The Influence of Stickleback on the Accumulation of Primary Production: a Comparison of Field and Experimental Data

Estuaries and Coasts

Volumn 39, Issue 1, 2016, Pages 248-257

  Candolin, Ulrika ^a   Johanson, Anna ^a   Budria, Alexandre ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Algal mats; Eutrophication; Filamentous algae; Grazers; Mesopredator release; Trophic cascades

Indexed keywords

ACCUMULATION; ALGAL MAT; EUTROPHICATION; FIELD METHOD; FILAMENTOUS ALGA; MESOCOSM; PRIMARY PRODUCTION; TELEOST;

ATLANTIC OCEAN; BALTIC SEA;

ALGAE; AMPHIPODA; GASTEROSTEUS;

EID: 84952988503     PISSN: 15592723     EISSN: 15592731     Source Type: Journal    
DOI: 10.1007/s12237-015-9984-9     Document Type: Article

References (64)

1. Arroyo, N.L., K. Aarnio, M. Maensivu, and E. Bonsdorff. 2012. Drifting filamentous algal mats disturb sediment fauna: Impacts on macro-meiofaunal interactions. Journal of Experimental Marine Biology and Ecology 420: 77–90.
2. Berglund, J., J. Mattila, O. Ronnberg, J. Heikkila, and E. Bonsdorff. 2003. Seasonal and inter-annual variation in occurrence and biomass of rooted macrophytes and drift algae in shallow bays. Estuarine, Coastal and Shelf Science 56: 1167–1175.
3. Bonsdorff, E., E.M. Blomqvist, J. Mattila, and A. Norkko. 1997. Coastal eutrophication: Causes, consequences and perspectives in the Archipelago areas of the northern Baltic Sea. Estuarine, Coastal and Shelf Science 44: 63–72.
4. Bruno, J.F., and M.I. O’Connor. 2005. Cascading effects of predator diversity and omnivory in a marine food web. Ecology Letters 8: 1048–1056.
5. Candolin, U. 2000. Changes in expression and honesty of sexual signalling over the reproductive lifetime of sticklebacks. Proceedings of the Royal Society B: Biological Sciences 267: 2425–2430.
6. Candolin, U. 2004. Effects of algae cover on egg acquisition in male three-spined stickleback. Behaviour 141: 1389–1399.
7. Candolin, U., and H.R. Voigt. 2003a. Do changes in risk-taking affect habitat shifts of sticklebacks? Behavioral Ecology and Sociobiology 55: 42–49.
8. Candolin, U., and H.R. Voigt. 2003b. Size-dependent selection on arrival times in sticklebacks: Why small males arrive first. Evolution 57: 862–871.
9. Candolin, U., J. Engström-Öst, and T. Salesto. 2008. Human-induced eutrophication enhances reproductive success through effects on parenting ability in sticklebacks. Oikos 117: 459–465.
10. Candolin, U., A. Nieminen, and J. Nyman. 2014. Indirect effects of human-induced environmental change on offspring production mediated by behavioural responses. Oecologia 174: 87–97.
11. Carpenter, S.R., J.J. Cole, J.R. Hodgson, J.F. Kitchell, M.L. Pace, D. Bade, K.L. Cottingham, T.E. Essington, J.N. Houser, and D.E. Schindler. 2001. Trophic cascades, nutrients, and lake productivity: Whole-lake experiments. Ecological Monographs 71: 163–186.
12. Casini, M., J. Lovgren, J. Hjelm, M. Cardinale, J.C. Molinero, and G. Kornilovs. 2008. Multi-level trophic cascades in a heavily exploited open marine ecosystem. Proceedings of the Royal Society B: Biological Sciences 275: 1793–1801.
13. Cloern, J.E. 2001. Our evolving conceptual model of the coastal eutrophication problem. Marine Ecology Progress Series 210: 223–253.
14. Cloern, J.E., S.Q. Foster, and A.E. Kleckner. 2014. Phytoplankton primary production in the world’s estuarine-coastal ecosystems. Biogeosciences 11: 2477–2501.
15. Dalton, C.M., A. Mokiao-Lee, T.S. Sakihara, M.G. Weber, C.A. Roco, Z. Han, B. Dudley, R.A. MacKenzie, and N.G. Hairston. 2013. Density- and trait-mediated top-down effects modify bottom-up control of a highly endemic tropical aquatic food web. Oikos 122: 790–800.
16. Des Roches, S., J.B. Shurin, D. Schluter, and L.J. Harmon. 2013. Ecological and evolutionary effects of stickleback on community structure. PLoS One 8: e59644.
17. Desouhant, E., G. Driessen, I. Amat, and C. Bernstein. 2005. Host and food searching in a parasitic wasp Venturia canescens: A trade-off between current and future reproduction? Animal Behaviour 70: 145–152.
18. Dodds, W.K. 1991. Community interactions between the filamentous alga Cladophora glomerata (L) Keutzing, its epiphytes, and epiphyte grazers. Oecologia 85: 572–580.
19. Dudley, T.L. 1992. Beneficial effects of herbivores on stream macroalgae via epiphyte removal. Oikos 65: 121–127.
20. Eklof, J.S., C. Alsterberg, J.N. Havenhand, K. Sundback, H.L. Wood, and L. Gamfeldt. 2012. Experimental climate change weakens the insurance effect of biodiversity. Ecology Letters 15: 864–872.
21. Eriksson, B.K., L. Ljunggren, A. Sandstrom, G. Johansson, J. Mattila, A. Rubach, S. Raberg, and M. Snickars. 2009. Declines in predatory fish promote bloom-forming macroalgae. Ecological Applications 19: 1975–1988.
22. Eriksson, B.K., C. van Sluis, K. Sieben, L. Kautsky, and S. Raberg. 2011. Omnivory and grazer functional composition moderate cascading trophic effects in experimental Fucus vesiculosus habitats. Marine Biology 158: 747–756.
23. Estes, J.A., and D.O. Duggins. 1995. Sea otters and kelp forests in Alaska—generality and variation in a community ecological paradigm. Ecological Monographs 65: 75–100.
24. Estes, J.A., J. Terborgh, J.S. Brashares, M.E. Power, J. Berger, W.J. Bond, S.R. Carpenter, T.E. Essington, R.D. Holt, J.B.C. Jackson, R.J. Marquis, L. Oksanen, T. Oksanen, R.T. Paine, E.K. Pikitch, W.J. Ripple, S.A. Sandin, M. Scheffer, T.W. Schoener, J.B. Shurin, A.R.E. Sinclair, M.E. Soule, R. Virtanen, and D.A. Wardle. 2011. Trophic downgrading of planet earth. Science 333: 301–306.
25. Fox, S.E., M. Teichberg, I. Valiela, and L. Heffner. 2012. The relative role of nutrients, grazing, and predation as controls on macroalgal growth in the Waquoit Bay estuarine system. Estuaries and Coasts 35: 1193–1204.
26. Heithaus, M.R., A. Frid, A.J. Wirsing, and B. Worm. 2008. Predicting ecological consequences of marine top predator declines. Trends in Ecology & Evolution 23: 202–210.
27. Hillebrand, H., and M. Kahlert. 2001. Effect of grazing and nutrient supply on periphyton biomass and nutrient stoichiometry in habitats of different productivity. Limnology and Oceanography 46: 1881–1898.
28. Hixon, M.A., S.W. Pacala, and S.A. Sandin. 2002. Population regulation: Historical context and contemporary challenges of open vs. closed systems. Ecology 83: 1490–1508.
29. Jakobsen, T.S., P.B. Hansen, E. Jeppesen, P. Gronkjaer, and M. Sondergaard. 2003. Impact of three-spined stickleback Gasterosteus aculeatus on zooplankton and chl a in shallow, eutrophic, brackish lakes. Marine Ecology Progress Series 262: 277–284.
30. Kohler, J., J. Hachol, and S. Hilt. 2010. Regulation of submersed macrophyte biomass in a temperate lowland river: Interactions between shading by bank vegetation, epiphyton and water turbidity. Aquatic Botany 92: 129–136.
31. Korpinen, S., T. Honkanen, O. Vesakoski, A. Hemmi, R. Koivikko, J. Loponen, and V. Jormalainen. 2007. Macroalgal communities face the challenge of changing biotic interactions: Review with focus on the Baltic Sea. Ambio 36: 203–211.
32. Korpinen, S., V. Jormalainen, and E. Pettay. 2010. Nutrient availability modifies species abundance and community structure of Fucus-associated littoral benthic fauna. Marine Environmental Research 70: 283–292.
33. Kraufvelin, P., A. Lindholm, M.F. Pedersen, L.A. Kirkerud, and E. Bonsdorff. 2010. Biomass, diversity and production of rocky shore macroalgae at two nutrient enrichment and wave action levels. Marine Biology 157: 29–47.
34. Lande, R. 2009. Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. Journal of Evolutionary Biology 22: 1435–1446.
35. Ljunggren, L., A. Sandstrom, U. Bergstrom, J. Mattila, A. Lappalainen, G. Johansson, G. Sundblad, M. Casini, O. Kaljuste, and B.K. Eriksson. 2010. Recruitment failure of coastal predatory fish in the Baltic Sea coincident with an offshore ecosystem regime shift. Ices Journal of Marine Science 67: 1587–1595.
36. Magnhagen, C. 1991. Predation risk as a cost of reproduction. Trends in Ecology & Evolution 6: 183–186.
37. Marczak, L.B., R.M. Thompson, and J.S. Richardson. 2007. Meta-analysis: Trophic level, habitat, and productivity shape the food web effects of resource subsidies. Ecology 88: 140–148.
38. Michel, M.J., L.M. Chevin, and J.H. Knouft. 2014. Evolution of phenotype—environment associations by genetic responses to selection and phenotypic plasticity in a temporally autocorrelated environment. Evolution 68: 1374–1384.
39. Murdoch, W.W. 1994. Population regulation in theory and practice. Ecology 75: 271–287.
40. Neutel, A.M., J.A.P. Heesterbeek, and P.C. de Ruiter. 2002. Stability in real food webs: Weak links in long loops. Science 296: 1120–1123.
41. Norkko, A., and E. Bonsdorff. 1996. Population responses of coastal zoobenthos to stress induced by drifting algal mats. Marine Ecology Progress Series 140: 141–151.
42. Olsson, J., L. Bergstrom, and A. Gardmark. 2013. Top-down regulation, climate and multi-decadal changes in coastal zoobenthos communities in two Baltic Sea areas. PLoS One 8.
43. Osterblom, H., S. Hansson, U. Larsson, O. Hjerne, F. Wulff, R. Elmgren, and C. Folke. 2007. Human-induced trophic cascades and ecological regime shifts in the Baltic Sea. Ecosystems 10: 877–889.
44. Pace, M.L., J.J. Cole, S.R. Carpenter, and J.F. Kitchell. 1999. Trophic cascades revealed in diverse ecosystems. Trends in Ecology & Evolution 14: 483–488.
45. Power, M., R. Lowe, P. Furey, J. Welter, M. Limm, J. Finlay, C. Bode, S. Chang, M. Goodrich, and J. Sculley. 2009. Algal mats and insect emergence in rivers under Mediterranean climates: Towards photogrammetric surveillance. Freshwater Biology 54: 2101–2115.
46. Reed, T.E., R.S. Waples, D.E. Schindler, J.J. Hard, and M.T. Kinnison. 2010. Phenotypic plasticity and population viability: The importance of environmental predictability. Proceedings of the Royal Society B: Biological Sciences 277: 3391–3400.
47. Relyea, R.A. 2003. Predators come and predators go: The reversibility of predator-induced traits. Ecology 84: 1840–1848.
48. Relyea, R.A., and E.E. Werner. 1999. Quantifying the relation between predator-induced behavior and growth performance in larval anurans. Ecology 80: 2117–2124.
49. Reynolds, P.L., and J.F. Bruno. 2013. Multiple predator species alter prey behavior, population growth, and a trophic cascade in a model estuarine food web. Ecological Monographs 83: 119–132.
50. Rochet, M.J., V.M. Trenkel, A. Carpentier, F. Coppin, L.G. de Sola, J.P. Leaute, J.C. Mahe, P. Maiorano, A. Mannini, M. Murenu, G. Piet, C.Y. Politou, B. Reale, M.T. Spedicato, G. Tserpes, and J.A. Bertrand. 2010. Do changes in environmental and fishing pressures impact marine communities? An empirical assessment. Journal of Applied Ecology 47: 741–750.
51. Rooney, N., K. McCann, G. Gellner, and J.C. Moore. 2006. Structural asymmetry and the stability of diverse food webs. Nature 442: 265–269.
52. Rosemond, A.D., P.J. Mulholland, and J.W. Elwood. 1993. Top-down and bottom-up control of stream periphyton—Effects of nutrients and herbivores. Ecology 74: 1264–1280.
53. Salovius, S., and P. Kraufvelin. 2004. The filamentous green algae Cladophora glomerata as a habitat for littoral macro-fauna in the northern Baltic Sea. Ophelia 58: 65–78.
54. Sanden, P., and B. Hakansson. 1996. Long-term trends in Secchi depth in the Baltic Sea. Limnology and Oceanography 41: 346–351.
55. Scharf, I., F. Peter, and O.Y. Martin. 2013. Reproductive trade-offs and direct costs for males in arthropods. Evolutionary Biology 40: 169–184.
56. Scheinin, M., S.B. Scyphers, L. Kauppi, K.L. Heck, and J. Mattila. 2012. The relationship between vegetation density and its protective value depends on the densities and traits of prey and predators. Oikos 121: 1093–1102.
57. Schmitz, O.J., A.P. Beckerman, and K.M. Obrien. 1997. Behaviorally mediated trophic cascades: Effects of predation risk on food web interactions. Ecology 78: 1388–1399.
58. Sieben, K., A.D. Rippen, and B.K. Eriksson. 2011. Cascading effects from predator removal depend on resource availability in a benthic food web. Marine Biology 158: 391–400.
59. Smith, V.H. 2003. Eutrophication of freshwater and coastal marine ecosystems—A global problem. Environmental Science and Pollution Research 10: 126–139.
60. Svensson, C.J., S. Baden, P.O. Moksnes, and P. Aberg. 2012. Temporal mismatches in predator-herbivore abundance control algal blooms in nutrient-enriched seagrass ecosystems. Marine Ecology Progress Series 471: 61–71.
61. Valiela, I., J. McClelland, J. Hauxwell, P.J. Behr, D. Hersh, and K. Foreman. 1997. Macroalgal blooms in shallow estuaries: Controls and ecophysiological and ecosystem consequences. Limnology and Oceanography 42: 1105–1118.
62. Wootton, R.J. 1976. The biology of the sticklebacks. London: Academic Press.
63. Worm, B., H.K. Lotze, H. Hillebrand, and U. Sommer. 2002. Consumer versus resource control of species diversity and ecosystem functioning. Nature 417: 848–851.
64. Zulkifly, S.B., J.M. Graham, E.B. Young, R.J. Mayer, M.J. Piotrowski, I. Smith, and L.E. Graham. 2013. The genus Cladophora Kutzing (Ulvophyceae) as a globally distributed ecological engineer. Journal of Phycology 49: 1–17.