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To grow or to reproduce? Sexual dimorphism and ontogenetic allometry in two Sesarmidae species (Crustacea: Brachyura)

Published online by Cambridge University Press:  28 March 2018

Murilo Zanetti Marochi Open the ORCID record for Murilo Zanetti Marochi [Opens in a new window] ,
Marcelo Costa ,
Renata Daldin Leite ,
Isis Danniele Cury Da Cruz  and
Setuko Masunari
Murilo Zanetti Marochi*
Affiliation:
Departamento de Zoologia, Programa de Pós-Graduação em Zoologia, Universidade Federal do Paraná, 81531970, Curitiba, Paraná, Brazil
Marcelo Costa
Affiliation:
Departamento de Ciências Biológicas, Universidade Estadual do Centro-Oeste, Cedeteg, Vila Carli, 85040-080, Guarapuava, Paraná, Brazil
Renata Daldin Leite
Affiliation:
Departamento de Zoologia, Programa de Pós-Graduação em Zoologia, Universidade Federal do Paraná, 81531970, Curitiba, Paraná, Brazil
Isis Danniele Cury Da Cruz
Affiliation:
Departamento de Zoologia, Programa de Pós-Graduação em Zoologia, Universidade Federal do Paraná, 81531970, Curitiba, Paraná, Brazil
Setuko Masunari
Affiliation:
Departamento de Zoologia, Programa de Pós-Graduação em Zoologia, Universidade Federal do Paraná, 81531970, Curitiba, Paraná, Brazil
*
Correspondence should be addressed to: M.Z. Marochi, Departamento de Zoologia, Programa de Pós-Graduação em Zoologia, Universidade Federal do Paraná, 81531970, Curitiba, Paraná, Brazil email: [email protected]
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Abstract

Differences between sexes may arise either during development or at the adult stage only. In both cases growth rate during development and level of allometry may influence sexual dimorphism and ontogenetic trajectories. To analyse the period in which sexual dimorphism appears during ontogeny and assess allometric ontogeny in Sesarmidae crabs, we evaluated: (1) sexual dimorphism in shape and size of the carapace and cheliped propodus of juveniles and adult Aratus pisonii and Armases rubripes, and (2) their ontogenetic trajectory, using geometric morphometric (GM) techniques. We tested the hypothesis that sexual dimorphism in sesarmid crab shape takes place before the puberty moult. In Aratus pisonii there was sexual dimorphism in the shape of the carapace in juveniles (before puberty moult) and variation between juveniles and adults was size-dependent, especially in the frontal region of the carapace. For Armases rubripes this shape sexual dimorphism was detected only after the puberty moult (adult phase). For males, carapace variation between juveniles and adults was also size-dependent, especially in the carapace frontal region, but for females, there was a change in shape with different trajectories. Our results also indicated that shape variation is a common pattern during growth for Sesarmidae species. This ontogenetic shape variation may be associated with spatial partitioning between juveniles and adults.

Keywords

Ontogenetic trajectoriesAratusArmasesshape variationgeometric morphometrics
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 99 , Issue 2 , March 2019 , pp. 473 - 486
Copyright
Copyright © Marine Biological Association of the United Kingdom 2018 

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References

REFERENCES

Abouheif, E. and Fairbairn, D.J. (1997) A comparative analysis of allometry for sexual size dimorphism: assessing Rensch's rule. American Naturalist 149, 540–562.Google Scholar
Adams, D.C., Rohlf, F.J. and Slice, D. (2004) Geometric morphometrics: ten years of progress following the ‘revolution’. Italian Journal of Zoology 71, 5–16.Google Scholar
Anastasiadou, C., Liasko, R. and Leonardos, I.D. (2009) Biometric analysis of lacustrine and riverine populations of Palemonetes antennarius (H Milne-Edwards, 1837) (Crustacea, Decapoda, Palaemonidae) from north-western Greece. Limnologica 39, 244–254.Google Scholar
Anholt, B.R., Marden, J.H. and Jenkins, D.M. (1991) Patterns of mass gain and sexual dimorphism in adult dragonflies (Insecta: Odonata). Canadian Journal of Zoology 69, 1156–1163.Google Scholar
Ayres, M., Ayres, M. Jr, Ayres, D.L. and Santos, A.S. (2007) Bioestat Versão 5.0. Belém: Sociedade Civil Mamirauá, MCT-CNPq.Google Scholar
Backwell, P.R.Y. and Passmore, N.I. (1996) Time constraints and multiple choice criteria in the sampling behaviour and mate choice of the fiddler crab, Uca annulipes. Behavioral Ecology and Sociobiology 38, 407–416.Google Scholar
Braña, F. (1996) Sexual dimorphism in lacertid lizards: male head increase vs female abdomen increase? Oikos 75, 511–523.Google Scholar
Callander, S., Kahn, A.T., Maricic, T., Jennions, M.D. and Backwell, P.R. (2013) Weapons or mating signals? Claw shape and mate choice in a fiddler crab. Behavior Ecology and Sociobiology 67, 1163–1167.Google Scholar
Cardini, A. and Elton, S. (2007) Sample size and sampling error in geometric morphometric studies of size and shape. Zoomorphology 126, 121–134.Google Scholar
Castiglioni, D.S., Santos, S., Reigada, A.L.D. and Negreiros-Fransozo, M.L. (2004) Reproductive ecology of Armases rubripes (Sesarmidae) from mangroves of Southeastern Brazil. Nauplius 12, 109–117.Google Scholar
Cock, A.G. (1966) Genetical aspects of metrical growth and form in animals. Quarterly Review of Biology 41, 131–190.Google Scholar
Crane, J. (1975) Fiddler crabs of the world. Princeton, NJ: Princeton University Press.Google Scholar
Dalabona, G. and Pinheiro, M.A.A. (2005) Size at morphological maturity of Ucides cordatus (Linnaeus, 1763)(Brachyura, Ocypodidae) in the Laranjeiras Bay, southern Brazil. Brazilian Archives of Biology and Technology 48, 139–145.Google Scholar
Fairbairn, D.J. (1997) Allometry for sexual size dimorphism: pattern and process in the coevolution of body size in males and females. Annual Review of Ecology and Systematics 28, 659–687.Google Scholar
Fairbairn, D.J. and Preziosi, R.F. (1994) Sexual selection and evolution of allometry for sexual size dimorphism in the water strider, Aquarius remigis. American Naturalist 144, 101–118.Google Scholar
Fairbairn, D.J. and Preziosi, R.F. (1996) Sexual selection and the evolution of sexual size dimorphism in the water strider, Aquarius remigis. Evolution 50, 1549–1559.Google Scholar
Green, A.J. (1992) Positive allometry is likely with mate choice, competitive display and other functions. Animal Behavior 43, 170–172.Google Scholar
Guerao, G., Anger, K., Nettelmann, U.W.E. and Schubart, C.D. (2004) Complete larval and early juvenile development of the mangrove crab Perisesarma fasciatum (Crustacea: Brachyura: Sesarmidae) from Singapore, with a larval comparison of Parasesarma and Perisesarma. Journal of Plankton Research 26, 1389–1408.Google Scholar
Guerao, G., Anger, K. and Schubart, C.D. (2007) Larvae and first stage juveniles of the American genus Armases Abele, 1992 (Brachyura: Sesarmidae): a morphological description of two complete developments and one first zoeal stage. Journal of Natural History 41, 1811–1839.Google Scholar
Hartnoll, R.G. (1974) Variation in growth pattern between some secondary sexual characters in crabs (Decapoda, Brachyura). Crustaceana 27, 131–136.Google 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, Volume 2. Embryology, morphology, and genetics. New York, NY: Academic Press, pp. 111–196.Google Scholar
Hartnoll, R.G. (1985) Growth, sexual maturity and reproductive output. In Wenner, A.M. (ed.) Factors in adult growth. Boston, MA: A.A. Balkema, pp. 101–128.Google Scholar
Hartnoll, R.G. (2001) Growth in Crustacea: twenty years on. Hydrobiologia 449, 111–122.Google Scholar
Hines, A.H. (1989) Geographic variation in size at maturity in brachyuran crabs. Bulletin of Marine Science 45, 356–368.Google Scholar
Huxley, J.S. (1950) Relative growth and form transformation. Proceedings of the Royal Society London 137, 465–469.Google Scholar
Judge, K.A. and Bonanno, V.L. (2008) Male weaponry in a fighting cricket. PLoS ONE 3, e3980.Google Scholar
Klingenberg, C.P. (1996) Multivariate allometry. In Marcus, L.F., Corti, M., Loy, A., Naylor, G.J.P. and Slice, D.E. (eds) Advances in morphometrics. New York, NY: Springer Press, pp. 23–49.Google Scholar
Klingenberg, C.P. (1998) Heterochrony and allometry: the analysis of evolutionary change in ontogeny. Biological Reviews of the Cambridge Philosophical Society 73, 79–123.Google Scholar
Klingenberg, C.P. (2011) Morphoj: an integrated software package for geometric morphometrics. Molecular Ecology Resources 11, 353–357.Google Scholar
Klingenberg, C.P. (2016) Size, shape, and form: concepts of allometry in geometric morphometrics. Development Genes and Evolution 226, 113–137.Google Scholar
Klingenberg, C.P., Barluenga, M. and Meyer, A. (2002) Shape analysis of symmetric structures: quantifying variation among individuals and asymmetry. Evolution 56, 1909–1920.Google Scholar
Kodric-Brown, A., Sibly, R.M. and Brown, J.H. 2006 The allometry of ornaments and weapons. Proceedings of the National Academy of Sciences USA 103, 8733–8738.Google Scholar
Koene, J.M. and Ter Maat, A. (2004) Energy budgets in the simultaneously hermaphroditic pond snail, Lymnaea stagnalis: a trade-off between growth and reproduction during development. Belgian Journal of Zoology 134, 41–46.Google Scholar
Koga, T., Backwell, P.R.Y., Christy, J.H., Murai, M. and Kasuya, E. (2001) Male biased predation of a fiddler crab. Animal Behavior 62, 201–207.Google Scholar
Kuris, A.M. (1971) Population interactions between a shore crab and two symbionts. Dissertation. University of California, Berkeley, USA.Google Scholar
Lailvaux, S.P., Reaney, L.T. and Backwell, P.R.Y. (2009) Dishonest signaling of fighting ability and multiple performance traits in the fiddler crab Uca mjoebergi. Functional Ecology 23, 359–366.Google Scholar
Lima, G.V. and Oshiro, L.M.Y. (2006) Sexual maturity of the crab Armases rubripes (Rathbun) (Crustacea, Brachyura, Sesarmidae) in Sepetiba Bay, Rio de Janeiro, Brazil. Revista Brasileira de Zoologia 23, 1078–1086.Google Scholar
Lima, G.V., Soares, M.R. and Oshiro, L.M. (2006) Reproductive biology of the sesarmid crab Armases rubripes (Decapoda, Brachyura) from na estuarine área of the Sahy River, SepetibaBay, Rio de Janeiro, Brazil. Iheringia: Série Zoologia 96, 47–52.Google Scholar
Marochi, M.Z., Moreto, T.F., Lacerda, M.B., Trevisan, A. and Masunari, S. (2013) Sexual maturity and reproductive period of the swimming blue crab Callinectes danae Smith, 1869 (Brachyura: Portunidae) from Guaratuba Bay, Paraná State, southern Brazil. Nauplius 21, 43–52.Google Scholar
Meyer-Rochow, V.B., Towers, D. and Ziedins, I. (1990) Growth patterns in the eye of Petrolisthes elongatus (Crustacea; Decapoda; Anomura). Experimental Biology 48, 329–340.Google Scholar
Milner, R.N.C., Detto, T., Jennions, M.D. and Backwell, P.R.Y. (2010) Experimental evidence for a seasonal shift in the strength of a female mating preference. Behavior Ecology 21, 311–316.Google Scholar
Monteiro, L.R. and Reis, S.F. (1999) Princípios de morfometria geométrica. Ribeirão Preto: Holos Editora.Google Scholar
Nagamine, C.M. and Knight, A.W. (1980) Development, maturation, and function of some sexually dimorphic structures of the Malaysian prawn, Macrobrachium rosenbergii (De Man) (Decapoda, Palaemonidae). Crustaceana 39, 141–152.Google Scholar
Nagamine, C., Knight, A.W., Maggenti, A. and Paxman, G. (1980) Effects of androgenic gland ablation on male primary and secondary sexual characteristics in the Malaysian prawn, Macrobrachium rosenbergii (de Man) (Decapoda, Palaemonidae), with first evidence of induced feminization in a nonhermaphroditic decapod. General and Comparative Endocrinology 41, 423–441.Google Scholar
Pahlas, J.M. (2013) Size dependent shifts in the diet of the mangrove tree crab, Aratus pisonii, as indicated by δ13c &δ15n from a mangrove ecosytem in Indian River Lagoon, FL. Dissertation. The University of Georgia, USA.Google Scholar
Pescinelli, R.A., Davanso, T.M. and Costa, R.C. (2015) Relative growth and morphological sexual maturity of the mangrove crab Aratus pisonii (H. Milne Edwards, 1837) on the southern coast of the state of São Paulo, Brazil. International Journal of Invertebrate Reproduction and Development 59, 55–60.Google Scholar
Petrie, M. (1992) Are all secondary sexual display structures positively allometric and, if so, why? Animal Behavior 43, 173–175.Google Scholar
Pezzuto, P.R. (1993) REGRANS: a “basic” program for an extensive analysis of relative growth. Atlântica 15, 91–105.Google Scholar
Punzalan, D. and Hosken, D.J. (2010) Sexual dimorphism: why the sexes are (and are not) different. Current Biology 20, 972–973.Google Scholar
R Development Core Team (2016) R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. ISBN 3-900051-07-0.Google Scholar
Roff, D.A. (2000) Trade-offs between growth and reproduction: an analysis of the quantitative genetic evidence. Journal of Evolutionary Biology 13, 434–445.Google Scholar
Rohlf, F.J. (2010) Tpsdig, ver. 2.16: a program for digitizing landmarks and outlines for geometric morphometrics. [Online]. Stony Brook, NY: Department of Ecology and Evolution, State University of New York.Google Scholar
Rosenberg, M.S. (2002) Fiddler crab claw shape variation: a geometric morphometric analysis across the genus Uca (Crustacea: Brachyura: Ocypodidae). Biological Journal of the Linnean Society 75, 147–162.Google Scholar
Sheets, H.D. and Zelditch, L.M. (2013) Studying ontogenetic trajectories using resampling methods and landmark data. Hystrix. Italian Journal of Mammalogy 24, 67–73.Google Scholar
Shine, R. (1989) Ecological causes for the evolution of sexual dimorphism: a review of the evidence. Quarterly Review of Biology 64, 419–461.Google Scholar
Smith, W.K. and Miller, P.C. (1973) The thermal ecology of two south Florida fiddler crabs: Uca rapax smith and Uca pugilator. Physiological Zoology 46, 186–207.Google Scholar
Sokal, R.R. and Rohlf, J.F. (1979) Biometry. New York, NY: Freeman.Google Scholar
Stearns, S.C. and Koella, J.C. (1986) The evolution of phenotypic plasticity in life-history traits: predictions of reaction norms for age and size at maturity. Evolution 40, 893–913.Google Scholar
Trevisan, A., Marochi, M.Z., Costa, M., Santos, S. and Masunari, S (2012) Sexual dimorphism in Aegla marginata (Decapoda: Anomura). Nauplius 20, 75–86.Google Scholar
Weckerly, F.W. (1998) Sexual-size dimorphism: influence of mass and mating system in the most dimorphic mammals. Journal of Mammalogy 79, 33–52.Google Scholar
Wenner, A.M., Fusaro, C. and Oaten, A. (1974) Size at onset of sexual maturity and growth rate in crustacean populations. Canadian Journal of Zoology 52, 1095–1106.Google Scholar