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Advances in the aquatic sciences
RESEARCH ARTICLE

Spatio-temporal variability of amphipod assemblages associated with rhodolith seabeds

Sandra Navarro-Mayoral https://orcid.org/0000-0002-1529-9629 A , Victoria Fernandez-Gonzalez B , Francisco Otero-Ferrer A and Fernando Tuya A
+ Author Affiliations
- Author Affiliations

A Grupo en Biodiversidad y Conservación, IU-ECOAQUA, Universidad de Las Palmas de Gran Canaria, Marine Scientific and Technological Park, Courta. Taliarte s/n, E-35214 Telde, Spain.

B Department of Marine Sciences and Applied Biology, University of Alicante, PO Box 99, E-03080 Alicante, Spain.

C Corresponding author. Email: sandra.navarro102@alu.ulpgc.es

Marine and Freshwater Research 72(1) 76-83 https://doi.org/10.1071/MF19360
Submitted: 14 November 2019  Accepted: 6 April 2020   Published: 26 May 2020

Abstract

Rhodolith seabeds are habitats underpinned by free-living calcareous macroalgae. We partitioned the relevance of the scale of temporal (four seasons throughout two successive years) and spatial (three depth strata: 18, 25 and 40 m) variation on the diversity, structure and abundance of amphipod assemblages living in rhodolith seabeds from Gran Canaria Island. In total, 3996 individuals, belonging to 32 taxa, were identified. Multivariate analyses showed consistent differences in assemblage structure among seasons and depths; more diverse and abundant amphipod assemblages were often observed during spring at 18- and 25-m than at 40-m depth. Ovigerous females of Gammaropsis ostroumowi and Ampithoe ramondi were observed mainly at 18 and 25 m. Juveniles of both species were exclusively recorded at 18 and 25 m, so denoting a clear segregation in their population structure with depth. In summary, this study has demonstrated that the ecological pattern of amphipods associated with rhodolith seabeds can vary greatly across both time (seasons) and space (depth).

Additional keywords: algal biomass, Atlantic Ocean, Canary Islands, crustaceans, maerl, population structure.


References

Amado-Filho, G. M., Maneveldt, G., Manso, R. C. C., Marins-Rosa, B. V., Pacheco, M. R., and Guimarães, S. M. P. B. (2007). Structure of rhodolith beds from 4 to 55 meters deep along the southern coast of Espírito Santo State, Brazil. Ciencias Marinas 33, 399–410.
Structure of rhodolith beds from 4 to 55 meters deep along the southern coast of Espírito Santo State, Brazil.Crossref | GoogleScholarGoogle Scholar |

Amado-Filho, G. M., Maneveldt, G., Pereira-Filho, G. H., Manso, R. C. C., and Bahia, R. (2010). Seaweed diversity associated with a Brazilian tropical rhodolith bed. Ciencias Marinas 36, 371–391.

Appadoo, C., and Myers, A. A. (2004). Reproductive bionomics and life history traits of three gammaridean amphipods, Cymadusa filosa Savigny, Ampithoe laxipodusAppadoo and Myers and Mallacoota schellenbergi Ledoyer from the tropical Indian Ocean (Mauritius). Acta Oecologica 26, 227–238.
Reproductive bionomics and life history traits of three gammaridean amphipods, Cymadusa filosa Savigny, Ampithoe laxipodusAppadoo and Myers and Mallacoota schellenbergi Ledoyer from the tropical Indian Ocean (Mauritius).Crossref | GoogleScholarGoogle Scholar |

Brokovich, E., Einbinder, S., Shashar, N., Kiflawi, M., and Kark, S. (2008). Descending to the twilight-zone: changes in coral reef fish assemblages along a depth gradient down to 65 m. Marine Ecology Progress Series 371, 253–262.
Descending to the twilight-zone: changes in coral reef fish assemblages along a depth gradient down to 65 m.Crossref | GoogleScholarGoogle Scholar |

Connell, S. D. (2005). Assembly and maintenance of subtidal habitat heterogeneity: synergistic effects of light penetration and sedimentation. Marine Ecology Progress Series 289, 53–61.
Assembly and maintenance of subtidal habitat heterogeneity: synergistic effects of light penetration and sedimentation.Crossref | GoogleScholarGoogle Scholar |

Cunha, M. R., Sorbe, J. C., and Moreira, M. H. (2000). The amphipod Corophium multisetosum (Corophiidae) in Ria de Aveiro (NW Portugal). I. Life history and aspects of reproductive biology. Marine Biology 137, 637–650.
The amphipod Corophium multisetosum (Corophiidae) in Ria de Aveiro (NW Portugal). I. Life history and aspects of reproductive biology.Crossref | GoogleScholarGoogle Scholar |

De Grave, S. (1999). The influence of sedimentary heterogeneity on within maerl bed differences in infaunal crustacean assemblage. Estuarine, Coastal and Shelf Science 49, 153–163.
The influence of sedimentary heterogeneity on within maerl bed differences in infaunal crustacean assemblage.Crossref | GoogleScholarGoogle Scholar |

de O Figueiredo, M. D., Santos-de Menezes, K., Costa-Paiva, E. M., Paiva, P. C., and Ventura, C. R. R. (2007). Experimental evaluation of rhodoliths as living substrata for infauna at the Abrolhos Bank, Brazil. Ciencias Marinas 33, 427–440.
Experimental evaluation of rhodoliths as living substrata for infauna at the Abrolhos Bank, Brazil.Crossref | GoogleScholarGoogle Scholar |

Eckman, J. E. (1983). Hydrodynamic processes affecting benthic recruitment 1. Limnology and Oceanography 28, 241–257.
Hydrodynamic processes affecting benthic recruitment 1.Crossref | GoogleScholarGoogle Scholar |

Fernandez-Gonzalez, V. (2017). Fouling amphipods on marine aquaculture facilities: ecological interactions and potential applications. Doctoral Dissertation, Universitat d’Alacant – Universidad de Alicante, Spain.

Foster, M. S. (2001). Rhodoliths: between rocks and soft places. Journal of Phycology 37, 659–667.
Rhodoliths: between rocks and soft places.Crossref | GoogleScholarGoogle Scholar |

Fulton, C. J., Bellwood, D. R., and Wainwright, P. C. (2005). Wave energy and swimming performance shape coral reef fish assemblages. Proceedings. Biological Sciences 272, 827–832.
Wave energy and swimming performance shape coral reef fish assemblages.Crossref | GoogleScholarGoogle Scholar | 15888415PubMed |

García-Sanz, S., Navarro, P. G., Png-Gonzalez, L., and Tuya, F. (2016). Contrasting patterns of amphipod dispersion in a seagrass meadow between day and night: consistency through a lunar cycle. Marine Biology Research 12, 56–65.
Contrasting patterns of amphipod dispersion in a seagrass meadow between day and night: consistency through a lunar cycle.Crossref | GoogleScholarGoogle Scholar |

Grall, J., and Hall-Spencer, J. M. (2003). Problems facing maerl conservation in Brittany. Aquatic Conservation 13, S55–S64.
Problems facing maerl conservation in Brittany.Crossref | GoogleScholarGoogle Scholar |

Guerra-García, J. M., Tierno de Figueroa, J. M., Navarro-Barranco, C., Ros, M., Sánchez-Moyano, J. E., and Moreira, J. (2014). Dietary analysis of the marine Amphipoda (Crustacea: Peracarida) from the Iberian Peninsula. Journal of Sea Research 85, 508–517.
Dietary analysis of the marine Amphipoda (Crustacea: Peracarida) from the Iberian Peninsula.Crossref | GoogleScholarGoogle Scholar |

Haroun, R. J., Gil-Rodríguez, M. C., de Castro, J. D., and Prud’Homme van Reine, W. F. (2002). A checklist of the marine plants from the Canary Islands (central eastern Atlantic Ocean). Botanica Marina 45, 139–169.
A checklist of the marine plants from the Canary Islands (central eastern Atlantic Ocean).Crossref | GoogleScholarGoogle Scholar |

Harrison, X. A., Donaldson, L., Correa-Cano, M. E., Evans, J., Fisher, D. N., Goodwin, C. E. D., Robinson, B. S., Hodgson, D. J., and Inger, R. (2018). A brief introduction to mixed effects modelling and multi-model inference in ecology. PeerJ 6, e4794.
A brief introduction to mixed effects modelling and multi-model inference in ecology.Crossref | GoogleScholarGoogle Scholar | 30479902PubMed |

Hayward, P. J., and Ryland, J. S. (Eds) (1990). ‘The Marine Fauna of the British Isles and North-West Europe. Vol. 1: Introduction and Protozoans to Arthropods.’ (Clarendon Press: Oxford, UK.)

Hinojosa-Arango, G., and Riosmena-Rodríguez, R. (2004). Influence of rhodolith-forming species and growth form on associated fauna of rhodolith beds in the central-west Gulf of California, México. Marine Ecology 25, 109–127.
Influence of rhodolith-forming species and growth form on associated fauna of rhodolith beds in the central-west Gulf of California, México.Crossref | GoogleScholarGoogle Scholar |

Jeong, S. J., Yu, O. H., and Suh, H. L. (2009). Reproductive patterns and secondary production of Gammaropsis japonicus (Crustacea, Amphipoda) on the seagrass Zoster amarina of Korea. Hydrobiologia 623, 63–76.
Reproductive patterns and secondary production of Gammaropsis japonicus (Crustacea, Amphipoda) on the seagrass Zoster amarina of Korea.Crossref | GoogleScholarGoogle Scholar |

Jiménez Prada, P., Hachero Cruzado, I., and Guerra García, J. M. (2015). Importancia de los anfípodos en la dieta de especies de interés acuícola del litoral andaluz. Zoologica Baetica 26, 3–29.

Johnson, W. S., Stevens, M., and Watling, L. (2001). Reproduction and development of marine peracaridans. Advances in Marine Biology 39, 107–261.

Jones, C. G., Lawton, J. H., and Shachak, M. (1994). Organisms as ecosystem engineers. Oikos 69, 130–147.

Konar, B., Riosmena-Rodriguez, R., and Iken, K. (2006). Rhodolith bed: a newly discovered habitat in the North Pacific Ocean. Botanica Marina 49, 355–359.
Rhodolith bed: a newly discovered habitat in the North Pacific Ocean.Crossref | GoogleScholarGoogle Scholar |

Kuznetsova, A., Brockhoff, P. B., and Christensen, R. H. B. (2017). lmerTest package: tests in linear mixed effects models. Journal of Statistical Software 82, .
lmerTest package: tests in linear mixed effects models.Crossref | GoogleScholarGoogle Scholar |

McConnico, L. A., Carmona, G. H., Morales, J. S. M., and Rodríguez, R. R. (2017). Temporal variation in seaweed and invertebrate assemblages in shallow rhodolith beds of Baja California Sur, México. Aquatic Botany 139, 37–47.
Temporal variation in seaweed and invertebrate assemblages in shallow rhodolith beds of Baja California Sur, México.Crossref | GoogleScholarGoogle Scholar |

Michel, L. N., Dauby, P., Gobert, S., Graeve, M., Nyssen, F., Thelen, N., and Lepoint, G. (2015). Dominant amphipods of Posidonia oceanica seagrass meadows display considerable trophic diversity. Marine Ecology 36, 969–981.
Dominant amphipods of Posidonia oceanica seagrass meadows display considerable trophic diversity.Crossref | GoogleScholarGoogle Scholar |

Mindel, B. L., Neat, F. C., Trueman, C. N., Webb, T. J., and Blanchard, J. L. (2016). Functional, size and taxonomic diversity of fish along a depth gradient in the deep sea. PeerJ 4, e2387.
Functional, size and taxonomic diversity of fish along a depth gradient in the deep sea.Crossref | GoogleScholarGoogle Scholar | 27672494PubMed |

Neill, K. F., Nelson, W. A., D’Archino, R., Leduc, D., and Farr, T. J. (2015). Northern New Zealand rhodoliths: assessing faunal and floral diversity in physically contrasting beds. Marine Biodiversity 45, 63–75.
Northern New Zealand rhodoliths: assessing faunal and floral diversity in physically contrasting beds.Crossref | GoogleScholarGoogle Scholar |

Nelson, W. A., Neill, K., Farr, T., Barr, N., D’archino, R., Miller, S., & Stewart, R. (2012). Rhodolith beds in northern New Zealand: characterisation of associated biodiversity and vulnerability to environmental stressors. New Zealand Aquatic Environment and Biodiversity report, 99, 106. Wellington, New Zealand.

Otero-Ferrer, F., Cosme, M., Tuya, F., Espino, F., and Haroun, R. (2020). Effect of depth and seasonality on the functioning of rhodolith seabeds. Estuarine, Coastal and Shelf Science 235, 106579.
Effect of depth and seasonality on the functioning of rhodolith seabeds.Crossref | GoogleScholarGoogle Scholar |

Pardo, C., Lopez, L., Peña, V., Hernández-Kantún, J., Le Gall, L., Bárbara, I., and Barreiro, R. (2014). A multilocus species delimitation reveals a striking number of species of coralline algae forming maerl in the OSPAR maritime area. PLoS One 9, e104073.
A multilocus species delimitation reveals a striking number of species of coralline algae forming maerl in the OSPAR maritime area.Crossref | GoogleScholarGoogle Scholar | 25111057PubMed |

Pascelli, C., Riul, P., Riosmena-Rodríguez, R., Scherner, F., Nunes, M., Hall-Spencer, J. M., Cabral de Oliveira, E., and Horta, P. (2013). Seasonal and depth-driven changes in rhodolith bed structure and associated macroalgae off Arvoredo island (southeastern Brazil). Aquatic Botany 111, 62–65.
Seasonal and depth-driven changes in rhodolith bed structure and associated macroalgae off Arvoredo island (southeastern Brazil).Crossref | GoogleScholarGoogle Scholar |

Peña, V., and Bárbara, I. (2008). Maërl community in the north-western Iberian Peninsula: a review of floristic studies and long-term changes. Aquatic Conservation 18, 339–366.
Maërl community in the north-western Iberian Peninsula: a review of floristic studies and long-term changes.Crossref | GoogleScholarGoogle Scholar |

Pérès, J. M. (1967). The Mediterranean benthos. Oceanography and Marine Biology - An Annual Review 5, 449–533.

Png-Gonzalez, L., Vázquez-Luis, M., and Tuya, F. (2014). Comparison of epifaunal assemblages between Cymodocea nodosa and Caulerpa prolifera meadows in Gran Canaria (eastern Atlantic). Journal of the Marine Biological Association of the United Kingdom 94, 241–253.
Comparison of epifaunal assemblages between Cymodocea nodosa and Caulerpa prolifera meadows in Gran Canaria (eastern Atlantic).Crossref | GoogleScholarGoogle Scholar |

Riera, R., Tuya, F., Rodríguez, M., Monterroso, Ó., and Ramos, E. (2013). Confounding response of macrofauna from a confluence of impacts: brine and sewage pollution. Acta Oceanologica Sinica 32, 74–81.
Confounding response of macrofauna from a confluence of impacts: brine and sewage pollution.Crossref | GoogleScholarGoogle Scholar |

Riosmena-Rodríguez, R., and Medina-López, M. A. (2010). The role of rhodolith beds in the recruitment of invertebrate species from the southwestern Gulf of California, Mexico. In ‘Seaweeds and their Role in Globally Changing Environments’. pp. 127–138. (Springer: Dordrecht, Netherlands.)

Riosmena-Rodríguez, R., Nelson, W., and Aguirre, J. (Eds) (2017). ‘Rhodolith/maërl Beds: a Global Perspective.’ (Springer International Publishing: Basel, Switzerland.)

Ruffo, S. (1982). ‘The Amphipoda of the Mediterranean. Part 1: Gammaridea (Acanthonotozomatidae to Gammaridae).’ Mémoires de l’Institut Océanographique, Monaco 13, p. 364. Prince de Monaco (Monaco).

Sainte-Marie, B. (1991). A review of the reproductive bionomics of aquatic gammaridean amphipods: variation of life history traits with latitude, depth, salinity and superfamily. Hydrobiologia 223, 189–227.

Sanchez-Jerez, P. (1997). Distribución espacio-temporal de la epifauna vágil asociada a praderas de Posidonia oceanica y Cymodocea nodosa (Sudeste Ibérico). Doctoral Dissertation, Universitat d’Alacant – Universidad de Alicante, Spain.

Sánchez-Moyano, J., García-Asencio, I., and Carlos García-Gómez, J. (2007). Effects of temporal variation of the seaweed Caulerpa prolifera cover on the associated crustacean community. Marine Ecology 28, 324–337.
Effects of temporal variation of the seaweed Caulerpa prolifera cover on the associated crustacean community.Crossref | GoogleScholarGoogle Scholar |

Sciberras, M., Rizzo, M., Mifsud, J. R., Camilleri, K., Borg, J. A., Lanfranco, E., and Schembri, P. J. (2009). Habitat structure and biological characteristics of a maerl bed off the northeastern coast of the Maltese Islands (central Mediterranean). Marine Biodiversity 39, 251–264.
Habitat structure and biological characteristics of a maerl bed off the northeastern coast of the Maltese Islands (central Mediterranean).Crossref | GoogleScholarGoogle Scholar |

Steller, D. L., and Foster, M. S. (1995). Environmental factors influencing distribution and morphology of rhodoliths in Bahía Concepción, BCS, México. Journal of Experimental Marine Biology and Ecology 194, 201–212.
Environmental factors influencing distribution and morphology of rhodoliths in Bahía Concepción, BCS, México.Crossref | GoogleScholarGoogle Scholar |

Steller, D. L., Hernández-Ayón, J. M., Riosmena-Rodríguez, R., and Cabello-Pasini, A. (2007). Effect of temperature on photosynthesis, growth and calcification rates of the free-living coralline alga Lithophyllum margaritae. Ciencias Marinas 33, 441–456.
Effect of temperature on photosynthesis, growth and calcification rates of the free-living coralline alga Lithophyllum margaritae.Crossref | GoogleScholarGoogle Scholar |

Steneck, R. S. (1986). The ecology of coralline algal crusts: convergent patterns and adaptative strategies. Annual Review of Ecology and Systematics 17, 273–303.
The ecology of coralline algal crusts: convergent patterns and adaptative strategies.Crossref | GoogleScholarGoogle Scholar |

Taylor, R. B., and Cole, R. G. (1994). Mobile epifauna on subtidal brown sea-weeds in northeastern New Zealand. Marine Ecology Progress Series 115, 271–282.
Mobile epifauna on subtidal brown sea-weeds in northeastern New Zealand.Crossref | GoogleScholarGoogle Scholar |

Teichert, S. (2015). Hollow rhodoliths increase Svalbard’s shelf biodiversity. Scientific Reports 4, 6972.
Hollow rhodoliths increase Svalbard’s shelf biodiversity.Crossref | GoogleScholarGoogle Scholar |

Thiel, M. (1998). Reproductive biology of a deposit-feeding amphipod, Casco bigelowi, with extended parental care. Marine Biology 132, 107–116.
Reproductive biology of a deposit-feeding amphipod, Casco bigelowi, with extended parental care.Crossref | GoogleScholarGoogle Scholar |

Thomsen, M. S. (2010). Experimental evidence for positive effects of invasive seaweed on native invertebrates via habitat-formation in a seagrass bed. Aquatic Invasions 5, 341–346.
Experimental evidence for positive effects of invasive seaweed on native invertebrates via habitat-formation in a seagrass bed.Crossref | GoogleScholarGoogle Scholar |

Thomsen, M. S., Wernberg, T., Altieri, A., Tuya, F., Gulbransen, D., McGlathery, K. J., Holmer, M., and Silliman, B. R. (2010). Habitat cascades: the conceptual context and global relevance of facilitation cascades via habitat formation and modification. Integrative and Comparative Biology 50, 158–175.
Habitat cascades: the conceptual context and global relevance of facilitation cascades via habitat formation and modification.Crossref | GoogleScholarGoogle Scholar | 21558196PubMed |

Tuya, F., Cisneros-Aguirre, J., Ortega-Borges, L., and Haroun, R. J. (2007). Bathymetric segregation of sea urchins on reefs of the Canarian Archipelago: role of flow-induced forces. Estuarine, Coastal and Shelf Science 73, 481–488.
Bathymetric segregation of sea urchins on reefs of the Canarian Archipelago: role of flow-induced forces.Crossref | GoogleScholarGoogle Scholar |

Vázquez-Luis, M., Sanchez-Jerez, P., and Bayle-Sempere, J. T. (2009). Comparison between amphipod assemblages associated with Caulerpa racemosa var. cylindracea and those of other Mediterranean habitats on soft substrate. Estuarine, Coastal and Shelf Science 84, 161–170.
Comparison between amphipod assemblages associated with Caulerpa racemosa var. cylindracea and those of other Mediterranean habitats on soft substrate.Crossref | GoogleScholarGoogle Scholar |

Wang, Y., Neuman, U., Wright, S., and Warton, D. I. (2012). mvabund: an R package for model-based analysis of multivariate abundance data. Methods in Ecology and Evolution 3, 471–474.
mvabund: an R package for model-based analysis of multivariate abundance data.Crossref | GoogleScholarGoogle Scholar |

Zakhama-Sraieb, R., Sghaier, Y. R., and Charfi-Cheikhrouha, F. (2011). Community structure of amphipods on shallow Posidonia oceanica meadows off Tunisian coasts. Helgoland Marine Research 65, 203–209.
Community structure of amphipods on shallow Posidonia oceanica meadows off Tunisian coasts.Crossref | GoogleScholarGoogle Scholar |

Zimmerman, R., Gibson, R., and Harrington, J. (1979). Herbivory and detritivory among gammaridean amphipods from a Florida seagrass community. Marine Biology 54, 41–47.
Herbivory and detritivory among gammaridean amphipods from a Florida seagrass community.Crossref | GoogleScholarGoogle Scholar |