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First record of the genus Anuropodione Bourdon, 1967 (Crustacea: Isopoda: Bopyridae) from the South Atlantic

Abstract

The family Bopyridae Rafinesque, 1815 is comprised of parasitic isopods with a life cycle involving an intermediate host (copepod) and a definitive host (decapod crustacean). The genus Anuropodione Bourdon, 1967 occurs in all oceans and encompasses five species that are only known as parasites of squat lobsters belonging to the genus Munida Leach, 1820. Despite the broad distribution of the genus, no species has ever been recorded from the South Atlantic. A total of 416 specimens of Munida iris A. Milne-Edwards, 1880 were collected in Potiguar Basin around the isobaths of 400 m, including 24 individuals (5.77%) containing parasites within their branchial chambers. Male parasites showed considerable variability in the number of pleomeres, with many showing four pleomeres, a number previously unknown for males of any species in the genus. These specimens represent the first occurrence of the genus Anuropodione and the species A. carolinensisMarkham, 1974 from the South Atlantic (Brazilian waters).

Keywords:
Anuropodione carolinensis; deep-sea; Brazil; Munida iris; parasitic isopod

The isopod family Bopyridae Rafinesque, 1815Rafinesque, C.S. 1815. Analyse de la Nature ou Tableau de l'Univers et des Corps Organisés. Palerme, 224p. contains species that are parasites of calanoid copepods as their intermediate hosts and decapod crustaceans as their definitive hosts. These parasites are usually found as a female and male pair in the branchial chamber of the definitive host, causing deformations in the carapace of the host or they can occur ventrally under the pleon of the host (Boyko and Williams, 2009Boyko, C.B. and Williams, J.D. 2009. Crustacean Parasites as Phylogenetic Indicators in Decapod Evolution. p. 197-220. In: J.W. Martin, K.A. Crandalland D.L. Felder (eds), Decapod Crustacean Phylogenetics, Crustacean Issues, Vol. 18. CRC Press Taylor & Francis Group.; Williams and Boyko, 2012Williams, J.D. and Boyko, C.B. 2012. The global diversity of parasitic isopods associated with crustacean hosts (isopoda: Bopyroidea and Cryptoniscoidea). PLoS One, 7: e35350.). According to Cardoso (2010Cardoso, I.A. 2010. Paragigantione americana Markham, 1973. p. 62-63. In: H.P. Lavrado and M.S. Brasil (eds), Biodiversidade da Região Oceânica Profunda da Bacia de Campos: Megafauna e Ictiofauna Demersal. Rio de Janeiro, SAG Serv.), Segadilha (2017Segadilha, J.L. 2017. Bopyridae. In: Catálogo Taxonômico da Fauna do Brasil PNUD. . Available from: Available from: http://fauna.jbrj.gov.br/fauna/faunadobrasil/154907 . Accessed on 19 september 2017.
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), Brito et al. (2018Brito, A.; Cardoso, I.A. and Boyko, C.B. 2018. A new species of Pseudione Kossmann, 1881 (Crustacea, Isopoda, Bopyridae) parasitizing the squat lobster Munida microphthalma A. Milne-Edwards, 1880 in the Southwestern Atlantic. Zootaxa, 4377: 444-450.), and Horch et al. (2018Horch, A.P.; Huber, A.F.; Araujo, P.B. and Ribeiro, F.B. 2018. A new species of Pseudione Kossmann, 1881 (Isopoda, Cymothoida, Bopyridae) parasitizing the lobster Nephropsis aculeata Smith, 1881 (Decapoda, Astacidea, Nephropidae) in the Southwestern Atlantic. Zootaxa, 4461: 245-252.), approximately 23 bopyrid species have been recorded from Brazilian waters, ranging from rivers (near coastal zones) as parasites of prawns (e.g., MacrobrachiumBate, 1868Bate, C.S. 1868. On a new genus, with four new species, of freshwater prawns. Proceedings of the Zoological Society of London, 1868: 363-368.) to the deep-sea, where they have been found parasitizing species of MunidaLeach, 1820Leach, W.E. 1820. Galatéadées, Galateadae. Dictionnaire des Sciences Naturelles, dans Lequel on Traite Méthodiquement des Différens êtres de la Nature, Considérés soit en eux-mêmes, d'après l'État Actuel de nos Connoissances, soit relativement a l'Utilité qu'en Peuvent Retirer la Médecine, l'Agriculture, le Commerce et les Artes. Suivi d'une Biographie des plus Célèbres Naturalistes, 18: 49-59., NephropsisWood-Mason, 1872Wood-Mason, J. 1872. On Nephropsis stewarti, a new genus and species of macrourus crustaceans, dredged in deep water off the eastern coast of the Andaman Islands. Proceedings of the Asiatic Society of Bengal, 1872: 1-151. and ParalomisWhite, 1856White, A. 1856. Some remarks on Crustacea of the genusLithodes with a brief description of a species apparently hitherto unrecorded. Proceedings of the Zoological Society of London, 1856: 132-135..

The genus AnuropodioneBourdon, 1967Bourdon, R. 1967. Sur trois nouveaux Bopyrides de Senegal. Bulletin de l'Institut Francaise d'Afrique Noire, 29: 107-122. has a widespread distribution, occurring in all oceans, especially in relatively deep waters around 200-700 m (Williams and Brown, 1972Williams, A.B. and Brown, W.S. 1972. Notes on structure and parasitism of Munida iris A. Milne-Edwards (Decapoda, Galatheidae) from North Carolina, U.S.A. Crustaceana, 22: 303-308.; Wenner and Windsor, 1979Wenner, E.L. and Windsor, N.T. 1979. Parasitism of galatheid crustaceans from the Norfolk Canyon and Middle Atlantic Bight by bopyrid isopods. Crustaceana, 37: 293-303.), and is composed of five species: A. amphiandra (Codreanu, Codreanu and Pike, 1966Codreanu, R.; Codreanu, M. and Pike, R.B. 1966. Pleurocrypta amphiandra n. sp., bopyrien parasite branchial de Munida iris ruttlanti [sic], galatheide [sic] d’Algérie et les effets d’interbiomorphose. p. 1071-1072. In: A. Corradetti (ed), Proceedings of the First International Congress of Parasitology (Roma, 21-26 September 1964), Vol. 2. Oxford, Pergamon Press.), A. carolinensisMarkham, 1974Markham, J.C. 1974. Six new species of bopyrid isopods parasitic on galatheid crabs of the genus Munida in the western Atlantic. Bulletin of Marine Science, 23: 613-648., A. dubius (Nierstrasz and Brender à Brandis, 1929Nierstrasz, H.F. and Brender à Brandis, G.A. 1929. Papers from Dr. Th. Mortensen's Pacific Expedition 1914-16. 48. Epicaridea 1. Videnskabelige Meddelelser fra Dansk Naturhistorisk Forening i Kjobenhavn, 87: 1-44.), A. megacephalonMarkham, 1974Markham, J.C. 1974. Six new species of bopyrid isopods parasitic on galatheid crabs of the genus Munida in the western Atlantic. Bulletin of Marine Science, 23: 613-648. and A. senegalensisBourdon, 1967Bourdon, R. 1967. Sur trois nouveaux Bopyrides de Senegal. Bulletin de l'Institut Francaise d'Afrique Noire, 29: 107-122. (Boyko et al., 2008Boyko, C.B.; Bruce, N.L.; Hadfield, K.A.; Merrin, K.L.; Ota, Y.; Poore, G.C.B.; Taiti, S.; Schotte, M. and Wilson, G.D.F. (eds) (2008 onwards). World Marine, Freshwater and Terrestrial Isopod Crustaceans database. Anuropodione Bourdon, 1967. Accessed through: World Register of Marine Species at: Accessed through: World Register of Marine Species at: http://www.marinespecies.org/aphia.php?p=taxdetails&id=248435 . Accessed on 29 August 2018.
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onwards). To date, species of Anuropodione have only been recorded as parasites of squat lobsters, especially those belonging to the genus Munida (Williams and Brown, 1972Williams, A.B. and Brown, W.S. 1972. Notes on structure and parasitism of Munida iris A. Milne-Edwards (Decapoda, Galatheidae) from North Carolina, U.S.A. Crustaceana, 22: 303-308.; Markham, 1974Markham, J.C. 1974. Six new species of bopyrid isopods parasitic on galatheid crabs of the genus Munida in the western Atlantic. Bulletin of Marine Science, 23: 613-648.; Wenner and Windsor, 1979Wenner, E.L. and Windsor, N.T. 1979. Parasitism of galatheid crustaceans from the Norfolk Canyon and Middle Atlantic Bight by bopyrid isopods. Crustaceana, 37: 293-303.); the host of A. dubius is not certain as it was given as “Galathea spec.” by Nierstrasz and Brender à Brandis (1929Nierstrasz, H.F. and Brender à Brandis, G.A. 1929. Papers from Dr. Th. Mortensen's Pacific Expedition 1914-16. 48. Epicaridea 1. Videnskabelige Meddelelser fra Dansk Naturhistorisk Forening i Kjobenhavn, 87: 1-44.). Despite wide distribution of the genus, no species of Anuropodione has ever been recorded from the South Atlantic. In this paper we report the first occurrence of the genus Anuropodione and the species A. carolinensisMarkham, 1974Markham, J.C. 1974. Six new species of bopyrid isopods parasitic on galatheid crabs of the genus Munida in the western Atlantic. Bulletin of Marine Science, 23: 613-648. collected as a parasite of the squat lobsters M. iris A. Milne-Edwards, 1880Milne-Edwards, A. 1880. Reports on the results of dredging under the supervision of Alexander Agassiz, in the Gulf of Mexico and in the Caribbean Sea, etc. VIII. Études préliminaires sur les Crustacés. Bulletin of the Museum of Comparative Zoology at Harvard College, 8: 1-68., from Brazilian waters in the South Atlantic.

The sampling was carried out on the continental slope of Potiguar Basin, located in the northeast of Brazil (03/05°S, 38/35°W), covering the states of Ceará (CE) and Rio Grande do Norte (RN). Specimens were collected on board the R/V Seward Johnson in May 2011, as part of the project Avaliação da biota bentônica e planctônica da Bacia Potiguar e Ceará (Bpot) coordinated by Petróleo Brasileiro S/A (Petrobras). Bottom trawls were carried out on the continental slope between 150 and 2068 m depth using a semi-balloon otter trawl with 50 mm mesh size and 18 m of mouth opening.

After sampling, specimens were fixed in 70% ethanol, with parasites initially identified to species following Markham (1974Markham, J.C. 1974. Six new species of bopyrid isopods parasitic on galatheid crabs of the genus Munida in the western Atlantic. Bulletin of Marine Science, 23: 613-648.) and deposited in the carcinological collection of the "Museu de Oceanografia Prof. Petrônio Alves Coelho (MOUFPE)" at the Federal University of Pernambuco in Recife, Brazil. The following body measurements were taken with a caliper (0.01 mm): total length (TL) (for M. iris and A. carolinensis); carapace length (CL) and carapace width (CW) (for M. iris); maximum pereon width (W) (for A. carolinensis).

Systematics

Family Bopyridae Rafinesque, 1815Rafinesque, C.S. 1815. Analyse de la Nature ou Tableau de l'Univers et des Corps Organisés. Palerme, 224p.

Subfamily Pseudioninae Codreanu, 1967Codreanu, R. 1967. Clasificarea evolutiva a bopirienilor, isopode parazite ale crustaceelor decapode si importanta lor biologica generala. Studii si Cercetari de Biologie Seria Zoologie, 19: 203-211.

Genus Anuropodione Bourdon, 1967Bourdon, R. 1967. Sur trois nouveaux Bopyrides de Senegal. Bulletin de l'Institut Francaise d'Afrique Noire, 29: 107-122.

Anuropodione carolinensis Markham, 1974Markham, J.C. 1974. Six new species of bopyrid isopods parasitic on galatheid crabs of the genus Munida in the western Atlantic. Bulletin of Marine Science, 23: 613-648.

(Figs. 1-4)

Figure 1
Munida iris A. Milne-Edwards, 1880Milne-Edwards, A. 1880. Reports on the results of dredging under the supervision of Alexander Agassiz, in the Gulf of Mexico and in the Caribbean Sea, etc. VIII. Études préliminaires sur les Crustacés. Bulletin of the Museum of Comparative Zoology at Harvard College, 8: 1-68., female (MOUFPE 17607) parasitized by Anuropodione carolinensisMarkham, 1974Markham, J.C. 1974. Six new species of bopyrid isopods parasitic on galatheid crabs of the genus Munida in the western Atlantic. Bulletin of Marine Science, 23: 613-648., collected in Potiguar Basin, #MT-61, 04°47.83’S, 36°11.02’W, 418 m, Rio Grande do Norte, northeastern Brazil. Scale bar = 1 cm.

Figure 2
Anuropodione carolinensisMarkham, 1974Markham, J.C. 1974. Six new species of bopyrid isopods parasitic on galatheid crabs of the genus Munida in the western Atlantic. Bulletin of Marine Science, 23: 613-648. (MOUFPE 18874), Potiguar Basin, station #MT-61, 418 m, Rio Grande do Norte, northeastern Brazil. (A) Mature female, dorsal; (B) mature female, ventral; (C) abdomen and pleotelson, detail; (D) antenna and antennule; (E) maxilliped (left and right); (F) barbula; (G) oostegite 1; (H) pereopod 1; (I) pereopod 7. Scale bar = A, B, 5 mm; C, 2 mm; D-G, 0.5 mm; H, I,1 mm.

Figure 3
Anuropodione carolinensisMarkham, 1974Markham, J.C. 1974. Six new species of bopyrid isopods parasitic on galatheid crabs of the genus Munida in the western Atlantic. Bulletin of Marine Science, 23: 613-648. (MOUFPE 18874), Potiguar Basin, station #MT-61, 418 m, Rio Grande do Norte, northeastern Brazil. (A) Male dorsal; (B) male ventral; (C) male with pleomere fused in dorsal view; (D) male with pleomere fused in ventral view. Scale bar = A-E, 1 mm.

Figure 4
Geographic distribution of Anuropodione carolinensisMarkham, 1974Markham, J.C. 1974. Six new species of bopyrid isopods parasitic on galatheid crabs of the genus Munida in the western Atlantic. Bulletin of Marine Science, 23: 613-648. in the Western Atlantic. Black circles = previous records; black star = new record.

Anuropodione carolinensisMarkham, 1974Markham, J.C. 1974. Six new species of bopyrid isopods parasitic on galatheid crabs of the genus Munida in the western Atlantic. Bulletin of Marine Science, 23: 613-648.: 620-624, 627, 629, 647, figs. 5-8; -Wenner and Windsor, 1979Wenner, E.L. and Windsor, N.T. 1979. Parasitism of galatheid crustaceans from the Norfolk Canyon and Middle Atlantic Bight by bopyrid isopods. Crustaceana, 37: 293-303.: 294-302, figs. 2-4; -Wenner, 1982: 362 (mention); -Ross, 1983Ross, D.M. 1983. Symbiotic Relations. p. 163-212. In: F.J. Vernberg and W.B. Vernberg (eds), The Biology of Crustacea. Volume 7. Behavior and Ecology. New York, Academic Press.: 157 (list); -Williams, 1984Williams, A.B. 1984. Shrimps, Lobsters, and Crabs of the Atlantic Coast of the Eastern United States, Maine to Florida. Washington, D.C., Smithsonian Institution Press, 550p.: 234 (mention); -Markham, 1988Markham, J.C. 1988. Descriptions and revisions of some species of Isopoda Bopyridae of the north western Atlantic Ocean. Zoologische Verhandelingen, 246: 1-63.: 55 (list); -Román-Contreras, 1993Román-Conteras, R. 1993. Aspectos Biológicos de Probopyrus Pacificensis Román-Contreras, 1993, Parásito del Langostino Macrobrachium tenellum (Smith, 1871) en la Laguna Coyuca, Guerrero, México. Universidad Nacional Autónoma de México, Facultad de Ciencias, Doctor en Ciencias (Biología), 86p. [Unpublished]: 46 (mention); -McDermott, 2002McDermott, J.J. 2002. Relationships between the parasitic isopods Stegias clibanarii Richardson, 1904 and Bopyrissa wolffi Markham, 1978 (Bopyridae) and the intertidal hermit crab Clibanarius tricolor (Gibbes, 1850) (Anomura) in Bermuda. Ophelia, 56: 33-42.: 39 (mention); -Oliveira and Masunari, 2006Oliveira, E. and Masunari, S. 2006. Distribuição temporal de densidade de Aporobopyrus curtatus (Richardson) (Crustacea, Isopoda, Bopyridae), um parasito de Petrolisthes armatus (Gibbes) (Crustacea, Anomura, Porcellanidae) na Ilha do Farol, Matinhos, Paraná, Brasil. Revista brasileira de Zoologia, 23: 1188-1195.: 1194 (mention); -Romero-Rodríguez and Román-Contreras, 2008Romero-Rodríguez, J. and Román-Contreras, R. 2008. Aspects of the reproduction of Bopyrinella thorii (Richardson, 1904) (Isopoda, Bopyridae), a branchial parasite of Thor floridanus Kingsley, 1878 (Decapoda, Hippolytidae) in Bahía de la Ascensión, Mexican Caribbean. Crustaceana, 81: 1201-1210.: 1207-1208 (mention); -Thoma and Heard, 2010Thoma, J.N. and Heard, R.W. 2010. A key to epicaridean isopods of the South Atlantic Bight. Available from: Available from: http://www.dnr.sc.gov/marine/sertc/Thoma%20%20Heard%20Epicaridean%20key.pdf. Accessed on 05 December 2018.
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: 3 (list), 16 (key), 18 (key), fig. 12a, b, 14e; -Boyko et al., 2012Boyko, C.B.; Williams, J.D. and Markham J.C. 2012. Recent and fossil Isopoda Bopyridae parasitic on squat lobsters and porcelain crabs (Crustacea: Anomura: Chirostyloidea and Galatheoidea), with notes on nomenclature and biogeography. Zootaxa, 3150: 1-35.: 4, 18 (list); -McLaughlin et al., 2005McLaughlin, P.A.; Camp, D.K.; Angel, M.V.; Bousfield, E.L.; Brunei, P.; Brusca, R.C.; Cadien, D.; Cohen, A.C.; Conlan, K.; Eldredge, L.G.; Felder, D.L.; Goy, J.W.; Haney, T.; Hann, B.; Heard, R.W.; Hendrycks, E.A.; Hobbs III, H.H.; Holsinger, J.R.; Kensley, B.; Laubitz, D.R.; LeCroy, S.E.; Lemaitre, R.; Maddocks, R.F.; Martin, J.W.; Mikkelsen, P.; Nelson, E.; Newman, W.A.; Overstreet, R.M.; Poly, W.J.; Price, W.W.; Reid, J.W.; Robertson, A.; Christopher Rogers, D.; Ross, A.; Schotte, M.; Schram, F.R.; Chiang-Tai, S.; Watling, L. and Wilson G.D. 2005. Common and scientific names of aquatic invertebrates from the United States and Canada: Crustaceans. American Fisheries Society Special Publication, 31: 1-326.: 187 (list); -Penha-Lopez et al., 2013Penha-Lopes, G.; Marques, J.F.; Leal, M.C.; Carvalho, A.F. and Paula, J. 2013. Population structure and reproduction of Pseudione elongata africana (Bopyridae, Isopoda). Western Indian Ocean Journal of Marine Science, 11: 27-39.: 35 (mention); -Cericola and Williams, 2015Cericola, M.J. and Williams, J.D. 2015. Prevalence, reproduction and morphology of the parasitic isopod Athelges takanoshimensis Ishii, 1914 (Isopoda: Bopyridae) from Hong Kong hermit crabs. Marine Biology Research, 11: 236-252.: 239 (list).

Anuropodione sp. Williams and Brown, 1972Williams, A.B. and Brown, W.S. 1972. Notes on structure and parasitism of Munida iris A. Milne-Edwards (Decapoda, Galatheidae) from North Carolina, U.S.A. Crustaceana, 22: 303-308.: 307 (mention); -Bursey, 1978Bursey, C.R. 1978. Histopathology of the parasitization of Munida iris (Decapoda: Galatheidae) by Munidion irritans (Isopoda: Bopyridae). Bulletin of Marine Science, 28: 566-570.: 569 (mention).

Anuropodione [sp.] Ross, 1983Ross, D.M. 1983. Symbiotic Relations. p. 163-212. In: F.J. Vernberg and W.B. Vernberg (eds), The Biology of Crustacea. Volume 7. Behavior and Ecology. New York, Academic Press.: 168 (mention).

Host material examined. Brazil: 1 female (28.26 mm TL, 25.41 mm CL; 23.37 mm CW), 1 male (22.69 mm TL, 20.24 mm CL, 17.11 mm CW), Potiguar Basin, #MT-61, 04°47.83’S 36°11.02’W, 418 m, temperature 8.15°C, 08.v.2011 (MOUFPE 17607) (Fig. 1); 2 females (18.25-28.3 mm TL, 16.69-25.38 mm CL, 13.07-22.24 mm CW), 4 males (20.52-26.89 mm TL, 18.45-24.01 mm CL, 15.58-17.98 mm CW), Potiguar Basin, #MT-62, 04°43.89'S 36°25.62'W, 415 m, temperature 7.56°C, 07.v.2011 (MOUFPE 17608); 9 females (20.52-26.89 mm TL, 16.86-24.09 mm CL, 9.19-18.84 mm CW), 7 males (17.21-28.47 mm TL, 15.61-25.89 mm CL, 14.86-20.31 mm CW), Potiguar Basin, #MT-64, 04°36.24’S, 36°45.73’W, 416 m, temperature 7.47°C, 12.v.2011 (MOUFPE 17609).

Parasite material examined. Brazil: 2 females (10.3-12.4 mm TL, 5.2-6.3 mm W), 2 males (3.4-4.2 mm TL, 2.5-3.1 mm W), Potiguar Basin, #MT-61, 04°47.83’S 36°11.02’W, 418 m, temperature 8.15°C, 08.v.2011 (MOUFPE 18874); 6 females (10.4-11.3 mm TL, 4.1-5.8 mm W), 6 males (2.6-3.4 mm TL, 2.1-2.8 mm W), Potiguar Basin, #MT-62, 04°43.89'S 36°25.62'W, 415 m, temperature 7.56°C, 07.v.2011 (MOUFPE 18875); 16 females (10.5-12.9 mm TL, 4.7-5.3 mm W), 16 males (2.8-3.1 mm TL, 2.3-2.9 mm W), Potiguar Basin, #MT-64, 04°36.24’S 036°45.73’W, 416 m, temperature 7.47°C, 12.v.2011 (MOUFPE 18876).

Diagnosis. Female: Body ovate, all segments and body regions distinct. Head with large frontal lamina; anterior margin smooth; eyes absent. Antennula with two articles, antenna of four articles. Maxilliped without palp; barbula with two smooth, falcate, lateral projections, median region smooth. Large coxal plates on all pereomeres; dorsolateral bosses on pereomeres 1-4; oostegite 1 posterior segment shorter than anterior, with few lobes on inner margin. Posterior pereopods much larger than anterior ones; bases with expanded dorsal carinae. Pleomeres tapering posteriorly; lateral plates present on pleomeres 1-4; pleotelson bulbous; biramous pleopods on pleomeres 1-5; uropods lacking.

Male: Pereon widest at pereomere 5, tapering anteriorly and posteriorly; all segments distinct. Antennula of two-three articles, antenna of three-five articles. Pereopods subequal in size and shape. Pleon with segmentation ranging from all segments fused to six distinct segments; pleopods and uropods absent.

Distribution. Western Atlantic: United States (North Carolina and Gulf of Mexico) and Brazil (Potiguar Basin, Rio Grande do Norte) (Markham, 1974Markham, J.C. 1974. Six new species of bopyrid isopods parasitic on galatheid crabs of the genus Munida in the western Atlantic. Bulletin of Marine Science, 23: 613-648.; Wenner, 1982Wenner, E.L. 1982. Notes on the distribution and biology of Galatheidae and Chirostylidae (Decapoda: Anomura) from the Middle Atlantic Bight. Journal of Crustacean Biology, 2: 360-377.; present study) (Fig. 4).

Remarks. A total of 416 specimens of M. iris were collected in Potiguar Basin, comprising 24 hosts (5.77%) bearing A. carolinensis in the branchial chambers (Fig. 1), females (Fig. 2 A-I) of which conformed in all characters with the description of Markham (1974Markham, J.C. 1974. Six new species of bopyrid isopods parasitic on galatheid crabs of the genus Munida in the western Atlantic. Bulletin of Marine Science, 23: 613-648.). Markham (1974Markham, J.C. 1974. Six new species of bopyrid isopods parasitic on galatheid crabs of the genus Munida in the western Atlantic. Bulletin of Marine Science, 23: 613-648.) stated that the antennae of females bear two articles, but this appears to have been an error because all our specimens have antennae with four articles (Fig. 2D). Additionally, all the male specimens we dissected had two or three antennular and three antennal articles, while Markham (1974Markham, J.C. 1974. Six new species of bopyrid isopods parasitic on galatheid crabs of the genus Munida in the western Atlantic. Bulletin of Marine Science, 23: 613-648.) reported three antennular and five antennal articles. Parasitization most frequently occurred in adult hosts without distinction as to the sex of the host (12 females and 12 males). A total of 24 males of A. carolinensis were examined, of which 33% (n = 8) had only a single pleomere (Fig. 3C, D), 46% (n = 11) had four pleomeres (including the pleotelson) and 21% (n = 5) had six pleomeres (including the pleotelson; Fig. 3A, B). Previous examination of A. carolinensis males were made by Markham (1974Markham, J.C. 1974. Six new species of bopyrid isopods parasitic on galatheid crabs of the genus Munida in the western Atlantic. Bulletin of Marine Science, 23: 613-648.) and Wenner and Windsor (1979Wenner, E.L. and Windsor, N.T. 1979. Parasitism of galatheid crustaceans from the Norfolk Canyon and Middle Atlantic Bight by bopyrid isopods. Crustaceana, 37: 293-303.), which revealed variability in the number of pleomeres with one, three, and six pleomeres being recorded; the single pleomere condition was by far the most common and very few specimens were found bearing three pleomeres. In contrast, our samples showed the most common condition as being four pleomeres for males of A. carolinensis. The presence of four pleomeres on males of this species and, in fact, on males of any species of Anuropodione was previously unknown (Boyko et al., 2018Boyko, C.B.; Williams, J.D. and Öktener, A. 2018. Redescription of the Mediterranean endemic parasitic isopod Anuropodione amphiandra (Codreanu, Codreanu & Pike, 1966) n. comb. (Crustacea: Isopoda: Bopyridae) from Munida rutllanti Zariquiey Alvarez, 1952, with new records from Turkey and a review of the genus Anuropodione Bourdon, 1967. Mediterranean Marine Science, 19: 611-619.).

Records of parasitism on M. iris by A. carolinensis were previously observed by Markham (1974Markham, J.C. 1974. Six new species of bopyrid isopods parasitic on galatheid crabs of the genus Munida in the western Atlantic. Bulletin of Marine Science, 23: 613-648.) from North Carolina (35°05'N, 75°11'W), Wenner and Windsor (1979Wenner, E.L. and Windsor, N.T. 1979. Parasitism of galatheid crustaceans from the Norfolk Canyon and Middle Atlantic Bight by bopyrid isopods. Crustaceana, 37: 293-303.) from Norfolk Canyon (36°56', 37°09'N, 75°06', 74°33'W) and Wenner (1982Wenner, E.L. 1982. Notes on the distribution and biology of Galatheidae and Chirostylidae (Decapoda: Anomura) from the Middle Atlantic Bight. Journal of Crustacean Biology, 2: 360-377.) in Norfolk Canyon (36°56', 37°09'N) and Tom's Canyon (38°18', 39°10'N), however, M. iris is also parasitized by Munidion irritansBoone, 1927Boone, P.L. 1927. Crustacea from tropical east American seas. Bulletin of the Bingham Oceanographic Collection, 1: 1-147. (Bursey, 1978Bursey, C.R. 1978. Histopathology of the parasitization of Munida iris (Decapoda: Galatheidae) by Munidion irritans (Isopoda: Bopyridae). Bulletin of Marine Science, 28: 566-570.). All of the specimens of M. iris examined herein were parasitized by individuals of both sexes of A. carolinensis (female and male pair), which were observed occurring in M. iris only at a depth of 400 m in Potiguar Basin. The depth range of parasites of A. carolinensis follow the bathymetric distribution of their hosts and, as the species of M. iris can be found in depths up to 1303 m (Melo-Filho, 2006Melo-Filho, G.A.S. 2006. Reports on the results of the N.Oc. Prof. W. Besnard expeditions to the southern coast of Brazil under the Revizee Program: Chirostylidae and Galatheidae (Crustacea: Decapoda: Anomura). Zootaxa, 1238: 1-22.). Anuropodione carolinensis is potentially present along a similar large depth range, although it has so far only been reported from 83-662 m (Boyko et al., 2012Boyko, C.B.; Williams, J.D. and Markham J.C. 2012. Recent and fossil Isopoda Bopyridae parasitic on squat lobsters and porcelain crabs (Crustacea: Anomura: Chirostyloidea and Galatheoidea), with notes on nomenclature and biogeography. Zootaxa, 3150: 1-35.). In the western Atlantic, M. iris has a large geographic distribution, occurring from the United States to Uruguay, and in Brazilian waters from Potiguar Basin (present record), Alagoas, Bahia, São Paulo and Rio Grande do Sul (Melo, 1999Melo, G.A.S. 1999. Manual de identificação dos Crustacea Decapoda do litoral brasileiro: Anomura; Thalassinidea; Palinuridea e Astacidea. São Paulo, Plêiade/Fapesp, 551p.; Melo-Filho, 2006Melo-Filho, G.A.S. 2006. Reports on the results of the N.Oc. Prof. W. Besnard expeditions to the southern coast of Brazil under the Revizee Program: Chirostylidae and Galatheidae (Crustacea: Decapoda: Anomura). Zootaxa, 1238: 1-22.; Serejo et al., 2007Serejo, C.S.; Young, P.S.; Cardoso, I.A.; Tavares, C.; Rodrigues, C. and Almeida, T.C. 2007. Abundância, diversidade e zonação dos crustáceos no talude da costa central do Brasil (11°-22°S) coletados pelo Programa REVIZEE/Score Central: prospecção pesqueira. p. 133-162. In: H.P. Lavrado, A.C. Brasil (eds), Biodiversidade da fauna marinha profunda na costa central brasileira, 2. Rio de Janeiro, Brasil, Museu Nacional.), however, despite of this wide host distribution, A. carolinensis has previously only been recorded from the southeastern United States and the Gulf of Mexico, and is only now known from Brazilian waters in the south Atlantic.

Acknowledgments

The first author would like to thank CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) for the postgraduate scholarship in Oceanography. The authors are also grateful to Petróleo Brasileiro S.A. (Petrobras) for making the material used in this study available. The authors would especially like to thank Dr. Paula Araujo for her support. The authors would like to thank the anonymous reviewers for their useful comments on this paper.

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Publication Dates

  • Publication in this collection
    28 Mar 2019
  • Date of issue
    2019

History

  • Received
    20 Sept 2018
  • Accepted
    07 Feb 2019
Sociedade Brasileira de Carcinologia Instituto de Biociências, UNESP, Campus Botucatu, Rua Professor Doutor Antônio Celso Wagner Zanin, 250 , Botucatu, SP, 18618-689 - Botucatu - SP - Brazil
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