Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-26T06:13:09.778Z Has data issue: false hasContentIssue false
  • English
  • Français

Shell shape, morphometrics and relative growth of four sympatric limpet species from the Algarve coast (southern Portugal)

Published online by Cambridge University Press:  09 November 2021

Paulo Vasconcelos Open the ORCID record for Paulo Vasconcelos [Opens in a new window] ,
Flávio Janeiro ,
Fábio Pereira ,
Paula Moura ,
André N. Carvalho  and
Miguel B. Gaspar
Paulo Vasconcelos*
Affiliation:
Instituto Português do Mar e da Atmosfera (IPMA), Avenida 5 de Outubro s/n, 8700-305 Olhão, Portugal
Flávio Janeiro
Affiliation:
Instituto Português do Mar e da Atmosfera (IPMA), Avenida 5 de Outubro s/n, 8700-305 Olhão, Portugal
Fábio Pereira
Affiliation:
Instituto Português do Mar e da Atmosfera (IPMA), Avenida 5 de Outubro s/n, 8700-305 Olhão, Portugal
Paula Moura
Affiliation:
Instituto Português do Mar e da Atmosfera (IPMA), Avenida 5 de Outubro s/n, 8700-305 Olhão, Portugal
André N. Carvalho
Affiliation:
Instituto Português do Mar e da Atmosfera (IPMA), Avenida 5 de Outubro s/n, 8700-305 Olhão, Portugal
Miguel B. Gaspar
Affiliation:
Instituto Português do Mar e da Atmosfera (IPMA), Avenida 5 de Outubro s/n, 8700-305 Olhão, Portugal Centro de Ciências do Mar (CCMAR), Universidade do Algarve, Campus de Gambelas, 8005-139 Faro, Portugal
*
Author for correspondence: Paulo Vasconcelos, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

This study analysed and compared the shell shape, morphometrics and relative growth of four sympatric limpet species (Patella depressa, Patella ulyssiponensis, Patella vulgata and Siphonaria pectinata) collected at Praia da Luz in Lagos (Algarve coast – southern Portugal). Morphometric relationships were established through regression analysis between linear (shell length, width and height), ponderal (total weight), area (shell base and surface areas) and volume variables (shell internal and total volumes). Relative growth (isometry vs allometry) was analysed to assess variation in the growth rate of morphometric variables throughout the species ontogeny. In addition, morphometric indices (ellipticity, conicity, density, surface area and volumetry) were calculated to further characterize shell shape. Overall, 1482 individuals with broad size and weight ranges were analysed (P. depressa = 354; P. ulyssiponensis = 306; P. vulgata = 408; S. pectinata = 414). All regressions were highly significant (P < 0.001) and the morphometric variables were strongly correlated (r = 0.761 to 0.994). Among 28 morphometric relationships, there were 14 isometries, 13 positive allometries and only one negative allometry. The morphometric indices revealed clear morphological differences between species and were mostly size-dependent, reflecting gradual changes in shell shape during growth. The main results are compared with a compilation of analogous data reported for these limpet species throughout their distributional range. Overall, the general trends in relative growth are discussed in terms of the species life habits, main traits and functional morphology.

Keywords

Algarve coastallometryGastropodaisometrymorphometric indicesmorphometric relationshipsPatellidaeshell morphologySiphonariidaesouthern Portugal
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 101 , Issue 5 , August 2021 , pp. 791 - 800
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

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.)

Footnotes

*

These authors contributed equally to this work and should be considered co-first authors of the article

References

Anderson, R and Gutreuter, S (1983) Length, weight, and associated structural indices. In Nielsen, L and Johnson, D (eds), Fisheries Techniques. Bethesda, MD: American Fisheries Society, pp. 283–300.Google Scholar
Antit, S, Gofas, S and Azzouna, A (2008) New records of upper shore Mollusca for the Tunisian coast: newcomers or overlooked? Marine Biodiversity Records 1, e99.CrossRefGoogle Scholar
Balaparameswara Rao, M and Ganapati, PN (1971) Ecological studies on a tropical limpet, Cellana radiata: structural variations in the shell in relation to distribution. Marine Biology 10, 236–243.CrossRefGoogle Scholar
Ballantine, WJ (1961) A biologically-defined exposure scale for the comparative description of rocky shores. Field Studies 1, 1–17.Google Scholar
Bannister, JV (1975) Shell parameters in relation to zonation in Mediterranean limpets. Marine Biology 31, 63–67.CrossRefGoogle Scholar
Battelli, C (2016) Morphometric characteristics, vertical distribution and density of the limpet Patella caerulea L. in relation to different substrata of the Bay of Koper (Gulf of Trieste, Northern Adriatic). Annales. Series Historia Naturalis 26, 145–156.Google Scholar
Baxter, JM (1983) Allometric relationships of Patella vulgata L. shell characters at three adjacent sites at Sandwick Bay in Orkney. Journal of Natural History 17, 743–755.CrossRefGoogle Scholar
Bicho, N and Haws, J (2008) At the land's end: marine resources and the importance of fluctuations in the coastline in the prehistoric hunter–gatherer economy of Portugal. Quaternary Science Reviews 27, 2166–2175.CrossRefGoogle Scholar
Boaventura, D (2000) Patterns of distribution in intertidal rocky shores: the role of grazing and competition in structuring communities. PhD thesis, Universidade do Algarve, Portugal, 149 pp.Google Scholar
Boaventura, D, Ré, P, Cancela da Fonseca, L and Hawkins, SJ (2002) Intertidal rocky shore communities of the continental Portuguese coast: analysis of distribution patterns. Marine Ecology 23, 69–90.CrossRefGoogle Scholar
Boaventura, D, Cancela da Fonseca, L and Hawkins, SJ (2003) Size matters: competition within populations of the limpet Patella depressa. Journal of Animal Ecology 72, 435–446.CrossRefGoogle Scholar
Borges, CDG, Doncaster, CP, MacLean, MA and Hawkins, SJ (2015) Broad-scale patterns of sex ratios in Patella spp.: a comparison of range edge and central range populations in the British Isles and Portugal. Journal of the Marine Biological Association of the United Kingdom 95, 1141–1153.CrossRefGoogle Scholar
Boukhicha, J, Ben Hassine, OK and Tlig-Zouari, S (2013) Morphological evidence for adaptive diversification of sympatric Mediterranean Patella limpets. Rapports de la Commission Internationale pour l'Exploration Scientifique de la Mer Méditerranée 40, 686.Google Scholar
Bouzaza, Z and Mezali, K (2018) Discriminant-based study of the shell morphometric relationships of Patella caerulea (Gastropoda: Prosobranchia) of the western Mediterranean Sea. Turkish Journal of Zoology 42, 513–522.CrossRefGoogle Scholar
Branch, GM and Marsh, AC (1978) Tenacity and shell shape in six Patella species: adaptive features. Journal of Experimental Marine Biology and Ecology 34, 111–130.CrossRefGoogle Scholar
Burgos-Rubio, V, De la Rosa, J, Altamirano, M and Espinosa, F (2015) The role of patellid limpets as omnivorous grazers: a new insight into intertidal ecology. Marine Biology 162, 2093–2106.CrossRefGoogle Scholar
Cabral, JP (2003) Characterization and multivariate analysis of Patella intermedia, Patella ulyssiponensis and Patela vulgata from Póvoa de Varzim (Northwest Portugal). Iberus 21, 1–17.Google Scholar
Cabral, JP (2007) Shape and growth in European Atlantic Patella limpets (Gastropoda, Mollusca). Ecological implications for survival. Web Ecology 7, 11–21.CrossRefGoogle Scholar
Cabral, JP and Natal Jorge, RM (2007) Compressibility and shell failure in the European Atlantic Patella limpets. Marine Biology 150, 585–597.CrossRefGoogle Scholar
Cabral, JP and Silva, ACF (2003) Morphometric analysis of limpets from an iron-age shell midden found in northwest Portugal. Journal of Archaeological Science 30, 817–829.CrossRefGoogle Scholar
Cañizares, JM, Castejón, D, Haroun, R, Nogueira, N and Andrade, CAP (2021) Enhancing oocyte maturation and fertilisation in the black-foot limpet Patella candei d′Orbigny, 1840 (Patellidae, Mollusca). Aquaculture Reports 21, 100856.CrossRefGoogle Scholar
Casal, G, Aceña-Matarranz, S, Fernández-Márquez, D and Fernández, N (2018) Distribution and abundance patterns of three coexisting species of Patella (Mollusca: Gastropoda) in the intertidal areas of the NW Iberian Peninsula: implications for management. Fisheries Research 198, 86–98.CrossRefGoogle Scholar
Christiaens, J (1973) Révision du genre Patella (Mollusca, Gastropoda). Bulletin du Muséum National d'Histoire Naturelle, 3e série, Part Zoologie 182, 1305–1392.Google Scholar
Coleman, RA, Underwood, AJ, Benedetti-Cecchi, L, Åberg, P, Arenas, F, Arrontes, J, Castro, J, Hartnoll, RG, Jenkins, SR, Paula, J, Della Santina, P and Hawkins, SJ (2006) A continental scale evaluation of the role of limpet grazing on rocky shores. Oecologia 147, 556–564.CrossRefGoogle ScholarPubMed
Côrte-Real, HBSM, Hawkins, SJ and Thorpe, JP (1996) Population differentiation and taxonomic status of the exploited limpet Patella candei in the Macaronesian islands (Azores, Madeira, Canaries). Marine Biology 125, 141–152.CrossRefGoogle Scholar
Crocetta, F (2016) Backdating the confirmed presence of Siphonaria pectinata (Gastropoda: Siphonariidae) along the northern Mediterranean shores and a discussion on its status in the basin. Marine Biodiversity Records 9, 55.CrossRefGoogle Scholar
Diogo, H, Pereira, JG and Schmiing, M (2016) Catch me if you can: non-compliance of limpet protection in the Azores. Marine Policy 63, 92–99.CrossRefGoogle Scholar
Fa, DA, Finlayson, JC, Finlayson, G, Giles-Pacheco, F, Rodríguez-Vidal, J and Gutiérrez-López, JM (2016) Marine mollusc exploitation as evidenced by the Gorham's Cave (Gibraltar) excavations 1998–2005: the middle–upper palaeolithic transition. Quaternary International 407(Part B), 16–28.CrossRefGoogle Scholar
Faria, J, Martins, GM, Pita, A, Ribeiro, PA, Hawkins, SJ, Presa, P and Neto, AI (2017) Disentangling the genetic and morphological structure of Patella candei complex in Macaronesia (NE Atlantic). Ecology and Evolution 7, 6125–6140.CrossRefGoogle Scholar
Fretter, V and Graham, A (1976) The prosobranch molluscs of Britain and Denmark. I. Pleurotomariacea, Fissurellacea, and Patellacea. Journal of Molluscan Studies Special Edition, Suppl. 1, 37.Google Scholar
Gaspar, MB, Santos, MN and Vasconcelos, P (2001) Weight-length relationships of 25 bivalve species (Mollusca: Bivalvia) from the Algarve coast (southern Portugal). Journal of the Marine Biological Association of the United Kingdom 81, 805–807.CrossRefGoogle Scholar
Gaspar, MB, Santos, MN, Vasconcelos, P and Monteiro, CC (2002) Shell morphometric relationships of the most common bivalve species (Mollusca: Bivalvia) of the Algarve coast (southern Portugal). Hydrobiologia 477, 73–80.CrossRefGoogle Scholar
Grenon, J-F and Walker, G (1981) The tenacity of the limpet, Patella vulgata L.: an experimental approach. Journal of Experimental Marine Biology and Ecology 54, 277–308.CrossRefGoogle Scholar
Guerra, MT and Gaudêncio, MJ (1986) Aspects of the ecology of Patella spp. on the Portuguese coast. Hydrobiologia 142, 57–69.CrossRefGoogle Scholar
Harley, CDG, Denny, MW, Mach, JK and Miller, LP (2009) Thermal stress and morphological adaptations in limpets. Functional Ecology 23, 292–301.CrossRefGoogle Scholar
Henriques, P, Sousa, R, Pinto, AR, Delgado, J, Faria, G, Alves, A and Khadem, M (2012) Life history traits of the exploited limpet Patella candei (Mollusca: Patellogastropoda) of the north-eastern Atlantic. Journal of the Marine Biological Association of the United Kingdom 92, 1379–1387.CrossRefGoogle Scholar
Henriques, P, Delgado, J and Sousa, R (2017) Patellid limpets: an overview of the biology and conservation of keystone species of the rocky shores. In Ray, S (ed.), Organismal and Molecular Malacology. Rijeka: IntechOpen, pp. 71–95.Google Scholar
Huxley, JS (1932) Problems of Relative Growth. Baltimore, MD: Johns Hopkins University Press.Google Scholar
Huxley, JS and Teissier, G (1936) Terminology of relative growth. Nature 137, 780–781.CrossRefGoogle Scholar
Jenkins, SR, Coleman, RA, Santina, PD, Hawkins, SJ, Burrows, MT and Hartnoll, RG (2005) Regional scale differences in determinism of grazing effects in the rocky intertidal. Marine Ecology Progress Series 287, 77–86.CrossRefGoogle Scholar
Jones, AM, Jones, YM and Baxter, JM (1979) Seasonal and annual variations in the allometric relationships of shell and soft-body characters of Patella vulgata L. In Naylor, E and Hartnoll, RG (eds), Cyclic Phenomena in Marine Plants and Animals. Proceedings of the 13th European Marine Biology Symposium, Isle of Man, 27 September–4 October 1978. Oxford: Pergamon Press, pp. 199–206.CrossRefGoogle Scholar
Khouw, AS (2006) Shell shape variation of tropical limpet Cellana testudinaria (Class: Gastropoda, Family: Patellidae) living on the rocky shore in relation to their zonal distribution. Ilmu Kelautan: Indonesian Journal of Marine Sciences 11, 171–180.Google Scholar
Lomovasky, BJ, de Aranzamendi, MC and Abele, D (2020) Shorter but thicker: analysis of internal growth bands in shells of intertidal vs subtidal Antarctic limpets, Nacella concinna, reflects their environmental adaptation. Polar Biology 43, 131–141.CrossRefGoogle Scholar
Lowell, RB (1984) Desiccation of intertidal limpets: effects of shell size, fit to substratum, and shape. Journal of Experimental Marine Biology and Ecology 77, 197–207.CrossRefGoogle Scholar
Martins, GM, Jenkins, SR, Hawkins, SJ, Neto, AI, Medeiros, AR and Thompson, RC (2011) Illegal harvesting affects the success of fishing closure areas. Journal of the Marine Biological Association of the United Kingdom 91, 929–937.CrossRefGoogle Scholar
Martins, GM, Borges, CDG, Vale, M, Ribeiro, PA, Ferraz, RR, Martins, HR, Santos, RS and Hawkins, SJ (2017) Exploitation promotes earlier sex change in a protandrous patellid limpet, Patella aspera Röding, 1798. Ecology and Evolution 7, 3616–3622.CrossRefGoogle Scholar
Mauro, A, Arculeo, M and Parrinello, N (2003) Morphological and molecular tools in identifying the Mediterranean limpets Patella caerulea, Patella aspera and Patella rustica. Journal of Experimental Marine Biology and Ecology 295, 131–143.CrossRefGoogle Scholar
Mayrat, A (1970) Allométrie et taxinomie. Révue de Statistique Appliquée 18, 47–58.Google Scholar
Nolan, CP (1991) Size, shape, and shell morphology in the Antarctic limpet Nacella concinna at Signy Island, South Orkney Islands. Journal of Molluscan Studies 57, 225–238.CrossRefGoogle Scholar
Ocaña, TMJ (2003) Growth, mortality and longevity in two populations of Siphonaria pectinata (Pulmonata) at Gibraltar. Journal of Molluscan Studies 69, 162–164.CrossRefGoogle Scholar
Orton, JH (1928) Observations on Patella vulgata. Part I. Sex-phenomena, breeding and shell-growth. Journal of the Marine Biological Association of the United Kingdom 15, 851–862.CrossRefGoogle Scholar
Richter, HC, Luckstadt, C, Focken, U and Becker, K (2000) An improved procedure to assess fish condition on the basis of length-weight relationships. Archive of Fishery and Marine Research 48, 255–264.Google Scholar
Santos, RS, Hawkins, S, Monteiro, LR, Alves, M and Isidro, EJ (1995) Marine research, resources and conservation in the Azores. Aquatic Conservation: Marine and Freshwater Ecosystems 5, 311–354.CrossRefGoogle Scholar
Silva, ACF, Hawkins, SJ, Boaventura, DM and Thompson, RC (2008) Predation by small mobile aquatic predators regulates populations of the intertidal limpet Patella vulgata (L.). Journal of Experimental Marine Biology and Ecology 367, 259–265.CrossRefGoogle Scholar
Simone, LRL and Seabra, MIGL (2017) Shell and body structure of the plesiomorphic pulmonate marine limpet Siphonaria pectinata (Linnaeus, 1758) from Portugal (Gastropoda: Heterobranchia: Siphonariidae). Folia Malacologia 25, 147–164.CrossRefGoogle Scholar
Sokal, RR and Rohlf, FJ (1987) Introduction to Biostatistics, 2nd Edn. New York, NY: Freeman.Google Scholar
Sousa, R, Vasconcelos, J, Henriques, P, Pinto, AR, Delgado, J and Riera, R (2019 a) Long-term population status of two harvested intertidal grazers (Patella aspera and Patella candei), before (1996–2006) and after (2007–2017) the implementation of management measures. Journal of Sea Research 144, 33–38.CrossRefGoogle Scholar
Sousa, R, Vasconcelos, J, Riera, R, Pinto, AR, Delgado, J and Henriques, P (2019 b) Potential impact of harvesting management measures on the reproductive parameters of the limpets Patella aspera and Patella candei from Madeira Island. Estuarine, Coastal and Shelf Science 226, 106264.CrossRefGoogle Scholar
Sousa, R, Riera, R, Vasconcelos, J, Gouveia, L, Pinto, AR, Delgado, J, Alves, A, González, JA, Freitas, M and Henriques, P (2020 a) Artisanal harvest of shellfish in the Northeastern Atlantic: the example of limpet and topshell fisheries in the archipelago of Madeira. In Ray, S, Diarte-Plata, G and Escamilla-Montes, R (eds), Invertebrates: Ecophysiology and Management. Rijeka: IntechOpen, pp. 147–164.Google Scholar
Sousa, R, Henriques, P, Vasconcelos, J, Pinto, AR, Delgado, J and Riera, R (2020 b) The protection effects of marine protected areas on exploited molluscs from an oceanic archipelago. Aquatic Conservation: Marine and Freshwater Ecosystems 30, 717–729.CrossRefGoogle Scholar
Sousa, R, Pinto, AR, Vasconcelos, J and Riera, R (2020 c) Does harvesting affect the relative growth in Patella aspera Röding, 1798? European Zoological Journal 87, 395–401.CrossRefGoogle Scholar
Southward, AJ, Hawkins, SJ and Burrows, MT (1995) Seventy years’ observations of changes in distribution and abundance of zooplankton and intertidal organisms in the western English Channel in relation to rising sea temperature. Journal of Thermal Biology 20, 127–155.CrossRefGoogle Scholar
Titselaar, FFLM (1998) A revision of the recent European Patellidae (Mollusca: Gastropoda) – Part 1. The Patellidae of the Azores, Madeira, the Selvagens and the Canary Islands. Vita Marina 45, 21–62.Google Scholar
Vafidis, D, Drosou, I, Dimitriou, K and Klaoudatos, D (2020) Population characteristics of the limpet Patella caerulea (Linnaeus, 1758) in Eastern Mediterranean (Central Greece). Water 12, 1186.CrossRefGoogle Scholar
Vasconcelos, P, Barroso, CM and Gaspar, MB (2016) Morphometric relationships and relative growth of Hexaplex trunculus and Bolinus brandaris (Gastropoda: Muricidae) from the Ria Formosa lagoon (southern Portugal). Journal of the Marine Biological Association of the United Kingdom 96, 1417–1425.CrossRefGoogle Scholar
Vasconcelos, P, Moura, P, Pereira, F, Pereira, AM and Gaspar, MB (2018 a) Morphometric relationships and relative growth of twenty uncommon bivalve species from the Algarve coast (southern Portugal). Journal of the Marine Biological Association of the United Kingdom 98, 463–474.CrossRefGoogle Scholar
Vasconcelos, P, Pereira, F, Carvalho, AN and Gaspar, MB (2018 b) Weight-length relationships and relative growth of the cuttlefish (Sepia officinalis): causes and effects of hypoallometry. Thalassas: An International Journal of Marine Sciences 34, 323–331.CrossRefGoogle Scholar
Vasconcelos, P, Umapathy, U, Moura, P, Pereira, F, Carvalho, AN and Gaspar, MB (2019) Size at sex change and reproductive cycle of the limpets Patella vulgata and Patella ulyssiponensis (Mollusca: Patellogastropoda) from intertidal rocky shores of the Algarve coast (southern Portugal). Invertebrate Reproduction & Development 63, 294–308.CrossRefGoogle Scholar
Vasconcelos, P, Santos, ACN, Pereira, F, Moura, P, Carvalho, AN and Gaspar, MB (2022) Shell morphology, morphometric relationships and relative growth of three topshell species (Gastropoda: Trochidae) from the Algarve coast (southern Portugal). Thalassas: An International Journal of Marine Sciences 38, in press.Google Scholar
Verdún-Castelló, E and Casabó i Bernad, J (2020) Shellfish consumption in the Early Upper Palaeolithic on the Mediterranean coast of the Iberian Peninsula: the example of Foradada Cave. Journal of Archaeological Science: Reports 29, 102035.Google Scholar
Vermeij, GJ (1973) Morphological patterns in high-intertidal gastropods: adaptive strategies and their limitations. Marine Biology 20, 319–346.CrossRefGoogle Scholar
WoRMS Editorial Board (2021) World Register of Marine Species. Available from VLIZ at http://www.marinespecies.org (accessed 1 July 2021).Google Scholar
Zischke, JA, Watabe, N and Wilbur, K (1970) Studies on shell formation: measurement of growth in the gastropod Ampullarius glaucus. Malacologia 10, 423–439.Google Scholar