Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-17T10:14:51.122Z Has data issue: false hasContentIssue false

Hexabothriidae and Monocotylidae (Monogenoidea) from the gills of neonate hammerhead sharks (Sphyrnidae) Sphyrna gilberti, Sphyrna lewini and their hybrids from the western North Atlantic Ocean

Published online by Cambridge University Press:  09 August 2022

Kaitlyn M. Dalrymple*
Affiliation:
Laboratory of Biological Interactions, Universidade Federal do Paraná, Curitiba, PR 81531-980, Brazil Department of Biology, College of Charleston, Charleston, SC 29424, USA
Isaure de Buron
Affiliation:
Department of Biology, College of Charleston, Charleston, SC 29424, USA
Kristina M. Hill-Spanik
Affiliation:
Department of Biology, College of Charleston, Charleston, SC 29424, USA
Ashley S. Galloway
Affiliation:
South Carolina Department of Natural Resources, Marine Resources Research Institute, 217 Fort Johnson Drive, Charleston, SC 29412, USA
Amanda Barker
Affiliation:
Marine Genomics Laboratory, Department of Life Sciences, Texas A&M University-Corpus Christi, 6300 Ocean Drive, Corpus Christi, TX 78412, USA
David S. Portnoy
Affiliation:
Marine Genomics Laboratory, Department of Life Sciences, Texas A&M University-Corpus Christi, 6300 Ocean Drive, Corpus Christi, TX 78412, USA
Bryan S. Frazier
Affiliation:
South Carolina Department of Natural Resources, Marine Resources Research Institute, 217 Fort Johnson Drive, Charleston, SC 29412, USA
Walter A. Boeger
Affiliation:
Laboratory of Biological Interactions, Universidade Federal do Paraná, Curitiba, PR 81531-980, Brazil
*
Author for correspondence: Kaitlyn M. Dalrymple, E-mail: [email protected]

Abstract

Neonates of hammerhead sharks (Sphyrnidae), Sphyrna lewini (Griffith and Smith, 1834), the sympatric cryptic species, Sphyrna gilberti Quattro et al., 2013, and their hybrids were captured in the western North Atlantic, along the coast of South Carolina, USA, between 2018 and 2019 and examined for gill monogenoids. Parasites were identified and redescribed from the gills of 79 neonates, and DNA sequences from partial fragments of the nuclear 28S ribosomal RNA (rDNA) and cytochrome c oxidase I mitochondrial DNA (COI) genes were generated to confirm species identifications. Three species of monogenoids from Hexabothriidae Price, 1942 and Monocotylidae Taschenberg, 1879 were determined and redescribed. Two species of Hexabothriidae, Erpocotyle microstoma (Brooks, 1934) and Erpocotyle sphyrnae (MacCallum, 1931), infecting both species of Sphyrna and hybrids; and 1 species of Monocotylidae, Loimosina wilsoni Manter, 1944, infecting only S. lewini and hybrids. Loimosina wilsoni 28S rDNA sequences matched those of Loimosina sp. from the southern coast of Brazil. Based on limited morphological analysis, Loimosina parawilsoni is likely a junior synonym of L. wilsoni. This is the first taxonomic study of monogenoids infecting S. gilberti and hybrids of S. gilberti and S. lewini.

Type
Research Article
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abercrombie, DL, Clarke, SC and Shivji, MS (2005) Global-scale genetic identification of hammerhead sharks: application to assessment of the international fin trade and law enforcement. Conservation Genetics 6, 775788.CrossRefGoogle Scholar
Altschul, SF, Gish, W, Miller, W, Myers, EW and Lipman, DJ (1990) Basic local alignment search tool. Journal of Molecular Biology 215, 403410.CrossRefGoogle ScholarPubMed
Anderson, EC and Thompson, EA (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160, 12171229.CrossRefGoogle ScholarPubMed
Araujo, SBL, Braga, MP, Brooks, DR, Agosta, SJ, Hoberg, EP, von Hartenthal, FW and Boeger, WA (2015) Understanding host-switching by ecological fitting. PLoS ONE 10, e0139225.CrossRefGoogle ScholarPubMed
Barker, AM, Adams, DH, Driggers, WB, Frazier, BS and Portnoy, DS (2019) Hybridization between sympatric hammerhead sharks in the western North Atlantic Ocean. Biology Letters 15, 20190004.CrossRefGoogle ScholarPubMed
Barker, AM, Frazier, BS, Adams, DH, Bedore, CN, Belcher, CN, Driggers, WB, Galloway, AS, Gelsleichter, J, Grubbs, RD, Reyier, EA and Portnoy, DS (2021) Distribution and relative abundance of scalloped (Sphyrna lewini) and Carolina (S. gilberti) hammerheads in the western North Atlantic Ocean. Fisheries Research 242, 106039.CrossRefGoogle Scholar
Boeger, WA and Kritksy, DC (2001) Phylogenetic relationships of the Monogenoidea. Interrelationships of the Platyhelminthes. London: Taylor & Francis, pp. 92102.Google Scholar
Boeger, W and Kritsky, D (1989) Phylogeny, coevolution, and revision of the Hexabothriidae Price, 1942 (Monogenea). International Journal for Parasitology 19, 425440.CrossRefGoogle Scholar
Boeger, WA, Kritsky, DC, Domingues, MV and Bueno-Silva, M (2014) The phylogenetic position of the Loimoidae Price, 1936 (Monogenoidea: Monocotylidea) based on analyses of partial rDNA sequences and morphological data. Parasitology International 63, 492499.CrossRefGoogle ScholarPubMed
Boudaya, L and Neifar, L (2016) Triloculotrema euzeti n. sp. (Monogenea, Monocotylidae) from the nasal tissues of the blackspotted smooth-hound Mustelus punctulatus (Carcharhiniformes, Triakidae) from off Tunisia. Parasite 23, 62.CrossRefGoogle Scholar
Bowles, J, Blair, D and Mcmanus, DP (1995) A molecular phylogeny of the human schistosomes. Molecular Phylogenetics and Evolution 4, 103109.CrossRefGoogle ScholarPubMed
Bravo-Hollis, M (1970) Helmintos de peces del Pacífico mexicano XXXI. Descripción de Loimosina parawilsoni sp. nov. (Fam. Loimoidae Bychowsky, 1957) de Sphyrna lewini (Griffith) de Mazatlán, Sinaloa. Anales del Instituto de Biología, Universidad Nacional Autónoma de México 41, 147152.Google Scholar
Brooks, GL (1934) Some new ectoparasitic trematodes (Onchocotylinae) from the gills of American sharks. Parasitology 26, 259267.CrossRefGoogle Scholar
Brooks, DR, Hoberg, EP and Boeger, WA (2019) The Stockholm Paradigm: Climate Change and Emerging Disease. Chicago, IL: The University of Chicago Press.Google Scholar
Bullard, SA and Dippenaar, SM (2003) Branchotenthes robinoverstreeti n. gen. and n. sp. (Monogenea: Hexabothriidae) from gill filaments of the bowmouth guitarfish, Rhina ancylostoma (Rhynchobatidae), in the Indian Ocean. Journal of Parasitology 89, 595601.CrossRefGoogle Scholar
Bullard, SA, Warren, MB and Dutton, HR (2021) Redescription of Cathariotrema selachii (MacCallum, 1916) Johnston and Tiegs, 1922 (Monogenoidea: Monocotylidae), emendation of monotypic Cathariotrema Johnston and Tiegs, 1922, and proposal of Cathariotrematinae n. subfam. Based on morphological and nucleotide evidence. Journal of Parasitology 107, 481513.CrossRefGoogle ScholarPubMed
Caballero, YCE, Hidalgo, EE and Grocott, RG (1956) Helmintos de la Republica de Panama, XVII: Cuatro especies de trematodos de peces marinos con descriptión de una nueva forma. Revista Brasileira de Biologia 16, 181194.Google Scholar
Cerfontaine, P (1899) Contribution à l’étude des octocotylidés: V-Les Onchocotylinae. Archives de Biologie 16, 345478.Google Scholar
Chero, JD, Cruces, CL, Sáez, G, Oliveira, AGL, Santos, CP and Luque, JL (2021) A new species of Loimopapillosum Hargis, 1955 (Monogenea: Monocotylidae) parasitizing Hypanus dipterurus (Myliobatiformes: Dasyatidae) off the Pacific coast of South America, and its phylogenetic relationships. Journal of Helminthology 95, 19, doi: 10.1017/S0022149X21000262CrossRefGoogle Scholar
Chisholm, LA, Whittington, ID, Morgan, JA and Adlard, RD (2001a) The Calicotyle conundrum: do molecules reveal more than morphology? Systematic Parasitology 49, 8187.CrossRefGoogle ScholarPubMed
Chisholm, LA, Morgan, JA, Adlard, RD and Whittington, ID (2001b) Phylogenetic analysis of the Monocotylidae (Monogenea) inferred from 28S rDNA sequences. International Journal for Parasitology 31, 15371547.CrossRefGoogle ScholarPubMed
Combes, C (2001) Parasitism: The Ecology and Evolution of Intimate Interactions. Chicago, IL: University of Chicago Press.Google Scholar
Compagno, LJV (1984) Vol 4. Sharks of the world – an annotated and illustrated catalogue of shark species known to date. Part 2. Carcharhiniformes. In FAO Species Catalogue No. 125, pp. 251–655. Rome.Google Scholar
Duncan, KM, Martin, AP, Bowen, BW and De Couet, HG (2006) Global phylogeography of the scalloped hammerhead shark (Sphyrna lewini). Molecular Ecology 15, 22392251.CrossRefGoogle ScholarPubMed
Euzet, L and Combes, C (1980) Les problèmes de l'espèce chez les animaux parasites. Bulletin de la Société Zoologique de France 40, 239285.Google Scholar
Euzet, L and Maillard, C (1967) Parasites de poissons de mer ouest-africaines, récoltés par J. Cadenat. Bulletin de l'Institut français d'Afrique noire 29, 14351493.Google Scholar
Fehlauer-Ale, KH and Littlewood, DTJ (2011) Molecular phylogeny of Potamotrygonocotyle (Monogenea, Monocotylidae) challenges the validity of some of its species. Zoologica Scripta 40, 638658.CrossRefGoogle Scholar
Felsenstein, J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783791.Google ScholarPubMed
Glennon, V, Chisholm, LA and Whittington, ID (2006) Three unrelated species, 3 sites, same host – monogenean parasites of the southern fiddler ray, Trygonorrhina fasciata, in South Australia: egg hatching strategies and larval behaviour. Parasitology 133, 5566.CrossRefGoogle ScholarPubMed
Griffith, E and Lieut-Col. Smith, CH (1834) The Class Pisces Arranged by the Baron Cuvier with Supplementary Additions. Whittaker and Co., London.Google Scholar
Hajibabaei, M, Smith, MA, Janzen, DH, Rodriguez, JJ, Whitfield, JB and Hebert, PDN (2006) A minimalist barcode can identify a specimen whose DNA is degraded. Molecular Ecology Notes 6, 959964.CrossRefGoogle Scholar
Hargis, WJ (1955) Monogenetic trematodes of Gulf of Mexico fishes. Part V. The superfamily Capsaloidea. Transactions of the American Microscopical Society 74, 203225.CrossRefGoogle Scholar
Humason, GL (1979) Animal Tissue Techniques, 4th Edn. San Francisco: W.H. Freeman.Google Scholar
Irigoitia, MM, Braicovich, PE, Rossin, MA, Canel, D, Levy, E, Farber, MD and Timi, JT (2019) Diversity of Empruthotrema Johnston and Tiegs, 1992 parasitizing batoids (Chondrichthyes: Rajiformes and Myliobatiformes) from the Southwest Atlantic Ocean, with description of three new species. Parasitology Research 118, 31133127.CrossRefGoogle ScholarPubMed
Jensen, K and Bullard, SA (2010) Characterization of a diversity of tetraphyllidean and rhinebothriidean cestode larval types, with comments on host associations and life-cycles. International Journal for Parasitology 40, 889910.CrossRefGoogle ScholarPubMed
Justine, J-L, Jovelin, R, Neifar, L, Mollaret, I, Lim, LHS, Hendrix, SS and Euzet, L (2002) Phylogenetic positions of the Bothitrematidae and Neocalceostomatidae (Monopisthocotylean Monogeneans) inferred from 28S rDNA sequences. Comparative Parasitology 69, 2025.CrossRefGoogle Scholar
Katoh, K, Misawa, K, Kuma, K and Miyata, T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30, 3059.CrossRefGoogle ScholarPubMed
Kearse, M, Moir, R, Wilson, A, Stones-Havas, S, Cheung, M, Sturrock, S, Buxton, S, Cooper, A, Markowitz, S, Duran, C, Thierer, T, Ashton, B, Meintjes, P and Drummond, A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 16471649.CrossRefGoogle ScholarPubMed
Khang, TF, Soo, OYM, Tan, WB and Lim, LHS (2016) Monogenean anchor morphometry: systematic value, phylogenetic signal, and evolution. PeerJ 4, e1668.CrossRefGoogle ScholarPubMed
Kheddam, H, Justine, J-L and Tazerouti, F (2016) Hexabothriid monogeneans from the gills of deep-sea sharks off Algeria, with the description of Squalonchocotyle euzeti n. sp. (Hexabothriidae) from the kitefin shark Dalatias licha (Euselachii, Dalatiidae). Helminthologia 53, 354362.CrossRefGoogle Scholar
Kitamura, A, Ogawa, K, Shimizu, T, Kurashima, A, Mano, N, Taniuchi, T and Hirose, H (2010) A new species of Calicotyle Diesing, 1850 (Monogenea: Monocotylidae) from the shortspine spurdog Squalus mitsukurii Jordan & Snyder and the synonymy of Gymnocalicotyle Nybelin, 1941 with this genus. Systematic Parasitology 75, 117124.CrossRefGoogle ScholarPubMed
Kumar, S, Stecher, G, Li, M, Knyaz, C and Tamura, K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 15471549.CrossRefGoogle ScholarPubMed
Lim, DD, Motta, P, Mara, K and Martin, AP (2010) Phylogeny of hammerhead sharks (Family Sphyrnidae) inferred from mitochondrial and nuclear genes. Molecular Phylogenetics and Evolution 55, 572579.CrossRefGoogle ScholarPubMed
Lockyer, AE, Olson, PD and Littlewood, DTJ (2003) Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): implications and a review of the cercomer theory. Biological Journal of the Linnean Society 78, 155171.CrossRefGoogle Scholar
MacCallum, GA (1931) Four new species of trematode worms of the subfamily Onchocotylinae. Proceedings of the United States National Museum 79, 18.CrossRefGoogle Scholar
Macdonald, S (1975) Hatching rhythms in three species of Diclidophora (Monogenea) with observations on host behaviour. Parasitology 71, 211228.CrossRefGoogle ScholarPubMed
Maillard, C and Paperna, I (1978) Hexabothriidae (Monogenea) du Requin Marteau (Sphyrna mokarran) de la Mer Rouge: Description d’une nouvelle espèce, Erpocotyle septistoma. Annales de Parasitologie (Paris) 53, 487494.Google Scholar
Manter, HW (1944) Notes on the trematode subfamily Loimoinae (Monogenea), with a description of a new genus. Journal of the Washington Academy of Sciences 34, 8689.Google Scholar
McEachran, JD and Séret, B (1987) Allocation of the name Sphyrna tudes (Valenciennes, 1822) and status of the nominal species Sphyrna couardi Cadenat, 1951 (Chondrichthyes, Sphyrnidae). French Ichthyological Society – Cybium 11, 3946.Google Scholar
Mollaret, I, Jamieson, BG, Adlard, RD, Hugall, A, Lecointre, G, Chombard, C and Justine, JL (1997) Phylogenetic analysis of the Monogenea and their relationships with Digenea and Eucestoda inferred from 28S rDNA sequences. Molecular and Biochemical Parasitology 90, 433438.CrossRefGoogle ScholarPubMed
Mollaret, I, Jamieson, BG and Justine, JL (2000) Phylogeny of the monopisthocotylea and Polyopisthocotylea (Platyhelminthes) inferred from 28S rDNA sequences. International Journal for Parasitology 30, 171185.CrossRefGoogle ScholarPubMed
Moravec, F, Dalrymple, KM, Galloway, AS, Barker, AM and de Buron, I (2020) First record of Piscicapillaria bursata (Nematoda: Capillariidae), a parasite of hammerhead sharks Sphyrna spp., in the western Atlantic Ocean. Diseases of Aquatic Organisms 138, 133136.CrossRefGoogle ScholarPubMed
Ñacari, LA, Sepulveda, FA, Droguet, F, Escribano, R and Oliva, ME (2020) Calicotyle hydrolagi n. sp. (Monogenea: Monocotylidae) infecting the deep-sea Eastern Pacific black ghost shark Hydrolagus melanophasma from the Atacama Trench, with comments on host specificity of Calicotyle spp. Parasitology International 75, 102025.CrossRefGoogle Scholar
Nitta, M (2019) A new Monocotylid species, Neoheterocotyle quadrispinata n. sp. (Monogenea), infecting gills of Rhinobatos hynnicephalus in Japan. Species Diversity 24, 145150.CrossRefGoogle Scholar
Ohashi, H, Umeda, N, Hirazawa, N, Ozaki, Y, Miura, C and Miura, T (2007) Purification and identification of a glycoprotein that induces the attachment of oncomiracidia of Neobenedenia girellae (Monogenea, Capsalidae). International Journal for Parasitology 37, 14831490.CrossRefGoogle ScholarPubMed
Penn, O, Privman, E, Ashkenazy, H, Landan, G, Graur, D and Pupko, T (2010 a) GUIDANCE: a web server for assessing alignment confidence scores. Nucleic Acids Research 38, W23W28.CrossRefGoogle ScholarPubMed
Penn, O, Privman, E, Landan, G, Graur, D and Pupko, T (2010 b) An alignment confidence score capturing robustness to guide tree uncertainty. Molecular Biology and Evolution 27, 17591767.CrossRefGoogle ScholarPubMed
Perkins, EM, Donnellan, SC, Bertozzi, T, Chisholm, LA and Whittington, ID (2009) Looks can deceive: molecular phylogeny of a family of flatworm ectoparasites (Monogenea: Capsalidae) does not reflect current morphological classification. Molecular Phylogenetics and Evolution 52, 705714.CrossRefGoogle Scholar
Pinacho-Pinacho, CD, Calixto-Rojas, M, García-Vásquez, A, Guzmán-Valdivieso, I, Barrios-Gutiérrez, JJ and Rubio-Godoy, M (2021) Species delimitation of Gyrodactylus (Monogenea: Gyrodactylidae) infecting the southernmost cyprinids (Actinopterygii: Cyprinidae) in the New World. Parasitology Research 120, 831848.CrossRefGoogle Scholar
Pinhal, D, Shivji, MS, Vallinoto, M, Chapman, DD, Gadig, OBF and Martins, C (2012) Cryptic hammerhead shark lineage occurrence in the western South Atlantic revealed by DNA analysis. Marine Biology 159, 829836.CrossRefGoogle Scholar
Pleijel, F, Jondelius, U, Norlinder, E, Nygren, A, Oxelman, B, Schander, C, Sundberg, P and Thollesson, M (2008) Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Molecular Phylogenetics and Evolution 48, 369371.CrossRefGoogle Scholar
Price, EW (1936) North American monogenetic trematodes. George Washington University Bulletin (Summaries of Doctoral Theses 1934–1936) 10–13.Google Scholar
Price, EW (1942) North American monogenetic trematodes. V. The family Hexabothriidae, n. n. (Polystomatoidea). Proceedings of the Helminthological Society of Washington 9, 3956.Google Scholar
Puritz, JB, Hollenbeck, CM and Gold, JR (2014) dDocent: a RADseq, variant-calling pipeline designed for population genomics of non-model organisms. PeerJ 2, e431.CrossRefGoogle ScholarPubMed
Quattro, JM, Stoner, DS, Driggers, WB, Anderson, CA, Priede, KA, Hoppmann, EC, Campbell, NH, Duncan, KM and Grady, JM (2006) Genetic evidence of cryptic speciation within hammerhead sharks (genus Sphyrna). Marine Biology 148, 11431155.CrossRefGoogle Scholar
Quattro, JM, Driggers, WB, Grady, JM, Ulrich, GF and Roberts, MA (2013) Sphyrna gilberti sp nov., a new hammerhead shark (Carcharhiniformes, Sphyrnidae) from the western Atlantic Ocean. Zootaxa 3702, 159178.CrossRefGoogle Scholar
Rohde, K (1994) Niche restriction in parasites: proximate and ultimate causes. Parasitology 109, S69S84.CrossRefGoogle ScholarPubMed
Saitou, N and Nei, M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406425.Google Scholar
Silvestro, D and Michalak, I (2012) raxmlGUI: a graphical front-end for RAxML. Organisms Diversity & Evolution 12, 335337.CrossRefGoogle Scholar
Springer, S (1941) A new species of hammerhead shark of the genus Sphyrna. Proceedings of the Florida Academy of Sciences 5, 4653.Google Scholar
Sproston, NG (1946) A synopsis of the monogenetic trematodes. Transactions of the Zoological Society of London 25, 185600.CrossRefGoogle Scholar
Stamatakis, A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 13121313.CrossRefGoogle ScholarPubMed
Suriano, DM and Labriola, JB (1998) Erpocotyle Van Beneden et Hesse, 1863 (Monogenea, Hexabothriidae), parasite of carcharhiniform fishes from the Southwestern Atlantic Ocean, with the description of E. schmitti sp. n. Acta Parasitologica 43, 410.Google Scholar
Tamura, K and Nei, M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10, 512526.Google ScholarPubMed
Tamura, K, Nei, M and Kumar, S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proceedings of the National Academy of Sciences 101, 1103011035.CrossRefGoogle ScholarPubMed
Teo, BG, Dhillon, SK and Lim, LHS (2013) A deformable generic 3D model of haptoral anchor of monogenean. PLoS ONE 8, e77650.CrossRefGoogle ScholarPubMed
Tinsley, RC and Jackson, JA (2002) Host factors limiting monogenean infections: a case study. International Journal for Parasitology 32, 353365.CrossRefGoogle ScholarPubMed
Tkach, VV, Littlewood, DTJ, Olson, PD, Kinsella, JM and Swiderski, Z (2003) Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea). Systematic Parasitology 56, 115.CrossRefGoogle ScholarPubMed
Torres-Carrera, G, Ruiz-Escobar, F, García-Prieto, L and Oceguera-Figueroa, A (2020) Narcinecotyle longifilamentus n. gen., n. sp. (Monogenea: Hexabothriidae), gill parasite of the numbfish Narcine entemedor (Torpediniformes: Narcinidae) from the Mexican Pacific coast. Parasitology International 76, 102095.CrossRefGoogle Scholar
Vaughan, D and Christison, K (2012) Towards addressing the current state of confusion within the Hexabothriidae Price, 1942 (1908): Callorhynchocotyle Suriano & Incorvaia, 1982 (Monogenea: Hexabothriidae) re-visited, with the preliminary evaluation of novel parameters for measuring haptoral armature of hexabothriids. Zootaxa 3229, 134.CrossRefGoogle Scholar
Vaughan, DB, Chisholm, LA and Hansen, H (2016) Electrocotyle whittingtoni n. gen., n. sp. (Monogenea: Monocotylidae: Heterocotylinae) from the gills of a captive onefin electric ray, Narke capensis (Narkidae) at Two Oceans Aquarium, Cape Town, South Africa. Parasitology Research 115, 35753584.CrossRefGoogle Scholar
Whittington, ID and Kearn, GC (2011) Hatching strategies in monogenean (Platyhelminth) parasites that facilitate host infection. Integrative and Comparative Biology 51, 9199.CrossRefGoogle ScholarPubMed
Whittington, ID, Cribb, BW, Hamwood, TE and Halliday, JA (2000) Host-specificity of monogenean (platyhelminth) parasites: a role for anterior adhesive areas? International Journal for Parasitology 30, 305320.CrossRefGoogle ScholarPubMed
Yamaguti, S (1968) Monogenetic trematodes of Hawaiian Fishes. Honolulu: University of Hawaii Press.CrossRefGoogle Scholar