Skip to main content

Testing limiting similarity in Quaternary terrestrial gastropods

  • John Warren Huntley (a1), Yurena Yanes (a2), Michał Kowalewski (a1), Carolina Castillo (a3), Antonio Delgado-Huertas (a4), Miguel Ibáñez (a3), María R. Alonso (a3), José E. Ortiz (a5) and Trinidad de Torres (a5)...

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.

Hide All
Abrams, P. 1983. The theory of limiting similarity. Annual Review of Ecology and Systematics 14:359376.
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.
Barton, D. E., and David, F. N. 1956. Some notes on ordered random intervals. Journal of the Royal Statistical Society B 18:7994.
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.
Bowers, M. A., and Brown, J. H. 1982. Body size and coexistence in desert rodents: chance or community structure? Ecology 63:391400.
Brown, W. L. Jr., and Wilson, E. O. 1956. Character displacement. Systematic Zoology 5:4964.
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.
Chiba, S. 1998. Synchronized evolution in lineages of land snails in oceanic islands. Paleobiology 24:99108.
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.
Cody, M. L. 2000. Antbird guilds in the lowland Caribbean rainforest of southeast Nicaragua. Condor 102:784794.
Cronin, T. M. 1999. Principles of paleoclimatology. Columbia University Press, New York.
Dayan, T., and Simberloff, D. 2005. Ecological and communitywide character displacement: the next generation. Ecology Letters 8:875894.
Dyar, H. G. 1890. The number of molts of lepidopterous larvae. Psyche 5:420422.
Efron, B. 1981. Nonparametric standard errors and confidence intervals. Canadian Journal of Statistics 9:139172.
Eldredge, N. 1974. Character displacement in evolutionary time. American Zoologist 14:10831097.
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.
Gittenberger, E., and Ripken, T. E. J. 1987. The genus Theba (Mollusca: Gastropoda: Helicidae), systematics and distribution. Zoologische Verhandelingen 241:162.
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.
Goodfriend, G. A. 1986. Variation in land snail shell form and size and its causes: a review. Systematic Zoology 35:204223.
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.
Goodfriend, G. A. 1987b. Radiocarbon age anomalies in shell carbonate of land snails from semi-arid areas. Radiocarbon 29:159167.
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.
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).
Hausdorf, B. 2007. Is the interspecific variation of body size of land snails correlated with rainfall in Israel and Palestine? Acta Oecologica 30:374379.
Hermoyian, C. S., Leighton, L. R., and Kaplan, P. 2002. Testing the role of competition in fossil communities using limiting similarity. Geology 30:1518.
Horn, H. S., and May, R. M. 1977. Limits to similarity among coexisting competitors. Nature 270:660661.
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.
Huntley, J. W., Xiao, S., and Kowalewski, M. 2006a. 1.3 billion years of acritarch history: an empirical morphospace approach. Precambrian Research 144:5268.
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.
Hutchinson, G. E. 1959. Homage to Santa Rosalia or why are there so many kinds of animals? American Naturalist 93:145159.
Jablonski, D. 1997. Body-size evolution in Cretaceous molluscs and the status of Cope's rule. Nature 385:250252.
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.
Kerney, M. P., and Cameron, R. A. D. 1979. A field guide to the land snails of Britain and north-west Europe. Collins.
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.
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.
Macarthur, R., and Levins, R. 1967. The limiting similarity, convergence, and divergence of coexisting species. American Naturalist 101:377385.
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.
Medina, F. M. 1999. Alimentación del alimoche, Neophron percnopterus (L.), en Fuerteventura, Islas Canarias (Aves, Accipitridae). Vieraea 27:7786.
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.
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.
Paine, R. T. 1966. Food web complexity and species diversity. American Naturalist 100:6575.
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.
Schindel, D. E., and Gould, S. J. 1977. Biological interaction between fossil species: character displacement in Bermudian land snails. Paleobiology 3:259269.
Schoener, T. W. 1965. The evolution of bill size differences among sympatric congeneric species of birds. Evolution 19:189213.
Simberloff, D., and Boecklen, W. 1981. Santa Rosalia reconsidered: size ratios and competition. Evolution 35:12061228.
Stanley, S. M. 2008. Predation defeats competition on the sea floor. Paleobiology 34:121.
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.
Stubbs, W. J., and Bastow Wilson, J. 2004. Evidence for limiting similarity in a sand dune community. Journal of Ecology 92:557567.
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.
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.
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).
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).
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

  • ISSN: 0094-8373
  • EISSN: 1938-5331
  • URL: /core/journals/paleobiology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *


Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed