REVIEW published: 22 April 2021 doi: 10.3389/fevo.2021.641974 Exploring the Kairomone-Based Foraging Behaviour of Natural Enemies to Enhance Biological Edited by: Anne Marie Cortesero, Control: A Review University of Rennes 1, France Reviewed by: Pascal M. Ayelo 1,2†, Christian W. W. Pirk 2†, Abdullahi A. Yusuf 2†, Anaïs Chailleux 3,4†, Cesar Rodriguez-Saona, Samira A. Mohamed 1† and Emilie Deletre 1,3* Rutgers, The State University of New Jersey, United States 1 International Centre of Insect Physiology and Ecology (icipe), Nairobi, Kenya, 2 Department of Zoology and Entomology, Maria Carolina Blassioli Moraes, University of Pretoria, Pretoria, South Africa, 3 UPR HORTSYS, Univ Montpellier, CIRAD, Montpellier, France, 4 Biopass2, Brazilian Agricultural Research Cirad-IRD-ISRA-UBG-Centre de coopération internationale en recherche agronomique pour le développement-Institut de Corporation (EMBRAPA), Brazil Recherche pour le Développement-Institut Sénégalais de Recherches Agricoles-Université Gaston Berger, Dakar, Senegal *Correspondence: Emilie Deletre [email protected] Kairomones are chemical signals that mediate interspecific interactions beneficial to organisms that detect the cues. These attractants can be individual compounds or †ORCID: Pascal M. Ayelo mixtures of herbivore-induced plant volatiles (HIPVs) or herbivore chemicals such as orcid.org/0000-0002-0027-2546 pheromones, i.e., chemicals mediating intraspecific communication between herbivores. Christian W. W. Pirk Natural enemies eavesdrop on kairomones during their foraging behaviour, i.e., location orcid.org/0000-0001-6821-7044 Abdullahi A. Yusuf of oviposition sites and feeding resources in nature. Kairomone mixtures are likely orcid.org/0000-0002-8625-6490 to elicit stronger olfactory responses in natural enemies than single kairomones. Anaïs Chailleux orcid.org/0000-0001-5653-8019 Kairomone-based lures are used to enhance biological control strategies via the Samira A. Mohamed attraction and retention of natural enemies to reduce insect pest populations and orcid.org/0000-0001-6836-7528 crop damage in an environmentally friendly way. In this review, we focus on ways to Specialty section: improve the efficiency of kairomone use in crop fields. First, we highlight kairomone This article was submitted to sources in tri-trophic systems and discuss how these attractants are used by natural Chemical Ecology, enemies searching for hosts or prey. Then we summarise examples of field application a section of the journal Frontiers in Ecology and Evolution of kairomones (pheromones vs. HIPVs) in recruiting natural enemies. We highlight the Received: 15 December 2020 need for future field studies to focus on the application of kairomone blends rather Accepted: 22 February 2021 than single kairomones which currently dominate the literature on field attractants for Published: 22 April 2021 natural enemies. We further discuss ways for improving kairomone use through attract Citation: Ayelo PM, Pirk CWW, Yusuf AA, and reward technique, olfactory associative learning, and optimisation of kairomone lure Chailleux A, Mohamed SA and formulations. Finally, we discuss why the effectiveness of kairomone use for enhancing Deletre E (2021) Exploring the biological control strategies should move from demonstration of increase in the number Kairomone-Based Foraging Behaviour of Natural Enemies to Enhance of attracted natural enemies, to reducing pest populations and crop damage below Biological Control: A Review. economic threshold levels and increasing crop yield. Front. Ecol. Evol. 9:641974. doi: 10.3389/fevo.2021.641974 Keywords: field application, attractant blend, HIPVs, pheromones, semiochemicals, crop yield, olfactory learning Frontiers in Ecology and Evolution | www.frontiersin.org 1 April 2021 | Volume 9 | Article 641974 Ayelo et al. Kairomone Use in Biological Control INTRODUCTION moth scales, increased the efficiency of host location by the parasitoids Trichogramma achaeae Nagaraja and Nagarkatti The foraging behaviour of a parasitoid or predator is a process (Hymenoptera: Trichogrammatidae) and Microplitis croceipes by which it searches for oviposition sites and feeding resources (Cresson) (Hymenoptera: Braconidae), thereby increasing the for its survival, growth, and reproductive success [reviewed in parasitisation rate in the field (Gross et al., 1975; Lewis et al., Kramer (2001)]. Natural enemies (used hereafter in reference to 1975). both parasitoids and predators) play a key role in the biological Pheromones are highly species-specific in mediating control of chewing, sucking, and gall-feeding herbivores (Vidal intraspecific interactions between the emitter and its conspecifics and Murphy, 2018). Understanding the foraging behaviour of (Dicke and Sabelis, 1988; Kost, 2008). They can be grouped into natural enemies is crucial for improving the biological control the following categories: (i) sex pheromones, (ii) aggregation of herbivorous pests (e.g., Mills and Wajnberg, 2008; Gunton pheromones, (iii) marking pheromones, and (iv) alarm and Pöyry, 2016; Mills and Heimpel, 2018). Parasitoids have long pheromones (Kost, 2008; Ruther, 2013). Eavesdropping is served as an insect model in the study of foraging behaviour a well-known phenomenon among natural enemies which for oviposition sites, which has often been viewed as a three- use pheromones of herbivorous insects as kairomones to sequence process: habitat location, host location, and host detect them (Aukema and Raffa, 2005). A typical example selection (Vinson, 1998; Fatouros et al., 2008). However, this is reported by Kpongbe et al. (2019) who demonstrated behavioural process can also be applied to predatory insects that isopentyl-butanoate—the aggregation pheromone of searching for prey (Fellowes et al., 2007; Pervez and Yadav, Clavigralla tomentosicollis Stål (Hemiptera: Coreidae)— 2018). During each of these foraging behavioural sequences, strongly attracts Gryon sp. (Hymenoptera: Scelionidae), the natural enemies rely on a combination of environmental stimuli parasitoid of Clavigralla species. However, not only herbivore to find their host and prey (hereafter jointly referred to pheromones play a role in the attraction of herbivore enemies, as herbivores). Although kairomones and visual signals are i.e., pheromones released by natural enemies also attract exploited by natural enemies, the former is well-known to play conspecific individuals seeking for mates (Ruther, 2013), an important role in their foraging behaviour (Colazza and and may modulate their responses to HIPVs (Cabello et al., Wanjberg, 2013; Lim and Ben-Yakir, 2020). Kairomones are 2017). For example, pheromones from males of the predator individual semiochemical molecules or mixtures that mediate Nabis pseudoferus Remane (Hemiptera: Nabidae) attracted interspecific interactions between living organisms (Dicke and conspecific females and enhanced their responses to HIPVs from Sabelis, 1988; Kost, 2008), while serving as long-range, short- Rhopalosiphum padi (L.) (Hemiptera: Aphididae)-infested wheat range, and contact cues during herbivore location by natural plants, whereas pheromones from males of the mirid predator enemies (Afsheen et al., 2008; Heil and Ton, 2008). Kairomones Nesidiocoris tenuis (Reuter) (Hemiptera: Miridae) attracted exploited by natural enemies are either plant volatiles or conspecific females but were found to reduce their attraction to herbivore-associated chemicals such as pheromones (Afsheen the HIPVs (Cabello et al., 2017). et al., 2008; Kaplan, 2012a; Kaiser et al., 2017; Peñaflor, Kairomone-based lures are deployed in crop plants of which 2019). the background odours shape the location of herbivores by Herbivory-induced plant volatiles (HIPVs) and oviposition- natural enemies (e.g., Schröder and Hilker, 2008; Randlkofer induced plant volatiles (OIPVs) are the reliable plant volatile et al., 2010). In this review, we focus on how to optimise field compounds that serve as long-range kairomones enabling applications of kairomones for improving biological control natural enemies to locate herbivore-infested plants (e.g., Dicke of insect pests. First, we present sources of kairomones in and van Loon, 2000; Mumm and Dicke, 2010; Hilker and tri-trophic systems and discuss how these kairomones are Fatouros, 2015; Turlings and Erb, 2018). The use of HIPVs exploited by natural enemies foraging for hosts or prey. Then and OIPVs to attract natural enemies has been pointed out we provide examples of kairomone field applications, and we as a novel avenue to achieve successful biological control stress how the attraction of natural enemies into crop fields (Kaplan, 2012a; Kelly et al., 2014; Murali-Baskaran et al., might be more efficient when using pheromones rather than 2018; Peri et al., 2018). For example, (E)-4,8-dimethyl-1,3,7- HIPVs. Finally, we highlight potential ways to improve the non-atriene (DMNT), an elm plant (Ulmus minor Mill use of kairomone-based lures for attracting enough natural [Ulmaceae]) OIPV induced by Xanthogaleruca luteola (Müller) enemies to reduce pest populations and crop damage below (Coleoptera: Chrysomelidae), attracted the parasitoid Oomyzus economic threshold levels while increasing crop yields in gallerucae (Fonscolombe) (Hymenoptera: Eulophidae) in the the field. field (Büchel et al., 2011). In addition to HIPVs and OIPVs, kairomones include chemicals emitted from different herbivore stages (eggs, larvae/nymphs, pupae, adults), herbivore by- CHEMICAL INTERACTIONS IN products (e.g., frass, honeydew, exuviae, mandibular