Bull. Eur. Ass. Fish Pathol., 35(5) 2015, 177
ȱ¢ȱȱCaecognathia coralliophila (Crustacea, Isopoda, Gnathiidae) in hatchery reared tiger grouper, ȱĴ
Y. T. Chong, K. Hatai* and J. Ransangan
Microbiology and Fish Disease Laboratory, Borneo Marine Research Institute, Universiti Malaysia Sabah, 88999 Kota Kinabalu, Sabah, Malaysia
Abstract ȱ¡¢ȱȱȱȱCaecognathia coralliophila has been described by Monod (1926) and ȱȱǯȱǻŘŖŗśǼǰȱȱȱȬ¢ȱȱȱ¢ȱ ǯȱȱȱȱȱȬ¢ȱȱC. coralliophila in hatchery reared tiger grouper, Epinephelus Ĵǯȱȱȱȱȱȱ ȱȱȱC. coralliophilaȱ ȱȱȱȱ¢ȱȱ¢ǯȱȱȱȱȱ- ȱȱȱęȱǰȱȱ£ȱȱȱȱȱȱȱȱȱ ȱǯȱ ȱȱȬ¢ȱȱȱȱȱȱȱȱȱǯ
Introduction ȱȱȱCaecognathia coralliophila was ǻĴȱ ȱ ǯǰȱ ŘŖŖŞȱ Ǽǯȱ ȱ ¢ǰȱ observed in the hatcheries broodstock tanks Gnathia lignophila and G. perimulica (Müller, ǻȱȱǯǰȱŘŖŗśǼǯȱ ȱ ȱęȱȱȱŘŖŗŘȱ ŗşşřǼȱȱȱȱȱȱȱȱ ȱȱȱ¢ȱȱȱŘŖŗřǯȱ ȱ the Tioman Archipelago, while recently, Chong the broodstock tanks, the larval stages, consist- ȱǯȱǻŘŖŗśǼȱȱC. coralliophila in hatchery ȱȱȱȱȱȱ£ȱǻǼȱȱ reared grouper, Epinephelus Ĵ in £ȱǻǼǰȱȱȱȱȱȱȱ Sabah, Malaysia. ȱȱ¢ȱǯȱȱ ȱĴȱȱ ȱȱ¢ȱȱȱęȱǻȱŗǼǯȱȱȱ ȱȱȱ¢ȱȱ¡ȱȱȱ ȱȱȱǻ£ȱȱ£Ǽȱȱȱ ȱȱ¢ȱȱȱȱȱ ȱ ȱ¢ȱȱȱ ȱ¢ǰȱ (Tanaka and Aoki, 1998; Smit et al., 2003; Smit ȱȱȱȱȱȱȱȱ and Davies, 2004; Tanaka, 2007). They are poly- ȱȱȱȱȱȱȱĴȱ Dzȱȱȱȱȱȱȱȱ ȱȱǯȱ ȱ¢ȱ¢ȱȱȱȱȱȱ eggs, enabling them to develop into larvae, ȱȱȱ¢ȱȱȱǰȱ ę¢ȱȱȱȱȱȱ and includes 12 genera and about 200 species brood pouch (Tinsley and Reilly, 2002). They
* Corresponding author’s e-mail: [email protected] 178, Bull. Eur. Ass. Fish Pathol., 35(5) 2015
Figure 1. ȱĴȱȱȱȱǰȱȱĴǯ
ȱȱȱȬ¢Dzȱȱȱ ȱȱȱ¡ȱȱ ȱȱ¢ȱȱŘŖȱ ȱȱȬȱȱȱǻȱȱ ȱȱȱȬȱȱȱȱ Davies, 2004; Tanaka, 2007). There are three system. The temperature in the tanks is almost larval stages with two phases in each stage; one constant throughout the year with the average phase being haematophagous called zuphea ȱŘŝǯśȱǚǯȱȱȱȱȱȱǰȱȱ ȱȱȱȬȱȱ ȱȱ parasites were visible throughout the water praniza (McKiernan et al., 2005). The basic column. Parasites were collected by randomly ȱ¢ȱȱȱȱȱȱȱ ȱȱ ȱȱȱŘśŖȱΐȱȱǻȱ G. maxillaris (Smith, 1904; Mouchet, 1928), G. 2). The sampled larvae were then sorted by piscivora (Paperna and Por, 1977), G. africana size into six larval groups, which are Zuphea (Smit et al., 2003), Paragnathia formica (Monod 1, Praniza 1, Zuphea 2, Praniza 2, Zuphea 3, 1926; Mouchet, 1928; Stoll, 1962; Amanieu, 1963; Praniza 3. Whereas, the adults were collected Upton, 1987), C. calva (Wägele, 1987, 1988), C. ȱȱȱȱȱȱĴȱȱȱǯȱ abyssorum (Klitgaard, 1991, 1997) and Elaphog- ȱęȱȱȱȱȱȱȱ nathia cornigera (Tanaka and Aoki, 1998, 1999, was done according to the description by Chong ŘŖŖŖǼǯȱȱȱȱȬ¢ȱȱC. et al (2015). coralliophilaȱȱȱȱ¢ǯ Ĵȱȱȱȱȱęȱȱȱ Materials and methods observation Sampling One tiger grouper, ǯȱĴ, measuring The sampling was conducted in the broodstock ŗŗǯŚȱȱ ȱȱȱȱŗŝȱȱȱęȱ ȱ ȱȱȱ¢ȱ ȱȱǰȱE. ęȱ ǯȱȱ£ȱ ȱȱȱ Ĵ, giant grouper, E. lanceolatus, Asian ȱȱȱ¢ȱǯȱȱȱęȱ ȱȱȱ seabass, Later calcarifer, humphead wrasse Che- ȱ¡ȱȱȱȱǯȱ linus undulatusȱȱ¢ȱǯȱȱęȱ ȱȱȱȱȱĴȱ¢ȱȱ Bull. Eur. Ass. Fish Pathol., 35(5) 2015, 179
Figure 2. ȱȱȱȱ ȱȱȱȱ¢ȱǯ
zuphea to tiger grouper were observed, and the £ȱȱȱ ȱǯȱȱȱ£ȱ ȱȱȱ£ǰȱȱ£ȱ ȱ- ȱǯȱȱȱȱȱȱ£ȱ to praniza was noted as well. The process was ȱȱ ŗȱȱȱǯȱȱ¡- ment was conducted at room temperature.
Results and discussion Zuphea 1 (Z1) ŗȱȱȱȱȱ¢ȱ ȱŖǯŜŞȬŖǯŞśȱ mm ( ± SD; 0.77 ± 0.06 mm, n =8) in body Figure 3. Zuphea 1. ȱǻȱřǼǯȱȱǰȱ¢ȱ ȱ ȱȱ ȱȱȱśȱ¢ȱȱ¢ȱȱ ȱęȱȱȱȱǯȱ ȱǰȱȱ ŗȱ ęȱȱȱ ȱȱȱȱĴȱ Praniza 1 (P1) ȱǯȱȱ£ȱȱ¢ȱ ȱ¢ȱȱŗȱ ȱȱȱȱȱȱ ȱȱęȱȱȱęǯȱȱȱȱȱȱ ȱȱȱȱȱȱȱȱŚȱȱ ǰȱ¢ȱ¢ȱȱȱȱȱęȱȱȱ śȱ¢ȱȱȱȱȱ Řǯȱ¢ȱȱ to 12 hours until they become praniza 1 (P1). at this stage, was 0.87 mm (0.87 ± 0 mm, n=2). ȱĴȱȱ ȱ¢ȱǰȱŗǯŜȬŗŘȱ The molting process was similar to the general hours (7.5 ± 5.07 hours, n=3). Z1 showed an isopod molt, with the posterior region being active swimming behaviour. ęȱǰȱ ȱ¢ȱȱȱǯ 180, Bull. Eur. Ass. Fish Pathol., 35(5) 2015
Zuphea 2 (Z2) Praniza 3 (P3) Řȱ¢ȱȱȱȱȱȱśȱ¢ȱȱ řȱȱȱ¢ȱȱȱŗǯśŖȬŘǯŜŞȱȱǻŘǯŗŞȱƹȱ ęȱȱȱȱǯȱȱȱȱ 0.35 mm, n = 38) (Figure 4). The molting process Z1, Z2 also showed a very energetic swim- ȱřȱ ȱȱȱȱȱȱ£ȱ ming behaviour. At this stage, the body length stages (Figure 5). At stage P3, it was possible ȱŖǯŞŞȬŗǯřŖȱȱǻŗǯřřȱƹȱŖǯŗřȱǰȱƽřŜǼǯȱȱ ȱěȱ ȱȱȱȱȱ ¢ȱȱȱǰȱȱŚȱȱȱşȱȱ ȱȱ¢ȱǯȱȱ¢ȱȱ ǻƽŘǼȱȱ ŘȱĴȱȱȱȱȱȱ the pereon made sexual observation possible. and become P2. ȱȱȱȱȱȱȱȱ adult was observed in C. calva (Wägele, 1987) in Praniza 2 (P2) contrast to C. coralliophila. It is unclear whether ȱȱŘȱǰȱȱȱȱȱĴȱȱ ȱȱȱȱęȱȱȱȱ ȱǯȱ ȱȱȱȱĴȱȱȱȱ Caecognathia. ȱ ȱ¢ȱȱȱȱęȱ¢ȱȱ ǯȱȱ¢ȱȱȱŘȱ ȱŗǯŖśȬŗǯřŖȱ ȱ mm (1.19 ± 0.11 mm, n = 4). Adult males were 1.87-2.45 mm (2.17 ± 0.14 mm, n = 15) in body length. In general male gnathiid Zuphea 3 (Z3) ȱ¢ȱȱěȱȱȱȱ¢ȱ ȱȱȱŘǰȱ¢ȱȱȱ ȱȱȱȱȱȱȱȱȱȱ řǯȱȱ¢ȱȱȱȱȱȱ ȱŗǯřŘȬ ȱǻȱŜǼǯȱ¢ȱȱȱȱȱǯȱ 1.65 mm (1.48 ± 0.08 mm, n = 25). Z3 actively However, harems have been reported in three ȱȱȱȱȱȱǰȱĴȱȱ¢ȱ species, namely P. formica (Monod 1926, Upton ȱȱȱǯȱȱĴǰȱ¢ȱȱȱ 1987), G. maxillaries (Mouchet, 1928) and C. calva ŘȬŗŘȱȱǻśǯŝśȱƹȱŚǯŝşȱǰȱƽŚǼȱȱ ȱ (Wägele, 1988). In this study, gnathiid adults ¢ȱȱȱřǯȱ ȱȱȱȱȱȱȱȱĴȱ ȱȱǯȱȱȱȱȱȱ
Figure 4.ȱ£ȱřDzȱDZȱǰȱȱȱȱ¢DzȱDZȱȱȱȱ¢ǯ Bull. Eur. Ass. Fish Pathol., 35(5) 2015, 181
Figure 5.ȱȱȱȱ£ȱřȱȱȱȱǯ in the wild where gnathiid adults have been ȱȱȱȱȱȱǰȱȱ corals, barnacle nests, and polychaete worm tubes where they dwell and reproduce (Cohen and Poore, 1994; Tanaka and Nishi, 2008).
ȱ ȱȱȱ¢ȱȱ ȱŗǯŞŖȱȱŗǯŞřȱ ȱǻŗǯŞŘȱƹȱŖǯŖŘȱǰȱȱƽȱŘǼǯȱȱȱȱ has large pereon with a distinctive ovary and/ or larvae development (Figure 7). Gnathiidae Figure 6. ȱȱȱCaecognathia coralliophila. ȱȱȱȱȱ¡¢ȱŘŖȱȱ ȱȱǯȱȱȱȱȱȱ¢ȱȱ ȱȱȱȱȱȱȱȱ£ȱ- pendent (Klitgaard, 1997). Due to the environ- ment it is inconclusive whether C. coralliophila ȱȱȱǯȱȱȱ ȱȱȱ ǰȱ¢ȱǻŜǚŘȂŗŗǯŜśȄǰȱŗŗŜǚŝȂŝǯŘŚȄǼǰȱ where the weather is almost constant ranging ȱŘŞȬřŘȱǚȱȱȱ¢ǯȱ - ȱȱ¢ǰȱ¢ȱȱ¢ȱȱȱȱǻȱ and Davies, 2004). Species such as G. africana are non-seasonal (Smit et al., 2003) whereas P. Figure 7. ȱȱȱCaecognathia coralliophila. formica (Hesse, 1864) and C. calva exhibit sea- ȱĴȱǻȱȱǰȱŘŖŖŖǼǯ 182, Bull. Eur. Ass. Fish Pathol., 35(5) 2015
Figure 8.ȱȱȱȱȱȱ¢ȱȱC. coralliophila. Z: Zuphea, P: Praniza.
ȱȱȱȱȱȱ Acknowledgement ȱȱęǯȱȱȬ¢ȱȱȱ- ȱ¢ȱ ȱę¢ȱȱ¢ȱȱ sociated to the ecology and its hosts have been ¢ȱȱȱ¢ȱȱ¢ȱ ȱ¢ȱ ĴȱǻŗşşŚǼǰȱ Ĵȱȱȱ Malaysia Sabah through research grants No. ǻŗşşŞǼȱȱȱȱǯȱǻŘŖŗŘǼǯȱȱȱ COE0007 and SBK0120-STWN-2013. existed during earlier gnathiid studies, par- ¢ȱȱȱęȱȱȱȱ References ěȱȱȱȱȱǯȱ ǰȱ Amanieu M (1963). Evolution des populations de Paragnathia formica (Hesse) au cours ȱȱȱȱ¢ȱȱȱęȱ d’un cycle annuel. Bulletin de L’Institut through many recent studies, concluding that Océanographique, Monaco 60, 1-12. ȱȱȱȱȱȱȱȱ Chong YT, Ota Y, Hatai K and Ransangan ¢ȱ ȱ¢ȱȱȬȱȱȱ ȱ ǻŘŖŗśǼǯȱ ȱ ȱ Caecognathia (Smit and Davies, 2004). Similarly, C. coral- coralliophila (Monod, 1926) (Crustacea, liophilaȱȱȱȱȱ¢ȱȱȱȱ Ǽȱȱȱȱęȱ¢ȱȱ Borneo Island. Proceedings of the Biological ȱȱ¢ȱǻȱŞǼǰȱęȱȱ¡- Society of Washington 128, 51-62. ȱȱȱȱȱȱȱȱȱ Cohen BF and Poore GCB (1994). Phylogeny by our study. Bull. Eur. Ass. Fish Pathol., 35(5) 2015, 183
ȱ ¢ȱ ȱ ȱ ȱ ûȱ ȱǻŗşşřǼǯȱ ȱȱȱȱ ǻDZȱ Ǽȱ ȱȱȱ in the Tioman Archipelago, Malaysia, with ȱȱȱǰȱȱȱȬ ȱȱ ȱ ȱȱǻDZȱ eastern Australia. Memoirs of the Museum of Isopoda: Cymothoidea). Ĵȱȱ Victoria 54, 271-397. dem Zoologischen Museum in Berlin 69, 3-17. Grutter AS (1994). Spatial and temporal Ota Y, Hoshino O, Hirose M, Tanaka K and ȱȱȱȱȱȱȱ ȱȱǻŘŖŗŘǼǯȬȱȱȱ ęȱȱȱ£ȱ ȱȱ ȱ ȱęȱȱȱȱȱȱ Island, Australia. Marine Ecology Progress the temporary parasitic isopod, Gnathia Series 115, 21-30. trimaculata (Crustacea; Gnathiidae). Marine Biology 159, 2333-2347. ĴȱȱȱȱȱǻŗşşŞǼǯȱ ęȱ ȱęȱȱ ȱȱ Paperna I and Por FD (1977). Preliminary data £ȱȱȱȱȱȱȱ ȱȱ ȱ ȱȱȱȱ ȱȱȱȱȱęǯȱMarine ȱ ǰȱ ȱ Ĵȱ ǰȱ £ȱ ǰȱ Ecology Progress Series 164, 263-271. Egypt and the Eastern Mediterranean ȱȱ¢ȱȱGnathia piscivora new Hesse E (1864). Mémoire sur les pranizes et species. Procès-Verbaux de la Commission les ancés et sur les moyens curieux àl’aide ȱȱȂ¡ȱęȱ dequels certains crustacés parasites assurent de la Mer Méditerranée 24,195-198. la conservation de leur espèce. Mémoires couronnés et mémoires des savants étrangers Schotte M, Boyko CB, Bruce NL, Poore 18, 231-302. GCB, Taiti S and Wilson GDF (eds.) 2008 onwards. Isopoda statistics. In “World Klitgaard AB (1991). Gnathia abyssorum (GO list of marine, freshwater and terrestrial Sars, 1872) (Crustacea, Isopoda) associated isopod crustaceans”. Available at: ĴDZȦȦ with sponges. Sarsia 76, 33-39. www.marinespecies.org/isopoda (Last Klitgaard AB (1997). The distribution and accessed 20 April 2015). ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ǰȱȱȱȱȱȱ ȱǻŘŖŖřǼǯȱȱ gnathiid species (Crustacea, Isopoda) and ¢ȱȱȱ¢ȱęȱǰȱGnathia their reproductive biology in the Denmark africana (Crustacea: Isopoda: Gnathiidae). Strait and North Iceland. Meddelelser om Folia Parasitologica 50, 135-142. Grønland, Bioscience 47, 1-32. Smit NJ and Davies AJ (2004). The curious McKiernan JP, Grutter AS and Davies Ȭ¢ȱȱȱȱȱȱȱ ȱ ǻŘŖŖśǼǯȱ ȱ ȱ ȱ isopods. Advances in Parasitology 58, 289-391. ¢ȱȱȱȱȱȱ ĴȱȱǻHemiscyllium ocellatum) ȱ ȱǻŗşŖŚǼǯȱȱȱȬ¢ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱ ȱGnathia maxillaris (Isopoda). Ĵȱ ȱ ȱ ȱ ǯȱ aus dem Zoologischen Station zu Neapel 16, International Journal for Parasitology 35, 19-27. 469-479. ȱ ȱ ǻŗşŘŜǼǯȱ ȱ ȱ ȱ ȱ ȱȱǻŗşŜŘǼǯȱ¢ȱ·ȱȱParagnathia Gnathiidae, including the morphology, formicaȱǻ Ǽȱǻ ȱȮȱ Ǽǯȱ ¢ȱ ȱ ¢ȱ ȱ ȱ ǯȱ Cahiers de Biologie Marine 3, 401- 416. Mémoires de la Société des Sciences Naturelles ȱ ȱ ǻŘŖŖŝǼǯȱ ȱ ¢ȱ ȱ ȱ du Maroc 13, 1-668. ȱȮȱȱ ȱȱȱ ȱȱǻŗşŘŞǼǯȱȱȱȱ¢ȱȱȱ directions. Plankton and Benthos Research Gnathiidae. Bulletin de la Société Zoologique 2, 1-11. de France 53, 392-400. Tanaka K and Aoki M (1998). Crustacean 184, Bull. Eur. Ass. Fish Pathol., 35(5) 2015
ȱȱȱȱHalichondria okadaiȱǻ Ǽȱ ȱȱȱȱȱ ¢ȱȱGnathia sp. (Isopoda: Gnathiidae). In “Sponge Science: multidisciplinary perspectives” (Y. Watanabe N, Fusetani, Eds.) pp 259-267 Springer-Verlag, Tokyo. Tanaka K and Aoki M (1999). Spatial distribution ĴȱȱȱȬ ȱȱ isopod Elaphognathia cornigera (Nunomura) ȱȱȱ¢ȱȱȱȱ £ȱ Peninsula, southern Japan. Crustacean Research 28, 160-167. Tanaka K and Aoki M (2000). Seasonal traits ȱ ȱ ȱ ȱ ȱ ȱ Elaphognathia cornigera (Nunomura, 1992). Zoological Science 17, 467-475. Tanaka K and Nishi E (2008). Habitat use by the gnathiid isopod Elaphognathia discolor living in terebellid polychaete tubes. Journal of the Marine Biological Association of the United Kingdom 88, 57-63. Tinsley MC and Reilly SD (2002). Reproductive ¢ȱȱȱȬ ȱȱ ectoparasite Paragnathia formica (Crustacea: Isopoda). Journal of the Marine Biological Association of the United Kingdom 82, 79-84. Upton NPD (1987). Asynchronous male and ȱȬ¢ȱȱȱ¡¢ȱǰȱ ȬȱȱParagnathia formica (Crustacea, Isopoda). Journal of Zoology 212, 677-690. §ȱ ȱ ǻŗşŞŝǼǯȱ ȱ ȱ ȱ ¢ȱȱȱȱȱęȱ parasite Gnathia calvaȱãěȱǻDZȱ Isopoda) and synonymy with Heterognathia Amar & Roman. Polar Biology 7, 77-92. §ȱ ȱǻŗşŞŞǼǯȱȱȱȱȬ¢ȱ ȱȱȱęȱȱGnathia calva ãěȱ ǻDZȱ Ǽǯȱ Polar Biology 8, 287-291.