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Reproductive biology and population structure of Axianassa australis (Crustacea, Axianassidae) on a sand-mud flat in north-eastern Brazil

Published online by Cambridge University Press:  16 January 2015

M.L. Botter-Carvalho Open the ORCID record for M.L. Botter-Carvalho [Opens in a new window] ,
L.B. Costa ,
L.L. Gomes ,
C.C.C. Clemente  and
P.V.V. Da C. Carvalho
M.L. Botter-Carvalho*
Affiliation:
Universidade Federal Rural de Pernambuco, Av. Dom Manoel de Medeiros s/n, Dois Irmãos, Recife-PE, Brazil
L.B. Costa
Affiliation:
Universidade Federal Rural de Pernambuco, Av. Dom Manoel de Medeiros s/n, Dois Irmãos, Recife-PE, Brazil
L.L. Gomes
Affiliation:
Universidade Federal Rural de Pernambuco, Av. Dom Manoel de Medeiros s/n, Dois Irmãos, Recife-PE, Brazil
C.C.C. Clemente
Affiliation:
Universidade Federal Rural de Pernambuco, Av. Dom Manoel de Medeiros s/n, Dois Irmãos, Recife-PE, Brazil
P.V.V. Da C. Carvalho
Affiliation:
Petrobras Transporte S/A, Rua Antônio Lumack Monte, 96, 4° andar, 51020-905, Recife-PE, Brazil
*
Correspondence should be addressed to: M.L. Botter-Carvalho, Universidade Federal Rural de Pernambuco, Av. Dom Manoel de Medeiros s/n, Dois Irmãos, Recife-PE, Brazil email: [email protected]
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Abstract

The life history of the mud shrimp Axianassa australis, a common and widespread burrower inhabiting coastal mangroves and mud flats, is poorly known. This contribution presents the first information about the population structure, reproductive biology and fecundity of A. australis, based on individuals collected from September 2011 to December 2012 on Casa Caiada Beach, located in a densely urbanized area in north-eastern Brazil, using a yabby pump. The sex ratio did not depart significantly from the expected 1:1 proportion. A significant trend of left-handedness of the major cheliped was observed in the population. Females reached a larger maximum cephalothorax length (CL) than males. The differential growth between CL and the propodus of the major cheliped showed negative allometric growth for females and positive allometric growth for males, suggesting a trade-off between somatic growth and reproductive effort. Females bearing uneyed orange embryos predominated during all months in which ovigerous females were collected. Mean fecundity was 2379 eggs, ranging from 5 (7.55 mm CL) to 8300 (14.19 mm CL) eggs per female. About 71% of the variation in the number of eggs carried per female was explained by CL. The mean egg size correlated negatively with fecundity, indicating that large females of A. australis produce more and larger eggs than smaller females.

Keywords

Gebiideaburrowing shrimprelative growthfecundityreproductionpopulation structuresex ratiohandednesstropical
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 95 , Issue 4 , June 2015 , pp. 735 - 745
Copyright
Copyright © Marine Biological Association of the United Kingdom 2015 

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References

REFERENCES

Alunno-Bruscia, M.B. and Sainte-Marie, B. (1998) Abdomen allometry, ovary development and growth of female snow crab, Chionoecetes opilio (Brachyura, Majidae), in the northwestern Gulf of St. Lawrence. Canadian Journal of Fisheries and Aquatic Sciences 55, 459–477.CrossRefGoogle Scholar
Anker, A. (2010) The mud-shrimp genus Axianassa Schmitt, 1924 (Crustacea, Decapoda, Axianassidae) in the Indo-West Pacific, with description of a new species from French Polynesia. Zootaxa 2557, 49–59.Google Scholar
Berkenbusch, K. and Rowden, A.A. (1998) Population dynamics of the burrowing ghost shrimp Callianassa filholi on an intertidal sand flat in New Zealand. Ophelia 49, 55–69.Google Scholar
Berkenbusch, K. and Rowden, A.A. (2000) Latitudinal variation in the reproductive biology of the burrowing ghost shrimp Callianassa filholi (Decapoda: Thalassinidea). Marine Biology 136, 497–504.CrossRefGoogle Scholar
Biffar, T. (1971) The genus Callianassa (Crustacea, Decapoda, Thalassinidea) in South Florida, with keys to the western Atlantic species. Bulletin of Marine Science 21, 637–715.Google Scholar
Botter-Carvalho, M.L., Santos, P.J.P. and Carvalho, P.V.V.C. (2007) Population dynamics of Callichirus major (Say, 1818) (Crustacea, Thalassinidea) on a beach in northeastern Brazil. Estuarine, Coastal and Shelf Science 71, 508–516.CrossRefGoogle Scholar
Buchanan, J.B. (1963) The biology of Calocaris macandreae (Crustacea, Thalassinidea). Journal of the Marine Biological Association of the United Kingdom 43, 729–747.CrossRefGoogle Scholar
Butler, S.N., Reid, M. and Bird, F.L. (2009) Population biology of the ghost shrimps, Trypaea australiensis and Biffarius arenosus (Decapoda: Thalassinidea), in Western Port, Victoria. Memoirs of Museum Victoria 6, 43–59.CrossRefGoogle Scholar
Clarke, A. (1993) Reproductive trade-offs in caridean shrimps. Functional Ecology 7, 411–419.CrossRefGoogle Scholar
Clarke, A. and Gore, D.J. (1992) Egg size and composition in Ceratoserolis (Crustacea: Isopoda) from the Weddell Sea. Polar Biology 12, 129–134.CrossRefGoogle Scholar
Clarke, A., Hopkins, C.C.E. and Nilssen, E.M. (1991) Egg size and reproductive output in the deep-water prawn Pandalus borealis Kroyer, 1838. Functional Ecology 5, 724–730.Google Scholar
Coelho, P.A., Almeida, A.O., Bezerra, L.E.A. and Souza-Filho, J.F. (2007) An updated checklist of decapod crustaceans (infraorders Astacidea, Thalassinidea, Polychelida, Palinura, and Anomura) from the northern and northeastern Brazilian coast. Zootaxa 1519, 1–16.CrossRefGoogle Scholar
Coelho, V.R. and Rodrigues, S.A. (2001) Trophic behaviour and functional morphology of the feeding appendages of the laomediid shrimp Axianassa australis (Crustacea: Decapoda: Thalassinidea). Journal of the Marine Biological Association of the United Kingdom 81, 441–445.Google Scholar
Corsetti, J.L. and Strasser, K.M. (2003) Population biology of the ghost shrimp Sergio trilobata (Biffar 1970) (Crustacea: Decapoda: Thalassinidea). Gulf and Caribbean Research 15, 13–19.CrossRefGoogle Scholar
de Vaugelas, J. (1986) Aspects of the biology of Callichirus armatus (A. Milne Edwards, 1870) (Decapoda, Thalassinidea) from French Polynesia. Crustaceana 50, 204–216.CrossRefGoogle Scholar
Dumbauld, B.R., Armstrong, D.A. and Feldman, K.L. (1996) Life-history characteristics of two sympatric Thalassinidean shrimps, Neotypaea californiensis and Upogebia pugettensis, with implications for oyster culture. Journal of Crustacean Biology 16, 689–708.CrossRefGoogle Scholar
Dworschak, P.C. (1988) The biology of Upogebia pusilla (Petagna) (Decapoda, Thalassinidea). 3. Growth and production. Marine Ecology – Pubblicazioni della Stazione Zoologica di Napoli I 9, 51–77.Google Scholar
Dworschak, P.C. (1998) Observations on the biology of Callianassa tyrrhena and C. candida (Crustacea, Thalassinidea). Journal of Natural History 32, 1535–1548.Google Scholar
Dworschak, P.C. (2012) On the identities of Callianassa bouvieri Nobili, 1904, C. maldivensis Borradaile, 1904, and C. gravieri Nobili, 1905 (Crustacea: Decapoda: Callianassidae): a morphometric approach. Zootaxa 49, 39–56.CrossRefGoogle Scholar
Dworschak, P.C. and Coelho, V.R. (1999) On two alpheids from Araça (Sao Paulo, Brazil) with a description of a new species of Leptalpheus (Decapoda: Caridea: Alpheidae). Annalen des Naturhistorischen Museums in Wien, Series B, 101, 475–488.Google Scholar
Dworschak, P.C., Felder, D.L. and Tudge, C.C. (2012) Infraorders Axiidea de Saint Laurent, 1979 and Gebiidea de Saint Laurent, 1979 (formerly known collectively as Thalassinidea). In Schram, F.R., Vaupel Klein, J.C., von Forest, J. and Charmantier-Daures, M. (eds) Treatise on zoology – anatomy, taxonomy, biology. The Crustacea. Complementary to the volumes translated from the French of the Traité de Zoologie [founded by P.-P. Grassé], v. 9, Part B. Leiden: Brill, pp. 109–219.Google Scholar
Dworschak, P.C. and Pervesler, P. (1988) Burrows of Callianassa bouvieri Nobili 1904 from Safaga (Egypt, Red Sea) with some remarks on the biology of the species. Senckenbergiana Maritima 20, 1–17.Google Scholar
Dworschak, P.C. and Rodrigues, S.A. (1997) A modern analogue for the trace fossil Gyrolithes: burrows of the thalassinidean shrimp Axianassa australis . Lethaia 30, 41–52.CrossRefGoogle Scholar
Felder, D.L. (2001) Diversity and ecological significance of deep-burrowing macrocrustaceans in coastal tropical waters of the Americas (Decapoda: Thalassinidea). Interciencia 26, 440–449.Google Scholar
Felder, D.L., Dworschak, P.C., Robles, R., Bracken, H.D., Windsor, A.M., Felder, J.M. and Lemaitre, R. (2009) Obvious invaders and overlooked infauna: unexpected constituents and new discoveries of the decapod crustacean assemblage at Twin Cays, Belize. Smithsonian Contributions to the Marine Sciences 38, 181–188.Google Scholar
Felder, D.L. and Lovett, D.L. (1989) Relative growth and sexual maturation in the estuarine ghost shrimp Callianassa louisianensis Schmitt, 1935. Journal of Crustacean Biology 9, 540–553.Google Scholar
Felder, D.L., Nates, S.F. and Robles, R.R. (2003) Hurricane Mitch: impacts of bioturbating crustaceans in shrimp ponds and adjacent estuaries of coastal Nicaragua. United States Geological Survey Open File Report 03–179, 1–70.Google Scholar
Forbes, A.T. (1977) Breeding and growth of the burrowing prawn Callianassa kraussi Stebbing (Crustacea: Decapoda: Thalassinidea). Zoologica Africana 12, 149–161.Google Scholar
Girard, T.C. (2009) Dinâmica populacional de Lepidophthalmus siriboia Felder and Rodrigues, 1993 (Decapoda: Callianassidae) da ilha de Maiandeua – PA . MSc dissertation. Universidade Federal do Pará, Belém, Brazil.Google Scholar
Griffis, R.B. and Suchanek, T.H. (1991) A model of burrow architecture and trophic modes in thalassinidean shrimp (Decapoda: Thalassinidea). Marine Ecology Progress Series 79, 171–183.CrossRefGoogle Scholar
Hailstone, T.S. and Stephenson, W. (1961) The biology of Callianassa (Trypaea) australiensis Dana, 1852 (Crustacea, Thalassinidea). University of Queensland, Department of Zoology, Papers 1, 259–285.Google Scholar
Hanekom, N. and Baird, D. (1992) Growth, production and consumption of the thalassinid prawn Upogebia africana (Ortmann) in the Swartkops estuary. South African Journal of Zoology 27, 130–139.CrossRefGoogle Scholar
Hanekom, N. and Erasmus, T. (1989) Determination of the reproductive output of populations of a thalassinid prawn Upogebia africana (Ortmann) in the Swartkops Estuary. South African Journal of Zoology 24, 244–250.CrossRefGoogle Scholar
Hartnoll, R.G. (1978) The determination of relative growth in Crustacea. Crustaceana 34, 281–293.Google Scholar
Hartnoll, R.G. (1982) Growth. In Abele, L.G. (ed) The biology of Crustacea 2. London: Academic Press, pp. 111–196.Google Scholar
Hernáez, P. and Wehrtmann, I.S. (2007) Population of the burrowing shrimp Callichirus seilacheri (Decapoda: Callianassidae) in northern Chile. Revista de Biología Tropical 55, 141–152.Google Scholar
Hill, B.J. (1977) The effect of heated effluent on egg production in the estuarine prawn Upogebia africana (Ortmann). Journal of Experimental Marine Biology and Ecology 29, 291–302.CrossRefGoogle Scholar
Huxley, J.S. (1950) Relative growth and form transformation. Proceedings of the Zoological Society of London 137, 465–469.Google ScholarPubMed
Kensley, B. and Heard, R. (1990) The genus Axianassa (Crustacea: Decapoda: Thalassinidea) in the Americas. Proceedings of the Biological Society of Washington 103, 558–572.Google Scholar
Kevrekidis, T., Gouvis, N. and Koukouras, A. (1997) Population dynamics, reproduction and growth of Upogebia pusilla (Decapoda, Thalassinidea) in the Evros Delta (north Aegean Sea). Crustaceana 70, 799–812.Google Scholar
Kubo, K., Shimoda, K. and Tamaki, A. (2006) Egg size and clutch size in three species of Nihonotrypaea (Decapoda: Thalassinidea: Callianassidae) from western Kyushu, Japan. Journal of the Marine Biological Association of the United Kingdom 86, 103–111.Google Scholar
Labadie, L.V. and Palmer, A.R. (1996) Pronounced heterochely in the ghost shrimp, Neotrypaea californiensis (Decapoda: Thalassinidea: Callianassidae): allometry, inferred function and development. Journal of Zoology 240, 659–675.Google Scholar
Lemaitre, R. and Rodrigues, S.A. (1991) Lepidophthalmus sinuensis: a new species of ghost shrimp (Decapoda: Thalassinidea: Callianassidae) of importance to the commercial culture of penaeid shrimps on the Caribbean Coast of Colombia, with observations on its ecology. Fisheries Bulletin 89, 623–630.Google Scholar
Lovett, D.L. and Felder, D.L. (1989) Application of regression techniques to studies of relative growth in crustaceans. Journal of Crustacean Biology 9, 529–539.Google Scholar
Mariappan, P., Balasundaram, C. and Schmitz, B. (2000) Decapod crustacean chelipeds: an overview. Journal of Biosciences 25, 301–313.Google Scholar
Marshall, D.J. and Keough, M.J. (2008) The evolutionary ecology of offspring size in marine invertebrates. Advances in Marine Biology 53, 1–60.Google Scholar
Mauchline, J. (1988) Egg and brood sizes of oceanic pelagic crustaceans. Marine Ecology Progress Series 43, 251–258.Google Scholar
Melo, G.A.S. (1999) Manual de identificação dos Crustacea Decapoda do litoral brasileiro: Anomura, Thalassinidea, Palinuridea, Astacidea. São Paulo: Editora Plêiade/FAPESP.Google Scholar
Melo, S.G., Loyola e Silva, J. and Masunari, S. (2006) First report of Axianassa australis Rodrigues & Shimizu (Crustacea: Decapoda: Thalassinidea) along the coast of the state of Paraná, Brazil. Acta Biológica Paranaense 35, 83–88.Google Scholar
Moran, A.L. and McAlister, J.S. (2009) Egg size as a life history character of marine invertebrates: Is it all it's cracked up to be? Biological Bulletin 216, 226–242.CrossRefGoogle ScholarPubMed
Nates, S.F. and Felder, D.L. (1998) Impacts of burrowing ghost shrimp, genus Lepidophthalmus Crustacea: Decapoda: Thalassinidea, on Penaeid shrimp culture. Journal of the World Aquaculture Society 29, 188–210.Google Scholar
Nates, S.F. and Felder, D.L. (1999) Growth and maturation of the ghost shrimp Lepidophthalmus sinuensis Lemaitre and Rodrigues, 1991 (Crustacea, Decapoda, Callianassidae), a burrowing pest in penaeid shrimp culture ponds. Fisheries Bulletin 97, 562–541.Google Scholar
Parker, G.A. and Begon, M.B. (1986) Optimal egg size and clutch size: effects of environment and maternal phenotype. American Naturalist 128, 573–592.Google Scholar
Pereira, L.C.C., Jimenez, J.A., Medeiros, C. and da Costa, R.M. (2003) The influence of the environmental status of Casa Caiada and Rio Doce beaches (NE-Brazil) on beaches users. Ocean and Coastal Management 46, 1011–1030.CrossRefGoogle Scholar
Pereira, L.C.C., Jimenez, J.A., Medeiros, C. and da Costa, R.M. (2006) Topographic changes in two highly sheltered beaches, Casa Caiada and Rio Doce, PE (Brazil). Journal of Coastal Research SI 39 (Proceedings of the 8th International Coastal Symposium), 644–647.Google Scholar
Pezzuto, P.R. (1993) Ecologia Populacional de Neocallichirus mirim (Rodrigues, 1971) (Decapoda: Callianassidae) na praia do Cassino, RS, Brasil . MSc dissertation. Universidade Federal do Rio Grande, Rio Grande, Brazil.Google Scholar
Pezzuto, P.R. (1998) Population dynamics of Sergio mirim (Rodrigues 1971) (Decapoda: Thalassinidea: Callianassidae) in Cassino Beach, southern Brazil. Marine Ecology – Pubblicazioni della Stazione Zoologica di Napoli I 19, 89–109.Google Scholar
Pillay, D. and Branch, G.M. (2011) Bioengineering effects of burrowing thalassinidean prawns on marine soft-bottom ecosystems. Oceanography and Marine Biology: An Annual Review 49, 1137–1192.Google Scholar
Pinheiro, M. and Fransozo, A. (1993) Relative growth of the speckled swimming crab Arenaeus cribrarius (Lamarck, 1818) (Brachyura: Portunidae), near Ubatuba, State of São Paulo, Brazil. Crustaceana 65, 377–389.CrossRefGoogle Scholar
Pohl, M.E. (1946) Ecological observations on Callianassa major Say at Beaufort, North Carolina. Ecology 1, 71–80.Google Scholar
Posey, M., Dumbauld, B. and Armstrong, D. (1991) Effects of a burrowing mud-shrimp, Upogebia pugettensis (Dana), on abundances of macroinfauna. Journal of Experimental Marine Biology and Ecology 148, 283–294.CrossRefGoogle Scholar
Robles, R., Tudge, C.C., Dworschak, P.C., Poore, G.C.B. and Felder, D.L. (2009) Molecular phylogeny of the Thalassinidea based on nuclear and mitochondrial genes. In Martin, J.W., Crandall, K.A. and Felder, D.L. (eds) Crustacean Issues 18: Decapod crustacean phylogenetics. Boca Raton, FL: Taylor and Francis/ CRC Press, pp. 309–326.CrossRefGoogle Scholar
Rodrigues, S. de A. (1976) Sobre a reprodução, embriologia e desenvolvimento larval de Callichirus major Say, 1818 (Crustacea, Decapoda, Thalassinidea). Boletim de Zoologia da Universidade de São Paulo 1, 85–104.Google Scholar
Rodrigues, S. de 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, 317–323.Google Scholar
Rosa, L.C. and Almeida, A.O. (2012) Axianassa australis Rodrigues and Shimizu, 1992 (Crustacea: Decapoda: Gebiidea: Axianassidae): First record from Sergipe, NE Brazil. Check List 8, 1321–1322.CrossRefGoogle Scholar
Rotherham, D. and West, R.J. (2009) Patterns in reproductive dynamics of burrowing ghost shrimp Trypaea australiensis from small to intermediate scales. Marine Biology 156, 1277–1287.Google Scholar
Rowden, A.A. and Jones, M.B. (1994) A contribution to the biology of the burrowing mud shrimp, Callianassa subterranea (Decapoda: Thalassinidea). Journal of the Marine Biological Association of the United Kingdom 74, 623–635.Google Scholar
Sakai, K. 2006. Upogebiidae of the World. Crustacean Monographs 6, 1–185.Google Scholar
Shimizu, R.M. (1997) Ecologia populacional de Scolelepis squamata (Muller, 1806) (Polychaeta: Spionidae) e Callichirus major (Say, 1818) (Crustacea: Decapoda: Thalassinidea) da praia de Barequeçaba (São Sebastião, SP) . PhD thesis. Universidade de São Paulo, São Paulo, Brazil.Google Scholar
Shimoda, K., Wardiatno, Y., Kubo, K. and Tamaki, A. (2005) Intraspecific behaviors and major cheliped sexual dimorphism in three congeneric callianassid shrimp. Marine Biology 146, 543–557.Google Scholar
Silva, D.C. and Martinelli-Lemos, J.M. (2012) Species composition and abundance of the benthic community of Axiidea and Gebiidea (Crustacea: Decapoda) in the Marapanim Bay, Amazon estuary, northern Brazil. Zoologia 29, 144–158.Google Scholar
Simão, D.S., Ramos, M.F. and Soares-Gomes, A. (2006) Population structure of Callichirus major (Say 1818) (Crustacea: Thalassinidea) in a sandy beach of Rio de Janeiro State, southeast Brazil coast. Journal of Coastal Research SI 39 (Proceedings of the 8th International Coastal Symposium), 1165–1168.Google Scholar
Souza, J.R.B. and Borzone, C.A. (1996) Distribuição de Callianassídeos (Crustacea: Decapoda: Thalassinidea) em praias do litoral paranaense, com especial referência à Callichirus major (Say, 1818). Arquivos de Biologia e Tecnologia 39, 553–565.Google Scholar
Souza, J.R.B., Borzone, C.A. and Brey, T. (1998) Population dynamics and secondary production of Callichirus major (Crustacea: Thalassinidea) on a southern Brazilian sandy beach. Archives of Fisheries and Marine Research 46, 151–164.Google Scholar
Strasser, K.M. and Felder, D.L. (2005) Larval development of the mud shrimp Axianassa australis (Decapoda: Thalassinidea) under laboratory conditions. Journal of Natural History 39, 2289–2306.Google Scholar
Suchanek, T.H. (1983) Control of seagrass communities and sediment distribution by Callianassa (Crustacea, Thalassinidea) bioturbation. Journal of Marine Research 41, 281–298.Google Scholar
Tamaki, A., Ingole, B., Ikebe, K., Muramatsu, K., Taka, M. and Tanaka, M. (1997) Life history of the ghost shrimp, Callianassa japonica Ortmann (Decapoda: Thalassinidea), on an intertidal sandflat in western Kyushu, Japan. Journal of Experimental Marine Biology and Ecology 210, 223–250.Google Scholar
Thessalou-Legaki, M. and Kiortsis, V. (1997) Estimation of the reproductive output of the burrowing shrimp Callianassa tyrrhena: a comparison of three different biometrical approaches. Marine Biology 127, 435–442.Google Scholar
Tunberg, B. (1986) Studies on the population ecology of Upogebia deltaura (Crustacea: Thalassinidea). Estuarine, Coastal and Shelf Science 22, 753–766.Google Scholar
Witbaard, R. and Duineveld, G.C.A. (1989) Some aspects of the biology and ecology of the burrowing shrimp Callianassa subterranea (Montagu) (Thalassinidea) from the southern North Sea. Sarsia 74, 145–222.Google Scholar
Zar, J.H. (1996) Biostatistical analysis. 3rd edition. Upper Saddle River, NJ: Prentice Hall.Google Scholar