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Type: Article
Published: 2023-01-23
Page range: 381-390
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First record of the cirripede Anelasma squalicola Darwin, 1852 (Pollicipedidae) in the Mediterranean Sea

1Cavanilles Institute of Biodiversity and Evolutionary Biology, Science Park, University of Valencia, Paterna, Valencia, Spain.
2Alfred Wegener Institute Helmholtz Centre for Polar and Marine Research (AWI) Bremenhaven, Germany.
1Cavanilles Institute of Biodiversity and Evolutionary Biology, Science Park, University of Valencia, Paterna, Valencia, Spain.
3Instituto Español de Oceanografía (I.E.O.—C.S.I.C.), C.O. Málaga, Fuengirola, Spain.
1Cavanilles Institute of Biodiversity and Evolutionary Biology, Science Park, University of Valencia, Paterna, Valencia, Spain.
Crustacea Barnacles Metazoan parasites Etmopterus spinax Distribution Alboran Sea

Abstract

Anelasma squalicola Darwin 1852, is a barnacle that occurs on elasmobranchs from the Atlantic, Pacific, Arctic and Indian Ocean. It infects sharks of the families Etmopteridae and Pentanchidae. The barnacle attaches sub-dermally to its hosts, relying on its interstitial fluid for its nourishment. Herein we present the first record of this species in the Mediterranean Sea, from Etmopterus spinax (Linnaeus, 1758) caught during a bottom-trawl survey in the Alboran Sea (western Mediterranean) in 2017. The overall prevalence of infection was very low (0.22%). The calculated HSI index for the parasitized individual was lower compared to overall means of other individuals and could indicate a potential physiological alteration in the host.

 

References

  1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. & Lipman, D.J. (1990) Basic local alignment search tool. Journal of Molecular Biology, 215 (3), 403–410. https://doi.org/10.1016/S0022-2836(05)80360-2
    Angulo, A. & Sibaja-Cordero, J.A. (2021) First record of the parasitic barnacle Anelasma squalicola Darwin, 1852 (Pollicipedomorpha: Pollicipedidae) in the Eastern Pacific Ocean and a new host report: Etmopterus benchleyi Vásquez, Ebert & Long, 2015 (Squaliformes: Etmopteridae). Zootaxa, 5072 (2), 165–172. https://doi.org/10.11646/zootaxa.5072.2.5
    Bergum, H.O.T. (2016) A morphological study of the parasitic barnacle, Anelasma squalicola (Lovén, 1844). The University of Bergen, Bergen, 93 pp.
    Bertrand, J.A., de Sola, L.G., Papaconstantinou, C., Relini, G. & Souplet, A. (2002) The general specifications of the MEDITS surveys. Scientia Marina, 66 (S2), 9–17. https://doi.org/10.3989/scimar.2002.66s29
    Besnard, L., Duchatelet, L., Bird, C.S., Le Croizier, G., Michel. L., Pinte, N., Lepoint. G., Schaal, G., Vieira, R.P., Gonçalves, J.M.S., Martin, U. & Mallefet, J. (2022) Diet consistency but large-scale isotopic variations in a deep-sea shark: The case of the velvet belly lantern shark, Etmopterus spinax, in the northeastern Atlantic region and Mediterranean Sea. Deep-Sea Research, Part 1: Oceanographic Research Papers, 182, 103708. https://doi.org/10.1016/j.dsr.2022.103708
    Biccard, A. & Griffiths, C.L. (2016) Additions to the barnacle (Crustacea: Cirripedia) fauna of South Africa. African Zoology, 51 (2), 99–116. https://doi.org/10.1080/15627020.2016.1196610
    Carrassón, M. & Cribb, T.H. (2014) Benign effect of the fish parasitic isopod Ceratothoa cf. imbricata on Selenotoca multifasciata (Scatophagidae) from Australia. Diseases of Aquatic Organisms, 100, 173–180. https://doi.org/10.3354/dao02751
    Catarino, D., Knutsen, H., Veríssimo, A., Olsen, E.M., Jorde, P.E., Menezes, G., Annæs, H., Stanković, D., Company, J.P., Neat, F., Danovaro, R., Dell’anno, A., Rochowski, B. & Stefanni, S. (2015) The Pillars of Hercules as a bathymetric barrier to gene flow promoting isolation in a global deep‐sea shark (Centroscymnus coelolepis). Molecular Ecology, 24(24), 6061–6079. https://doi.org/10.1111/mec.13453
    Causey, D. (1957) Another barnacle. The Educational Focus, 28 (2), 18–20.
    Chan, B.K., Dreyer, N., Gale, A. S., Glenner, H., Ewers-Saucedo, C., Pérez-Losada, M., Kolbasov, G.A., Crandall K.A. & Høeg, J.T. (2021) The evolutionary diversity of barnacles, with an updated classification of fossil and living forms. Zoological Journal of the Linnean Society, 193 (3), 789–846. https://doi.org/10.1093/zoolinnean/zlaa160
    Coelho, R. & Erzini, K. (2007) Population parameters of the smooth lantern shark, Etmopterus pusillus, in southern Portugal (NE Atlantic). Fisheries Research, 86, 42–57. https://doi.org/10.1016/j.fishres.2007.04.006
    Coelho, R. & Erzini, K. (2008) Life history of a wide-ranging deepwater lantern shark in the north-east Atlantic, Etmopterus spinax (Chondrichthyes: Etmopteridae), with implications for conservation. Journal of Fish Biology, 73, 1419–1443. https://doi.org/10.1111/j.1095-8649.2008.02021.x
    Coelho, R. & Erzini, K. (2010) Depth distribution of the velvet belly, Etmopterus spinax, in relation to growth and reproductive cycle: The case study of a deep-water lantern shark with a wide-ranging critical habitat. Marine Biology Research, 6, 381–389. https://doi.org/10.1080/17451000802644706
    Compagno, L.J.V. (1984) An annotated and illustrated catalogue of shark species known to date. Part 1 Hexanchiformes to Lamniformes. Rome, FAO species catalogue, Rome, 249 pp.
    Compagno, L., Dando, M. & Fowler, S. (2005) Guía de campo de los tiburones del mundo. OMEGA, Barcelona, 378 pp.
    Cressey, D. (2013) Barnacles trust their sperm to the waves. Nature News, Springer Nature, 2013, 1–2. https://doi.org/10.1038/nature.2013.12220
    Eliassen, L. (2016) An investigation into the parasitic barnacle, Anelasma squalicola; prevalence, infection behaviour and effects on its host, Etmopterus spinax, in Lusterfjord, Norway. The University of Bergen, Bergen, 88 pp.
    Espínola-Novelo, J.F., Escribano, R. & Oliva, M.E. (2018) Metazoan parasite communities of two deep-sea elasmobranchs: the southern lanternshark, Etmopterus granulosus, and the largenose catshark, Apristurus nasutus, in the Southeastern Pacific Ocean. Parasite, 25, 1–9. https://doi.org/10.1051/parasite/2018054
    Fernández-Ovies, C.L. (1995) Crustáceos parásitos sobre tiburones bentopelágicos del talud continental asturiano. 2. Anelasma squalicola (Loven) (Cirripedia: Thoracica: Anelasmatidae). Boletín de Ciencias de la Naturaleza, 43, 7–14.
    Ferrón, H.G., Herráiz, J.L., Botella, H. & Martínez-Pérez, C. (2019) Pre-Messinian ecological diversity of Mediterranean sharks revealed by the study of their dermal denticles. Journal of Palaeontology, 34 (2), 289–298. https://doi.org/10.7203/sjp.34.2.16118
    Finucci, B., Derrick, D., Dia, M., Ducrocq, M., Neat, F.C., Pacoureau, N., Serena, F. & VanderWright, W.J. (2002) Etmopterus spinax. The IUCN Red List of Threatened Species 2021. Available from: https://www.iucnredlist.org/species/161388/124475610 (accessed 31 March 2022)
    Froese, R. & Pauly, D. (2022) FishBase. Available from: https://www.fishbase.org (accessed 21 June 2022)
    Frost, W.E. (1928) The nauplius larva of Anelasma squalicola (Lovén). Journal of the Marine Biological Association of the United Kingdom, 15.1, 125–128. https://doi.org/10.1017/S0025315400055570
    Fulton, T.W. (1902) The rate of growth of fishes. 20th Annual Report of the Fishery Board of Scotland, 1902, 326–446.
    Gaines, S., Brown, S. & Roughgarden, J. (1985) Spatial variation in larval concentrations as a cause of spatial variation in settlement for the barnacle Balanus glandula. Oecologia, 67, 267–272. https://doi.org/10.1007/BF00384297
    Gubili, C., Macleod, K., Perry, W., Hanel, P., Batzakas, I., Farrell, E.D., Lynghammar, A., Mancusi, C., Mariani, S. & Menezes, G.M. (2016) Connectivity in the deep: Phylogeography of the velvet belly lanternshark. Deep Sea Research Part I: Oceanographic Research Papers, 115, 233–239. https://doi.org/10.1016/j.dsr.2016.07.002
    Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic acids symposium Series, 41 (41), 95–98.
    Hickling, C.F. (1963) On the small deep-sea shark Etmopterus spinax L., and its cirripede parasite Anelasma squalicola (Lovén). Journal of the Linnean Society of London, Zoology, 45 (303), 17–4. https://doi.org/10.1111/j.1096-3642.1963.tb00484.x
    Hussey, N.E., Cocks, D.T., Dudley, S.F.J., McCarthy, I.D. & Wintner, S.P. (2009) The condition conundrum: application of multiple condition indices to the dusky shark Carcharhinus obscurus. Marine Ecology Progress Series, 380, 199–212. https://doi.org/10.3354/meps07918
    Karvonen, A., Kristjánsson, B.K., Skúlason, S., Lanki, M., Rellstab, C. & Jokela, J. (2013) Water temperature, not fish morph, determine parasite infections of sympatric Icelandic threespine sticklebacks (Gasterosterus aculeatus). Ecology and Evolution, 3 (6), 1507–1517. https://doi.org/10.1002/ece3.568
    Kawanishi, R., Kohya, N., Sogabe, A. & Hata, H. (2019) A comparison of body condition of the yellowstriped butterfish Labracoglossa argenteiventris in relation to parasitism by the cymothoid isopod Ceratothoa arimae. Parasitology International, 72, 101932. https://doi.org/10.1016/j.parint.2019.101932
    Kinne, O. (1985) Diseases of Marine Animals. Vol. IV. Part 2. Introduction, Reptilia, Aves, Mammalia. Hamburg: Biologische Anstalt Helgoland, 884 pp.
    Krkošek, M. (2010) Host density thresholds and disease control for fisheries and aquaculture. Aquaculture Environment Interactions, 1 (1), 21–32. https://doi.org/10.3354/aei0004
    L‘Helguen, S., Le Corre, P., Madec, C., Morin, P. (2002) New and regenerated production in the Almeria-Oran front area, eastern Alboran Sea. Deep Sea Research, Part I: Oceanographic Research Papers, 49, 83–99. https://doi.org/10.1016/S0967-0637(01)00044-9
    Long, D.J. & Waggoner, B.M. (1993) The ectoparasitic barnacle Anelasma (Cirripedia, Thoracica, Lepadomorpha) on the shark Centroscyllium nigrum (Chondrichthyes, Squalidae) from the Pacific sub-Antarctic. Systematic Parasitology, 26 (2), 133–136. https://doi.org/10.1007/BF00009220
    Marques, D.C.R.D. (2019) Metazoan Parasites in deep-sea sharks Part I. A Review of the Parasite Fauna of sharks of the genus Etmopterus Part II. Metazoan gastrointestinal parasites of Etmopterus spinax (L., 1758) from southern Norwegian waters. The Arctic University of Norway, Tromsø, 93 pp.
    Martín-Lázaro, A. (2014) Aspectes de la biologia reproductiva del tauró batipelàgic Etmopterus spinax (Elasmobranchii, Squalidae) en el Mar Balear. Universitat de València, Valencia, 62 pp.
    McMillan, M.N., Izzo, C., Junge, C., Albert, O.T., Jung, A. & Gillanders, B.M. (2017) Analysis of vertebral chemistry to assess stock structure in a deep-sea shark, Etmopterus spinax. ICES Journal of Marine Science, 74 (3), 793–803. https://doi.org/10.1093/icesjms/fsw176
    Nuun, G., Theisen, B., Christensen, B. & Arctander, P. (1996) Simplicity correlated size of the nuclear 28S ribosomal DNA D3 expansion segment in the crustacean order Isopoda. Journal of Molecular Evolution, 42, 211–223. https://doi.org/10.1007/BF02198847
    Ommundsen, A., Noever, C. & Glenner, H. (2016) Caught in the act: phenotypic consequences of a recent shift in feeding strategy of the shark barnacle Anelasma squalicola (Lovén, 1844). Zoomorphology, 135, 51–65. https://doi.org/10.1007/s00435-015-0296-1
    Patarnello, T., Volckaert, F.A. & Castillo, R. (2007) Pillars of Hercules: is the Atlantic-Mediterranean transition a phylogeographical break? Molecular Ecology, 16, 4426–4444. https://doi.org/10.1111/j.1365-294X.2007.03477.x
    Rees, D.J., Noever, C., Finucci, B., Schnabel, K., Leslie, R.E., Drewery, J., Bergum, H.O.T., Dutilloy, A. & Glenner, H. (2019) De novo innovation allows shark parasitism and global expansion of the barnacle Anelasma squalicola. Current Biology, 29 (12), R562–R563. https://doi.org/10.1016/j.cub.2019.04.053
    Rees, D.J., Noever, C., Høeg, J.T., Ommundsen, A. & Glenner, H. (2014) On the origin of a novel parasitic-feeding mode within suspension-feeding barnacles. Current Biology, 24, 1429–1434. https://doi.org/10.1016/j.cub.2014.05.030
    Rey, J., De Sola, L.G. & Massutí, E. (2005) Distribution and Biology of the Blackmouth Catshark Galeus melastomus in the Alboran Sea (Southwestern Mediterranean). Journal of Northwest Atlantic Fishery Science, 35, 215–223. https://doi.org/10.2960/J.v35.m484
    Rogowski, D.L. & Stockwell, C.A. (2005) Parasites and salinity: costly tradeoffs in a threatened species. Oecologia, 146 (4), 615–622. https://doi.org/10.1007/s00442-005-0218-x
    Sabadel, A.J.M., Cresson, P., Finucci, B. & Bennett, J. (2022) Unravelling the trophic interaction between a parasitic barnacle (Anelasma squalicola) and its host Southern lanternshark (Etmopterus granulosus) using stable isotopes. Parasitology, 2022, 1–9. https://doi.org/10.1017/ S0031182022001299
    Soto-Navarro, J., Somot, S., Sevault, F., Beuvier, J., Criado-Aldeanueva, F., García-Lafuente, J. & Béranger, K. (2015) Evaluation of regional ocean circulation models for the Mediterranean Sea at the Strait of Gibraltar: volume transport and thermohaline properties of the outflow. Climate Dynamics, 44 (5), 1277–1292. https://doi.org/10.1007/s00382-014-2179-4
    Spedicato, M.T., Massutí, E., Mérigot, B., Tserpes, G., Jadaud, A. & Relini, G. (2019) The MEDITS trawl survey specifications in an ecosystem approach to fishery management. Scientia Marina, 83 (S1), 9–20. https://doi. org/10.3989/scimar.04915.11X
    Tintore, J., Violette, P.E., Blade, I. & Cruzado, A. (1988) A Study of an Intense Density Front in the Eastern Alboran Sea: The Almeria-Oran Front. Journal of Physical Oceanography, 18 (10), 1384–1297. https://doi.org/10.1175/1520-0485(1988)018<1384:ASOAID>2.0.CO;2
    Whiting, M.F. (2002) Mecoptera is paraphyletic: multiple genes and phylogeny of Mecoptera and Siphonaptera. Zoologica Scripta, 31 (1), 93–104. https://doi.org/10.1046/j.0300-3256.2001.00095.x
    WoRMS. (2022). Pollicipedidae Leach, 1817. Available from: https://www.marinespecies.org/aphia.php?p=taxdetails&id=106054 (accessed 23 April 2022)
    Yano, K. & Musick, J.A. (2000) The effect of the mesoparasitic barnacle Anelasma on the development of the reproductive organs of deep-sea squaloid sharks, Centroscyllium and Etmopterus. Environmental Biology of Fishes, 59 (3), 329–339. https://doi.org/10.1023/A:1007649227422

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