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Male influence on the ovarian development of the crustacean parasite Bopyrina abbreviata (Isopoda, Bopyridae)

Published online by Cambridge University Press:  15 February 2016

Jesús Romero-Rodríguez*
Affiliation:
Departamento de Biología Marina, Facultad de Veterinaria y Zootecnia, Universidad Autónoma de Yucatán (UADY), Km 15.5 carretera Mérida-Xmatkuil, Apartado Postal 4-116 Itzimná, Mérida Yucatán, Mexico
Ramiro Román-Contreras
Affiliation:
Laboratorio de Carcinoparasitología, Unidad de Ecología y Biodiversidad Acuática, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México (UNAM), Apartado Postal 70-305, Mexico, DF 04510, Mexico
José Luis Bortolini-Rosales
Affiliation:
Departamento de Biología Comparada, Facultad de Ciencias, Universidad Nacional Autónoma de México (UNAM), DF 04510, Mexico
*
Correspondence should be addressed to:J. Romero-Rodríguez, Departamento de Biología Marina, Facultad de Veterinaria y Zootecnia, Universidad Autónoma de Yucatán (UADY), Km 15.5 carretera Mérida-Xmatkuil, Apartado Postal 4-116 Itzimná, Mérida Yucatán, Mexico email: [email protected]

Abstract

The presence of a male in a population of terrestrial isopods can accelerate the onset of female reproduction, a feature that has been suggested also to occur in bopyrid isopods. This paper aims to estimate the influence of the male presence on the ovarian maturation of Bopyrina abbreviata. Females of B. abbreviata of different sizes were collected at Términos lagoon, Campeche, Mexico. The organisms were morphometrically classified as immature or mature, the male presence or absence at female's marsupium was recorded, and the degree of ovarian development was determined histologically. The internal organization of B. abbreviata agrees with that described for bopyrids and isopods in general. The ovarian cells originate from a dorsal lamina germinal layer that extends horizontally. The ovarian development of lone and paired immature females was classified as incipient and medium, respectively. In mature females it was classified as advanced, in the paired females and in the one lone mature female studied. The lone mature female differed from paired mature females only in the presence of reabsorption process in some oocytes located closer to the ventral wall of the ovary. Morphology variations between lone and paired females suggests that the presence of a cryptoniscus larva or a male between the female's pleopods stimulates the onset of reproduction and accelerates the ovarian development of B. abbreviata.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2016 

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References

REFERENCES

Álvarez, F., Bortolini, J.L. and Høeg, J.T. (2010) Anatomy of virgin and mature externae of Loxothylacus texanus, parasitic on the dark blue crab Callinectes rathbunae (Crustacea: Cirripedia: Rhizocephala: Sacculinidae). Journal of Morphology 271, 190199.Google Scholar
Barba, M.E., Raz-Guzmán, A. and Sánchez, J. (2005) Distribution patterns of estuarine caridean shrimps in the southwestern Gulf of Mexico. Crustaceana 78, 709726.Google Scholar
Barba, M.E., Sánchez, M.J., Raz-Guzmán, A. and Gallegos, E.M. (2000) Dieta natural y tasa de forrajeo del camarón carideo Hippolyte zostericola Smith sobre epífitas de Thalassia testudinum Banks et Solander ex König. Hidrobiológica 10, 139146.Google Scholar
Beck, J.T. (1980) Life history relationships between the bopyrid isopod Probopyrus pandalicola and one of its caridean shrimp hosts Palaemonetes paludosus . American Midland Naturalist 104, 135154.Google Scholar
Bell, T.A. and Lightner, D.V. (1988) A handbook of normal Penaeid shrimp histology. Lawrence, KS: World Aquaculture Society Press.Google Scholar
Bortolini, J.L. and Álvarez, F. (2008) Hepatopancreas alteration of the blue crab Callinectes sapidus by the rhizocephalan barnacle Loxothylacus texanus . Journal of Invertebrate Pathology 99, 354356.CrossRefGoogle ScholarPubMed
Cash, C.E. and Bauer, R.T. (1993) Adaptations of the branchial ectoparasite Probopyrus pandalicola (Isopoda: Bopyridae) for survival and reproduction related to ecdysis of the host, Palaemonetes pugio (Caridea: Palaemonidae). Journal of Crustacean Biology 13, 111124.CrossRefGoogle Scholar
Caubet, Y., Juchault, P. and Mocquard, J.P. (1998) Biotic triggers of female reproduction in the terrestrial isopod Armadillidium vulgare Latr. (Crustacea, Oniscidea). Ethology, Ecology and Evolution 10, 209226.CrossRefGoogle Scholar
Cornalia, E. and Panceri, P. (1858) Osservazioni zoologiche ed anatimiche sopra un nuovo genere di isopodo sedentari (Gyge branchialis). Memorie della Reale Accademia delle Scienze di Torino 19, 85118.Google Scholar
Hiraiwa, Y.K. (1933) Studies on a bopyrid, Epipenaeon japonica Thielemann. I. Morphological studies in both sexes. Journal of Science of the Hiroshima University series B div. 1 , 2, 4970.Google Scholar
Hiraiwa, Y.K. (1934) Studies on a bopyrid, Epipenaeon japonica Thielemann. II. Reproductive and excretory organs. Journal of Science of the Hiroshima University series B div. 1 , 3, 4563.Google Scholar
Jassem, W., Juchault, P. and Mocquard, J.P. (1982) Déterminisme de la reproduction saisonnière des femelles d’Armadillidium vulgare Latr. (Crustacé, Isopode, Oniscoïde). V. Rôle du mâle dans le cycle de reproduction des femelles (induction et durée de la période de reproduction). Annales de Sciences Naturelles (Zoologie) 4, 195201.Google Scholar
Jassem, W., Juchault, P., Souty-Grosset, C. and Mocquard, J.P. (1991) Male-induced stimulation of the initiation of female reproduction in the terrestrial isopod Armadillidium vulgare Latr. (Crustacea, Oniscidea). Acta Oecologica 12, 643653.Google Scholar
Kossmann, R. (1881) Studien über Bopyriden. II. Bopyrina virbii; beiträge zur kenntnis der anatomie und metamorphose der Bopyriden. Zeitschrift Wissensch (Zoologie) 35, 652680.Google Scholar
Lefebvre, F. and Caubet, Y. (1999) On the male-effect in the terrestrial crustacean Armadillidium vulgare (Latreille, 1804). Invertebrate Reproduction and Development 35, 5564.Google Scholar
Lemos de Castro, A. and Brasil-Lima, I.M. (1980) Crustáceos isópodes epicarídeos do Brasil. XII. Variaçoes intraespecíficas, hospedeiros e distribuiçao geográfica de Bopyrina abbreviata Richardson. Boletim do Museu Nacional Nova Série 9 Zoologia, 16.Google Scholar
Markham, J.C. (1985) A review of the bopyrid isopods infesting caridean shrimps in the northwestern Atlantic Ocean, with special reference to those collected during the Hourglass cruises in the Gulf of Mexico. Memoirs of the Hourglass Cruises 7, 1156.Google Scholar
Masunari, S.A., Da Silva, C. and Oliveira, E. (2000) The population structure of Probopyrus floridensis (Isopoda, Bopyridae) a parasite of Macrobrachium potiuna (Decapoda, Palaemonidae) from the Perenquê River, Paranaguá Basin, Southern Brazil. Crustaceana 73, 10951108.Google Scholar
McDermott, J.J. (1998) Prevalence of two epicaridean isopods (Bopyridae and Entoniscidae) associated with the hermit crab Pagurus longicarpus Say, 1817 (Anomura) from the New Jersey coast (U.S.A.). Journal of Parasitology 84, 10421045.Google Scholar
McLaughlin, P.A. (1983) Internal anatomy. In Bliss, D.L. and Mantel, L.H. (eds) The biology of crustaceans: internal anatomy and physiological regulation, Vol. 5. New York, NY: Academic Press, pp. 152.Google Scholar
Oliveira, E. and Masunari, S. (1998) Population relationships between the parasite Aporobopyrus curtatus (Richardson, 1904) (Isopoda: Bopyridae) and one of its porcelain crab host Petrolisthes armatus (Gibbes, 1850) (Decapoda: Porcellanidae) from Farol Island, southern Brazil. Journal of Natural History 32, 17071717.CrossRefGoogle Scholar
Picaud, J.L., Souty-Grosset, C. and Martin, G. (1989) Vitellogenesis in terrestrial isopods: female specific proteins and their control. Monitore Zoologico Italiano 4, 305332.Google Scholar
Rathke, H. (1837) De Bopyro et Nereide, commentationes anatómico-physiologicae duae. Rigae et Dorpati, apud Eduardum Frantzen.Google Scholar
Raz-Guzmán, A. and Sánchez, J.A. (1996) Trophic structure related to seagrass habitat complexity. In Kuo, J., Phillips, R.C., Walker, I.D. and Kirkman, H. (eds) Seagrass biology: Proceedings of an international workshop, Rottnest Island, Western Australia, 5–29 January, 1996. Perth: University of Western Australia Press, pp. 241248.Google Scholar
Román-Contreras, R. and Romero-Rodríguez, J. (2005) Incidence of infestation by Bopyrina abbreviata Richardson, 1904 (Isopoda: Bopyridae) on Hippolyte zostericola (Smith, 1873) (Decapoda: Hippolytidae) in Laguna de Términos, Gulf of Mexico. Nauplius 13, 8388.Google Scholar
Romero-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 Ascension, Mexican Caribbean. Crustaceana 81, 12011210.Google Scholar
Romero-Rodríguez, J. and Román-Contreras, R. (2013) Prevalence and reproduction of Bopyrina abbreviata (Isopoda, Bopyridae) in Laguna de Términos, SW Gulf of Mexico. Journal of Crustacean Biology 33, 641650.Google Scholar
Romero-Rodríguez, J. and Román-Contreras, R. (2014) Relationships of the branchial parasite Bopyrinella thorii (Isopoda, Bopyridae) and its host Thor floridanus (Decapoda, Hippolytidae). Crustaceana 87, 463475.Google Scholar
Sánchez, A.J., Raz-Guzmán, A. and Barba, E. (1996) Habitat value of seagrass for decapods in tropical coastal lagoons of the southwestern Gulf of Mexico: an overview. In Kuo, J., Phillips, R.C., Walker, I.D. and Kirkman, H. (eds) Seagrass biology: Proceedings of an international workshop, Rottnest Island, Western Australia, 5–29 January, 1996. Crawley: University of Western Australia Press, pp. 89104.Google Scholar
Schuldt, M. (1993) El ciclo ovárico de Probopyrus ringueleti Verdi y Schuldt, 1988 (Isopoda: Epicaridea: Bopyridae). Gayana Zoología 57, 89104.Google Scholar
Torres, G.M.P. and Bortolini, R.J.L. (2002) Histological alterations in Macrobrachium panamensis caused by Probopyrus sp. In Escobar-Briones, E. and Álvarez, F. (eds) Modern approaches to the study of Crustacea. New York, NY: Kluwer Academic/Plenum Publishers, pp. 6365.Google Scholar
Wägele, J.W. (1992) Isopoda. In Harrison, F.W. and Ruppert, E.E. (eds) Microscopic anatomy of invertebrates: Crustacea, Volume 9. New York, NY: Wiley-Liss Press, pp. 529617.Google Scholar
Warburg, M.R. (2011) The oniscid isopod female reproductive system and gestation, with a partial review. Invertebrate Reproduction and Development 56, 124.Google Scholar
Warburg, M.R. (2013) Post-parturial reproduction in terrestrial isopods: a partial review. Invertebrate Reproduction and Development 57, 1026.Google Scholar
Wilson, G.D.F. (1991) Functional morphology and evolution of isopod genitalia. In Bauer, R.T. and Martin, J.W. (eds) Crustacean sexual biology. New York, NY: Columbia University Press, pp. 228245.Google Scholar
Yáñez-Arancibia, A., Lara-Domínguez, A.L., Chavance, P. and Flores-Hernández, D. (1988) Comportamiento ambiental de la Laguna de Términos. In Yáñez-Arancibia, A. and Day, J.W. Jr (eds) Ecología de los Ecosistemas Costeros en el sur del Golfo de México: La Región de la Laguna de Términos. Distrito Federal, México: Instituto de Ciencias del Mar y Limnología, UNAM Press, pp. 2740.Google Scholar