Skip to main content
Log in

Predator functional responses and the biocontrol of aphids and mites

  • Published:
BioControl Aims and scope Submit manuscript

Abstract

Biocontrol with predators is a key tool for controlling agricultural pests and preserving the productive efficiency of crops. Determining which predators to use for biocontrol often involves measuring their functional response—the relationship between foraging rate and prey abundance, yet comparisons of functional responses across predators are complicated by differences in experimental procedures. Here we use a compilation of functional responses standardized for time and space units to illustrate key sources of variation in functional responses for predators being tested for control of aphids and mites. Our results show that arena size (as a proxy for habitat structure) is a crucial predictor of predator performance, indicating that assessments of functional responses on the crops of interest may be necessary for accurate comparisons. Our results also suggest that larger predators may generally be more efficient, and that warming linked to climate change could make biocontrol using predators more effective when pests are abundant.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

All data are publicly available online.

Code availability

Our code is available upon request and we plan to post it to FigShare.

References

  • Alexander ME, Kaiser H, Weyl OLF, Dick JTA (2015) Habitat simplification increases the impact of a freshwater invasive fish. Environ Biol Fish 98:477–486

    Article  Google Scholar 

  • Amarasekare P (2015) Effects of temperature on consumer–resource interactions. J Anim Ecol 84:665–679

    Article  PubMed  Google Scholar 

  • Anwer A (ed) (2017) Biopesticides and bioagents: novel tools for pest management. Apple Academic Press, Boca Raton

    Google Scholar 

  • Barrios-O’Neill D, Dick JTA, Emmerson MC, Ricciardi A, MacIsaac HJ (2015) Predator-free space, functional responses and biological invasions. Funct Ecol 29:377–384

    Article  Google Scholar 

  • Bebber DP, Ramotowski MAT, Gurr SJ (2013) Crop pests and pathogens move polewards in a warming world. Nat Clim Change 3:985–988

    Article  Google Scholar 

  • Bergström U, Englund G (2004) Spatial scale, heterogeneity and functional responses. J Anim Ecol 73:487–493

    Article  Google Scholar 

  • Blackman RL, Eastop VF (2000) Aphids on the world’s crops: an identification and information guide. Wiley, Hoboken

    Google Scholar 

  • Brown J, Gillooly J, Allen A, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789

    Article  Google Scholar 

  • Bruce TJA (2010) Tackling the threat to food security caused by crop pests in the new millennium. Food Secur 2:133–141

    Article  Google Scholar 

  • Burnside WR, Erhardt EB, Hammond ST, Brown JH (2014) Rates of biotic interactions scale predictably with temperature despite variation. Oikos 123:1449–1456

    Article  Google Scholar 

  • Calvo FJ, Knapp M, van Houten YM, Hoogerbrugge H, Belda JE (2015) Amblyseius swirskii: what made this predatory mite such a successful biocontrol agent? Exp Appl Acarol 65:419–433

    Article  CAS  PubMed  Google Scholar 

  • Clausen CP (1978) Introduced parasites and predators of arthropod pests and weeds: a world review. Agricultural handbook number 480. U.S. Department of Agriculture, New York

    Google Scholar 

  • Costanza R, d’Arge R, de Groot R, Fraber S, Grasso M, Hannon B, Limburg K, Naeem S, O’Neill RV, Paruelo J, Raskin RG, Sutton P, van den Belt M (1997) The value of the world’s ecosystem services and natural capital. Nature 387:253–260

    Article  CAS  Google Scholar 

  • Cuthbert RN, Dalu T, Wasserman RJ, Callaghan A, Weyl OLF, Dick JTA (2019) Using functional responses to quantify notonectid predatory impacts across increasingly complex environments. Acta Oecol 95:116–119

    Article  Google Scholar 

  • de Brooke ML, Hanley S, Laughlin SB (1999) The scaling of eye size with body mass in birds. Proc R Soc Lond B Biol Sci 266:405–412

    Article  Google Scholar 

  • DeLong JP (2021) Predator ecology: the evolutionary ecology of the functional response. Oxford University Press

    Book  Google Scholar 

  • DeLong JP, Vasseur DA (2012) A dynamic explanation of size-density scaling in carnivores. Ecology 93:470–476

    Article  PubMed  Google Scholar 

  • Devictor V, van Swaay C, Brereton T, Brotons L, Chamberlain D, Heliölä J, Herrando S, Julliard R, Kuussaari M, Lindström Å, Reif J, Roy DB, Schweiger O, Settele J, Stefanescu C, van Strien A, van Turnhout C, Vermouzek Z, WallisDeVries M, Wynhoff I, Jiguet F (2012) Differences in the climatic debts of birds and butterflies at a continental scale. Nat Clim Change 2:121–124

    Article  Google Scholar 

  • Ding-Xu L, Juan T, Zuo-Rui S (2007) Functional response of the predator Scolothrips takahashii to hawthorn spider mite, Tetranychus viennensis: effect of age and temperature. BioControl 52:41–61

    Article  Google Scholar 

  • Englund G, Öhlund G, Hein CL, Diehl S (2011) Temperature dependence of the functional response. Ecol Lett 14:914–921

    Article  PubMed  Google Scholar 

  • Fletcher NH (2004) A simple frequency-scaling rule for animal communication. J Acoust Soc Am 115:2334–2338

    Article  PubMed  Google Scholar 

  • Forster J, Hirst AG, Atkinson D (2012) Warming-induced reductions in body size are greater in aquatic than terrestrial species. Proc Natl Acad Sci 109:19310–19314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gergs A, Ratte HT (2009) Predicting functional response and size selectivity of juvenile Notonecta maculata foraging on Daphnia magna. Ecol Model 220:3331–3341

    Article  Google Scholar 

  • Gilbert B, Tunney TD, McCann KS, DeLong JP, Vasseur DA, Savage V, Shurin JB, Dell AI, Barton BT, Harley CDG, Kharouba HM, Kratina P, Blanchard JL, Clements C, Winder M, Greig HS, O’Connor MI (2014) A bioenergetic framework for the temperature dependence of trophic interactions. Ecol Lett 17:902–914

    Article  PubMed  Google Scholar 

  • Ho C-C (2000) Spider-mite problems and control in Taiwan. Exp Appl Acarol 24:453–462

    Article  CAS  PubMed  Google Scholar 

  • Hoddle MS (2003) The effect of prey species and environmental complexity on the functional response of Franklinothrips Orizabensis: a test of the fractal foraging model. Ecol. Entomol. 28:309–318

    Article  Google Scholar 

  • Holling CS (1959) The components of predation as revealed by a study of small-mammal predation of the European pine sawfly. Can Entomol 91:293–320

    Article  Google Scholar 

  • Hullé M, Cœur d’Acier A, Bankhead-Dronnet S, Harrington R (2010) Aphids in the face of global changes. Comp Rend Biol 333:497–503

    Article  Google Scholar 

  • Islam Y, Shah FM, Shah MA, Khan MM, Rasheed MA, Rehman SU, Ali S, Zhou X (2020) Temperature-dependent functional response of Harmonia axyridis (Coleoptera: Coccinellidae) on the eggs of Spodoptera litura (Lepidoptera: Noctuidae) in laboratory. Insects 11:583

    Article  PubMed Central  Google Scholar 

  • Islam Y, Shah FM, Rubing X, Razag M, Yabo M, Xihong L, Zhou X (2021) Functional response of Harmonia axyridis preying on Acyrthosiphon pisum nymphs: the effect of temperature. Sci Rep 11:13565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeppson LR, Keifer HH, Baker EW (1975) Mites injurious to economic plants. University of California Press

    Book  Google Scholar 

  • Kalinoski RM, DeLong JP (2016) Beyond body mass: how prey traits improve predictions of functional response parameters. Oecologia 180:543–550

    Article  PubMed  Google Scholar 

  • Kiørboe T, Thomas MK (2020) Heterotrophic eukaryotes show a slow-fast continuum, not a gleaner–exploiter trade-off. Proc Natl Acad Sci 117:24893–24899

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Koski ML, Johnson BM (2002) Functional response of kokanee salmon (Oncorhynchus nerka) to Daphnia at different light levels. Can J Fish Aquat Sci 59:707–716

    Article  Google Scholar 

  • Kreuzinger-Janik B, Hüttemann HB, Traunspurger W (2019) Effect of prey size and structural complexity on the functional response in a nematode–nematode system. Sci Rep 9:5696

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kumar B, Omkar (2018) Insect pest management. In: Omkar (ed) Pests and their management. Springer, Singapore, pp 1015–1078

    Chapter  Google Scholar 

  • Kundoo AA, Khan A (2017) Coccinellids as biological control agents of soft bodied insects: a review. J Entomol Zool Stud 5:1362–1373

    Google Scholar 

  • Lang B, Rall BC, Brose U (2012) Warming effects on consumption and intraspecific interference competition depend on predator metabolism. J Anim Ecol 81:516–523

    Article  PubMed  Google Scholar 

  • Lehmann P, Ammunét T, Barton M, Battisti A, Eigenbrode SD, Jepsen JU, Kalinkat G, Neuvonen S, Niemelä P, Terblanche JS, Økland B, Björkman C (2020) Complex responses of global insect pests to climate warming. Front Ecol Environ 18:141–150

    Article  Google Scholar 

  • McGill BJ, Mittelbach GC (2006) An allometric vision and motion model to predict prey encounter rates. Evol Ecol Res 8:691–701

    Google Scholar 

  • Memmott J, Martinez ND, Cohen JE (2000) Predators, parasitoids and pathogens: species richness, trophic generality and body sizes in a natural food web. J Anim Ecol 69:1–15

    Article  Google Scholar 

  • Messina FJ, Hanks JB (1998) Host plant alters the shape of the functional response of an aphid predator (Coleoptera: Coccinellidae). Environ Entomol 27:1196–1202

    Article  Google Scholar 

  • Naranjo SE, Ellsworth PC, Frisvold GB (2015) Economic value of biological control in integrated pest management of managed plant systems. Annu Rev Entomol 60:621–645

    Article  CAS  PubMed  Google Scholar 

  • Naranjo S, Frisvold G, Ellsworth PC (2019) Economic value of arthropod biological control. In: Onstad DW, Crain P (eds) The economics of integrated pest management of insects. CABI, Wallingford, pp 49–85

    Chapter  Google Scholar 

  • Neuenschwander P, Borgemeister C, Langewald J (2003) Biological control in IPM systems in Africa. CABI, Wallingford

    Book  Google Scholar 

  • Oerke E-C (2006) Crop losses to pests. J Agric Sci 144:31–43

    Article  Google Scholar 

  • Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42

    Article  CAS  PubMed  Google Scholar 

  • Rall BC, Brose U, Hartvig M, Kalinkat G, Schwarzmüller F, Vucic-Pestic O, Petchey OL (2012) Universal temperature and body-mass scaling of feeding rates. Philos Trans R Soc B Biol Sci 367:2923–2934

    Article  Google Scholar 

  • Roy S, Muraleedharan N, Mukhopadhyay A (2014) The red spider mite, Oligonychus coffeae (Acari: Tetranychidae): its status, biology, ecology and management in tea plantations. Exp Appl Acarol 63:431–463

    Article  CAS  PubMed  Google Scholar 

  • Singh K (2014) Biocontrol: an overview. Int J Sci Innov Res 2:83–89

    Google Scholar 

  • Singh R, Singh G (2016) Aphids and their biocontrol. In: Omkar (ed) Ecofriendly pest management for food security. Academic Press, San Diego, pp 63–108

    Chapter  Google Scholar 

  • Skendžić S, Zovko M, Živković IP, Lešić V, Lemić D (2021) The impact of climate change on agricultural insect pests. Insects 12:440

    Article  PubMed  PubMed Central  Google Scholar 

  • Solomon ME (1949) The natural control of animal populations. J Anim Ecol 18:1–35

    Article  Google Scholar 

  • Song YH, Heong KL (1997) Changes in searching responses with temperature of Cyrtorhinus lividipennis reuter (Hemiptera: Miridae) on the eggs of the brown planthopper, Nilaparvata lugens (Stål.) (Homoptera: Delphacidae). Popul Ecol 39:201–206

    Article  Google Scholar 

  • Stiling P, Cornelissen T (2005) What makes a successful biocontrol agent? A meta-analysis of biological control agent performance. Biol Control 34:236–246

    Article  Google Scholar 

  • Symondson WOC, Sunderland KD, Greenstone MH (2002) Can generalist predators be effective biocontrol agents? Annu Rev Entomol 47:561–594

    Article  CAS  PubMed  Google Scholar 

  • Thompson DJ (1978) Towards a realistic predator-prey model: the effect of temperature on the functional response and life history of larvae of the damselfly, Ischnura elegans. J Anim Ecol 47:757–767

    Article  Google Scholar 

  • Uiterwaal SF, DeLong JP (2018) Multiple factors, including arena size, shape the functional responses of ladybird beetles. J Appl Ecol 55:2429–2438

    Article  CAS  Google Scholar 

  • Uiterwaal SF, DeLong JP (2020) Functional responses are maximized at intermediate temperatures. Ecology 101:e02975

    Article  PubMed  Google Scholar 

  • Uiterwaal SF, Lagerstrom IT, Lyon SR, DeLong JP (2018) Data paper: FoRAGE (functional responses from around the globe in all ecosystems) database: a compilation of functional responses for consumers and parasitoids. BioRxiv. https://doi.org/10.1101/503334

    Article  Google Scholar 

  • Uiterwaal SF, Dell AI, DeLong JP (2019) Arena size modulates functional responses via behavioral mechanisms. Behav Ecol 30:483–489

    Article  Google Scholar 

  • Uszko W, Diehl S, Englund G, Amarasekare P (2017) Effects of warming on predator–prey interactions—a resource-based approach and a theoretical synthesis. Ecol Lett 20:513–523

    Article  PubMed  Google Scholar 

  • van Emden HF, Harrington R (2017) Aphids as crop pests. CABI, Wallingford

    Book  Google Scholar 

  • van Lenteren JC (2012) The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. BioControl 57:1–20

    Article  Google Scholar 

  • van Lenteren JC, Bolckmans K, Köhl J, Ravensberg WJ, Urbaneja A (2018) Biological control using invertebrates and microorganisms: plenty of new opportunities. BioControl 63:39–59

    Article  Google Scholar 

  • Vucic-Pestic O, Rall BC, Kalinkat G, Brose U (2010) Allometric functional response model: body masses constrain interaction strengths. J Anim Ecol 79:249–256

    Article  PubMed  Google Scholar 

  • Ware DM (1972) Predation by rainbow trout (Salmo gairdneri): the influence of hunger, prey density, and prey size. J Fish Res Board Can 29:1193–1201

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by a National Science Foundation Graduate Research Fellowship to SFU and by a James S. McDonnell Foundation Studying Complex Systems Scholar Award to JPD.

Funding

This work was supported by a National Science Foundation Graduate Research Fellowship (DGE-1610400) and a James S. McDonnell Foundation Studying Complex Systems Scholar Award.

Author information

Authors and Affiliations

Authors

Contributions

Both authors conceived of the work, contributed to analysis, and wrote and edited the paper.

Corresponding author

Correspondence to John P. DeLong.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

Not applicable.

Research involving humans and/or animals

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Additional information

Handling Editor: Marta Montserrat.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

DeLong, J.P., Uiterwaal, S.F. Predator functional responses and the biocontrol of aphids and mites. BioControl 67, 161–172 (2022). https://doi.org/10.1007/s10526-021-10127-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-021-10127-1

Keywords

Navigation