Scaling up our understanding of non-consumptive effects in insect systems

Hermann, Sara L.; Landis, Douglas A.

doi:10.1016/j.cois.2017.03.010

Cited by 87 publications

(92 citation statements)

References 50 publications

(64 reference statements)

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“…Initially, there was a taxonomic bias towards large terrestrial mammals in the landscape of fear literature. However, within the past several years, the term has been applied to a wide range of taxa, including birds [13,36], fish [98], and invertebrates [99,100]. Amidst this trend, it has become increasingly common to attribute observed ecological phenomena to landscapes of fear.…”

Section: Box 2 Emergence and Limitations Of The Landscape Of Fear Comentioning

confidence: 99%

Landscapes of Fear: Spatial Patterns of Risk Perception and Response

Gaynor

Brown

Middleton

et al. 2019

Trends in Ecology & Evolution

485

420

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Animals experience varying levels of predation risk as they navigate heterogeneous landscapes, and behavioral responses to perceived risk can structure ecosystems. The concept of the landscape of fear has recently become central to describing this spatial variation in risk, perception, and response. We present a framework linking the landscape of fear, defined as spatial variation in prey perception of risk, to the underlying physical landscape and predation risk, and to resulting patterns of prey distribution and antipredator behavior. By disambiguating the mechanisms through which prey perceive risk and incorporate fear into decision making, we can better quantify the nonlinear relationship between risk and response and evaluate the relative importance of the landscape of fear across taxa and ecosystems. HighlightsBehavioral and Population Ecology Behavioral ecologists have long recognized the importance of spatially variable predation risk and prey responses in stabilizing predator-prey population dynamics [76][77][78]. Charnov introduced the concept of 'behavioral resource depression' to describe changes in prey microhabitat selection in response to predation risk, which made prey less accessible to predators [79]. Early studies of the 'ecology of fear' [80] combined mass action models (in which the lethal effects of predators drive numeric responses in prey populations), with optimal foraging theory [81]. These conceptual models provided the theoretical framework for empirical studies of free-ranging predators and prey on complex landscapes.Subsequent studies linked antipredator strategies to physiological outcomes, including stress and reproduction [82,83]. Mesocosm experiments have demonstrated that in some contexts, these risk effects of predation have a greater influence on prey population dynamics than the consumptive effects [84]. While the study of risk effects has proven challenging in heterogeneous natural landscapes, patterns of spatial variation in predation risk and response likely have important consequences for spatial demographic patterns [85,86]. Community EcologyMeanwhile, community ecologists observed that foraging behavior of fearful grazers structured the distribution of primary producers. Spatial variation in predation risk was hypothesized as a mechanism behind the formation of 'grazing halos', denuded areas at the edge of coral reefs where urchins sought refuge from predatory fish [87]. Similar patterns were observed in terrestrial systems; for example, the effects of pika (Ochotona princeps) on vegetation were strongest near rocks that provided refuge [88]. Through experiments, ecologists linked the structural complexity of the habitat back to predator efficiency, with refuges from predators reducing prey mortality rates and transforming prey communities [89]. Spatial variation in predation risk and accompanying patterns of prey foraging activity have been found to shape lower trophic levels via 'predator-induced resource avoidance' [90].The indirect effects of predators on lower trop...

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Section: Box 2 Emergence and Limitations Of The Landscape Of Fear Comentioning

confidence: 99%

Landscapes of Fear: Spatial Patterns of Risk Perception and Response

Gaynor

Brown

Middleton

et al. 2019

Trends in Ecology & Evolution

485

420

View full text Add to dashboard Cite

show abstract

“…This tripartite complex, comprising EPNs, their bacterial symbionts and the infected host, produces a variety of metabolites with different roles in EPN ecology, development and reproduction (Hu, Li, & Webster, ; Hu & Webster, ; Kaplan et al, ; Lu et al, ). Based on studies from above‐ground systems, it is clear that many prey species avoid chemical cues from potential predators (Hermann & Landis, ; Kats & Dill, ). Female insects also frequently use chemical cues to select suitable oviposition sites and to avoid plant defences, competition or elevated predation risk for their offspring (Kariyat et al, ; De Moraes, Mescher, & Tumlinson, ).…”

Section: Introductionmentioning

confidence: 99%

Chemical cues linked to risk: Cues from below‐ground natural enemies enhance plant defences and influence herbivore behaviour and performance

et al. 2019

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Chemical cues are essential for many ecological interactions. Previous studies of chemically mediated multitrophic interactions have typically focused on responses to cues from plants or herbivores above‐ground. It is increasingly clear, however, that below‐ground cues and those produced by organisms at higher trophic levels also have ecological importance. Prey animals often avoid predator odours to improve survival, and previous research has documented enhanced plant resistance following contact with below‐ground natural enemies, though the ecological basis was unknown. Here, we investigated plant and insect responses to chemical cues from below‐ground natural enemies and explored the ecological significance of these cues for multitrophic interactions. More specifically, we examined the influence of odours emitted by entomopathogenic nematodes (EPNs), a natural enemy of insect herbivores, on the performance and behaviour of their insect prey and the defence responses of nearby plants. Our findings revealed that EPN‐infected insect cadavers emit a characteristic blend of volatile compounds with bioactivity in plants and insects. EPN chemical cues influenced both performance and preference of a specialist herbivore, Colorado potato beetle (CPB, Leptinotarsa decemlineata), feeding on its host plant, potato (Solanum tuberosum). CPB larvae consumed less leaf tissue and gained less mass feeding on plants exposed to EPN cues compared to control plants. Female CPBs laid fewer eggs on plants with EPN cues than on controls, indicating deterrence by EPN cues or EPN‐altered plant defences. Plant defences were enhanced by exposure to live EPNs or EPN chemical cues. Potato plants exposed to EPN infective juveniles induced higher amounts of the defence hormone salicylic acid (SA) and had higher expression of the pathogenisis‐related gene PR‐1(PR4) in foliar tissue. Exposing plants to EPN cues primed induction of SA and jasmonic acid in response to feeding damage by CPB larvae. These findings suggest that herbivores avoid cues from their EPN natural enemies and plants respond to the beneficial nematodes by enhancing systemic defences that reduce herbivore performance. This work has important implications for the chemical ecology of tritrophic interactions as we report that the third trophic level can play direct and indirect roles in plant defence. A plain language summary is available for this article.

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“…While there is ample evidence for the prevalence of NCEs in predator-prey interactions (Lima and Dill 1990, Peckarsky et al 2008, Hermann and Landis 2017, our knowledge of NCEs across the most diverse group of animals -arthropods -is especially lacking. Insects and other arthropods (e.g.…”

Section: Synthesismentioning

confidence: 99%

A meta‐analysis of non‐consumptive predator effects in arthropods: the influence of organismal and environmental characteristics

Buchanan

Hermann

Lund

et al. 2017

Oikos

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Non‐consumptive effects (NCEs) – changes in prey behavior or physiology in response to predator threat – are common and can be as strong as consumptive effects. However, our knowledge of NCEs in arthropod systems is lacking. Factors related to study organism and environment have the potential to influence the occurrence and magnitude of NCEs in arthropod systems. While factors such as coevolutionary history of natural enemies and their prey, predator cue, predator or prey feeding mode, and refuge availability have been theoretically and empirically examined, no trends have been proposed for arthropods. We compiled 62 studies, yielding 128 predator–prey interactions, which explicitly examined NCEs in experiments where arthropods were identified to species, using a previously published database of papers from 1990 to 2005 and a new database of papers published from 2006 to 2015. Using these data, we conducted a meta‐analysis to explore the influence of organismal and environmental characteristics on the magnitude of predator NCEs. Our analysis addressed the following three questions. 1) Does predator–prey coevolution give rise to stronger NCEs than when predator and prey species did not coevolve? 2) What influence does habitat type and refuge availability have on NCEs? 3) How do predator characteristics (cue type, hunting mode and life stage) and prey characteristics (mobility, life stage, specialization, gregariousness and feeding mode) influence NCEs? We found that while NCEs were similar across most measured characteristics, NCEs on prey activity were significantly stronger when predator and prey shared an evolutionary history. Our results support growing evidence that NCEs have a negative effect on prey traits and that behavioral NCEs are stronger than physiological ones. Additional studies are needed to be confident in any emerging patterns, therefore we identify key gaps in the literature on NCEs in arthropod systems and discuss ideas for moving forward.

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Scaling up our understanding of non-consumptive effects in insect systems

Cited by 87 publications

References 50 publications

Landscapes of Fear: Spatial Patterns of Risk Perception and Response

Landscapes of Fear: Spatial Patterns of Risk Perception and Response

Chemical cues linked to risk: Cues from below‐ground natural enemies enhance plant defences and influence herbivore behaviour and performance

A meta‐analysis of non‐consumptive predator effects in arthropods: the influence of organismal and environmental characteristics

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