Skip to main content
Log in

Growth, Sexual Maturity and Dimorphism in Six Species of Snapping Shrimps of the Genus Alpheus (Decapoda: Alpheidae)

  • Published:
Thalassas: An International Journal of Marine Sciences Aims and scope Submit manuscript

Abstract

This study investigated the sexual dimorphism, allometric growth, and morphological maturity of six sympatric species of Alpheus. The samplings occurred in August 2015, February and August 2016, and February 2017, in the intertidal, during low spring tides, in two localities in the northeastern Brazilian coast. In total, 3038 individuals were captured: 302 A. angulosus, 400 A. bouvieri, 516 A. buckupi, 410 A. carlae, 1002 A. estuariensis, and 408 A. nuttingi. According to our data, the six species lack sexual dimorphism regarding the carapace length. However, the major chelipeds were more robust in males of five species, whereas abdominal structures (pleurae and sternites) were larger in females, both indicatives of sexual dimorphism. The analyses of the relative growth of cheliped dimensions versus body size demonstrate that males of six species invest more energy in the chelipeds during the adult and juvenile phases. On the other hand, in the females the cheliped growth is higher during the juvenile phase. The analysis of energy allocation (calculated using body and chelipeds mass) also confirmed a high energetic investment in this appendage in males (minimum 32% of the body mass). Our results also show that females can also invest a lot of energy in the chelipeds (minimum 22% of the body mass). However, the intraspecific sex differences may be consequences of a trade-off between embryo production and cheliped development. The growth rate of pleura and sternites were higher in the adult females of all species except for A. bouvieri. In the males of the six species the appendix masculina grows faster during the juvenile phase. Lastly, in the six species of Alpheus studied, males and females reach the morphological maturity at very similar sizes, indicating a synchrony of reproduction and growth.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Ahamed F, Ohtomi J (2014) Relative growth and sexual maturity of the pandalid shrimp Plesionika izumiae (Decapoda, Caridea) in Kagoshima bay, Southern Japan. Crustaceana 87:1567–1577

    Article  Google Scholar 

  • Almeida AC, Hiyodo CM, Cobo VJ, Bertini G, Fransozo V, Teixeira GM (2013) Relative growth, sexual maturity, and breeding season of three species of the genus Persephona (Decapoda: Brachyura: Leucosiidae): a comparative study. J Mar Biol Assoc U K 96:1581–1591

    Article  Google Scholar 

  • Anger K, Moreira GD (1998) Morphometric and reproductive traits of tropical caridean shrimps. J Crustac Biol 18:823–838

    Article  Google Scholar 

  • Anker (2001) Taxonomie et évolution des Alpheidae (Crustacea, Decapoda). PhD thesis. Muséum National d’Histoire Naturelle, Paris

    Google 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 3386:109

    Article  Google Scholar 

  • Anker A, Ahyong ST, Noel PY, Palmer AR (2006) Morphological phylogeny of alpheid shrimps: parallel preadaptation and the origin of a key morphological innovation, the snapping claw. Evolution 60:2507–2528

    Article  Google Scholar 

  • Araújo MSLC, Coelho PA, Castiglioni DS (2012) Relative growth and determination of morphological sexual maturity of the fiddler crab Uca thayeri Rathbun (Crustacea, Ocypodidae) in two mangrove areas from Brazilian tropical coast. Pan-American J Aquat Sci 3:156–170

    Google Scholar 

  • Atkinson RJA, Gramitto ME, Froglia C (2003) Aspects of the biology of the burrowing shrimp Alpheus glaber (Olivi) (Decapoda: Caridea: Alpheidae) from the Central Adriatic. Ophelia 57:27–42

    Article  Google Scholar 

  • Baeza JA (2008) Social monogamy in the shrimp Pontonia margarita, a symbiont of Pinctada mazatlantica, off the Pacific coast of Panama. Mar Biol 153:387–395

    Article  Google Scholar 

  • Baeza JA, Bolaños JA, Hernandez JE, Lira C, López R (2011) Monogamy does not last long in Pontonia mexicana, a symbiotic shrimp of the amber pen-shell Pinna carnea from the southeastern Caribbean Sea. J Exp Mar Biol Ecol 407:41–47

    Article  Google Scholar 

  • Baeza JA, Simpson L, Ambrosio LJ, Guéron R, Mora N (2016) Monogamy in a hyper-symbiotic shrimp. PLoS One 11:e0149797. https://doi.org/10.1371/journal.pone.0149797

    Article  Google Scholar 

  • Bauer RT (2004) Remarkable shrimps: adaptations and natural history of the carideans. University of Oklahoma Press, Norman

    Google Scholar 

  • Boltaña S, Thiel M (2001) Associations between two species of snapping shrimp Alpheus inca and Alpheopsis chilensis (Decapoda: Caridea: Alpheidae). J Mar Biol Assoc U K 81:633–638

    Article  Google Scholar 

  • Bueno SL, Shimizu RM (2009) Allometric growth, sexual maturity, and adult male chelae dimorphism in Aegla franca (Decapoda: Anomura: Aeglidae). J Crustac Biol 29:317–328

    Article  Google Scholar 

  • Castiglioni DS, Negreiros-Fransoso ML (2004) Comparative analysis of the relative growth of Uca rapax (Smith) (Crustacea, Ocypodidae) from two mangroves in São Paulo, Brazil. Rev Bras Zool 21:137–144

    Article  Google Scholar 

  • Castilho AL, Gavio MA, Costa RC, Boschi EE, Bauer RT, Fransozo A (2007) Latitudinal variation in population structure and reproductive pattern of the endemic South American shrimp Artemesia longinaris (Decapoda: Penaeoidea). J Crustac Biol 27:548–552

  • Clarke A, Hopkins CCE, Nilssen EM (1991) Egg size and reproductive output in the deep-water prawn Pandalus borealis Kroyer, 1838. Funct Ecol 5:724–730

    Article  Google Scholar 

  • Clayton DA (1990) Crustacean allometric growth: a case for caution. Crustaceana 58:270–290

    Article  Google Scholar 

  • Costa-Souza AC, Rocha SS, Bezerra LEA, Almeida AO (2014) Breeding and heterosexual pairing in the snapping shrimp Alpheus estuariensis (Caridea: Alpheidae) in a tropical bay in northeastern Brazil. J Crustac Biol 35:593–603

    Article  Google Scholar 

  • Costa-Souza AC, Souza JRB, Araújo MSLC, Almeida AO (2018) Population structure of the shrimp Alpheus estuariensis (Caridea: Alpheidae) in a tropical estuarine tidal mudflat. Thalassas 34:1–11

    Article  Google Scholar 

  • Coutière H (1899) Les “Alpheidae”, morphologie externe et interne, formes larvaires, bionomie. Ann Sci Nat, Zool, Sér 8(9):1–560 pls. 1–6. [Masson, Paris

    Google Scholar 

  • Dabbagh A-R, Kamrani E, Taherizadeh MR (2012) Studies on social monogamy in the snapping shrimp, Alpheus lobidens De Haan, 1849. Asian J Anim Vet Adv 7:361–365

    Article  Google Scholar 

  • Fernández-Muñoz R, García-Raso JE (1987) Study of a population of Alpheus dentipes Guerin, 1832 from calcareous bottoms in the southern Spain. Investig Pesq 51:343–359

    Google Scholar 

  • Giri F, Loy A (2008) Size and shape variation of two freshwater crabs in Argentinean Patagonia: the influence of sexual dimorphism, habitat, and species interactions. J Crustac Biol 28:37–45

    Article  Google Scholar 

  • Hartnoll RG (1974) Variation in growth pattern between some secondary sexual characters in crabs (Decapoda, Brachyura). Crustaceana 27:131–136

    Article  Google Scholar 

  • Hartnoll RG (1978) The determination of relative growth in Crustacea. Crustaceana 34:281–293

    Article  Google Scholar 

  • Hartnoll RG (1982) Growth. In: Abele LG (ed) Embryology, morphology and genetics. The biology of crustacea. Academic Press, New York, pp 111–196

    Google Scholar 

  • Hartnoll RG (1985) Growth, sexual maturity and reproductive output. In: Wenner AM (ed) Factors in adult growth. A.A. Balkema, Rotterdam, pp 101–128

    Google Scholar 

  • Hartnoll RG (2001) Growth in Crustacea – twenty years on. Hydrobiologia 449:111–122

    Article  Google Scholar 

  • Herrera DR, Davanso TM, Costa RC (2017) Relative growth and morphological sexual maturity of the caridean shrimp Nematopalaemon schmitti (Decapoda: Caridea: Palaemonidae) in an upwelling region in the Western Atlantic. Invertebr Reprod Dev 62:56–62

    Article  Google Scholar 

  • Hughes M, Williamson T, Hollowell K, Vickery R (2014) Sex and weapons: contrasting sexual dimorphisms in weaponry and aggression in snapping shrimp. Ethology 120:982–994

    Article  Google Scholar 

  • Huxley JS (1950) Relative growth and form transformation. Proc Royal Soc Lond 137:465–469

    Article  Google Scholar 

  • Jormalainen V (1998) Precopulatory mate guarding in crustaceans: male competitive strategy and intersexual conflict. Q Rev Biol 73:275–304

    Article  Google Scholar 

  • Knowlton N (1980) Sexual selection and dimorphism in two demes of a symbiotic, pair-bonding snapping shrimp. Evolution 34:161–173

    Article  Google Scholar 

  • Mantelatto FL, Barbosa LR (2005) Population structure and relative growth of freshwater prawn Macrobrachuim brasiliense (Decapoda, Palaemonidae) from São Paulo State, Brazil. Acta Limnol Bras 17:245–255

    Google Scholar 

  • Mariappan P, Balasundaram C, Schmitz B (2000) Decapod crustacean chelipeds: an overview. J Biosci 25:301–331

    Article  Google Scholar 

  • Mathews LM (2002a) 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)? Behav Ecol Sociobiol 51:426–432

    Article  Google Scholar 

  • Mathews LM (2002b) Territorial cooperation and social monogamy: factors affecting intersexual behaviours in pair-living snapping shrimp. Animal Behav 63:767–777

    Article  Google Scholar 

  • Moraes EE, Nunesmaia BJB, Pinheiro MA (2015) Population biology of the ‘uçá’-crab, Ucides cordatus (Linnaeus, 1763) (Brachyura: Ucididae), in mangroves of the Joanes River, Bahia State, Brazil. Nauplius 23:59–71

    Article  Google Scholar 

  • Moreno G, Selvakumaraswamy P, Byrne M, Hoegh-Guldberg O (2001) A test of the ash-free dry weight technique on the developmental stages of Patiriella spp. (Echinodermata: Asteroidea). Limnol Oceanogr 46:1214–1220

    Article  Google Scholar 

  • Mossolin EC, Bueno SLS (2003) Relative growth of the second pereiopod in Macrobrachium olfersi (Wiegmann, 1836) (Decapoda: Palemonidae). Crustaceana 76:363–376

    Article  Google Scholar 

  • Mossolin EC, Shimizu RM, Bueno SLS (2006) Population structure of Alpheus armillatus (Decapoda, Alpheidae) in São Sebastião and Ilhabela, southeastern Brazil. J Crustac Biol 26:48–54

    Article  Google Scholar 

  • Nagamine CM (1980) Development, maturation, and function of some sexually dimorphic structures of the Malaysian prawn, Macrobrachium rosenbergii (De Man) (Decapoda, Palaemonidae). Crustaceana 39:141–152

    Article  Google Scholar 

  • Nolan BA, Salmon M (1970) The behavior and ecology of snapping shrimp (Crustacea: Alpheus heterochaelis and Alpheus normanni). Forma et functio 2:289–335

    Google Scholar 

  • Paschoal LRP, Guimarães FJ, Couto ECG (2013) Relative growth and sexual maturity of the freshwater shrimp Palaemon pandaliformis (Crustacea, Palaemonidae) in northeastern of Brazil (Canavieiras, Bahia). Iheringia, Sér Zool 103:31–36

    Article  Google Scholar 

  • Pescinelli RA, Davanso TM, Costa RC (2017) Social monogamy and egg production in the snapping shrimp Alpheus brasileiro (Caridea: Alpheidae) from the south-eastern coast of Brazil. J Mar Biol Assoc U K 97:1519–1526

    Article  Google Scholar 

  • Pescinelli RA, Almeida AO, Costa RC (2018) Population structure, relative growth and morphological sexual maturity of the snapping shrimp Alpheus brasileiro Anker, 2012 (Caridea: Alpheidae) from the south-eastern coast of Brazil. Mar Biol Res 14:610–620

    Article  Google Scholar 

  • Pinheiro MAA, Hattori GY (2006) Relative growth of the mangrove crab Ucides cordatus (Linnaeus, 1763) (Crustacea, Brachyura, Ocypodidae) at Iguape, São Paulo, Brazil. Braz Arch Biol Technol 49:813–823

    Article  Google Scholar 

  • Rahman N, Dunham MDW, Govind C (2003) Social monogamy in the big clawed snapping shrimp Alpheus heterochaelis. Ethology 109:457–473

    Article  Google Scholar 

  • Rahman N, Dunham DW, Govind CK (2004) Mate choice in the big-clawed in the snapping shrimp Alpheus heterochaelis Say, 1818. Crustaceana 77:95–111

    Article  Google Scholar 

  • Rasband WS (2006) ImageJ: image processing and analysis in Java. National Institutes of Health, Research Services Branch Bethesda. http://rsb.info.nih.gov/ij/docs/index.html. Accessed 10 February 2018

  • Saito T (2002) Development of external sexual characters in the deep-sea sponge-associated shrimp Spongicola japonica Kubo (Crustacea: Decapoda: Spongicolidae). J Nat Hist 36:819–829

    Article  Google Scholar 

  • Sampedro ME, González-Gurriarán J, Freire J, Muiño R (1999) Morphometry and sexual maturity in the spider crab Maja squinado (Decapoda: Majidae) in Galicia, Spain. J Crustac Biol 19:578–592

    Article  Google Scholar 

  • Santos MCF, Garcia-Mendes E (1982) Biometric studies and mechanical advantages in the dimorphic chelae of the mangrove crab, Ucides cordatus. Bol Fisiol Animal USP 6:143–150

    Google Scholar 

  • Sganga DE, Piana LRF, Greco LSL (2016) Sexual dimorphism in a freshwater atyid shrimp (Decapoda: Caridea) with direct development: a geometric morphometrics approach. Zootaxa 4196:120–128

    Article  Google Scholar 

  • Silva TR, Rocha SS, Costa Neto EM (2014a) Relative growth, sexual dimorphism and morphometric maturity of Trichodactylus fluviatilis (Decapoda: Brachyura: Trichodactylidae) from Santa Terezinha, Bahia, Brazil. Zoologia 31:20–27

    Article  Google Scholar 

  • Silva TE, Fumis PB, Almeida AC, Bertini G, Fransozo V (2014b) Morphometric analysis of the mud crab Hexapanopeus paulensis Rathbun, 1930 (Decapoda, Xanthoidea) from the southeastern coast of Brazil. Lat Am J Aquat Res 42:588–597

    Article  Google Scholar 

  • Silva FMRO, Ribeiro FB, Bezerra LEA (2016) Population biology and morphometric sexual maturity of the fiddler crab Uca (Uca) maracoani (Latreille, 1802) (Crustacea: Decapoda: Ocypodidae) in a semi-arid tropical estuary of northeastern Brazil. Lat Am J Aquat Res 44:671–682

    Article  Google Scholar 

  • Soledade GO, Almeida AO (2013) Snapping shrimps of the genus Alpheus Fabricius, 1798 from Brazil (Caridea: Alpheidae): updated checklist and key for identification. Nauplius 21:89–122

    Article  Google Scholar 

  • Soledade GO, Santos PS, Araujo MSLC, Mantelatto FL, Almeida AO (2018) Heterosexual pairing in three Alpheus (crustacea: alpheidae) snapping shrimps from northeastern Brazil. Vie et Milieu-Life and Environment 68:109–117

    Google Scholar 

  • Vazzoler AEAM (1996) Biologia da reprodução de peixes teleósteos: teorias e prática. EDUEM, Maringá

  • Zar JH (2010) Biostatistical analysis. Pearson Prentice-Hall, New Jersey

    Google Scholar 

Download references

Acknowledgements

To the team of the Laboratório de Biologia de Crustáceos da UFPE, to Laboratório de Biofísica de Biomembranas e Células Tronco/Oleg Krasilnikov da UFPE and to Laboratório de Cultivo de Meiofauna Marinha e Ecotoxicologia da UFPE. To Maria Laís Vieira, Thais Kananda and João Victor Nunes for support during the laboratory procedures, and to Ricardo Paiva and Flávio Almeida for their help in the samplings. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de nível Superior – Brasil (CAPES) – Finance Code 001 (doctorate’s scholarship to ACC-S). AOA is thankful to the “Conselho Nacional de Desenvolvimento Científico e Tecnólogico” (CNPq) for the Research Scholarship support (305939/2015-7). We would like to thank the anonymous reviewers for the suggestions that improved the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ana Carla Costa-Souza.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Costa-Souza, A.C., de Souza, J.R.B. & Almeida, A.O. Growth, Sexual Maturity and Dimorphism in Six Species of Snapping Shrimps of the Genus Alpheus (Decapoda: Alpheidae). Thalassas 35, 451–464 (2019). https://doi.org/10.1007/s41208-019-00146-2

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s41208-019-00146-2

Keywords

Navigation