Abstract
The biology, including accompanying ectoparasitic fauna, remains unstudied for several elasmobranchs off the Canary Islands in spite of concerns over their conservation. Within this region, this is the first report of copepod associations with these fishes. Twenty smooth hammerhead sharks, Sphyrna zygaena, and one common stingray, Dasyatis pastinaca, were inspected for symbionts on their body surface. Symbiotic siphonostomatoids were collected from 18 S. zygaena hosts and represent two different species, i.e., Alebion crassus (Caligidae) and Pandarus cranchii (Pandaridae). A high prevalence of 90% and a mean infection of 8.3 individuals per infected host were exhibited by A. crassus, while only a single P. cranchii was collected. Both these findings represent new geographical records. Additionally, one free-ranging common stingray Dasyatis pastinaca was opportunistically inspected and 11 Pseudocharopinus pillaii (Lernaeopodidae) collected which constitutes a new host record and a new geographical record. A re-description with detail regarding the morphology of the appendages is provided for the first time. Due to the morphological similarity between P. pillaii and P. malleus, a molecular analysis of the partial mitochondrial DNA cytochrome oxidase I gene was done in an attempt to determine if there is molecular divergence between the two species. This provided an estimate of the phylogenetic relationships amongst four Pseudocharopinus species (P. bicaudatus, P. pteromylaei, P. malleus, and P. pillaii) with Charopinus dubius as an outgroup as an alternative hypothesis to compare with the previous morphological topology estimated for all Pseudocharopinus species.
Similar content being viewed by others
Data availability
The datasets generated during and/or analyzed during the current study are available in the GenBank repository, https://www.ncbi.nlm.nih.gov.
Code availability
Not applicable.
References
Boxshall GA, Halsey SH (2004) An introduction to copepod diversity. The Ray Society, London
Brito A, Pascual PJ, Falcón J, Sancho A, González G (2002) Peces de las Islas Canarias: catálogo comentado e ilustrado. Francisco Lemus, La Laguna
Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al revisited. J Parasitol 83:575–583. https://doi.org/10.2307/3284227
CITES (Convention on International Trade in Endangered Species of wild fauna and flora) Proposal (2013) Inclusion of Sphyrna lewini (scalloped hammerhead shark) in Appendix II in accordance with Article II paragraph 2(a) of the Convention and satisfying Criterion A in Annex 2a of Resolution Conf. 9.24 (Rev. CoP14). Inclusion of Sphyrna mokarran (great hammerhead shark) and Sphyrna zygaena (smooth hammerhead shark) in Appendix II in accordance with Article II paragraph 2(b) of the Convention and satisfying Criterion A in Annex 2b of Resolution Conf. 9.24 (Rev. CoP14), CoP16 Proposal 43 by Brazil, Costa Rica and Honduras. https://cites.org/sites/default/files/eng/cop/16/prop/E-CoP16-Prop-63.pdf.
Cressey RF (1967) Revision of the family Pandaridae (Copepoda: Caligoida). Proc US Natl Mus 121:1–133. https://doi.org/10.5479/si.00963801.121-3570.1
Cressey RF (1972) Revision of the genus Alebion (Copepoda: Caligoida). Smithson Contrib Zool 123:1–29. https://doi.org/10.5479/si.00810282.123
Dippenaar SM (2018a) Resurrection of Alebion difficile (van Beneden, 1892) (Copepoda: Siphonostomatoida: Caligidae) with notes on other species of Alebion Krøyer, 1863 collected from elasmobranchs off South Africa and an updated key of the adult females. Syst Parasitol 95:881–891. https://doi.org/10.1007/s11230-018-9811-3
Dippenaar SM (2018b) Symbiotic Siphonostomatoida (Copepoda) collected from white sharks, Carcharodon carcharias (Lamniformes, Lamnidae), during the OCEARCH expedition along the coast of South Africa. Crustaceana 91:103–111. https://doi.org/10.1163/15685403-00003746
Dippenaar SM (2019) Cladistic analysis of the morphological characters of Pseudocharopinus Kabata, 1964 and keys to the species of Pseudocharopinus and Charopinus Krøyer, 1963 based on the morphology of the adult females. Syst Parasitol 96:799–804. https://doi.org/10.1007/s11230-019-09889-1
Dippenaar SM, Molele RA (2015) Siphonostomatoid copepods infecting Squalus acutipinnis Regan, 1908 off South Africa. Afr J Mar Sci 37:605–608. https://doi.org/10.2989/1814232x.2015.1093024
Dippenaar SM, van Tonder RC, Wintner SP (2009) Is there evidence of niche restriction in the spatial distribution of Kroyeria dispar Wilson, 1935, K. papillipes Wilson, 1932 and Eudactylina pusilla Cressey, 1967 (Copepoda: Siphonostomatoida) on the gill filaments of tiger sharks Galeocerdo cuvier off KwaZulu-Natal, South Africa? Hydrobiologia 619:89–101. https://doi.org/10.1007/s10750-008-9602-y
Dippenaar SM, Mathibela RB, Bloomer P (2010) Cytochrome oxidase I sequences reveal possible cryptic diversity in the cosmopolitan symbiotic copepod Nessipus orientalis Heller, 1868 (Pandaridae: Siphonostomatoida) on elasmobranch hosts from the KwaZulu-Natal coast of South Africa. Exp Parasitol 125:42–50. https://doi.org/10.1016/j.exppara.2009.08.017
Ebert DA, Stehmann MFW (2013) Sharks, batoids and chimaeras of the North Atlantic. Species Catalogue for Fishery Purposes No. 7. Food and Agriculture Organization of the United Nations, Rome
Fitch WM (1971) Toward defining the course of evolution: minimum change for a specified tree topology. Syst Zool 20:406–416. https://doi.org/10.2307/2412116
Folmer O, Black N, Hoen W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of Mitochondrial Cytochrome C Oxidase subunit 1 from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299
Froese R, Pauly D (eds) (2020) FishBase. http://www.fishbase.org. Accessed 25 February 2021
Humes AG, Gooding RU (1964) A method for studying the external anatomy of copepods. Crustaceana 6:238–240. https://doi.org/10.1163/156854064x00650
Huys R, Boxshall GA (1991) Copepod evolution. The Ray Society, London
Izawa K (2010) Redescription of eight species of parasitic copepods (Siphonostomatoida, Pandaridae) infecting Japanese elasmobranchs. Crustaceana 83:313–341. https://doi.org/10.1163/001121609x12591347509329
Kabata Z (1964) Revision of the genus Charopinus Krøyer, 1863 (Copepoda: Lernaeopodidae). Vidensk Meddr Dansk Naturh Foren 127:85–112
Kabata Z (1968) Copepoda parasitic on Australian fishes. J Nat His 2:505–523
Kabata Z (1979) Parasitic copepods of British fishes. The Ray Society, London
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Last PR, White WT, de Carvalho MR, Séret B, Stehmann MFW, Naylor GJ (eds) (2016) Rays of the World. CSIRO Publising, Clayton South
Luque JL, Farfán C (1991) Some copepods parasitic on elasmobranch fishes from the Peruvian coast, with the description of two new species of Eudactylina van Beneden, 1853 (Eudactylinidae) and four new records. J Nat His 25:1233–1246. https://doi.org/10.1080/00222939100770761
Maddison DR, Maddison WP (2001) MacClade version 4: analysis of phylogeny and character evolution. Sinauer Associates, Sunderland
Mangena T, Jordaan BP, Dippenaar SM (2014) Phylogenetic relationships and genetic diversity of Nemesis Risso, 1926 species found on different elasmobranch host species off the KwaZulu-Natal coast, South Africa. Afr J Mar Sci 36:163–173. https://doi.org/10.2989/1814232x.2014.912992
Narváez K, Osaer F (2017a) The marine leech Stibarobdella macrothela parasitic on the angel shark Squatina squatina. Mar Biodivers 47:153–154. https://doi.org/10.1007/s12526-016-0444-y
Narváez K, Osaer F (2017b) The marine leech Branchellion torpedinis parasitic on the angelshark Squatina squatina and the marbled electric ray Torpedo marmorata. Mar Biodivers 47:987–990. https://doi.org/10.1007/s12526-016-0535-9
Øines Ø, Heuch PA (2007) Caligus elongatus Nordmann genotypes on wild and farmed fish. J Fish Dis 30:81–91. https://doi.org/10.1111/j.1365-2761.2007.00783.x
Osaer F, Narváez K (2016) The angel shark Squatina squatina prey of the isopod Aegapheles deshaysiana. Mar Biodivers 46:29–30. https://doi.org/10.1007/s12526-015-0358-0
Pillai NK (1962) Copepods parasitic on south Indian fishes: families Lernaeopodidae and Naobranchidae. J Mar Biol Ass India 4:58–94
Pillai NK (1985) Copepod parasites of marine fishes. Director, Zoological Survey of India, Calcutta
QIAGEN CLC Genomics Workbench 20.0. https://digitalinsights.qiagen.com/
Raibaut A, Maamouri K (1975) Remarques sur deux espèces de Copépodes parasites de Sélaciens de Tunisie. Bull Mus Natl Hist Nat 3:1037–1047
RD (Royal Decree) (139/2011) Publication of 4 February, for the development of the List of Wild Species in Regime of Special Protection and the Spanish Catalog of Endangered Species. Official State Gazette, Spain 46 (BOE-A-2011–35829)
Rokicki J, Bychawska D (1991) Parasitic copepods of Carcharhinidae and Sphyridae (Elasmobranchia) from the Atlantic Ocean. J Nat His 25:1439–1448. https://doi.org/10.1080/00222939100770911
Sepahvand V, Shahabi S (2021) First molecular evidence for two new associate copepods of genus Clausidium Kossmann, 1874 (Copepoda: Cyclopoida: Clausidiidae) from the Persian Gulf and Gulf of Oman. Nauplius 29. https://doi.org/10.1590/2358-2936e2021019
Shiino SM (1955) Alebion echinatus Capart from Japanese Waters, with observations on the newly found male form. Pac Sci 9:177–182
Swofford DL (2002) PAUP* 4.0b10. Phylogenetic analysis using parsimony and other methods. Sinauer Associations, Sunderland
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 25:4876–4882. https://doi.org/10.1093/nar/25.24.4876
Acknowledgements
We wish to thank O. Mustad & Son A.S. for providing research equipment and the General Secretary for Fisheries and the service from the Marine Reserve Isla Graciosa e islotes del norte de Lanzarote. Additionally, the University of Limpopo is acknowledged for laboratory support.
Funding
Partial financial support to ElasmoCan for field work was received from Loro Parque Fundación.
Author information
Authors and Affiliations
Contributions
SMD collected specimens used for molecular study, examined, dissected, drew, and identified the collected copepods and wrote the manuscript; KN and FO collected and quantified the copepods from elasmobranchs off the Canary Islands; and TM assisted with copepod collection in South Africa and did the molecular analysis. All authors contributed to the literature search and the final version of the manuscript.
Corresponding author
Ethics declarations
Ethics approval
No approval of research ethics committees was required for the described sampling work in the Canary Islands according to Spanish law (Royal Decree 53/2013). Field sampling and specimen collection off the Canary Islands and genetic access to Pseudocharopinus pillaii off the Canary Islands, compliant with the Nagoya Protocol on Access to Genetic Resources, were done following the national legislation under administrative authorizations from the Spanish Ministry for the Ecologic Transition and the Demographic Challenge.
Conflict of interest
The authors declare no competing interests.
Additional information
Section Editor: Guillermo Salgado-Maldonado
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Dippenaar, S.M., Narváez, K., Osaer, F. et al. Symbiotic Siphonostomatoida (Copepoda) of the hammerhead shark species Sphyrna zygaena (Carcharhiniformes: Sphyrnidae) and stingray Dasyatis pastinaca (Myliobatiformes: Dasyatidae) off the Canary Islands, with a re-description of Pseudocharopinus pillaii Kabata, 1979. Parasitol Res 120, 3739–3747 (2021). https://doi.org/10.1007/s00436-021-07332-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-021-07332-3