Abstract
The life cycle of the fish ectoparasitic isopod Gnathia trimaculata is described based on both field samplings and laboratory observations. Species identification of the larvae was based on morphological observation and supported by molecular analysis. As the results of field samplings in several sites of southwestern and central Japan (24–34°N, 124–139°E) from 2005–2011, approximately 900 third-stage larvae of G. trimaculata were found on 25 elasmobranch species, and 220 first- and second-stage larvae were found on three teleost species. No third-stage larvae were found on the teleosts, and the larvae of younger stages never infested elasmobranchs. Therefore, G. trimaculata is supposed to shift its host from teleosts to elasmobranchs as it develops. We discuss the developmental periods, life span, distribution, and predation risk of the present species compared with other gnathiid species.
Similar content being viewed by others
References
Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552
Coetzee ML, Smit NJ, Grutter AS, Davies AJ (2008) A new gnathiid (Crustacea: Isopoda) parasitizing two species of requiem sharks from Lizard Island, Great Barrier Reef, Australia. J Parasitol 94(3):608–615
Coetzee ML, Smit NJ, Grutter AS, Davies AJ (2009) Gnathia trimaculata n. sp. (Crustacea: Isopoda: Gnathiidae), an ectoparasite found parasitising requiem sharks from off Lizard Island, Great Barrier Reef, Australia. Syst Parasitol 72:97–112
Costa FO, deWaard JR, Boutillier J, Ratnasingham S, Dooh RT, Hajibabaei M, Hebert PDN (2007) Biological identifications through DNA barcodes: the case of the Crustacea. Can J Fish Aquat Sci 64:272–295
Davies AJ (1995) Studies on the gut flora of the haematophagous fish parasite Gnathia maxillaris Montagu. Bull Eur Ass Fish Pathol 15(1):32
Davies AJ, Smit NJ (2001) The life cycle of Haemogregarina bigemina (Adeleina: Haemogregarinidae) in South African hosts. Folia Parasitol 48:169–177
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797
Ferreira ML, Smit NJ, Grutter AS, Davies AJ (2009) A new species of gnathiid (Crustacea: Isopoda) parasitizing teleosts from Lizard Island, Great Barrier Reef, Australia. J Parasitol 95(5):1066–1075
Froese R, Pauly D (2011) Fishbase. World wide web electronic publication. www.fishbase.org, version (08/2011). Accessed 19 Dec 2011
Grutter AS (1996) Parasite removal rates by the cleaner wrasse Labroides dimidiatus. Mar Ecol Prog Ser 130:61–70
Grutter AS (1997) Size-selective predation by the cleaner fish Labroides dimidiatus. J Fish Biol 50:1303–1308
Grutter AS (2002) Cleaning symbiosis from the parasites’ perspective. Parasitology 124:S65–S81
Grutter AS, Morgan JAT, Adlard RD (2000) Characterising parasitie gnathiid isopod species and matching life stages with ribosomal DNA ITS2 sequences. Mar Biol 136:201–205
Hadfield KA, Smit NJ, Avenant-Oldewage A (2009) Life cycle of the temporary fish parasite, Gnathia pilosus (Crustacea: Isopoda: Gnathiidae) from the east coast of South Africa. J Mar Biol Assoc UK 89(7):1331–1339
Heupel MR, Bennet MB (1999) The occurrence, distribution and pathology associated with gnathiid isopod larvae infecting the epaulette shark, Hemiscyllium ocellatum. Int J Parasitol 29:321–330
Hirose M, Yokobori S, Hirose E (2009) Potential speciation of morphotypes in the photosymbiotic ascidian Didemnum molle in the Ryukyu Archipelago, Japan. Coral Reefs 28:119–126
Honma Y, Chiba A (1991a) Pathological changes in the branchial camber wall of stingrays, Dasyatis spp., associated with the presence of juvenile gnathiids (Isopoda, Crustacea). Gyobyo Kenkyu 26:9–16
Honma Y, Chiba A (1991b) Histological studies on the juvenile gnathiid (Isopoda, Crustacea) parasitic on the branchial chamber wall of the stingray, Dasyatis akajei, in the Sea of Japan. Rep Sado Mar Biol Stat, Niigata Univ 21:37–47
Jobb G (2008) TREEFINDER ver. Jan 2008. Munich, Germany. www.treefinder.de
Jones CM, Nagel L, Hughes GL, Cribb TH, Grutter AS (2007) Host specificity of two species of Gnathia (Isopoda) determined by DNA sequencing blood meals. Int J Parasitol 37:927–935
Juilfs HB, Wägele JW (1987) Symbiotic bacteria in the gut of the blood-sucking Antarctic fish parasite Gnathia calva (Crustacea: Isopoda). Mar Biol 95:493–499
Klitgaard AB (1997) The distribution and habitats in the North Atlantic of two gnathiid species (Crustacea, Isopoda) and their reproductive biology in the Denmark Strait and north of Iceland. Meddr Grønland, Biosci 47:5–32
Klossa-Kilia E, Kilias G, Tryfonopoulos G, Koukou K, Sfenthourakis S, Parmaklis A (2006) Molecular phylogeny of the Greek populations of the genus Ligidium (Isopoda, Oniscidea) using three mtDNA gene segments. Zool Scr 35:459–472
Lester RJG (2005) Isopoda (isopods). In: Rohde K (ed) Marine parasitology. CSIRO Publishing, Collingwood, pp 138–144
McKiernan JP, Grutter AS, Davies AJ (2005) Reproductive and feeding ecology of parasitic gnathiid isopods of epaulette sharks (Hemiscyllium ocellatum) with consideration of their role in the transmission of a haemogregarine. Int J Parasitol 35:19–27
Monod T (1926) Les Gnathiidae. Essai monographique (morphologie, biologie, systématique). Mém Soc Sci Nat Maroc 13:1–667
Nakabo T (1993) Fishes of Japan with pictorial keys to the species. Tokai University Press, Tokyo. (In Japanese)
Neil H (2006) Osmoregulation in elasmobranchs: a review for fish biologists, behaviourists and ecologists. Mar Freshw Behav Physiol 39(3):209–228
Nunomura N, Honma Y (2004) Gnathia capillata, a new species of the genus Gnathia (Crustacea, Isopoda) from Sado Island, the Sea of Japan. Contr boil Lab Kyoto Univ 29:343–349
Ota Y (2011) A new species of the gnathiid isopod, Gnathia teruyukiae (Crustacea: Malacostraca), from Japan, parasitizing elasmobranch fish. Bull Natl Mus Nat Sci Ser A Suppl 5:41–51
Ota Y, Hirose E (2009a) Description of Gnathia maculosa and a new record of Gnathia trimaculata (Crustacea, Isopoda, Gnathiidae), ectoparasites of elasmobranchs from Okinawan coastal waters. Zootaxa 2114:50–60
Ota Y, Hirose E (2009b) Gnathia nubila n. sp. and a new record of Gnathia grandilaris (Crustacea, Isopoda, Gnathiidae) that parasitizes elasmobranchs from Okinawan coastal waters, Japan. Zootaxa 2238:43–55
Ota Y, Tanaka K, Hirose M, Hirose E (2010) Description of a new species of Elaphognathia (Isopoda: Gantheidae) from Japan based on morphological and molecular traits. J Crust Biol 30:710–720
Paperna I, Por FD (1977) Preliminary data on the Gnathiidae (Isopoda) of the Northern Red Sea, the Bitter Lakes and the Eastern Mediterranean and the biology of the Gnathia piscivora n sp. Rapp Comm Int Mer Medit 24(4):195–197
Podsiadlowski L, Bartolomaeus T (2005) Organization of the mitochondrial genome of Mantis shrimp Peudosquilla ciliata (Crustacea: Stomatopoda). Mar Biotech 7:618–624
Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256
Poulin R (1995) Evolutionary influences on body size in free-living and parasitic isopods. Biol J Linnean Soc 54:231–244
Ratnasingham S, Hebert PD (2007) Bold: the barcode of life data system (http://www.barcodinglife.org). Mol Ecol Notes 7:355–364
Rivera MAJ, Howarth FG, Taiti S, Roderick GK (2002) Evolution in Hawaiian cave-adapted isopods (Oniscidea: Philosciidae): vicariant speciation or adaptive shifts? Mol Phylogenet Evol 25:1–9
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, New York
Schotte M, Boyko C, Bruce NL, Poore GCB, Taiti S, Wilson GDF (Eds) (2008 onwards) Isopoda statistics. World Marine, Freshwater and Terrestrial Isopod Crustaceans. http://www.marinespecies.org/isopoda. Accessed 22 Feb 2012
Smit NJ, Basson L (2002) Gnathia pantherina sp. n. (Crustacea: Isopoda: Gnathiidae), a temporary ectoparasite of some elasmobranch species from southern Africa. Folia Parasitol 49:137–151
Smit NJ, Davies AJ (2004) The curious life-style of the parasitic stages of gnathiid isopods. Adv Parasitol 58:289–391
Smit NJ, Basson L, Van As JG (2003) Life cycle of the temporary fish parasite, Gnathia africana (Crustacea: Isopoda: Gnathiidae). Folia Parasitol 50:135–142
Stoll C (1962) Cycle évolitif de Paragnathia formica (Hesse) (Isopode—Gnathiidae). Cah Biol Mar 3:401–416
Swofford D (2003) PAUP* 4.0b7a, Phylogenetic analysis using parsimony (*and other methods). Sinauer Associates, Sunderland, MA
Tanaka K (2002) Predation risks involved in the parasitic behaviour of gnathiid isopods (Crustacea). Jpn J Benthol 57:85–89 (In Japanese with English abstract)
Tanaka K (2003) Population dynamics of the sponge-dwelling gnathiid isopod Elaphognathia cornigera. J Mar Biol Assoc UK 83:95–102
Tanaka K (2007) Life histology of gnathiid isopods-current knowledge and future directions. Plankton Benthos Res 2(1):1–11
Tanaka K, Aoki M (1998) Crustacean infauna of the demosponge Halichondria okadai (Kabota) with reference to life cycle of Gnathia sp. (Isopoda: Gnathiidea). In: Watanabe Y, Fusetani N (eds) Sponge science: multidisciplinary perspectives. Springer, Tokyo, pp 259–267
Tanaka K, Aoki M (2000) Seasonal traits of reproduction in a gnathiid isopod Elaphognathia cornigera (Nunomura, 1992). Zool Sci 17:467–475
Tanaka K, Nishi E (2011) Male dimorphism in the harem-forming gnathiid isopod Elaphognathia discolor (Crustacea: Isopoda). Zool Sci 28:587–592
Upton NPD (1987) Asynchronous male and female life cycles in the sexually dimorphic, harem-forming isopod Paragnathia formica (Crustacea: Isopoda). J Zool Lond 212:677–690
Wägele J-W (1987) Description of the postembryonal stages of the Antarctic fish parasite Gnathia calva Vanhöffen (Crustacea: Isopoda) and synonymy with Heterognathia Amar & Roman. Polar Biol 7:77–92
Wägele J-W (1988) Aspects of the life-cycle of the Antarctic fish parasite Gnathia calva Vanhöffen (Crustacea: Isopoda). Polar Biol 8:287–291
Acknowledgments
We thank Makio Yanagisawa (Okinawa Churaumi Aquarium), Hirohito Arima (Izu-Oshima Island) and Mitsuko Chikuchishin (Kagoshima City Aquarium) for providing specimens. Dr. Daisuke Uyeno (University of the Ryukyus) helped us with collecting the specimens. A part of the material examined was collected during the KUMEJIMA 2009 Expedition organized by the Transdisciplinary Research Organization for Subtropical and Island Studies of the University of the Ryukyus, the Center for Marine Bioscience & Biotechnology of the National Taiwan Ocean University, the Raffles Museum of Biodiversity Research of the National University of Singapore, and the Biodiversity Research Center of the Academia Sinica. The expedition operated under a permit granted to Dr. T. Naruse by the Okinawa Prefectural Governor and the Kumejima Fisheries Cooperative. The present study includes the contribution from Shimoda Marine Research Center (No. 758). This study was partly supported by a Grant-in-Aid JSPS Fellows (No. 23-527) (YO), a joint-research in Japanese Association for Marine Biology (YO, KT, and EH), and “International Research Hub Project for Climate Change and Coral Reef/Island Dynamics” from University of the Ryukyus (EH). The authors would like to thank three anonymous reviewers for valuable comments.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by S. A. Poulet.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ota, Y., Hoshino, O., Hirose, M. et al. Third-stage larva shifts host fish from teleost to elasmobranch in the temporary parasitic isopod, Gnathia trimaculata (Crustacea; Gnathiidae). Mar Biol 159, 2333–2347 (2012). https://doi.org/10.1007/s00227-012-2018-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-012-2018-2