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Morphometric analysis of the shell of the intertidal gastropod Echinolittorina lineolata (d'Orbigny, 1840) at different latitudes along the Brazilian coast

Published online by Cambridge University Press:  30 July 2020

Alisson Sousa Matos Open the ORCID record for Alisson Sousa Matos [Opens in a new window] ,
Helena Matthews-Cascon  and
Oscar R. Chaparro
Alisson Sousa Matos*
Affiliation:
Laboratório de Invertebrados Marinhos do Ceará, Departamento de Biologia, Centro de Ciências, Universidade Federal do Ceará, Campus do Pici, Bloco 909, Pici, Fortaleza, 60455760, Brasil Instituto de Ciências do Mar, Universidade Federal do Ceará, 3207, Meireles, Fortaleza, 60165081, Brasil
Helena Matthews-Cascon
Affiliation:
Laboratório de Invertebrados Marinhos do Ceará, Departamento de Biologia, Centro de Ciências, Universidade Federal do Ceará, Campus do Pici, Bloco 909, Pici, Fortaleza, 60455760, Brasil Instituto de Ciências do Mar, Universidade Federal do Ceará, 3207, Meireles, Fortaleza, 60165081, Brasil
Oscar R. Chaparro
Affiliation:
Instituto de Ciencias Marinas y Limnológicas, Universidad Austral de Chile, Valdivia, Chile
*
Author for correspondence: Alisson Sousa Matos, E-mail: [email protected]
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Abstract

Morphometric analysis is one of the tools widely used to quantify, analyse and describe the variations in the biological forms of animals. In this study, we examined the linear morphometric variations of the shell of the small intertidal gastropod Echinolittorina lineolata and compared the patterns to identify variations among populations and between sexes. The individuals were collected from latitudes 3°S, 14°S, 21°S and 23°S along the Brazilian coast. Traditional morphometric analysis was performed, and the morphometric variables of the shells, namely, the length and width of the shell and the length and width of the shell opening were obtained. The observed size pattern was influenced by latitude, as well as by local spatial responses to factors such as the substrate changing the morphometric variables of the snail. Of the morphometric variables, the length and the width of the shell were the most representative variables that influenced the gastropods in the different latitudes. These variables were also different in males and females, with females having larger shell lengths and widths across all latitudes.

Keywords

Littorinidaemolluscsshell shapesnail
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 100 , Issue 5 , August 2020 , pp. 725 - 731
Copyright
Copyright © Marine Biological Association of the United Kingdom 2020

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References

Absalão, RS, Alves, R and Roberg, P (1999) Complexo Littorina ziczac (Gmelin) (Mollusca, Gastropoda, Caenogastropoda) no litoral fluminense: análise morfométrica, distribuição vertical e bioquímica. Revista Brasileira de Zoologia 16, 381–395.CrossRefGoogle Scholar
Almeida, FFM and Carneiro, CDR (1998) Origem e Evolução da Serra do Mar. Revista Brasileira de Geociências 28, 135–150.CrossRefGoogle Scholar
Angielczyk, KD, Burroughs, RW and Feldman, CR (2015) Do turtles follow the rules? Latitudinal gradients in species richness, body size, and geographic range area of the world's turtles. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 324, 270–294.CrossRefGoogle ScholarPubMed
Anjos, DC, Hernandez, FFF, Bañuelos, GS, Dangi, SR, Tirado-Corbalá, R, da Silva, FN and Filho, PFM (2018) Microbial community and heavy metals content in soils along the Curu River in Ceará, Brazil. Geoderma Regional 14, e00173.CrossRefGoogle Scholar
Apolinário, M, Coutinho, R and Baeta-Neves, MH (1999) Periwinkle (Gastropoda: Littorinidae) habitat selection and its impact upon microalgal populations. Revista Brasileira de Biologia 59, 211–218.Google Scholar
Araújo, R, Serrão, EA, Sousa-Pinto, I, Arenas, F, Monteiro, CA, Toth, G, Pavia, H and Åberg, P (2015) Trade-offs between life-history traits at range-edge and central locations. Journal of Phycology 51, 808–818.CrossRefGoogle ScholarPubMed
Avaca, MS, 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, 567–577.CrossRefGoogle Scholar
Bernardino, AF, Netto, SA, Pagliosa, PR, Barros, F, Christofoletti, RA, Rosa Filho, JS, Colling, A and Lana, PC (2015) Predicting ecological changes on benthic estuarine assemblages through decadal climate trends along Brazilian Marine Ecoregions. Estuarine, Coastal and Shelf Science 166, 74–82.Google Scholar
Blanckenhorn, WU and Demont, M (2004) Bergmann and converse Bergmann latitudinal clines in arthropods: two ends of a continuum? Integrative and Comparative Biology 44, 413–424.CrossRefGoogle ScholarPubMed
Bulleri, F and Chapman, MG (2010) The introduction of coastal infrastructure as a driver of change in marine environments. Journal of Applied Ecology 47, 26–35.CrossRefGoogle Scholar
Cadrin, SX (2000) Advances in morphometric identification of fishery stocks. Reviews in Fish Biology and Fisheries 10, 91–112.CrossRefGoogle Scholar
Casagranda, C and Boudoresque, CF (2002) A sieving method for rapid determination of size-frequency distribution small gastropods. Example of the mud snail Hydrobia ventrosa (Gastropoda: Prosobranchia). Hydrobiologia 5099761, 1–10.Google Scholar
Chapman, MG (1995) Spatial patterns of shell shape of three species of co-existing littorinid snails in New South Wales, Australia. Journal of Molluscan Studies 61, 141–162.CrossRefGoogle Scholar
Chapman, MG (1997) Relationships between shell shape, water reserves, survival and growth of highshore littorinids under experimental conditions in New South Wales, Australia. Journal of Molluscan Studies 63, 511–529.Google Scholar
Chapperon, C, Le Bris, C and Seuront, L (2013) Thermally mediated body temperature, water content and aggregation behaviour in the intertidal gastropod Nerita atramentosa. Ecological Research 28, 407–416.CrossRefGoogle Scholar
Doyle, D, Gammell, MP and Nash, R (2018) Morphometric methods for the analysis and classification of gastropods: a comparison using Littorina littorea. Journal of Molluscan Studies 84, 190–197.CrossRefGoogle Scholar
Fisher, RA (1930) The Genetical Theory of Natural Selection. Oxford: Clarendon Press.CrossRefGoogle Scholar
Goodsell, PJ, Chapman, MG and Underwood, AJ (2007) Differences between biota in anthropogenically fragmented habitats and in naturally patchy habitats. Marine Ecology Progress Series 351, 15–23.CrossRefGoogle Scholar
Grahame, J and Mill, PJ (1989) Shell shape variation in Littorina saxatilis and L. arcana: a case of character displacement. Journal of the Marine Biological Association of the United Kingdom 69, 837–855.CrossRefGoogle Scholar
Han, G, Cartwright, SR, Ganmanee, M, Chan, BKK, Adzis, KAA, Hutchinson, N, Wang, J, Hui, TY, Williams, GA and Dong, Y (2019) High thermal stress responses of Echinolittorina snails at their range edge predict population vulnerability to future warming. Science of the Total Environment 647, 763–771.CrossRefGoogle ScholarPubMed
Hayes, KA, Burks, RL, Castro-Vazquez, A, Darby, PC, Heras, H, Martín, PR, Qiu, J-W, Thiengo, SC, Vega, IA, Wada, T, Yusa, Y, Burela, S, Cadierno, MP, Cueto, JA, Dellagnola, FA, Dreon, MS, Frassa, MV, Giraud-Billoud, M, Godoy, MS, Ituarte, S, Koch, E, Matsukura, K, Pasquevich, MY, Rodriguez, C, Saveanu, L, Seuffert, ME, Strong, EE, Sun, J, Tamburi, NE, Tiecher, MJ, Turner, RL, Valentine-Darby, PL and Cowie, RH (2015) Insights from an integrated view of the biology of apple snails (Caenogastropoda: Ampullariidae). Malacologia 58, 245–302.CrossRefGoogle Scholar
Hollander, J, Collyer, ML, Adams, DC and Johannesson, K (2006) Phenotypic plasticity in two marine snails: constraints superseding life history. Journal of Evolutionary Biology 19, 1861–1872.CrossRefGoogle ScholarPubMed
Ito, A, Ilano, AS, Goshima, S and Nakao, S (2002) Seasonal and tidal-height variations in body weight and radular length in Nodilittorina radiata (Eydoux & Souleyet, 1852). Journal of Molluscan Studies 68, 197–203.CrossRefGoogle Scholar
Johannesson, K (2003) Evolution in Littorina: ecology matters. Journal of Sea Research 49, 107–117.CrossRefGoogle Scholar
Johnson, MS and Black, R (1999) Nodilittorina nodosa (Gray, 1839) is a plastic morphotype of Nodilittorina australis (Gray, 1826). Journal of Molluscan Studies 65, 111–119.CrossRefGoogle Scholar
Keshavarz, M and Jahromi, MS (2017) Effects of primary sex ratio on operational sex ratio in sea urchin, Echinometra mathaei. Pakistan Journal of Zoology 49, 1373–1381.CrossRefGoogle Scholar
Lathlean, JA, Ayre, DJ and Minchinton, TE (2014) Estimating latitudinal variability in extreme heat stress on rocky intertidal shores. Journal of Biogeography 41, 1478–1491.CrossRefGoogle Scholar
Lima, FP, Gomes, F, Seabra, R, Wethey, DS, Seabra, MI, Cruz, T, Santos, AM and Hilbish, TJ (2016) Loss of thermal refugia near equatorial range limits. Global Change Biology 22, 254–263.CrossRefGoogle ScholarPubMed
Linse, K, Barnes, DKA and Enderlein, P (2006) Body size and growth of benthic invertebrates along an Antarctic latitudinal gradient. Deep Sea Research II 53, 921–931.CrossRefGoogle Scholar
Magalhães, CA (1998) Density and shell-size variation of Nodilittorina lineolata (Orbigny, 1840) in the intertidal region in southeastern Brazil. Hydrobiologia 378, 143–148.CrossRefGoogle Scholar
Malvé, ME, Gordillo, S and Rivadeneira, MM (2018) Connecting pH with body size in the marine gastropod Trophon geversianus in a latitudinal gradient along the south-western Atlantic coast. Journal of the Marine Biological Association of the United Kingdom 98, 449–456 doi: https://doi.org/10.1017/S0025315416001557.CrossRefGoogle Scholar
Mayr, E (1956) Geographical character gradients and climatic adaptation. Evolution 10, 105–108.CrossRefGoogle Scholar
Merkt, RE and Ellison, AM (1998) Geographic and habitat-specific morphological variation of Littoraria (Littorinopsis) angulifera (Lamarck, 1822). Malacologia 40, 279–295.Google Scholar
Minton, D and Gochfeld, DJ (2001) Is life on a tropical shore really so hard? The role of abiotic factors in structuring a supralittoral molluscan assemblage. Journal of Shellfish Research 20, 477–483.Google Scholar
Ng, TPT and Williams, GA (2012) Contrasting reproductive traits in two species of mangrove-dwelling littorinid snails in a seasonal tropical habitat. Invertebrate Biology 131, 177–186.CrossRefGoogle Scholar
Ng, TPT, Saltin, SH, Davies, MS, Johannesson, K, Stafford, R and Williams, GA (2013) Snails and their trails: the multiple functions of trail-following in gastropods. Biological Reviews 88, 683–700.CrossRefGoogle ScholarPubMed
Ng, TPT, Davies, MS, Stafford, R and Williams, GA (2016) Fighting for mates: the importance of individual size in mating contests in rocky shore littorinids. Marine Biology 163, 50.CrossRefGoogle Scholar
Olson, VA, Davies, RG, Orme, CDL, Thomas, GH, Meiri, S, Blackburn, TM, Gaston, KJ, Owens, IPF and Bennett, PM (2009) Global biogeography and ecology of body size in birds. Ecology Letters 12, 249–259.CrossRefGoogle ScholarPubMed
Pardal-Souza, AL, Dias, GM, Jenkins, SR, Ciotti, ÁM and Christofoletti, RA (2017) Shading impacts by coastal infrastructure on biological communities from subtropical rocky shores. Journal of Applied Ecology 54, 826–835.CrossRefGoogle Scholar
Pastorino, G (2007) Sexual dimorphism in shells of the southwestern Atlantic gastropod Olivella plata (Ihering, 1908) (Gastropoda: Olividae). Journal of Molluscan Studies 73, 283–285.CrossRefGoogle Scholar
Pie, MR and Traniello, JFA (2007) Morphological evolution in a hyperdiverse clade: the ant genus Pheidole. Journal of Zoology 271, 99–109.CrossRefGoogle Scholar
Proater (2011) Programa De Assistência Técnica E Extensão Rural Proater 2011–2013. Governo do Estado do Espírito Santo.Google Scholar
R Core Team (2018). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. https://www.R-project.org/.Google Scholar
Reid, DG (2009) The genus Echinolittorina Habe, 1956 (Gastropoda: Littorinidae) in the western Atlantic ocean. Zootaxa 2184, 1–103.CrossRefGoogle Scholar
Reid, DG, Dyal, P and Williams, ST (2012) A global molecular phylogeny of 147 periwinkle species (Gastropoda, Littorininae). Zoologica Scripta 41, 125–136.CrossRefGoogle Scholar
Rivest, BR (1983) Development and the influence of nurse egg allotment on hatching size in Searlesia dira (Reeve, 1846) (Prosobranchia: Buccinidae). Journal of Experimental Marine Biology and Ecology 69, 217–241.CrossRefGoogle Scholar
Rocha Filho, CA (1976). Recursos hídricos. Diagnóstico socioeconômico da Região Cacaueira. Rio de Janeiro: IICA/CEPLAC.Google Scholar
Rolán-Alvarez, E (2007) Sympatric speciation as a by-product of ecological adaptation in the Galician Littorina saxatilis hybrid zone. Journal of Molluscan Studies 73, 1–10.CrossRefGoogle Scholar
Roth, VL and Mercer, JM (2000) Morphometrics in development and evolution. American Zoologist 40, 801–810.Google Scholar
Saltin, SH, Schade, H and Johannesson, K (2013) Preference of males for large females causes a partial mating barrier between a large and a small ecotype of Littorina fabalis (W. Turton, 1825). Journal of Molluscan Studies 79, 128–132.CrossRefGoogle Scholar
Santana, SO, Ramos, JV, Ruiz, MA, Araújo, QR, Almeida, HA, Filho, AFF, Mendonça, JR and Santos, LFC (2003) Zoneamento agroecológico do município de Ilhéus, Bahia, Brasil. Boletim Técnico.Google Scholar
Seuront, L and Ng, TPT (2016) Standing in the sun: infrared thermography reveals distinct thermal regulatory behaviours in two tropical high-shore littorinid snails. Journal of Molluscan Studies 82, 336–340.CrossRefGoogle Scholar
Seuront, L, Ng, TPT and Lathlean, JA (2018) A review of the thermal biology and ecology of molluscs, and of the use of infrared thermography in molluscan research. Journal of Molluscan Studies 84, 203–232.CrossRefGoogle Scholar
Silva, SE, Silva, IC, Madeira, C, Sallema, R, Paulo, O and Paula, J (2013) Genetic and morphological variation in two littorinid gastropods: evidence for recent population expansions along the East African coast. Biological Journal of the Linnean Society 108, 494–508.CrossRefGoogle Scholar
Somero, GN (2012) The physiology of global change: linking patterns to mechanisms. Annual Review of Marine Science 4, 39–61.CrossRefGoogle ScholarPubMed
Spalding, MD, Fox, HE, Allen, GR, Davidson, N, Ferdaña, ZA, Finlayson, M, Halpern, BS, Jorge, MA, Lombana, A, Lourie, SA, Martin, KD, McManus, E, Molnar, J, Recchia, CA and Robertson, J (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. BioScience 57, 573–583.CrossRefGoogle Scholar
Stephenson, TA and Stephenson, A (1949) The universal features of zonation between tide-marks on rocky coast. Journal of Ecology 37, 289–305.CrossRefGoogle Scholar
Tanaka, MO and Maia, RC (2006) Shell morphological variation of Littoraria angulifera among and within mangroves in NE Brazil. Hydrobiologia 559, 193–202.CrossRefGoogle Scholar
Trussel, GC (1997) Phenotypic plasticity in the foot size of an intertidal snail. Ecology 78, 1033–1048.CrossRefGoogle Scholar
Trussell, GC (2000) Phenotypic clines, plasticity, and morphological trade-offs in an intertidal snail. Evolution; International Journal of Organic Evolution 54, 151–166.CrossRefGoogle Scholar
Vaquer-Sunyer, R and Duarte, CM (2008) Thresholds of hypoxia for marine biodiversity. PNAS 105, 15452–15457.CrossRefGoogle ScholarPubMed
Vermeij, GJ (1972) Intraspecific shore-level size gradients in intertidal molluscs. Ecology 53, 693–700.CrossRefGoogle Scholar
Walker, T and Grahame, J (2011) Shell shape variation and fitness variables in the gastropod Littorina saxatilis. Marine Ecology Progress Series 430, 103–111.CrossRefGoogle Scholar
Wang, X-G, Johnson, MW, Daane, KM and Yokoyama, VY (2009) Larger olive fruit size reduces the efficiency of Psyttalia concolor, as a parasitoid of the olive fruit fly. Biological Control 49, 45–51.CrossRefGoogle Scholar
West, S (2009). Sex Allocation. Princeton, NJ: Princeton University Press.CrossRefGoogle Scholar
Wickham, H (2016) ggplot2: Elegant Graphics for Data Analysis. New York, NY: Springer-Verlag.CrossRefGoogle Scholar
Yusa, Y (2007) Causes of variation in sex ratio and modes of sex determination in the Mollusca – an overview. American Malacological Bulletin 23, 89–98.CrossRefGoogle Scholar
Yusa, Y, Breton, S and Hoeh, WR (2013) Population genetics of sex determination in Mytilus mussels: reanalyses and a model. Journal of Heredity 104, 380–385.CrossRefGoogle ScholarPubMed
Yusa, Y, Kitaura, J and Cazzaniga, NJ (2016) Variation in the sex ratio of apple snails (Pomacea spp.) in their native range. Malacologia 59, 239–245.CrossRefGoogle Scholar
Zahradnik, TD, Lemay, MA and Boulding, EG (2008) Choosy males in a littorinid gastropod: male Littorina subrotundata prefer large and virgin females. Journal of Molluscan Studies 74, 245–251.CrossRefGoogle Scholar
Zouros, E (2013) Biparental inheritance through uniparental transmission: the doubly uniparental inheritance (DUI) of mitochondrial DNA. Evolutionary Biology 40, 1–31.CrossRefGoogle Scholar
Zuur, AF, Ieno, EN and Elphick, CS (2010) A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution 1, 3–14.CrossRefGoogle Scholar
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