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RESEARCH ARTICLE

Spatial variability and human disturbance of sponge assemblages associated with mangrove roots in the southern Caribbean

Edlin Guerra-Castro A B E , Paula Young B , Adriana Pérez-Vázquez B , Sophie Carteron C and Adriana Alvizu D
+ Author Affiliations
- Author Affiliations

A Centro de Ecología, Instituto Venezolano de Investigaciones Científicas, POB 21827, Caracas 1020-A, Venezuela.

B Escuela de Ciencias Aplicadas del Mar, Universidad de Oriente, Núcleo Nueva Esparta, Boca de Río, Isla de Margarita, Venezuela.

C Centre d’Océanologie de Marseille, Université de la Mediterranée, 13007 Marseille, France.

D Departamento de Biología de Organismos, Universidad Simón Bolívar, Caracas 1080-A, Venezuela.

E Corresponding author. Email: eguerra@ivic.gob.ve

Marine and Freshwater Research 62(5) 491-501 https://doi.org/10.1071/MF10267
Submitted: 28 October 2010  Accepted: 11 March 2011   Published: 25 May 2011

Abstract

Assemblages growing on Caribbean red-mangrove roots are very diverse and characteristically dominated by sponges. The scales of spatial variation of this fauna in the Caribbean region have not been hierarchically quantified, although such information is necessary to understand the relative importance of ecological processes and possible responses to anthropogenic disturbances. We used a hierarchical nested design to identify patterns of spatial variability at different scales, namely among roots, sites, localities and regions within the southern Caribbean. Simultaneously, the sampling considered the relative distance from sources of human disturbance to test the null hypothesis of no difference in sponge diversity among localities as a result of anthropogenic stress. Significant spatial variability in species composition was detected at all spatial scales, especially at the among-root scale. However, there were no differences associated with distance from human disturbance. These results indicate high regional and local β diversity, and also suggest that results from small-scale experiments cannot be scaled up to the entire community. Further, spatial analysis of sponge assemblages is not enough to detect deleterious effects of human disturbances on mangrove areas.

Additional keywords: beta diversity, management, spatial scales, taxonomic distinctness, variance components.


References

Allen, T. F. H., and Starr, T. B. (1982). ‘Hierarchy: Perspectives for Ecological Complexities.’ (University of Chicago Press: Chicago, IL.)

Álvarez, A. (1989). Establecimiento, desarrollo y mantenimiento de una comunidad epibentónica tropical. Ph.D. Thesis, Universidad Central de Venezuela, Caracas.

Anderson, M. J. (2001). A new method for non-parametric multivariate analysis of variance. Austral Ecology 26, 32–46.

Anderson, M. J. (2006). Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62, 245–253.
Distance-based tests for homogeneity of multivariate dispersions.Crossref | GoogleScholarGoogle Scholar | 16542252PubMed |

Anderson, M. J., Diebel, C. E., Blom, W. M., and Landers, T. J. (2005). Consistency and variation in kelp holdfast assemblages: spatial patterns of biodiversity for the major phyla at different taxonomic resolutions. Journal of Experimental Marine Biology and Ecology 320, 35–56.
Consistency and variation in kelp holdfast assemblages: spatial patterns of biodiversity for the major phyla at different taxonomic resolutions.Crossref | GoogleScholarGoogle Scholar |

Anderson, M. J., Gorley, R. N., and Clarke, K. R. (2008). ‘PERMANOVA for PRIMER: Guide to Software and Statistical Methods.’ (PRIMER-E Ltd: Plymouth, UK.)

Anderson, M. J., Crist, T. O., Chase, J. M., Vellend, M., Inouye, B. D., et al. (2010). Navigating the multiple meanings of β diversity: a roadmap for the practicing ecologist. Ecology Letters 14, 19–28.
Navigating the multiple meanings of β diversity: a roadmap for the practicing ecologist.Crossref | GoogleScholarGoogle Scholar | 21070562PubMed |

Barnes, P. B., Davis, A. R., and Roberts, D. E. (2006). Sampling patchily distributed taxa: a case study using cost–benefit analyses for sponges and ascidians in coastal lakes of New South Wales, Australia. Marine Ecology Progress Series 319, 55–64.
Sampling patchily distributed taxa: a case study using cost–benefit analyses for sponges and ascidians in coastal lakes of New South Wales, Australia.Crossref | GoogleScholarGoogle Scholar |

Benedetti-Cecchi, L. (2001). Variability in abundance of algae and invertebrates at different spatial scales on rocky sea shores. Marine Ecology Progress Series 215, 79–92.
Variability in abundance of algae and invertebrates at different spatial scales on rocky sea shores.Crossref | GoogleScholarGoogle Scholar |

Benedetti-Cecchi, L., Bertocci, I., Micheli, F., Maggi, E., Fosella, T., et al. (2003). Implications of spatial heterogeneity for management of marine protected areas (MPAs): examples from assemblages of rocky coasts in the northwest Mediterranean. Marine Environmental Research 55, 429–458.
Implications of spatial heterogeneity for management of marine protected areas (MPAs): examples from assemblages of rocky coasts in the northwest Mediterranean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhs1Wrs70%3D&md5=1f7d7856ebaa012f4c07c08b80308739CAS | 12628195PubMed |

Bingham, B. L. (1992). Life histories in an epifaunal community: coupling of adult and larval processes. Ecology 73, 2244–2259.
Life histories in an epifaunal community: coupling of adult and larval processes.Crossref | GoogleScholarGoogle Scholar |

Bingham, B. L., and Young, C. M. (1995). Stochastic events and dynamics of a mangrove root epifaunal community. Marine Ecology (Berlin) 16, 145–163.
Stochastic events and dynamics of a mangrove root epifaunal community.Crossref | GoogleScholarGoogle Scholar |

Bone, D., Cróquer, A., Klein, E., Pérez, D., Losada, F., et al. (2001). Programa CARICOMP: monitoreo a largo plazo de los ecosistemas marinos del Parque Nacional Morrocoy, Venezuela. Interciencia 26, 457–462.

Carballo, J. L., Naranjo, S. A., and García-Gómez, J. C. (1996). Use of marine sponges as stress indicators in marine ecosystems at Algeciras Bay (southern Iberian Peninsula). Marine Ecology Progress Series 135, 109–122.
Use of marine sponges as stress indicators in marine ecosystems at Algeciras Bay (southern Iberian Peninsula).Crossref | GoogleScholarGoogle Scholar |

Clarke, K. R. (1993). Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18, 117–143.
Non-parametric multivariate analyses of changes in community structure.Crossref | GoogleScholarGoogle Scholar |

Clarke, K. R., Somerfield, P. J., and Chapman, M. G. (2006). On resemblance measures for ecological studies, including taxonomic dissimilarities and a zero-adjusted Bray–Curtis coefficient for denuded assemblages. Journal of Experimental Marine Biology and Ecology 330, 55–80.
On resemblance measures for ecological studies, including taxonomic dissimilarities and a zero-adjusted Bray–Curtis coefficient for denuded assemblages.Crossref | GoogleScholarGoogle Scholar |

Cruz-Mota, J. J. (2007). Spatial analysis of intertidal tropical assemblages associated with rocky shores in Venezuela. Ciencias Marinas 33, 133–148.

D’Croz, L., Del Rosario, J. B., and Góndola, P. (2005). The effect of fresh water runoff on the distribution of dissolved inorganic nutrients and plankton in the Bocas del Toro Archipielago, Caribbean Panama. Caribbean Journal of Science 41, 414–429.

Díaz, M. C., and Rützler, K. (2009). Biodiversity and abundance of sponges in Caribbean mangrove: indicators of environmental quality. In ‘Proceedings of the Smithsonian Marine Science Symposium’. (Eds M. A. Lang, I. G. Macintyre and K. Rützler.) pp. 151–172. (Smithsonian Institution Scholarly Press: Washington, DC.)

Díaz, M. C., Smith, K. P., and Rützler, K. (2004). Sponge species richness and abundance as indicators of mangrove epibenthic community health. Atoll Research Bulletin 518, 1–17.

Ellison, A. M., and Farnsworth, E. J. (1992). The ecology of Belizean mangrove-root fouling communities: patterns of epibiont distribution and abundance, and effects on root growth. Hydrobiologia 247, 87–98.
The ecology of Belizean mangrove-root fouling communities: patterns of epibiont distribution and abundance, and effects on root growth.Crossref | GoogleScholarGoogle Scholar |

Ellison, A. M., and Farnsworth, E. J. (1996). Anthropogenic disturbance of Caribbean mangrove ecosystems: past impacts, present trends, and future predictions. Biotropica 28, 549–565.
Anthropogenic disturbance of Caribbean mangrove ecosystems: past impacts, present trends, and future predictions.Crossref | GoogleScholarGoogle Scholar |

Ellison, A. M., and Farnsworth, E. J. (2001). Mangrove communities. In ‘Marine Community Ecology’. (Eds M. D. Bertness, S. D. Gaines and M. Hay.) pp. 423–442. (Sinauer Associates: Sunderland, MA.)

Farnsworth, E. J., and Ellison, A. M. (1996). Scale-dependent spatial and temporal variability in biogeography of mangrove root epibiont communities. Ecological Monographs 66, 45–66.
Scale-dependent spatial and temporal variability in biogeography of mangrove root epibiont communities.Crossref | GoogleScholarGoogle Scholar |

Faul, F., Erdfelder, E., Lang, A.-G., and Buchner, A. (2007). G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behavior Research Methods 39, 175–191.
G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences.Crossref | GoogleScholarGoogle Scholar | 17695343PubMed |

Fraschetti, S., Bianchi, C. N., Terlizzi, A., Fanelli, G., Morri, C., et al. (2001). Spatial variability and human disturbance in shallow subtidal hard substrate assemblages: a regional approach. Marine Ecology Progress Series 212, 1–12.
Spatial variability and human disturbance in shallow subtidal hard substrate assemblages: a regional approach.Crossref | GoogleScholarGoogle Scholar |

Garrity, S. D., and Levings, S. C. (1993). Effects of an oil spill on some organisms living on mangrove (Rhizophora mangle L.) roots in low wave-energy habitats in Caribbean Panama. Marine Environmental Research 35, 251–271.
Effects of an oil spill on some organisms living on mangrove (Rhizophora mangle L.) roots in low wave-energy habitats in Caribbean Panama.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXhvVGgtro%3D&md5=ad9d662309649e4221a9349a7b75be05CAS |

Gaston, K. J., and Chown, S. (2005). Neutrality and the niche. Functional Ecology 19, 1–6.
Neutrality and the niche.Crossref | GoogleScholarGoogle Scholar |

Gill, A. M., and Tomlinson, P. B. (1977). Studies on the growth of red mangrove (Rhizophora mangle L.) 4. The adult root system. Biotropica 9, 145–155.
Studies on the growth of red mangrove (Rhizophora mangle L.) 4. The adult root system.Crossref | GoogleScholarGoogle Scholar |

Glasby, T. M. (1998). Estimating spatial variability in developing assemblages of epibiota on subtidal hard substrata. Marine and Freshwater Research 49, 429–437.
Estimating spatial variability in developing assemblages of epibiota on subtidal hard substrata.Crossref | GoogleScholarGoogle Scholar |

Gómez Gaspar, A. (1991). Interacción entre un estuario negativo (Laguna de La Restinga, Isla de Margarita) y el mar Caribe adyacente. Boletín del Instituto Oceanográfico de Venezuela 30, 47–55.

Hunter, J. E., and Schmidt, F. L. (2004). ‘Methods of Meta Analysis: Correcting Error and Bias in Research Findings.’ (Sage Publications: Sage, CA, USA.)

Hunting, E. R., van Soest, R. W. M., van der Geest, H. G., Vos, A., and Debrot, A. O. (2008). Diversity and spatial heterogeneity of mangrove associated sponges of Curaçao and Aruba. Contributions to Zoology (Amsterdam, Netherlands) 77, 205–215.

Hunting, E. R., van der Geest, H., Krieg, A., van Mierlo, M., and van Soest, R. (2010). Mangrove–sponge associations: a possible role for tannins. Aquatic Ecology 44, 679–684.
Mangrove–sponge associations: a possible role for tannins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVahtLfK&md5=f8d7724054a26098381e54239ff43a05CAS |

Inclán Rivadeneyra, R. (1989). Ecology of the epibiosis on the submerged roots of Rhizophora mangle in Bahía de la Ascensión, Quintana Roo, México. Ciencias Marinas 15, 1–20.

Lacerda, L. D., Conde, J. E., Kjerfve, J. E., Alvarez-León, R., Alarcón, C., et al. (2002). American mangroves. In ‘Mangrove Ecosystems: Function and Management’. (Ed. L. D. Lacerda.) pp. 1–62. (Springer-Verlag: Berlin.)

Legendre, P., Borcard, D., and Peres-Neto, P. R. (2005). Analyzing beta diversity: partitioning the spatial variation of community composition data. Ecological Monographs 75, 435–450.
Analyzing beta diversity: partitioning the spatial variation of community composition data.Crossref | GoogleScholarGoogle Scholar |

Lewin, R. (1986). Supply-side ecology. Science 234, 25–27.
Supply-side ecology.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cvitFSntw%3D%3D&md5=d498476e827d80696d657ce1d5c76b57CAS | 17742631PubMed |

Liebold, M. A. (1995). The niche concept revisited: Mechanistic models and community context. Ecology 76, 1371–1382.
The niche concept revisited: Mechanistic models and community context.Crossref | GoogleScholarGoogle Scholar |

López, B., Vera, B., and Conde, J. E. (2009). Macroalgas asociadas a las raíces de Rhizophora mangle L. en la península de Paraguaná, estado Falcón, Venezuela. Boletín del Instituto Oceanográfico de Venezuela 48, 11–21.

Nagelkerken, I., Blaber, S. J. M., Bouillon, S., Green, P., Haywood, M., et al. (2008). The habitat function of mangroves for terrestrial and marine fauna: a review. Aquatic Botany 89, 155–185.
The habitat function of mangroves for terrestrial and marine fauna: a review.Crossref | GoogleScholarGoogle Scholar |

Orihuela, B., Díaz, H., and Conde, J. E. (1991). Mass mortality in a mangrove roots fouling community in a hypersaline tropical lagoon. Biotropica 23, 592–601.
Mass mortality in a mangrove roots fouling community in a hypersaline tropical lagoon.Crossref | GoogleScholarGoogle Scholar |

Pawlik, J. R., McMurray, S. E., and Henkel, T. P. (2007). Abiotic factors control sponge ecology in Florida mangroves. Marine Ecology Progress Series 339, 93–98.
Abiotic factors control sponge ecology in Florida mangroves.Crossref | GoogleScholarGoogle Scholar |

Ricklefs, R. E. (2008). Disintegration of the ecological community. American Naturalist 172, 741–750.
Disintegration of the ecological community.Crossref | GoogleScholarGoogle Scholar | 18954264PubMed |

Rocha, R. M., Guerra-Castro, E., Lira, C., Pauls, S. M., Hernández, I., et al. (2010). Inventory of ascidians (Tunicata, Ascidiacea) from the National Park La Restinga, Isla Margarita, Venezuela. Results from a NaGISA workshop. Biota Neotropica 10, 1–10.
Inventory of ascidians (Tunicata, Ascidiacea) from the National Park La Restinga, Isla Margarita, Venezuela. Results from a NaGISA workshop.Crossref | GoogleScholarGoogle Scholar |

Rützler, K. (1969). The mangrove communitie, aspects of its structure, faunistics and ecology. In ‘Lagunas Costeras’. (Eds A. Ayala-Castañares and F. B. Phleger.) pp. 515–535. (UNAM-UNESCO: México, DF.)

Rützler, K. (1995). Low-tide exposure of sponges in a Caribbean Mangrove Community. Marine Ecology (Berlin) 16, 165–179.
Low-tide exposure of sponges in a Caribbean Mangrove Community.Crossref | GoogleScholarGoogle Scholar |

Spalding, M. D., Fox, H. E., Allen, G. R., Davidson, N., Ferdaña, Z. A., et al. (2007). Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. BioScience 57, 573–583.
Marine ecoregions of the world: a bioregionalization of coastal and shelf areas.Crossref | GoogleScholarGoogle Scholar |

Sutherland, J. P. (1980). Dynamics of the epibentics communiy on roots of the mangrove Rhizophora mangle, at Bahía de Buche, Venezuela. Marine Biology 58, 75–84.
Dynamics of the epibentics communiy on roots of the mangrove Rhizophora mangle, at Bahía de Buche, Venezuela.Crossref | GoogleScholarGoogle Scholar |

Underwood, A. J. (1991). Beyond BACI: experimental designs for detecting human environmental impacts on temporal variations in natural populations. Australian Journal of Marine and Freshwater Research 42, 569–587.
Beyond BACI: experimental designs for detecting human environmental impacts on temporal variations in natural populations.Crossref | GoogleScholarGoogle Scholar |

Underwood, A. J. (1997). ‘Experiments in Ecology: Their Logical Design and Interpretation Using Analysis of Variance.’ (Cambridge University Press: Cambridge, UK.)

Underwood, A. J., and Chapman, M. G. (1996). Scales of spatial patterns of distribution of intertidal invertebrates. Oecologia 107, 212–224.
Scales of spatial patterns of distribution of intertidal invertebrates.Crossref | GoogleScholarGoogle Scholar |

Underwood, A. J., and Chapman, M. G. (2003). Power, precaution, Type II error and sampling design in assessment of environmental impacts. Journal of Experimental Marine Biology and Ecology 296, 49–70.
Power, precaution, Type II error and sampling design in assessment of environmental impacts.Crossref | GoogleScholarGoogle Scholar |

Underwood, A. J., and Fairweather, P. G. (1989). Supply-side ecology and benthic marine assemblages. Trends in Ecology & Evolution 4, 16–20.
Supply-side ecology and benthic marine assemblages.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7gvFeqsw%3D%3D&md5=846d8e8d322a618e005aa02e67d79818CAS | 21227303PubMed |

Underwood, A. J., Chapman, M. G., and Connell, S. D. (2000). Observations in ecology: you can’t make progress on processes without understanding the patterns. Journal of Experimental Marine Biology and Ecology 250, 97–115.
Observations in ecology: you can’t make progress on processes without understanding the patterns.Crossref | GoogleScholarGoogle Scholar | 10969165PubMed |

van Soest, R. W. M., Boury-Esnault, N., Hooper, J. N. A., Rützler, K., de Voogd, N. J., et al. (2008). World Porifera database. Available at http://www.marinespecies.org/porifera [accessed 15 February 2011].

Waddell, B., and Pawlik, J. R. (2000). Defenses of Caribbean sponges against invertebrate predators. II. Assays with sea stars. Marine Ecology Progress Series 195, 133–144.
Defenses of Caribbean sponges against invertebrate predators. II. Assays with sea stars.Crossref | GoogleScholarGoogle Scholar |

Warwick, R. M., and Clarke, K. R. (1995). New ‘biodiversity’ measures reveal a decrease in taxonomic distinctness with increasing stress. Marine Ecology Progress Series 129, 301–305.
New ‘biodiversity’ measures reveal a decrease in taxonomic distinctness with increasing stress.Crossref | GoogleScholarGoogle Scholar |

Warwick, R. M., and Clarke, K. R. (2001). Practical measures of marine biodiversity based on relatedness of species. Oceanography and Marine Biology: an Annual Review 39, 207–231.

Wulff, J. L. (2000). Sponge predators may determine differences in sponge fauna between two sets of mangrove cays, Belize Barrier Reef. Atoll Research Bulletin 477, 250–263.

Wulff, J. L. (2005). Trade-offs in resistance to competitors and predators, and their effects on the diversity of tropical marine sponges. Journal of Animal Ecology 74, 313–321.
Trade-offs in resistance to competitors and predators, and their effects on the diversity of tropical marine sponges.Crossref | GoogleScholarGoogle Scholar |