Skip to main content Accessibility help
Hostname: page-component-59b7f5684b-frvt8 Total loading time: 0.465 Render date: 2022-09-25T03:37:01.343Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "useRatesEcommerce": false, "displayNetworkTab": true, "displayNetworkMapGraph": false, "useSa": true } hasContentIssue true

Article contents

Gill monogenean communities (Platyhelminthes, Monogenea, Dactylogyridae) of butterflyfishes from tropical Indo-West Pacific Islands

Published online by Cambridge University Press:  24 August 2016

CRIOBE, USR3278-EPHE/CNRS/UPVD, Paris Sciences et Lettres (PSL), University of Perpignan Via Domitia, 52 Avenue Paul Alduy, 66860 Perpignan, France Laboratoire d'Excellence ‘CORAIL’, 98729 Moorea, French Polynesia
School of Biological Sciences, The University of Queensland, Brisbane, Queensland 4072, Australia
Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK
School of Biological Sciences, The University of Queensland, Brisbane, Queensland 4072, Australia
CRIOBE, USR3278-EPHE/CNRS/UPVD, Paris Sciences et Lettres (PSL), University of Perpignan Via Domitia, 52 Avenue Paul Alduy, 66860 Perpignan, France Laboratoire d'Excellence ‘CORAIL’, 98729 Moorea, French Polynesia
*Corresponding author: CRIOBE, USR3278-EPHE/CNRS/UPVD, Paris Sciences et Lettres (PSL), University of Perpignan Via Domitia, 52 Avenue Paul Alduy, 66860 Perpignan, France. E-mail:


We studied the monogenean communities of 34 species of butterflyfish from the tropical Indo-West Pacific, identifying 13 dactylogyrid species (including two species that are presently undescribed). Monogenean assemblages differed significantly between host species in terms of taxonomic structure, intensity and prevalence. Parasite richness ranged from 0 (Chaetodon lunulatus) to 11 (C. auriga, C. citrinellus and C. lunula). Host specificity varied between the dactylogyrids species, being found on 2–29 of the 34 chaetodontid species examined. Sympatric butterflyfish species were typically parasitized by different combinations of dactylogyrid species, suggesting the existence of complex host–parasite interactions. We identified six clusters of butterflyfish species based on the similarities of their dactylogyrid communities. Dactylogyrid richness and diversity were not related to host size, diet specialization, depth range or phylogeny of butterflyfish species. However, there was a weak positive correlation between monogenean richness and diversity and host geographical range. Most communities of dactylogyrids were dominated by Haliotrema aurigae and H. angelopterum, indicating the importance of the genus Haliotrema in shaping monogenean communities of butterflyfishes. This study casts light on the structure of the monogenean communities of butterflyfishes, suggesting that the diversity and complexity of community structures arises from a combination of host species-specific parameters.

Research Article
Copyright © Cambridge University Press 2016 

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.)



Abouheif, E. (1999). A method for testing the assumption of phylogenetic independence in comparative data. Evolutionary Ecology Research 1, 895909.Google Scholar
Alarcos, A. J. and Timi, J. T. (2012). Parasite communities in three sympatric flounder species (Pleuronectiformes: Paralichthyidae): similar ecological filters driving toward repeatable assemblages. Parasitology Research 110, 21552166.CrossRefGoogle ScholarPubMed
Berumen, M. L., Pratchett, M. S. and Goodman, B. A. (2011). Relative gut lengths of coral reef butterflyfishes (Pisces: Chaetodontidae). Coral Reefs 30, 10051010.CrossRefGoogle Scholar
Bottegoni, G., Rocchia, W., Recanatini, M. and Cavalli, A. (2006). AClAP, Autonomous hierarchical agglomerative Cluster Analysis based protocol to partition conformational datasets. Bioinformatics 22, e58e65.CrossRefGoogle ScholarPubMed
Boutin, S., Sauvage, C., Bernatchez, L., Audet, C. and Derome, N. (2014). Inter individual variations of the fish skin microbiota: host genetics basis of mutualism? PLoS ONE 9, e102649.CrossRefGoogle ScholarPubMed
Bray, R. A. and Cribb, T. H. (2000). A new species of Aponurus Looss, 1907 (Digenea: Lecithasteridae) in butterflyfishes (Perciformes: Chaetodontidae) from New Caledonia. Systematics Parasitology 46, 181189.CrossRefGoogle ScholarPubMed
Buchmann, K. (1999). Immune mechanisms in fish skin against monogeneans – a model. Folia Parasitologica 46, 19.Google ScholarPubMed
Buchmann, K. and Lindenstrøm, T. (2002). Interactions between monogenean parasites and their fish hosts. International Journal for Parasitology 32, 309319.CrossRefGoogle ScholarPubMed
Bullard, S. A., Benz, G. W., Overstreet, R. M., Williams, E. H. and Hemdal, J. (2000). Six new host records and an updated list of wild hosts for Neobenedenia melleni (MacCallum) (Monogenea: Capsalidae). Comparative Parasitology 67, 190196.Google Scholar
Cirtwill, A. R., Stouffer, D. B., Poulin, R. and Lagrue, C. (2016). Are parasite richness and abundance linked to prey species richness and individual feeding preferences in fish hosts? Parasitology 143, 7586.CrossRefGoogle ScholarPubMed
Cribb, T. H., Adlard, R. D., Bray, R. A., Sasal, P. and Cutmore, S. C. (2014). Biogeography of tropical Indo-West Pacific parasites: a cryptic species of Transversotrema and evidence for rarity of Transversotrematidae (Trematoda) in French Polynesia. Parasitology International 63, 285294.CrossRefGoogle Scholar
Diaz, P. E., Bray, R. A. and Cribb, T. H. (2013). Paradiscogaster flindersi and P. oxleyi n. sp. (Digenea: Faustulidae): overlapping host and geographical distributions in corallivore chaetodontid fishes in the tropical Indo-west Pacific. Systematic Parasitology 86, 8799.CrossRefGoogle ScholarPubMed
Emslie, M. J., Pratchett, M. S., Cheal, A. J. and Osborne, K. (2010). Great Barrier Reef butterflyfish community structure: the role of shelf position and benthic community type. Coral Reefs 29, 705715.CrossRefGoogle Scholar
Fessler, J. L. and Westneat, M. W. (2007). Molecular phylogenetics of the butterflyfishes (Chaetodontidae): taxonomy and biogeography of a global coral reef fish family. Molecular Phylogenetics and Evolution 45, 5068.CrossRefGoogle ScholarPubMed
Findley, J. S. and Findley, M. T. (2001). Global, regional and local patterns in species richness and abundance of butterflyfishes. Ecological Monographs 71, 6991.CrossRefGoogle Scholar
Froese, R. and Pauly, D. (eds) (2016). FishBase. Worldwide web electronic publication. Retrieved March, 2016. Scholar
Gómez, A. and Nichols, E. (2013). Neglected wild life: parasitic biodiversity as a conservation target. International Journal for Parasitology: Parasites and Wildlife 2, 222227.Google ScholarPubMed
Gomez, D., Sunyer, J. O. and Salinas, I. (2013). The mucosal immune system of fish: the evolution of tolerating commensals while fighting pathogens. Fish and Shellfish Immunology 35, 17291739.CrossRefGoogle ScholarPubMed
Hatcher, M. J., Dick, J. T. and Dunn, A. M. (2012). Diverse effects of parasites in ecosystems: linking interdependent processes. Frontiers in Ecology and the Environment 10, 186194.CrossRefGoogle Scholar
Hsu, K., Chen, J. and Shao, K. (2007). Molecular phylogeny of Chaetodon (Teleostei: Chaetodontidae) in the Indo-west Pacific: evolution in geminate species pairs and groups. Raffles Bulletin of Zoology 14, 7786.Google Scholar
Hughes, W. O. H. and Boomsma, J. J. (2004). Let your enemy do the work: within-host interactions between two fungal parasites of leaf-cutting ants. Proceedings of the Royal Society B: Biological Sciences 271, S104S106.CrossRefGoogle ScholarPubMed
IUCN (2016). IUCN Red List of Threatened Species. Version 2016. Retrieved 10 February 2016.Google Scholar
Kearn, G. C. (1994). Evolutionary expansion of the Monogenea. International Journal for Parasitology 24, 12271271.CrossRefGoogle ScholarPubMed
Kritsky, D. C. (2012). Dactylogyrids (Monogenoidea: Polyonchoinea) parasitizing the gills of snappers (Perciformes: Lutjanidae): revision of Euryhaliotrema with new and previously described species from the Red Sea, Persian Gulf, the eastern and Indo-west Pacific Ocean, and the Gulf of Mexico. Zoologia 29, 227276.CrossRefGoogle Scholar
Kulbicki, M. and Bozec, Y. M. (2005). The use of butterflyfish (Chaetodontidae) species richness as a proxy of total species richness of reef fish assemblages in the Western and Central Pacific. Aquatic Conservation of Marine and Freshwater Ecosystems 15, S127S141.CrossRefGoogle Scholar
Kulbicki, M., Parravicini, V., Bellwood, D. R., Arias-Gonzàlez, E., Chabanet, P., Floeter, S. R., Friedlander, A., McPherson, J., Myers, R. E., Vigliola, L. and Mouillot, D. (2013). Global biogeography of reef fishes: a hierarchical quantitative delineation of regions. PLoS ONE 8, e81847.CrossRefGoogle ScholarPubMed
Larsen, A., Tao, Z., Bullard, S. A. and Arias, C. R. (2013). Diversity of the skin microbiota of fishes: evidence for host species specificity. FEMS Microbiology and Ecology 85, 483494.CrossRefGoogle ScholarPubMed
Lowrey, L., Woodhams, D. C., Tacchi, L. and Salinas, I. (2015). Topographical mapping of the Rainbow trout (Oncorhynchus mykiss) microbiome reveals a diverse bacterial community with antifungal properties in the skin. Applied Environmental Microbiology 81, 69156925.CrossRefGoogle Scholar
Luguterah, A. and Lawer, E. A. (2015). Effect of dietary guild (frugivory and insectivory) and other host characteristics on ectoparasite abundance (mite and nycteribiid) of chiropterans. Folia Parasitologica 62, 21.CrossRefGoogle ScholarPubMed
Luque, J. L., Mouillot, D. and Poulin, R. (2004). Parasite biodiversity and its determinants in coastal marine teleost fishes of Brazil. Parasitology 128, 671682.CrossRefGoogle ScholarPubMed
McNamara, M. K. A. and Cribb, T. H. (2011). Taxonomy, host specificity and dietary implications of Hurleytrematoides (Digenea: Monorchiidae) from chaetodontid fishes on the Great Barrier Reef. Parasitology International 60, 255269.CrossRefGoogle ScholarPubMed
McNamara, M. K. A., Adlard, R. D., Bray, R. A., Sasal, P. and Cribb, T. H. (2012). Monorchiids (Platyhelminthes: Digenea) of chaetodontid fishes (Perciformes): biogeographical patterns in the tropical Indo-West Pacific. Parasitology International 61, 288306.CrossRefGoogle ScholarPubMed
McNamara, M. K. A., Miller, T. L. and Cribb, T. H. (2014). Evidence for extensive cryptic speciation in trematodes of butterflyfishes (Chaetodontidae) of the tropical Indo-West Pacific. International Journal for Parasitology 44, 3748.CrossRefGoogle ScholarPubMed
Morand, S., Cribb, T. H., Kulbicki, M., Rigby, M. C., Chauvet, C., Dufour, V., Faliex, E., Galzin, R., Lo, C. M., Lo-Yat, A., Pichelin, S. and Sasal, P. (2000). Endoparasite species richness of New Caledonian butterfly fishes: host density and diet matter. Parasitology 121, 6573.CrossRefGoogle ScholarPubMed
Muñoz, G., Grutter, A. S. and Cribb, T. H. (2006). Endoparasite communities of five fish species (Labridae: Cheilininae) from Lizard Island: how important is the ecology and phylogeny of the hosts? Parasitology 132, 363374.CrossRefGoogle ScholarPubMed
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 Scholar
Pavoine, S. and Ricotta, C. (2013). Testing for phylogenetic signal in biological traits: the ubiquity of cross-product statistics. Evolution 67, 828840.CrossRefGoogle ScholarPubMed
Pavoine, S., Ollier, S., Pontier, D. and Chessel, D. (2008). Testing for phylogenetic signal in phenotypic traits: new matrices of phylogenetic proximities. Theoretical Population Biology 73, 7991.CrossRefGoogle ScholarPubMed
Plaisance, L. and Kritsky, D. C. (2004). Dactylogyrids (Platyhelminthes: Monogenoidea) parasitizing butterfly fishes (Teleostei: Chaetodontidae) from the coral reefs of Palau, Moorea, Wallis, New Caledonia, and Australia: species of Euryhaliotrematoides n. gen. and Aliatrema n. gen. Journal of Parasitology 90, 328341.CrossRefGoogle ScholarPubMed
Plaisance, L., Bouamer, S. and Morand, S. (2004). Description and redescription of Haliotrema species (Monogenoidea: Poloyonchoinea: Dactylogyridae) parasitizing butterfly fishes (Teleostei: Chaetodontidae) in the Indo-West Pacific Ocean. Parasitology Research 93, 7278.CrossRefGoogle ScholarPubMed
Plaisance, L., Littlewood, D. T. J., Olson, P. D. and Morand, S. (2005). Molecular phylogeny of gill monogeneans (Platyhelminthes, Monogenea, Dactylogyridae) and colonization of Indo-West Pacific butterflyfish hosts (Perciformes, Chaetodontidae). Zoologica Scripta 34, 425436.CrossRefGoogle Scholar
Poulin, R. (2004). Macroecological patterns of species richness in parasite assemblages. Basic and Applied Ecology 5, 423434.CrossRefGoogle Scholar
Poulin, R., Krasnov, B. R., Mouillot, D. and Thieltges, D. W. (2011). The comparative ecology and biogeography of parasites. Philosophical Transactions of the Royal Society of London: B, Biological Sciences 366, 23792390.CrossRefGoogle ScholarPubMed
Pratchett, M. S. (2005). Dietary overlap among coral-feeding butterflyfishes (Chaetodontidae) at Lizard Island, northern Great Barrier Reef. Marine Biology 148, 373382.CrossRefGoogle Scholar
Pratchett, M. S., Pradjakusuma, O. A. and Jones, G. P. (2006). Is there a reproductive basis to solitary living versus pair-formation in coral reef fishes? Coral Reefs 25, 8592.CrossRefGoogle Scholar
Pratchett, M. S., Hoey, A. S., Wilson, S. K., Messmer, V. and Graham, N. A. J. (2011). Changes in biodiversity and functioning of reef fish assemblages following coral bleaching and coral loss. Diversity 3, 424452.CrossRefGoogle Scholar
Pratchett, M. S., Hoey, A. S., Cvitanovic, C., Hobbs, J.-P. A. and Fulton, C. J. (2014). Abundance, diversity, and feeding behavior of coral reef butterflyfishes at Lord Howe Island. Ecology and Evolution 4, 36123625.CrossRefGoogle ScholarPubMed
Quigley, B. J. Z., López, D. G., Buckling, A., McKane, A. J. and Brown, S. P. (2012). The mode of host–parasite interaction shapes coevolutionary dynamics and the fate of host cooperation. Proceedings of the Royal Society of London B: Biological Sciences 279, 37423748.CrossRefGoogle ScholarPubMed
Rakers, S., Niklasson, L., Steinhagen, D., Kruse, C., Schauber, J., Sundell, K. and Paus, R. (2013). Antimicrobial peptides (AMPs) fromfishepidermis: perspectives for investigative dermatology. Journal of Investigative Dermatology 133, 11401149.CrossRefGoogle Scholar
Sanchez, L. M., Wong, W. R., Riener, R. M., Schulze, C. J. and Linington, R. G. (2012). Examining the fish microbiome: vertebrate-derived bacteria as an environmental niche for the discovery of unique marine natural products. PLoS ONE 7, e35398.CrossRefGoogle ScholarPubMed
Sasal, P. and Morand, S. (1998). Comparative analysis: a tool for studying monogenean ecology and evolution. International Journal for Parasitology 28, 16371644.CrossRefGoogle ScholarPubMed
Sasal, P., Morand, S. and Guégan, J.-F. (1997). Determinants of parasite species richness in mediterranean marine fishes. Marine Ecology Progress Series 149, 6171.CrossRefGoogle Scholar
Sikkel, P. C., Nemeth, D., McCammon, A. and Williams, E. H. (2009). Habitat and species differences in prevalence and intensity of Neobenedenia melleni (Monogenea: Capsalidae) on sympatric Caribbean surgeon fishes (Acanthuridae). Journal of Parasitology 95, 6368.CrossRefGoogle Scholar
Simková, A., Morand, S., Matejusová, I., Jurajda, P. V. and Gelnar, M. (2001). Local and regional influences on patterns of parasite species richness of central European fishes. Biodiversity Conservation 10, 511525.CrossRefGoogle Scholar
Simková, A., Verneau, O., Gelnar, M. and Morand, S. (2006). Specificity and specialization of congeneric monogeneans parasitizing cyprinid fish. Evolution 60, 10231037.CrossRefGoogle ScholarPubMed
Soler-Jiménez, L. C. and Fajer-Avila, E. J. (2012). The microecology of dactylogyrids (Monogenea: Dactylogyridae) on the gills of wild spotted rose snapper Lutjanus guttatus (Lutjanidae) from Mazatlan Bay, Mexico. Folia Parasitologica 59, 5358.CrossRefGoogle ScholarPubMed
Tavares, L. E. R. and Luque, J. L. (2008). Similarity between metazoan parasite communities of two sympatric brackish fish species from Brazil. Journal of Parasitology 94, 985989.CrossRefGoogle ScholarPubMed
Ullal, A. J., Wayne-Litaker, R. and Noga, E. J. (2008) Antimicrobial peptides derived from hemoglobin are expressed in epithelium of channel catfish (Ictalurus punctatus, Rafinesque). Developmental & Comparative Immunology 32, 13011312.CrossRefGoogle Scholar
Whittington, I. D., Cribb, B. W., Hamwood, T. E. and Halliday, J. A. (2000). Host-specificity of monogenean (platyhelminth) parasites: a role for anterior adhesive areas? International Journal for Parasitology 30, 305320.CrossRefGoogle ScholarPubMed
Yong, R. Q.-Y., Cutmore, S. C., Miller, T. L., Adlard, R. D. and Cribb, T. H. (2013). The ghost of parasites past: eggs of the blood fluke Cardicola chaetodontis (Aporocotylidae) trapped in the heart and gills of butterflyfishes (Perciformes: Chaetodontidae) of the Great Barrier Reef. Parasitology 140, 11861194.CrossRefGoogle ScholarPubMed
Yoshinaga, T., Nagakura, T., Ogawa, K., Fukuda, Y. and Wakabayashi, H. (2002). Attachment-inducing capacities of fish skin epithelial extracts on oncomiracidia of Benedenia seriolae (Monogenea: Capsalidae). International Journal for Parasitology 32, 381384.CrossRefGoogle Scholar
Cited by

Save article to Kindle

To save this article to your Kindle, first ensure is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the or variations. ‘’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Gill monogenean communities (Platyhelminthes, Monogenea, Dactylogyridae) of butterflyfishes from tropical Indo-West Pacific Islands
Available formats

Save article to Dropbox

To save this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Dropbox account. Find out more about saving content to Dropbox.

Gill monogenean communities (Platyhelminthes, Monogenea, Dactylogyridae) of butterflyfishes from tropical Indo-West Pacific Islands
Available formats

Save article to Google Drive

To save this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Google Drive account. Find out more about saving content to Google Drive.

Gill monogenean communities (Platyhelminthes, Monogenea, Dactylogyridae) of butterflyfishes from tropical Indo-West Pacific Islands
Available formats

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *