Agroecology; Biodiversity conservation; Biodiversity – ecosystem functioning; Functional ecology; Species richness; Parasitoids; Predators; Entomopathogenic Fungi; Biological control
Abstract :
[en] Ecosystem functions such as biological pest control are mediated by the richness and abundance of service providers i.e., biological control agents (BCAs), relative contributions of individual taxa and community structure. This is especially relevant in the native range of agricultural herbivores, where a speciose community of co-evolved BCAs can prevent them from attaining pest status. Here, we use a powerful graphical approach to assess the functional structure of BCA communities of the fall armyworm (FAW) Spodoptera frugiperda (Lepidoptera: Noctuidae) on maize in the Neotropics. Drawing upon a curated database of all-time field and laboratory studies, we graphed patterns in the functional contribution, abundance and niche breadth for a respective 69, 53 and 3 taxa of resident parasitoids, predators and pathogens. Regardless of varying taxon coverage and rigor of the underlying studies, functional structure follows a saturating relationship in which the first three taxa account for 90–98% of aggregate biological control function. Abundance-functionality matrices prove critically incomplete, as more than 80% of invertebrate taxa miss empirically derived efficiency metrics while associated FAW infestation data are scarce. Despite its methodological shortfalls and data gaps, our work pinpoints Chelonus insularis, several taxa of egg parasitoids, Doru spp. and Orius spp. as taxa with outsized (average) functionality and conservation potential. This is also exemplified by the highly variable aggregate function across studies, with dispersion indices of 1.52 and 2.14 for invertebrate BCAs. Our work underlines the critical importance of functional ecology research, networked trials and standardized methodologies in advancing conservation biological control globally.
Disciplines :
Entomology & pest control
Author, co-author :
Wyckhuys, Kris A.G. ; Chrysalis Consulting, Danang, Viet Nam ; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China ; School of the Environment, University of Queensland, Saint Lucia, Australia ; Food and Agriculture Organization (FAO), Rome, Italy
Akutse, Komivi S.; International Centre of Insect Physiology and Ecology (icipe), Nairobi, Kenya ; Unit for Environmental Sciences and Management, North-West University, Potchefstroom, South Africa
Amalin, Divina M.; De La Salle University, Manila, Philippines
Araj, Salah-Eddin; School of Agriculture, The University of Jordan, Amman, Jordan
Barrera, Gloria; Centro de Investigación Tibaitatá, Corporación Colombiana de Investigación Agropecuaria - Agrosavia, Mosquera, Colombia
Joy B. Beltran, Marie; National Crop Protection Center, University of the Philippines Los Baños, Laguna, Philippines
Ben Fekih, Ibtissem ; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs
Calatayud, Paul-André; International Centre of Insect Physiology and Ecology (icipe), Nairobi, Kenya ; Institut Diversité Ecologie et Evolution du Vivant (IDEEV), Université Paris-Saclay, CNRS, IRD, UMR Evolution, Génomes, Comportement et Ecologie, Gif‑sur‑Yvette, France
Cicero, Lizette; Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias (INIFAP), Yucatán, Mexico
Espinel, Carlos; Centro de Investigación Tibaitatá, Corporación Colombiana de Investigación Agropecuaria - Agrosavia, Mosquera, Colombia
Fernández-Triana, José L.; Canadian National Collection of Insects, Arachnids and Nematodes, Agriculture and Agri-Food Canada, Ottawa, Canada
Francis, Frédéric ; Université de Liège - ULiège > TERRA Research Centre > Gestion durable des bio-agresseurs
Gómez, Juliana; Centro de Investigación Tibaitatá, Corporación Colombiana de Investigación Agropecuaria - Agrosavia, Mosquera, Colombia
Haddi, Khalid; Laboratory of Molecular Entomology and Ecotoxicology, Department of Entomology, Universidade Federal de Lavras, Brazil
Harrison, Rhett D.; CIFOR-ICRAF, Lusaka, Gambia
Haseeb, Muhammad; Center for Biological Control, Florida A&M University, Tallahassee, United States
Iwanicki, Natasha S.A.; Luiz de Queiroz College of Agriculture, University of São Paulo, Piracicaba, São Paulo, Brazil
Jaber, Lara R.; School of Agriculture, The University of Jordan, Amman, Jordan
Khamis, Fathiya M.; International Centre of Insect Physiology and Ecology (icipe), Nairobi, Kenya
Legaspi, Jesusa C.; United States Department of Agriculture-Agricultural Research Service (USDA-ARS), Center for Medical, Agricultural and Medical Entomology, Tallahassee, United States
Lomeli-Flores, Refugio J.; Posgrado en Fitosanidad, Colegio de Postgraduados, Montecillo, Mexico
Lopes, Rogerio B.; EMBRAPA Genetic Resources and Biotechnology, Brazil
Lyu, Baoqian; China Academy of Tropical Agricultural Sciences (CATAS), Haikou, China
Montoya-Lerma, James; Department of Biology, Universidad del Valle, Cali, Colombia
Nguyen, Tung D.; Vietnam National University of Agriculture, Hanoi, Viet Nam
Nurkomar, Ihsan; Universitas Muhammadiyah Yogyakarta, Indonesia
Perier, Jermaine D.; Department of Entomology, University of Georgia, Tifton, United States
Pozsgai, Gabor; cE3c - Centre for Ecology, Evolution and Environmental Changes & CHANGE - Global Change and Sustainability Institute, University of the Azores, Angra do Heroísmo, Portugal
Ramírez-Romero, Ricardo; Biological Control Laboratory (LabCB-AIFEN), University of Guadalajara, Guadalajara, Mexico
Robinson-Baker, Annmarie S.; Center for Biological Control, Florida A&M University, Tallahassee, United States
Sanchez-Garcia, Francisco J.; Instituto Murciano de Investigación y Desarrollo Agrario y Alimentario (IMIDA), Murcia, Spain
Silveira, Luis C.; Laboratory of Molecular Entomology and Ecotoxicology, Department of Entomology, Universidade Federal de Lavras, Brazil
Simeon, Larisner; Center for Biological Control, Florida A&M University, Tallahassee, United States
Solter, Leellen F.; Illinois Natural History Survey, Prairie Research Institute, University of Illinois, Champaign, United States
Santos-Amaya, Oscar F.; Department of Agronomy, Universidad de Pamplona, Pamplona, Colombia
de Souza Tavares, Wagner; Riau Andalan Pulp and Paper (RAPP), Riau, Indonesia
Trabanino, Rogelio; Zamorano, Apartado Postal 93, Tegucigalpa, Honduras
Vásquez, Carlos; Faculty of Agronomical Sciences, Technical University of Ambato, Province of Tungurahua, Cevallos, Ecuador
Wang, Zhenying; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
Wengrat, Ana P.G.S.; Luiz de Queiroz College of Agriculture, University of São Paulo, Piracicaba, São Paulo, Brazil
Zang, Lian-Sheng; National Key Laboratory of Green Pesticide, Key Laboratory of Green Pesticide and Agricultural Bioengineering, Guizhou University, Guiyang, China
Zhang, Wei; National Key Laboratory of Green Pesticide, Key Laboratory of Green Pesticide and Agricultural Bioengineering, Guizhou University, Guiyang, China
Zimba, Kennedy J.; School of Agricultural Sciences, University of Zambia, Lusaka, Gambia
Wu, Kongming; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
Elkahky, Maged; Food and Agriculture Organization (FAO), Rome, Italy
This work was funded by the European Commission through project GCP/GLO/220/EC and executed by the United Nations Food and Agriculture Organization (FAO). Drawings of predators and parasitoids were produced by Visuals in Science LAB. We wish to thank two anonymous reviewers for their valuable comments and suggestions on an earlier draft.
Alhadidi, S.N., Fowler, M.S., Griffin, J.N., Functional diversity of predators and parasitoids does not explain aphid biocontrol efficiency. BioControl 64 (2019), 303–313.
Altieri, M.A., Diversification of corn agroecosystems as a means of regulating fall armyworm populations. Fla. Entomol., 1980, 450–457.
Andrews, K.L., The whorlworm, Spodoptera frugiperda. Central America and neighboring areas. Fla. Entomol. 63:4 (1980), 456–467.
Aragón-Sánchez, M., Román-Fernández, L.R., Martínez-García, H., Aragón-García, A., Pérez-Moreno, I., Marco-Mancebón, V.S., Rate of consumption, biological parameters, and population growth capacity of Orius laevigatus fed on Spodoptera exigua. BioControl 63 (2018), 785–794.
Balvanera, P., Kremen, C., Martínez-Ramos, M., Applying community structure analysis to ecosystem function: examples from pollination and carbon storage. Ecol. Appl. 15:1 (2005), 360–375.
Baudron, F., Zaman-Allah, M.A., Chaipa, I., Chari, N., Chinwada, P., Understanding the factors influencing fall armyworm (Spodoptera frugiperda JE Smith) damage in African smallholder maize fields and quantifying its impact on yield. A case study in Eastern Zimbabwe. Crop Prot. 120 (2019), 141–150.
Begg, G.S., Cook, S.M., Dye, R., Ferrante, M., Franck, P., Lavigne, C., et al. A functional overview of conservation biological control. Crop Prot. 97 (2017), 145–158.
Bellone, D., Björkman, C., Klapwijk, M.J., Top-down pressure by generalist and specialist natural enemies in relation to habitat heterogeneity and resource availability. Basic Appl. Ecol. 43 (2020), 16–26.
Cardinale, B.J., Harvey, C.T., Gross, K., Ives, A.R., Biodiversity and biocontrol: emergent impacts of a multi-enemy assemblage on pest suppression and crop yield in an agroecosystem. Ecol. Lett. 6:9 (2003), 857–865.
Cave, R.D., Biology, ecology and use in pest management of Telenomus remus. Biocontrol News and Information 21:1 (2000), 21N–N26.
Colmenarez, Y. C., Babendreier, D., Ferrer Wurst, F. R., Vásquez-Freytez, C. L., & de Freitas Bueno, A. (2022). The use of Telenomus remus (Nixon, 1937)(Hymenoptera: Scelionidae) in the management of Spodoptera spp.: potential, challenges and major benefits. CABI Agriculture and Bioscience, 3(1), 5.
Dainese, M., Martin, E.A., Aizen, M.A., Albrecht, M., Bartomeus, I., Bommarco, R., et al. A global synthesis reveals biodiversity-mediated benefits for crop production. Sci. Adv., 5(10), 2019, eaax0121.
Delattre, T., Memah, M.M., Franck, P., Valsesia, P., Lavigne, C., Best organic farming expansion scenarios for pest control: a modeling approach. Peer Community Journal, 3, 2023.
Denoth, M., Frid, L., Myers, J.H., Multiple agents in biological control: improving the odds?. Biol. Control 24:1 (2002), 20–30.
Dequech, S.T.B., Camera, C., Sturza, V.S., Ribeiro, L.D.P., Querino, R.B., Poncio, S., Population fluctuation of Spodoptera frugiperda eggs and natural parasitism by Trichogramma in maize. Acta Sci. Agron. 35 (2013), 295–300.
Di, N., Zhang, K., Xu, Q., Zhang, F., Harwood, J.D., Wang, S., Desneux, N., Predatory ability of Harmonia axyridis (Coleoptera: Coccinellidae) and Orius sauteri (Hemiptera: Anthocoridae) for suppression of fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae). Insects, 12(12), 2021, 1063.
Diaz, R., Knutson, A., Bernal, J.S., Effect of the red imported fire ant on cotton aphid population density and predation of bollworm and beet armyworm eggs. J. Econ. Entomol. 97:2 (2004), 222–229.
Eschen, R., Beale, T., Bonnin, J.M., Constantine, K.L., Duah, S., Finch, E.A., et al. Towards estimating the economic cost of invasive alien species to African crop and livestock production. CABI Agriculture and Bioscience 2 (2021), 1–18.
Faria, M., Souza, D.A., Sanches, M.M., Schmidt, F.G.V., Oliveira, C.M., Benito, N.P., Lopes, R.B., Evaluation of key parameters for developing a Metarhizium rileyi-based biopesticide against Spodoptera frugiperda (Lepidoptera: Noctuidae) in maize: laboratory, greenhouse, and field trials. Pest Manag. Sci. 78:3 (2022), 1146–1154.
Figueiredo, M.D.L.C., Cruz, I., Da Silva, R.B., Foster, J.E., Biological control with Trichogramma pretiosum increases organic maize productivity by 19.4%. Agron. Sustain. Dev. 35 (2015), 1175–1183.
Frank, S.D., Shrewsbury, P.M., Denno, R.F., Plant versus prey resources: Influence on omnivore behavior and herbivore suppression. Biol. Control 57:3 (2011), 229–235.
Gardarin, A., Pigot, J., Valantin-Morison, M., The hump-shaped effect of plant functional diversity on the biological control of a multi-species pest community. Sci. Rep., 11(1), 2021, 21635.
Gardiner, M.M., Landis, D.A., Gratton, C., DiFonzo, C.D., O'Neal, M., et al. Landscape diversity enhances biological control of an introduced crop pest in the north-central USA. Ecol. Appl. 19:1 (2009), 143–154.
Goergen, G., Kumar, P.L., Sankung, S.B., Togola, A., Tamò, M., First report of outbreaks of the fall armyworm Spodoptera frugiperda (JE Smith)(Lepidoptera, Noctuidae), a new alien invasive pest in West and Central Africa. PLoS One, 11(10), 2016, e0165632.
González-Chang, M., Tiwari, S., Sharma, S., Wratten, S.D., Habitat management for pest management: limitations and prospects. Ann. Entomol. Soc. Am. 112:4 (2019), 302–317.
González-Chang, M., Wratten, S.D., Shields, M.W., Costanza, R., Dainese, M., Gurr, G.M., et al. Understanding the pathways from biodiversity to agro-ecological outcomes: A new, interactive approach. Agr Ecosyst Environ, 301, 2020, 107053.
Griffin, J.N., Byrnes, J.E., Cardinale, B.J., Effects of predator richness on prey suppression: a meta-analysis. Ecology 94:10 (2013), 2180–2187.
Gross, H.R. Jr., Pair, S.D., The fall armyworm: Status and expectations of biological control with parasitoids and predators. Fla. Entomol. 69 (1986), 502–515.
Gu, M., Tian, J., Lou, Y., Ran, J., Mohamed, A., Keyhani, N.O., et al. Efficacy of Metarhizium rileyi granules for the control of Spodoptera frugiperda and its synergistic effects with chemical pesticide, sex pheromone and parasitoid. Entomologia Generalis, 43(6), 2023.
Gurr, G.M., Wratten, S.D., Landis, D.A., You, M., Habitat management to suppress pest populations: progress and prospects. Annu. Rev. Entomol. 62 (2017), 91–109.
Harrison, P.A., Berry, P.M., Simpson, G., Haslett, J.R., Blicharska, M., Bucur, M., Dunford, R., Egoh, B., Garcia-Llorente, M., Geamana, N., Geertsema, W., Lommelen, E., Meiresonne, L., Turkelboom, F., Linkages between biodiversity attributes and ecosystem services: A systematic review. Ecosyst. Serv. 9 (2014), 191–203.
Iuliano, B., Gratton, C., Temporal resource (dis) continuity for conservation biological control: From field to landscape scales. Frontiers in Sustainable Food Systems, 4, 2020, 127.
Janssen, A., van Rijn, P.C., Pesticides do not significantly reduce arthropod pest densities in the presence of natural enemies. Ecol. Lett. 24:9 (2021), 2010–2024.
Jones, J.A., Driscoll, C.T., Long-term ecological research on ecosystem responses to climate change. Bioscience 72:9 (2022), 814–826.
Karp, D.S., Chaplin-Kramer, R., Meehan, T.D., Martin, E.A., DeClerck, F., Grab, H., et al. Crop pests and predators exhibit inconsistent responses to surrounding landscape composition. Proc. Natl. Acad. Sci. 115:33 (2018), E7863–E7870.
Kenis, M., Prospects for classical biological control of Spodoptera frugiperda (Lepidoptera: Noctuidae) in invaded areas using parasitoids from the Americas. J. Econ. Entomol. 116:2 (2023), 331–341.
Kenis, M., Du Plessis, H., Van den Berg, J., Ba, M.N., Goergen, G., et al. Telenomus remus, a candidate parasitoid for the biological control of Spodoptera frugiperda in Africa, is already present on the continent. Insects, 10(4), 2019, 92.
Kenis, M., Benelli, G., Biondi, A., Calatayud, P.A., Day, R., Desneux, N., et al. Invasiveness, biology, ecology, and management of the fall armyworm, Spodoptera frugiperda. Entomologia Generalis 43 (2023), 187–241.
Kleijn, D., Bommarco, R., Fijen, T.P., Garibaldi, L.A., Potts, S.G., Van Der Putten, W.H., Ecological intensification: bridging the gap between science and practice. Trends Ecol. Evol. 34:2 (2019), 154–166.
Kremen, C., Managing ecosystem services: What do we need to know about their ecology?. Ecol. Lett. 8 (2005), 468–479.
Landis, D.A., Wratten, S.D., Gurr, G.M., Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu. Rev. Entomol. 45:1 (2000), 175–201.
Letourneau, D.K., Bothwell Allen, S.G., Stireman, J.O. III, Perennial habitat fragments, parasitoid diversity and parasitism in ephemeral crops. J. Appl. Ecol. 49:6 (2012), 1405–1416.
Letourneau, D.K., Bothwell Allen, S.G., Kula, R.R., Sharkey, M.J., Stireman, J.O. III, Habitat eradication and cropland intensification may reduce parasitoid diversity and natural pest control services in annual crop fields. Elementa, 3, 2015, 000069.
Luck, G.W., Harrington, R., Harrison, P.A., Kremen, C., Berry, P.M., Bugter, R., et al. Quantifying the contribution of organisms to the provision of ecosystem services. Bioscience 59:3 (2009), 223–235.
Lundgren, J.G., Fausti, S.W., Trading biodiversity for pest problems. Sci. Adv., 1(6), 2015, e1500558.
Macfadyen, S., Craze, P.G., Polaszek, A., van Achterberg, K., Memmott, J., Parasitoid diversity reduces the variability in pest control services across time on farms. Proc. R. Soc. B Biol. Sci. 278:1723 (2011), 3387–3394.
Michalko, R., Pekár, S., Different hunting strategies of generalist predators result in functional differences. Oecologia 181 (2016), 1187–1197.
Miller, K.E., Aguilera, G., Bommarco, R., Roslin, T., Land-use intensity affects the potential for apparent competition within and between habitats. J. Anim. Ecol. 90:8 (2021), 1891–1905.
Mitchell, M.G., Qiu, J., Cardinale, B.J., Chan, K.M., Eigenbrod, F., Felipe-Lucia, M.R., Jacob, A.L., Jones, M.S., Sonter, L.J., Key questions for understanding drivers of biodiversity-ecosystem service relationships across spatial scales. Landsc. Ecol., 39(2), 2024, 36.
Moeller, N.I., Analysis of funding flows to agroecology: the case of European Union monetary flows to the United Nations’ Rome-based agencies and the case of the Green Climate Fund. Cooperation Internationale pour le Développement et la Solidarité, 2020, Iowa Cooperative Service Special Report, vol, 52.
Molina-Ochoa, J., Carpenter, J.E., Lezama-Gutiérrez, R., Foster, J.E., González-Ramírez, M., Angel-Sahagún, C.A., Farías-Larios, J., Natural distribution of hymenopteran parasitoids of Spodoptera frugiperda (Lepidoptera: Noctuidae) larvae in Mexico. Fla. Entomol. 87:4 (2004), 461–472.
Mouillot, D., Villéger, S., Scherer-Lorenzen, M., Mason, N.W., Functional structure of biological communities predicts ecosystem multifunctionality. PLoS One, 6(3), 2011, e17476.
Murúa, G., Molina-Ochoa, J., Coviella, C., Population dynamics of the fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae) and its parasitoids in Northwestern Argentina. Fla. Entomol. 89:2 (2006), 175–182.
Naranjo, S.E., Ellsworth, P.C., Frisvold, G.B., Economic value of biological control in integrated pest management of managed plant systems. Annu. Rev. Entomol. 60 (2015), 621–645.
Naranjo, S.E., Cañas, L., Ellsworth, P.C., Mortality dynamics of a polyphagous invasive herbivore reveal clues in its agroecosystem success. Pest Manag. Sci. 78:10 (2022), 3988–4005.
Naranjo-Guevara, N., Peñaflor, M.F.G., Cabezas-Guerrero, M.F., Bento, J.M.S., Nocturnal herbivore-induced plant volatiles attract the generalist predatory earwig Doru luteipes Scudder. The Science of Nature 104 (2017), 1–11.
O'Connor, M.I., Gonzalez, A., Byrnes, J.E., Cardinale, B.J., Duffy, J.E., Gamfeldt, L., Griffin, J.N., Hooper, D., Hungate, B.A., Paquette, A., et al. A general biodiversity–function relationship is mediated by trophic level. Oikos 126:1 (2017), 18–31.
Ordóñez-García, M., Rios-Velasco, C., Berlanga-Reyes, D.I., Acosta Muñiz, C.H., Salas-Marina, M.A., Cambero-Campos, O.J., Occurrence of natural enemies of Spodoptera frugiperda (Lepidoptera: Noctuidae) in Chihuahua. Mexico. Florida Entomologist 98:3 (2015), 843–847.
Overton, K., Maino, J.L., Day, R., Umina, P.A., Bett, B., Carnovale, D., et al. Global crop impacts, yield losses and action thresholds for fall armyworm (Spodoptera frugiperda): A review. Crop Prot., 145, 2021, 105641.
Pacheco, R.C., Silva, D.D., Mendes, S.M., Lima, K.P., Figueiredo, J.E.F., Marucci, R.C., How omnivory affects the survival and choices of earwig Doru luteipes (Scudder)(Dermaptera: Forficulidae)?. Braz. J. Biol., 83, 2021, e243890.
Pavageau, C., Pondini, S., Geck, M., Money flows: what is holding back investment in agroecological research for Africa?. Zürich: Biovision Foundation for Ecological Development & International Panel of Experts on Sustainable Food Systems, 2020.
Perennes, M., Diekötter, T., Hoffmann, H., Martin, E.A., Schröder, B., Burkhard, B., Modelling potential natural pest control ecosystem services provided by arthropods in agricultural landscapes. Agr Ecosyst Environ, 342, 2023, 108250.
Perez-Alvarez, R., Grab, H., Polyakov, A., Poveda, K., Landscape composition mediates the relationship between predator body size and pest control. Ecol. Appl., 31(6), 2021, e02365.
Perfecto, I., Indirect and direct effects in a tropical agroecosystem: the maize-pest-ant system in Nicaragua. Ecology 71:6 (1990), 2125–2134.
Perović, D.J., Gámez-Virués, S., Landis, D.A., Wäckers, F., Gurr, G.M., Wratten, S.D., You, M.S., Desneux, N., Managing biological control services through multi-trophic trait interactions: review and guidelines for implementation at local and landscape scales. Biol. Rev. 93:1 (2018), 306–321.
Poelen, J.H., Simons, J.D., Mungall, C.J., Global biotic interactions: An open infrastructure to share and analyze species-interaction datasets. Eco. Inform. 24 (2014), 148–159.
Power, M.E., Tilman, D., Estes, J.A., Menge, B.A., Bond, W.J., Mills, L.S., Daily, G., Castilla, J.C., Lubchenco, J., Paine, R.T., Challenges in the quest for keystones. Bioscience 46:8 (1996), 609–620.
Pratissoli, D., Thuler, R.T., Pereira, F.F., Reis, E.F.D., Ferreira, A.T., Ação transovariana de lufenuron (50 G/L) sobre adultos de Spodoptera frugiperda (JE Smith)(Lepidoptera: Noctuidae) e seu efeito sobre o parasitóide de ovos Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae). Ciência e Agrotecnologia 28 (2004), 9–14.
Quispe, R., Mazón, M., Rodríguez-Berrío, A., Do refuge plants favour natural pest control in maize crops?. Insects, 8(3), 2017, 71.
Redoan, A.C.M., Carvalho, G.A., Cruz, I., Figueiredo, M.D.L.C., Silva, R.B.D., Physiological selectivity of insecticides to adult of Doru luteipes (Scudder, 1876) (Dermaptera: Forficulidae). Rev. Ciênc. Agron. 44 (2013), 842–850.
Risch, S.J., Carroll, C.R., Effect of a keystone predaceous ant, Solenopsis geminata, on arthropods in a tropical agroecosystem. Ecology, 1982, 1979–1983.
Ritchie, S.W., Hanway, J.J., Benson, G.O., How a corn plant develops. Revised edition, 1986, Iowa Cooperative Service Special Report, vol, 48.
Rodriguez, M.A., Hawkins, B.A., Diversity, function and stability in parasitoid communities. Ecol. Lett. 3:1 (2000), 35–40.
Rosenheim, J., Corbett, A., Omnivory and the indeterminacy of predator function: can a knowledge of foraging behavior help?. Ecology 84:10 (2003), 2538–2548.
Rosenheim, J.A., Kaya, H.K., Ehler, L.E., Marois, J.J., Jaffee, B.A., Intraguild predation among biological control agents: theory and evidence. Biol. Control 5:3 (1995), 303–335.
Sanders, D., Vogel, E., Knop, E., Individual and species-specific traits explain niche size and functional role in spiders as generalist predators. J. Anim. Ecol. 84:1 (2015), 134–142.
Settele, J., Settle, W.H., Conservation biological control: Improving the science base. Proc. Natl. Acad. Sci. 115:33 (2018), 8241–8243.
Spiegal, S., Bestelmeyer, B.T., Archer, D.W., Augustine, D.J., Boughton, E.H., et al. Evaluating strategies for sustainable intensification of US agriculture through the Long-Term Agroecosystem Research network. Environ. Res. Lett., 13(3), 2018, 034031.
Straub, C.S., Finke, D.L., Snyder, W.E., Are the conservation of natural enemy biodiversity and biological control compatible goals?. Biol. Control 45 (2008), 225–237.
Straub, C.S., Snyder, W.E., Species identity dominates the relationship between predator biodiversity and herbivore suppression. Ecology 87:2 (2006), 277–282.
Tambo, J.A., Day, R.K., Lamontagne-Godwin, J., Silvestri, S., Beseh, P.K., Oppong-Mensah, B., et al. Tackling fall armyworm (Spodoptera frugiperda) outbreak in Africa: an analysis of farmers’ control actions. International Journal of Pest Management 66:4 (2020), 298–310.
Tamburini, G., Bommarco, R., Wanger, T.C., Kremen, C., Van Der Heijden, M.G., Liebman, M., Hallin, S., Agricultural diversification promotes multiple ecosystem services without compromising yield. Sci. Adv., 6(45), 2020, eaba1715.
Tavares, W.S., Cruz, I., Silva, R.B., Serrão, J.E., Zanuncio, J.C., Prey consumption and development of Chrysoperla externa (Neuroptera: Chrysopidae) on Spodoptera frugiperda (Lepidoptera: Noctuidae) eggs and larvae and Anagasta kuehniella (Lepidoptera: Pyralidae) eggs. Maydica, 56(3), 2011, 283.
Tepa-Yotto, G.T., Tonnang, H.E., Goergen, G., Subramanian, S., Kimathi, E., et al. Global habitat suitability of Spodoptera frugiperda (JE Smith)(Lepidoptera, Noctuidae): key parasitoids considered for its biological control. Insects, 12(4), 2021, 273.
Tooker, J.F., Douglas, M.R., Krupke, C.H., Neonicotinoid seed treatments: limitations and compatibility with integrated pest management. Agric. Environ. Lett., 2(1), 2017, ael2017-08.
Tooker, J.F., O'Neal, M.E., Rodriguez-Saona, C., Balancing disturbance and conservation in agroecosystems to improve biological control. Annu. Rev. Entomol. 65 (2020), 81–100.
Tylianakis, J.M., Romo, C.M., Natural enemy diversity and biological control: making sense of the context-dependency. Basic Appl. Ecol. 11:8 (2010), 657–668.
van Huis, A., Integrated pest management in the small farmer's maize crop in Nicaragua. 1981, Wageningen University and Research, The Netherlands PhD thesis.
Wengrat, A.P., Coelho Junior, A., Parra, J.R., Takahashi, T.A., Foerster, L.A., et al. Integrative taxonomy and phylogeography of Telenomus remus (Scelionidae), with the first record of natural parasitism of Spodoptera spp. Brazil. Scientific Reports, 11(1), 2021, 14110.
Wilby, A., Villareal, S.C., Lan, L.P., Heong, K.L., Thomas, M.B., Functional benefits of predator species diversity depend on prey identity. Ecol. Entomol. 30:5 (2005), 497–501.
Wyckhuys, K.A.G., Akutse, K.S., Amalin, D.M., Araj, S.E., Barrera, G., Beltran, M.J.B., et al. Global scientific progress and shortfalls in biological control of the fall armyworm Spodoptera frugiperda. Biol. Control, 2024, 105460.
Wyckhuys, K.A.G., Pozsgai, G., Fekih, I.B., Sanchez-Garcia, F.J., Elkahky, M., Biodiversity loss impacts top-down regulation of insect herbivores across ecosystem boundaries. Sci. Total Environ., 930, 2024, 172807.
Wyckhuys, K.A.G., O'Neil, R.J., Population dynamics of Spodoptera frugiperda Smith (Lepidoptera: Noctuidae) and associated arthropod natural enemies in Honduran subsistence maize. Crop Prot. 25:11 (2006), 1180–1190.
Yang, F., Liu, B., Zhu, Y., Wyckhuys, K.A.G., van der Werf, W., Lu, Y., Species diversity and food web structure jointly shape natural biological control in agricultural landscapes. Communications Biology, 4(1), 2021, 979.
Yang, X., Wyckhuys, K.A.G., Jia, X., Nie, F., Wu, K., Fall armyworm invasion heightens pesticide expenditure among Chinese smallholder farmers. J. Environ. Manage., 282, 2021, 111949.
Young, O.P., Edwards, G.B., Spiders in United States field crops and their potential effect on crop pests. J. Arachnol., 1990, 1–27.
