Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter April 18, 2017

Redescription of Philometra margolisiMoravec, Vidal-Martínez et Aguirre-Macedo, 1995 (Nematoda: Philometridae), a gonad-infecting parasite of the red grouper Epinephelus morio (Serranidae) in the Gulf of Mexico

František Moravec, Micah D. Bakenhaster and Erin H. Leone
From the journal Acta Parasitologica


The insufficiently known nematode species Philometra margolisiMoravec, Vidal-Martínez et Aguirre-Macedo, 1995 (Philometridae) is redescribed based on light and scanning electron microscopical (SEM) examinations of specimens collected from the gonad of the type host, the red grouper Epinephelus morio (Valenciennes) (Serranidae, Perciformes), in the northern Gulf of Mexico off Florida, USA. Also, new prevalence data for females of P. margolisi were derived from 188 fish, and a subset of these (n = 38) were used to determine prevalence and intensity of male nematodes. The male of this species was studied with SEM for the first time, which revealed some new, taxonomically important morphological features. The male posterior end had a V-shaped caudal mound, four pairs of minute adanal papillae, a pair of large papillae located posterior to the cloacal aperture and a pair of very small phasmids. The distal end of the gubernaculum is unique among all gonad-infecting species of Philometra parasitizing serranids in that its ventral surface is flat, smooth, without the usual two longitudinal grooves; the dorsal lamellate structures on the gubernaculum are also different in this species. In contrast to data in the original species description, the body length of gravid females of P. margolisi was 132–280 mm. Overall prevalence for male nematodes (76.3%) was much higher than for females (15.4%), and female nematode prevalence was higher in samples collected during host spawing season than out of season (27.1% and 3.3%, respectively).


The authors owe thanks to many colleagues at the Fish and Wildlife Research Institute (FWRI). Loanna Torrance, Jason Rock, Susan Hilber, Theresa Cody, Lauren Partridge, Susan Fogelson, Maki Tabuchi, Malcolm S. Richardson, Clark Gray, Melissa Garnett, C. J. McGuigan, and Eli Bastian provided assistance with parasite sampling in the field and laboratory. Sean Keenan, Jenna Tortorelli, Chris Stafford, Julie Vecchio, and Theresa Warner were lead scientists on research cruises and supported our shipboard efforts along with too many other members of the FWRI Fisheries Independent Monitoring Program to name individually. Theresa Cody, Bob McMichael, Deb Leffler, and Ted Switzer allocated program resources to this project. Laura Crabtree helped to identify and locate references. Thanks are also due to the staff of the Laboratory of Electron Microscopy, Institute of Parasitology, Biology Centre of the CAS, České Budějovice for their technical assistance, and to Blanka Škoríková of the same Institute for help with illustrations. This study was partly supported by the Czech Science Foundation (grant No. P505/12/G112) and the Institute of Parasitology, BC AS CR (institutional support RVO:60077344). Funding for field and laboratory sampling was provided to FWRI by the US Department of the Interior US Fish and Wildlife Service (USFWS) Federal Sportfish Restoration Grants F-72-12, 13, 14, 15, and16, and F121AF00878, F13AF00529, F14AF00955, F15AF00893, F16AF00544, F-43-24, F-43-26, F12AF00222, F13AF00325, F14AF00328, and F16AF00413, and by National Oceanic and Atmospheric Administration (NOAA) grants NA06NMF4350009, NA08NMF4330403, and NA11NMF45 40116. The views and conclusions contained in this document are those of the authors and should not be interpreted as necessarily representing the opinions or policies of the U.S. government, the USFWS, or NOAA.


Bashirullah A. K. M., Adams J. R. 1983. Philonema oncorhynchi: effect of hormones on maturation in anadromous sockey, Oncorhynchus nerka. International Journal of Parasitology, 13, 261–26510.1016/0020-7519(83)90037-1Search in Google Scholar

Brulé T., Déniel C., Colás-Marrufo T., Sánchez-Crespo M. 1999. Red grouper reproduction in the southern Gulf of Mexico. Transactions of the American Fisheries Society, 128, 385–402. 10.1577/1548-8659(1999)128<0385:RGRITS>2.0CO;2Search in Google Scholar

Bullock L.H., Smith G.B. 1991. Seabasse (Pisces: Serranidae). Memoirs of the Hourglass Cruises, 8, 1–206Search in Google Scholar

Clarke L.M., Dove A.D.M., Conover D.O. 2006. Prevalence, intensity, and effect of a nematode (Philometra saltatrix) in the ovaries of bluefish (Pomatomus saltatrix). Fisheries Bulletin, 104, 118–124. DOI: in Google Scholar

Coleman F.C., Koenig C.C., Scanlon K.M., Heppell S., Heppell S., Miller M.W. 2010. Benthic habitat modification through excavation by red grouper, Epinephelus morio, in the northeastern Gulf of Mexico. The Open Fish Science Journal, 3, 1–15. DOI: in Google Scholar

Collins L.A., Fitzhugh G.R., Lombardi-Carlson L.A., Lyon H.M., Walling W.T., Oliver D.W. 2002. Characterization of red grouper (Serranidae: Epinephelus morio) reproduction from the eastern Gulf of Mexico. Contribution Series 2002-07 National Marine Fisheries Service, Panama City, Florida, pp. 21Search in Google Scholar

Froese R., Pauly D. (Eds) 2016. FishBase. World Wide Web electronic publication., version 10/2016Search in Google Scholar

Giménez-Hurtado E., Coyula-Pérez-Puelles R., Lluch-Cota S.E., Ganzález-Yañez A.A., Moreno-García V., Burgos-de-la-Rosa R. 2005. Historical biomass, fishing mortality, and recruitment trends of the Campeche Bank red grouper (Epinephelus morio). Fisheries Research, 71, 267–277. DOI: in Google Scholar

Heemstra P.C. 2002. Groupers (seabasses, creolefish, coney, hinds, hamlets, anthiines, and soapfishes). In: Camperter K.E. (Ed.), The living marine resources of the Western Central Atlantic. Volume 2: Bony fishes part 1 (Acipenseridae to Grammatidae). FAO Species Identification Guide for Fishery Purposes and American Society of Ichthyologists and Herpetologists Special Publication No. 5. Rome: FAO, 1308–1369Search in Google Scholar

Lowerre-Barbieri S., Crabtree L., Switzer T.S., McMichael R.H. Jr. 2014. Maturity, sexual transition, and spawning seasonality in the protogynous red grouper on the West Florida Shelf. SEDAR42-DW-7. SEDAR, North Charleston, South Carolina, pp. 21Search in Google Scholar

Moe M.A. 1969. Biology of the red grouper Epinephelus morio (Valenciennes) from the eastern Gulf of Mexico. Professional Papers Series, Florida Department of Natural Resources Marine Research Laboratory 10, St. Petersburg, Florida, USA, pp. 1–5Search in Google Scholar

Molnár K. 1966. Life-history of Philometra ovata (Zeder, 1803) and Ph. rischta Skrjabin, 1917. Acta Veterinaria Academiae Scientiarum Hungaricae, 16, 227–242Search in Google Scholar

Moravec F. 1977. The life history of the nematode Philometra abdominalis in the Rokytka Brook, Czechoslovakia. Acta Societatis Zoologicae Bohemoslovacae, 41, 114–120Search in Google Scholar

Moravec F. 2006. Dracunculoid and anguillicoloid nematodes parasitic in vertebrates. Prague: Academia, pp. 634Search in Google Scholar

Moravec F., Bakenhaster M.D. 2013. Two new gonad-infecting philometrids (Nematoda: Philometridae) from the yellowedge grouper Hyporthodus flavolimbatus (Serranidae) and the great northern tilefish Lopholatilus chamaeleonticeps (Malacanthidae) in the northern Gulf of Mexico. Systematic Parasitology, 86, 113–123. 10.1007/s11230-013-9438-3Search in Google Scholar

Moravec F., Bakenhaster M.D., Adams D.H. 2016b. Two new species of Philometra Costa, 1845 (Nematoda: Philometridae) from Mycteroperca spp. (Serranidae) in the western Atlantic and northern Gulf of Mexico, USA. Systematic Parasitology, 93, 479–491. 10.1007/s11230-016-9642-zSearch in Google Scholar

Moravec F., Chaabane A., Justine J.-L., Neifar L. 2016a. Two-gonad infecting species of Philometra (Nematoda: Philometridae) from groupers (Serranidae) off Tunisia, with a key to Philometra species infecting serranid gonads. Parasite, 23, 8. 10.1051/parasite/2016008Search in Google Scholar

Moravec F., Chaabane A., Neifar L., Gey D., Justine J.-L. 2016c. Descriptions of Philometra aenei n. sp. and P. tunisiensis n. sp. (Nematoda: Philometridae) from Epinephelus spp. off Tunisia confirm a high degree of host specificity of gonad-infecting species of Philometra Costa, 1845 in groupers (Serranidae). Systematic Parasitology, 93, 115–128. 10.1007/s11230-015-9610-zSearch in Google Scholar

Moravec F., de Buron I. 2013. A synthesis of our current knowledge of philometrid nematodes, a group of increasingly important fish parasites. Folia Parasitologica, 60, 81–101. 10.14411/fp.2013.010Search in Google Scholar

Moravec F., Justine J.-L. 2008. Some philometrid nematodes (Philometridae), including four new species of Philometra, from marine fishes off New Caledonia. Acta Parasitologica, 53, 369–381. 10.2478/s11686-008-0050-7Search in Google Scholar

Moravec F., Justine J.-L. 2014. Philometrids (Nematoda: Philometridae) in carangid and serranid fishes off New Caledonia, including three new species. Parasite, 21, 21. 10.1051/parasite/2014022Search in Google Scholar PubMed PubMed Central

Moravec F., Justine J.-L. 2015. New records of species of Philometra (Nematoda: Philometridae) from marine fishes off New Caledonia, including P. cephalopholidis sp. n. from Cephalopholis sonnerati (Serranidae). Parasitology Research, 114, 3223–3228. 10.1007/s00436-015-4538-4Search in Google Scholar PubMed

Moravec F., Manoharan J. 2014. Gonad-infecting species of Philometra (Nematoda: Philometridae) from groupers Epinephelus spp. (Osteichthyes: Serranidae) in the Bay of Bengal, India. Acta Parasitologica, 59, 596–605. 10.2478/s11686-014-0285-4Search in Google Scholar PubMed

Moravec F., Salgado-Maldonado G. 2007. A new species of Philometra (Nematoda, Philometridae) from the gonads of the rock hind Epinephelus adscensionis (Osteichthyes) from the southern Gulf of Mexico. Acta Parasitologica, 52, 376–381. 10.2478/s11686-007-0044-xSearch in Google Scholar

Moravec F., Vidal-Martínez V.M., Aguirre-Macedo L. 1995. Philometra margolisi n. sp. (Nematoda: Philometridae) from the gonads of the red grouper, Epinephelus morio (Pisces: Serranidae), in Mexico. Canadian Journal of Fisheries and Aquatic Sciences, 52 (Suppl. 1), 161–165. 10.1139/f95-522Search in Google Scholar

Moravec F., Vidal-Martínez V.M., Vargas-Vázquez J., Vivas-Rodríguez C., González-Solís D., Mendoza-Franco E., Simá-Alvárez R., Güemez-Ricalde J. 1997. Helminth parasites of Epinephelus morio (Pisces: Serranidae) of the Yucatan Peninsula, southeastern Mexico. Folia Parasitologica, 44, 255–266Search in Google Scholar

Paperna I., Zwerner D. E. 1976. Parasites and diseases of striped bass, Morone saxatilis (Walbaum), from the lower Chesapeake Bay. Journal of Fish Biology, 9, 267–287. 10.1111/j.1095-8649.1976.tb04678.xSearch in Google Scholar

Perez G.R., Roumillat W.A., Levesque E.M., Connors V.A., de Buron I. 2008. Synchronization of occurrence of the ovarian philometrid, Philometra carolinensis, with the spawning season of its fish host, the spotted seatrout, Cynoscion nebulosus. Parasitology Research, 104, 1079–1085. 10.1007/s00436-008-1291-ySearch in Google Scholar PubMed

Platzer E. G., Adams J. R. 1967. The life history of a dracunculoid, Philonema oncorhynchi, in Oncorhynchus nerka. Canadian Journal of Zoology, 45, 31–43. 10.1139/z67-004Search in Google Scholar

Quiazon K.M.A., Yoshinaga T., Ogawa K. 2008a. Taxonomic study into two new species of Philometra (Nematoda: Philometridae) previously identified as Philometra lateolabracis (Yamaguti, 1935). Folia Parasitologica, 55, 29–41. 10.14411/fp.2008.005Search in Google Scholar PubMed

Quiazon K.M.A., Yoshinaga T., Ogawa K. 2008b. Philometra sawara sp. n. and a redescription of Philometra sciaenae Yamaguti, 1941 and Philometra nemipteri Luo, 2001 (Nematoda: Philometridae): a morphological and molecular approach. Folia Parasitologica, 55, 277–290. 10.14411/fp.2008.036Search in Google Scholar PubMed

Schirripa M.J., Legault C.M., Ortiz M. 1999. The red grouper fishery of the Gulf of Mexico: Assessment 3.0. Sustainable Fisheries Division Contribution No. SFD-98/99-56Search in Google Scholar

Smith C.L. 1971. A revision of the American groupers: Epinephelus and allied genera. Bulletin of the American Museum of Natural History, 146, 67–242Search in Google Scholar

Uhazy L. S. 1977. Biology of Philometroides huronensis (Nematoda: Dracunculoidea) in the white sucker (Catostomus commersoni). Canadian Journal of Zoology, 55, 1430–1441. 10.1139/z77-186Search in Google Scholar

Vidal-Martínez V.M., Aguirre-Macedo M.L., Vivas-Rodríguez C.M., Moravec F. 1998. Las comunidades de macroparasitos del mero Epinephelus morio (Pisces: Serranidae) en la Peninsula de Yucatan, Mexico. Proceedings of the Gulf and Caribbean Fisheries Institute, 50, 764–779Search in Google Scholar

Wang S.-X., Li L., Zhang L.-P. 2015. Redescription and genetic characterization of Philometra lagocephali Moravec et Justine 2008 (Nematoda: Philometridae) from Lagocephalus lunaris (Bloch and Schneider) (Tetraodontiformes: Tetraodontidae) in the South China Sea. Acta Parasitologica, 60, 395–406. 10.1515/ap-2015-0055Search in Google Scholar PubMed

Williams C. F., Moravec F., Thurnbull J. F., Ferguson H. W. 2012.Seasonal development and pathological changes associated with the parasitic nematode Philometroides sanguineus in wild crucian carp Carassius carassius (L.) in England. Journal of Helminthology, 86, 329–338. in Google Scholar PubMed

Received: 2016-11-16
Revised: 2017-1-20
Accepted: 2017-1-26
Published Online: 2017-4-18
Published in Print: 2017-6-1

© 2017 W. Stefański Institute of Parasitology, PAS