Skip to main content
SpringerLink
Log in

Algal defenses, population stability, and the risk of herbivore extinctions: a chemostat model and experiment

  • Original Article
  • Published:
Ecological Research

Abstract

The effects of inducible defenses and constitutive defenses on population dynamics were investigated in a freshwater plankton system with rotifers as predators and different algal strains as prey. We made predictions for these systems using a chemostat predator–prey model and focused on population stability and predator persistence as a function of flow-through rate. The model exhibits three major types of behavior at a high nutrient concentration: (1) at high dilution rates, only algae exist; (2) at intermediate dilution rates, algae and rotifers show stable coexistence; (3) at low dilution rates, large population fluctuations occur, with low minimum densities entailing a risk of stochastic rotifer extinctions. The size and location of the corresponding areas in parameter space critically depend on the type of algal defense strategy. In an 83-day high-nutrient chemostat experiment we changed the dilution rate every 3 weeks, from 0.7 to 0.5 to 0.3 to 0.1 per day. Within this range of dilution rates, rotifers and algae coexisted, and population fluctuations of algae clearly increased as dilution rates decreased. The CV of herbivore densities was highest at the end of the experiment, when the dilution rate was low. On day 80, herbivorous rotifers had become undetectable in all three chemostats with permanently defended algae (where rotifer densities had already been low) and in two out of three chemostats where rotifers had been feeding on algae with inducible defenses (that represented more edible food). We interpret our results in relation to the paradox of enrichment.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abrams PA, Walters CJ (1996) Invulnerable prey and the paradox of enrichment. Ecology 77:1125–1133

    Article  Google Scholar 

  • Boraas ME (1983) Population dynamics of food-limited rotifers in two-stage chemostat culture. Limnol Oceanogr 28:546–563

    Google Scholar 

  • Edelstein-Keshet L, Rausher MD (1989) The effects of inducible plant defenses on herbivore populations. 1. Mobile herbivores in continuous time. Am Nat 133:787–810

    Article  Google Scholar 

  • Fussmann GF, Ellner SP, Shertzer KW, Hairston NG (2000) Crossing the Hopf bifurcation in a live predator–prey system. Science 290:1358–1360

    Article  PubMed  CAS  Google Scholar 

  • Gabriel W, Luttbeg B, Sih A, Tollrian R (2005) Environmental tolerance, heterogeneity, and the evolution of reversible plastic responses. Am Nat 166:339–353

    Article  PubMed  Google Scholar 

  • Harvell CD (1990) The ecology and evolution of inducible defenses. Q Rev Biol 65:323–340

    Article  PubMed  CAS  Google Scholar 

  • Haukioja E (1980) On the role of plant defences in the fluctuations of herbivore populations. Oikos 35:202–213

    Article  Google Scholar 

  • Hessen DO, Van Donk E (1993) Morphological changes in Scenedesmus induced by substances released from Daphnia. Arch Hydrobiol 127:129–140

    Google Scholar 

  • Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, Chicago

    Google Scholar 

  • Kilham SS, Kreeger DA, Lynn SG, Goulden CE, Herrera L (1998) COMBO: a defined freshwater culture medium for algae and zooplankton. Hydrobiol 377:147–159

    Article  CAS  Google Scholar 

  • Kooi BW, Boer MP, Kooijman S (1998) On the use of the logistic equation in models of food chains. Bull Math Biol 60:231–246

    Article  Google Scholar 

  • Kopp M, Gabriel W (2006) The dynamic effects of an inducible defense in the Nicholson–Bailey model. Theor Popul Biol 70:43–55

    Article  PubMed  Google Scholar 

  • Lundberg S, Jaremo J, Nilsson P (1994) Herbivory, inducible defence and population oscillations: a preliminary theoretical analysis. Oikos 71:537–539

    Article  Google Scholar 

  • Lürling M, Van Donk E (2000) Grazer-induced colony formation in Scenedesmus: are there costs to being colonial? Oikos 88:111–118

    Article  Google Scholar 

  • Lürling M, Arends H, Beekman W, Vos M, van der Stap I, Mooij WM, Scheffer M (2005) Effect of grazer-induced morphological changes in the green alga Scenedesmus obliquus on growth of the rotifer Brachionus calyciflorus. Proc Int Assoc Theor Appl Limnol 29:698–703

    Google Scholar 

  • Peacor SD, Werner EE (2000) Predator effects on an assemblage of consumers through induced changes in consumer foraging behavior. Ecology 81:1998–2010

    Google Scholar 

  • Raimondi PT, Forde SE, Delph LF, Lively CM (2000) Processes structuring communities: evidence for trait-mediated indirect effects through induced polymorphisms. Oikos 91:353–361

    Article  Google Scholar 

  • Ramos-Jiliberto R (2003) Population dynamics of prey exhibiting inducible defenses: the role of associated costs and density-dependence. Theor Popul Biol 64:221–231

    Article  PubMed  Google Scholar 

  • Rothhaupt KO (1990a) Differences in particle size-dependent feeding efficiencies of closely related rotifer species. Limnol Oceanogr 35:16–23

    Article  Google Scholar 

  • Rothhaupt KO (1990b) Changes of the functional responses of the rotifers Brachionus rubens and Brachionus calyciflorus with particle sizes. Limnol Oceanogr 35:24–32

    Google Scholar 

  • Tollrian R, Harvell CD (1999) The ecology and evolution of inducible defenses. Princeton University Press, Princeton

    Google Scholar 

  • Turner AM, Bernot RJ, Boes CM (2000) Chemical cues modify species interactions: the ecological consequences of predator avoidance by freshwater snails. Oikos 88:148–158

    Article  CAS  Google Scholar 

  • Underwood N (1999) The influence of plant and herbivore characteristics on the interaction between induced resistance and herbivore population dynamics. Am Nat 153:282–294

    Article  Google Scholar 

  • Underwood N, Rausher M (2002) Comparing the consequences of induced and constitutive plant resistance for herbivore population dynamics. Am Nat 160:20–30

    Article  PubMed  Google Scholar 

  • van der Stap, I (2007) Inducible defenses and the dynamics of planktonic food chains. PhD Thesis, Radboud University Nijmegen, NIOO thesis 53

  • van der Stap I, Vos M, Mooij WM (2006) Linking herbivore-induced defences to population dynamics. Freshw Biol 51:424–434

    Article  Google Scholar 

  • van der Stap I, Vos M, Mooij WM (2007a) Inducible defenses and rotifer food chain dynamics. Hydrobiol 593:103–110

    Article  CAS  Google Scholar 

  • van der Stap I, Vos M, Verschoor AM, Helmsing NR, Mooij WM (2007b) Induced defenses in herbivores and plants differentially modulate a trophic cascade. Ecology 88:2474–2481

    Article  PubMed  Google Scholar 

  • Verschoor AM, van der Stap I, Helmsing NR, Lürling M, Van Donk E (2004a) Inducible colony formation within the Scenedesmaceae: adaptive responses to infochemicals from two different herbivore taxa. J Phycol 40:808–814

    Article  Google Scholar 

  • Verschoor AM, Vos M, van der Stap I (2004b) Inducible defences prevent strong population fluctuations in bi- and tritrophic food chains. Ecol Lett 7:1143–1148

    Article  Google Scholar 

  • Verschoor AM, Bekmezci OK, Vijverberg J (2005) Inducible defences: slow relaxation is costly. In: Verschoor AM (2005) Hard to handle. Inducible defences in plankton. Radboud University Nijmegen, PhD Thesis, pp 121-139

  • Verschoor AM, Zadereev YS, Mooij WM (2007) Infochemical-mediated trophic interactions between the rotifer Brachionus calyciflorus and its food algae. Limnol Oceanogr 52:2109–2119

    CAS  Google Scholar 

  • Vos M, Flik BJG, Vijverberg J, Ringelberg J, Mooij WM (2002) From inducible defences to population dynamics: modelling refuge use and life history changes in Daphnia. Oikos 99:386–396

    Article  Google Scholar 

  • Vos M, Kooi BW, DeAngelis DL, Mooij WM (2004a) Inducible defences and the paradox of enrichment. Oikos 105:471–480

    Article  Google Scholar 

  • Vos M, Verschoor AM, Kooi BW, Wäckers FL, DeAngelis DL, Mooij WM (2004b) Inducible defenses and trophic structure. Ecology 85:2783–2794

    Article  Google Scholar 

  • Vos M, Kooi BW, DeAngelis DL, Mooij WM (2005) Inducible defenses in food webs. In: De Ruiter PC, Wolters V, Moore JC (eds) Dynamic food webs: multispecies assemblages, ecosystem development, and environmental change. Academic Press, Amsterdam, pp 114–127

    Google Scholar 

  • Walz N (ed) (1993) Plankton regulation dynamics: experiments and models in rotifer continuous cultures. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Yoshida T, Ellner SP, Jones LE, Bohannan BJM, Lenski RE, Hairston NG Jr (2007) Cryptic population dynamics: rapid evolution masks trophic interactions. PLoS Biol 5(9):e235

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Arie Kersbergen for technical assistance, sampling and rotifer counts, Nico Helmsing, Miguel Dionisio Pires for help with sampling; Anthony Verschoor for the use of a pilot experimental setup to test and improve our chemostat system. This research was supported by a grant from the Netherlands Organisation for Scientific Research (NWO-ALW) for IvdS to W.M.M and M.V.

Author information

Authors and Affiliations

  1. Department of Aquatic Food Webs, Centre for Limnology, Netherlands Institute of Ecology (NIOO-KNAW), Rijksstraatweg 6, 3631 AC, Nieuwersluis, The Netherlands

    Irene van der Stap, Bram T. M. Mulling, Ellen van Donk & Wolf M. Mooij

  2. Department of Ecosystem Studies, Centre for Estuarine and Marine Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Korringaweg 7, 4401 NT, Yerseke, The Netherlands

    Matthijs Vos

  3. Department of Theoretical Biology, Faculty of Earth and Life Sciences, Free University Amsterdam, Boelelaan 1087, 1081 HV, Amsterdam, The Netherlands

    Bob W. Kooi

Authors
  1. Irene van der Stap
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Matthijs Vos
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bob W. Kooi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bram T. M. Mulling
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ellen van Donk
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Wolf M. Mooij
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Matthijs Vos.

About this article

Cite this article

van der Stap, I., Vos, M., Kooi, B.W. et al. Algal defenses, population stability, and the risk of herbivore extinctions: a chemostat model and experiment. Ecol Res 24, 1145–1153 (2009). https://doi.org/10.1007/s11284-009-0596-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11284-009-0596-3

Keywords

Search

Navigation