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Herbivore population dynamics in response to plant allocation strategies

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Abstract

When herbivores feed, plants may respond by altering the quantity of edible biomass available to future feeders through mechanisms such as compensatory regrowth of edible structures or allocation of biomass to inedible reserves. Previous work showed that some forms of compensatory regrowth can drive insect outbreaks, but this work assumed regrowth occurred without any energetic cost to the plant. While this is a useful simplifying assumption for gaining preliminary insights, plants face an inherent trade-off between allocating energy to regrowth versus storage. Therefore, we cannot truly understand the role of compensatory regrowth in driving insect outbreaks without continuing on to more realistic scenarios. In this paper, we model the interaction between insect herbivores and plants that have a trade-off between compensatory regrowth and allocation to inedible reserves in response to herbivory. We found that the plant’s allocation strategy, described in our model by parameters representing the strength of the overcompensatory response and the rates at which energy is stored and mobilized for growth, strongly affects whether herbivore outbreaks occur. Additional factors, such as the strength of food limitation and herbivore interference while feeding, influence the frequency of the outbreaks. Overall, we found a possible new role of overcompensation to promote herbivore fluctuations when it co-occurs with allocation to inedible reserves. We highlight the importance of considering trade-offs between tolerance mechanisms that plants use in response to herbivory by showing that new dynamics arise when different plant allocation strategies occur simultaneously.

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Data availability

There were no data collected for this study.

Code availability

Code is available at https://github.com/fang-ji/modeling_projects/tree/main/insect_outbreaks.

References

  • Abbott KC, Morris WF, Gross K (2008) Simultaneous effects of food limitation and inducible resistance on herbivore population dynamics. Theor Popul Biol 73(1):63–78

    Article  Google Scholar 

  • Agrawal AA (2000) Overcompensation of plants in response to herbivory and the by-product benefits of mutualism. Trends Plant Sci 5(7):309–313

    Article  CAS  Google Scholar 

  • Alward RD, Joern A (1993) Plasticity and overcompensation in grass responses to herbivory. Oecologia 95(3):358–364

    Article  Google Scholar 

  • Anderson KE, Inouye BD, Underwood N (2009) Modeling herbivore competition mediated by inducible changes in plant quality. Oikos 118(11):1633–1646

  • Belsky A (1986) Does Herbivory Benefit Plants? A Review of the Evidence. Am Nat 127(6):870–892

    Article  Google Scholar 

  • Berryman AA (1987) The theory and classification of outbreaks. Insect Outbreaks 3–30

  • Briske DD, Boutton TW, Wang Z (1996) Contribution of flexible allocation priorities to herbivory tolerance in C 4 perennial grasses: an evaluation with 13 C labeling. Oecologia 105(2):151–159

    Article  CAS  Google Scholar 

  • Crutchfield BA, Potter DA (1995) Feeding by Japanese beetle and southern masked chafer grubs on lawn weeds. Crop Sci 35(6):1681–1684

    Article  Google Scholar 

  • De Mazancourt C, Loreau M, Abbadie L (1998) Grazing optimization and nutrient cycling: when do herbivores enhance plant production? Ecology 79(7):2242–2252

    Article  Google Scholar 

  • DuToit JT, Bryant JP, Frisby K (1990) Regrowth and palatability of Acacia shoots following pruning by African savanna browsers. Ecology 71(1):149–154

    Article  Google Scholar 

  • Dyer MI, Acra MA, Wang GM, Coleman DC, Freckman DW, McNaughton SJ, Strain BR (1991) Source-sink carbon relations in two Panicum coloratum ecotypes in response to herbivory. Ecology 72(4):1472–1483

    Article  Google Scholar 

  • Elton CS (1924) Periodic fluctuations in the numbers of animals: their causes and effects. J Exp Biol 2(1):119–163

    Article  Google Scholar 

  • Fay PA, Hartnett DC, Knapp AK (1996) Plant tolerance of gall-insect attack and gall-insect performance. Ecology 77(2):521–534

    Article  Google Scholar 

  • Garcia LC, Eubanks MD (2019) Overcompensation for insect herbivory: a review and meta-analysis of the evidence. Ecology 100(3):e02585

  • Kendall BE, Briggs CJ, Murdoch WW, Turchin P, Ellner SP, McCauley E, Wood SN (1999) Why do populations cycle? A synthesis of statistical and mechanistic modeling approaches. Ecology 80(6):1789–1805

    Article  Google Scholar 

  • Kessler A, Baldwin IT (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annu Rev Plant Biol 53(1):299–328

    Article  CAS  Google Scholar 

  • Lennartsson T, Nilsson P, Tuomi J (1998) Induction of overcompensation in the field gentian. Gentianella campestris. Ecology 79(3):1061–1072

    Article  Google Scholar 

  • Liebhold AM (2019) Air pollution as an experimental probe of insect population dynamics. J Anim Ecol 88(5):662–664

    Article  Google Scholar 

  • Lundberg S, Järemo J, Nilsson P (1994) Herbivory, inducible defence and population oscillations: a preliminary theoretical analysis. Oikos 71(3):537–540

    Article  Google Scholar 

  • McNaughton SJ (1979) Grazing as an optimization process: grass-ungulate relationships in the Serengeti. Am Nat 113(5):691–703

    Article  Google Scholar 

  • McNaughton SJ (1983) Compensatory Plant Growth as a Response to Herbivory. Oikos 14:1158–1169

    Google Scholar 

  • Miller TE, Tyre AJ, Louda SM (2006) Plant reproductive allocation predicts herbivore dynamics across spatial and temporal scales. Am Nat 168(5):608–616

    Article  Google Scholar 

  • Murdoch WW, Kendall BE, Nisbet RM, Briggs CJ, McCauley E, Bolser R (2002) Single-species models for many-species food webs. Nature 417(6888):541–543

    Article  CAS  Google Scholar 

  • Nabeshima E, Murakami M, Hiura T (2001) Effects of herbivory and light conditions on induced defense in Quercus crispula. J Plant Res 114(4):403–409

    Article  Google Scholar 

  • Orians CM, Thorn A, Gómez S (2011) Herbivore-induced resource sequestration in plants: Why bother? Oecologia 167(1):1–9

    Article  Google Scholar 

  • Paige KN, Whitham TG (1987) Overcompensation in response to mammalian herbivory: the advantage of being eaten. Am Nat 129(3):407–416

    Article  Google Scholar 

  • Pratt PD, Rayamajhi MB, Van TK, Center TD, Tipping PW (2005) Herbivory alters resource allocation and compensation in the invasive tree Melaleuca quinquenervia. Ecol Entomol 30(3):316–326

    Article  Google Scholar 

  • Rosenzweig ML (1971) Paradox of enrichment: destabilization of exploitation ecosystems in ecological time. Science 171(3969):385–387

    Article  CAS  Google Scholar 

  • Sadras VO (1996) Cotton compensatory growth after loss of reproductive organs as affected by availability of resources and duration of recovery period. Oecologia 106(4):432–439

    Article  Google Scholar 

  • Schat M, Blossey B (2005) Influence of natural and simulated leaf beetle herbivory on biomass allocation and plant architecture of purple loosestrife (Lythrum salicaria L.). Environ Entomol 34(4):906–914

  • Stevens MH (2009). A Primer of Ecology with R. Springer Science & Business Media

  • Stieha CR, Abbott KC, Poveda K (2016) The effects of plant compensatory regrowth and induced resistance on herbivore population dynamics. Am Nat 187(2):167–181

    Article  Google Scholar 

  • Thomas SM, Abbott KC, Moloney KA (2017) Effects of aboveground herbivory on plants with long-term belowground biomass storage. Thyroid Res 10(1):35–50

    Google Scholar 

  • Turchin P (2013) Complex population dynamics. Princeton University Press

    Book  Google Scholar 

  • Underwood N, Rausher MD (2000) The effects of host-plant genotype on herbivore population dynamics. Ecology 81(6):1565–1576

    Article  Google Scholar 

  • Vos M, Kooi BW, DeAngelis DL, Mooij WM (2004) Inducible defences and the paradox of enrichment. Oikos 105(3):471–480

    Article  Google Scholar 

  • Zhou S, Lou YR, Tzin V, Jander G (2015) Alteration of plant primary metabolism in response to insect herbivory. Plant Physiol 169(3):1488–1498

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank Annika Weder, Amy Patterson, Samantha Catella, Angela Lenard, Hilary Rollins, Robin Snyder, and Jean Burns for their valuable comments on this manuscript. All authors were partially supported by McDonnell Foundation Complex Systems Scholar grant #220020364. Fang Ji and Karen Abbott received additional support from National Science Foundation DMS-1840221.

Funding

All authors were partially supported by McDonnell Foundation Complex Systems Scholar grant #220020364. Fang Ji and Karen Abbott received additional support from NSF DMS-1840221.

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Karen Abbott, Christopher Stieha, and Fang Ji conceived the ideas and designed methodology; Fang Ji and Christopher Stieha constructed the model; Fang Ji analyzed the model; Fang Ji and Karen Abbott led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.

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Correspondence to Fang Ji.

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Ji, F., Stieha, C.R. & Abbott, K.C. Herbivore population dynamics in response to plant allocation strategies. Theor Ecol 15, 191–202 (2022). https://doi.org/10.1007/s12080-022-00536-y

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