Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-22T15:39:35.325Z Has data issue: false hasContentIssue false

Observations on the life history of a rare shrimp, Salmoneus carvachoi (Crustacea: Caridea: Alpheidae), a possible simultaneous hermaphrodite

Published online by Cambridge University Press:  29 September 2015

M.V. Oliveira
Affiliation:
Departamento de Ciências Biológicas, Universidade Estadual de Santa Cruz, Ilhéus, Bahia, Brazil
A.C. Costa-Souza
Affiliation:
Departamento de Ciências Biológicas, Universidade Estadual de Santa Cruz, Ilhéus, Bahia, Brazil Departamento de Zoologia, Universidade Federal de Pernambuco (UFPE), Centro de Ciências Biológicas, Recife, Pernambuco, Brazil
F.J. Guimarães
Affiliation:
Departamento de Ciências Biológicas, Universidade Estadual de Santa Cruz, Ilhéus, Bahia, Brazil
A.O. Almeida*
Affiliation:
Departamento de Ciências Biológicas, Universidade Estadual de Santa Cruz, Ilhéus, Bahia, Brazil Departamento de Zoologia, Universidade Federal de Pernambuco (UFPE), Centro de Ciências Biológicas, Recife, Pernambuco, Brazil
J.A. Baeza
Affiliation:
Department of Biological Sciences, Clemson University, Clemson, South Carolina, USA Smithsonian Marine Station at Fort Pierce, Fort Pierce, Florida, USA Departamento de Biología Marina, Facultad de Ciencias del Mar, Universidad Católica del Norte, Coquimbo, Chile
*
Correspondence should be addressed to: A.O. Almeida, Universidade Federal de Pernambuco (UFPE), Centro de Ciências Biológicas, Departamento de Zoologia, Avenida Prof. Moraes Rêgo, 1235, Cidade Universitária, 50670-901 Recife, Pernambuco, Brazil email: [email protected]
Get access

Abstract

This study reports on the life history of a rare alpheid shrimp, Salmoneus carvachoi, in the tropical western Atlantic. At an intertidal flat in Pontal Bay, Ilhéus, Bahia, north-eastern Brazil, S. carvachoi was collected from within burrows of the axianassid mud shrimp Axianassa australis and the caridean snapping shrimps Alpheus estuariensis and Alpheus chacei. These and earlier studies that reported S. carvachoi in dwellings constructed by other larger burrowing crustaceans suggest that S. carvachoi is a generalist species that establishes facultative symbiotic partnerships with larger burrowing decapods. We collected a total of 52 individuals during the sampling period (1 year); 19 (36.5%) of these shrimps carried embryos underneath the abdomen. The mean ± SD carapace length was 4.7 ± 0.7 and 5.5 ± 0.3 mm in non-brooding and brooding shrimps, respectively. All collected specimens, whether or not brooding embryos, bear appendices masculinae on the endopods of the second pleopods. Burrows harboured only one or two shrimps and never three or more shrimps. Pairs of shrimp that inhabited burrows consisted of two brooding shrimps (N = 3 pairs), two non-brooding shrimps (N = 3), or one brooding and one non-brooding shrimp (N = 1). The presence of appendices masculinae in all collected shrimps, whether or not brooding embryos, and the pairing of brooding shrimp within host burrows suggest that S. carvachoi is a simultaneously hermaphroditic species.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2015 

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.)

References

REFERENCES

Almeida, A.O., Boehs, G., Araújo-Silva, C.L. and Bezerra, L.E.A. (2012) Shallow-water caridean shrimps from southern Bahia, Brazil, including the first record of Synalpheus ul (Ríos & Duffy, 2007) (Alpheidae) in the southwestern Atlantic Ocean. Zootaxa 3347, 135.Google Scholar
Almeida, A.O., Coelho, P.A., Santos, J.T.A. and Ferraz, N.R. (2006) Crustáceos decápodos estuarinos de Ilhéus, Bahia, Brasil. Biota Neotropica 6, 1–24. Available at: www.biotaneotropica.org.br/v6n2/pt/abstract?inventory+bn03406022006 (accessed 31 July 2014).CrossRefGoogle Scholar
Almeida, A.O., Terossi, M., Araújo-Silva, C.L. and Mantelatto, F.L. (2013) Description of Alpheus buckupi spec. nov., a new amphi-Atlantic snapping shrimp (Caridea: Alpheidae), based on morphological and molecular data. Zootaxa 3652, 437452.Google Scholar
Anker, A. (2003) Alpheid shrimps from the mangroves and mudflats of Singapore. Part 1. genera Salmoneus, Athanas and Potamalpheops, with the description of two new species (Crustacea: Decapoda: Caridea). Raffles Bulletin of Zoology 51, 283314.Google Scholar
Anker, A. (2007) New species and records of alpheid shrimps, genera Salmoneus Holthuis and Parabetaeus Coutière, from the tropical western Atlantic (Decapoda, Caridea). Zootaxa 1653, 2139.Google Scholar
Anker, A. (2010) The shrimp genus Salmoneus Holthuis, 1955 (Crustacea, Decapoda, Alpheidae) in the tropical western Atlantic, with description of five new species. Zootaxa 2372, 177205.CrossRefGoogle Scholar
Anker, A. (2011a) Three new species of the alpheid shrimp genus Salmoneus Holthuis, 1955 (Crustacea, Decapoda) from the tropical Western Pacific. Zootaxa 2839, 6784.Google Scholar
Anker, A. (2011b) Two new species of Salmoneus Holthuis, 1955 with a deep dorsal depression on the carapace (Crustacea, Decapoda, Alpheidae). Zootaxa 3041, 3950.CrossRefGoogle Scholar
Anker, A. (2012) Revision of the western Atlantic members of the Alpheus armillatus H. Milne Edwards, 1837 species complex (Decapoda, Alpheidae), with description of seven new species. Zootaxa 3386, 1109.Google Scholar
Anker, A., Firdaus, M. and Pratama, I.S. (2014) Salmoneus yoyo nov. sp., a peculiar new infaunal shrimp from Lombok, Indonesia (Decapoda, Caridea, Alpheidae). Zootaxa 3852, 489495.Google Scholar
Anker, A. and Marin, I.N. (2006) New records and species of Alpheidae (Crustacea: Decapoda) from Vietnam. Part I. genus Salmoneus Holthuis, 1955. Raffles Bulletin of Zoology 54, 295319.Google Scholar
Anker, A., Pratama, I.S., Firdaus, M. and Rahayu, D. (2015) On some interesting marine decapod crustaceans (Alpheidae, Laomediidae, Strahlaxiidae) from Lombok, Indonesia. Zootaxa 3911, 301342.CrossRefGoogle ScholarPubMed
Baeza, J.A. (2008) Social monogamy in the shrimp Pontonia margarita, a symbiont of Pinctada mazatlanica of the Pacific coast of Panama. Marine Biology 153, 387395.Google Scholar
Baeza, J.A. (2009) Protandric simultaneous hermaphroditism is a conserved trait in Lysmata (Caridea: Lysmatidae): implications for the evolution of hermaphroditism in the genus. Smithsonian Contributions to the Marine Sciences 38, 95110.Google Scholar
Baeza, J.A. (2015) Crustaceans as symbionts: an overview of their diversity, host use and life styles. In Watling, L. and Thiel, M. (eds) The life styles and feeding biology of the crustacea. Oxford: Oxford University Press, pp. 163189.Google Scholar
Baeza, J.A., Farías, N.E., Luppi, T.A. and Spivak, E.D. (2010). Habitat size, social grouping and symbiosis: testing the ‘resource economic monopolization’ hypothesis with the shrimp Betaeus lilianae and description of its partnership with the crab Platyxanthus crenulatus. Journal of Experimental Marine Biology and Ecology 389, 8592.Google Scholar
Baeza, J.A., Hemphill, C.A. and Ritson-Williams, R. (2015) The sexual and mating system of the shrimp Odontonia katoi (Palaemonidae, Pontoniinae), a symbiotic guest of the ascidian Polycarpa aurata in the Coral Triangle. PLoS ONE 10, e0121120, doi: 10.1371/journal.pone.0121120.Google Scholar
Baeza, J.A. and Thiel, M. (2007) The mating system of symbiotic crustaceans. A conceptual model based on optimality and ecological constraints. In Duffy, J.E. and Thiel, M. (eds) Reproductive and social behavior: crustaceans as model systems. Oxford: Oxford University Press, pp. 245255.Google Scholar
Barnard, K.H. (1962) New records of marine Crustacea from the East African region. Crustaceana 3, 239245.Google Scholar
Bauer, R.T. (2000) Simultaneous hermaphroditism in caridean shrimps: a unique and puzzling sexual system in the Decapoda. Journal of Crustacean Biology 20, 118128.Google Scholar
Bauer, R.T. (2004) Remarkable Shrimps: Adaptations and Natural History of the Carideans. Norman, OK: University of Oklahoma Press.Google Scholar
Borradaile, L.A. (1900) On the stomatopoda and macrura brought by Dr Willey from the South Seas. In Willey, A. (ed.) Zoological results based on material from New Britain, New Guinea, Loyalty Islands and elsewhere, collected during the years 1895, 1896, and 1897, by Arthur Willey, D.Sc. Lond., Hon. M.A. Cantab. Cambridge: Cambridge University Press, pp. 395428, pls. 36–39.Google Scholar
Braga, A.A., López-Greco, L.S., Santos, D.C. and Fransozo, A. (2009) Morphological evidence for protandric simultaneous hermaphroditism in the caridean Exhippolysmata oplophoroides. Journal of Crustacean Biology 29, 3441.CrossRefGoogle Scholar
Carvacho, A. (1979) Les crevettes carides de la mangrove guadeloupéenne. Bulletin du Muséum national d'Histoire naturelle (4), section A, Zoologie, Biologie et Écologie animales 1, 445470.Google Scholar
Carvacho, A. (1989) Sur l'appendix masculina chez Salmoneus (Decapoda, Alpheidae). Crustaceana 57, 253256.CrossRefGoogle Scholar
Christoffersen, M.L. (1982) Geographic distribution of warm water alpheoid shrimp (Crustacea, Caridea) on the continental shelf of eastern South America between 23 and 35° Lat. S. Boletim do Instituto Oceanográfico 31, 93112.Google Scholar
Christoffersen, M.L. (1984) The western Atlantic snapping shrimps related to Alpheus heterochaelis Say (Crustacea, Caridea), with the description of a new species. Papéis Avulsos de Zoologia 35, 189208.Google Scholar
Costa-Souza, A.C., Rocha, S.S., Bezerra, L.E.A. and Almeida, A.O. (2014) Breeding and heterosexual pairing in the snapping shrimp Alpheus estuariensis (Caridea: Alpheidae) in a tropical bay in northeastern Brazil. Journal of Crustacean Biology 34, 593603.Google Scholar
De Grave, S. and Fransen, C.H.J.M. (2011) Carideorum catalogus: the recent species of the dendrobrachiate, stenopodidean, procarididean and caridean shrimps (Crustacea: Decapoda). Zoologische Mededelingen 85, 195588.Google Scholar
De Grave, S., Pentcheff, N.D., Ahyong, S.T., Chan, T.Y., Crandall, K.A., Dworschak, P.C., Felder, D.L., Feldmann, R.M., Fransen, C.H.J.M., Goulding, L.Y.D., Lemaitre, R., Low, M.E.Y., Martin, J.W., Ng, P.K.L., Schweitzer, C.E., Tan, S.H., Tshudy, D. and Wetzer, R. (2009) A classification of living and fossil genera of decapod crustaceans. Raffles Bulletin of Zoology Suppl. 21, 1109.Google Scholar
de Man, J.G. (1908) Diagnoses of new species of macrurous decapod Crustacea from the ‘Siboga-Expedition’. Notes from the Leyden Museum 30, 98112.Google Scholar
Diesel, R. (1988) Discrete storage of multiple-mating sperm in the spider crab Inachus phalangium. Naturwissenschaften 75, 148149.Google Scholar
Duffy, J.E. (1996a) Synalpheus regalis, new species, a sponge-dwelling shrimp from the Belize Barrier Reef, with comments on host specificity in Synalpheus. Journal of Crustacean Biology 16, 564573.Google Scholar
Duffy, J.E. (1996b) Eusociality in a coral-reef shrimp. Nature 381, 512514.CrossRefGoogle Scholar
Dworschak, P.C., Anker, A. and Abed-Navandi, D. (2000) A new genus and three new species of alpheids (Decapoda: Caridea) associated with thalassinids. Annalen des Naturhistorisches Museum in Wien 102b, 301320.Google Scholar
Fabricius, J.C. (1775) Systema Entomologiae, sistens Insectorum classes, ordines, genera, species, adiectis synonymis, locis, descriptionibus, observationibus, i–xxx, 1–832. Flensbergi et Lipsiae.Google Scholar
Fabricius, J.C. (1798) Supplementum Entomologiae Systematicae, 1572. Hafniae: Proft et Storch.CrossRefGoogle Scholar
Folk, R.L. and Ward, W.C. (1957) Brazos River bar, a study in the significance of grain size parameters. Journal Sedimentary Petrology 27, 326.Google Scholar
Fransen, C.H.J.M. (1991) Salmoneus sketi, a new species of alpheid shrimp (Crustacea: Decapoda: Caridea) from a submarine cave in the Adriatic. Zoologische Mededelingen 65, 171179.Google Scholar
Gibbes, L.R. (1850) On the carcinological collections of the United States, and an enumeration of species contained in them, with notes on the most remarkable, and descriptions of new species. Proceedings of the American Association for the Advancement of Science 3, 165201.Google Scholar
Holthuis, L.B. (1955) The recent genera of the caridean and stenopodidean shrimps (Class Crustacea, order Decapoda, supersection Natantia) with keys for their determination. Zoologische Verhandelingen 26, 1157.Google Scholar
Holthuis, L.B. (1990) Notes on Salmoneus arubae (Schmitt, 1936) (Crustacea, Decapoda, Caridea). Beaufortia 41, 109113.Google Scholar
Knowlton, N. (1980) Sexual selection and dimorphism in two demes of a symbiotic, pair-bonding snapping shrimp. Evolution 34, 161173.Google Scholar
Komai, T. (2009) A new species of the alpheid shrimp genus Salmoneus (Decapoda, Caridea) from the Ryukyu Islands, Japan, associated with a callianassid ghost shrimp (Decapoda, Thalassinidea). Crustaceana 82, 869880.Google Scholar
Komai, T. and Anker, A. (2012) A distinctive new species of the alpheid genus Salmoneus Holthuis, 1955 (Crustacea: Decapoda: Caridea) from the northwestern Pacific. Zootaxa 3344, 6068.Google Scholar
Leach, W.E. (1813–1814) Crustaceology. In Brewster, D. (ed.) The Edinburgh encyclopaedia. Edinburgh: A. Balfour, pp. 383437.Google Scholar
Marin, I.N. and Mapnh, N.H. (2014) An unusual habitat for hermit crab-associated alpheid shrimp Aretopsis amabilis De Man, 1910 (Crustacea: Decapoda: Alpheidae): a possible evidence of socially monogamous species? Arthropoda Selecta 23, 265268.Google Scholar
Mathews, L. (2002a) Territorial cooperation and social monogamy: factors affecting intersexual behaviours in pair-living snapping shrimp. Animal Behaviour 66, 767777.Google Scholar
Mathews, L. (2002b) Tests of the mate-guarding hypothesis for social monogamy: does population density, sex ratio, or female synchrony affect behavior of male snapping shrimp (Alpheus angulatus)? Behavioural Ecology and Sociobiology 51, 426432.Google Scholar
Milne-Edwards, A. (1870) Revision du genre Callianassa (Leach) et description de plusieurs espèces nouvelles de ce groupe fausant parte de la collection du muséum. Nouvelle Archives du Muséum d'Histoire Naturelle, Paris 6, 75102.Google Scholar
Miya, Y. and Miyake, S. (1969) Description of Alpheus bellulus sp. nov. associated with gobies from Japan (Crustacea, Decapoda, Alpheidae). Publications from the Seto Marine Biological Laboratory 16, 307314.Google Scholar
Mossolin, E.C., Shimizu, R.M. and Bueno, S.L.S. (2006) Population structure of Alpheus armillatus (Decapoda, Alpheidae) in São Sebastião and Ilhabela, southeastern Brazil. Journal of Crustacean Biology 26, 4854.Google Scholar
Nacif, P., Costa, L., Soadi, A., Fernandes-Filho, E., Ker, J., Costa, O. and Moreau, M. (2003) Ambientes Naturais da Bacia Hidrográfica do Rio Cachoeira. Available at: www.corredores.org.br/?pageId=adminOpenDoc&docId=1664 (accessed 31 July 2014).Google Scholar
Onaga, H., Fiedler, G.C. and Baeza, J.A. (2012) Protandric simultaneous hermaphroditism in Parhippolyte misticia (Clark, 1989) (Caridea: Hippolytidae): implications for the evolution of mixed sexual systems in shrimp. Journal of Crustacean Biology 32, 383394.Google Scholar
Pennant, T. (1777) British zoology, Volume IV. Crustacea. Mollusca. Testacea, i–viii, 1–154, pls. 1–93. London: Benj. White.Google Scholar
Petagna, V. (1792) Institutiones entomologicae, i–xii, 1–718, pls. 1–10. Neapoli: Typis Cajetani Raymundi.Google Scholar
Placklett, R.L. (1953) The truncated Poisson distribution. Biometrics 9, 485488.CrossRefGoogle Scholar
Rahman, N., Dunham, D.W. and Govind, C. (2003) Social monogamy in the big-clawed snapping shrimp, Alpheus heterochaelis. Ethology 109, 457473.Google Scholar
Ramos-Porto, M., Viana, G.F.S. and Lacerda, P.R. (1994) Ocorrência de Salmoneus ortmanni (Rankin, 1898) no Nordeste brasileiro. Revista Nordestina de Zoologia 1, 4460.Google Scholar
Rankin, W.M. (1898) The Northrop collection of Crustacea from the Bahamas. Annals of the New York Academy of Sciences 11, 225258.CrossRefGoogle Scholar
Rathbun, M.J. (1901) Investigations of the aquatic resources and fisheries of Porto Rico by the United States Fish Commission Steamer Fish Hawk in 1899. The Brachyura and Macrura of Porto Rico. Bulletin of the United States Fish Commission 20 [for 1900, preprint dated 1901, published in journal in 1902], 1127, pls. 1–2.Google Scholar
Rasband, W.S. (2006) ImageJ: image processing and analysis in Java. Bethesda, MD: National Institutes of Health, Research Services Branch Bethesda, MD.Google Scholar
Risso, A. (1816) Histoire naturelle des crustacés des environs de Nice. Paris: Librairie Grecque-Latine-Allemande, pp. 1175, pls. 1–3.CrossRefGoogle Scholar
Rodrigues, S.A. and Shimizu, R.M. (1992) Description of a new Axianassa (Crustacea: Decapoda: Thalassinidea) from Brazil, and its first larval stage. Proceedings of the Biological Society of Washington 105, 317323.Google Scholar
Sokal, R.R. and Rohlf, F.J. (1995) Biometry: the principles and practice of statistics in biological research, 3rd ed.New York, NY: Freeman.Google Scholar
Souza, M.F.L., Eça, G.F., Silva, M.A.M., Amorim, F.A.C. and Lôbo, I.P. (2009) Distribuição de nutrientes dissolvidos e clorofila-a no estuário do Rio Cachoeira, nordeste do Brasil. Atlântica 31, 107121.Google Scholar
Spence Bate, C. (1888) Report on the Crustacea Macrura collected by the Challenger during the years 1873–76. Report on the Scientific Results of the Voyage of H.M.S. ‘Challenger’ During the Years 1873–1876, Zoology 24, i–xc, 1–942, pls. 1–57.Google Scholar
Stebbing, T.R.R. (1915) South African Crustacea. Part VIII of S.A. Crustacea, for the marine investigations in South Africa. Annals of the South African Museum 15, 57103, pls. 13–25.Google Scholar
Stimpson, W. (1860) Prodromus descriptionis animalium evertebratorum, quae in Expeditione ad Oceanum Pacificum Septentrionalem, a Republic Federata missa, Cadwaladore Ringgold et Johanne Rodgers Ducibus, observavit et descripsit. Pars VIII, Crustacea Macrura. Proceedings of the Academy of Natural Sciences of Philadelphia 1860, 2247.Google Scholar
Suguio, K. (1973) Introdução à sedimentologia. São Paulo: Edgard Blücher/EDUSP.Google Scholar
Tóth, E. and Bauer, R.T. (2007) Gonopore sexing technique allows determination of sex ratios and helper composition in eusocial shrimps. Marine Biology 151, 18751886.Google Scholar
Verrill, A.E. (1869) On the parasitic habits of Crustacea. American Naturalist 3, 239250.Google Scholar
Versluis, M., Schmitz, B., Von der Heydt, A. and Lohse, D. (2000) How snapping shrimp snap: through cavitating bubbles. Science 289, 21142117.Google Scholar
von Martens, E. (1868) Über eine neue Art und Untergattung der Cyprinoiden, Homaloptera (Octonema) rotundicauda, über einige neue Crustaceen und über die neuholländischen Süsswasserkrebse. Monatsberichte der Königlichen Akademie der Wissenschaften zu Berlin, Physikalisch-mathematische Klasse 1868, 607619.Google Scholar