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Testing limiting similarity in Quaternary terrestrial gastropods

Published online by Cambridge University Press:  08 April 2016

John Warren Huntley
Affiliation:
Department of Geosciences, Virginia Polytechnic Institute and State University, Blacksburg, Virginia 24061. E-mail: jhuntley@vt.edu
Yurena Yanes
Affiliation:
Savannah River Ecology Laboratory, University of Georgia, Drawer E, Aiken, South Carolina 29802
Michał Kowalewski
Affiliation:
Department of Geosciences, Virginia Polytechnic Institute and State University, Blacksburg, Virginia 24061. E-mail: jhuntley@vt.edu
Carolina Castillo
Affiliation:
Departamento de Biología Animal, Universidad de La Laguna, Avenida Astrofísico Francisco Sánchez s/n 38206, La Laguna, Tenerife, Canary Islands, Spain
Antonio Delgado-Huertas
Affiliation:
Laboratorio de Biogeoquímica de Isótopos Estables, Estación Experimental del Zaidín (CSIC), Prof. Albareda 1, 18008, Granada, Spain
Miguel Ibáñez
Affiliation:
Departamento de Biología Animal, Universidad de La Laguna, Avenida Astrofísico Francisco Sánchez s/n 38206, La Laguna, Tenerife, Canary Islands, Spain
María R. Alonso
Affiliation:
Departamento de Biología Animal, Universidad de La Laguna, Avenida Astrofísico Francisco Sánchez s/n 38206, La Laguna, Tenerife, Canary Islands, Spain
José E. Ortiz
Affiliation:
Laboratorio de Estratigrafía Biomolecular, Escuela Técnica Superior de Ingenieros de Minas de Madrid, C/Ríos Rosas 21, 28003, Madrid, Spain
Trinidad de Torres
Affiliation:
Laboratorio de Estratigrafía Biomolecular, Escuela Técnica Superior de Ingenieros de Minas de Madrid, C/Ríos Rosas 21, 28003, Madrid, Spain

Abstract

The hypothesis of limiting similarity, which postulates that morphologically and/or ecologically similar species will differ enough in shape, size, or other variables to minimize competition, has been controversial among ecologists and paleoecologists. Many studies have reported the occurrence of limiting similarity in modern environments or in time-averaged fossil deposits; however, empirical high-resolution time series demonstrating limiting similarity over longer time scales are lacking. We have integrated radiocarbon-calibrated amino acid dating techniques, stable isotope estimates, and morphometric data to test the hypothesis of limiting similarity in late Quaternary land snails from the Canary Islands over a period of 42,500 years. We tested for both ecological character displacement (two closely related species will differ in size in order to minimize competition in sympatry and these differences will be minimized in allopatry) and communitywide character displacement (overdispersion of body size among competitors in a guild). Multiple proxies of body size consistently show that two endemic congeneric pulmonate gastropod species (Theba geminata and T. arinagae) maintained a difference in size from ~42,500 B.P. through the last occurrence of T. arinagae 14,900 B.P., with a concomitant trend of a decreasing body size. Theba geminata body size did not converge on that of T. arinagae and variation in T. geminata body size did not increase significantly following the extinction of T. arinagae; therefore, ecological character displacement and release did not occur. Community-wide character displacement was found in only one time bin over the last 42,500 years. These results suggest that limiting similarity is a transient ecological phenomenon rather than a long-term evolutionary process. This study not only demonstrates the problems inherent in biological “snapshot” studies and geological studies of time-averaged deposits to test limiting similarity adequately, but it also presents a more adequate research protocol to test the importance of interspecific competition in the history of life.

Type
Articles
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Abrams, P. 1983. The theory of limiting similarity. Annual Review of Ecology and Systematics 14:359376.Google Scholar
Balakrishnan, M., and Yapp, C. J. 2004. Flux balance model for the oxygen and carbon isotope compositions of land snail shells. Geochimica et Cosmochimica Acta 68:20072024.CrossRefGoogle Scholar
Barton, D. E., and David, F. N. 1956. Some notes on ordered random intervals. Journal of the Royal Statistical Society B 18:7994.Google Scholar
Beyerle, U., Rueedi, J., Leuenberger, M., Aeschbach-Hertig, W., Peeters, F., and Kipfer, R. 2003. Evidence for periods of wetter and cooler climate in the Sahel between 6 and 40 Kyr BP derived from groundwater. Geophysical Research Letters 30:11731177.Google Scholar
Bowers, M. A., and Brown, J. H. 1982. Body size and coexistence in desert rodents: chance or community structure? Ecology 63:391400.CrossRefGoogle Scholar
Brown, W. L. Jr., and Wilson, E. O. 1956. Character displacement. Systematic Zoology 5:4964.Google Scholar
Castillo, C., Martín-González, E., Yanes, Y., Ibáñez, M., De la Nuez, J., Alonso, M. R., and Quesada, M. L. 2002. Estudio preliminar de los depósitos dunares de los Islotes del Norte de Lanzarote: implicaciones paleoambientales. Geogaceta 32:7982.Google Scholar
Chiba, S. 1998. Synchronized evolution in lineages of land snails in oceanic islands. Paleobiology 24:99108.CrossRefGoogle Scholar
Chiba, S. 2004. Ecological and morphological patterns in communities of land snails of the genus Mandarina from the Bonin Islands. Journal of Evolutionary Biology 17:131143.Google Scholar
Cody, M. L. 2000. Antbird guilds in the lowland Caribbean rainforest of southeast Nicaragua. Condor 102:784794.Google Scholar
Cronin, T. M. 1999. Principles of paleoclimatology. Columbia University Press, New York.Google Scholar
Dayan, T., and Simberloff, D. 2005. Ecological and communitywide character displacement: the next generation. Ecology Letters 8:875894.Google Scholar
Dyar, H. G. 1890. The number of molts of lepidopterous larvae. Psyche 5:420422.Google Scholar
Efron, B. 1981. Nonparametric standard errors and confidence intervals. Canadian Journal of Statistics 9:139172.CrossRefGoogle Scholar
Eldredge, N. 1974. Character displacement in evolutionary time. American Zoologist 14:10831097.CrossRefGoogle Scholar
Farquhar, G. D., Ehleringer, J. R., and Hubick, K. T. 1989. Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 40:503537.CrossRefGoogle Scholar
Gittenberger, E., and Ripken, T. E. J. 1987. The genus Theba (Mollusca: Gastropoda: Helicidae), systematics and distribution. Zoologische Verhandelingen 241:162.Google Scholar
Gittenberger, E., Ripken, T. E. J., and Bueno, M. L. 1992. The forgotten Theba species (Gastropoda, Pulmonata, Helicidae). Proceedings of the 10th Malacological Congress, pp. 145151.Google Scholar
Goodfriend, G. A. 1986. Variation in land snail shell form and size and its causes: a review. Systematic Zoology 35:204223.Google Scholar
Goodfriend, G. A. 1987a. Chronostratigraphic studies of sediments in the Negev Desert, using amino acid epimerization analysis of land snails shells. Quaternary Research 28:374392.Google Scholar
Goodfriend, G. A. 1987b. Radiocarbon age anomalies in shell carbonate of land snails from semi-arid areas. Radiocarbon 29:159167.Google Scholar
Goodfriend, G. A., and Gould, S. J. 1996. Paleontology and chronology of two evolutionary transitions by hybridization in the Bahamian land snail Cerion . Science 274:18941897.Google Scholar
Hammer, O., Harper, D. A. T., and Ryan, P. D. 2001. PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4(1).Google Scholar
Hausdorf, B. 2007. Is the interspecific variation of body size of land snails correlated with rainfall in Israel and Palestine? Acta Oecologica 30:374379.Google Scholar
Hermoyian, C. S., Leighton, L. R., and Kaplan, P. 2002. Testing the role of competition in fossil communities using limiting similarity. Geology 30:1518.Google Scholar
Horn, H. S., and May, R. M. 1977. Limits to similarity among coexisting competitors. Nature 270:660661.Google Scholar
Huntley, J. W., and Kowalewski, M. 2007. Strong coupling of predation intensity and diversity in the Phanerozoic fossil record. Proceedings of the National Academy of Sciences USA 104:1500615010.CrossRefGoogle ScholarPubMed
Huntley, J. W., Xiao, S., and Kowalewski, M. 2006a. 1.3 billion years of acritarch history: an empirical morphospace approach. Precambrian Research 144:5268.Google Scholar
Huntley, J. W. 2006b. On the morphological history of Proterozoic and Cambrian acritarchs. Pp. 2456 in Xiao, S. and Kaufman, A. J., eds. Neoproterozoic geobiology and paleobiology. Springer, Dordrecht.Google Scholar
Hutchinson, G. E. 1959. Homage to Santa Rosalia or why are there so many kinds of animals? American Naturalist 93:145159.Google Scholar
Jablonski, D. 1997. Body-size evolution in Cretaceous molluscs and the status of Cope's rule. Nature 385:250252.Google Scholar
Kaufman, D. S., and Manley, W. F. 1998. A new procedure for determining DL amino acid ratios in fossils using reverse phase liquid chromatography. Quaternary Geochronology 17:9871000.Google Scholar
Kerney, M. P., and Cameron, R. A. D. 1979. A field guide to the land snails of Britain and north-west Europe. Collins.Google Scholar
Kowalewski, M., Goodfriend, G. A., and Flessa, K. W. 1998. High-resolution estimates of temporal mixing within shell beds: the evils and virtues of time-averaging. Paleobiology 24:287304.Google Scholar
Kutzbach, J., Bonan, G., Foley, J., and Harrison, S. P. 1996. Vegetation and soil feedbacks on the response of the African monsoon to orbital forcing in the early to middle Holocene. Nature 384:623626.Google Scholar
Macarthur, R., and Levins, R. 1967. The limiting similarity, convergence, and divergence of coexisting species. American Naturalist 101:377385.Google Scholar
McKinney, F. K. 1995. One hundred million years of competitive interactions between bryozoan clades: asymmetrical but not escalating. Biological Journal of the Linnean Society 56:465481.Google Scholar
Medina, F. M. 1999. Alimentación del alimoche, Neophron percnopterus (L.), en Fuerteventura, Islas Canarias (Aves, Accipitridae). Vieraea 27:7786.Google Scholar
Metref, S., Rousseau, D. D., Bentaleb, I., Labonne, M., and Vinaey-Liaud, M. 2003. Study of the diet effect on d13C of shell carbonate of the land snail Helix aspersa in experimental conditions. Earth and Planetary Science Letters 211:381393.Google Scholar
Ortiz, J. E., Torres, T., Yanes, Y., Castillo, C., de la Nuez, J., Ibanez, M., and Alonso, M. R. 2006. Climatic cycles inferred from the aminostratigraphy and aminochronology of Quaternary dunes and paleosols from the eastern islands of the Canary Archipelago. Journal of Quaternary Science 21(3):287306.Google Scholar
Paine, R. T. 1966. Food web complexity and species diversity. American Naturalist 100:6575.Google Scholar
Petit, J. R., Jouzel, J., Raynaud, D., Barkov, N. I., Barnola, J.-M., Basile, I., Benders, M., Chappellaz, J., Davis, M., Delaygue, G., Delmotte, M., Kotlyakov, V. M., Legrand, M., Lipenkov, V. Y., Lorius, C., Pepin, L., Ritz, C., Saltzman, E., and Stievenard, M. 1999. Climate and atmospheric history of the past 420,000 years from the Vostok ice core, Antarctica. Nature 399:429436.CrossRefGoogle Scholar
Schindel, D. E., and Gould, S. J. 1977. Biological interaction between fossil species: character displacement in Bermudian land snails. Paleobiology 3:259269.Google Scholar
Schoener, T. W. 1965. The evolution of bill size differences among sympatric congeneric species of birds. Evolution 19:189213.Google Scholar
Simberloff, D., and Boecklen, W. 1981. Santa Rosalia reconsidered: size ratios and competition. Evolution 35:12061228.CrossRefGoogle ScholarPubMed
Stanley, S. M. 2008. Predation defeats competition on the sea floor. Paleobiology 34:121.Google Scholar
Stott, L. D. 2002. The influence of diet on the d13C of shell carbon in the pulmonate snail Helix aspersa . Earth and Planetary Science Letters 195:249259.Google Scholar
Stubbs, W. J., and Bastow Wilson, J. 2004. Evidence for limiting similarity in a sand dune community. Journal of Ecology 92:557567.CrossRefGoogle Scholar
Yanes, Y., Castillo, C., Alonso, M. R., Ibáñez, M., de la Nuez, J., Quesada, M. L., Martín-González, E., La Roche, F., Liché, D., and Armas, R. F. 2004. Gasterópodos terrestres cuaternarios del Archipiélago Chinijo, Islas Canarias. Vieraea 32:123134.Google Scholar
Yanes, Y., Kowalewski, M., Ortiz, J. E., Castillo, C., de Torres, T., and de la Nuez, J. 2007. Scale and structure of time-averaging (age mixing) in terrestrial gastropod assemblages from Quaternary eolian deposits of the eastern Canary Islands. Palaeogeography, Palaeoclimatology, Palaeoecology 251:283299.CrossRefGoogle Scholar
Yanes, Y., Delgado-Huertas, A., Castillo, C., Alonso, M. R., Ibáñez, M., De la Nuez, J., and Kowalewski, M. 2008a. Stable Isotope (d18O, d13C, and dD) signatures of Recent terrestrial communities from a low-latitude, oceanic setting: endemic land snails, plants, rain, and carbonate sediments from the eastern Canary Islands. Chemical Geology (in press).Google Scholar
Yanes, Y., Tomašových, A., Kowalewski, M., Castillo, C., Aguirre, J., Alonso, M. R., and Ibáñez, M. 2008b. Taphonomy and compositional fidelity of Quaternary fossil assemblages of terrestrial gastropods from carbonate-rich environments of the Canary Islands. Lethaia (in press).CrossRefGoogle Scholar