Scientia Marina, Vol 81, No 1 (2017)

Northernmost record of the pantropical portunid crab Cronius ruber in the eastern Atlantic (Canary Islands): natural range extension or human-mediated introduction?


https://doi.org/10.3989/scimar.04551.17B

José A. González
Ecología Marina Aplicada y Pesquerías, i-UNAT, Universidad de Las Palmas de Gran Canaria, Spain
orcid http://orcid.org/0000-0001-8584-6731

Raül Triay-Portella
Ecología Marina Aplicada y Pesquerías, i-UNAT, Universidad de Las Palmas de Gran Canaria, Spain
orcid http://orcid.org/0000-0002-7591-6254

Aitor Escribano
Université de Liège, Belgium
orcid http://orcid.org/0000-0002-1405-5227

José A. Cuesta
Instituto de Ciencias Marinas de Andalucía, CSIC, Spain
orcid http://orcid.org/0000-0001-9482-2336

Abstract


The pantropical crab Cronius ruber (Lamarck, 1818) (Brachyura: Portunidae) is recorded for the first time from the Canary Islands. Previously known from off Cape Verde Islands and Senegal, this is the northernmost record of the species in the eastern Atlantic Ocean. Crabs have been caught by means of a collecting small trap for sampling in shallow waters, and then identified by both morphological characters and DNA barcoding (16S). Cytochrome c oxidase I partial sequence has been obtained for this species for the first time. This relatively large and very aggressive crab species seems to be rapidly occupying both hard substrates (sublittoral caves) and soft substrates (sand with seagrass meadow) adjacent to shallow rocky bottoms, at depths between 2 and 10 m, in the warm southern waters of Gran Canaria Island. The reasons for this species’ occurrence are discussed herein. Among them, natural range extension may be a consequence of tropicalization in the eastern Atlantic. Also, a human-mediated introduction could be based on the heavy traffic of ships (ballast waters or oil platforms) arriving at the Canary Islands from African countries and from Brazil in the last decade.

Keywords


zoogeografía; expansión natural; introducción antropogénica; Brachyura; cangrejo; Cronius ruber; Islas Canarias; Atlántico oriental; código de barras genético

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References


Afonso P., Porteiro F.M., Fontes J., et al. 2013. New and rare coastal fishes in the Azores islands: occasional events or tropicalization process? J. Fish. Biol. 83: 272-294. https://doi.org/10.1111/jfb.12162 PMid:23902306

Araújo R., Wirtz P. 2015. The decapod crustaceans of Madeira Island – an annotated checklist (Crustacea, Decapoda). Spixiana 38: 205-218.

Atchison A.D., Sammarco P.W., Brazeau D.A. 2008. Genetic connectivity in corals on the Flower Garden Banks and surrounding oil/gas platforms, Gulf of Mexico. J. Exp. Mar. Biol. Ecol. 365: 1-12. https://doi.org/10.1016/j.jembe.2008.07.002

Attrill M.J., Hartnoll R.G., Rice A.L. 1991. Aspects of the biology of the deep-sea crab Geryon trispinosus from the Porcupine Seabight. J. Mar. Biol. Assoc. U.K. 71: 311-328. https://doi.org/10.1017/S0025315400051626

Barton E.D., Arístegui J., Tett P., et al. 1998. The transition zone of the Canary Current upwelling region. Prog. Oceanogr. 41: 455-504. https://doi.org/10.1016/S0079-6611(98)00023-8

Biscoito M., Freitas M., Pajuelo J.G., et al. 2015. Sex-structure, depth distribution, intermoult period and reproductive pattern of the deep-sea red crab Chaceon affinis (Brachyura, Geryonidae) in two populations in the north-eastern Atlantic. Deep-Sea Res. I 95: 99-114. https://doi.org/10.1016/j.dsr.2014.10.010

Brito A., Falcón J.M., Herrera R. 2005. Sobre la tropicalización reciente de la ictiofauna litoral de las islas Canarias y su relación con cambios ambientales y actividades antrópicas. Vieraea 33: 515-525.

Brito A., Clemente S., Herrera R. 2011. On the occurrence of the African hind, Cephalopholis taeniops, in the Canary Islands (eastern subtropical Atlantic): introduction of large-sized demersal littoral fishes in ballast water of oil platforms? Biol. Invasions 13: 2185-2189. https://doi.org/10.1007/s10530-011-0049-0

Brullé M. 1837-1839. Crustacés. In: Webb P.B., Berthelot S., Histoire naturelle des Iles Canaries, Zoologie, 2 (2: Entomologie): 13-18, 1 pl. (Crustacés) Atlas (1837); Text (1839). Paris.

Capart A. 1951. Crustacés Décapodes Brachyures. Expédition Océanographique Belge dans les Eaux Côtières Africaines de l'Atlantique Sud (1948-1949). Résultats Scientifiques 3: 11-205 + pl. 1-3.

Crandall K.A., Fitzpatrick J.F.J. 1996. Crayfish molecular systematics: using a combination of procedures to estimate phylogeny. Syst. Biol. 45: 1-26. https://doi.org/10.1093/sysbio/45.1.1

Cuesta J.A., Almón B., Pérez-Dieste J., et al. 2016. Role of ships' hull fouling and tropicalization process on European carcinofauna: new records in Galician waters (NW Spain). Biol. Invasions 18: 619-630. https://doi.org/10.1007/s10530-015-1034-9

Dauvin J.C., Tous Rius A., Ruellet T. 2009. Recent expansion of two invasive crabs species Hemigrapsus sanguineus (de Haan, 1835) and H. takanoi Asakura and Watanabe 2005 along the Opal Coast, France. Aquat. Invasions 4: 451-465. https://doi.org/10.3391/ai.2009.4.3.3

Davie P. 2015. Cronius tumidulus (Stimpson, 1871). Accessed through: World Register of Marine Species at http://www.marinespecies.org/aphia.php?p=taxdetails&id=422040 on 27/07/2016.

Dineen J.F., Clark P.F., Hines A.H., et al. 2001. Life history, larval description, and natural history of Charybdis hellerii (Decapoda, Brachyura, Portunidae), an invasive crab in the western Atlantic. J. Crustac. Biol. 21: 774-805. https://doi.org/10.1163/20021975-99990173

Estoup A., Largiadèr C.R., Perrot E., et al. 1996. Rapid one-tube DNA extraction for reliable PCR detection of fish polymorphic markers and transgenes. Mol. Mar. Biol. Biotech. 5: 295-298.

Fransen C.H.J.M. 1991. Preliminary report on Crustacea collected in the eastern part of the North Atlantic during the CANCAP and Mauritania expeditions of the former Rijksmuseum van Natuurlijke Historie, Leiden. Nationaal Naturhistorisch Museum, Leiden: i-vi + 1-200.

Fransen C.H.J.M. 2002. Taxonomy, phylogeny, historical biogeography, and historical ecology of the genus Pontonia Latreille (Crustacea: Decapoda: Caridea: Palaemonidae). Zool. Verh. Leiden 336: 1-433.

Fransen C.H.J.M. 2015. Cronius ruber (Lamarck, 1818). Accessed on 27/07/2016 through: World Register of Marine Species at http://www.marinespecies.org/aphia.php?p=taxdetails&id=241109

Friedlander A.M., Ballesteros E., Fay M., et al. 2014. Marine communities on oil platforms in Gabon, West Africa: high biodiversity oases in a low biodiversity environment. PLoS One 9: e103709. https://doi.org/10.1371/journal.pone.0103709 PMid:25083704 PMCid:PMC4118950

Galil B.S., Clark P.F., Carlton J.T. (eds) 2011. In the wrong place – Alien Marine Crustaceans: Distribution, Biology and Impact. Springer Series in Invasion Ecology 6.

González J.A. 1995. Catálogo de los Crustáceos Decápodos de las islas Canarias. Publicaciones Turquesa, Santa Cruz de Tenerife, 282 pp.

González J.A. 2016. Brachyuran crabs (Crustacea: Decapoda) from the Canary Islands (eastern Atlantic): checklist, zoogeographic considerations and conservation. Sci. Mar. 80: 89-102.

González J.A., Martín L., Herrera R., et al. 2012. Cirripedia of the Canary Islands: distribution and ecological notes. J. Mar. Biol. Assoc. U.K. 92: 129-141

Horta Costa B., Assis J., Franco G., et al. 2014. Tropicalization of fish assemblages in temperate biogeographic transition zones. Mar. Ecol. Prog. Ser. 504: 241-252. https://doi.org/10.3354/meps10749

Landeira J.M., Lozano-Soldevilla F., Hernández-León S., et al. 2009. Horizontal distribution of invertebrate larvae around the oceanic island of Gran Canaria: the effect of mesoscale variability. Sci. Mar. 73: 757-767. https://doi.org/10.3989/scimar.2009.73n4757

Le Loeuff P., Intès A. 1968. La faune benthique du plateau continental de Côte d'Ivoire, récoltes au chalut, abondance-répartition-variations saisonnières (Mars 1966-Février 1967). Centre de Recherches Océanographiques, Abidjan, Doc. Scient. Provisoire 25: 1-78.

Lockett M.M., Gomon M.F. 2001. Ship mediated fish invasions in Australia: two new introductions and a consideration of two previous invasions. Biol. Invasions 3: 187-192. https://doi.org/10.1023/A:1014584201815

Luiz O.J., Allen A.P., Robertson D.R., et al. 2015. Seafarers or castaways: ecological traits associated with rafting dispersal in tropical reef fishes. J. Biogeogr. 42: 2323-2333. https://doi.org/10.1111/jbi.12574

Manfrin C., Turolla E., Chung J.S., et al. 2015. First occurrence of Callinectes sapidus (Rathbun, 1896) within the Sacca di Goro (Italy) and surroundings. Check List 11: 1640. https://doi.org/10.15560/11.3.1640

Manning R.B., Holthuis L.B. 1981. West African Brachyuran Crabs (Crustacea: Decapoda). Smithson. Contr. Zool. 306: i-xii + 1-379.

Mantelatto F.L., Robles R., Schubart C.D., et al. 2009. Molecular phylogeny of the genus Cronius Stimpson 1860, with reassignment of C. tumidulus and several American species of Portunus to the genus Achelous de Haan, 1833 (Brachyura: Portunidae). In: Martin J.W., Crandall K.A., Felder D.L. (eds), Decapod Crustacean Phylogenetics. Crustac. Issues 18: 567-579.

Minchin D., Cook E., Clark P. 2013. Alien species in British brackish and marine waters. Aquat. Invasions 8: 3-19. https://doi.org/10.3391/ai.2013.8.1.02

Mittelstaedt E. 1983. The upwelling area off Northwest Africa–A description of phenomena related to coastal upwelling. Prog. Oceanogr. 12: 307-331. https://doi.org/10.1016/0079-6611(83)90012-5

Molnar J.L., Gamboa R.L., Revenga C., et al. 2008. Assessing the global threat of invasive species to marine biodiversity. Front. Ecol. Environ. 6: 485-492. https://doi.org/10.1890/070064

Monod T. 1956. Hippidea et Brachyura ouest-africains. Mém. I.F.A.N. 45: 1-674.

Moro L., Herrera R., Ortea J., et al. 2014. Aportaciones al conocimiento y distribución de los decápodos y estomatópodos (Crustacea: Malacostraca) de las islas Canarias. Rev. Acad. Canar. Cienc. 26: 33-82.

Ng P.K., Guinot D., Davie P.J. 2008. Systema brachyurorum: Part I. An annotated checklist of extant brachyuran crabs of the world. Raff. Bull. Zool. 17: 1-286.

Occhipinti-Ambrogi A. 2007. Global change and marine communities: Alien species and climate change. Mar. Pollut. Bull. 55: 342-352. https://doi.org/10.1016/j.marpolbul.2006.11.014 PMid:17239404

Pajuelo J.G., González J.A., Triay-Portella R., et al. 2016. Introduction of non-native marine fish species to the Canary Islands waters through oil platforms as vectors. J. Mar. Syst. 163: 23-30. https://doi.org/10.1016/j.jmarsys.2016.06.008

Perry A.L., Low P.J., Ellis J.R., et al. 2005. Climate change and distribution shifts in marine fishes. Science 308: 1912-1915. https://doi.org/10.1126/science.1111322 PMid:15890845

Rossignol M. 1957. Crustacés Décapodes marins de la région de Pointe-Noire. In: Collignon J., Rossignol M., Roux C., Mollusques, Crustacés, Poissons Marins des côtes d'A.E.F. en collection au Centre d'Océanographie de l'Institut d'Études Centrafricaines de Pointe-Noire. Paris: pp. 71-136.

Sant'Anna B.S., Watanabe T.T., Turra A., et al. 2012. First record of the non-indigenous portunid crab Charybdis variegata from the western Atlantic coast. BioInvasions Rec. 1: 11-16. https://doi.org/10.3391/bir.2012.1.1.03

Schubart C.D., Huber M.G.J. 2006. Genetic comparisons of German populations of the stone crayfish, Austropotamobius torrentium (Crustacea: Astacidae). Bull. Fr. Pêche Piscic. 380-381: 1019-1028. https://doi.org/10.1051/kmae:2006008

Schubart C.D., Reuschel S. 2009. A proposal for a new classification of Portunoidea and Cancroidea (Brachyura: Heterotremata) based on two independent molecular phylogenies. In: Martin J.W., Crandall K.A., Felder D.L. (eds), Decapod Crustacean Phylogenetics. Crustac. Issues 18: 533-549.

Schubart C.D., Cuesta J.A., Felder D.L. 2002. Glyptograpsidae, a new brachyuran family from Central America: larval and adult morphology, and a molecular phylogeny of the Grapsoidea. J. Crustac. Biol. 22: 28-44. https://doi.org/10.1163/20021975-99990206

Spalding M.D., Fox H.E., Allen G.R., et al. 2007. Marine ecoregions of the world: A bioregionalization of coastal and shelf areas. BioScience 57: 573-583. https://doi.org/10.1641/B570707

Spiridonov V.A., Neretina T.V., Schepetov D. 2014. Morphological characterization and molecular phylogeny of Portunoidea Rafinesque, 1815 (Crustacea Brachyura): Implications for understanding evolution of swimming capacity and revision of the family-level classification. Zool. Anz. 253: 404-429. https://doi.org/10.1016/j.jcz.2014.03.003

Streftaris N., Zenetos A., Papathanassiou E. 2005. Globalisation in marine ecosystems: the story of non-indigenous marine species across European seas. Oceanogr. Mar. Biol. 43: 419-453.

Tamura K., Stecher G., Peterson D., et al. 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol. Biol. Evol. 30: 2725-2729. https://doi.org/10.1093/molbev/mst197 PMid:24132122 PMCid:PMC3840312

Tavares M., Amouroux J.M. 2003. First record of the non-indigenous crab, Charybdis hellerii (A. Milne-Edwards, 1867) from French Guyana (Decapoda, Brachyura, Portunidae). Crustaceana 76: 625-630. https://doi.org/10.1163/156854003322316254

Tavares M., Mendonça Jr. J.B. 1996. Charybdis hellerii (A. Milne Edwards, 1867) (Brachyura: Portunidae), eighth non indigenous marine decapod recorded from Brazil. Crustac. Res. 25: 151-157.

Tavares M., Mendonça Jr. J.B. 2011. The occurrence of the Indo- Pacific swimming crab Scylla serrata (Forskål, 1775) in the Southwestern Atlantic (Crustacea: Brachyura: Portunidae). Aquat. Invasions 6: 49-51. https://doi.org/10.3391/ai.2011.6.S1.011

Triay-Portella R., González J.A., Santana J.I., et al. 2014. Reproductive pattern and egg development of the deep-sea crab Paromola cuvieri (Brachyura, Homolidae) around the Canary Islands (NE Atlantic). Deep-Sea Res. I 85: 1-14. https://doi.org/10.1016/j.dsr.2013.12.001

Triay-Portella R., Pajuelo J.G., Manent P., et al. 2015. New records of non-indigenous fishes (Perciformes and Tetraodontiformes) from the Canary Islands (eastern Atlantic). Cybium 39: 163-174.

Türkay M. 1976. Die Madeirensischen Brachyuren des Museu Municipal do Funchal und des Forschungs Instituts Senckenberg, I: Familien Dromidae, Homolidae, Calappidae, Leucosiidae, Cancridae, Portunidae, Xanthidae, Geryonidae, Goneplacidae und Palicidae (Crustacea: Decapoda). Bol. Mus. Mun. Funchal 30: 57-74.

Türkay M. 1987. On the Mediterranean and eastern Atlantic records of Portunus sayi (Crustacea: Decapoda: Portunidae). Inv. Pesq. 51 (Suppl. 1): 63-66.

Turney S., Cameron E.R., Cloutier C.A., et al. 2015. Non-repeatable science: assessing the frequency of voucher specimen deposition reveals that most arthropod research cannot be verified. PeerJ 3: e1168. https://doi.org/10.7717/peerj.1168 PMid:26339546 PMCid:PMC4558062

Vergés A., Steinberg P.D., Hay M.E., et al. 2014. The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts. Proc. R. Soc. B 281: 1-10. https://doi.org/10.1098/rspb.2014.0846 PMid:25009065 PMCid:PMC4100510

Wernberg T., Bennett S., Babcock R.C., et al. 2016. Climate-driven regime shift of a temperate marine ecosystem. Science 353: 169-172. https://doi.org/10.1126/science.aad8745 PMid:27387951

Wirtz P., Fricke R., Biscoito M.J. 2008. The coastal fishes of Madeira Island – new records and an annotated checklist. Zootaxa 1715: 1-26.

Wonham M.J., Carlton J.T., Ruiz G.M., et al. 2000. Fish and ships: relating dispersal frequency to success in biological invasions. Mar. Biol. 136: 1111-1121. https://doi.org/10.1007/s002270000303




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