Abstract
Anthropogenic nutrient enrichment stimulates primary production and threatens natural communities worldwide. Herbivores may counteract deleterious effects of enrichment by increasing their consumption of primary producers. However, field tests of herbivore control are often done by adding nutrients at small (e.g., sub-meter) scales, while enrichment in real systems often occurs at much larger scales (e.g., kilometers). Therefore, experimental results may be driven by processes that are not relevant at larger scales. Using a mathematical model, we show that herbivores can control primary producer biomass in experiments by concentrating their foraging in small enriched plots; however, at larger, realistic scales, the same mechanism may not lead to herbivore control of primary producers. Instead, other demographic mechanisms are required, but these are not examined in most field studies (and may not operate in many systems). This mismatch between experiments and natural processes suggests that many ecosystems may be less resilient to degradation via enrichment than previously believed.
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References
Agrawal AA (1998) Induced responses to herbivory and increased plant performance. Science 279:1201–1202. doi:10.1126/science.279.5354.1201
Augustine DJ, McNaughton SJ (1998) Ungulate effects on the functional species composition of plant communities: herbivore selectivity and plant tolerance. J Wildl Manage 62:1165–1183. doi:10.2307/3801981
Bell PF, Elmetri I, Lapointe B (2014) Evidence of large-scale chronic eutrophication in the Great Barrier Reef: quantification of chlorophyll a thresholds for sustaining coral reef communities. Ambio 43:361–376. doi:10.1007/s13280-013-0443-1
Bellwood DR, Hughes TP, Folke C, Nystrom M (2004) Confronting the coral reef crisis. Nature 429:827–833. doi:10.1038/nature02691
Bellwood DR, Hughes TP, Hoey AS (2012) Sleeping functional group drives coral-reef recovery. Curr Biol 16:2434–2439. doi:10.1016/j.cub.2006.10.030
Breitburg DL, Hondorp DW, Davias LA, Diaz RJ (2009) Hypoxia, nitrogen, and fisheries: integrating effects across local and global landscapes. Annu Rev Mar Sci 1:329–349. doi:10.1146/annurev.marine.010908.163754
Burkepile DE, Hay ME (2006) Herbivore vs. nutrient control of marine primary producers: context-dependent effects. Ecology 87:3128–3139
Burkholder J, Tomasko D, Touchette B (2007) Seagrasses and eutrophication. J Exp Mar Biol Ecol 350:46–72. doi:10.1016/j.jembe.2007.06.024
Carpenter SR, Kitchell JF (1988) Consumer control of lake productivity. Bioscience 38:764–769. doi:10.2307/1310785
Connell SD et al (2008) Recovering a lost baseline: missing kelp forests from a metropolitan coast. Mar Ecol Prog Ser 360:63–72. doi:10.3354/meps07526
Dixson DL, Abrego D, Hay ME (2014) Chemically mediated behavior of recruiting corals and fishes: a tipping point that may limit reef recovery. Science 345:892–897. doi:10.1126/science.1255057
Ehrlich PR, Birch LC (1967) Balance of nature and population control. Am Nat 101:97. doi:10.1086/282477
Elser JJ et al (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142. doi:10.1111/j.1461-0248.2007.01113.x
Englund G (1997) Importance of spatial scale and prey movements in predator caging experiments. Ecology 78:2316–2325
Fabricius KE (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Mar Pollut Bull 50:125–146. doi:10.1016/j.marpolbul.2004.11.028
Fretwell SD, Lucas HL (1970) On territorial behaviour and other factors influencing habitat distribution in birds. I. Theoretical development. Acta Biotheor 19:16–36
Ghedini G, Russell BD, Connell SD (2015) Trophic compensation reinforces resistance: herbivory absorbs the increasing effects of multiple disturbances. Ecol Lett 18:182–187. doi:10.1111/ele.12405
Gresens SE (1995) Grazer diversity, competition, and the response of the periphyton community. Oikos 73:336–346. doi:10.2307/3545957
Gruner DS et al (2008) A cross-system synthesis of consumer and nutrient resource control on producer biomass. Ecol Lett 11:740–755. doi:10.1111/j.1461-0248.2008.01192.x
Hairston NG, Smith FE, Slobodkin LB (1960) Community structure, population control, and competition. Am Nat 94:421–425. doi:10.1086/282146
Hatcher BG, Larkum AWD (1983) An experimental analysis of factors controlling the standing crop of the epilithic algal community on a coral reef. J Exp Mar Biol Ecol 69:61–84. doi:10.1016/0022-0981(83)90172-7
Hixon MA, Pacala SW, Sandin SA (2002) Population regulation: historical context and contemporary challenges of open vs. closed systems. Ecology 83:1490–1508. doi:10.2307/3071969
Holling CS (1965) The functional response of predators to prey density and its role in mimicry and population regulation. Mem Entomol Soc Can 97:5–60
Hughes TP, Graham NAJ, Jackson JBC, Mumby PJ, Steneck RS (2010) Rising to the challenge of sustaining coral reef resilience. Trends Ecol Evol 25:633–642. doi:10.1016/j.tree.2010.07.011
Lapointe BE (1997) Nutrient thresholds for bottom-up control of macroalgal blooms on coral reefs in Jamaica and southeast Florida. Limnol Oceanogr 42:1119–1131
Lapointe BE, Littler MM, Littler DS (1992) Nutrient availability to marine macroalgae in siliciclastic versus carbonate-rich coastal waters. Estuaries 15:75–82
Lapointe BE, Barile PJ, Matzie WR (2004) Anthropogenic nutrient enrichment of seagrass and coral reef communities in the Lower Florida Keys: discrimination of local versus regional nitrogen sources. J Exp Mar Biol Ecol 308:23–58. doi:10.1016/j.jembe.2004.01.019
Ledlie MH et al (2007) Phase shifts and the role of herbivory in the resilience of coral reefs. Coral Reefs 26:641–653. doi:10.1007/s00338-007-0230-1
Leibold MA (1989) Resource edibility and the effects of predators and productivity on the outcome of trophic interactions. Am Nat 134:922–949. doi:10.1086/285022
Levin SA (1992) The problem of pattern and scale in ecology: the Robert H. MacArthur Award lecture. Ecology 73:1943–1967. doi:10.2307/1941447
McCook LJ, Jompa J, Diaz-Pulido G (2001) Competition between corals and algae on coral reefs: a review of evidence and mechanisms. Coral Reefs 19:400–417
Mittelbach GG, Osenberg CW, Leibold MA (1988) Trophic relations and ontogenetic niche shifts in aquatic ecosystems. In: Ebenman B, Persson L (eds) Size-structured populations: ecology and evolution. Springer, Berlin, pp 219–235
Nicotri ME (1980) Factors involved in herbivore food preference. J Exp Mar Biol Ecol 42:13–26. doi:10.1016/0022-0981(80)90163-x
Nixon SW (2009) Eutrophication and the macroscope. Hydrobiologia 629:5–19. doi:10.1007/s10750-009-9759-z
Nyström M et al (2012) Confronting feedbacks of degraded marine ecosystems. Ecosystems 15:695–710. doi:10.1007/s10021-012-9530-6
Oksanen L, Fretwell SD, Arruda J, Niemela P (1981) Exploitation ecosystems in gradients of primary productivity. Am Nat 118:240–261. doi:10.2307/2460513
Oksanen T, Power ME, Oksanen L (1995) Ideal free habitat selection and consumer–resource dynamics. Am Nat 146:565–585. doi:10.2307/2462979
Osenberg CW, Mittelbach GG (1996) The relative importance of resource limitation and predator limitation in food chains. In: Polis GA, Winemiller KO (eds) Food webs: integration of patterns and dynamics. Chapman and Hall, New York, pp 134–148
Paddack MJ et al (2009) Recent region-wide declines in Caribbean reef fish abundance. Curr Biol 19:590–595. doi:10.1016/j.cub.2009.02.041
Paerl HW, Valdes LM, Peierls BL, Adolf JE, Harding LW (2006) Anthropogenic and climatic influences on the eutrophication of large estuarine ecosystems. Limnol Oceanogr 51:448–462
Penna N, Capellacci S, Ricci F (2004) The influence of the Po River discharge on phytoplankton bloom dynamics along the coastline of Pesaro (Italy) in the Adriatic Sea. Mar Pollut Bull 48:321–326. doi:10.1016/j.marpolbul.203.08.007
Power ME (1984) Habitat quality and the distribution of algae-grazing catfish in a Panamanian stream. J Anim Ecol 53:357–374. doi:10.2307/4521
Quinn GP, Keough MJ (1993) Potential effect of enclosure size on field experiments with herbivorous intertidal gastropods. Mar Ecol Prog Ser 98:199–201. doi:10.3354/meps098199
Rasher DB, Hay ME (2010) Chemically rich seaweeds poison corals when not controlled by herbivores. Proc Natl Acad Sci USA 107:9683–9688. doi:10.1073/pnas.0912095107
Rosenzweig M (1971) Paradox of enrichment: destabilization of exploitation ecosystems in ecological time. Science 171:385–387. doi:10.1126/science.171.3969.385
Schindler DW et al (2008) Eutrophication of lakes cannot be controlled by reducing nitrogen input: results of a 37-year whole-ecosystem experiment. Proc Natl Acad Sci 105:11254–11258. doi:10.1073/pnas.0805108105
Sih A, Crowley P, McPeek M, Petranka J, Strohmeier K (1985) Predation, competition, and prey communities: a review of field experiments. Annu Rev Ecol Syst 16:269–311. doi:10.2307/2097050
Silliman BR, Bertness MD (2002) A trophic cascade regulates salt marsh primary production. Proc Natl Acad Sci 99:10500–10505. doi:10.1073/pnas.162366599
Smith SV, Kimmerer WJ, Laws EA, Brock RE, Walsh TW (1981) Kaneohe Bay sewage diversion experiment: perspectives on ecosystem responses to nutritional perturbation. Pac Sci 35:279–402
Smith JE et al (2006) Indirect effects of algae on coral: algae-mediated, microbe-induced coral mortality. Ecol Lett 9:835–845. doi:10.1111/j.1461-0248.2006.00937.x
Sutherland WJ (1983) Aggregation and the ‘ideal free’ distribution. J Anim Ecol 52:821–828. doi:10.2307/4456
Van de Koppel J et al (2005) The effects of spatial scale on trophic interactions. Ecosystems 8:801–807. doi:10.1007/s10021-005-0134-2
Vitousek PM et al (1997) Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–750. doi:10.2307/2269431
Walker DI, Ormond RFG (1982) Coral death from sewage and phosphate pollution at Aqaba, Red Sea. Mar Pollut Bull 13:21–25
Acknowledgments
Support was provided by a National Science Foundation (NSF) Graduate Research Fellowship (DGE-0802270), a Florida Sea Grant Fellowship, and NSF Grant OCE-1130359. We thank B. R. Silliman, T. Frazer, R. Fletcher, and anonymous reviewers for constructive comments on previous versions of this manuscript, and N. Hackney for assistance with our literature review.
Author contribution statement
M. A. G. and C. W. O. conceptualized the study; M. A. G., C. W. O. and J. J. developed the model; M. A. G. drafted the manuscript, and all authors revised the text.
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Communicated by Steven Kohler.
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Gil, M.A., Jiao, J. & Osenberg, C.W. Enrichment scale determines herbivore control of primary producers. Oecologia 180, 833–840 (2016). https://doi.org/10.1007/s00442-015-3505-1
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DOI: https://doi.org/10.1007/s00442-015-3505-1