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An experimental investigation of interactions in snail-macrophyte-epiphyte systems

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Summary

An experimental investigation under field conditions of enclosures containing freshwater pulmonate snails, the macrophyteCeratophyllum demersum and epiphytes, produced evidence of beneficial interactions.Ceratophyllum growth, measured in terms of stem length, numbers of leaf-nodes and growing tips and leaf survival was significantly enhanced in the presence of snails. This effect was attributed to the increased availability of plant nutrients of snail origin, such as phosphates and ammonia, as well as to the snails' action as “cleaning symbionts” in reducing the density of bacterial and algal epiphyton potentially deleterious to macrophytes. Principal component analysis revealed both seasonal and treatment effects of snail grazing on algal epiphyton. Small adnate algal species (e.g.Cocconeis placentula) survived grazing and benefited from the removal of larger, competitor, species. Snail densities increased in all treatments, despite high (86%) juvenile mortality. It is concluded that freshwater pulmonate snails are strong interactors in lentic habitats, enhancing the growth ofCeratophyllum and producing characterisic epiphyte communities. This benefits not only the snails, but also the plants and epiphytes that are associated with them. Thus the interactions between these component parts of the community can be considered as mutualistic.

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References

  • Aram RH (1970) Studies on the population biology ofLymnaea peregra (Mull.) andPlanorbis planorbis (L.). Unpublished D. Phil Thesis, University of Sussex, UK

  • Arber A (1963) Water plants, a study of aquatic angiosperms. Reprint J. Cramer Weinheim. Hafner, New York

    Google Scholar 

  • Bronmark C (1985) Interactions between macrophytes, epiphytes and herbivores: an experimental approach. Oikos 45:26–30

    Google Scholar 

  • Bronmark C (1989) Interactions between epiphytes, macrophytes and freshwater snails: a review. J Moll Stud 55:299–311

    Google Scholar 

  • Bronmark C, Rundle SD, Erlandsson A (1991) Interactions between freshwater snails and tadpoles: competition and facilitation. Oecologia 87:8–18

    Google Scholar 

  • Brown KM (1982) Resource overlap and competition in pond snails: an experimental analysis. Ecology 63:412–422

    Google Scholar 

  • Calow P (1978) The evolution of life-cycle strategies in fresh-water gastropods. Malacologia 17:351–364

    Google Scholar 

  • Cattaneo A (1983) Grazing on epiphytes. Limnol Oceanogr 32:124–132

    Google Scholar 

  • Cattaneo A, Kalff J (1986) The effect of grazer size manipulation on periphyton communities. Oecologia 69:612–617

    Article  Google Scholar 

  • Coen LD (1988) Herbivory by crabs and the nature of algal epibionts on caribbean host corals. Oecologia 75:198–203

    Article  Google Scholar 

  • Cuker BE (1983a) Grazing and nutrient interactions in controlling the activity and composition of the epilithic algal community in an arctic lake. Limnol Oceanogr 28:133–141

    CAS  Google Scholar 

  • Cuker BE (1983b) Competition and coexistance among the grazing snailLymnaea, Chironomidae, and microcrustacea in an arctic epilithic lacustrine community. Ecology 64:10–15

    Google Scholar 

  • Dethier MN, Duggins DO (1984) An “indirect commensalism” between marine herbivores and the importance of competitive hierarchies. Am Nat 124:205–219

    Article  Google Scholar 

  • Eisenberg RM (1970) The role of food in the regulation of the pond snail,Lymnaea elodes. Ecology 51:680–684

    Google Scholar 

  • Fairchild GW, Sherman JW, Acker FW (1989) Effects of nutrient (N,P,C) enrichment, grazing and depth upon littoral periphyton of a softwater lake. Hydrobiologia 173:69–83

    Article  CAS  Google Scholar 

  • Feminella JW, Resh VH (1991) Herbivorous caddisflies, macroalgae, and epilithic microalgae: dynamic interactions in a stream grazing system. Oecologia 87:247–256

    Article  Google Scholar 

  • Gaten E (1986) Life cycle ofLymnaea peregra (Gastropoda: Pulmonata) in the Leicester Canal, UK with an estimate of annual production. Hydrobiologia 135:45–54

    Article  Google Scholar 

  • Gauch HG Jr (1984) Multivariate analysis in community ecology (Cambridge Studies in Ecology 1) Cambridge University Press, Cambridge

    Google Scholar 

  • Gregory SV (1983) Plant herbivore interactions in stream systems. In: Barnes JR, Minshall GW (eds) Stream ecology: Application and testing of general ecological theory. Plenum Press, New York London, pp 157–189

    Google Scholar 

  • Hill WR, Knight AW (1988) Concurrent grazing effects of two stream insects on periphyton. Limnol Oceanogr 33:15–26

    Google Scholar 

  • Hoagland KD, Roemer SC, Rosowski JR (1982) Colonization and community structure of two periphytic assemblages, with emphasis on the diatoms (Bacillariophyceae). Am J Bot 69:188–213

    Google Scholar 

  • Hootsmans MJM, Vermaat JE (1985) The effects of periphyton grazing by three epifaunal species on the growth ofZostera marina L. under experimental conditions. Aquat Bot 22:83–88

    Article  Google Scholar 

  • Hossell JC, Baker JH (1979) A note on the enumeration of epiphytic bacteria by microscopic methods with particular reference to two freshwater plants. J Appl Bacteriol 46:87–92

    Google Scholar 

  • Howard RK, Short FT (1986) Seagrass growth and survivorship under the influence of epiphyte grazers. Aquat Bot 24:287–302

    Article  Google Scholar 

  • Jacoby JM (1985) Grazing effects on periphyton byTheodoxus fluviatilis (Gastropoda) in a lowland stream. J Freshw Ecol 3:265–274

    Google Scholar 

  • Jacoby JM (1987) Alterations in periphyton characteristics due to grazing in a cascade foothill stream. Freshw Biol 18:495–508

    Google Scholar 

  • Kairesalo T, Koskimies I (1987) Grazing by oligochactes and snails on epiphytes. Freshw Biol 17:317–324

    Google Scholar 

  • Kesler DH (1981) Periphyton grazing byAmnicola limosa: an enclosure exclosure experiment. J Freshw Ecol 1:51–59

    Google Scholar 

  • Lam PKS, Calow P (1989) Intraspecific life-history variation inLymnaea peregra (Gastropoda: Pulmonata) 1. Field study. J Anim Ecol 58:571–588

    Google Scholar 

  • Lamberti GA, Ashkenas LR, Gregory SV, Steinman AD (1987) Effects of three herbivores on periphyton communities in laboratory streams. J N Am Benthol Soc 6:92–104

    Google Scholar 

  • Lodge DM (1985) Macrophyte-gastropod associations: observations and experiments on macrophyte choice by gastropods. Freshw Biol 15:695–708

    Google Scholar 

  • Lodge DM (1986) Selective grazing on periphyton: a determinant of freshwater gastropod microdistributions. Freshw Biol 16:831–841

    Google Scholar 

  • Lodge DM, Kelly P (1985) Habitat disturbance and the stability of freshwater gastropod populations. Oecologia 68:111–117

    Article  Google Scholar 

  • Lowe RL, Hunter RD (1988) Effects of grazing byPhysa integra on periphyton community structure. J N Am Benthol Soc 7:29–36

    Google Scholar 

  • Mat I (1988) Ecophysiological aspects of nitrogen metabolism in the freshwater snailBiomphalaria glabrata. D. Phil Thesis, University of Sussex, UK

  • Mason CF, Bryant RJ (1975) Periphyton production and grazing by chironomids in Alderfen Broad, Norfolk. Freshw Biol 5:271–277

    Google Scholar 

  • Morin JO (1986) Initial colonization of periphyton on natural and artifical apices ofMyriophyllum heterophyllum Michx. Freshw Biol 16:685–694

    Google Scholar 

  • Osenberg CW (1989) Resource limitation, competition and the influence of life history in a freshwater snail community. Oecologia 79:512–519

    Article  Google Scholar 

  • Peterson CG (1987) Gut passage and insect grazer selectivity of lotic diatoms. Freshw Biol 18:455–460

    Google Scholar 

  • Porter KG (1976) Enhancement of algal growth and productivity by grazing zooplankton. Science 192:1332–1333

    Google Scholar 

  • Power ME (1990) Resource enhancement by indirect effects of grazers: Armoured Catfish, algae and sediment. Ecology 71:897–904

    Google Scholar 

  • Pringle CM (1990) Nutrient-spatial heterogeneity: effects on community structure, physiognomy, and diversity of stream algae. Ecology 71:905–920

    Google Scholar 

  • Pyke DA, Thompson JN (1986) Statistical analysis of survival and removal rate experiments. Ecology 67:240–245

    Google Scholar 

  • roemer SC, Hoagland KD, Rosowski JR (1984) Development of a freshwater periphyton community as influenced by diatom mucilages. Can J Bot 62:1799–1813

    Google Scholar 

  • Rogers KH, Breen CM (1981) Effects of epiphyton onPotamogeton crispus L. leaves. Microb Ecol 7:351–363

    Google Scholar 

  • Rogers KH, Breen CM (1983) An investigation of macophyte, epiphyte, and grazer interactions. In: Wetzel RG (Ed) Periphyton of Freshwater ecosystems. Junk, The Hague

    Google Scholar 

  • Subramaniam J (1990) The biochemical ecology of freshwater communities with particular reference to the neuston. D.Phil Thesis, University of Sussex, UK

  • Tilman D, Kiesling R, Sterner R, Kilham SS, Johnson FA (1986) Green, bluegreen and diatom algae: taxonomic differences in competitive ability for phosphorus, silicon and nitrogen. Arch Hydrobiol 106:473–485

    Google Scholar 

  • Thomas JD (1987) An evaluation of the interactions between freshwater pulmonate snail hosts of human schistosomes and macrophytes. Phil Trans R Soc London B 315:75–125

    CAS  Google Scholar 

  • Thomas JD (1990) Mutualistic interactions in freshwater modular systems with molluscan components. Adv Ecol Res 20:125–178

    Google Scholar 

  • Thomas JD, Tait AI (1984) Control of the snail hosts of schistosomiasis by environmental manipulation: a field and laboratory appraisal in the Ibadan area, Nigeria. Phil Trans R Soc London B305:201–253

    CAS  Google Scholar 

  • Thomas JD, Nwanko DI, Sterry PR (1985) The feeding strategies of juvenile and adultBiomphalaria glabrata (Say) under simulated natural conditions and their relavance to ecological theory and snail control. Proc R Soc London B 266:177–209

    Google Scholar 

  • Thomas JD, Kowalczyk C, Somasundaram B (1989) The biochemical ecology ofBiomphalaria glabrata, a snail host ofSchistosoma mansoni: Short chain carboxylic and amino acids as phagostimulants. Comp Biochem Physiol 93A:899–911

    CAS  Google Scholar 

  • Underwood GJC (1991a) Note: Colonization and invasion of leaves of the aquatic macrophyteCeratophyllum demersum L. by epiphytic bacteria. Microb Ecol 21:267–275

    Google Scholar 

  • Underwood GJC (1991b) Growth enhancement of the macrophyteCeratophyllum demersum in the presence of the snailPlanorbis planorbis: the effect of grazing and chemical conditioning. Freshw Biol 26:325–334

    CAS  Google Scholar 

  • Underwood GJC, Baker JH (1991) The effect of various aquatic bacteria on the growth and senescence of duckweed (Lemna minor). J Appl Bacteriol 70:92–196

    Google Scholar 

  • Underwood GJC, Thomas JD (1990) Grazing interactions between pulmonate snails and epiphytic algae and bacteria. Freshw Biol 23:505–521

    Google Scholar 

  • van Aardt WJ, Wolmarans CT (1981) Evidence for non-assimilation ofChlorella by the african freshwater snailBulinus (Physopsis) globosus. S Afr J Sci 77 319–320

    Google Scholar 

  • Zar JH (1984) Biostatisical analysis. 2nd edn. Prentice Hall Int Inc, New Jersey

    Google Scholar 

Download references

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Authors and Affiliations

  1. School of Biology, University of Sussex, Falmer, BN1 9QG, Brighton, Sussex, UK

    G. J. C. Underwood & J. D. Thomas

  2. N.E.R.C., Polaris House, North Star Avenue, SN2 1EU, Swindon, Wiltshire, UK

    J. H. Baker

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  1. G. J. C. Underwood
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  2. J. D. Thomas
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  3. J. H. Baker
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Underwood, G.J.C., Thomas, J.D. & Baker, J.H. An experimental investigation of interactions in snail-macrophyte-epiphyte systems. Oecologia 91, 587–595 (1992). https://doi.org/10.1007/BF00650335

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