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INTRASPECIFIC VARIATION IN THE GROWTH RATE OF GASTROPODS: FIVE HYPOTHESES

Published online by Cambridge University Press:  31 May 2012

Diane M. Shibata  and
C. David Rollo
Diane M. Shibata
Affiliation:
Department of Biology, McMaster University, 1280 Main St. W., Hamilton, Ontario, Canada L8S 4K1
C. David Rollo
Affiliation:
Department of Biology, McMaster University, 1280 Main St. W., Hamilton, Ontario, Canada L8S 4K1
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Abstract

Gastropods commonly show enormous variation in growth rate, even among identically reared siblings. This was investigated using a small isolated population of Deroceras laeve (Müller) — a species with low genetic variability. A high degree of variation in growth rate was evident, even among offspring from unmated mothers. This confirmed our hypothesis that this variation does not require high genetic polymorphism. Four additional hypotheses concerning the causal mechanism(s) for this variation were investigated: (1) Maternal influence through variation of egg quality was rejected as a possible cause for the variation since animals from mothers raised on either high- or low-quality diets did not differ significantly in growth or maturation rates (when egg size was controlled). (2) The possibility that animals might have their growth trajectory fixed by early nutritional experience was tested by initially rearing slugs on either high- or low-quality diets, and then reversing their food. Such "nutritional imprinting" was not supported. (3) Intraspecific interaction among individuals was not supported as a cause of variation either since stunted slugs did not show improved growth when isolated from conspecifics, and there was equal variation among individuals reared from the egg in isolation. (4) Variation in the egg size was the only characteristic investigated that significantly changed rates of juvenile growth and the timing of maturation. Larger eggs produced slower-growing slugs that matured later, and egg size seemed to account for the full range of observed variation. The ultimate function of the mechanism remains to be determined, but possibilities include adjusting the performance of offspring to resource supply, ensuring availability of mature individuals to breed during favourable microclimates, reducing competition among members of a cohort, or ensuring sexual heterogeneity for hermaphroditic breeding.

Résumé

Les résultats d'études effectuées sur Deroceras laeve (Müller), une espèce montrant peu de variabilité génétique, ont confirmé que la variation communément observée du taux de croissance chez les gastropodes ne résulte pas d'un haut niveau de polymorphisme génétique, et se manifeste même chez des progénitures issues de mères non inséminés. On a éliminé l'influence maternelle via la qualité des oeufs comme source possible de la variation, puisque les taux de croissance et de maturation de progénitures issues de mères élevées sur régime de bonne ou mauvaise qualité ne différaient pas significativement (la variation de la taille des oeufs étant contrôlée). De même, on a pu rejeter la possibilité de fixation de la trajectoire de croissance sous l'effet d'une première expérience nutritionnelle, car aucune différence n'a été observée entre des limaces d'abord nourries d'un régime de bonne ou mauvaise qualité, puis ensuite transférées sur l'autre régime. L'interaction entre individus n'est pas apparue non plus comme une cause possible de la variation, puisque des limaces nanisées n'ont pas récupéré lorsque mises en isolation, et que la variation était aussi grande chez des individus élevés en isolation. La taille des oeufs est la seule caractéristique étudiée qui a pu être liée avec la taux de croissance juvénile et avec le moment de maturation. Plus les oeufs était gros, plus la croissance était lente; la taille des oeufs semblait expliquer toute la variation observée. La fonction n'est pas encore déterminé, mais certaines des possibilités sont les suivantes : l'ajustement de la performance de la progéniture à la disponibilité des ressources, l'assurance que des individus seront disponibles pour s'accoupler lors des périodes microclimatiques favorables, la réduction de la compétition entre membres d'une même cohorte, et l'assurance de l'existence d'hétérogénéité sexuelle pour la reproduction hermaphrodite.

Type
Research Article
Information
The Memoirs of the Entomological Society of Canada , Volume 120 , Supplement S146 , 1988 , pp. 199 - 213
Copyright
Copyright © Entomological Society of Canada 1988

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References

Abeloos, M. 1964. Recherches expérimentales sur la croissance. La croissance des mollusques arionidés. Biol. Bull. Fr. Belg. 78: 215–256.Google Scholar
Arias, R.O., and Crowell, H.H.. 1963. A contribution to the biology of the gray garden slug. Bull. South. Calif. Acad. Sci. 62: 83–97.Google Scholar
Atchley, W.R. 1984. Ontogeny, timing of development, and genetic variance–covariance structure. Am. Nat. 123: 519–540.Google Scholar
Berrie, A.D. 1968. Prolonged inhibition of growth in a natural population of the fresh water snail Biomphalaria sudanica tanganyicensis (Smith) in Uganda. Ann. Trop. Med. Parasitol. 62: 45–51.Google Scholar
Blinn, W.C. 1963. Ecology of the landsnail Mesodon thyroidus and Allogona profunda. Ecology 44: 498–505.Google Scholar
Boer, P.J. den 1968. Spreading of risk and stabilization of animal numbers. Ada Biotheor. 18: 165–194.Google Scholar
Butler, A.J. 1976. A shortage of food for the terrestrial snail Helicella virgata in South Australia. Oecologia (Berlin) 25: 349–371.Google Scholar
Calow, P. 1981a. Growth in lower invertebrates. Comp. Anim. Nutr. 4: 53–76.Google Scholar
Calow, P. 1981b. Resource utilization and reproduction, pp. 245–270in Townsend, C.R., and Calow, P. (Eds.), Physiological Ecology: an Evolutionary Approach to Resource Use. Sinauer Assoc., Sunderland, Massachusetts.Google Scholar
Calow, P., and Townsend, C.R.. 1981. Resource utilization in growth, pp. 220–244in Townsend, C.R., and Calow, P. (Eds.), Physiological Ecology: an Evolutionary Approach to Resource Use. Sinauer Assoc., Sunderland, Massachusetts.Google Scholar
Cameron, R.A.D., and Carter, M.A.. 1979. Intra- and interspecific effects of population density on growth and activity of some helicid land snails (Gastropoda: Pulmonata). J. Anim. Ecol. 48: 237–246.Google Scholar
Carrick, R. 1938. The life-history and development of Agriolimax agrestis L., the gray field slug. Trans. R. Soc. Edinb. 59: 563–597.Google Scholar
Carter, M.C., and Ashdown, M.. 1984. Experimental studies on the effects of density, size, shell colour and banding phenotypes on the fecundity of Cepaea nemoralis. Malacologia 25: 219–302.Google Scholar
Cook, L.M., and Cain, A.J.. 1980. Population dynamics, shell size and morph frequency in experimental populations of the snail Cepaea nemoralis (L.). Biol. J. Linn. Soc. 14: 259–292.Google Scholar
Dan, N.A., and Bailey, S.E.R.. 1982. Growth, mortality and feeding rates of the snail Helix aspersa at different population densities in the laboratory and the depression of activity of helicid snails by other individuals or their mucus. J. Molluscan Stud. 48: 257–265.Google Scholar
Eisenberg, R.M. 1966. The regulation of density in a natural population of the pond snail, Lymnaea elodes. Ecology 47: 889–906.Google Scholar
Eisenberg, R.M. 1970. The role of food in the regulation of the pond snail, Lymnaea elodes. Ecology 51: 680–684.Google Scholar
Elwell, A.S., and Ulmer, M.I.. 1971. Notes on the biology of Anguispira alternata (Stylommatophora: Endodontidae). Malacologia 10: 199–215.Google Scholar
Foltz, D.W., Schaitkin, B.M., and Selander, R.K.. 1982. Gametic disequilibrium in the self-fertilizing slug Deroceras laeve. Evolution 36: 80–85.Google Scholar
Forbes, G.S., and Crampton, H.E.. 1942. The effects of population density upon growth and size in Lymnaea palustris. Biol. Bull. (Woods Hole) 83: 283–289.Google Scholar
Herzberg, F. 1965. Crowding as a factor in growth and reproduction of Helix aspersa. Am. Zool. 5: 254.Google Scholar
Hoffmann, R.J. 1983. The mating system of the terrestrial slug Deroceras laeve. Evolution 37: 423–425.Google Scholar
Horie, Y., and Watanabe, K.. 1983. Effect of various kinds of dietary protein and supplementation with limiting amino acids on growth, haemolymph components and uric acid excretion in the silkworm, Bombyx mori. J. Insect Physiol. 29: 187–199.Google Scholar
Judge, F.D. 1972. Aspects of the biology of the gray garden slug (Deroceras reticulatum Müller). N.Y. Exp. Stn, Geneva, Search 2: 1–18.Google Scholar
Karlin, E.J., and Bacon, C.. 1960. Courtship, mating and egg-laying behavior in the Limacidae (Mollusca). Trans. Am. Microsc. Soc. 80: 399–406.Google Scholar
Kosinska, M. 1980. The life cycle of Deroceras sturanyi (Simroth, 1894) (Pulmonata Limacidae). Zool. Pol. 28: 113–155.Google Scholar
Laurent, J., Deray, A., and Grimard, A.M.. 1984. Influence de la photopériode du degré d'hétérogénéité de la population sur la dynamique de croissance et la maturation sexuelle de l'escargot Helix aspersa. C. R. Soc. Biol. 178: 421–441.Google Scholar
Levy, M.G., Tunis, M., and Isseroff, H.. 1973. Population control in snails by natural inhibitors. Nature 241: 65–66.Google Scholar
Lusis, O. 1961. Postembryonic changes in the reproductive system of the slug Arion ater ruflis L. Proc. Zool. Soc. Lond. 137: 433–468.Google Scholar
Maury, M.F., and Reygrobellet, D.. 1963. Sur les distinctions specifiques chez les mollusques limacidés du genre Deroceras. C. R. Hebd. Seances Acad. Sci. Paris 257: 276–277.Google Scholar
McCracken, G.F., and Selander, R. K.. 1980. Self-fertilization and monogenic strains in natural populations of terrestrial slugs. Proc. Natl. Acad. Sci. U.S.A. 77: 684–688.Google Scholar
Mooij-Vogelaar, J.W., Jager, J.C., and Van der Steen, W.J.. 1970. The effect of density changes on the reproduction of the pond snail Lymnaea stagnalis (L.). Neth. J. Zool. 20: 279–288.Google Scholar
Mooij-Vogelaar, J.W., Jager, J.C., and Van der Steen, W.J.. 1973. Effects of density levels and changes in density levels on reproduction, feeding and growth in the pond snail Lymnaea stagnalis (L.). Proc. K. Ned. Akad. Wet. Ser. C Biol. Med. Sci. 76: 245–256.Google Scholar
Nicklas, N.L., and Hoffmann, R.J.. 1981. Apomictic parthenogenesis in a hermaphroditic terrestrial slug, Deroceras laeve (Muller). Biol. Bull. 160: 123–135.Google Scholar
Oosterhoff, L.M. 1977. Variation in growth rate as an ecological factor in the landsnail Cepaea nemoralis (L.). Neth. J. Zool. 27: 1–132.Google Scholar
Pollard, E. 1975. Aspects of the ecology of Helix pomatia L. J. Anim. Ecol. 44: 305–339.Google Scholar
Pomeroy, D.E. 1969. Some aspects of the ecology of the land snail Helicella virgata in South Australia. Aust. J. Zool. 17: 495–514.Google Scholar
Prior, D.J. 1983. The relationship between age and body size of individuals in isolated clutches of the terrestrial slug, Limax maximus (Linnaeus, 1858). J. Exp. Zool. 225: 321–324.Google Scholar
Rollo, C.D. 1974. Ecology of the slugs Deroceras reticulatum, D. laeve, and Arion fasciatus in Ontario corn fields. M.Sc. thesis, Univ. of Guelph, Guelph.Google Scholar
Rollo, C.D. 1983a. Consequences of competition on the reproduction and mortality of three species of terrestrial slugs. Res. Popul. Ecol. (Kyoto) 25: 20–43.Google Scholar
Rollo, C.D. 1983b. Consequences of competition on the time budgets, growth and distributions of three species of terrestrial slugs. Res. Popul. Ecol. (Kyoto) 25: 44–68.Google Scholar
Rollo, C.D. 1986. A test of the principle of allocation using two sympatric species of cockroaches. Ecology 67: 616–628.Google Scholar
Rollo, C.D. 1987. The feeding of terrestrial slugs in relation to food characteristics, starvation, maturation and life history. Malacolgia 28: 29–39.Google Scholar
Rollo, C.D., and Wellington, W.G.. 1979. Intra- and inter-specific agonistic behaviour among terrestrial slugs (Pulmonata: Stylommatophora). Can. J. Zool. 57: 846–855.Google Scholar
Rose, S.M. 1960. A feedback mechanism of growth control in tadpoles. Ecology 41: 188–199.Google Scholar
Runham, N.W., and Hunter, P.J.. 1970. Terrestrial slugs. Hutchinson Publ., London. 184 pp.Google Scholar
Runham, N.W., and Laryea, A.A.. 1968. Studies on the maturation of the reproductive system of Agriolimax reticulatus (Pulmonata: Limacidae). Malacologia 7: 93–108.Google Scholar
Smith, B.J. 1966. Maturation of the reproductive tract of Arion ater (Pulmonata: Arionidae). Malacologia 4: 325–349.Google Scholar
Steen, W.J. van der. 1977. Effects of crowding in freshwater snails: reality or myth? Malacologia 16: 265–266.Google Scholar
Stephenson, J.W. 1966. Notes on the rearing and behaviour in soil of Milax budapestensis (Hazay). J. Conchol. 26: 141–145.Google Scholar
Tattersfield, P. 1981. Density and environmental effects on shell size in some sand dune snail populations. Biol. J. Linn. Soc. 16: 71–81.Google Scholar
Tattersfield, P. 1982. Behavioural aspects of niche separation and population dynamics in terrestrial molluscs. Ph.D. thesis, Univ. of Birmingham, England.Google Scholar
Thomas, J.D., Goldsworthy, G.J., and Aram, R.H.. 1975a. Studies on the chemical ecology of snails: the effects of chemical conditioning by adult snails on the growth of juvenile snails. J. Anim. Ecol. 44: 1–28.Google Scholar
Thomas, J.D., Goldsworthy, G.J., and Benjamin, M.. 1975b. Studies on the chemical ecology of Biomphalaria glabrata: the effects of chemical conditioning by the snails kept at various densities on their growth and metabolism. J. Zool. Lond. 175: 421–437.Google Scholar
Thomas, J.D., Grealy, B., and Fennell, C.F.. 1983. The effects of varying the quantity and quality of various plants on feeding and growth of Biomphalaria glabrata (Gastropoda). Oikos 41: 77–90.Google Scholar
Wagge, L.E. 1952. Quantitative studies of calcium metabolism in Helix aspersa. J. Exp. Zool. 120: 311–342.Google Scholar
Wellington, W.G. 1957. Individual differences as a factor in population dynamics: the development of a problem. Can. J. Zool. 35: 293–323.Google Scholar
Wellington, W.G. 1960. Qualitative changes in natural populations during changes in abundance. Can. J. Zool. 38: 289–314.Google Scholar
Wellington, W.G. 1965. Some maternal influences on progeny quality in the western tent-caterpillar Malacosoma pluviale (Dyar). Can. Ent. 97: 1–14.Google Scholar
Wellington, W.G. 1977. Returning the insect to insect ecology: some consequences for pest management. Environ. Ent. 6: 1–8.Google Scholar
Wilbur, H.M. 1984. Complex cycles and community organization in amphibians, pp. 195–224in Price, P.W., Slobodchikoff, C.N., and Gand, W.S. (Eds.), A New Ecology: Novel Approaches to Interactive Systems. John Wiley, New York.Google Scholar
Williamson, P., Cameron, R.A.D., and Carter, M.A.. 1976. Population density affecting adult shell size of snail Cepaea nemoralis (L.). Nature 263: 496–497.Google Scholar
Wolda, H. 1970. Variation in growth rate in the landsnail Cepaea nemoralis. Res. Popul. Ecol. (Kyoto) 12: 185–204.Google Scholar
Wolda, H. 1971. Ecological variation and its implications for the dynamics of populations of the landsnail Cepaea nemoralis. pp. 98–108in den Boer, P.J., and Gradwell, G.R. (Eds.), Dynamics of Populations. PUDOC, Wageningen.Google Scholar
Wolda, H., and Kreulen, D.. 1973. Ecology of some experimental populations of the land snail Cepaea nemoralis (L.). 2: Production and survival of eggs and juveniles. Neth. J. Zool. 23: 168–188.Google Scholar