Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-10T15:05:44.488Z Has data issue: false hasContentIssue false
  • English
  • Français

Coexistence in a subtidal habitat in southern Chile: the effects of giant kelp Macrocystis pyrifera overgrowth on the slipper limpet Crepipatella fecunda

Published online by Cambridge University Press:  26 August 2014

Francisco J. Díaz ,
Sandra V. Pereda  and
Alejandro H. Buschmann
Francisco J. Díaz
Affiliation:
Centro i-mar, Universidad de Los Lagos, Camino Chinquihue km 6, Puerto Montt, Chile
Sandra V. Pereda*
Affiliation:
Centro i-mar, Universidad de Los Lagos, Camino Chinquihue km 6, Puerto Montt, Chile
Alejandro H. Buschmann
Affiliation:
Centro i-mar, Universidad de Los Lagos, Camino Chinquihue km 6, Puerto Montt, Chile
*
Correspondence should be addressed to: S.V. Pereda, Centro i-mar, Universidad de Los Lagos, Camino Chinquihue km 6, Casilla, 557 Puerto Montt, Chile email: spereda@ulagos.cl
Get access Rights & Permissions [Opens in a new window]

Abstract

In many coastal areas substrate is the limiting resource for benthic organisms. Some sessile species can be used as secondary substrate, reducing competition and increasing coexistence. In southern Chile, annual populations of Macrocystis pyrifera recruit and grow on the shells of Crepipatella fecunda. This study describes ecological interactions between the kelp and the slipper limpet over an annual cycle. The degree of kelp overgrowth was established by collecting sporophytes and through in situ submarine photography over a 10 month period (starting when kelp recruits became visible and ending when sporophytes were no longer present). Changes in the biochemical composition of the limpet tissue were also recorded by chemical analyses, to evaluate the potential effects (positive/neutral/negative) of kelp on C. fecunda nutritional condition. The results indicate that both species coexist, although kelp overgrowth may cause a decrease in carbohydrates in C. fecunda tissues, restricted to the period when the kelp forest reaches its maximum biomass. Individually, the short duration of the maximum overgrowth period and the size reached by C. fecunda females (up to 65 mm shell length) may enable rapid limpet recovery, avoiding competitive exclusion. On a population level, the M. pyrifera annual cycle generates the needed ‘break’ for C. fecunda populations, reducing the effects of kelp overgrowth. Thus, in the view of the neutral effect of kelp overgrowth, together with the positive effect of C. fecunda on M. pyrifera recruitment described somewhere else, this ecological interaction can be categorized as commensalism.

Keywords

coexistencekelpMacrocystis pyriferaCrepipatella fecundabiochemical compositionkelp overgrowthcommensalism
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 95 , Issue 1 , February 2015 , pp. 25 - 33
Copyright
Copyright © Marine Biological Association of the United Kingdom 2014 

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

REFERENCES

Amarasekare, P. (2003) Competitive coexistence in spatially structured environments: a synthesis. Ecology 6, 1109–1122.Google Scholar
Armstrong, R.A. and McGehee, R. (1980) Competitive exclusion. American Naturalist 115, 151–170.Google Scholar
Ayala, F.J. (1970) Competition, coexistence, and evolution. In Hecht, M.K. and Steere, W.C. (eds) Essays in evolution and genetics in honor of Theodosius Dobzhansky. New York: Appleton-Century-Crofts, pp. 121–158.Google Scholar
Barnes, H. and Heath, J.R. (1966) The extraction of glycogen from marine invertebrate tissues. Helgoländer Wissenschaftliche Meeresuntersuchungen 13, 115–117.Google Scholar
Bolker, B.M. and Pacala, S.W. (1999) Spatial moment equations for plant competition: understanding spatial strategies and the advantages of short dispersal. American Naturalist 153, 575–602.Google Scholar
Botts, P.S., Patterson, B.A. and Schloesser, D.W. (1996) Zebra mussel effects on benthic invertebrates: physical or biotic? Journal of the North American Benthological Society 15, 179–184.CrossRefGoogle Scholar
Bruno, J.F. and Bertness, M.D. (2001) Habitat modification and facilitation in benthic marine communities. In Bertness, M.D., Hay, M.E. and Gaines, S.D. (eds) Marine community ecology. Sunderland, MA: Sinauer Associates, pp. 201–218.Google Scholar
Buschmann, A.H. (1992) Algal communities of a wave-protected intertidal rocky shore in southern Chile. In Seeliger, U. (ed.) Coastal plant communities of Latin America. Miami, FL: Academic Press, pp. 91–104.Google Scholar
Buschmann, A.H., Moreno, C., Vásquez, J.A. and Hernández-González, M.C. (2006) Reproduction strategies of Macrocystis pyrifera (Phaeophyta) in southern Chile: the importance of population dynamics. Journal of Applied Phycology 18, 575–582.Google Scholar
Buschmann, A.H., Vásquez, J.A., Osorio, P., Reyes, E., Filún, L., Hernández-González, M.C. and Vega, A. (2004) The effect of water movement, temperature and salinity on abundance and reproductive patterns of Macrocystis spp. (Phaeophyta) at different latitudes in Chile. Marine Biology 145, 849–862.Google Scholar
Buss, L.W. (1980) Competitive intransitivity and size–frequency distributions of interacting populations. Proceedings of the National Academy of Sciences of the United States of America 77, 5355–5359.Google Scholar
Callaway, R.M. and Walker, L.R. (1997) Competition and facilitation: a synthetic approach to interactions in plant communities. Ecology 78, 1958–1965.Google Scholar
Chaparro, O.R., Pereda, S.V. and Bahamondes-Rojas, I. (2001) Effects of protandric sex change on radula, pedal morphology, and mobility in Crepidula fecunda (Gastropoda: Calyptraeidae). New Zealand Journal of Marine and Freshwater Research 35, 881–890.Google Scholar
Chaparro, O.R., Saldivia, C.L., Pereda, S.V., Segura, C.J., Montiel, Y.A. and Collin, R. (2005) The reproductive cycle and development of Crepipatella fecunda (Gastropoda: Calyptraeidae) from southern Chile. Journal of the Marine Biological Association of the United Kingdom 85, 157–161.Google Scholar
Chaparro, O.R., Thompson, R.J. and Pereda, S.V. (2002) Feeding mechanisms in the gastropod Crepidula fecunda . Marine Ecology Progress Series 234, 171–181.Google Scholar
Chesson, P. (2000a) Mechanisms of maintenance of species diversity. Annual Review of Ecology and Systematics 31, 343–366.Google Scholar
Chesson, P. (2000b) General theory of competitive coexistence in spatially-varying environments. Theoretical Population Biology 58, 211–237.Google Scholar
Collin, R. (2003) Phylogenetic relationships among calyptraeid gastropods and their implications for the biogeography of marine speciation. Systematic Biology 52, 618–640.Google Scholar
Connell, J.H. (1961) The influence of interspecific competition and other factors on the distribution of the barnacle Chthamalus stellatus . Ecology 42, 710–723.Google Scholar
Connell, J.H. (1972) Community interactions on marine rocky intertidal shores. Annual Review of Ecology and Systematics 3, 169–192.Google Scholar
Creed, J.C. (2000) Epibiosis on cerith shells in a seagrass bed: correlation of shell occupant with epizoite distribution and abundance. Marine Biology 137, 775–782.Google Scholar
Dahlhoff, E.P. (2004) Biochemical indicators of stress and metabolism: applications for marine ecological studies. Annual Review of Physiology 66, 183–207.Google Scholar
Dayton, P.K. (1971) Competition, disturbance, and community organization: the provision and subsequent utilization of space in a rocky intertidal environment. Ecological Monographs 41, 351–389.Google Scholar
Denny, M.W. (1988) Biology and the mechanics of the wave-swept environment. Princeton, NJ: Princeton University Press.Google Scholar
Douros, W.J. (1987) Stacking behavior of an intertidal abalone: an adaptive response or a consequence of space limitation? Journal of Experimental Biology 108, 1–14.Google Scholar
Dubois, M., Gilles, K.A., Hamilton, J.K., Rebers, P.A. and Smith, F. (1956) Colorimetric method for determination of sugars and related substances. Analytical Chemistry 28, 350–356.Google Scholar
Dudgeon, S.R., Steneck, R.S., Davison, I.R. and Vadas, R.L. (1999) Coexistence of similar species in a space-limited intertidal zone. Ecological Monographs 69, 331–352.Google Scholar
Gallardo, C.S. (1977) Two modes of development in the morphospecies Crepidula dilatata (Gastropoda: Calyptraeidae) from southern Chile. Marine Biology 39, 241–251.Google Scholar
Gallardo, C.S. (1979) Especies gemelas del género Crepidula (Gastropoda, Calyptraeidae) en la costa de Chile; una redescripción de C. dilatata Lamarck y descripción de C. fecunda n. sp. Studies in Neotropical Fauna and Environment 14, 215–226.Google Scholar
Gnaiger, E. (1983) Calculation of energetic and biochemical equivalents of respiratory oxygen consumption. In Gnaiger, E. and Forstner, H. (eds) Polarographic oxygen sensor. Berlin: Springer-Verlag, pp. 337–345.Google Scholar
Goldberg, D.E. (1990) Components of resource competition in plant communities. In Grace, J. and Tilman, D. (eds) Perspectives on plant competition. San Diego, CA: Academic Press, pp. 27–49.Google Scholar
Graham, M.H., Vásquez, J.A. and Buschmann, A.H. (2007) Global ecology of the giant kelp Macrocystis: from ecotypes to ecosystems. Oceanography and Marine Biology: an Annual Review 45, 39–88.Google Scholar
Gutiérrez, J.L., Jones, C.G., Strayer, D.L. and Iribarne, O.O. (2003) Mollusks as ecosystem engineers: the role of shell production in aquatic habitats. Oikos 101, 79–90.Google Scholar
Henríquez, L.A., Buschmann, A.H., Maldonado, M.A., Graham, M.H., Hernández-González, M.C., Pereda, S.V. and Bobadilla, M.I. (2011) Grazing on giant kelp microscopic phases and the recruitment success of annual populations of Macrocystis pyrifera (Laminariales, Phaeophyta) in southern Chile. Journal of Phycology 47, 252–258.Google Scholar
Jackson, J.B.C. (1977) Competition on marine hard substrata: the adaptive significance of solitary and colonial strategies. American Naturalist 111, 743–767.Google Scholar
Kawai, T. and Tokeshi, M. (2006) Asymmetric coexistence: bidirectional abiotic and biotic effects between goose barnacles and mussels. Journal of Animal Ecology 75, 928–941.Google Scholar
Kay, A.M. (1980) The organization of sessile guilds on pier pilings . PhD thesis. University of Adelaide, South Australia.Google Scholar
Korringa, P. (1951) The shell of Ostrea edulis as a habitat. Netherlands Journal of Zoology 10, 32–152.Google Scholar
Lowry, O.H., Rosebrough, N.J., Farr, A.L. and Randall, R.J. (1951) Protein measurement with the phenol reagent. Journal of Biological Chemistry 193, 265–275.Google Scholar
Marsh, J.B. and Weinstein, D.B. (1966) Simple charring method for determination of lipids. Journal of Lipids Research 7, 574–576.Google Scholar
McShane, P.W. and Naylor, J.R. (1995) Density independent growth of Haliotis iris Martyn (Mollusca: Gastropoda). Journal of Experimental Biology 190, 51–60.Google Scholar
Noda, T. (2009) Metacommunity-level coexistence mechanism in rocky intertidal sessile assemblages based on a new empirical synthesis. Population Ecology 51, 41–55.Google Scholar
Odling-Smee, F.J., Laland, K.N. and Feldman, M.W. (2003) Niche construction: the neglected process in evolution. Princeton, NJ: Princeton University Press.Google Scholar
Ojea, J., Pazos, A.J., Martinez, D., Novoa, S., Sanchez, J.L. and Abad, M. (2004) Seasonal variation in weight and biochemical composition of the tissues of Ruditapes decussatus in relation to the gametogenic cycle. Aquaculture 238, 451–468.Google Scholar
Olabarria, C. (2000) Epibiont molluscs on neogastropod shells from sandy bottoms, Pacific coast of Mexico. Journal of the Marine Biological Association of the United Kingdom 80, 291–298.Google Scholar
Pacala, S.W. and Rees, M. (1998) Models suggesting field experiments to test two hypotheses explaining successional diversity. American Naturalist 152, 729–737.Google Scholar
Paine, R.T. (1976) Size-limited predation: an observational and experimental approach with the Mytilus–Pisaster interaction. Ecology 57, 858–873.Google Scholar
Peteiro, L.G., Labarta, U. and Fernández-Reiriz, M.J. (2007) Variability in biochemical components of the mussel (Mytilus galloprovincialis) cultured after prestige oil spill. Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology 145, 588–594.Google Scholar
Raghupathi, R.V. and Diwan, A.M. (1994) A protocol for protein estimation that gives a nearly constant color yield with simple proteins and nullifies the effects of four known interfering agents: microestimation of peptide groups. Analytical Biochemistry 219, 356–359.Google Scholar
Rossi, S., Snyder, M.J. and Gili, J-M. (2006) Protein, carbohydrate, lipid concentrations and HSP 70–HSP 90 (stress protein) expression over an annual cycle: useful tools to detect feeding constraints in a benthic suspension feeder. Helgoland Marine Research 60, 7–17.Google Scholar
Russ, G.R. (1982) Overgrowth in marine epifaunal community: competitive hierarchies and competitive networks. Oecologia 53, 12–19.Google Scholar
Rutzler, K. (1970) Spatial competition among Porifera: solution by epizooismo. Oecologia 5, 85–95.Google Scholar
Sebens, K.P. (1982) Competition for space: growth rate, reproductive output, and escape in size. American Naturalist 120, 189–197.Google Scholar
Witman, J.D. (1985) Refuges, biological disturbances, and rocky subtidal community structure in New England. Ecological Monographs 55, 421–445.Google Scholar
Witman, J.D. (1987) Subtidal coexistence: storm, grazing, mutualism, and the zonation of kelp and mussels. Ecological Monographs 57, 167–187.Google Scholar
Witman, J.D. and Suchanek, T.H. (1984) Mussels in flow: drag and dislodgement by epizoans. Marine Ecology Progress Series 16, 259–268.Google Scholar
Zarnoch, C.B. and Schreibman, M.P. (2008) Influence of temperature and food availability on the biochemical composition and mortality of juvenile Mercenaria mercenaria (L.) during the over-winter period. Aquaculture 274, 281–291.Google Scholar