Three-way symbiotic relationships in whale sharks
Bradley M. Norman A B , Samantha D. Reynolds B C and David L. Morgan A DA Centre for Sustainable Aquatic Ecosystems, Harry Butler Institute, Murdoch University, 90 South Street, Murdoch, WA, Australia.
B ECOCEAN Inc., Serpentine, WA, Australia.
C Franklin Eco-Laboratory, The School of Biological Sciences, The University of Queensland, St Lucia, Qld, Australia.
D Corresponding author. Email: d.morgan@murdoch.edu.au
Pacific Conservation Biology 28(1) 80-83 https://doi.org/10.1071/PC20043
Submitted: 29 April 2020 Accepted: 18 February 2021 Published: 9 March 2021
Journal Compilation © CSIRO 2022 Open Access CC BY
Abstract
Symbiotic relationships between fishes and other organisms are not always easily defined, and three-way symbiotic relationships are rarely reported. Here we examine the relationship between the endangered whale shark, echeneids (remoras and sharksuckers) and a symbiotic copepod. Through their symbiosis with whale sharks, sharksuckers gain one food source from the host’s parasites and energetically-free transportation to foraging areas, where they are also able to feed on the prey targeted by their hosts. The relationship between whale sharks and sharksuckers is complex, and most accurately described as mutualism. Likewise, the whale shark and copepod relationship is also complex, and could be described as a parasitic relationship with commensal or even mutualistic characteristics. Although echeneids are not considered to form host-specific relationships and can be free-ranging, the whale shark copepod occurs only on whale sharks; its survival inextricably linked to that of its host.
Keywords: commensalism, copepods, Echeneidae, mutualism, parasitism, sharksuckers.
References
Britz, R., and Johnson, G. D. (2012). Ontogeny and homology of the skeletal elements that form the sucking disc of remoras (Teleostei, Echeneoidei, Echeneidae). Journal of Morphology 273, 1353–1366.| Ontogeny and homology of the skeletal elements that form the sucking disc of remoras (Teleostei, Echeneoidei, Echeneidae).Crossref | GoogleScholarGoogle Scholar | 22833478PubMed |
Brunnschweiler, J. M. (2006). Sharksucker-shark interaction in two carcharhinid species. Marine Ecology 27, 89–94.
| Sharksucker-shark interaction in two carcharhinid species.Crossref | GoogleScholarGoogle Scholar |
Clark, E., and Nelson, D. R. (1997). Young whale sharks, Rhincodon typus, feeding on a copepod bloom near La Paz, Mexico. Environmental Biology of Fishes 50, 63–73.
| Young whale sharks, Rhincodon typus, feeding on a copepod bloom near La Paz, Mexico.Crossref | GoogleScholarGoogle Scholar |
Cressey, R. F., and Lachner, E. A. (1970). The parasitic copepod diet and life history of diskfishes (Echeneidae). Copeia 1970, 310–318.
| The parasitic copepod diet and life history of diskfishes (Echeneidae).Crossref | GoogleScholarGoogle Scholar |
Gleiss, A. C., Wright, S., Liebsch, N., Wilson, R. P., and Norman, B. (2013). Contrasting diel patterns in vertical movement and locomotor activity of whale sharks at Ningaloo Reef. Marine Biology 160, 2981–2992.
| Contrasting diel patterns in vertical movement and locomotor activity of whale sharks at Ningaloo Reef.Crossref | GoogleScholarGoogle Scholar |
Helfman, G. S., Collette, B. B., Facey, D. E., and Bowen, B. W. (2009). The diversity of fishes. Second Edition. Vivar Printing, Malaysia.
Kwak, M. L., Heath, A. C. G., and Cardoso, P. (2020). Methods for the assessment and conservation of threatened animal parasites. Biological Conservation 248, .
| Methods for the assessment and conservation of threatened animal parasites.Crossref | GoogleScholarGoogle Scholar |
Lymbery, A. J., Lymbery, S. J., and Beatty, S. J. (2020). Fish out of water: Aquatic parasites in a drying world. IJP: Parasites and Wildlife 12, 300–307.
| Fish out of water: Aquatic parasites in a drying world.Crossref | GoogleScholarGoogle Scholar |
Meekan, M., Austin, C. M., Tan, M. H., Wei, N.-W. V., Miller, A., Pierce, S. J., Rowat, D., Stevens, G., Davies, T. K., Ponzo, A., and Gan, H. M. (2017). iDNA at sea: recovery of whale shark (Rhincodon typus) mitochondrial DNA sequences from the whale shark copepod (Pandarus rhincodonicus) confirms global population structure. Frontiers in Marine Science 4, 420.
| iDNA at sea: recovery of whale shark (Rhincodon typus) mitochondrial DNA sequences from the whale shark copepod (Pandarus rhincodonicus) confirms global population structure.Crossref | GoogleScholarGoogle Scholar |
Misganaw, K., and Getu, A. (2016). Review of major parasitic crustacean in fish. Fisheries and Aquaculture 7, 3.
Morgan, D. L., Tang, D., and Peverell, S. C. (2010). Critically endangered Pristis microdon (Elasmobranchii), as a host for the Indian parasitic copepod, Caligus furcisetifer Redkar, Rangnekar et Murti, 1949 (Siphonostomatoida): New records from northern Australia. Acta Parasitologica 55, 419–423.
| Critically endangered Pristis microdon (Elasmobranchii), as a host for the Indian parasitic copepod, Caligus furcisetifer Redkar, Rangnekar et Murti, 1949 (Siphonostomatoida): New records from northern Australia.Crossref | GoogleScholarGoogle Scholar |
Norman, B. M., Holmberg, J. A., Arzoumanian, Z., Reynolds, S. D., Wilson, R. P., Rob, D., Pierce, S. J., Gleiss, A. C., De La Parra, R., Galvan, B., Ramirez-macias, D., Robinson, D., Fox, S., Graham, R., Rowat, D., Potenski, M., Levine, M., Mckinney, J. A., Hoffmayer, E., Dove, A., Hueter, R., Ponzo, A., Araujo, G., Aca, E., David, D., Rees, R., Duncan, A., Rohner, C. A., Prebble, C. E. M., Hearn, A., Acuna, D., Berumen, M. L., Vázquez, A., Green, J., Bach, S. S., Schmidt, J. V., Beatty, S. J., and Morgan, D. L. (2017). Undersea constellations: the global biology of an endangered marine mega-vertebrate further informed through citizen science. BioScience 67, 1029–1043.
| Undersea constellations: the global biology of an endangered marine mega-vertebrate further informed through citizen science.Crossref | GoogleScholarGoogle Scholar |
Norman, B. M., Newbound, D. R., and Knott, B. (2000). A new species of Pandaridae (Copepoda), from the whale shark Rhincodon typus (Smith). Journal of Natural History 34, 355–366.
| A new species of Pandaridae (Copepoda), from the whale shark Rhincodon typus (Smith).Crossref | GoogleScholarGoogle Scholar |
Pierce, S. J., and Norman, B. M. (2016). Rhincodon typus. International Union for Conservation of Nature (IUCN) Red List of Threatened Species. Available at www.iucnredlist.org/details/19488/0 (accessed 30 June 2020).
Ritter, E. K. (2002). Analysis of sharksucker, Echeneis naucrates, induced behavior patterns in the blacktip shark, Carcharhinus limbatus. Environmental Biology of Fishes 65, 111–115.
| Analysis of sharksucker, Echeneis naucrates, induced behavior patterns in the blacktip shark, Carcharhinus limbatus.Crossref | GoogleScholarGoogle Scholar |
Rowat, D., and Brooks, K. S. (2012). A review of the biology, fisheries and conservation of the whale shark Rhincodon typus. Journal of Fish Biology 80, 1019–1056.
| A review of the biology, fisheries and conservation of the whale shark Rhincodon typus.Crossref | GoogleScholarGoogle Scholar | 22497372PubMed |
Stead, D. G. (1963). ‘Sharks and rays of Australian seas.’ (Angus and Robinson: Sydney.)
Thomson, J. A., Araujo, G., Labaja, J., McCoy, E., Murray, R., and Ponzo, A. (2017). Feeding the world’s largest fish: highly variable whale shark residency patterns at a provisioning site in the Philippines. Royal Society Open Science 4, 170394.
| Feeding the world’s largest fish: highly variable whale shark residency patterns at a provisioning site in the Philippines.Crossref | GoogleScholarGoogle Scholar | 28989750PubMed |
Williams, E. H., Mignucci-Giannoni, A. A., Bunkley-Williams, L., Bonde, R. K., Self-Sullivan, C., Preen, A., and Cockcroft, V. G. (2003). Echeneid-sirenian associations, with information on sharksucker diet. Journal of Fish Biology 63, 1176–1183.
| Echeneid-sirenian associations, with information on sharksucker diet.Crossref | GoogleScholarGoogle Scholar |