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The structure of gammarid amphipod (Crustacea, Peracarida) assemblages associated with Sargassum (Phaeophyta, Fucales) and their link with the structural complexity of algae

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Abstract

The structural complexity of algae is an important factor driving the structure of epifaunal assemblages associated with marine macroalgae. We tested how the structural complexity of four Sargassum species is related to the structure of gammarid assemblages. We measured different algae traits (frond length, number of branches, and epiphytic hydroid and algae cover) and different ecological descriptors of gammarid assemblages (richness, density, diversity, and evenness). Samples were obtained in southeastern Brazil in early and late summer. Structural complexity was associated with the occurrence of significantly different gammarid assemblages. Sargassum cymosum had more branches and greater hydroid coverage, and a higher gammarid species richness, diversity, and density. The characteristics of the gammarids inhabiting the different Sargassum species were similar between sampling periods, indicating that the relationships between the Sargassum traits and associated gammarids are strong and persistent. Species richness, diversity, and density were all more dependent on habitat heterogeneity (number of branches and coverage of epiphytic hydroid) than the quantity of habitable space, i.e., frond length. Overall, the variation in structural complexity among Sargassum species had a significant effect on gammarid assemblage structure.

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References

  • Alarcón-Ortega, L. C., J. M. Guerra-García, J. E. Sánchez-Moyano & F. Cuoul-Magaña, 2012. Feeding habits of caprellids (Crustacea: Amphipoda) from the west coast of Mexico. Do they feed on their hosting substrates? Zoologica Baetica 23: 11–20.

    Google Scholar 

  • Amsler, C., 2008. Algal Chemical Ecology. Springer, Berlin: 468.

    Book  Google Scholar 

  • Anderson, M. J., 2000. DISTLM: a FORTRAN computer program to calculate a distance-based multivariate analysis for a linear model. Department of Statistics, University of Auckland, Auckland.

    Google Scholar 

  • Anderson, M. J. & T. J. Willis, 2003. Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84: 511–525.

    Article  Google Scholar 

  • Anderson, M. J., R. N. Gorley & K. R. Clarke, 2008. PERMANOVA+. Guide to Software and Statistical Methods. PRIMER-E, Plymouth.

    Google Scholar 

  • Attrill, M. J., J. A. Strong & A. A. Rowden, 2000. Are macroinvertebrate communities influenced by seagrass structural complexity? Ecography 23: 114–121.

    Article  Google Scholar 

  • Bavestrello, G., C. Cerrano, R. Cattaneo-Vietti & M. Sarà, 1996. Relations between Eudendrium glomeratum (Cnidaria, Hydromedusae) and its associated vagile fauna. Scientia Marina 60: 137–143.

    Google Scholar 

  • Berchez, F. A., R. T. Pereira & N. F. Kamiya, 1993. Culture of Hypnea musciformis (Rhodophyta, Gigartinales) on artificial substrates attached to linear ropes. Hydrobiologia 260: 415–420.

    Article  Google Scholar 

  • Bradshaw, C., P. Collins & A. R. Brand, 2003. To what extent does upright sessile epifauna affect benthic biodiversity and community composition? Marine Biology 143: 783–791.

    Article  Google Scholar 

  • Breitburg, D. L., 1985. Development of a subtidal epibenthic community: factors affecting species composition and the mechanisms of succession. Oecologia 65: 173–184.

    Article  PubMed  Google Scholar 

  • Buschbaum, C., A. S. Chapman & B. Saier, 2006. How an introduced seaweed can affect epibiota diversity in different coastal systems. Marine Biology 148: 743–754.

    Article  Google Scholar 

  • Buschmann, A. H. & P. Gómez, 1993. Interaction mechanisms between Gracilaria chilensis (Rhodophyta) and epiphytes. Hydrobiologia 260: 345–351.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Christie, H., K. M. Norderhaug & S. Fredriksen, 2009. Macrophytes as habitat for fauna. Marine Ecology Progress Series 396: 221–233.

    Article  Google Scholar 

  • Conlan, K. E., 1982. Revision of the gammaridean amphipod family Ampithoidae using numerical analytical methods. Canadian Journal of Zoology 60: 2015–2027.

    Article  Google Scholar 

  • Cunha, A. F. & G. B. Jacobucci, 2010. Seasonal variation of epiphytic hydroids (Cnidaria: Hydrozoa) associated to a subtropical Sargassum cymosum (Phaeophyta: Fucales) bed. Zoologia (Curitiba) 27: 945–955.

    Article  Google Scholar 

  • Cunha, F. L. R., A. F. Cunha & G. B. Jacobucci, 2009. Is the occurrence of caprellid amphipods associated with Sargassum (Phaeophyta) influenced by algal and hydrozoan epibiosis? Revista Brasileira de Zoociências 10: 257–264.

    Google Scholar 

  • Davenport, J. P., J. A. Pugh & J. McKechnie, 1996. Mixed fractals and anisotropy in subantarctic marine macroalgae from South Georgia: implications for epifaunal biomass and abundance. Marine Ecology Progress Series 136: 245–255.

    Article  Google Scholar 

  • Denadai, M. R., A. C. Z. Amaral & A. Turra, 2005. Structure of molluscan assemblages in sheltered intertidal unconsolidated environments. Brazilian Archives of Biology and Technology 48: 825–839.

    Article  Google Scholar 

  • Di Camillo, C. G., G. Bavestrello, L. Valisano & S. Puce, 2008. Spatial and temporal distribution in a tropical hydroid assemblage. Journal of the Marine Biological Association of the United Kingdom 88: 1589–1599.

    Article  Google Scholar 

  • Downes, B. J., P. S. Lake, E. S. G. Schreiber & A. Glaister, 2000. Habitat structure, resources and diversity: the separate effects of surface roughness and macroalgae on stream invertebrates. Oecologia 123: 569–581.

    Article  PubMed  CAS  Google Scholar 

  • Dubiaski-Silva, J. & S. Masunari, 1995. Population ecology of Amphipoda (Crustacea) from the phytals of Caiobá, Matinhos, Paraná, Brazil. Revista Brasileira de Zoologia 12: 373–396.

    Article  Google Scholar 

  • Duffy, J. E., 1990. Amphipods on seaweeds: partners or pests? Oecologia 83: 267–276.

    Article  PubMed  CAS  Google Scholar 

  • Ebbs, N., 1966. The coral-inhabiting polychaetes of the Northern Florida reef tract, part 1. Bulletin of Marine Science 16: 485–555.

    Google Scholar 

  • Edgar, G. J. & A. I. Robertson, 1992. The influence of seagrass structure on the distribution and abundance of motile epifauna: pattern and process in a western Australian Amphibolis bed. Journal of Experimental Marine Biology and Ecology 160: 13–31.

    Article  Google Scholar 

  • Fenwick, G. D., 1976. The effect of wave exposure on the amphipod fauna of the alga Caulerpa brownii. Journal of Experimental Marine Biology and Ecology 3: 1–43.

    Article  Google Scholar 

  • Graham, N. A. J. & K. L. Nash, 2013. The importance of structural complexity in coral reef ecosystems. Coral Reefs 32: 315–326.

    Article  Google Scholar 

  • Groemping, U., 2006. Relative importance for linear regression in R: the package relaimpo. Journal of Statistical Software 17: 1–27.

    Article  Google Scholar 

  • Guerra-García, J. M., J. T. Figueroa, C. Navarro-Barranco, M. Ros, J. E. Sánchez-Moyano & J. Moreira, 2014. Dietary analysis of the marine Amphipoda (Crustacea: Peracarida) from the Iberian Peninsula. Journal of Sea Research 85: 508–517.

    Article  Google Scholar 

  • Hacker, S. D. & R. S. Steneck, 1990. Habitat architecture and the abundance and body-size dependent habitat selection of a phytal amphipod. Ecology 71: 2269–2285.

    Article  Google Scholar 

  • Harari, J. & A. R. Mesquita, 2007. Tábua de marés para Ubatuba, Santos e Cananéia. Relatório Técnico do Instituto Oceanográfico 81: 1–17.

    Google Scholar 

  • Heck Jr., K. L. & G. S. Wetstone, 1977. Habitat complexity and invertebrate species richness and abundance in tropical seagrass meadows. Journal of Biogeography 1: 135–142.

    Article  Google Scholar 

  • Hutchinson, G. E., 1957. Population studies, animal ecology and demography, concluding remarks. Cold Spring Harbor Symposia on Quantitative Biology 22: 415–427.

    Article  Google Scholar 

  • Hutchinson, G. E., 1959. Homage to Santa Rosalia or why are there so many kinds of animals? The American Naturalist 93: 145–159.

    Article  Google Scholar 

  • Jacobucci, G. B. & F. P. P. Leite, 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: 87–100.

    Article  Google Scholar 

  • Jacobucci, G. B. & F. P. P. Leite, 2014. The role of epiphytic algae and different species of Sargassum in the distribution and feeding of herbivorous amphipods. Latin American Journal Aquatic Research 42: 353–363.

    Article  Google Scholar 

  • James, P. L. & K. L. Heck, 1994. The effects of habitat complexity and light intensity on ambush predation within a simulated seagrass habitat. Journal of Experimental Marine Biology and Ecology 176: 187–200.

    Article  Google Scholar 

  • Leite, F. P. P., M. O. Tanaka & R. S. Gebara, 2007a. Structural variation in the brown alga Sargassum cymosum and its effects on associated amphipod assemblages. Brazilian Journal of Biology 67: 215–221.

    Article  CAS  Google Scholar 

  • Leite, F. P. P., M. O. Tanaka, D. B. Sudatti & R. S. Gebara, 2007b. Diel density variation of amphipods associated with Sargassum beds from two shores of Ubatuba, Southeastern, Brasil. Iheringia. Série Zoologia 97: 400–405.

    Article  Google Scholar 

  • Little, C., G. A. William & D. Trowbridge, 2015. The Biology of Rocky Shores. Oxford University Press, Oxford.

    Google Scholar 

  • Machado, G. B. D. O., A. B. Neufeld, S. A. Dena, S. G. L. Siqueira & F. P. P. Leite, 2015. Variation of amphipod assemblage along the Sargassum stenophyllum (Phaeophyta, Fucales) thallus. Nauplius 23: 73–78.

    Article  Google Scholar 

  • MacLeod, P. & I. Valiela, 1975. The effect of density and mutual interference by a Predator: a laboratory study of predation by the Nudibranch Coryphella rufibranchialis on the hydroid Tubularia larynx. Hydrobiologia 47: 339–346.

    Article  Google Scholar 

  • Mahiques, M. M., G. Tessler & V. V. Furtado, 1998. Characterization of energy gradient in enclosed bays of Ubatuba region, South-eastern Brazil. Estuarine Coastal and Shelf Science 47: 431–446.

    Article  Google Scholar 

  • Martin-Smith, K. M., 1993. Abundance of mobile epifauna: the role of habitat complexity and predation by fishes. Journal of Experimental Marine Biology and Ecology 174: 243–260.

    Article  Google Scholar 

  • Montouchet, P. G. C., 1979. Sur la communauté des animaux vagiles associés à Sargassum cymosum C. Agardh, à Ubatuba, Etat de São Paulo Brésil. Studies on Neotropical Fauna and Environment 18: 151–161.

    Google Scholar 

  • Nakamura, Y., M. Horinouchi, T. Nakai & M. Sano, 2003. Food habits of fishes in a seagrass bed on a fringing coral reef at Iriomote Island, southern Japan. Ichthyological Research 50: 15–22.

    Article  Google Scholar 

  • Nelson, W. G., 1979. Experimental studies of selective predation on amphipods: consequences for amphipod distribution and abundance. Journal of Experimental Marine Biology and Ecology 38: 225–245.

    Article  Google Scholar 

  • Paradis, E., J. Claude & K. Strimmer, 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20: 289–290.

    Article  PubMed  CAS  Google Scholar 

  • Paula, E. J., 1988. O gênero Sargassum C. Ag. (Phaeophyta-Fucales) no litoral do Estado de São Paulo, Brasil. Boletim de Botânica da Universidade de São Paulo 10: 65–118.

    Article  Google Scholar 

  • Poore, A. G., A. H. Campbell, R. A. Coleman, G. J. Edgar, V. Jormalainen, P. L. Reynolds, E. E. Sotka, J. J. Stachowicz, R. B. Taylor, M. A. Vanderklift & J. E. Duffy, 2012. Global patterns in the impact of marine herbivores on benthic primary producers. Ecology Letters 15: 912–922.

    Article  PubMed  Google Scholar 

  • Reis, R. P., M. C. R. Leal, Y. Yoneshigue-Valentin & F. Belluco, 2003. Efeito de fatores bióticos no crescimento de Hypnea musciformis (Rhodophyta-Gigartinales). Acta Botanica Brasilica 17: 279–286.

    Article  Google Scholar 

  • Ronowicz, M., M. Wlodarska-Kowalczuk & P. Kuklinski, 2008. Factors influencing hydroids (Cnidaria: Hydrozoa) biodiversity and distribution in Arctic kelp forest. Journal of the Marine Biological Association of the United Kingdom 88: 1567–1575.

    Article  Google Scholar 

  • Rosenzweig, M. L., 1995. Species diversity in space and time. Cambridge University Press, Cambridge.

    Book  Google Scholar 

  • RStudio, 2018. RStudio: integrated development environment for R (Version 1.1.442) [Computer software]. Boston, MA. Retrieved May 20, 2012. [available on internet at http://www.rstudio.org/]

  • Russell, D. J. & J. W. Hedgpeth, 1990. Host utilization during ontogeny by two pycnogonid species (Tanystylum duospinum and Ammothea hilgendorfi) parasitic on the hydroid Eucopella everta (Coelenterata:Campanulariidae). Bijdragen tot de Dierkunde 60: 215–224.

    Google Scholar 

  • Russo, A. R., 1990. The role of seaweed complexity in structuring Hawaiian epiphytal amphipod communities. Hydrobiologia 194: 1–12.

    Article  Google Scholar 

  • Schreider, M. J., T. M. Glasby & A. J. Underwood, 2003. Effects of height on the shore and complexity of habitat on abundances of amphipods on rocky shores in New South Wales, Australia. Journal of Experimental Marine Biology and Ecology 293: 57–71.

    Article  Google Scholar 

  • Serejo, C. S., 2004. Cladistic revision of talitroidean amphipods (Crustacea, Gammaridea), with a proposal of a new classification. Zoologica Scripta 33: 551–586.

    Article  Google Scholar 

  • Staples, D. A. & J. E. Watson, 1987. Associations between pycnogonids and hydroids. In Bouillon, J., F. Boero, F. Cicogna & P. F. S. Cornelius (eds), Modern Trends in the Systematics, Ecology and Evolution of Hydroids and Hydromedusae. Oxford University Press, Oxford: 215–226.

    Google Scholar 

  • Stein, A., K. Gerstner & H. Kreft, 2014. Environmental heterogeneity as a universal driver of species richness across taxa, biomes and spatial scales. Ecology Letters 17: 866–880.

    Article  PubMed  Google Scholar 

  • Széchy, M. T. M. & E. J. Paula, 2000. Padrões estruturais quantitativos em bancos de Sargassum (Phaeophyta-Fucales) do litoral dos estados do Rio de Janeiro e São Paulo, Brasil. Revista Brasileira de Botânica 23: 121–132.

    Google Scholar 

  • Széchy, M. T. M., V. G. Veloso & E. J. Paula, 2001. Brachyura (Decapoda, Crustacea) of phytobenthic communities of the sublittoral region of rocky shores of Rio de Janeiro and São Paulo, Brazil. Tropical Ecology 42: 231–242.

    Google Scholar 

  • Tanaka, M. O. & F. P. P. Leite, 2004. Distance effects on short-term recolonization of Sargassum stenophyllum by mobile epifauna, with an analysis of gammarid life habits. Journal of the Marine Biological Association of the United Kingdom 84: 901–910.

    Article  Google Scholar 

  • Tararam, A. S. & Y. Wakabara, 1981. The mobile fauna-especially Gammaridea of Sargassum cymosum. Marine Ecology Progress Series 5: 157–163.

    Article  Google Scholar 

  • Taylor, R. B. & R. G. Cole, 1994. Mobile epifauna on subtidal brown sea-weeds in northeastern New Zealand. Marine Ecology Progress Series 115: 271.

    Article  Google Scholar 

  • Torres, A. C., P. Veiga, M. Rubal & 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.

    Article  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.

    Article  PubMed  CAS  Google Scholar 

  • Viejo, R. M., 1999. Mobile epifauna inhabiting the invasive Sargassum muticum and two local seaweeds in northern Spain. Aquatic Botany 64: 131–149.

    Article  Google Scholar 

  • Wikstrom, S. A. & L. Kautsky, 2004. Invasion of a habitat-forming seaweed: effects on associated biota. Biological Invasions 6: 141–150.

    Article  Google Scholar 

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Acknowledgements

The authors would like to thank Leyton Tierney and Terence A. Palmer for the English revision of the manuscript and to the anonymous reviewers for valuable and indispensable guidelines.

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Authors and Affiliations

  1. Instituto Oceanográfico, Universidade de São Paulo, Praça do Oceanográfico, 191 -Cidade Universitária, São Paulo, SP, 05508-120, Brazil

    Nayara Ferreira Carvalho

  2. Departamento de Oceanografia, Centro de Tecnologia e Geociências, Universidade Federal de Pernambuco, Cidade Universitária, Recife, PE, 50670-901, Brazil

    Henrique Grande & José Souto Rosa Filho

  3. Laboratório de Ecologia de Ecossistemas Aquáticos, Instituto de Biologia, Universidade Federal de Uberlândia, Uberlândia, MG, 38400-902, Brazil

    Giuliano Buzá Jacobucci

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  1. Nayara Ferreira Carvalho
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  2. Henrique Grande
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Carvalho, N.F., Grande, H., Rosa Filho, J.S. et al. 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 (2018). https://doi.org/10.1007/s10750-018-3661-5

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