Skip to main content
Log in

Consumer adaptation mediates top–down regulation across a productivity gradient

  • Community ecology – original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Humans have artificially enhanced the productivity of terrestrial and aquatic ecosystems on a global scale by increasing nutrient loading. While the consequences of eutrophication are well known (e.g., harmful algal blooms and toxic cyanobacteria), most studies tend to examine short-term responses relative to the time scales of heritable adaptive change. Thus, the potential role of adaptation by organisms in stabilizing the response of ecological systems to such perturbations is largely unknown. We tested the hypothesis that adaptation by a generalist consumer (Daphnia pulicaria) to toxic prey (cyanobacteria) mediates the response of plankton communities to nutrient enrichment. Overall, the strength of Daphnia’s top–down effect on primary producer biomass increased with productivity. However, these effects were contingent on prey traits (e.g., rare vs. common toxic cyanobacteria) and consumer genotype (i.e., tolerant vs sensitive to toxic cyanobacteria). Tolerant Daphnia strongly suppressed toxic cyanobacteria in nutrient-rich ponds, but sensitive Daphnia did not. In contrast, both tolerant and sensitive Daphnia genotypes had comparable effects on producer biomass when toxic cyanobacteria were absent. Our results demonstrate that organismal adaptation is critical for understanding and predicting ecosystem-level consequences of anthropogenic environmental perturbations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • An JS, Carmichael WW (1994) Use of a colorimetric protein phosphatase inhibition assay and enzyme-linked-immunosorbent assay for the study of microcystins and nodularins. Toxicon 32:1495–1507

    Article  CAS  PubMed  Google Scholar 

  • Bassar RD et al (2010) Local adaptation in Trinidadian guppies alters ecosystem processes. Proc Natl Acad Sci USA 107:3616–3621

    Article  PubMed  PubMed Central  Google Scholar 

  • Birtel J, Matthews B (2016) Grazers structure the bacterial and algal diversity of aquatic metacommunities. Ecology 97:3472–3484

    Article  PubMed  Google Scholar 

  • Boyd CE, Shelton JL (1984) Observations on the hydrology and morphometry of ponds on the Auburn University Fisheries Research Unit. Agricultural Experiment Station Bulletin, vol 558, pp 1–33

  • Carlsson NOL, Sarnelle O, Strayer D (2009) Native predators and exotic prey—an acquired taste? Front Ecol Environ 7:525–532

    Article  Google Scholar 

  • Carmichael WW (1992) Cyanobacteria secondary metabolites—the cyanotoxins. J Appl Bacteriol 72:445–459

    Article  CAS  PubMed  Google Scholar 

  • Carpenter SR et al (1985) Cascading trophic interactions and lake productivity. Bioscience 35:634–639

    Article  Google Scholar 

  • Carpenter SR et al (1998) Nonpoint pollution of surface waters with phosphorus and nitrogen. Ecol Appl 8:559–568

    Article  Google Scholar 

  • Chase JM et al (2000) The effects of productivity, herbivory, and plant species turnover in grassland food webs. Ecology 81:2485–2497

    Article  Google Scholar 

  • Chislock MF et al (2013) Large effects of consumer offense on ecosystem structure and function. Ecology 94:2375–2380

    Article  PubMed  Google Scholar 

  • Chislock MF, Sharp KL, Wilson AE (2014) Cylindrospermopsis raciborskii dominates under very low and high nitrogen-to-phosphorus ratios. Water Res 49:207–214

    Article  CAS  PubMed  Google Scholar 

  • Daskalov GM et al (2007) Trophic cascades triggered by overfishing reveal possible mechanisms of ecosystem regime shifts. Proc Natl Acad Sci USA 104:10518–10523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Des Roches S, Post DM, Turley NE, Bailey JK, Hendry AP, Kinnison MT, Schweitzer JA, Palkovacs EP (2018) The ecological importance of intraspecific variation. Nat Ecol Evol 2:57–64

    Article  PubMed  Google Scholar 

  • Downing JA, Watson SB, McCauley E (2001) Predicting cyanobacteria dominance in lakes. Can J Fish Aquat Sci 58:1905–1908

    Article  Google Scholar 

  • Estes JA et al (2011) Trophic downgrading of planet earth. Science 333:301–306

    Article  CAS  PubMed  Google Scholar 

  • Frisch D, Morton PK, Culver BW, Edlund MB, Jeyasingh PD, Weider LJ (2017) Paleogenetic records of Daphnia pulicaria in two North American lakes reveal the impact of cultural eutrophication. Glob Change Biol 23:708–718

    Article  Google Scholar 

  • Gliwicz ZM (1990) Food thresholds and body size in cladocerans. Nature 343:638–640

    Article  Google Scholar 

  • Grant PR, Grant BR (2002) Unpredictable evolution in a 30-year study of Darwin’s finches. Science 296:707–711

    Article  CAS  PubMed  Google Scholar 

  • Gray DK, Arnott SE (2009) Recovery of acid damaged zooplankton communities: measurements, extent, and limiting factors. Environ Rev 17:81–99

    Article  Google Scholar 

  • Hairston NG, Smith FE, Slobodkin LB (1960) Community structure, population control, and competition. Am Nat 94:421–425

    Article  Google Scholar 

  • Hairston NG et al (1999) Rapid evolution revealed by dormant eggs. Nature 401:446

    Article  Google Scholar 

  • Hairston NG et al (2001) Natural selection for grazer resistance to toxic cyanobacteria: evolution of phenotypic plasticity? Evolution 55:2203–2214

    Article  PubMed  Google Scholar 

  • Harmon LJ et al (2009) Evolutionary diversification in stickleback affects ecosystem functioning. Nature 458:1167–1170

    Article  CAS  PubMed  Google Scholar 

  • Hatton IA et al (2015) The predator-prey power law: biomass scaling across terrestrial and aquatic biomes. Science. https://doi.org/10.1126/science.aac6284

    Article  PubMed  Google Scholar 

  • Hautier Y et al (2015) Plant ecology. Anthropogenic environmental changes affect ecosystem stability via biodiversity. Science 348:336–340

    Article  CAS  PubMed  Google Scholar 

  • Heathcote AJ, Filstrup CT, Kendall D, Downing JA (2016) Biomass pyramids in lake plankton: influence of cyanobacteria size and abundance. Inland Waters 6:250–257

    Article  Google Scholar 

  • Higgins SN, Althouse B, Devlin SP, Vadeboncoeur Y, Vander Zanden MJ (2014) Potential for large-bodied zooplankton and dreissenids to alter the productivity and autotrophic structure of lakes. Ecology 95:2257–2267

    Article  PubMed  Google Scholar 

  • Isbell F et al (2013) Nutrient enrichment, biodiversity loss, and consequent declines in Ecosystem productivity. Proc Natl Acad Sci USA 110:11911–11916

    Article  PubMed  PubMed Central  Google Scholar 

  • Karban R, Agrawal AA (2002) Herbivore offense. Annu Rev Ecol Evol Syst 33:641–664

    Article  Google Scholar 

  • Leibold MA (1989) Resource edibility and the effects of predators and productivity on the outcome of trophic interactions. Am Nat 134:922–949

    Article  Google Scholar 

  • Leibold MA et al (1997) Species turnover and the regulation of trophic structure. Annu Rev Ecol Evol Syst 28:467–494

    Article  Google Scholar 

  • Lohbeck KT, Riebesell U, Reusch TBH (2012) Adaptive evolution of a key phytoplankton species to ocean acidification. Nat Geosci 6:346–351

    Article  CAS  Google Scholar 

  • Mazumder A (1994) Patterns of algal biomass in dominant odd- vs even-link lake ecosystems. Ecology 75:1141–1149

    Article  Google Scholar 

  • Monchamp M-E, Spaak P, Domaizon I, Dubois N, Bouffard D, Pomati D (2018) Homogenization of lake cyanobacterial communities over a century of climate change and eutrophication. Nat Ecol Evol 2:317–324

    Article  PubMed  Google Scholar 

  • Oksanen L et al (1981) Exploitation ecosystems in gradients of primary productivity. Am Nat 118:240–261

    Article  Google Scholar 

  • Paine RT (1966) Food web complexity and species diversity. Am Nat 100:65–75

    Article  Google Scholar 

  • Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669

    Article  Google Scholar 

  • Pennisi E (2012) The great guppy experiment. Science 24:904–908

    Article  Google Scholar 

  • Pimentel D, Edwards CA (1982) Pesticides and ecosystems. Bioscience 32:595–600

    Article  CAS  Google Scholar 

  • Polis GA (1999) Why are parts of the world green? Multiple factors control productivity and the distribution of biomass. Oikos 86:3–15

    Article  Google Scholar 

  • Post DM et al (2008) Intraspecific variation in a predator affects community structure and cascading trophic interactions. Ecology 89:2019–2032

    Article  PubMed  Google Scholar 

  • Rhoades DF (1985) Offensive-defensive interactions between herbivores and plants: their relevance in herbivore population dynamics and ecological theory. Am Nat 125:205–238

    Article  Google Scholar 

  • Sarnelle O (1992) Nutrient enrichment and grazer effects on phytoplankton in lakes. Ecology 73:551–560

    Article  Google Scholar 

  • Sarnelle O (2007) Initial conditions mediate the interaction between Daphnia and bloom-forming cyanobacteria. Limnol Oceanogr 52:2120–2127

    Article  CAS  Google Scholar 

  • Sarnelle O, Wilson AE (2005) Local adaptation of Daphnia pulicaria to toxic cyanobacteria. Limnol Oceanogr 50:1565–1570

    Article  Google Scholar 

  • Sartory DP, Grobbelaar JU (1984) Extraction of chlorophyll-a from fresh-water phytoplankton for spectrophotometric analysis. Hydrobiologia 114:177–187

    Article  CAS  Google Scholar 

  • Schindler DW (1974) Eutrophication and recovery in experimental lakes: implications for lake management. Science 184:897–899

    Article  CAS  PubMed  Google Scholar 

  • Smith VH, Schindler DW (2009) Eutrophication science: where to do we go from here? Trends Ecol Evol 24:201–207

    Article  PubMed  Google Scholar 

  • Sommer U, Gliwicz ZM, Lampert W, Duncan A (1986) The PEG-model of seasonal succession of planktonic events in fresh waters. Arch Hydrobiol 106:433–471

    Google Scholar 

  • Tilman D (1982) Resource competition and community structure. Princeton University, Princeton

    Google Scholar 

  • Urban MC (2013) Evolution mediates the effects of apex predation on aquatic food webs. Proc R Soc Lond B 280:20130859

    Article  Google Scholar 

  • Urban MC, Richardson JL, Friedenfields NA (2014) Plasticity and genetic adaptation mediate amphibian and reptile responses to climate change. Evol Appl 7:88–103

    Article  PubMed  Google Scholar 

  • Utermöhl H (1958) Zur Vervollkommnung der quantitativen Phytoplankton-Methodik. Mitt Int Ver Theor Angew Limnol 9:1–38

    Google Scholar 

  • Vitousek PM et al (1997a) Human domination of Earth’s ecosystems. Science 277:494–499

    Article  CAS  Google Scholar 

  • Vitousek PM et al (1997b) Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–750

    Google Scholar 

  • Walsh MR, DeLong JP, Hanley TC, Post DM (2012) A cascade of evolutionary change alters consumer-resource dynamics and ecosystem function. Proc R Soc Lond Ser B Biol Sci 279:3184–3192

    Article  Google Scholar 

  • Weider LJ, Jeyasingh PD, Frisch D (2018) Evolutionary aspects of resurrection ecology: progress, scope, and applications—an overview. Evol Appl 11:3–10

    Article  PubMed  Google Scholar 

  • Young HS et al (2015) Context-dependent effects of large-wildlife declines on small mammal communities in central Kenya. Ecol Appl 25:348–360

    Article  PubMed  Google Scholar 

  • Yousey AM, Chowdhury PR, Biddinger N, Shaw JH, Jeyasingh PD, Weider LJ (2018) Resurrected ‘ancient’ Daphnia genotypes show reduced thermal stress tolerance compared to modern descendants. R Soc Open Sci 5:172193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank Randall Goodman, Mark Peterman, and the staff of the Auburn University E.W. Shell Fisheries Research Center for logistical support. Steve Cason provided assistance in the lab. Dennis DeVries, Sharon Hermann, Rusty Wright, Volker Rudolf, Bri Reed, Andy Turner, Alan Tessier, Doug Levey, Sam Scheiner, Jon Chase, Jason Hoverman, and Mike Vanni provided helpful comments on the manuscript. This study was supported by an EPA STAR Graduate Fellowship, NSF Grants DEB-0841864, DEB-0841944, and DBI-0965272, and the Alabama Agricultural Experiment Station, and the Hatch program of the National Institute of Food and Agriculture, U.S. Department of Agriculture.

Author information

Authors and Affiliations

Authors

Contributions

MFC, OS, and AEW conceived and designed the experiments. MFC, LMJ, VRA, and AEW performed the experiments. MFC, OS, AA, and AEW analyzed the data. MFC, OS, AA, and AEW wrote the manuscript; other authors provided editorial advice.

Corresponding author

Correspondence to Alan E. Wilson.

Additional information

Communicated by Ulrich Sommer.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 733 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chislock, M.F., Sarnelle, O., Jernigan, L.M. et al. Consumer adaptation mediates top–down regulation across a productivity gradient. Oecologia 190, 195–205 (2019). https://doi.org/10.1007/s00442-019-04401-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-019-04401-4

Keywords

Navigation