Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-22T17:49:19.141Z Has data issue: false hasContentIssue false

Sexual dimorphism in the shell of a nassariid gastropod. A 3D geometric morphometrics approach

Published online by Cambridge University Press:  07 March 2016

Federico Márquez*
Affiliation:
LEEIN, Instituto de Biología de Organismos Marinos – CONICET, Blvd. Brown 2915 (U9120ACD), Puerto Madryn, Argentina Universidad Nacional de la Patagonia San Juan Bosco, Blvd Brown 3100, Puerto Madryn (U9120ACD), Chubut, Argentina
Andres Averbuj
Affiliation:
LARBIM, Instituto de Biología de Organismos Marinos – CONICET, Blvd. Brown 2915 (U9120ACD), Puerto Madryn, Argentina
*
Correspondence should be addressed to:F. Márquez, LEEIN, Instituto de Biología de Organismos Marinos – CONICET, Blvd. Brown 2915 (U9120ACD), Puerto Madryn, Argentina and Universidad Nacional de la Patagonia San Juan Bosco, Blvd Brown 3100, Puerto Madryn (U9120ACD), Chubut, Argentina email: [email protected]

Abstract

Among gastropods, dimorphism is reported in shell size, radular characteristic, and to a lesser extent in shell shape. The relationship of dimorphic characters of the shell with spawning is scarcely studied in literature. Buccinanops globulosus is an interesting model to study sexual dimorphism in shell shape, because the adults attach their egg capsules to the females’ own shells (callus zone). Our hypothesis is that the shell dimorphism is evidenced in the form (size and shape) of callus zones of the females' shells, compared with the males'. In order to test this hypothesis we use a 3D geometric morphometrics (GM) method with several advantages over 2D GM. The relationship between callus shape and size was allometric. During growth, the main callus shape changes are related to the mean size increment, which is more evident in larger females. These callus zones are characteristically slender in males and small females, and more inflated in large females. Our analyses revealed that female shells are different from male ones and those differences are significant on the callus zone where the egg capsules are attached by the female. This finding suggests a relationship of the shell form with spawning. Our findings are not only relevant in terms of the shell dimorphism of the particular spawning substrate area (callus zones) and its reproductive implications, but also provide insights into the evaluation of shell shape variation on areas without type I or II anatomical landmarks in 3D GM.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2016 

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

Adams, D.C., Rohlf, F.J. and Slice, D. (2004) Geometric morphometrics: ten years of progress following the ‘revolution’. Italian Journal of Zoology 71, 516.Google Scholar
Arak, A. (1988) Sexual dimorphism in body size: a model and a test. Evolution 42, 820825.CrossRefGoogle Scholar
Arakawa, K. and Hayashi, S. (1972) On sexual dimorphism of fig shell, Ficus subintermedius (d'Orbigny). Venus 31, 6370.Google Scholar
Avaca, M.S., Narvarte, M. and Martín, P. (2012) Size-assortative mating and effect of maternal body size on the reproductive output of the nassariid Buccinanops globulosus . Journal of Sea Research 69, 1622.Google Scholar
Avaca, M.S., Narvarte, M., Martín, P. and Van der Molen, S. (2013) Shell shape variation in the Nassariid Buccinanops globulosus in northern Patagonia. Helgoland Marine Research 67, 567577.Google Scholar
Averbuj, A. and Penchaszadeh, P.E. (2010) Reproductive seasonality, oviposition and development of the nassariid whelk Buccinanops cochlidium (Dillwyn, 1817) in Patagonia, Argentina. Journal of Molluscan Studies 76, 2532.Google Scholar
Averbuj, A. and Penchaszadeh, P.E. (in press) Reproductive biology in the South Western Atlantic genus Buccinanops (Nassariidae): the case of Buccinanops paytensis . Molluscan Research 35. http://dx.doi.org/10.1080/13235818.2015.1115384.Google Scholar
Averbuj, A., Bigatti, G. and Penchaszadeh, P.E. (2010) Gametogenic cycle and size at first maturity of the Patagonic edible snail Buccinanops cochlidium from Argentina. Marine Biology 157, 22292240.Google Scholar
Averbuj, A., Rocha, M. and Zabala, M.S. (2014) Embryonic development and reproductive seasonality of Buccinanops globulosus (Nassariidae) (Kiener, 1834) in Patagonia, Argentina. Invertebrates Reproduction and Development 58, 138147.Google Scholar
Bookstein, F.L. (1991) Morphometric tools for landmark data. New York, NY: Cambridge University Press.Google Scholar
Cardini, A. (2014) Missing the third dimension in geometric morphometrics: how to assess if 2D images really are a good proxy for 3D structures? Hystrix, the Italian Journal of Mammalogy 25, 7381.Google Scholar
Gilbert, J.J. and Williamson, C.E. (1983) Sexual dimorphism in zooplankton (Copepoda, Cladocera, and Rotifera). Annual Review of Ecology, Evolution, and Systematics 14, 133.Google Scholar
HallerStjabbes, C.T. (1979) Sexual dimorphism in Buccinum undatum L. Malacologia 18, 1317.Google Scholar
Kantor, Y. and Sysoev, A. (1991) Sexual dimorphism in the apertural notch of a new species of Gemmula (Gastropoda: Turridae). Journal of Molluscan Studies 57, 205209.Google Scholar
Klingenberg, C.P. (2011) MorphoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources 11, 353357.CrossRefGoogle ScholarPubMed
Maddux, S.D. and Franciscus, R.G. (2009) Allometric scaling of infraorbital surface topography in Homo . Journal of Human Evolution 56, 161174.Google Scholar
Márquez, F., González-José, R. and Bigatti, G. (2011) Combined methods to detect pollution effects on shell shape and structure in Neogastropods. Ecological Indicators 11, 248254.Google Scholar
Márquez, F., Nieto Vilela, R.A., Lozada, M. and Bigatti, G. (2015) Morphological and behavioral differences in gastropod Trophon geversianus associated to distinct environmental conditions, as revealed by a multidisciplinary approach. Journal of Sea Research 95, 239247.Google Scholar
Minton, R.L. and Wang, L.L. (2011) Evidence of sexual shape dimorphism in Viviparus (Gastropoda: Viviparidae). Journal of Molluscan Studies 77, 315317.Google Scholar
Monteiro, L.R. (1999) Multivariate regression models and geometric morphometrics: the search for causal factors in the analysis of shape. Systematic Biology 48, 192199.Google Scholar
Narvarte, M.A. (2006) Biology and fishery of the whelk Buccinanops globulosum (Kiener, 1834) in northern coastal waters of the San Matías Gulf (Patagonia, Argentina). Fisheries Research 77, 131137.Google Scholar
Pastorino, G. (1993) The taxonomic status of Buccinanops d́Orbigny, 1841 (Gastropoda: Nassariidae). The Veliger 36, 160165.Google Scholar
Pastorino, G. (2007) Sexual dimorphism in shells of the southwestern Atlantic gastropod Olivella plata (Ihering, 1908) (Gastropoda: Olividae). Journal of Molluscan Studies 73, 283285.CrossRefGoogle Scholar
Penchaszadeh, P.E. (1971) Aspectos de la embriogénesis de algunos gasterópodos del género Buccinanops d'Orbigny, 1841 (Gastropoda, Prosobranchiata, Buccinidae). Physis 30, 475482.Google Scholar
Primost, M.A., Bigatti, G. and Márquez, F. (2016). Shell shape as indicator of pollution in marine gastropods affected by imposex. Journal of Marine and Freshwater Research 17, 167171.Google Scholar
Rios, E.C. (2009) Compendium of Brazilian seashells. Rio Grande: Evangraf, 676 pp.Google Scholar
Rohlf, F.J. and Marcus, L.F. (1993) A revolution in morphometrics. Trends in Ecology and Evolution 8, 129132.Google Scholar
Rohlf, F.J. and Slice, D. (1990) Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Zoology 39, 4059.CrossRefGoogle Scholar
Scarabino, V. (1977) Moluscos del Golfo San Matías, provincia de Río Negro, República Argentina. Inventario y claves para su identificación. Comisión de la Sociedad Malacológica de Uruguay 4, 177285.Google Scholar
Son, M.H. and Hughes, R.N. (2000) Sexual dimorphism of Nucella lapillus (Gastropoda: Muricidae) in North Wales, UK. Journal of Molluscan Studies 66, 489498.Google Scholar
Shimek, R. (1984) The biology of the northeastern Pacific Turridae. IV: Shell morphology and sexual dimorphism in Aforia circinata (Dall, 1873). Veliger 26, 258263.Google Scholar
Shine, R. (1989) Ecological causes for the evolution of sexual dimorphism: a review of the evidence. Quarterly Review of Biology 64, 419461.Google Scholar
Slice, D.E., Bookstein, F.L., Marcus, L.E. and Rohlf, F.J. (1996) Appendix I: a glossary for geometric morphometrics. In Marcus, L.E., Corti, M., Loy, A., Naylor, G.J.P. and Slice, D. (eds) Advances in morphometrics. New York, NY: Plenum Press, pp. 531551.Google Scholar
Ueno, S. (1997) Sexual dimorphism in shell shape of the spider shell, Lambis lambis in Amitori Bay, Iriomote Island. Bulletin of the Institute of Oceanic Research and Development Tokai University 18, 1116.Google Scholar
Voltzow, J. (1994) Gastropoda: Prosobranchia. In Harrison, F.W. and Kohn, A.J. (eds) Microscopic anatomy of invertebrates. New York, NY: Wiley, pp. 111252.Google Scholar
Zelditch, M.L., Swiderski, D.L., Sheets, H.D. and Fink, W.L. (2004) Geometric morphometrics for biologists: a primer. New York, NY: Elsevier.Google Scholar