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Combining gut fluorescence technique and spatial analysis to determine Littorina littorea grazing dynamics in nutrient-enriched and nutrient-unenriched littoral mesocosms

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Abstract

Spatiotemporal distribution patterns in relation to feeding behavior of herbivorous gastropods have been studied extensively, but still knowledge about small-scale patterns is limited in relation to eutrophication. This experimental study aimed to describe the small-scale distribution of Littorina littorea in nutrient-enriched and nutrient-unenriched mesocosms in a merely atidal region and relate the distribution to food abundance and possible competing organisms, while checking simultaneously for feeding activities. The latter part was accomplished through the “gut fluorescence technique” GFT (which, to our knowledge, has not previously been used for benthic grazers) to estimate per capita grazing rates and the former part through monitoring of spatial heterogeneity of L. littorea and co-variation with sessile organisms (using semivariograms and cross-semivariograms, respectively). After 5 months of nutrient addition, the abundance and biomass of L. littorea had increased in enriched systems, which also had significantly higher total biomass of green algae. Gut pigment content was higher in L. littorea from enriched mesocosms, and gut depletion rate was higher in L. littorea from unenriched mesocosms. Spatial analysis showed that L. littorea exhibited generally random patterns (suggesting feeding activities) but sometimes (often in the morning) spatial patchiness (clumped distribution) in both enriched and unenriched conditions. There was mainly positive co-variation between L. littorea and biofilm, while different nutrient conditions exhibited contrasting co-variation between L. littorea and barnacles (positive co-variation in enriched and negative co-variation in unenriched mesocosms). The study offered insights into how feeding behavior and spatial distribution of a species may interact with community components differently under different nutrient regimes. The applied methodology can be useful for purposes of faster examination of grazing effects among different regions and also to compare grazing intensities and interactions between grazers and the benthic communities in disturbed (including pollution and nutrient enrichment) and non-disturbed systems, as well as in up-welling versus non-upwelling areas.

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References

  • Asmus H (1987) Secondary production of an intertidal mussel bed community related to its storage and turnover compartments. Mar Ecol Prog Ser 39:251–266

    Article  Google Scholar 

  • Båmstedt U, Gifford DJ, Irigoien X, Atkinson A, Roman A (2000) Feeding. In: Harris R, Wiebe P, Lenz J, Skjoldal HR (eds) ICES zooplankton methodology manual. Academic Press, London, pp 297–399

    Chapter  Google Scholar 

  • Bernard KS, Froneman PW (2005) Mesozooplankton Community structure and grazing impact in the Polar Frontal Zone of the South Indian Ocean during Austral Autumn 2002. Polar Biol 26:268–275

    Google Scholar 

  • Bertness MD, Yund PO, Brown AF (1983) Snail grazing and the abundance of algal crusts on a sheltered New England rocky beach. J Exp Mar Biol Ecol 71:147–164

    Article  Google Scholar 

  • Boaventura D, Alexander M, Della Santina P, Smith ND, Re P, da Fonseca LC, Hawkins SJ (2002) The effects of grazing on the distribution and composition of low-shore algal communities on the central coast of Portugal and on the southern coast of Britain. J Exp Mar Biol Ecol 267:185–206

    Article  Google Scholar 

  • Bokn T, Lein TE (1978) Long-term changes in fucoid associations of inner Oslofjord, Norway. Norw J Bot 25:9–14

    Google Scholar 

  • Bokn TL, Moy FE, Christie H, Engelbert S, Karez R, Kersting K, Kraufvelin P, Lindblad C, Marbà N, Pedersen MF, Sørensen K (2002) Are rocky shore ecosystems affected by nutrient enriched seawater? Some preliminary results from a mesocosm experiment. Hydrobiologia 484:167–175

    Article  Google Scholar 

  • Bokn TL, Duarte CM, Pedersen MF, Marbà N, Moy FE, Barrón C, Bjerkeng B, Borum J, Christie H, Engelbert S, Fotel FL, Hoell EE, Karez R, Kersting K, Kraufvelin P, Lindblad C, Olsen M, Sommer U, Sørensen K (2003) The response of experimental rocky shore communities to nutrient additions. Ecosystems 6:577–594

    Article  CAS  Google Scholar 

  • Boyd CM, Smith SL, Cowles TJ (1980) Grazing patterns of copepods in the upwelling systems off Peru. Limnol Oceanogr 25:583–596

    Article  Google Scholar 

  • Burkepile DE, Hay ME (2006) Herbivore vs. nutrient control of marine primary producers: context-dependent effects. Ecology 87:3128–3139

    Article  Google Scholar 

  • Buschbaum C (2000) Direct and indirect effects of Littorina littorea (L.) on barnacles growing on mussel beds in the Wadden Sea. Hydrobiologia 440:119–128

    Article  Google Scholar 

  • Carlson RL, Shulman MJ, Ellis JC (2006) Factors contributing to spatial heterogeneity in the abundance of the common periwinkle Littorina littorea. J Mol Stud 72:149–156

    Article  Google Scholar 

  • Chang AL, Blakeslee AMH, Miller AW, Ruiz GM (2011) Establishment failure in biological invasions: a case history of Littorina littorea in California, USA. PLOS One 6(1):e16035

    Article  CAS  Google Scholar 

  • Chapman MG (2000) Variability of foraging in highshore habitats: dealing with unpredictability. Hydrobiologia 426:75–87

    Article  Google Scholar 

  • Chapman MG, Underwood AJ (1996) Influence of tidal conditions, temperature and desiccation on patterns of aggregation of the high-shore periwinkle, Littorina unifasciata, in the New South Wales, Australia. J Exp Mar Biol Ecol 196:213–237

    Article  Google Scholar 

  • Cloern JE (2001) Our evolving conceptual model of the coastal eutrophication problem. Mar Ecol Prog Ser 210:223–253

    Article  CAS  Google Scholar 

  • Coleman RA (2010) Limpet aggregation does not alter desiccation in the limpet Cellana tramoserica. J Exp Mar Biol Ecol 386:113–118

    Article  Google Scholar 

  • Coleman RA, Benedetti-Cecchi L, Åberg P, Arenas F, Arrontes J, Castro J, Hartnoll RG, Jenkins SR, Paula J, Della Santina P, Underwood AJ, Hawkins SJ (2006) A continental scale evaluation of limpet grazing on rocky shores. Oecologia 147:556–564

    Article  Google Scholar 

  • Connell JH (1985) Variation and persistence of rocky shore populations. In: Moore PG, Seed R (eds) The ecology of rocky coasts. Hodder and Stoughton Educational Press, Kent, England, pp 57–69

    Google Scholar 

  • Connell SD, Irwing AD (2009) The subtidal ecology of rocky coasts: local-regional biogeographic patterns and their experimental analysis. In: Witman JD, Kaustuv R (eds) Marine macroecology. University of Chicago Press, Chicago, pp 392–417

    Google Scholar 

  • Dale MRT (2000) Spatial pattern analysis in plant ecology. Cambridge University Press, Cambridge. 326 pp

  • Diaz ER, McQuiad CD (2011) A spatially explicit approach to trophic interactions and landscape formation: patchiness in small-scale variability of grazing effects along an intertidal stress gradient. J Ecol 99:416–430

    Google Scholar 

  • Diaz ER, Erlandsson J, McQuaid CD (2011) Detecting spatial heterogeneity in intertidal algal functional groups, grazers and their co-variation among shore levels and sites. J Exp Mar Biol Ecol 409:123–135

    Article  Google Scholar 

  • Durbin EG, Campbell RG (2007) Reassessment of the gut pigment method for estimating in situ zooplankton ingestion. Mar Ecol Prog Ser 331:305–307

    Google Scholar 

  • Eriksson BK, Rubach A, Hillebrand H (2006) Biotic habitat complexity controls species diversity and nutrient effects on net biomass production. Ecology 87:246–254

    Article  Google Scholar 

  • Eriksson BK, Ljunggren L, Sandström A, Johansson G, Mattila J, Rubach A, Råberg S, Snickars M (2009) Declines in predatory fish promote bloom-forming macroalgae. Ecol Appl 19:1975–1988

    Article  Google Scholar 

  • Erlandsson J, McQuaid CD (2004) Spatial structure of recruitment in the mussel Perna perna at local scales: effects of adults, algae and recruit size. Mar Ecol Prog Ser 267:173–185

    Article  Google Scholar 

  • Erlandsson J, McQuaid CD, Kostylev V (2005) Contrasting spatial heterogeneity of sessile organisms within mussel (Perna perna L.) beds in relation to topographic variability. J Exp Mar Biol Ecol 314:79–97

    Article  Google Scholar 

  • Gamfeldt L, Hillebrand H, Jonsson P (2005) Species richness changes across two trophic levels simultaneously affect prey and consumer biomass. Ecol Lett 8:696–703

    Article  Google Scholar 

  • Gray J, Naylor E (1995) Foraging and homing behaviour of the limpet Patella vulgata: a geographical comparison. J Moll Stud 62:121–124

    Article  Google Scholar 

  • Griffin J, Noël LM-LJ, Crowe TP, Burrows MT, Hawkins SJ, Thompson RC, Jenkins SR (2010) Consumer effects on ecosystem functioning in rock pools: roles of species richness and composition. Mar Ecol Prog Ser 420:45–56

    Article  Google Scholar 

  • Hawkins SJ, Hartnoll RG (1983) Grazing of intertidal algae by marine invertebrates. Oceanogr Mar Biol Annu Rev 21:195–282

    Google Scholar 

  • Hillebrand H (2003) Opposing effects of grazing and nutrients on diversity. Oikos 100:592–600

    Article  Google Scholar 

  • Hillebrand H, Worm B, Lotze HK (2000) Marine microbenthic community structure regulated by nitrogen loading and grazing pressure. Mar Ecol Prog Ser 204:27–38

    Article  CAS  Google Scholar 

  • Hochberg Y (1988) A sharper Bonferroni procedure for multiple tests of significance. Biometrika 75:800–802

    Article  Google Scholar 

  • Hutchinson N, Williams GA (2003) An assessment of variation in molluscan grazing pressure on Hong Kong rocky shores. Mar Biol 142:495–507

    Google Scholar 

  • Jaschinski S, Sommer U (2011) How do nutrient conditions and species identity influence the impact of mesograzers in eelgrass-epiphyte systems? Mar Biol 158:193–203

    Article  Google Scholar 

  • Johnson MP, Burrows MT, Hartnoll RG, Hawkins SH (1997) Spatial structure on moderately exposed rocky shores: patch scales and the interactions between limpets and algae. Mar Ecol Prog Ser 160:209–215

    Article  Google Scholar 

  • Jones KMM, Boulding EG (1999) State-dependent habitat selection by an intertidal snail: the costs of selecting a physically stressful microhabitat. J Exp Mar Biol Ecol 242:149–177

    Article  Google Scholar 

  • Karez R, Engelbert S, Kraufvelin P, Pedersen MF, Sommer U (2004) Biomass response and changes in composition of ephemeral macroalgal assemblages along an experimental gradient of nutrient enrichment. Aquat Bot 78:103–117

    Article  Google Scholar 

  • Kostylev V, Erlandsson J (2001) A fractal approach for detecting spatial hierarchy and structure on mussel beds. Mar Biol 139:497–506

    Google Scholar 

  • Kostylev V, Erlandsson J, Johannesson K (1997) Microdistribution of the polymorphic snail Littorina saxatilis (Olivi) in a patchy rocky shore habitat. Ophelia 47:1–12

    Google Scholar 

  • Kraufvelin P (1999) Baltic hard bottom mesocosms unplugged: replicability, repeatability and ecological realism examined by multivariate techniques. J Exp Mar Biol Ecol 240:229–258

    Article  Google Scholar 

  • Kraufvelin P (2007) Responses to nutrient enrichment, wave action and disturbance in rocky shore communities. Aquat Bot 87:262–274

    Article  CAS  Google Scholar 

  • Kraufvelin P, Christie H, Olsen M (2002) Littoral macrofauna (secondary) responses to experimental nutrient addition to rocky shore mesocosms and a coastal lagoon. Hydrobiologia 484:149–166

    Article  Google Scholar 

  • Kraufvelin P, Salovius S, Christie H, Moy FE, Karez R, Pedersen MF (2006a) Eutrophication-induced changes in benthic algae affect the behaviour and fitness of the marine amphipod Gammarus locusta. Aquat Bot 84:199–209

    Article  Google Scholar 

  • Kraufvelin P, Moy FE, Christie H, Bokn TL (2006b) Nutrient addition to experimental rocky shore communities revisited: delayed responses, rapid recovery. Ecosystems 9:1076–1093

    Article  CAS  Google Scholar 

  • Kraufvelin P, Lindholm A, Pedersen MF, Kirkerud LA, Bonsdorff E (2010) Biomass, diversity and production of rocky shore macroalgae at two nutrient enrichment and wave action levels. Mar Biol 157:29–47

    Article  Google Scholar 

  • Kristiansen S, Paasche E (1982) Nitrogen nutrition of the phytoplankton in the Oslofjord. Estuar Coast Shelf Sci 14:237–249

    Article  Google Scholar 

  • Little C (1989) Factors governing patterns of foraging activity in littoral marine herbivorous mollusks. J Moll Stud 55:273–284

    Article  Google Scholar 

  • Little C, Partridge J, Teagle L (1991) Foraging activity of limpets in normal and abnormal tidal regimes. J Mar Biol Assoc UK 71:537–554

    Article  Google Scholar 

  • Lubchenco J, Gaines SD (1981) A unified approach to marine plant-herbivore interactions. I. Populations and communities. Annu Rev Ecol Syst 12:405–437

    Article  Google Scholar 

  • Mackas D, Bohrer R (1976) Fluorescence analysis of zooplankton gut contents and an investigation of diel feeding patterns. J Exp Mar Biol Ecol 25:77–85

    Article  Google Scholar 

  • Madikiza LO (2005) The role of grazers and basal substrate cover in the control of intertidal algal distribution. MSc-thesis, University of Western Cape, South Africa

  • Masterson P, Arenas FA, Thompson RC, Jenkins SR (2008) Interaction of top down and bottom up factors in intertidal rockpools: effects on early successional macroalgal community composition, abundance and productivity. J Exp Mar Biol Ecol 363:12–20

    Article  Google Scholar 

  • McQuaid CD (1996) Biology of the gastropod family Littorinidae. II. Role in the ecology of intertidal and shallow marine ecosystems. Oceanogr Mar Biol Ann Rev 34:263–302

    Google Scholar 

  • Newell RC et al (1971) Factors affecting feeding rate of winkle Littorina littorea. Mar Biol 9:138–144

    Article  Google Scholar 

  • Norton TA, Hawkins SJ, Manley NL, Williams GA, Watson DC (1990) Scraping a living: a review of littorinid grazing. Hydrobiologia 193:117–138

    Article  Google Scholar 

  • Paine RT (2002) Trophic control of production in a rocky intertidal community. Science 296:736–739

    Article  CAS  Google Scholar 

  • Pakhomov EA, Froneman PW (2004) Zooplankton dynamics in the eastern Atlantic sector of the Southern Ocean during the austral summer 1997/1998—Part 2: Grazing impact. Deep-Sea Res Pt II 51:2617–2631

    Article  Google Scholar 

  • Penry DL, Jumars PA (1986) Chemical reactor analysis and optimal digestion theory. Bioscience 36:310–315

    Article  CAS  Google Scholar 

  • Perez KA (1995) Role and significance of scale to ecotoxicology. In: Cairns J, Niederlehner BR (eds) Ecological toxicity testing: scale, complexity and relevance. Lewis Publishers, CRC Press, Boca Raton, pp 49–72

  • Perez KO, Carlson RL, Shulman MJ, Ellis JC (2009) Why are intertidal snails rare in the subtidal? Predation, growth and the vertical distribution of Littorina littorea (L.) in the Gulf of Maine. J Exp Mar Biol Ecol 369:79–86

    Article  Google Scholar 

  • Perissinotto R (1992) Mesozooplankton size-selectivity and grazing impact on phytoplankton community of the prince Edward Archipelago (Southern Ocean). Mar Ecol Prog Ser 79:243–258

    Article  Google Scholar 

  • Raffaelli DG, Hughes RN (1978) The effects of crevice size and availability on the population structure of Littorina rudis Maton. J Anim Ecol 47:71–83

    Article  Google Scholar 

  • Russell BD, Connell SD (2007) Responses of grazers to sudden nutrient pulses in oligotrophic versus eutrophic conditions. Mar Ecol Prog Ser 349:73–80

    Article  Google Scholar 

  • Scheiner SM, Gurevitch J (1993) Design and analysis of ecological experiments. Chapman and Hall, New York

    Google Scholar 

  • Schmid PE (2000) Fractal properties of habitat and patch structure in benthic ecosystems. Adv Ecol Res 30:339–401

    Article  Google Scholar 

  • Skov MW, Volkelt-Igoe M, Hawkins SJ, Jesus B, Thompson RC, Doncaster CP (2010) Past and present grazing boosts the photo-autotrophic biomass of biofilms. Mar Ecol Prog Ser 401:101–111

    Article  CAS  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry, the principles and practice of statistics in biological research, 3rd edn. WH Freeman and Company, New York, 887 pp

  • Taghon GL (1981) Beyond selection: optimal ingestion rate as a function of food value. Am Nat 118:202–214

    Article  Google Scholar 

  • Thompson RC, Crowe TP, Hawkins SJ (2002) Rocky intertidal communities, past environmental changes, present status and predictions for the next 25 years. Environ Conserv 29:168–191

    Article  Google Scholar 

  • Underwood AJ (1980) The effect of grazing by gastropods and physical factors on the upper limits of distribution of intertidal macroalgae. Oecologia 46:201–213

    Article  Google Scholar 

  • Underwood AJ, Chapman MG (1996) Scales of spatial patterns of distribution of intertidal invertebrates. Oecologia 107:212–224

    Article  Google Scholar 

  • Underwood AJ, Jernakoff P (1984) The effects of tidal height, wave exposure, seasonality and rock-pools on grazing and the distribution of intertidal macroalgae in the South Wales. J Exp Mar Biol Ecol 75:71–96

    Article  Google Scholar 

  • Valdivia N, Thiel M (2006) Effects of point-source nutrient addition and mussel removal on epibiotic assemblages in Perumytilus purpuratus beds. J Sea Res 56:271–283

    Article  Google Scholar 

  • Wahl M, Sönnichsen H (1992) Marine epibiosis. IV. The periwinkle Littorina littorea lacks typical antifouling defences–why are some populations so little fouled? Mar Ecol Prog Ser 88:225–235

    Article  Google Scholar 

  • Wahl M, Link H, Alexandridis N, Thomason J, Cifuentes M, Costello MJ, da Gama BAP, Hillock K, Hobday AJ, Kaufmann MJ, Keller S, Kraufvelin P, Krüger I, Lauterbach L, Antunes BL, Molis M, Nakaoka M, Nyström J, bin Radzi Z, Stockhausen B, Thiel M, Vance T, Weseloh A, Whittle M, Wiesmann L, Wunderer L, Yamakita T, Lenz M (2011) Re-structuring of marine communities exposed to environmental change: a global study on the interactive effects of species and functional richness. PLOS One 6(5):e19514

    Article  CAS  Google Scholar 

  • Wilhelmsen U, Reise K (1994) Grazing on green algae by the periwinkle Littorina littorea in the Wadden Sea. Helgolander Meeresun 48:233–242

    Article  Google Scholar 

  • Worm B, Lotze HK (2006) Effects of eutrophication, grazing, and algal blooms on rocky shores. Limnol Oceanogr 51:569–579

    Article  Google Scholar 

  • Worm B, Lotze HK, Hillebrand H, Sommer U (2002) Consumer versus resource control of species diversity and ecosystem functioning. Nature 417:848–851

    Article  CAS  Google Scholar 

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Acknowledgments

ED and JE were funded by Formas (The Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning), whereas PK was funded by Svenska Kulturfonden. We are grateful to Hartvig Christie and Sofie Knutar for field assistance, to Per-Ivar Johannessen and Oddbjørn Pettersen for excellent daily maintenance of the Solbergstrand mesocosms, and to William Froneman and Kim Bernard for insights about the use of GFT. Hartvig Christie’s and Frithjof Moy’s scientific project SACCHARINA (from the Research Council of Norway 2007–2010) covered the costs for operative mesocosms during 2008 and their kind approval of our simultaneous research activities in the systems is highly appreciated. The Solbergstrand mesocosms can be viewed live at the web-cam link: http://151.157.160.150/view/index.shtml (username and password = guest).

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  1. Johan Erlandsson

    Present address: Vattenmyndigheten, Västerhavets Vattendistrikt, Vattenvårdsenheten, Länstyrelsen i Västra Götalands län, 403 40, Göteborg, Sweden

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  1. ARONIA Coastal Zone Research Team, Ǻbo Akademi University and Novia University of Applied Sciences, Raseborgsvägen 9, 10600, Ekenäs, Finland

    Eliecer Rodrigo Díaz, Patrik Kraufvelin & Johan Erlandsson

  2. Environmental and Marine Biology, Åbo Akademi University, Artillerigatan 6, 20520, Turku/Åbo, Finland

    Patrik Kraufvelin

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  1. Eliecer Rodrigo Díaz
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Correspondence to Patrik Kraufvelin.

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Communicated by F. Bulleri.

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Díaz, E.R., Kraufvelin, P. & Erlandsson, J. Combining gut fluorescence technique and spatial analysis to determine Littorina littorea grazing dynamics in nutrient-enriched and nutrient-unenriched littoral mesocosms. Mar Biol 159, 837–852 (2012). https://doi.org/10.1007/s00227-011-1860-y

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