Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-22T18:30:15.507Z Has data issue: false hasContentIssue false
  • English
  • Français

The highly diverse gastropod assemblages associated with Sargassum spp. (Phaeophyceae: Fucales) habitats

Published online by Cambridge University Press:  03 May 2019

Pedro Augusto Dos Santos Longo ,
Karine Ferreira Ribeiro Mansur ,
Fosca Pedini Pereira Leite  and
Flávio Dias Passos
Pedro Augusto Dos Santos Longo*
Affiliation:
Department of Animal Biology, State University of Campinas, Biology Institute, Monteiro Lobato Street, 255, Campinas, São Paulo, 13083-862, Brazil Pedro Augusto dos Santos Longo, Graduate Program in Ecology, State University of Campinas (UNICAMP), Campinas, SP 13083-970,Brazil
Karine Ferreira Ribeiro Mansur
Affiliation:
Department of Animal Biology, State University of Campinas, Biology Institute, Monteiro Lobato Street, 255, Campinas, São Paulo, 13083-862, Brazil Graduate Program in Animal Biology, State University of Campinas (UNICAMP), Campinas, SP 13083-970, Brazil
Fosca Pedini Pereira Leite
Affiliation:
Department of Animal Biology, State University of Campinas, Biology Institute, Monteiro Lobato Street, 255, Campinas, São Paulo, 13083-862, Brazil
Flávio Dias Passos
Affiliation:
Department of Animal Biology, State University of Campinas, Biology Institute, Monteiro Lobato Street, 255, Campinas, São Paulo, 13083-862, Brazil
*
Author for correspondence: Pedro Augusto dos Santos Longo, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Macrophytes provide a habitat for many species of marine invertebrates, the gastropods being one of the main components. This study provides new information about Sargassum-associated gastropod biodiversity, through characterization of the fauna from a highly impacted area of Brazil, investigating its variation at a small spatial scale and between two main seasons of the year, as well as its relationship with macroalgae parameters. Density of gastropods was higher during the warmest season and varied throughout sampling sites. A significant and positive, however weak, relationship between gastropod density and Sargassum dry weight was found in all localities. For all sites, a marked and unusual dominance of Bittiolum varium was observed. The high dominance of this species seems to be related to the impacts caused by shipping activities and highway construction in the 1970s and 1980s, which caused a decline in local species diversity that seems to have continued until now. Many species, both typical of these habitats and characteristic of other, nearby habitats, benefit from Sargassum sp. These macrophytes allow gastropods to establish and grow during their most vulnerable stages, as shown by the growth series and juvenile forms found for most species of gastropods. The present data highlight the importance of macrophyte habitats for gastropod biodiversity in coastal areas and call attention to the importance of raising knowledge on this fauna, especially in impacted areas, thus contributing to the conservation of these highly diverse and ecologically important macrophyte–gastropod systems.

Keywords

Biodiversitymacroalgaegrowth seriesmarine diversitymolluscsmarine snails
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 99 , Issue 6 , September 2019 , pp. 1295 - 1307
Copyright
Copyright © Marine Biological Association of the United Kingdom 2019 

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

Almeida, SM (2007) Malacofauna associada ao fital de Sargassum spp. no Pontal do Cupe, Ipojuca, PE. Master's dissertation. Federal University of Pernambuco, Pernambuco, Brazil.Google Scholar
Amin, B, Ismail, A, Arshad, A, Yap, CK and Kamarudin, MS (2009) Gastropod assemblages as indicators of sediment metal contamination in mangroves of Dumai, Sumatra, Indonesia. Water, Air and Soil Pollution 201, 9–18.Google Scholar
Amsler, M, Huang, YM, Engl, W, McClintock, JB and Amsler, CD (2015) Abundance and diversity of gastropods associated with dominant subtidal macroalgae from the western Antarctic Peninsula. Polar Biology 38, 1171–1181.Google Scholar
Arroyo, MC, Salas, C, Rueda, JL and Gofas, S (2006) Temporal changes of mollusc populations from a Zostera marina bed in southern Spain (Alboran Sea), with biogeographic considerations. Marine Biology 27, 417–430.Google Scholar
Barros, KVS and Rocha-Barreira, CA (2013) Responses of the molluscan fauna to environmental variations in a Halodule wrightii Ascherson ecosystem from Northeastern Brazil. Anais da Academia Brasileira de Ciências 85, 1397–1410.Google Scholar
Bulleri, F, Airoldi, L, Branca, GM and Abbiati, M (2006) Positive effects of the introduced green alga, Codium fragile ssp. tomentosoides, on recruitment and survival of mussels. Marine Biology 148, 1213–1220.Google Scholar
Buzato, E (2012) Avaliação de impactos ambientais no município de Ubatuba: uma proposta a partir de geoindicadores. PhD thesis. University of São Paulo, São Paulo, Brazil.Google Scholar
Carvalho, NF, Grande, H, Filho, JSR and Jacobucci, GB (2018) The structure of gammarid amphipod (Crustacea, Peracarida) assemblages associated with Sargassum (Phaeophyta, Fucales) and their link with the structural complexity of algae. Hydrobiologia 820, 245–254.Google Scholar
CETESB – Companhia Ambiental do Estado de São Paulo (2014) Qualidade das águas superficiais do estado de São Paulo. Parte 2 – Águas salinas e salobras. 164 pp.Google Scholar
CETESB – Companhia Ambiental do Estado de São Paulo (2015) Qualidade das águas superficiais do estado de São Paulo. Parte 2 – Águas salinas e salobras. 164 pp.Google Scholar
CETESB – Companhia Ambiental do Estado de São Paulo (2016) Qualidade das águas superficiais do estado de São Paulo. Parte 2 – Águas salinas e salobras. 164 pp.Google Scholar
Chemello, R and Milazzo, M (2002) Effect of algal architecture on associated fauna: some evidence from phytal molluscs. Marine Biology 140, 981–990.Google Scholar
Christie, H, Norderhaug, KM and Fredriksen, S (2009) Macrophytes as habitat for fauna. Marine Ecology Progess Series 396, 221–233.Google Scholar
Climate-data.org. (2016) Climate data for cities worldwide. Available at http://en.climate-data.org/location/34847/ (accessed 24 June 2016).Google Scholar
Cocheret de la Morinière, E, Pollux, BJA, Nagelkerken, I and Van der Velde, G (2002) Post-settlement life cycle migration patterns and habitat preference of coral reef fish that use seagrass and mangrove habitats as nurseries. Estuarine, Coastal and Shelf Science 55, 309–321.Google Scholar
Conti, ME and Cecchetti, G (2003) A biomonitoring study: trace metals in algae and molluscs from Tyrrhenian coastal areas. Environmental Research 93, 99–112.Google Scholar
Creed, JC and Kinupp, M (2011) Small scale change in mollusk diversity along a depth gradient in a seagrass bed off Cabo Frio (Southeast Brazil). Brazilian Journal of Oceanography 59, 267–276.Google Scholar
Duarte, CM (2002) The future of seagrass meadows. Environmental Conservation 29, 192–206.Google Scholar
Duarte, RCS, Mota, ELS, Almeida, ICS, Pessanha, ALM, Christoffersen, ML and Dias, TLP (2015) Gastropods associated to three reef macrophytes with different architectures. Strombus 22, 5–18.Google Scholar
Feldstein, T, Kashman, Y, Abelson, A, Fishelson, L, Mokady, O, Bresler, V and Erel, Y (2003) Marine molluscs in environmental monitoring. III. Trace metals and organic pollutants in animal tissue and sediments. Helgoland Marine Research 57, 212–219.Google Scholar
García, AF, Bueno, M and Leite, FPP (2015) The Bostrychietum community of pneumatophores in Aracá Bay: an analysis of the diversity of macrofauna. Journal of the Marine Biological Association of the United Kingdom 86, 1617–1624.Google Scholar
Haywood, MDE, Vance, DJ and Loneragan, NR (1995) Seagrass and algal beds as nursery habitats for tiger prawns (Penaeus semisulcatus and P. esculentus) in a tropical Australian estuary. Marine Biology 122, 213–223.Google Scholar
Heck, KL Jr., Hays, G and Orth, RJ (2003) Critical evaluation of the nursery role hypothesis for seagrass meadows. Marine Ecology Progress Series 253, 123–136.Google Scholar
Heck, KL Jr., Carruthers, TJB, Duarte, CM, Hughes, AR, Kendrick, G, Orth, RJ and Williams, SW (2008) Trophic transfers from seagrass meadows subsidize diverse marine and terrestrial consumers. Ecosystems 11, 1198–1210.Google Scholar
Hillebrand, H, Bennett, DM and Cadotte, MW (2008) Consequences of dominance: a review of evenness effects on local and regional ecosystem processes. Ecology 89, 1510–1520.Google Scholar
Hothorn, T, Bretz, F and Westfall, P (2008) Simultaneous inference in general parametric models. Biometrical Journal 50, 346–363.Google Scholar
Jacobucci, GB and Leite, FPP (2002) Distribuição vertical e flutuação sazonal da macrofauna vágil associada a Sargassum cymosum C. Agardh, na praia do Lázaro, Ubatuba, São Paulo, Brasil. Revista Brasileira de Zoologia 19 (Suppl.1), 87–100.Google Scholar
Jacobucci, GB, Güth, AZ, Turra, A, Magalhães, CA, Denadai, MR, Chaves, AMR and Souza, ECF (2006) Levantamento de Mollusca, Crustacea e Echinodermata associados a Sargassum spp. na Ilha da Queimada Pequena, Estação Ecológica dos Tupiniquins, litoral sul do estado de São Paulo, Brasil. Biota Neotropica 6, 1–8.Google Scholar
Jiménez-Ramos, R, Egea, LG, Vergara, JJ, Bouma, TJ and Brun, FG (2019) The role of flow velocity combined with habitat complexity as a top–down regulator in seagrass meadows. Oikos 128, 64–76.Google Scholar
Johnston, EL and Roberts, DA (2009) Contaminants reduce the richness and evenness of marine communities: a review and meta-analysis. Environmental Pollution 157, 1745–1752.Google Scholar
Lançone, RB, Duleba, W and Mahiques, MM (2005) Dinâmica de fundo da Enseada do Flamengo, Ubatuba, Brasil, inferida a partir da distribuição espacial, morfometria e tafonomia de foraminíferos. Revista Brasileira de Paleontologia 8, 181–192.Google Scholar
Leite, FPP and Martins, RF (1991) Variação sazonal dos gastrópodos associados a Sargassum cymosum da Praia do Lamberto, Ubatuba (SP). In Abstract from the XVIII Brazilian Congress of Zoology. Salvador: Federal University of Bahia, vol. 1, pp. 527–527.Google Scholar
Leite, FPP and Turra, A (2003) Temporal variation in Sargassum biomass, Hypnea epiphytism and associated fauna. Brazilian Archives of Biology and Technology 46, 665–671.Google Scholar
Leite, FPP, Tanaka, MO and Gebara, RS (2007) Structural variation in the brown alga Sargassum cymosum and its effects on associated amphipod assemblages. Brazilian Journal of Biology 67, 215–221.Google Scholar
Leite, FPP, Tambourgi, MRS and Cunha, CM (2009) Gastropods associated with the green seaweed Caulerpa racemosa, on two beaches of the northern coast of the state of São Paulo, Brazil. Strombus 16, 1–10.Google Scholar
Lolas, A, Antoniadou, C and Vafidis, D (2018) Spatial variation of molluscan fauna associated with Cystoseira assemblages from a semi-enclosed gulf in the Aegean Sea. Regional Studies in Marine Science 19, 17–24.Google Scholar
Longo, PAS, Fernandes, MC, Leite, FPP and Passos, FD (2014) Gastropoda (Mollusca) associated to Sargassum sp. beds in São Sebastião Channel – São Paulo, Brazil. Biota Neotropica 14, 1–10.Google Scholar
Martin, TH, Crowder, LB, Dumas, CF and Burkholder, JM (1992) Indirect effects of fish on macrophytes in Bays Mountain Lake: evidence for a littoral trophic cascade. Oecologia 89, 476–481.Google Scholar
Mendes, CLT, Soares-Gomes, A and Tavares, M (2006) Seasonal and spatial distribution of sublittoral soft-bottom mollusks assemblages at Guanabara Bay, Rio de Janeiro, Brazil. Journal of Coastal Research 39, 136–140.Google Scholar
Montfrans, JV, Orth, RJ and Vay, SA (1982) Preliminary studies of grazing by Bittium varium on eelgrass periphyton. Aquatic Botany 14, 75–89.Google Scholar
Montouchet, PCG (1979) Sur La communauté dês animaux vagiles associés à Sargassum cymosum C. Agardh, à Ubatuba, Etat de São Paulo, Brésil. Studies on Neotropical Fauna and Environment 14, 33–64.Google Scholar
Norton, TA and Benson, MR (1983) Ecological interactions between the brown seaweed Sargassum muticum and its associated fauna. Marine Biology 75, 169–177.Google Scholar
Perkins-Visser, E, Wolcott, TG and Wolcott, DL (1996) Nursery role of seagrass beds: enhanced growth of juvenile blue crabs (Callinectes sapidus Rathbun). Journal of Experimental Marine Biology and Ecology 198, 155–173.Google Scholar
Pinheiro, JC and Bates, DM (2000) Mixed-Effects Models in S and S-PLUS. New York, NY: Springer.Google Scholar
Pinheiro, JC, Bates, D, DebRoy, S and Sarkar, D and R Core Team (2018) nlme: linear and nonlinear mixed effects models. R package version 3.1-137. Available at https://CRAN.R-project.org/package=nlme.Google Scholar
Pitacco, V, Orlando-Bonaca, M, Mavrič, B, Popović, A and Lipej, L (2014) Mollusc fauna associated with the Cystoseira algal associations in the Gulf of Trieste (Northern Adriatic Sea). Mediterranean Marine Science 15, 225–238.Google Scholar
Queiroz, RNM and Dias, TLP (2014). Molluscs associated with the macrophytes of the genus Gracilaria (Rhodophyta): importance of algal fronds as microhabitat in a hypersaline mangrove in Northeastern Brazil. Brazilian Journal of Biology 74 (suppl. 3), S52–S63.Google Scholar
R Core Team (2015) R: A Language and Environment for Statistical Computing. Vienna: R Foundation.Google Scholar
Roberts, DA, Johnston, EL and Poore, AGB (2008) Contamination of marine biogenic habitats and effects upon associated epifauna. Marine Pollution Bulletin 56, 1057–1065.Google Scholar
Rubal, M, Costa-Garcia, R, Besteiro, C, Souza-Pinto, I and Veiga, P (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.Google Scholar
Rueda, JL and Salas, C (2003) Seasonal variation of a molluscan assemblage living in a Caulerpa prolifera meadow within the inner Bay of Cádiz (SW Spain). Estuarine, Coastal and Shelf Science 57, 909–918.Google Scholar
Rueda, JL, Urra, J and Salas, C (2008) Diel and seasonal variation of a molluscan taxocoenosis associated with a Zostera marina bed in southern Spain (Alboran Sea). Helgoland Marine Research 62, 227–240.Google Scholar
Rumisha, C, Elskens, M, Leermakers, M and Kochzius, M (2012) Trace metal pollution and its influence on the community structure of soft bottom molluscs in intertidal areas of the Dar es Salaam coast, Tanzania. Marine Pollution Bulletin 64, 521–531.Google Scholar
Sánchez-Moyano, JE, Estacio, FJ, García-Adiego, EM and García-Gómez, JC (2000) The molluscan epifauna of the alga Halopteris scoparia in southern Spain as a bioindicator of coastal environmental condition. Journal of Molluscan Studies 66, 431–448.Google Scholar
Stoner, AW (2003) What constitutes essential nursery habitat for a marine species? A case study of habitat form and function for queen conch. Marine Ecology Progress Series 257, 275–289.Google Scholar
Széchy, MTM and Paula, EJ (2000) Padrões estruturais quantitativos de bancos de Sargassum (Phaeophyta, Fucales) do litoral dos estados do Rio de Janeiro e São Paulo, Brasil. Revista Brasileira de Botânica, São Paulo 23, 121–132.Google Scholar
Tanaka, MO and Leite, FPP (2003) Spatial scaling in the distribution of macrofauna associated with Sargassum stenophyllum (Mertens) Martius: analyses of faunal groups, gammarid life habits, and assemblage structure. Journal of Experimental Marine Biology and Ecology 293, 1–22.Google Scholar
Terlizzi, A, Scuderi, D, Fraschetti, S and Anderson, MJ (2005) Quantifying effects of pollution on biodiversity: a case study of highly diverse molluscan assemblages in the Mediterranean. Marine Biology 148, 293–305.Google Scholar
Thomaz, SM and Cunha, ER (2010) The role of macrophytes in habitat structuring in aquatic ecosystems: methods of measurement, causes and consequences on animal assemblages’ composition and biodiversity. Acta Limnologica Brasiliensia 22, 218–236.Google Scholar
Torres, AC, Veiga, P, Rubal, M and Souza-Pinto, I (2015) The role of annual macroalgal morphology in driving its epifaunal assemblages. Journal of Experimental Marine Biology and Ecology 464, 96–106.Google Scholar
Urra, J, Ramírez, AM, Marina, P, Salas, C, Gofas, S and Rueda, JL (2013) Highly diverse molluscan assemblages of Posidonia oceanica meadows in northwestern Alboran Sea (W Mediterranean): seasonal dynamics and environmental drivers. Estuarine, Coastal and Shelf. Science 117, 136–147.Google Scholar
Veiga, P, Rubal, M and Sousa-Pinto, I (2014) Structural complexity of macrophytes influences epifaunal assemblages associated with native and invasive species. Marine Environmental Research 101, 115–123.Google Scholar
Veiga, P, Torres, AC, Besteiro, C and Rubal, M (2018) Mollusc assemblages associated with invasive and native Sargassum species. Continental Shelf Research 161, 12–19.Google Scholar
Villanueva, VD, Font, J, Schwartz, T and Romaní, AM (2011) Biofilm formation at warming temperature: acceleration of microbial colonization and microbial interactive effects. Biofouling 27, 59–71.Google Scholar
Vincent, B, Rioux, H and Harvey, M (1991) Factors affecting the structure of epiphytic gastropod communities in the St. Lawrence River (Quebec, Canada). Hydrobiologia 220, 57–71.Google Scholar
Walsh, K, Dunstan, RH, Murdoch, RN, Conroy, BA, Roberts, TK and Lake, P (1994) Bioaccumulation of pollutants and changes in population parameters in the gastropod mollusk Austrocochlea constricta. Archives of Environmental Contamination and Toxicology 26, 367–373.Google Scholar
Wang, H, Pan, B, Liang, X and Wang, H (2006) Gastropods on submersed macrophytes in Yangtze lakes: community characteristics and empirical modeling. International Review of Hydrobiology 91, 521–538.Google Scholar
Waycott, M, Duarte, CM, Carruthers, TJB, Orth, RJ, Dennison, WC, Olyarnik, S, Calladine, A, Fourqurean, JW, Heck, KL Jr., Hughes, AR, Kendrick, GA, Kenworthy, WJ, Short, FT and Williams, SL (2009) Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proceedings of the National Academy of Sciences USA 106, 12377–12381.Google Scholar
Wise, JB (1996) Morphology and phylogenetic relationships of certain pyramidellid taxa (Heterobranchia). Malacologia 37, 443–511.Google Scholar
Zamprogno, GC, Costa, MB, Barbiero, DC, Ferreira, BS and Souza, FTVM (2013) Gastropod communities associated with Ulva spp. in the littoral zone in southeast Brazil. Latin American Journal of Aquatic Research 41, 968–978.Google Scholar