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Influence of macroalgal morphology on the functional structure of molluscan community from hypersaline estuary

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Abstract

Studies based on functional approach seek to understand the ecological roles developed by species as well as their interactions with the environment in which they are inserted. The hypothesis tested was that functional richness and diversity of molluscan community will be higher at the most complex macroalgal habitat. The study was carried out at Casqueira river estuary (Rio Grande do Norte, Brazil). Three species of macroalgae were collected—Gracilaria domingensis (Kützing) Sonder ex Dickie 1874, Gracilaria cuneata Areschoug 1854, and Solieria filiformis (Kützing) P.W.Gabrielson 1985—and the composition of seven functional traits of the mollusk fauna associated to the algae was characterized in 22 categories. The highest values of functional richness and diversity were for macroalgae with greater habitat complexity (G. domingensis). Some functional traits were influenced more by macroalgal morphology, like ‘life way,’ feeding strategy, body size, and larval development. Thus, we show that the greatest richness and functional diversity of the communities is related to sites with more complex habitat, sites with more shelter and refuge, and food. This highlights the importance of the quality of habitat for shellfish communities and shows that it can be assessed from the use of a functional approach.

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References

  • Alongi, D. M., 2009. Paradigm shifts in mangrove biology. In Perillo, G. M. E., E. Wolanski, D. R. Cahoon & M. M. Brinson (eds), Coastal Wetlands an Integrated Ecosystem Approach. Elsevier, Amsterdam: 615–640.

    Google Scholar 

  • Alves, M. S. & M. J. G. Araújo, 1999. Moluscos associados ao fital de Halodule wrightii Aschers na Ilha de Itamaracá—PE. Tropical Oceanography 27(1): 91–99.

    Google Scholar 

  • Arruda, E. P., O. Domaneschi & A. C. Z. Amaral, 2003. Mollusc feeding guilds on sandy beaches in São Paulo State, Brazil. Marine Biology 143: 691–701.

    Google Scholar 

  • Backes, A. R. & O. M. Bruno, 2005. Técnicas de estimativa da dimensão fractal: um estudo comparativo. INFOCOMP Journal of Computer Science 4: 50–58.

    Google Scholar 

  • Bady, P., S. Dolédec, C. Fesl, S. Gayraud, M. Bacchi & F. Schöll, 2005. Use of invertebrate traits for the biomonitoring of European large rivers: the effects of sampling effort on genus richness and functional diversity. Freshwater Biology 50: 159–173.

    Google Scholar 

  • Barbosa, D. F., T. L. P. Dias, S. F. Lopes, R. C. S. Duarte & F. M. D. Amaral, 2019. Community structure and functional traits of mollusks associated with coastal reef macroalgae in Northeastern Brazil. Marine Ecology 40: e12563.

    Google Scholar 

  • Botta-Dukát, Z., 2005. Rao’s quadratic entropy as a measure of functional diversity based on multiple traits. Journal of Vegetation Science 16: 533–540.

    Google Scholar 

  • Breine, N. T., A. De Backer, C. Van Colen, T. Moens, K. Hostens & G. Van Hoey, 2018. Structural and functional diversity of soft-bottom macrobenthic communities in the Southern North Sea. Estuarine, Coastal and Shelf Science 214: 173–184.

    Google Scholar 

  • Brown, B. L., 2007. Habitat heterogeneity and disturbance influence patterns of community temporal variability in a small temperate stream. Hydrobiologia 586: 93–106.

    Google Scholar 

  • Cacabelos, E., C. Olabarria, M. Incera & J. S. Troncoso, 2010. Effects of habitat structure and tidal height on epifaunal assemblages associated with macroalgae. Estuarine, Coastal and Shelf Science 89: 43–52.

    Google Scholar 

  • Cadotte, M. W., K. Carscadden & N. Mirotchnick, 2011. Beyond species: functional diversity and the maintenance of ecological processes and services. Journal of Applied Ecology 48: 1079–1087.

    Google Scholar 

  • Calapez, A. R., S. R. Q. Serra, J. M. Santos, P. Branco, T. Hein, A. G. Brito & M. J. Feio, 2018. The effect of hypoxia and flow decrease in macroinvertebrate functional responses: a trait-based approach to multiple-stressors in mesocosms. Science of the Total Environment 637–638: 647–656.

    Google Scholar 

  • Chapin, F. S., B. H. Walker, R. J. Hobbs, D. U. Hooper, J. H. Lawton, O. E. Sala & D. Tilman, 1997. Biotic control over the functioning of ecosystems. Science 277: 500–504.

    CAS  Google Scholar 

  • Chemello, R. & M. Milazzo, 2002. Effect of algal architecture on associated fauna: some evidence from phytal molluscs. Marine Biology 140: 981–990.

    Google Scholar 

  • Chen, Q., Q. Zhao, S. Jian & P. Chen, 2018. Changes in the functional feeding groups of macrobenthic fauna during mangrove forest succession in Zhanjiang, South China. Ecological Research 33: 959–970.

    Google Scholar 

  • Chittaro, P. M., 2004. Fish-habitat associations across multiple spatial scales. Coral Reefs 23: 235–244.

    Google Scholar 

  • Christie, H., N. M. Jørgensen & K. M. Norderhaug, 2007. Bushy or smooth, high or low: importance of habitat architecture and vertical position for distribution of fauna on kelp. Journal of Sea Research 58: 198–208.

    Google Scholar 

  • Christie, H., K. M. Norderhaug & S. Fredriksen, 2009. Macrophytes as habitat for fauna. Marine Ecology Progress Series 396: 221–234.

    Google Scholar 

  • Curley, B. G., M. J. Kingsford & B. M. Gillanders, 2002. Spatial and habitat-related patterns of temperate reef fish assemblages: implications for the design of marine protected areas. Marine and Freshwater Research 53: 1197–1210.

    Google Scholar 

  • Dayton, P. K., 1971. Competition, disturbance, and community organization: the provision and subsequent utilization of space in a rocky intertidal community. Ecological Monographs 41: 351–389.

    Google Scholar 

  • Dias, T. L. P. & E. L. S. Mota, 2015. First record of Cassis tuberosa spawning in the wild (north-east Brazil). Marine Biodiversity Records 8: 1–3.

    Google Scholar 

  • Dimitriadis, C., A. Evagelopoulos & D. Koutsoubas, 2012. Functional diversity and redundancy of soft bottom communities in brackish waters areas: local vs regional effects. Journal of Experimental Marine Biology and Ecology 426: 53–59.

    Google Scholar 

  • Dolédec, S., B. Statzner & M. Bournard, 1999. Species traits for future biomonitoring across ecoregions: patterns along a human-impacted river. Freshwater Biology 42: 737–758.

    Google Scholar 

  • Duarte, R. C., E. L. Mota & T. L. P. Dias, 2014. Mollusk fauna from shallow-water back reef habitats of Paraíba coast, northeastern Brazil. Strombus 21: 15–29.

    Google Scholar 

  • Duarte, R. C. S., E. L. S. Mota, I. C. Almeida, A. L. M. Pessanha, M. L. Christoffersen & T. L. P. Dias, 2015. Gastropods associated to three reef macroalgae with different architectures. Strombus 22: 5–18.

    Google Scholar 

  • Edgar, G. J., 1983. The ecology of south-east Tasmanian phytal animal communities I. Spatial organization on a local scale. Journal of Experimental Marine Biology and Ecology 70: 129–157.

    Google Scholar 

  • Garcia, A. F., M. Bueno & F. P. P. Leite, 2016. The Bostrychietum community of pneumathofores in Araça Bay: an analysis of the diversity of macrofauna. Journal of the Marine Biological Association of the United Kingdom 96: 1617–1624.

    Google Scholar 

  • Gibson, R., M. Barnes & R. Atkison, 2001. Functional group ecology in soft-sediment marine benthos: the role of bioturbation. Oceanography and Marine Biology 39: 233–267.

    Google Scholar 

  • Heller, J., 1990. Longevity in molluscs. Malacologia 31: 259–295.

    Google Scholar 

  • IDEMA – Instituto de Desenvolvimento Econômico e Meio Ambiente do Rio Grande do Norte, 2004. Mapeamento geoambiental da Reserva de Desenvolvimento Sustentável Ponta do Tubarão. Relatório Técnico, Natal, Brasil: 23p.

    Google Scholar 

  • Ilarri, M. I., L. Amorim, A. T. Souza & R. Sousa, 2018. Physical legacy of freshwater bivalves: effects of habitat complexity on the taxonomical and functional diversity of invertebrates. Science of the Total Environment 634: 1398–1405.

    CAS  Google Scholar 

  • INMET—Instituto Nacional de Meteorologia, 2015. http://www.inmet.gov.br/portal/. Accessed 15 Jan 2016.

  • Jelinek, H., D. Cornforth & L. Weymouth, 2003. Fractop v. 0.3. http://seal.tst.adfa.edu.au/fractop. Accessed 15 April 2016.

  • Kovalenko, K., E. Dibble & R. Fugi, 2009. Fish feeding in changing habitats: effects of invasive macrophyte control and habitat complexity. Ecology of Freshwater Fish 18: 305–313.

    Google Scholar 

  • Laliberté, E., P. Legendre & B. Shipley, 2014. FD: measuring functional diversity from multiple traits, and other tools for functional ecology. R package version 1.0-12. https://cran.r-project.org/web/packages/FD/. Accessed 20 Feb 2017.

  • Legendre, P., R. Galzin & M. L. Harmelin-Vivien, 1997. Relating behavior to habitat: solutions to the fourth-corner problem. Ecology 78: 547–562.

    Google Scholar 

  • Lucena, L.A.F., 2012. Estrutura e composição de macroalgas de manguezais hipersalinos do Rio Grande do Norte, Brasil: diversidade e suas correlações com as variáveis ambientais. MSc thesis, Programa de Pós-Graduação em Ecologia e Conservação, Universidade Estadual da Paraíba.

  • MacArthur, R. H., 1965. Patterns of species diversity. Biological Reviews 40: 510–533.

    Google Scholar 

  • Macdonald, T. A., B. Burd, V. Macdonald & A. Van Roodselaar, 2010. Taxonomic and feeding guild classification for the marine benthic macroinvertebrates of the Strait of Georgia, British Columbia. Canadian Technical Report of Fisheries and Aquatic Sciences 2874: 1–63.

    Google Scholar 

  • Marina, P., J. Urra, J. L. Rueda & C. Salas, 2012. Composition and structure of the molluscan assemblage associated with a Cymodocea nodosa bed in south-eastern Spain: seasonal and diel variation. Helgoland Marine Research 66: 585–599.

    Google Scholar 

  • Matthews-Cascon, H., C. A. Rocha-Barreira, P. Penchaszadeh & G. Bigatti, 2010. Description of egg capsules of Voluta ebraea Linnaeus, 1758 (Gastropoda: Neogastropoda). Comunicaciones de la Sociedad Malacológica del Uruguay 93: 237–244.

    Google Scholar 

  • McAbendroth, L., P. Ramsay, A. Foggo, S. Rundle & D. Bilton, 2005. Does macrophyte fractal complexity drive invertebrate diversity, biomass and body size distributions? Oikos 111: 279–290.

    Google Scholar 

  • Petchey, O. L. & K. J. Gaston, 2006. Functional diversity: back to basics and looking forward. Ecology Letters 9: 741–758.

    PubMed  Google Scholar 

  • Piló, D., R. Ben-Hamadou, F. Pereira, A. Carriço, P. Pereira, A. Corzo, M. Gaspar & S. Carvalho, 2016. How functional traits of estuarine macrobenthic assemblages respond to metal contamination? Ecological Indicators 71: 645–659.

    Google Scholar 

  • Queiroz, R. & T. L. P. Dias, 2014. Molluscs associated with the macroalgae of the genus Gracilaria (Rhodophyta): importance of algal fronds as microhabitat in a hypersaline mangrove in Northeastern Brazil. Brazilian Journal of Biology 74: S052–S063.

    Google Scholar 

  • Reiss, H., S. Degraer, G. C. Duineveld, I. Kröncke, J. Aldridge, J. A. Craeymeersch, J. D. Eggleton, H. Hillewaert, M. S. Lavaleye & A. Moll, 2009. Spatial patterns of infauna, epifauna, and demersal fish communities in the North Sea. ICES Journal of Marine Science 67: 278–293.

    Google Scholar 

  • Rios, E. C., 2009. Compendium of Brazilian Seashells. Editora da FURG, Rio Grande: 668.

    Google Scholar 

  • Rubal, M., R. Costa-Garcia, C. Besteiro, I. Sousa-Pinto & P. Veiga, 2018. Mollusc diversity associated with the non-indigenous macroalga Asparagopsis armata Harvey, 1855 along the Atlantic coast of the Iberian Peninsula. Marine Environmental Research 136: 1–7.

    CAS  PubMed  Google Scholar 

  • Rueda, J. L., S. Gofas, J. Urra & C. Salas, 2009. A highly diverse molluscan assemblage associated with eelgrass beds (Zostera marina L.) in the Alboran Sea: micro-habitat preference, feeding guilds and biogeographical distribution. Scientia Marina 73: 679–700.

    Google Scholar 

  • Savenije, H. H. G. & J. Pagès, 1992. Hypersalinity: a dramatic change in the hydrology of Sahelian estuaries. Journal of Hydrology 135: 157–174.

    CAS  Google Scholar 

  • Tano, S., M. Eggertsen, S. A. Wikström, C. Berkström, A. Buriyo & C. Halling, 2016. Tropical seaweed beds are important habitats for mobile invertebrate epifauna. Estuarine, Coastal and Shelf Science 183: 1–12.

    Google Scholar 

  • Tilman, D., 2001. Functional diversity. In Levin, S. A. (ed.), Encyclopedia of Biodiversity. Academic Press, San Diego: 109–120.

    Google Scholar 

  • Tilman, D., J. Knops, D. Wedin, P. Reich, M. Ritchie & E. Siemann, 1997. The influence of functional diversity and composition on ecosystem processes. Science 277: 1300–1302.

    CAS  Google Scholar 

  • Torres, A. C., P. Veiga, M. Ruball & I. Sousa-Pinto, 2015. The role of annual macroalgal morphology in driving its epifaunal assemblages. Journal of Experimental Marine Biology and Ecology 464: 96–106.

    Google Scholar 

  • Tunnell, J. W., J. Andrews, N. C. Barrera & F. Moretzsohn, 2010. Encyclopedia of Texas Seashells: Identification, Ecology, Distribution, and History. Texas A&M University Press, Corpus Christi: 512.

    Google Scholar 

  • Turgeon, D. D., W. G. Lyons, P. Mikkelsen, G. Rosenberg, F. Moretzsohn, D. Felder & D. Camp, 2009. Bivalvia (Mollusca) of the Gulf of Mexico. In Felder, D. L. & D. K. Camp (eds), Gulf of Mexico: Origin, Waters, and Biota. Texas A&M University, College Station: 711–744.

    Google Scholar 

  • Valle-Levinson, A., 2011. Classification of Estuarine circulation. In Wolanski, E. & D. S. McLusky (eds), Treatise on Estuarine and Coastal Science, Vol. 1. Academic Press, Waltham: 75–86.

    Google Scholar 

  • Van der Linden, P., A. Marchini, C. J. Smith, M. Dolbeth, L. R. L. Simone, J. C. Marques, J. Molozzi, C. R. Medeiros & J. Patrício, 2017. Functional changes in polychaete and mollusc communities in two tropical estuaries. Estuarine, Coastal and Shelf Science 187: 62–73.

    Google Scholar 

  • Van der Zee, E. M., C. Angelini, L. L. Govers, M. J. Christianen, A. H. Altieri, K. J. van der Reijden, B. R. Silliman, J. van de Koppel, M. van der Geest, J. A. van Gils, H. W. van der Veer, T. Piersma, P. C. de Ruiter, H. Olff & T. van der Heide, 2016. How habitat-modifying organisms structure the food web of two coastal ecosystems. Proceedings of the Royal Society Sciences 283: 1–9.

    Google Scholar 

  • Veiga, P., M. Rubal & I. Sousa-Pinto, 2014. Structural complexity of macroalgae influences epifaunal assemblages associated with native and invasive species. Marine Environmental Research 101: 115–123.

    CAS  PubMed  Google Scholar 

  • Veiga, P., A. C. Torres, C. Besteiro & M. Rubal, 2018. Mollusc assemblages associated with invasive and native Sargassum species. Continental Shelf Research 161: 12–19.

    Google Scholar 

  • Villéger, S., N. W. H. Mason & D. Mouillot, 2008. New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89(8): 2290–2301.

    PubMed  Google Scholar 

  • Walker, B. H., 1992. Biodiversity and ecological redundancy. Conservation Biology 6: 18–23.

    Google Scholar 

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Acknowledgements

We are also thankful to Dona Dalci and family for their logistical support in the community of Diogo Lopes. We are grateful to our colleague Luis Carlos for their essential support in the fieldwork. We are also grateful to Leidson Allan Ferreira de Lucena for the identification of macroalgae. This study was financially supported by Programa de Pós-Graduação em Ciências Biológicas (Zoologia), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES/Brazilian Ministry of Education) by granting the doctoral scholarship to R. C. S. Duarte, and the Paraíba State University (Programa de Pós-Graduação em Ecologia e Conservação and Marine Biology Laboratory) for logistical support.

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Authors and Affiliations

  1. Programa de Pós-Graduação em Ciências Biológicas (Zoologia), CCEN, Departamento de Sistemática e Ecologia, Universidade Federal da Paraíba, Campus Universitário I, Cidade Universitária, João Pessoa, PB, 58051-090, Brazil

    Rafaela Cristina de Souza Duarte & Thelma Lucia Pereira Dias

  2. Programa de Pós-Graduação em Ecologia e Conservação da Biodiversidade, Universidade Federal de Mato Grosso, Avenida Fernando Corrêa da Costa s/n, Cuiabá, Mato Grosso, 78060-900, Brazil

    Graciele de Barros

  3. Departamento de Biologia, Universidade Regional Integrada do Alto Uruguai e das Missões - URI/RS, Avenida 7 de setembro, Erechim, RS, 99709-910, Brazil

    Silvia Vendruscolo Milesi

  4. Programa de Pós-Graduação em Ecologia e Conservação, Laboratório de Biologia Marinha, CCBS, Departamento de Biologia, Universidade Estadual da Paraíba, Rua das Baraúnas, 351, Bairro Universitário, Campina Grande, PB, 58429-500, Brazil

    Thelma Lucia Pereira Dias

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  1. Rafaela Cristina de Souza Duarte
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Duarte, R.C.S., de Barros, G., Milesi, S.V. et al. Influence of macroalgal morphology on the functional structure of molluscan community from hypersaline estuary. Hydrobiologia 847, 1107–1119 (2020). https://doi.org/10.1007/s10750-019-04171-3

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