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Influence of canopy-forming algae on temperate sponge assemblages

Published online by Cambridge University Press:  28 January 2015

César A. Cárdenas ,
Simon K. Davy  and
James J. Bell
César A. Cárdenas*
Affiliation:
School of Biological Sciences, Victoria University of Wellington, P.O. Box 600, Wellington 6140, New Zealand Departamento Científico, Instituto Antártico Chileno (INACH), Plaza Muñoz Gamero 1055, Punta Arenas 6200965, Chile
Simon K. Davy
Affiliation:
School of Biological Sciences, Victoria University of Wellington, P.O. Box 600, Wellington 6140, New Zealand
James J. Bell
Affiliation:
School of Biological Sciences, Victoria University of Wellington, P.O. Box 600, Wellington 6140, New Zealand
*
Correspondence should be addressed to:C.A. Cárdenas, Departamento Científico, Instituto Antártico Chileno (INACH), Plaza Muñoz Gamero 1055, Punta Arenas 6200965, Chile email: [email protected]
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Abstract

Experimental removals of the dominant canopy-forming kelp Ecklonia radiata were conducted at two sites on rocky walls in New Zealand and monitored for approximately 1.5 years. We hypothesized that the removal of the E. radiata canopy would affect the structure of subcanopy assemblages, such that there would be a reduction in sponge species richness and abundance. Furthermore, we investigated the biological and physical (predictor) variables that best explained variability in sponge assemblages after canopy removal. Canopy removal led to a community dominated by turf algae, which corresponded with a decrease in sponge abundance and richness. Our results suggest that the Ecklonia canopy may positively influence the presence of sponge species such as Crella incrustans; we propose that the canopy may allow its coexistence with turf algae underneath the canopy by altering the light regime and other environmental factors, which may be detrimental for some species. Our results highlight how any loss of canopy-forming species might have negative effects on sponge assemblages, which could affect the energy flow and the overall biodiversity found in these habitats.

Keywords

spongesCrella incrustansEcklonia radiatamacroalgaecanopy-algaefacilitationcompetitionrocky walls
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 96 , Issue 2: Proceedings of the 9th World Sponge Conference held in Fremantle Australia in 2013: New Frontiers in Sponge Science , March 2016 , pp. 351 - 362
Copyright
Copyright © Marine Biological Association of the United Kingdom 2015 

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References

REFERENCES

Airoldi, L. (2003) The effects of sedimentation on rocky coast assemblages. Oceanography and Marine Biology: An Annual Review 41, 161–236.Google Scholar
Anderson, M.J., Gorley, R.N. and Clarke, K.R. (2008) Permanova for primer: guide to software and statistical methods. Plymouth: PRIMER-E.Google Scholar
Arkema, K.K., Reed, D.C. and Schroeter, S.C. (2009) Direct and indirect effects of giant kelp determine benthic community structure and dynamics. Ecology 90, 3126–3137.CrossRefGoogle ScholarPubMed
Ávila, E., Blancas-Gallangos, N.I., Riosmena-Rodríguez, R. and Paul-Chávez, L. (2010) Sponges associated with Sargassum spp. (Phaeophyceae: Fucales) from the south-western Gulf of California. Journal of the Marine Biological Association of the United Kingdom 90, 193–202.CrossRefGoogle Scholar
Ayling, A.L. (1983) Growth and regeneration rates in thinly encrusting demospongiae from temperate waters. Biological Bulletin 165, 343–352.CrossRefGoogle ScholarPubMed
Barott, K.L., Williams, G.J., Vermeij, M.J.A., Harris, J., Smith, J.E., Rohwer, F.L. and Sandin, S.A. (2012) Natural history of coral–algae competition across a gradient of human activity in the Line Islands. Marine Ecology Progress Series 460, 1–12.CrossRefGoogle Scholar
Bell, J.J. (2002) The sponge community in a semi-submerged temperate sea cave: density, diversity and richness. Marine Ecology 23, 297–311.CrossRefGoogle Scholar
Bell, J.J. (2007) The ecology of sponges in Lough Hyne Marine Nature Reserve (south-west Ireland): past, present and future perspectives. Journal of the Marine Biological Association of the United Kingdom 87, 1655–1668.CrossRefGoogle Scholar
Bell, J.J. (2008) The functional roles of marine sponges. Estuarine, Coastal and Shelf Science 79, 341–353.CrossRefGoogle Scholar
Bell, J.J. and Barnes, D.K.A. (2000a) The distribution and prevalence of sponges in relation to environmental gradients within a temperate sea lough: inclined cliff surfaces. Diversity and Distributions 6, 305–323.CrossRefGoogle Scholar
Bell, J.J. and Barnes, D.K.A. (2000b) A sponge diversity centre within a marine ‘island’. Hydrobiologia 440, 55–64.CrossRefGoogle 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.CrossRefGoogle Scholar
Benedetti-Cecchi, L., Pannacciulli, F., Bulleri, F., Moschella, P.S., Airoldi, L., Relini, G. and Cinelli, F. (2001) Predicting the consequences of anthropogenic disturbance: large-scale effects of loss of canopy algae on rocky shores. Marine Ecology Progress Series 214, 134–150.CrossRefGoogle Scholar
Berman, J. and Bell, J.J. (2010) Spatial variability of sponge assemblages on the Wellington South Coast, New Zealand. Open Journal of Marine Biology 4, 12–25.CrossRefGoogle Scholar
Bertness, M.D. and Callaway, R. (1994) Positive interactions in communities. Trends in Ecology and Evolution 9, 191–193.CrossRefGoogle ScholarPubMed
Bertness, M.D. and Leonard, G.H. (1997) The role of positive interactions in communities: lessons from intertidal habitats. Ecology 78, 1976–1989.CrossRefGoogle Scholar
Bertness, M.D., Leonard, G.H., Levine, J.M., Schmidt, P.R. and Ingraham, A.O. (1999) Testing the relative contribution of positive and negative interactions in rocky intertidal communities. Ecology 80, 2711–2726.CrossRefGoogle Scholar
Bonanomi, G., Incerti, G. and Mazzoleni, S. (2011) Assessing occurrence, specificity, and mechanisms of plant facilitation in terrestrial ecosystems. Plant Ecology 212, 1777–1790.CrossRefGoogle Scholar
Bruno, J.F. and Bertness, M.D. (2001) Habitat modification and facilitation in benthic marine communities. In Bertness, M.D., Gaine, S.D. and Hay, M.E. (eds) Marine community ecology. Sunderland, MA: Sinauer, pp. 201–218.Google Scholar
Bruno, J.F., Stachowicz, J.J. and Bertness, M.D. (2003) Inclusion of facilitation into ecological theory. Trends in Ecology and Evolution 18, 119–125.CrossRefGoogle Scholar
Bulleri, F. (2009) Facilitation research in marine systems: state of the art, emerging patterns and insights for future developments. Journal of Ecology 97, 1121–1130.CrossRefGoogle Scholar
Bulleri, F., Benedetti-Cecchi, L., Acunto, S., Cinelli, F. and Hawkins, S.J. (2002) The influence of canopy algae on vertical patterns of distribution of low-shore assemblages on rocky coasts in the northwest Mediterranean. Journal of Experimental Marine Biology and Ecology 267, 89–106.CrossRefGoogle Scholar
Burnham, K.P. and Anderson, D.R. (2002) Model selection and multi-model inference: a practical information-theoretic approach. New York, NY: Springer-Verlag.Google Scholar
Cárdenas, C.A., Bell, J.J., Davy, S.K., Hoggard, M. and Taylor, M.W. (2014) Influence of environmental variation on symbiotic bacterial communities of two temperate sponges. FEMS Microbiology Ecology 88, 516–527.CrossRefGoogle ScholarPubMed
Cárdenas, C.A., Davy, S.K. and Bell, J.J. (2012) Correlations between algal abundance, environmental variables and sponge distribution patterns on southern hemisphere temperate rocky reefs. Aquatic Biology 16, 229–239.CrossRefGoogle Scholar
Carter, L. and Lewis, K. (1995) Variability of the modern sand cover on a tide and storm driven inner shelf, south Wellington, New Zealand. New Zealand Journal of Geology and Geophysics 38, 451–470.CrossRefGoogle Scholar
Choat, J.H. and Schiel, D.R. (1982) Patterns of distribution and abundance of large brown algae and invertebrate herbivores in subtidal regions of northern New Zealand. Journal of Experimental Marine Biology and Ecology 60, 129–162.CrossRefGoogle Scholar
Clarke, K.R. (1993) Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18, 117–143.CrossRefGoogle Scholar
Clarke, K.R. and Gorley, R.N. (2006) Primer v6: user manual/tutorial. Plymouth: PRIMER-E.Google Scholar
Clarke, K.R., Somerfield, P.J., Airoldi, L. and Warwick, R.M. (2006) Exploring interactions by second-stage community analyses. Journal of Experimental Marine Biology and Ecology 338, 179–192.CrossRefGoogle Scholar
Connell, J.H. (1983) On the prevalence and relative importance of interspecific competition: evidence from field experiments. American Naturalist 122, 661–696.CrossRefGoogle Scholar
Connell, S.D. (2003a) The monopolization of understorey habitat by subtidal encrusting coralline algae: a test of the combined effects of canopy-mediated light and sedimentation. Marine Biology 142, 1065–1071.CrossRefGoogle Scholar
Connell, S.D. (2003b) Negative effects overpower the positive of kelp to exclude invertebrates from the understorey community. Oecologia 137, 97–103.CrossRefGoogle ScholarPubMed
Davis, A.R., Fyfe, S.K., Turon, X. and Uriz, M.J. (2003) Size matters sometimes: wall height and the structure of subtidal benthic invertebrate assemblages in south-eastern Australia and Mediterranean Spain. Journal of Biogeography 30, 1797–1807.CrossRefGoogle Scholar
Dayton, P.K. (1975) Experimental evaluation of ecological dominance in a rocky intertidal algal community. Ecological Monographs 45, 137–159.CrossRefGoogle Scholar
Dayton, P.K. (1985a) Ecology of kelp communities. Annual Review of Ecology and Systematics 16, 215–245.CrossRefGoogle Scholar
Dayton, P.K. (1985b) The structure and regulation of some South American kelp communities. Ecological Monographs 55, 447–468.CrossRefGoogle Scholar
Dayton, P.K., Robilliard, G.A., Paine, R.T. and Dayton, L.B. (1974) Biological accommodation in the benthic community at McMurdo Sound, Antarctica. Ecological Monographs 44, 105–128.CrossRefGoogle Scholar
Duggins, D., Eckman, J.E. and Sewell, A.T. (1990) Ecology of understory kelp environments. II. Effects of kelps on recruitment of benthic invertebrates. Journal of Experimental Marine Biology and Ecology 143, 27–45.CrossRefGoogle Scholar
Duggins, D.O. and Eckman, J.E. (1997) Is kelp detritus a good food for suspension feeders? Effects of kelp species, age and secondary metabolites. Marine Biology 128, 489–495.CrossRefGoogle Scholar
Eckman, J.E. and Duggins, D.O. (1991) Life and death beneath macrophyte canopies: effects of understory kelps on growth rates and survival of marine, benthic suspension feeders. Oecologia 87, 473–487.CrossRefGoogle ScholarPubMed
Edgar, G.J., Barrett, N.S., Morton, A.J. and Samson, C.R. (2004) Effects of algal canopy clearance on plant, fish and macroinvertebrate communities on eastern Tasmanian reefs. Journal of Experimental Marine Biology and Ecology 312, 67–87.CrossRefGoogle Scholar
Flukes, E.B., Johnson, C.R., and Wright, J.T. (2014) Thinning of kelp canopy modifies understory assemblages: the importance of canopy density. Marine Ecology Progress Series 514, 57–70.CrossRefGoogle Scholar
Foster, M.S. and Schiel, D.R. (1985) The ecology of giant kelp forests in California: a community profile. U.S. Fish and Wildlife Service Biological Report 85, 1–152.Google Scholar
Fowler-Walker, M.J., Gillanders, B.M., Connell, S.D. and Irving, A.D. (2005) Patterns of association between canopy-morphology and understorey assemblages across temperate Australia. Journal of Experimental Marine Biology and Ecology 63, 133–141.Google Scholar
Ginn, B.K., Logan, A. and Thomas, M.L.H. (2000) Sponge ecology on sublittoral hard substrates in a high current velocity area. Estuarine, Coastal and Shelf Science 50, 403–414.CrossRefGoogle Scholar
Gouhier, T.C., Menge, B.A. and Hacker, S.D. (2011) Recruitment facilitation can promote coexistence and buffer population growth in metacommunities. Ecology Letters 14, 1201–1210.CrossRefGoogle ScholarPubMed
Hobbs, N.T. and Hilborn, R. (2006) Alternatives to statistical hypothesis testing in ecology: a guide to self teaching. Ecological Applications 16, 5–19.CrossRefGoogle ScholarPubMed
Jenkins, S.R., Norton, T.A. and Hawkins, S.J. (1999) Settlement and post-settlement interactions between Semibalanus balanoides (L.) (Crustacea: Cirripedia) and three species of fucoid canopy algae. Journal of Experimental Marine Biology and Ecology 236, 49–67.CrossRefGoogle Scholar
Jones, C.G., Lawton, J.H. and Shachak, M. (1997) Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78, 1946–1957.CrossRefGoogle Scholar
Kaandorp, J.A. and de Kluijver, M.J. (1992) Verification of fractal growth models of the sponge Haliclona oculata (Porifera) with transplantation experiments. Marine Biology 113, 133–143.CrossRefGoogle Scholar
Kennelly, S.J. (1987a) Physical disturbances in an Australian kelp community. I. Temporal effects. Marine Ecology Progress Series 40, 145–153.CrossRefGoogle Scholar
Kennelly, S.J. (1987b) Physical disturbances in an Australian kelp community. II. Effects on understorey species due to differences in kelp cover. Marine Ecology Progress Series 40, 155–165.CrossRefGoogle Scholar
Kennelly, S.J. (1989) Effects of kelp canopies on understorey species due to shade and scour. Marine Ecology Progress Series 50, 215–224.CrossRefGoogle Scholar
Kennelly, S.J. and Underwood, A.J. (1993) Geographic consistencies of effects of experimental physical disturbance on understorey species in sublittoral kelp forests in central New South Wales. Journal of Experimental Marine Biology and Ecology 168, 35–58.CrossRefGoogle Scholar
Knott, N.A., Underwood, A.J., Chapman, M.G. and Glasby, T.M. (2004) Epibiota on vertical and on horizontal surfaces on natural reefs and on artificial structures. Journal of the Marine Biological Association of the United Kingdom 84, 1117–1130.CrossRefGoogle Scholar
Kohler, K.E. and Gill, S.M. (2006) Coral Point Count with Excel extensions (CPCe): A Visual Basic program for the determination of coral and substrate coverage using random point count methodology. Computers and Geosciences 32, 1259–1269.CrossRefGoogle Scholar
Leonard, G.H. (1999) Positive and negative effects of intertidal algal canopies on recruitment and survival of barnacles. Marine Ecology Progress Series 178, 241–249.CrossRefGoogle Scholar
Mann, K.H. (1973) Seaweeds: their productivity and strategy for growth. Science 182, 975–981.CrossRefGoogle ScholarPubMed
McArdle, B. and Anderson, M. (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82, 290–297.CrossRefGoogle Scholar
Melville, A.J. and Connell, S.D. (2001) Experimental effects of kelp canopies on subtidal coralline algae. Austral Ecology 26, 102–108.CrossRefGoogle Scholar
Miller, R.J. and Etter, R.J. (2008) Shading facilitates sessile invertebrate dominance in the rocky subtidal Gulf of Maine. Ecology 89, 452–462.CrossRefGoogle ScholarPubMed
Morrow, K. and Carpenter, R. (2008) Shallow kelp canopies mediate macroalgal composition: effects on the distribution and abundance of Corynactis californica (Corallimorpharia). Marine Ecology Progress Series 361, 119–127.CrossRefGoogle Scholar
Naranjo, S.A., Carballo, J.L. and García-Gómez, J.C. (1996) Effects of environmental stress on ascidian populations in Algeciras bay (southern Spain). Possible marine bioindicators? Marine Ecology Progress Series 144, 119–131.CrossRefGoogle Scholar
NIWA National Climate Database (2013) New Zealand's national climate database. National Institute of Water and Atmospheric Research. http://cliflo.niwa.co.nz.Google Scholar
O'Connor, N.E., Crowe, T.P. and McGrath, D. (2006) Effects of epibiotic algae on the survival, biomass and recruitment of mussels, Mytilus L. (Bivalvia: Mollusca). Journal of Experimental Marine Biology and Ecology 328, 265–276.CrossRefGoogle Scholar
Perea-Blázquez, A., Davy, S.K. and Bell, J.J. (2012) Estimates of particulate organic carbon flowing from the pelagic environment to the benthos through sponge assemblages. PloS One 7, e29569.CrossRefGoogle Scholar
Preciado, I. and Maldonado, M. (2005) Reassessing the spatial relationship between sponges and macroalgae in sublittoral rocky bottoms: a descriptive approach. Helgoland Marine Research 59, 141–150.CrossRefGoogle Scholar
Reed, D.C. and Foster, M.S. (1984) The effects of canopy shadings on algal recruitment and growth in a giant kelp forest. Ecology 65, 937–948.CrossRefGoogle Scholar
Roberts, D.E., Davis, A.R. and Cummins, S.P. (2006) Experimental manipulation of shade, silt, nutrients and salinity on the temperate reef sponge Cymbastela concentrica. Marine Ecology Progress Series 307, 143–154.CrossRefGoogle Scholar
Russell, B.D. (2007) Effects of canopy-mediated abrasion and water flow on the early colonisation of turf-forming algae. Marine and Freshwater Research 58, 657–665.CrossRefGoogle Scholar
Schiel, D.R. (1988) Algal interactions on shallow subtidal reefs in northern New Zealand: a review. New Zealand Journal of Marine and Freshwater Research 22, 481–489.CrossRefGoogle Scholar
Schiel, D.R. and Hickford, M.J.H. (2001) Biological structure of nearshore rocky subtidal habitats in southern New Zealand. Science for Conservation 182, 1–54.Google Scholar
Sebens, K.P. (1985) Community ecology of vertical rock walls in the Gulf of Maine, U.S.A.: Small-scale processes and alternative states. In Moore, P.G. and Seed, R. (eds) The ecology of rocky coasts. New York, NY: Columbia University Press, pp. 346–371.Google Scholar
Shears, N.T. and Babcock, R.C. (2007) Quantitative description of mainland New Zealand's shallow subtidal reef communities. Science for Conservation 280, 1–126.Google Scholar
Smale, D.A., Burrows, M.T., Moore, P., O'Connor, N. and Hawkins, S.J. (2013) Threats and knowledge gaps for ecosystem services provided by kelp forests: a northeast Atlantic perspective. Ecology and Evolution 3, 4016–4038.CrossRefGoogle ScholarPubMed
Smale, D.A., Kendrick, G.A. and Wernberg, T. (2011) Subtidal macroalgal richness, diversity and turnover, at multiple spatial scales, along the southwestern Australian coastline. Estuarine, Coastal and Shelf Science 91, 224–231.CrossRefGoogle Scholar
Smith, S.D.A. (1996) The macrofaunal community of Ecklonia radiata holdfasts: variation associated with sediment regime, sponge cover and depth. Australian Journal of Ecology 21, 144–153.CrossRefGoogle Scholar
Sousa, W. (2000) Natural disturbance and the dynamics of marine benthic communities. In Bertness, M.D., Gaines, S.D. and Hay, M.E. (eds) Marine community ecology. Sunderland, MA: Sinauer Associates, pp. 85–130.Google Scholar
Stachowicz, J.J. (2001) Facilitation, and the structure of ecological communities. BioScience 51, 235–246.CrossRefGoogle Scholar
Symonds, M.R.E. and Moussalli, A. (2011) A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike's information criterion. Behavioral Ecology and Sociobiology 65, 13–21.CrossRefGoogle Scholar
Syvitski, J.P.M., Vörösmarty, C.J., Kettner, A.J. and Green, P. (2005) Impact of humans on the flux of terrestrial sediment to the global coastal ocean. Science 308, 376–380.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Toohey, B.D. and Kendrick, G.A. (2008) Canopy-understorey relationships are mediated by reef topography in Ecklonia radiata kelp beds. European Journal of Phycology 43, 133–142.CrossRefGoogle Scholar
Turon, X., Tarjuelo, I. and Uriz, M.J. (1998) Growth dynamics and mortality of the encrusting sponge Crambe crambe (Poecilosclerida) in contrasting habitats: correlation with population structure and investment in defence. Functional Ecology 12, 631–639.CrossRefGoogle Scholar
Velimirov, B. and Griffiths, C.L. (1979) Wave-induced kelp movement and its importance for community structure. Botanica Marina 22, 169–172.CrossRefGoogle Scholar
Wernberg, T., Kendrick, G.A. and Toohey, B.D. (2005) Modification of the physical environment by an Ecklonia radiata (Laminariales) canopy and implications for associated foliose algae. Aquatic Ecology 39, 419–430.CrossRefGoogle Scholar
Wilkinson, C.R. and Vacelet, J. (1979) Transplantation of marine sponges to different conditions of light and current. Journal of Experimental Marine Biology and Ecology 37, 91–104.CrossRefGoogle Scholar
Wright, J.T., Benkendorff, K. and Davis, A.R. (1997) Habitat associated differences in temperate sponge assemblages: the importance of chemical defence. Journal of Experimental Marine Biology and Ecology 213, 199–213.CrossRefGoogle Scholar
Wulff, J. (2012) Ecological interactions and the distribution, abundance, and diversity of sponges. Advances in Marine Biology 61, 273–344.CrossRefGoogle ScholarPubMed
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