Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-22T18:25:41.699Z Has data issue: false hasContentIssue false
  • English
  • Français

Diet breadth of the aphid predator Chrysoperla rufilabris Burmeister (Neuroptera: Chrysopidae)

Published online by Cambridge University Press:  08 March 2022

Michela C. Batista Open the ORCID record for Michela C. Batista [Opens in a new window] ,
George E. Heimpel Open the ORCID record for George E. Heimpel [Opens in a new window] ,
Mariana Bulgarella Open the ORCID record for Mariana Bulgarella [Opens in a new window]  and
Madelaine Venzon Open the ORCID record for Madelaine Venzon [Opens in a new window]
Michela C. Batista*
Affiliation:
Programa de Pós-Graduação em Agricultura e Ambiente, Universidade Estadual do Maranhão, Balsas, Brazil Departamento de Entomologia, Universidade Federal de Viçosa, Viçosa, Brazil
George E. Heimpel
Affiliation:
Department of Entomology, University of Minnesota, St Paul, USA
Mariana Bulgarella
Affiliation:
School of Biological Sciences, Victoria University of Wellington, Wellington, New Zealand
Madelaine Venzon
Affiliation:
Empresa de Pesquisa Agropecuária de Minas Gerais – EPAMIG, Viçosa, Brazil
*
Author for correspondence: Michela C. Batista, Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The performance (development and reproduction) of generalist predators can vary greatly among the prey species that they use, and these differences can influence the ability of predatory insects to suppress pest populations. The aim of this study was to compare the performance of larvae of the green lacewing Chrysoperla rufilabris (Burmeister, 1839) by offering 16 species of aphids and by assessing the effects of each species on the survival, larval development time, prey consumption, pupal mass and egg load of adult Chr. rufilabris females taking aphid phylogeny into account. Chrysoperla rufilabris larvae preyed on individuals from all 16 aphid species, but complete development, adult emergence and egg load production were achieved only in seven species. As a general pattern, the best levels of performance were achieved for an aphid clade that includes the soybean aphid, Aphis glycines (Matsumara, 1917), and for a milkweed-feeding species, Myzocallis asclepiadis (Monell, 1879). We found significant phylogenetic clustering for most of the performance traits indicating the aspects of specialization in the diet breadth of Chr. rufilabris despite the fact that this species is considered a generalist aphid predator. These findings can help us to understand the interactions of this species in agroecological food webs, where it is commonly found, and provide insights into why natural, conservation biological control or augmentative releases may succeed or fail.

Keywords

Biological controlgeneralist predatorphylogenyprey range
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 112 , Issue 4 , August 2022 , pp. 528 - 535
Check for updates
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abram, PK, Labbe, RM and Mason, PG (2021) Ranking the host range of biological control agents with quantitative metrics of taxonomic specificity. Biological Control 152, 104427.CrossRefGoogle Scholar
Agrawal, AA and Kotanen, PM (2003) Herbivores and the success of exotic plants: a phylogenetically controlled experiment. Ecology Letters 6, 712–715.CrossRefGoogle Scholar
Albuquerque, GS (2009) Crisopídeos (Neuroptera: Chrysopidae). In Panizzi, RA and Parra, JRP (eds), Bioecologia e nutrição de insetos: base para o manejo integrado de pragas. Brasília, BRA: Embrapa Informações Tecnológicas, pp. 969–1022.Google Scholar
Asplen, MK, Bruns, E, David, AS, Denison, RF, Epstein, B, Kaiser, MC, Lacroix, C, Mohl, EK, Quiram, G, Prescott, K, Stanton-Geddes, J, Vincent, JB, Wragg, PD and May, G (2012) Do trade-offs have explanatory power for the evolution of organismal interactions? Evolution 66, 1297–1307.CrossRefGoogle ScholarPubMed
Bilde, T and Toft, S (2001) The value of three cereal aphid species as food for a generalist predator. Physiological Entomology 26, 58–68.Google Scholar
Blomberg, SP, Garland, T Jr and Ives, AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57, 717–745.Google ScholarPubMed
Brooks, SJ (1994) A taxonomic review of the common green lacewing genus Chrysoperla (Neuroptera: Chrysopidae). Bulletin of the British Museum (Natural History). Entomology 63, 137–210.Google Scholar
Brousseau, PM, Gravel, D and Handa, TI (2018) Trait-matching and phylogeny as predictors of predator–prey interactions involving ground beetles. Functional Ecology 32, 192–202.CrossRefGoogle Scholar
Bulgarella, M and Heimpel, GE (2015) Host range and community structure of bird parasites in the genus Philornis (Diptera: Muscidae) on the Island of Trinidad. Ecology and Evolution 5, 3695–3703.CrossRefGoogle ScholarPubMed
Canard, M and Volkovich, TA (2001) Outlines of lacewing development. In Mcewen, PK, New, TR and Whittington, AE (eds), Lacewings in the Crop Environment. New York: Cambridge University Press, pp. 130–154.CrossRefGoogle Scholar
Cavender-Bares, J, Kozak, KH, Fine, PVA and Kembel, SW (2009) The merging of community ecology and phylogenetic biology. Ecology Letters 12, 693–715.CrossRefGoogle ScholarPubMed
Chen, TY and Liu, TX (2001) Relative consumption of three aphid species by the lacewing, Chrysoperla rufilabris, and effects on its development and survival. BioControl 46, 481–491.CrossRefGoogle Scholar
Cohen, AC and Smith, LK (1998) A new concept in artificial diets for Chrysoperla rufilabris: the efficacy of solid diets. Biological Control 13, 49–54.CrossRefGoogle Scholar
Crawley, MJ (2013) The R Book, 2nd Edn. New York: John Wiley and Sons.Google Scholar
Daane, KM (2001) Ecological studies of released lacewings in crops. In Mcewen, PK, New, TR and Whittington, AE (eds), Lacewings in the Crop Environment. New York: Cambridge University Press, pp. 338–350.CrossRefGoogle Scholar
Desneux, N, Barta, RJ, Hoelmer, KA, Hopper, KR and Heimpel, GE (2009) Multifaceted determinants of host specificity in an aphid parasitoid. Oecologia 160, 387–398.CrossRefGoogle Scholar
Desneux, N, Blahnik, R, Delebecque, CJ and Heimpel, GE (2012) Host phylogeny and specialisation in parasitoids. Ecology Letters 15, 453–460.CrossRefGoogle ScholarPubMed
Dhandapani, N, Pallavi, S and Mishra, G (2016) Chrysopids. In Omkar, (ed.), Ecofriendly Pest Management for Food Security. San Diego, USA: Elsevier, pp. 331–327.Google Scholar
Eklof, A and Stouffer, DB (2016) The phylogenetic component of food web structure and intervality. Theoretical Ecology 9, 107–115.CrossRefGoogle Scholar
Erb, M and Robert, CAM (2016) Sequestration of plant secondary metabolites by insect herbivores: molecular mechanisms and ecological consequences. Current Opinion in Insect Science 14, 8–11.CrossRefGoogle ScholarPubMed
Forister, ML, Dyer, LA, Singer, MS, Stireman, JO and Lill, JT (2012) Revisiting the evolution of ecological specialization, with emphasis on insect-plant interactions. Ecology 93, 981–991.CrossRefGoogle ScholarPubMed
Futuyma, DJ and Moreno, G (1988) The evolution of ecological specialization. Annual Review of Ecology, Evolution and Systematics 19, 207–233.CrossRefGoogle Scholar
Giles, KL, Madden, RD, Payton, ME and Dillwith, JW (2000) Survival and development of Chrysoperla rufilabris (Neuroptera: Chrysopidae) supplied with pea aphids (Homoptera: Aphididae) reared on alfalfa and faba bean. Environmental Entomology 29, 304–311.CrossRefGoogle Scholar
Goodheart, JA, Bazinet, AL, Valdés, A, Collins, AG and Cummings, MP (2017) Prey preference follows phylogeny: evolutionary dietary patterns within the marine gastropod group Cladobranchia (Gastropoda: Heterobranchia: Nudibranchia). BMC Evolutionary Biology 17, 221.CrossRefGoogle ScholarPubMed
Gordon, ERL and Weirauch, CE (2016) Efficient capture of natural history data reveals prey conservatism of cryptic termite predators. Molecular Phylogenetics and Evolution 94, 65–73.CrossRefGoogle ScholarPubMed
Hagenbucher, S, Wäckers, FL and Romeis, J (2014) Indirect multi-trophic interactions mediated by induced plant resistance: impact of caterpillar feeding on aphid parasitoids. Biology Letters 10, 20130795.CrossRefGoogle ScholarPubMed
Heimpel, GE and Mills, NJ (2017) Biological Control: Ecology and Applications. Cambridge, UK: Cambridge University Press.CrossRefGoogle Scholar
Heimpel, GE, Abram, PK and Brodeur, J (2021) A phylogenetic perspective on parasitoid host ranges with implications for biological control. Current Opinion in Insect Science 44, 95–100.CrossRefGoogle ScholarPubMed
Helms, SE, Connelly, SJ and Hunter, MD (2004) Effects of variation among plant species on the interaction between a herbivore and its parasitoid. Ecological Entomology 29, 44–51.CrossRefGoogle Scholar
Hydorn, S and Whitcomb, WH (1979) Effects of larval diets on Chrysopa rufilabris. Florida Entomologist 62, 293–298.CrossRefGoogle Scholar
Khuhro, N, Chen, H, Zhang, Y, Zhang, L and Wang, M (2012) Effect of different prey species on the life history parameters of Chrysoperla sinica (Neuroptera: Chrysopidae). European Journal of Entomology 109, 175–180.CrossRefGoogle Scholar
Legaspi, JC, Carruthers, RI and Nordlund, DA (1994) Life history of Chrysoperla rufilabris (Neuroptera: Chrysopidae) provided sweetpotato whitefly Bemisia tabaci (Homoptera: Aleyrodidae) and other food. Biological Control 4, 178–184.CrossRefGoogle Scholar
Leppla, NC, Johnson, MW, Merritt, JL and Zalom, FG (2018) Applications and trends in commercial biological control for arthropod pests of tomato. In Wakil, W, Brust, GE and Perring, TM (eds), Sustainable Management of Arthropod Pests of Tomato. Cambridge, USA: Academic Press, pp. 283–303.CrossRefGoogle Scholar
Martel, JW and Malcolm, SB (2004) Density-dependent reduction and induction of milkweed cardenolides by a sucking insect herbivore. Journal of Chemical Ecology 30, 545–561.CrossRefGoogle ScholarPubMed
Michalko, R, Pekár, S and Entling, MH (2019) An updated perspective on spiders as generalist predators in biological control. Oecologia 189, 21–36.CrossRefGoogle ScholarPubMed
Mohl, EK, Stenoien, CM and Heimpel, GE (2020) The effects of host plant species on adult oviposition and larval performance of the aphid predator Aphidoletes aphidimyza. Ecological Entomology 45, 606–616.CrossRefGoogle Scholar
Monticelli, LS, Le Thu Ha, N, Amiens-Desneux, E, Luo, C, Lavoir, A-V, Gatti, J-L and Desneux, N (2019) The preference-performance relationship as a means of classifying parasitoids according to their specialization degree. Evolutionary Applications 12, 1626–1640.CrossRefGoogle ScholarPubMed
Monticelli, LS, Desneux, N and Heimpel, GE (2021) Parasitoid-mediated indirect interactions between unsuitable and suitable hosts generate apparent predation in microcosm and modeling studies. Ecology and Evolution 11, 2449–2460.CrossRefGoogle ScholarPubMed
Mooney, KA, Jones, P and Agrawal, AA (2008) Coexisting congeners: demography, competition, and interactions with cardenolides for two milkweed-feeding aphids. Oikos 117, 450–458.CrossRefGoogle Scholar
Opitz, SW and Müller, C (2009) Plant chemistry and insect sequestration. Chemoecology 19, 117–154.CrossRefGoogle Scholar
Pappas, ML, Broufas, GD and Koveos, DS (2007) Effects of various prey species on development, survival and reproduction of the predatory lacewing Dichochrysa prasina (Neuroptera: Chrysopidae). Biological Control 43, 163–170.CrossRefGoogle Scholar
Pappas, ML, Broufas, GD and Koveos, DS (2011) Chrisopid predators and their role in biological control. Journal of Entomology 8, 301–326.CrossRefGoogle Scholar
Perring, TM, Stansly, PA, Liu, TX, Smith, HA and Andreason, SA (2018) Whiteflies: biology, ecology, and management. In Wakil, W, Brust, GE and Perring, TM (eds), Sustainable Management of Arthropod Pests of Tomato. Cambridge, USA: Academic Press, pp. 73–110.CrossRefGoogle Scholar
Poreddy, S, Mitra, S, Schöttner, M, Chandran, J, Schneider, B, Baldwin, IT, Kumar, P and Pandit, SS (2015) Detoxification of hostplant's chemical defence rather than its anti-predator co-option drives [beta]-glucosidase-mediated lepidopteran counteradaptation. Nature Communications 6, 8525.CrossRefGoogle ScholarPubMed
R Development Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria URL https://www.R-project.org/.Google Scholar
Rana, JS, Dixon, AFG and Jarosik, V (2002) Costs and benefits of prey specialization in a generalist insect predator. Journal of Animal Ecology 71, 15–22.CrossRefGoogle Scholar
Straub, CS, Ives, AR and Gratton, C (2011) Evidence for a trade-off between host-range breadth and host-use efficiency in aphid parasitoids. American Naturalist 177, 389–395.CrossRefGoogle ScholarPubMed
Symondson, WOC, Sunderland, KD and Greenstone, MH (2002) Can generalist predators be effective biocontrol agents? Plant Science 47, 561–594.Google ScholarPubMed
Tauber, MJ, Tauber, CA, Daane, KM and Hagen, KS (2000) Commercialization of predators: recent lessons from green lacewings (Neuroptera: Chrysopidae: Chrysoperla). American Entomologist 46, 26–38.CrossRefGoogle Scholar
Toft, S (2005) The quality of aphids as food for generalist predators: implications for natural control of aphids. European Journal of Entomology 102, 371–383.CrossRefGoogle Scholar
Tscharntke, T, Bommarco, R, Clough, Y, Crist, TO, Kleijn, D, Rand, TA, Tylianakis, JM, van Nouhuys, S and Vidal, S (2007) Conservation biological control and enemy diversity on a landscape scale. Biological Control 43, 294–309.CrossRefGoogle Scholar
van Driesche, R, Hoddle, M and Center, T (2008) Control of Pests and Weeds by Natural Enemies: An Introduction to Biological Control. Victoria, AUS: Blackwell Publishing Ltd.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.CrossRefGoogle Scholar
Woolfolk, SW, Cohen, AC and Inglis, GD (2004) Morphology of the alimentary canal of Chrysoperla rufilabris (Neuroptera: Chrysopidae) adults in relation to microbial symbionts. Annals of the Entomological Society of America 97, 796–808.CrossRefGoogle Scholar