Occurrence of Metacaligus rufus (Wilson, 1908) (Copepoda, Caligidae) parasitizing the cownose ray Rhinoptera bonasus (Mitchill, 1815) (Elasmobranchii, Myliobatidae) in Brazil

R. Ducatti V. Takatsuka V. G. Azevedo E. G. Sanches F. Paschoal J. L. Luque About the authors

The family Caligidae are predominantly external parasites of fishes, inhabiting the outer surface, the mouth, the gills and opercular cavity of their hosts (Boxshall and Halsey, 2004BOXSHALL, G.A. and HALSEY, S.H., 2004. An introduction to copepod diversity. London: The Ray Society. 940 p.). This family comprises one of the most speciose group within the Copepoda, currently encompassing 31 genera, including Metacaligus (Thomsen, 1949) which consistis of five nominal species (Walter and Boxshall, 2008WALTER, T.C. and BOXSHALL, G.A., 2008 [viewed 5 November 2016]. World of Copepods database [online]. Available from: www.marinespecies.org/copepoda
www.marinespecies.org/copepoda...
). Members of Metacaligus have been associated with actinopterygian fishes or obtained from plankton, particularly from American and Asian waters (Ho and Bashirullah, 1977HO, J.S. and BASHIRULLAH, A.K.M., 1977. Two species of caligid copepods (Crustacea) parasitic on marine fishes of Venezuela, with discussion of Metacaligus Thomsen, 1949. Journal of Natural History, vol. 11, no. 6, pp. 703-714. http://dx.doi.org/10.1080/00222937700770601.
http://dx.doi.org/10.1080/00222937700770...
; Suárez-Morales et al., 2012SUÁREZ-MORALES, E.; KIM, I.H. and ESCAMILLA, B.J., 2012. On some caligids (Copepoda: Caligidae) from plankton of a Coastal Lagoon in the Gulf of Mexico with a description of a new species of Metacaligus. Zoological Studies, vol. 51, no. 6, pp. 804-818.). In the seaboard of Brazil, two species have been hitherto recorded, i.e., Metacaligus rufus (Wilson, 1908WILSON, C.B., 1908. North American parasitic copepods: new genera and species of Caliginae. Proceedings of the United States National Museum, vol. 33, pp. 593-643.) from the gills of Merluccius sp., Oligoplites palometa (Cuvier, 1832), O. saliens (Bloch, 1793), Scomberomorus sp., Selene vomer (Linnaeus, 1758), Trichiurus lepturus (Linnaeus, 1758) and Umbrina sp.; and M. trichiuri (Krøyer, 1863) from the gills of T. lepturus (Luque and Tavares, 2007LUQUE, J.L. and TAVARES, L.E.R., 2007. Checklist of Copepoda associated with fishes from Brazil. Zootaxa, vol. 1579, pp. 1-39.; Luque et al., 2013LUQUE, J.L.; VIEIRA, F.M.; TAKEMOTO, R.M.; PAVANELLI, G.C. and EIRAS, J.C., 2013. Checklist of Crustacea parasitizing fishes from Brazil. Journal of Species List and Distribution, vol. 9, no. 6, pp. 1449-1470.).

The Cownose ray Rhinoptera bonasus (Mitchill, 1815) (Myliobatidae) is an oceanic species found occasionally in sandy bottoms near the coast, feeding a variety number of bivalve mollusks and other benthic prey (Figueiredo, 1977FIGUEIREDO, J.L., 1977. Manual de peixes marinhos do Sudeste do Brasil. I. Introdução: cações, raias e quimeras. São Paulo: Museu de Zoologia, Universidade de São Paulo. 104 p.; Froese and Pauly, 2016FROESE, R. and PAULY, D., eds., 2016 [viewed 6 November 2016]. FishBase [online]. Available from: www.fishbase.org
www.fishbase.org...
). This species is widely distributed in the Atlantic Ocean, found in the Western Atlantic: northern Florida (USA), throughout the Gulf of Mexico to south Brazil; and in the Eastern Atlantic: Mauritania, Senegal and Guinea (Froese and Pauly, 2016FROESE, R. and PAULY, D., eds., 2016 [viewed 6 November 2016]. FishBase [online]. Available from: www.fishbase.org
www.fishbase.org...
). Among the species of genus Rhinoptera, The International Union for Conservation of Nature (IUCN) listed this species as Near Threatened (NT) in relation to the state of conservation (Froese and Pauly, 2016FROESE, R. and PAULY, D., eds., 2016 [viewed 6 November 2016]. FishBase [online]. Available from: www.fishbase.org
www.fishbase.org...
; International Union for Conservation of Nature and Natural Resources, 2016INTERNATIONAL UNION FOR CONSERVATION OF NATURE AND NATURAL RESOURCES – IUCN, 2016 [viewed 20 October 2016]. Red List of Threatened Species [online]. Cambridge. Available from: http//:www.iucnredlist.org
http//:www.iucnredlist.org...
).

One specimen of Rhinoptera bonasus (body length 46 cm, weight 6,04kg) was caught in June 2016 in the coast of Ubatuba (23º27’05.4”S, 45º02’48.4”W), State of São Paulo, southeastern Brazil. The fish was taken to the Laboratório de Piscicultura Marinha of the Instituto de Pesca de São Paulo, where it was anesthetized by immersion in eugenol K-Dent® 60mg/L, diluted alcohol at a ratio of 1:5 (Griffiths, 2000GRIFFITHS, S.P., 2000. The use of clove oil as an anaesthetic and method for sampling intertidal rockpool fishes. Journal of Fish Biology, vol. 57, no. 6, pp. 1453-1464. http://dx.doi.org/10.1111/j.1095-8649.2000.tb02224.x.
http://dx.doi.org/10.1111/j.1095-8649.20...
) for monitoring of biometrics values and ectoparasites. After monitoring, collected copepods were fixed and preserved in ethanol (70% GL) and cleared in a drop of 85% lactic acid or lactophenol before examination using a phase-contrast microscope. Specimens were measured intact using an ocular micrometer, dissected and examined according to the wooden slide procedure of Humes and Gooding (1964)HUMES, A.G. and GOODING, R.U., 1964. A method for studying the external anatomy of Copepods. Crustaceana, vol. 6, no. 3, pp. 238-240. http://dx.doi.org/10.1163/156854064X00650.
http://dx.doi.org/10.1163/156854064X0065...
. Measurements based on six females and six males are given in millimetres, unless otherwise stated, with the range followed by the mean in parentheses. Host identification was based on the key of Figueiredo (1977)FIGUEIREDO, J.L., 1977. Manual de peixes marinhos do Sudeste do Brasil. I. Introdução: cações, raias e quimeras. São Paulo: Museu de Zoologia, Universidade de São Paulo. 104 p.; the nomenclature and classification are updated according to FishBase (Froese and Pauly, 2016FROESE, R. and PAULY, D., eds., 2016 [viewed 6 November 2016]. FishBase [online]. Available from: www.fishbase.org
www.fishbase.org...
). Voucher specimens of M. rufus are deposited in the Crustacea Collection of the National Museum, Rio de Janeiro (MNRJ No 28601- 3♀/28602 - 3♂), and of the Museu de Zoologia da Universidade de São Paulo (MZUSP No 36052 - 2♀/36052 - 3♂), Brazil.

Based in the morphology of cephalothorax, genital process, abdomen, small appendages and body proportion, specimens collected in Ubatuba corresponds to the description of M. rufus given by Wilson (1908)WILSON, C.B., 1908. North American parasitic copepods: new genera and species of Caliginae. Proceedings of the United States National Museum, vol. 33, pp. 593-643. and Suárez-Morales et al. (2012)SUÁREZ-MORALES, E.; KIM, I.H. and ESCAMILLA, B.J., 2012. On some caligids (Copepoda: Caligidae) from plankton of a Coastal Lagoon in the Gulf of Mexico with a description of a new species of Metacaligus. Zoological Studies, vol. 51, no. 6, pp. 804-818.. A total of 17 specimens of M. rufus were collected, all attached the external surface of the host (Figure 1A), of these, six are mature females and eleven mature males. The following measurements were made on the specimens of M. rufus, collected from R. bonasus: Female (Figure 1B), Total length (excluding setae on caudal rami), 5.01-3.97 (4.33) mm. Cephalothoracic shield oval, longer 2.71-2.59 (2.49) mm than wide 1.91-1.57 (1.73) mm. Genital complex roughly subrectangular (Figure 1C), longer 1.39-1.10 (1.24) mm than wide 0.81-0.72 (0.78) mm. Abdomen widest at proximal part (Figure 1C), longer 0.73-0.44 (0.57) mm than wide 0.36-0.20 (0.28) mm. Caudal rami longer 0.20-0.16 (0.18) mm than wide 0.14-0.07 (0.08) mm. Male (Figure 1D), Total length (excluding setae on caudal rami), 4.63-4.08 (4.28) mm. Cephalothoracic shield longer 2.57-2.36 (2.44) mm than wide 1.75-1.57 (1.66) mm. Genital complex elongate, longer 0.93-0.88 (0.90) mm than wide 0.54-0.51 (0.53) mm. Abdomen 2-segmented, first segment oblong 0.29-0.26 (0.27) mm long, 0.35-0.32 (0.33) mm wide, second segment elongate longer 0.42-0.35 (0.39) mm than wide 0.27-0.24 (0.25) mm. Caudal rami longer 0.19-0.18 (0.18) mm than wide 0.08-0.07 (0.08) mm. Females specimens from Ubatuba are larger (5.01-3.97 mm) than the specimens collected in Chelem, Mexico (3.25-3.79 mm), and probably with similar size to the type specimens, collected in North Carolina, USA (4.4 mm) (Wilson, 1908WILSON, C.B., 1908. North American parasitic copepods: new genera and species of Caliginae. Proceedings of the United States National Museum, vol. 33, pp. 593-643.; Suárez-Morales et al., 2012SUÁREZ-MORALES, E.; KIM, I.H. and ESCAMILLA, B.J., 2012. On some caligids (Copepoda: Caligidae) from plankton of a Coastal Lagoon in the Gulf of Mexico with a description of a new species of Metacaligus. Zoological Studies, vol. 51, no. 6, pp. 804-818.).

Figure 1
Metacaligus rufus (Wilson 1908WILSON, C.B., 1908. North American parasitic copepods: new genera and species of Caliginae. Proceedings of the United States National Museum, vol. 33, pp. 593-643.). (A) Infection by female specimen on the external surface: arrow showing the specimen; (B) Female, Habitus: dorsal view; (C) Female, detail of genital complex and abdomen: ventral view; (D) Male, Habitus: dorsal view; (E) Male, anterior part of Cephalothoracic shield: arrow showing the absence of sternal furca in ventral view. Scale bars: A, 8 mm; B, D 1 mm; C, E 500 µm.

According to Dojiri and Ho (2013)DOJIRI, M. and HO, J.S., 2013. Systematics of the Caligidae, copepods parasitic on marine fishes. Crustaceana Monograph Series, vol. 18, pp. 448. the genus Metacaligus can be distinguished from other genera within the Caligidae by the absence of sternal furca (Figure 1E), absence of accessory process on terminal spines 2 and 3 on exopodal segment of leg 1, three short plumose setae on inner margin of second exopodal segment of leg 1 and only one outer spine on terminal exopodal segment of leg 2. Although some species of Caligus display one or two characteristics found in the genus Metacaligus, however, the presence of all features above mentioned, support Metacaligus as a validly genus (Boxshall and Halsey, 2004BOXSHALL, G.A. and HALSEY, S.H., 2004. An introduction to copepod diversity. London: The Ray Society. 940 p.; Dojiri and Ho, 2013DOJIRI, M. and HO, J.S., 2013. Systematics of the Caligidae, copepods parasitic on marine fishes. Crustaceana Monograph Series, vol. 18, pp. 448.).

Metacaligus rufus was originally described by Wilson (1908)WILSON, C.B., 1908. North American parasitic copepods: new genera and species of Caliginae. Proceedings of the United States National Museum, vol. 33, pp. 593-643. from Bagre marinus (Mitchill, 1815) in Beaufort (USA), and since its description this species has been recorded parasitizing hosts of the families Ariidae, Carangidae, Merlucciidae, Sciaenidae, Scombridae and Trichiuridae (Luque and Tavares, 2007LUQUE, J.L. and TAVARES, L.E.R., 2007. Checklist of Copepoda associated with fishes from Brazil. Zootaxa, vol. 1579, pp. 1-39.; Suárez-Morales et al., 2012SUÁREZ-MORALES, E.; KIM, I.H. and ESCAMILLA, B.J., 2012. On some caligids (Copepoda: Caligidae) from plankton of a Coastal Lagoon in the Gulf of Mexico with a description of a new species of Metacaligus. Zoological Studies, vol. 51, no. 6, pp. 804-818.; Luque et al., 2013LUQUE, J.L.; VIEIRA, F.M.; TAKEMOTO, R.M.; PAVANELLI, G.C. and EIRAS, J.C., 2013. Checklist of Crustacea parasitizing fishes from Brazil. Journal of Species List and Distribution, vol. 9, no. 6, pp. 1449-1470.). The probable dissemination of this caligid copepod on the elasmobranch host occurred through the B. marinus that occurs in some regions with R. bonasus, inhabiting over mud and sandy bottoms of the coast of Gulf of Mexico, Cuba, western margin of the Caribbean, and the northern margin of South America (Robins and Ray, 1986ROBINS, C.R. and RAY, G.C., 1986. A field guide to Atlantic coast fishes of North America. Boston: Houghton Mifflin Company. 354 p.; Froese and Pauly, 2016FROESE, R. and PAULY, D., eds., 2016 [viewed 6 November 2016]. FishBase [online]. Available from: www.fishbase.org
www.fishbase.org...
).

Records of parasitic copepods on elasmobranch fishes in Brazil are scarce, and today of the 211 known species copepods found to parasite fishes in the Brazilian coast, only 16 have been reported from cartilaginous fishes, accounting for 10% of the total (Luque et al., 2013LUQUE, J.L.; VIEIRA, F.M.; TAKEMOTO, R.M.; PAVANELLI, G.C. and EIRAS, J.C., 2013. Checklist of Crustacea parasitizing fishes from Brazil. Journal of Species List and Distribution, vol. 9, no. 6, pp. 1449-1470.; Paschoal et al., 2016PASCHOAL, F., NAGASAWA, K. and LUQUE, J.L., 2016. A new species of Leposphilus Hesse, 1866 (Copepoda: Philichthyidae) parasitic in the interorbital canals of the whitemouth croaker Micropogonias furnieri (Desmarest) (Sciaenidae) off Brazil with an amended diagnosis of the genus. Systematic Parasitology, vol. 93, no. 5, pp. 501-515. PMid:27221003.http://dx.doi.org/10.1007/s11230-016-9637-9.
http://dx.doi.org/10.1007/s11230-016-963...
; Taborda et al., 2016TABORDA, N.L., PASCHOAL, F. and LUQUE, J.L., 2016. A new species of Ergasilus (Copepoda: Ergasilidae) from Geophagus altifrons and G. argyrostictus (Perciformes: Cichlidae) in the Brazilian Amazon. Acta Parasitologica, vol. 61, no. 3, pp. 549-555. PMid:27447219.http://dx.doi.org/10.1515/ap-2016-0073.
http://dx.doi.org/10.1515/ap-2016-0073...
). To date, there are no previous records of parasitic copepods on the cownose ray, for this in the present paper we documented the first record of a caligid copepod on R. bonasus, and the first occurrence of M. rufus parasitizing an elasmobranch host into world’s oceans.

  • (With 1 figure)

References

  • BOXSHALL, G.A. and HALSEY, S.H., 2004. An introduction to copepod diversity London: The Ray Society. 940 p.
  • DOJIRI, M. and HO, J.S., 2013. Systematics of the Caligidae, copepods parasitic on marine fishes. Crustaceana Monograph Series, vol. 18, pp. 448.
  • FIGUEIREDO, J.L., 1977. Manual de peixes marinhos do Sudeste do Brasil. I. Introdução: cações, raias e quimeras São Paulo: Museu de Zoologia, Universidade de São Paulo. 104 p.
  • FROESE, R. and PAULY, D., eds., 2016 [viewed 6 November 2016]. FishBase [online]. Available from: www.fishbase.org
    » www.fishbase.org
  • GRIFFITHS, S.P., 2000. The use of clove oil as an anaesthetic and method for sampling intertidal rockpool fishes. Journal of Fish Biology, vol. 57, no. 6, pp. 1453-1464. http://dx.doi.org/10.1111/j.1095-8649.2000.tb02224.x
    » http://dx.doi.org/10.1111/j.1095-8649.2000.tb02224.x
  • HO, J.S. and BASHIRULLAH, A.K.M., 1977. Two species of caligid copepods (Crustacea) parasitic on marine fishes of Venezuela, with discussion of Metacaligus Thomsen, 1949. Journal of Natural History, vol. 11, no. 6, pp. 703-714. http://dx.doi.org/10.1080/00222937700770601
    » http://dx.doi.org/10.1080/00222937700770601
  • HUMES, A.G. and GOODING, R.U., 1964. A method for studying the external anatomy of Copepods. Crustaceana, vol. 6, no. 3, pp. 238-240. http://dx.doi.org/10.1163/156854064X00650
    » http://dx.doi.org/10.1163/156854064X00650
  • INTERNATIONAL UNION FOR CONSERVATION OF NATURE AND NATURAL RESOURCES – IUCN, 2016 [viewed 20 October 2016]. Red List of Threatened Species [online]. Cambridge. Available from: http//:www.iucnredlist.org
    » http//:www.iucnredlist.org
  • LUQUE, J.L. and TAVARES, L.E.R., 2007. Checklist of Copepoda associated with fishes from Brazil. Zootaxa, vol. 1579, pp. 1-39.
  • LUQUE, J.L.; VIEIRA, F.M.; TAKEMOTO, R.M.; PAVANELLI, G.C. and EIRAS, J.C., 2013. Checklist of Crustacea parasitizing fishes from Brazil. Journal of Species List and Distribution, vol. 9, no. 6, pp. 1449-1470.
  • PASCHOAL, F., NAGASAWA, K. and LUQUE, J.L., 2016. A new species of Leposphilus Hesse, 1866 (Copepoda: Philichthyidae) parasitic in the interorbital canals of the whitemouth croaker Micropogonias furnieri (Desmarest) (Sciaenidae) off Brazil with an amended diagnosis of the genus. Systematic Parasitology, vol. 93, no. 5, pp. 501-515. PMid:27221003.http://dx.doi.org/10.1007/s11230-016-9637-9
    » http://dx.doi.org/10.1007/s11230-016-9637-9
  • ROBINS, C.R. and RAY, G.C., 1986. A field guide to Atlantic coast fishes of North America Boston: Houghton Mifflin Company. 354 p.
  • SUÁREZ-MORALES, E.; KIM, I.H. and ESCAMILLA, B.J., 2012. On some caligids (Copepoda: Caligidae) from plankton of a Coastal Lagoon in the Gulf of Mexico with a description of a new species of Metacaligus. Zoological Studies, vol. 51, no. 6, pp. 804-818.
  • TABORDA, N.L., PASCHOAL, F. and LUQUE, J.L., 2016. A new species of Ergasilus (Copepoda: Ergasilidae) from Geophagus altifrons and G. argyrostictus (Perciformes: Cichlidae) in the Brazilian Amazon. Acta Parasitologica, vol. 61, no. 3, pp. 549-555. PMid:27447219.http://dx.doi.org/10.1515/ap-2016-0073
    » http://dx.doi.org/10.1515/ap-2016-0073
  • WALTER, T.C. and BOXSHALL, G.A., 2008 [viewed 5 November 2016]. World of Copepods database [online]. Available from: www.marinespecies.org/copepoda
    » www.marinespecies.org/copepoda
  • WILSON, C.B., 1908. North American parasitic copepods: new genera and species of Caliginae. Proceedings of the United States National Museum, vol. 33, pp. 593-643.

Publication Dates

  • Publication in this collection
    27 Nov 2017
  • Date of issue
    Aug 2018

History

  • Received
    03 Feb 2017
  • Accepted
    24 Feb 2017
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