The enemy of my enemy is not always my friend: Negative effects of carnivorous arthropods on plants

A free Plain Language Summary can be found within the Supporting Information of this article. The importance carnivorous arthropods in shaping plant-herbivore interactions has been well investigated (Abdala-Roberts et al., 2019; Price 1980). By “carnivorous”, we mean habit feeding on other animals, which includes omnivores that feed both plants and animals as intraguild predators (Boitani & Powell, 2012; Coll Guershon, 2002; Polis 1989). In addition to direct suppression herbivores by consumption (Gómez Zamora, 1994), landscape fear presence extends its effect through non-consumptive effects (Abram 2019). benefit for herbivore may also result selection plant traits incidentally maximise predator performance means indirect defence (Price There is extensive support select structures offer housing predators, food bodies or extrafloral nectar nourish predators. Moreover, herbivore-induced volatiles (HIPVs) reveal are hypothesized function a ‘cry help’ (Dicke Baldwin, 2010). So far, only few studies have highlighted attraction natural enemies lead fitness benefits (Kergunteuil Schuman 2012). principle ‘the enemy my friend’, stimulated fundamental research evolution applied use biological control agents agriculture (Aartsma 2017; Turlings Erb, 2018). However, negative performance. This apparent when directly plant, indirectly increase herbivory via decrease pollination (Puentes Björkman, Romero Koricheva, 2011). some cases, damage maximize their own fitness, (omnivores; Puentes 2018) increasing host (koinobiont parasitoids; Rahman, 1970; Xi 2015). an antagonistic relationship between because opposed interests: usually under reduce (including from parasitized herbivores) while include (Kaplan 2016). carnivores affect with members carnivore communities plant-mediated predation (Polis 1989; Stam 2014). Hence, causes complex cascading feedback (Kessler Halitschke, 2007; Poelman Dicke, We hypothesize such scenarios become especially tri-trophic placed wider arthropod community context. Nevertheless, costs resulting rarely experimentally addressed considered concepts (but see Ode, 2006; As stated Pearse al. (2020), might come costs, received considerably less attention than benefits. present review, it not argued overall all interacting during whole season negative. Instead, (1) depending context, positive plants, (2) could sum (3) large part these (affecting arthropods). Therefore, experiments performed environments, arthropods, underestimate effects. addition, act balancing counter-selective force against traits. implies always positively selected but instead influenced different carnivores, Here, review interaction types (Figure 1) and/or parasitoid at individual level, composition. most caused omnivorous (Coll Figure 2). Despite documented role pest (van Lenteren 2018), much true 2017). Negative even more vector pathogens specifically reproductive (Albajes 2006). tissue loss, induces costly defences (Pérez-Hedo 2015), waste resources performance, context (Züst Agrawal, Plant induction efficient resistance strategy some—but all—subsequent (Pappas 2015; Zhang Such response reduces growth, carbon fluxes photosynthetic capacity Two important factors affecting dietary choice quality prey availability (Hunter, 2009; Kester Jackson, 1996). Many prefer nutritious source (Moerkens 2020), case (Eubanks Denno, 1999). An (or quality) leads omnivore (Agrawal good limited prey, reduction, although remains demonstrated (Table 1; Adar Parasitoids insects (usually wasps flies) lay eggs will killed upon development (Godfray, 1994). Koinobiont parasitoids do fully arrest growing larva developing (as idiobiont parasitoids, growth after oviposition paralyzing host; Mackauer Sequeira, 1993). koinobiont still able move certain amount time. solitary grow compared unparasitized ones, reduced (Bustos-Segura Gols Hoballah Turlings, 2001). enhance benefit, leading causing ones (Ode, Some aphids assimilation efficiency (Cloutier Mackauer, reproduce fecundity before death, producing heavier offspring higher fecundity, immediate consequences population (Kaiser Heimpel, regulate according resource needs (Harvey, 2005). Accordingly, behaviour likely several inside (e.g. gregarious superparasitism) potential (Smallegange 2008). Solitary if available herbivorous sufficient optimal one (Harvey Finally, speculate increased due parasitism particularly common ecological hosts (increased superparasitism risks) poor need regulation reach maximal development). When would differential interests (Xi Table 1). arise consume organisms beneficial pollinators (Knight Plants areas high density suffer avoiding high-risk (Romero substantial. For example, crab spiders generalist sit-and-wait ambush flowers Vasconcellos-Neto, 2004); yet, they decreasing pollinator visits seed set (Antiqueira Romero, 2016; Gonçalves-Souza interfering reward pollinators. rare ants wasps, floral without pollinating (Maloof Inouye, 2000). Both robbers, make hole petal access nectar, thieves, morphological mismatch, visitation time (Irwin 2001, Fitness solely depend reproduction pollen (Burkle Ibarra-Isassi Oliveira, enter food-for-protection mutualisms (see Section 4), beneficial. If fail restrict vegetative parts, movement inflorescences robbing, repellence (Ibarra-Isassi 2018; Levan Holway, Ohm Miller, order minimize effects, produce ant-repellent compounds (Junker 2011) EFNs localize (and carnivores) distracting them visiting lowering (Ness, Villamil affects pollinators, behaviour. Herbivores adapt dispersal risks (Lima Dill, 1990). hiding, (Sih Wooster, On hand, neighbouring ways escape behaviours prophylactic herbivores). Herbivore “original” released (Sabelis cases where neighbourhood consists mostly kin inclusive expected; vectors (Culshaw-Maurer 2020). Non-consumptive extend specific ant-mediated plants. While herbivores, engage non-consumptive, mutualistic relationships honeydew-producing (mainly Hemiptera). return food, protect honeydew producers competing (Ohm 2014; Way, 1963). (Styrsky Eubanks, 2007), ant deleterious (Canedo-Júnior Renault 2005; Aphid-tending cause outbreaks tended (Ortega-Ramos 2020) co-occurring hemipterans (Yoo 2013) remove Hemiptera-produced honeydew, reducing disease incidence (Nielsen hemipteran pressure non-hemipteran low, services 2020; Styrsky arises enables exceed inflicted absence colonization ant-attack, profit deterrence local (Alves-Silva Del-Claro, Less about trait-mediated networks species interactions. cost induced effective subsequent herbivores. phloem feeders perform equally omnivore-induced non-induced (Section 2.1), susceptibility, facilitating (Underwood, 1998). using piercing-sucking mode mirids) secrete effectors responsible susceptibility (Dong revealing location van Loon, Citrus infested phytoseiid Eusius stipulatus were attractive Tetranychus urticae, no clear pattern conspecifics (Cruz-Miralles system two resulted Tuta absoluta quantified consequence attracts numerous enough suppress arriving Furthermore, specialist pests find damaged omnivores, learn avoid type cue (Stephens, negatively impact disrupting members. Physiological changes mediate parasitoid-plant (Poelman Parasitized caterpillars levels salivary elicitors, (Cusumano Tan (Stam larvae manipulate host's Bukovinszky 2009) and, thus, conflict interest plant. may, however, strongly degree specialization secondary ability detoxify sequester them. induce level (Ode Vaello (Tan 2019), resources. parallel defences, differentially affected Zhu 2015) repelling detect HIPVs those over (Fatouros Kafle How respond elicited hosting unknown. repel prevention death critical represents another example conflicting parasitoid. Differential exploited trophic levels, hyperparasitoids, locate Hyperparasitoids efficacy production allelochemicals. These environments suitable present, locally releasing (Höller 1994; Petersen Additionally, attacked generations herbivore, hyperparasitization first generation populations next (Tougeron Tena, cross-resistance former (McArt 2013). called “plant vaccination” (sensu Kessler 2004) whereby early-season neglectable defensive (Agrawal, Baldwin (2004) showed mirid bugs Tupiocoris notatus same tobacco Manduca quinquemaculata reduction. result, protected thereby realize significant benefit. bug likelihood colonisation larger mirid. apply period wide range commonly agricultural systems (Gagnon individually pressure, co-occurrence synergistic each other. (Finke Müller Brodeur, 2002). Intraguild (IGP) described (extraguild prey), combination competition carnivores. IGP variety 2002), alleviation dominate (Müller appear strongest simple habitats low biodiversity. Increased structural complexity habitat chance taking place, refuges alternative subordinate (Snyder, contexts diversity (such agroecosystems) overlapping traits, (direct indirect) expected fitness. Direct often asymmetrical: feeds vice versa. Asymmetrical suppression. outcome dependent size, mobility style involved Snyder, suffers vulnerable main regulator (Vance-Chalcraft 2007) aggressive (Rosenheim interact (foraging) behaviour, activity guild members, (Schmitz 2004). Behavioural alterations enemy-associated cues frass, aggregation pheromones, contact infochemicals) dynamics, alleviating ultimately focal patch (Raymond 2000) site (Pineda 2007). foraging leaving patch, contacting (Mouratidis 2021). mainly strong dominating poorly sub-optimally) controlling pests, strengthened domatia mites, facilitate discussed multifunctional, suggesting prevents becoming specialized towards functions. specificity carnivore-plant factor toward role. argue play counter-selection possible situation trait favours (indirect function) favours, lesser extent, stress plant-carnivore should along commensal better understanding forces driving Although omnivory characterized 2011), initiated largely overlooked. notion responses identification provided evidence new enhanced damage. Major challenges future unravel whether indeed translate into studied community. achieved field exposing naturally environment. our study focused similar take place non-arthropod aboveground lizards, birds) belowground nematodes; Mäntylä 2011; Rasmann costs. Arguing perspective, earlier presented examples selective 3). Alternatively, driven enemies, neutral insect create environment feeding, HIPVs), der Meijden Klinkhamer, counter elicitors oral secretions recognize place. conclusion, summarising current knowledge urge work quantify selecting recommend thank three anonymous reviewers insightful suggestions previous version manuscript. Our was funded Early Postdoc Mobility fellowship Swiss National Science Foundation M.A.C.C. Open Competition grant Netherlands Organization Scientific Research (NWO) ALWOP.368 E.H.P. authors declare interest. M.A.C.C., M.E.B., had original idea M.E.B. wrote manuscript; M.D. edited manuscript contributed substantially final version. 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