Impact of herbivory and competition on lake ecosystem structure: underwater experimental manipulation
Language English Country England, Great Britain Media electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
PubMed
30108255
PubMed Central
PMC6092342
DOI
10.1038/s41598-018-30598-0
PII: 10.1038/s41598-018-30598-0
Knihovny.cz E-resources
- MeSH
- Biodiversity * MeSH
- Herbivory physiology MeSH
- Chara physiology MeSH
- Plant Dispersal * MeSH
- Lakes MeSH
- Potamogetonaceae physiology MeSH
- Environmental Restoration and Remediation MeSH
- Fishes physiology MeSH
- Astacoidea physiology MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
Two basic ecological relationships, herbivory and competition, distinctively influence terrestrial ecosystem characteristics, such as plant cover, species richness and species composition. We conducted a cage experiment under natural conditions in an aquatic ecosystem to test the impacts of two treatments combined in a factorial manner: (i) a pulse treatment - removal of dominant competitors among primary producers (macroalgae Chara sp. and Vaucheria sp.), and (ii) a press treatment - preventing herbivore (fish, crayfish) access to caged plots. The plots were sampled once before the treatments were established and four more times within two years. Both treatments had a significantly positive impact on macrophyte cover and species richness and changed the macrophyte species composition. The effect of the macroalgae removal was immediate with the highest species richness occurrence during the first post-treatment monitoring, but the positive effect vanished with time. In contrast, preventing herbivore access had a gradual but long-lasting effect and reached a more steady-state over time. Two of the most common species showed contrasting responses, the palatable Potamogeton pectinatus was most supported by caging, while the distasteful Myriophyllum spicatum preferred open plots. Our findings may be applicable during the revitalisation of aquatic ecosystems that aims to increase macrophyte biodiversity.
See more in PubMed
Herms DA, Mattson WJ. The dilemma of plants: to grow or defend. Q. Rev. Biol. 1992;67:283–335. doi: 10.1086/417659. DOI
Rooney TP. Deer impacts on forest ecosystems: a North American perspective. Forestry. 2001;7:201–208. doi: 10.1093/forestry/74.3.201. DOI
Bond WJ. What Limits Trees in C-4 Grasslands and Savannas? Annu. Rev. Ecol. Evol. Syst. 2008;39:641–659. doi: 10.1146/annurev.ecolsys.39.110707.173411. DOI
Berenbaum, M. R. Herbivores: their interactions with secondary plant metabolites, the chemical participants. Physiol. Entomol. 17, 308 pp (1992).
Adler PB, Raff DA, Lauenroth WK. The effect of grazing on the spatial heterogeneity of vegetation. Oecologia. 2001;128:465–479. doi: 10.1007/s004420100737. PubMed DOI
Barko JW, Smart RM. Sediment-related mechanisms of growth limitation in submerged macrophytes. Ecology. 1986;67:1328–1340. doi: 10.2307/1938689. DOI
Duarte CM, Kalff J. Littoral slope as a predictor of the maximum biomass soft submerged macrophyte communities. Limnol. Oceanogr. 1986;31:1072–1080. doi: 10.4319/lo.1986.31.5.1072. DOI
Squires MM, Lesack LFW, Huebert D. The influence of water transparency on the distribution and abundance of macrophytes among lakes of the Mackenzie Delta, Western CanadianArctic. Freshw. Biol. 2002;47:2123–2135. doi: 10.1046/j.1365-2427.2002.00959.x. DOI
Szoszkiewicz K, et al. Parameters structuring macrophyte communities in rivers and lakes – results from a case study in North-Central Poland. Knowl. Manag. Aquat. Ec. 2014;415:08. doi: 10.1051/kmae/2014034. DOI
Jeppesen, E., Søndergaard, M., Søndergaard, M. & Christoffersen, K. The structuring role of submerged macrophytes in lakes. 423pp (Springer, 1992).
Vergés A, Becerro MA, Alcoverro T, Romero J. Experimental evidence of chemical detergence against multiple herbivores in the seagrass Posidonia oceanica. Mar. Ecol. Prog. Ser. 2007;343:107–114. doi: 10.3354/meps06885. DOI
Vergés A, Alcoverro T, Ballesteros E. Role of fish herbivory in structuring the vertical distribution of canopy algae Cystoseira spp. in the Mediterranean Sea. Mar. Ecol. Prog. Ser. 2009;375:1–11. doi: 10.3354/meps07778. DOI
Taylor DI, Schiel DR. Algal populations controlled by fish herbivory across a wave exposure gradient on southern temperate shores. Ecology. 2010;91:201–211. doi: 10.1890/08-1512.1. PubMed DOI
Vergés A, et al. Tropical rabbitfish and the deforestation of a warming temperate sea. J. Ecol. 2014;102:1518–1527. doi: 10.1111/1365-2745.12324. DOI
Bennett S, Wernberg T, Harvey ES, Santana-Garcon J, Saunders BJ. Tropical herbivores provide resilience to a climate-mediated phase shift on temperate reefs. Ecol. Lett. 2015;18:714–723. doi: 10.1111/ele.12450. PubMed DOI
Vergés A, et al. Long-term empirical evidence of ocean warming leading to tropicalization of fish communities, increased herbivory, and loss of kelp. Proc. Natl. Acad. Sci. USA. 2016;113:13791–13796. doi: 10.1073/pnas.1610725113. PubMed DOI PMC
Vejříková I, et al. Distribution of herbivorous fish is frozen by low temperature. Sci. Rep. 2016;6:39600. doi: 10.1038/srep39600. PubMed DOI PMC
Lake MD, Hicks BJ, Wells R, Dugdale TM. Consumption of submerged aquatic macrophytes by rudd (Scardinius erythrophthalmus L.) in New Zealand. Hydrobiologia. 2002;470:13–22. doi: 10.1023/A:1015689432289. DOI
Miller SA, Crowl TA. Effects of Common Carp (Cyprinus carpio) on macrophytes and invertebrate communities in a shallow lake. Freshw. Biol. 2006;51:85–94. doi: 10.1111/j.1365-2427.2005.01477.x. DOI
Kapuscinski KL, et al. Selective herbivory by an invasive cyprinid, the rudd Scardinius erythrophthalmus. Freshw. Biol. 2014;59:2315–2327. doi: 10.1111/fwb.12433. DOI
Guinan ME, Jr., Kapuscinski KL, Teece MA. Seasonal diet shifts and trophic position of an invasive cyprinid, the rudd Scardinius erythrophthalmus (Linnaeus, 1758), in the upper Niagara River. Aquat. Invasions. 2015;10:217–225. doi: 10.3391/ai.2015.10.2.10. DOI
Matsuzaki SS, Usio N, Takamura N, Washitani I. Contrasting impacts of invasive engineers on freshwater ecosystems: an experiment and meta-analysis. Oecologia. 2009;158:673–686. doi: 10.1007/s00442-008-1180-1. PubMed DOI
Dorenbosch M, Bakker ES. Herbivory in omnivorous fishes: effect of plant secondary metabolites and prey stoichiometry. Freshw. Biol. 2011;56:1783–1797. doi: 10.1111/j.1365-2427.2011.02618.x. DOI
Gross EM, Meyer H, Schilling G. Release and ecological impact of algicidal hydrolysable polyphenols in Myriophyllum spicatum. Phytochemistry. 1996;41:133–138. doi: 10.1016/0031-9422(95)00598-6. DOI
Choi C, Bareiss C, Walenciak O, Gross EM. Impact of polyphenols on growth of the aquatic herbivore Acentria ephemerella. J. Chem. Ecol. 2002;28:2245–2256. doi: 10.1023/A:1021049332410. PubMed DOI
Marko PD, Gross EM, Newman RM, Gleason FK. Chemical profile of the North American native Myriophyllum sibiricum compared to the invasive M. spicatum. Aquat. Bot. 2008;88:57–65. doi: 10.1016/j.aquabot.2007.08.007. DOI
Sotka EE, et al. The emerging role of pharmacology in understanding consumer-prey interactions in marine and freshwater systems. Integr. Comp. Biol. 2009;49:291–313. doi: 10.1093/icb/icp049. PubMed DOI
Fink P. Ecological functions of volatile organic compounds in aquatic systems. Mar. Freshw. Behav. Phy. 2007;40:155–168. doi: 10.1080/10236240701602218. DOI
Novotny V, et al. Insects on Plants: Explaining the Paradox of Low Diversity within Specialist Herbivore Guilds. Am. Nat. 2012;179:351–362. doi: 10.1086/664082. PubMed DOI
Parkyn SM, Collier KJ, Hicks BJ. New Zealand stream crayfish: functional omnivores but trophic predators? Freshw. Biol. 2001;46:641–652. doi: 10.1046/j.1365-2427.2001.00702.x. DOI
González-Bergonzoni I, et al. Meta-analysis shows a consistent and strong latitudinal pattern in fish omnivory across ecosystems. Ecosystems. 2012;15:492–503. doi: 10.1007/s10021-012-9524-4. DOI
Nurminen L, Horppila J, Lappalainen J, Malinen T. Implications of rudd (Scardinius erythrophthalmus) herbivory on submerged macrophytes in a shallow eutrophic lake. Hydrobiologia. 2003;506–509:511–518. doi: 10.1023/B:HYDR.0000008577.16934.a9. DOI
Dorenbosch M, Bakker ES. Effects of contrasting omnivorous fish on submerged macrophyte biomass in temperate lakes: a mesocosm experiment. Freshw. Biol. 2012;57:1360–1372. doi: 10.1111/j.1365-2427.2012.02790.x. DOI
Glenn-Lewin, D. C. & van der Maarel, E. Pattern and process of vegetation dynamics. In: Plant succession, theory and prediction. (eds Glenn-Lewin, D. C., Peet, R. K., Veblen, T. T.) 11–59 (Chapman & Hall, 1992).
Johnson, E. & Miyanishi, K. Plant disturbance ecology. The process and the response. 673pp (Elsevier, 2007).
Wilson JB. The twelve theories of co-existence in plant communities: the doubtful, the important and the unexplored. J. Veg. Sci. 2011;22:184–195. doi: 10.1111/j.1654-1103.2010.01226.x. DOI
Connell JH, Slatyer RO. Mechanisms of succession in natural communities and their role in community stability and organization. Am. Nat. 1977;111:1119–1144. doi: 10.1086/283241. DOI
Tilman D. Constraints and tradeoffs: toward a predictive theory of competition and succession. Oikos. 1990;58:3–15. doi: 10.2307/3565355. DOI
Levins R, Culver D. Regional co-existence of species and competition between rare species. Proc. Natl. Acad. Sci. USA. 1971;68:1246–1248. doi: 10.1073/pnas.68.6.1246. PubMed DOI PMC
Roxburgh SH, Shea K, Wilson JB. The intermediate disturbance hypothesis: patch dynamics and mechanisms of species coexistence. Ecology. 2004;85:359–371. doi: 10.1890/03-0266. DOI
Cadotte MW. Competition–colonization trade offs and disturbance effects at multiple scales. Ecology. 2007;88:823–829. doi: 10.1890/06-1117. PubMed DOI
Arthaud F, Vallod D, Robin J, Wezel A, Bornette G. Short-term succession of aquatic plant species richness along ecosystem productivity and dispersal gradients in shallow lakes. J. Veg. Sci. 2013;24:148–156. doi: 10.1111/j.1654-1103.2012.01436.x. DOI
Bornette G, Amoros C, Lamouroux N. Aquatic plant diversity in riverine wetlands: the role of connectivity. Freshw. Biol. 1998;39:267–283. doi: 10.1046/j.1365-2427.1998.00273.x. DOI
Chambers PA, Prepas EE. Competition and coexistence in submerged aquatic plant communities: the effect of species interactions versus abiotic factors. Freshw. Biol. 1990;23:541–550. doi: 10.1111/j.1365-2427.1990.tb00293.x. DOI
van Donk E, Otte A. Effects of grazing by fish and waterfowl on the biomass and species composition of submerged macrophytes. Hydrobiologia. 1996;340:285–290. doi: 10.1007/BF00012769. DOI
Kapuscinski KL, Farrell JM, Wilkinson MA. Feeding patterns and population structure of an invasive cyprinid, the rudd Scardinius erythrophthalmus (Cypriniformes, Cyprinidae), in Buffalo Harbor (Lake Erie) and the upper Niagara River. Hydrobiologia. 2012;693:169–181. doi: 10.1007/s10750-012-1106-0. DOI
Bender EA, Case TJ, Gilpin ME. Perturbation experiments in community ecology: theory and practice. Ecology. 1984;65:1–13. doi: 10.2307/1939452. DOI
Schmitz OJ. Press perturbations and the predictability of Ecological interactions in a food web. Ecology. 1997;78:55–69.
Cottenie K, Michels E, Nuytten N, DeMeester L. Zooplankton metacommunity structure: regional vs. local processes in highly interconnected ponds. Ecology. 2003;84:991–1000. doi: 10.1890/0012-9658(2003)084[0991:ZMSRVL]2.0.CO;2. DOI
Cook WM, Yao J, Foster BL, Holt RD, Patrick B. Secondary succession in an experimentally fragmented landscape: community patterns across space and time. Ecology. 2005;86:1267–1279. doi: 10.1890/04-0320. DOI
Josefsson, M. Invasive Species Fact Sheet – Elodea canadensis, Elodea nuttallii and Elodea callitrichoides– From: Online Database of the European Network on Invasive Alien Species. Preprint at www.nobanis.org (2011).
Krahulec F, Lepš J, Rauch O. Vegetation succession on new lowland reservoir. Arch. Hydrobiol.–Beih. Ergebn. Limnol. 1987;27:83–93.
Figuerola J, Green AJ. Dispersal of aquatic organisms by waterbirds: a review of past research and priorities for future studies. Freshw. Biol. 2002;47:483–494. doi: 10.1046/j.1365-2427.2002.00829.x. DOI
Soons MB, Van Der Vlugt C, Van Lith B, Heil GW, Klaassen M. Small seed size increases the potential for dispersal of wetland plants by ducks. J. Ecol. 2008;96:619–627. doi: 10.1111/j.1365-2745.2008.01372.x. DOI
Brochet AL, Guillemain M, Fritz H, Gauthier-Clerc M, Green AJ. Plant dispersal by teal (Anas crecca) in the Camargue: duck guts are more important than their feet. Freshw. Biol. 2010;55:1262–1273. doi: 10.1111/j.1365-2427.2009.02350.x. DOI
Bakker ES, et al. Herbivory on freshwater and marine macrophytes: A review and perspective. Aquat. Bot. 2016;135:18–36. doi: 10.1016/j.aquabot.2016.04.008. DOI
Wood KA, et al. Herbivore regulation of plant abundance in aquatic ecosystems. Biol. Rev. 2016;92:1128–1141. doi: 10.1111/brv.12272. PubMed DOI
Vejříková I, et al. Macrophytes shape trophic niche variation among generalist fishes. Plos One. 2017;12:e0177114. doi: 10.1371/journal.pone.0177114. PubMed DOI PMC
Holm TE, Laursen K, Clausen P. The feeding ecology and distribution of common coots Fulica atra are affected by hunting taking place in adjacent areas. Bird Study. 2011;58:321–329. doi: 10.1080/00063657.2011.575927. DOI
Bakker ES, Pagès JF, Arthur R, Alcoverro T. Assessing the role of large herbivores in the structuring and functioning of freshwater and marine angiosperm ecosystems. Ecography. 2016;39:162–179. doi: 10.1111/ecog.01651. DOI
Kouba A, et al. The significance of droughts for hyporheic dwellers: evidence from freshwater crayfish. Sci. Rep. 2016;6:26569. doi: 10.1038/srep26569. PubMed DOI PMC
Collins B, Wein G, Philippi T. Effects of disturbance intensity and frequency on early old-field succession. J. Veg. Sci. 2001;12:721–728. doi: 10.2307/3236913. DOI
Lepš J. Nutrient status, disturbance and competition: an experimental test of relationships in a wet meadow. J. Veg. Sci. 1999;10:219–230. doi: 10.2307/3237143. DOI
Short FT, Wyllie-Echeverria S. Natural and human-induced disturbance of seagrasses. Environ. Conserv. 1996;23:17–27. doi: 10.1017/S0376892900038212. DOI
Brooks JL, Dodson SI. Predation, body size, and composition of plankton. Science. 1965;150:28–35. doi: 10.1126/science.150.3692.28. PubMed DOI
Hillebrand H. Meta-analysis of grazer control of periphyton biomass across aquatic ecosystems. J. Phycol. 2009;45:798–806. doi: 10.1111/j.1529-8817.2009.00702.x. PubMed DOI
Van den Brink PJ, Ter Braak CJF. Principal response curves: Analysis of time-dependent multivariate responses of biological community to stress. Environ. Toxicol. Chem. 1999;18:138–148. doi: 10.1002/etc.5620180207. DOI
Šmilauer, P. & Lepš, J. Multivariate Analysis of Ecological Data Using CANOCO 5. (Cambridge University Press, 2014).
Esri, Working with ArcMap. ArcGIS Help 10.2.2. (2016). Available at: http://resources.arcgis.com/en/help/main/10.2/#/Mapping_and_visualization_in_ArcGIS_for_Desktop/018q00000004000000/ (accessed 16th April 2018).