 65 host-parasite combinations, only five taxa identified at the species level (three monogeneans and two digeneans) were shared at both localities. Parasite biodiversity in lethrinids was of similar magnitude to that in groupers (Serranidae Epinephelinae) in the same area, and this study confirms a previous prediction of 10 parasite species per coral reef fish species. Although this study required significant sampling and identification, we estimate that only 13% of the parasites of lethrinids are known in New Caledonia.
PDF (40 pages, 727 ko) available here (Zootaxa)
Justine J.-L., Beveridge I., Boxshall G.A., Bray R.A., Moravec F., Trilles, J.-P., Whittington I.D. (2010) An annotated list of parasites (Isopoda, Copepoda, Monogenea, Digenea, Cestoda and Nematoda) collected in groupers (Serranidae, Epinephelinae) in New Caledonia emphasizes parasite biodiversity in coral reef fish. Folia Parasitologica, 57, 237-262
Abstract Over a 7-year period, parasites have been collected from 28 species of groupers (Serranidae, Epinephelinae) in the waters off New Caledonia. Host-parasite and parasite-hosts lists are provided, with a total of 337 host-parasite combinations, including 146 parasite identifications at the species level. Results are included for isopods (5 species), copepods (19), monogeneans (56), digeneans (28), cestodes (12), and nematodes (12). When results are restricted to those 14 fish species for which more than five specimens were examined and to parasites identified at the species level, 109 host-parasite combinations were recorded, with 63 different species, of which monogeneans account for half (32 species), and an average of 4.5 parasite species per fish species. Digenean records were compared for 16 fish species shared with the study of Cribb et al. (2002); based on a total of 90 parasite records identified at the species level, New Caledonia has 17 new records and only seven species were already known from other locations. We hypothesize that the present results represent only a small part of the actual biodiversity, and we predict a biodiversity of 10 different parasite species and 30 host-parasite combinations per serranid. A comparison with a study on Heron Island (Queensland, Australia) by Lester and Sewell (1989) was attempted: of the four species of fish in common and in a total of 91 host-parasite combinations, only six parasites identified at the species level were shared. This suggests strongly that insufficient sampling impairs proper biogeographical or ecological comparisons. Probably only 3% of the parasite species of coral reef fish are already known in New Caledonia.
PDF (26 pages, 1351 ko) available here (Folia Parasitologica)
Justine, J.-L (2010) Parasites of coral reef fish: how much do we know? With a bibliography of fish parasites in New Caledonia. Belgian Journal of Zoology, 140 (Suppl.), 155-190.
Abstract A compilation of 107 references dealing with fish parasites in New Caledonia permitted the production of a parasite-host list and a host-parasite list. The lists include Turbellaria, Monopisthocotylea, Polyopisthocotylea, Digenea, Cestoda, Nematoda, Copepoda, Isopoda, Acanthocephala and Hirudinea, with 580 host-parasite combinations, corresponding with more than 370 species of parasites. Protozoa are not included. Platyhelminthes are the major group, with 239 species, including 98 monopisthocotylean monogeneans and 105 digeneans. Copepods include 61 records, and nematodes include 41 records. The list of fish recorded with parasites includes 195 species, in which most (ca. 170 species) are coral reef associated, the rest being a few deep-sea, pelagic or freshwater fishes. The serranids, lethrinids and lutjanids are the most commonly represented fish families. Although a list of published records does not provide a reliable estimate of biodiversity because of the important bias in publications being mainly in the domain of interest of the authors, it provides a basis to compare parasite biodiversity with other localities, and especially with other coral reefs. The present list is probably the most complete published account of parasite biodiversity of coral reef fishes. However, it is estimated that the present state of knowledge (370 parasite species) represents only 2% of the possible number of metazoan parasites of fish present in a coral reef environment.
PDF (36 pages, 1293 ko) available here