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Diel activity cycles of freshwater gastropods under natural light: Patterns and ecological implications

Published online by Cambridge University Press:  15 February 2010

Paola Lombardo ,
Francesco Paolo Miccoli ,
Marco Giustini  and
Bruno Cicolani
Paola Lombardo*
Affiliation:
Department of Environmental Sciences – Ecology Section, University of L'Aquila, Coppito Science Center, via Vetoio 20, Coppito, 67100 L'Aquila, Italy
Francesco Paolo Miccoli
Affiliation:
Department of Environmental Sciences – Ecology Section, University of L'Aquila, Coppito Science Center, via Vetoio 20, Coppito, 67100 L'Aquila, Italy
Marco Giustini
Affiliation:
Department of Environmental Sciences – Ecology Section, University of L'Aquila, Coppito Science Center, via Vetoio 20, Coppito, 67100 L'Aquila, Italy
Bruno Cicolani
Affiliation:
Department of Environmental Sciences – Ecology Section, University of L'Aquila, Coppito Science Center, via Vetoio 20, Coppito, 67100 L'Aquila, Italy
*
physa@tiscali.it
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Abstract

Though much is known about freshwater snail ecology, their circadian rhythms remain poorly investigated. Well-fed, stress-free, mid-size adults of six species common in central Italian lakes were exposed to natural sunlight and photoperiod, and their activity status was recorded at 3-h intervals during a 9-d indoor experiment. All species exhibited evident diurnal habits despite high individual variability, with midday-to-early-afternoon activity peaks. Activity was correlated with diel light conditions but not with short-term changes in albedo. The prosobranch Bithynia (=Codiella) leachii and the pulmonates Physa (=Physella) acuta and Planorbis planorbis were the most active species and exhibited the longest-lasting response to daytime food addition. The prosobranch Valvata piscinalis exhibited long periods retracted in its shell with the operculum shut, and the remaining taxa (the pulmonates Galba (=Lymnaea) truncatula and Radix (=Lymnaea) auricularia) exhibited an intermediate degree of activity. P. acuta was the most active species at night and exhibited the quicker response to nighttime food addition. Alertedness to (diurnal) predators may be highest for the highly active P. acuta and P. planorbis, whose antipredator defenses are mainly behavioral. Diel activity patterns and other ecological characteristics suggest that P. acuta may be favored in food-rich habitats, while V. piscinalis may not be able to fully exploit food resources, especially if in limiting quantities. All snail species – and P. acuta in particular – may stimulate periphyton metabolism while keeping its biomass low by grazing mainly during the time of maximum photosynthesis.

Keywords

Circadian rhythmslight irradiancefeeding behaviorherbivorypredation
Type
Research Article
Information
Annales de Limnologie - International Journal of Limnology , Volume 46 , Issue 1 , 2010 , pp. 29 - 40
Copyright
© EDP Sciences, 2010

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References

Anderson, R., 2003. Physella (Costatella) acuta Draparnaud in Britain and Ireland – Its taxonomy, origins and relationships to other introduced Physidae. J. Conchol. , 38, 7–21.
Bank R.A., 2007. Fauna Europaea: Mollusca: Gastropoda – Fauna Europaea version 1.3, available at http://www.faunaeur.org, last visited 2nd January 2010.
Batschelet E., 1965. Statistical Methods for the Analysis of Problems in Animal Orientation and Certain Biological Rhythms, American Institute of Biological Sciences, Washington, DC.
Batschelet E., 1981. Circular Statistics in Biology, Academic Press, New York.
Beeston, D.E. and Morgan, E., 1977. The locomotor activity rhythm of a tropical freshwater prosobranch. J. Moll. Stud. , 43, 453–454.
Berg, K. and Ockelmann, K.W., 1959. The respiration of freshwater snails. J. Exp. Biol. , 36, 690–708.
Bourassa, N. and Cattaneo, A., 1998. Control of periphyton biomass in Laurentian streams (Québec). J. N. Am. Benthol. Soc. , 17, 420–429.
Brönmark, C. and Malmqvist, B., 1986. Interactions between the leech Glossiphonia complanata and its gastropod prey. Oecologia , 69, 268–276. CrossRef
Brönmark C. and Weisner S.E.B., 1992. Indirect effects of fish community structure on submerged vegetation in shallow, eutrophic lakes: an alternative mechanism. Hydrobiologia, 243/244, 293–301.
Brown, K.M., 1982. Resource overlap and competition in pond snails: an experimental analysis. Ecology , 63, 412–422. CrossRef
Brown K.M., 2001. Mollusca: Gastropoda. In: Thorp J.H. III and Covich A.P. (eds.), Ecology and Classification of North American Freshwater Invertebrates, 2nd edn., Academic Press, San Diego, 297–329.
Burgmer, T., Hillebrand, H. and Pfenninger, M., 2007. Effects of climate-driven temperature changes on the diversity of freshwater macroinvertebrates. Oecologia , 151, 93–103. CrossRef
Chaudry, M. and Morgan, E., 1987. Factors affecting the growth and fecundity of Bulinus tropicus. J. Moll. Stud. , 53, 52–61.
Cianfanelli S., Lori E. and Bodon M., 2007. Non-indigenous freshwater molluscs and their distribution in Italy. In: Gherardi F. (ed.), Biological Invaders in Inland Waters: Profiles, Distribution, and Threats, Springer, Dordrecht, 103–121.
Costil, K., 1994. Influence of temperature on survival and growth of two freshwater planorbid species, Planorbarius corneus (L.) and Planorbis planorbis (L.). J. Moll. Stud. , 60, 223–235.
Costil, K. and Clement, B., 1996. Relationship between freshwater gastropods and plant communities reflecting various trophic levels. Hydrobiologia , 321, 7–16. CrossRef
Crowl, T.A. and Covich, A.P., 1990. Predator-induced life-history shifts in a freshwater snail. Science , 247, 949–951. CrossRef
DeWitt, T.J., Robinson, B.W. and Wilson, D.S., 2000. Functional diversity among predators of a freshwater snail imposes an adaptive trade-off for shell morphology. Evol. Ecol. Res. , 2, 129–148.
Dillon R.T. Jr., 2000. The Ecology of Freshwater Molluscs, Cambridge University Press, Cambridge.
Dillon, R.T Jr., Wethington, A.R., Rhett, J.M. and Smith, T.P., 2002. Populations of the European freshwater pulmonate Physa acuta are not reproductively isolated from American Physa heterostropha or Physa integra. Invert. Biol. , 121, 226–234.
Ferreri, D., 1995. Molluschi, irudinei, e turbellaria tricladi delle acque dolci della Provincia di Lecce. Thal. Salent. , 21, 29–49.
Gaino E., Cianficconi F., Corallini Sorcetti C., Lancioni T., Todini B., Rebora M., Chiappafreddo U., Bicchierai M.C. and Spinelli G., 2001. Lago di Piediluco: Monitoraggio della Fauna del Canneto (Poriferi e Macroinvertebrati), 1999–2000. Unpublished report, Department of Animal Biology and Ecology, University of Perugia.
García-Berthou E., Boix D. and Clavero M., 2007. Non-indigenous animal species naturalized in Iberian inland waters. In: Gherardi F. (ed.), Biological Invaders in Inland Waters: Profiles, Distribution, and Threats, Springer, Dordrecht, 123–140.
Girod A., Bianchi I. and Mariani M., 1980. Guide per il Riconoscimento delle Specie Animali delle Acque Interne Italiane. 7. Gasteropodi, 1. (Pulmonata; Prosobranchia: Neritidae, Viviparidae, Bithyniidae, Valvatidae), CNR Publication # AQ/1/44, Consiglio Nazionale delle Ricerche, Verona.
Gotelli N.J. and Ellison A.M., 2004. A Primer of Ecological Statistics, Sinauer, Sunderland.
Gross, E.M., 2003. Differential response of tellimagrandin II and total bioactive hydrolysable tannins in an aquatic angiosperm to changes in light and nitrogen. Oikos , 103, 497–504. CrossRef
Hodasi, J.K.M., 1976. The effects of low temperature on Lymnaea truncatula. Zeits. Parasitenk. , 48, 281–286. CrossRef
Hotelling, H., 1931. The generalization of Student's ratio. Ann. Math. Statist. , 2, 360–378.
Hourdin, P., Vignoles, P., Dreyfuss, G. and Rondelaud, D., 2006. Galba truncatula (Gastropoda, Lymnaeida): effects of daily water level variations on the ecology and ethology of populations living upstream from a dam. Ann. Limnol. - Int. J. Lim. , 42, 173–180.
Hurlbert, S.H., 1984. Pseudoreplication and the design of ecological field experiments. Ecol. Monogr. , 54, 187–211. CrossRef
Jokinen, E.H., 1987. Structure of freshwater snail communities: species–area relationships and incidence categories. Am. Malacol. Bull. , 5, 9–19.
Jones J.I., Young J.O., Haynes G.M., Moss B., Eaton J.W. and Hardwick K.J., 1999. Do submerged aquatic plants influence their periphyton to enhance the growth and reproduction of invertebrate mutualists? Oecologia, 120, 463–474.
Jones, J.I., Eaton, J.W. and Hardwick, K., 2000. The influence of periphyton on boundary layer conditions: a pH microelectrode investigation. Aquat. Bot. , 67, 191–206.
Kabat A.K. and Hershler R., 1993. The Prosobranch Snail Family Hydrobiidae (Gastropoda: Rissoidea): Review of Classification and Supraspecific Taxa, Smithsonian Contributions to Zoology #547, Smithsonian Institution Press, Washington.
Kelly, P.M. and Cory, J.S., 1987. Operculum closing as a defence against predatory leeches in four British freshwater prosobranch snails. Hydrobiologia , 144, 121–124. CrossRef
Kesler, D.H. and Munns, W.R Jr., 1989. Predation by Belostoma flumineum (Hemiptera): an important cause of mortality in freshwater snails. J. N. Am. Benthol. Soc. , 8, 342–350.
Lakowitz, T., Brönmark, C. and Nyström, P., 2008. Tuning in to multiple predators: conflicting demands for shell morphology in a freshwater snail. Freshw. Biol. , 53, 2184–2191.
Lombardo, P., 1997. Predation by Enallagma nymphs (Odonata, Zygoptera) under different conditions of spatial heterogeneity. Hydrobiologia , 356, 1–9. CrossRef
Lombardo P., 2001. Effects of freshwater gastropods on epiphyton, macrophytes, and water transparency under meso- to eutrophic conditions, Ph.D. Dissertation, Kent State University, Kent.
Lombardo, P., 2005. Applicability of littoral food-web biomanipulation for lake management purposes: snails, macrophytes, and water transparency in northeast Ohio shallow lakes. Lake Reserv. Manage. , 21, 186–202.
Lombardo, P. and Cooke, G.D., 2002. Consumption and preference of selected food types by two freshwater gastropod species. Arch. Hydrobiol. , 155, 667–685.
Lombardo, P. and Cooke, G.D., 2004. Resource use and partitioning by two co-occurring freshwater gastropod species. Arch. Hydrobiol. , 159, 229–251. CrossRef
Lowe, R.L. and Hunter, R.D., 1988. Effects of grazing by Physa integra on periphyton community structure. J. N. Am. Benthol. Soc. , 7, 29–36.
Macan, T.T., 1977. The influence of predation on the composition of fresh-water animal communities. Biol. Rev. , 52, 45–70.
Mastrantuono, L. and Mancinelli, T., 2005. Littoral invertebrates associated with aquatic plants and bioassessment of ecological status in Lake Bracciano (Central Italy). J. Limnol. , 64, 43–53. CrossRef
McDonald, S., 1973. Activity patterns of Lymnaea stagnalis (L.) in relation to temperature conditions: a preliminary study. Malacologia , 14, 395–396.
Moeller, R.E., Burkholder, J.M. and Wetzel, R.G., 1988. Significance of sedimentary phosphorus to a submersed freshwater macrophyte (Najas flexilis) and its algal epiphytes. Aquat. Bot. , 32, 261–281.
Morgan, E. and Last, V., 1982. The behavior of Bulinus africanus: a circadian profile. Anim. Behav. , 30, 557–567. CrossRef
Mouthon, J. and Daufresne, M., 2008. Population dynamics and life cycle of Pisidium amnicum (Müller) (Bivalvia: Sphaeriidae) and Valvata piscinalis (Müller) (Gastropoda: Prosobranchia) in the Saône River, a nine-year study. Ann. Limnol. - Int. J. Lim. , 44, 241–251.
Muñoz, I., Real, M., Guasch, H., Navarro, E. and Sabater, S., 2000. Resource limitation by freshwater snail (Stagnicola vulnerata) grazing pressure: an experimental study. Arch. Hydrobiol. , 148, 517–532.
Overbeck, J., 1962. Untersuchungen zum Phosphathaushalt von Grünalgen. III. Das Verhalten der Zellfraktionen von Scenedesmus quadricauda (Turp.) Bréb. im Tagescyclus unter verschiedenen Belichtungsbedingungen und bei verschidenen Phosphatverbindungen. Arch. Mikrobiol. , 41, 11–26. CrossRef
Peckarsky, B.L. and Cowan, C.A., 1995. Microhabitat and activity periodicity of predatory stoneflies and their mayfly prey in a western Colorado stream. Oikos , 74, 513–521. CrossRef
Perrin, N., 1986. Les paramètres du cycle vital de Physa acuta (Gastropoda, Mollusca) en milieu expérimental. Rev. Suisse Zool. , 93, 725–736. CrossRef
Pianka E.R., 1976. Competition and niche theory. In: May R.M. (ed.), Theoretical Ecology, Principles and Applications, Blackwell Scientific Publications, Oxford, 114–141.
Pimentel-Souza, F., Schall, V.T., Lautner, R Jr., Barbosa, N.D.C., Schettino, M. and Fernandes, N., 1984. Behavior of Biomphalaria glabrata (Gastropoda: Pulmonata) under different lighting conditions. Can. J. Zool. , 62, 2328–2334.
Rotenberg, L., Jurberg, P. and Pieri, O.S., 1989. Relationship between light conditions and behavior of the freshwater snail Biomphalaria glabrata (Say). Hydrobiologia , 174, 111–116. CrossRef
Russell-Hunter, W., 1961. Life cycles of four freshwater snails in limited populations in Loch Lomond with a discussion of infraspecific variation. Proc. Zool. Soc. London , 137, 135–171.
Scheffer M., 1998. Ecology of Shallow Lakes, reprinted with corrections in 2004, Kluwer Academic Publishers, Dordrecht.
Soeder C.J., 1965. Some aspects of phytoplankton growth and activity. Mem. Ist. Ital. Idrobiol., 18, Suppl., 47–59.
Ter Maat, A., Zonneveld, C., de Visser, J.A.G.M., Jansen, R.F., Montagne-Wajer, K. and Koene, J.M., 2007. Food intake, growth, and reproduction as affected by day length and food availability in the pond snail Lymnaea stagnalis. Am. Malacol. Bull. , 23, 113–120.
Tomba, A.M., Keller, T.A. and Moore, P.A., 2001. Foraging in complex odor landscapes: chemical orientation strategies during stimulation by conflicting chemical cues. J. N. Am. Benthol. Soc. , 20, 211–222.
Tripet, F. and Perrin, N., 1994. Size-dependent predation by Dugesia lugubris (Turbellaria) on Physa acuta (Gastropoda): experiments and model. Funct. Ecol. , 8, 458–463.
Turner, A.W., Fetterolf, S.A. and Bernot, R.J., 1999. Predator identity and consumer behavior: differential effects of fish and crayfish on the habitat use of a freshwater snail. Oecologia , 118, 242–247. CrossRef
Underwood A.J., 1997. Experiments in Ecology: Their Logical Design and Interpretation Using Analysis of Variance, Cambridge University Press, Cambridge.
Wojdak, J.M. and Mittelbach, G.G., 2007. Consequences of niche overlap for ecosystem functioning: an experimental test with pond grazers. Ecology , 88, 2072–2083. CrossRef
Zar J.H., 1998. Biostatistical Analysis, 4th edn., Prentice Hall, Upper Saddle Creek.
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