Global change-driven modulation of bottom–up forces and cascading effects on biocontrol services

doi:10.1016/j.cois.2019.05.005

Current Opinion in Insect Science

Volume 35, October 2019, Pages 27-33

https://doi.org/10.1016/j.cois.2019.05.005 Get rights and content

Highlights

•
Plant-mediated bottom–up forces can reach and impact natural enemies on the third trophic level and thus modify related biocontrol services.
•
Agricultural intensification can indirectly impact biocontrol services through the alteration of plant traits and/or landscape structure.
•
Climate change can influence biocontrol services by impacting plant availability, plant quality, as well as multitrophic interactions.
•
Integrating multitrophic plant-arthropod interactions and multi-driver effects helps to understand biocontrol services.

Abiotic and biotic factors affect plants in various ways which in turn affect associated arthropod communities through direct and/or indirect bottom–up interactions. Several review articles have synthesized studies examining the indirect effects of abiotic factors on plant–arthropod interactions, mainly focusing on soil nitrogen, soil water status, and climate change. However, these studies have mostly focused on bitrophic interactions, whereas most ecological systems are composed of at least three trophic levels. Lately, research on plant-mediated multitrophic interactions in plant–arthropod food web has received increasing interest. Both the intensification of agriculture and the global climate change have the potential to trigger bottom–up effects that cascade through trophic links. In this review article, we synthesize the most recent studies describing how abiotic changes could modulate plant-mediated bottom–up forces and how it could affect arthropod communities and associated biocontrol services. We discuss potential for increasing the sustainability of managed and natural ecosystems, and highlight road maps for future studies.

Introduction

Most ecosystem services ultimately rely on interactions between organisms [1,2]. Tritrophic interactions such as plant–herbivorous pest–natural enemies are particularly important in the context of sustainable agriculture as they dictate potential biocontrol services [3,4^••]. Because of this trophic interdependency, biological control might be influenced by trophic cascades, that is, a modification propagating either up or down in a food web with negative and/or positive effects at successive levels [5]. Bottom–up forces define consumer–prey interactions, in which a lower trophic level influences the upper one. In the plant–pest–natural enemies system, these forces are mediated by the lower trophic level that is plants. Abiotic environmental changes such as fertilization regime, climate, or landscape structure can influence plant chemistry, physiology, phenology, morphology and/or, diversity. These changes can impact the survival and/or performance of herbivorous arthropods which, in turn, can affect arthropods from higher trophic levels, as well as their interactions [6,7^••,8].

Understanding the processes that underpin ecosystem services is crucial to characterize and/or quantify global change impacts on ecosystems and the services they provide [2,9]. Global change has been shown to influence plant–herbivorous insect interactions through plant-mediated bottom–up effects [10, 11, 12, 13, 14]. However, whether these alterations reach the third trophic level and modify biocontrol services remains an open question. Here, we review studies looking for bottom–up forces triggered by abiotic factors in tri-trophic systems and their impact on biocontrol services. Even if biocontrol programs are emerging in aquatic systems [15], most previous studies have focused on terrestrial systems, particularly on agroecosystems. We thus focus on terrestrial systems and address how two important global environmental drivers (agricultural intensification and climate change) may impact biocontrol services through bottom–up effects.

Section snippets

Agricultural intensification, bottom–up forces and biocontrol services

Over the past 60 years, economic and technological incentives to achieve higher crop yields have resulted in unprecedented agricultural intensification based on agronomic innovations such as crop breeding advances, chemical nutrition and crop protection [16]. Here, we focus on factors that are likely to trigger plant-mediated bottom–up effects on biocontrol services through the alteration of plant traits and/or landscape structure (Figure 1).

Climate change, bottom–up forces, and biocontrol services

Climate change can influence organisms at each trophic level with important consequences for trophic interactions and the efficiency of biocontrol services [7^••,44, 45, 46, 47]. Precipitation, CO₂, and humidity mainly affect primary producers, whereas temperature has a wider action range and can impact each trophic level directly [10,11,14,44,46,48]. Consequences of changing temperature thus depend on the relative thermal sensitivity: higher trophic levels are more sensitive than lower ones and

Interactions between ‘agricultural intensification’ and ‘climate change’

Climate change can interact with local effects of agricultural intensification to influence biocontrol services in agroecosystems, and the creation of one integrative conceptual framework was suggested to enhance predictive capacities [7^••]. One example is how elevated atmospheric CO₂ or O₃ interact with transgenic insecticidal and the biological control of Bt-target [76] and non-target pests [77] with varying outcomes.

Other environmental factors such as drought/lower irrigation and soil

Conclusions and future research priorities

Previous studies showed the importance of bottom–up forces mediated by plants on herbivorous pests and their natural enemies (Figure 1), but future experiments and mainly field ones are needed. For instance, quantifying the structure and dynamics of pest-based arthropod food webs using molecular approaches [79] could help to accurately characterize predator–prey and/or parasitoid–host interactions and thus help to explain variations in biocontrol efficiency.

Not only linear food chains but also

Conflict of interest statement

Nothing declared.

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

• of special interest
•• of outstanding interest

Acknowledgements

The author would like to thank anonymous reviewers for comments and suggested edits to this manuscript. The author of this work was supported by funds of the Recruitment Program of Global Experts, funds from the Hessen State Ministry of Higher Education, Research and the Arts, funds from the ICAEA project French region Provence-Alpes-Cote d'Azur, funds from the ERA-NET ARIMNet2 project STomP, and funds from the Marie-Curie FP7 COFUND People Programme, through the award of an AgreenSkills+

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Conservation biological control of crop pests by natural enemies relies on management strategies to favour their trophic interactions. In agricultural landscapes, natural enemies acting across habitat boundaries may feed on non-pest prey, resulting in apparent competition between non-pest prey and pests. Such communities, including pests, non-pest prey, and natural enemies have been shown to be affected by landscape heterogeneity depending on the dispersal capacity of the interacting organisms. Nonetheless, a mechanistic understanding of how natural enemies’ dispersal capacity interacts with landscape heterogeneity affecting conservation biological control is, however, lacking. Here, we contribute to such mechanistic understanding through modelling. We simulated the consequences of differences in landscape heterogeneity defined by the contrast of plant resource distribution in a semi-natural habitat compared to a crop and variation in natural enemy dispersal capacity on biological control of a pest. Our model showed that variation in plant resource distribution resulted in bottom-up effects that led to shifts in the dominant mechanism underlying biological control. At high landscape heterogeneity when resources differ strongly between crop and the semi-natural habitat, non-pest prey benefitted from the plant resources available, promoting apparent-competition-mediated biocontrol for high-dispersing natural enemies. At low landscape heterogeneity, pests benefitted mostly from plant resources available, promoting direct plant-pest-enemy mediated biocontrol. Interestingly, intermediate levels of landscape heterogeneity resulted in the lowest levels of biocontrol. Our results highlight the importance of potential bottom-up effects that the matching between plant resources available in a habitat and the resource preference of herbivores can induce on conservation biological control.
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Bottom-up effects are major ecological forces in plant–herbivore–parasitoid multitrophic interactions. Biochar amendment in the field alters the bottom-up effects, as it can directly affect the soil environment and plant nutrient uptake, which in turn, indirectly affects herbivores and their natural enemies. However, such effects are poorly documented. We examined the influence of biochar on soil enzyme activity, soybean defense chemicals, and fitness of Spodoptera litura and its parasitoid Meteorus pulchricornis. As the biochar application rate increased, soil urease and sucrase activities, soybean trypsin protease inhibitor content, and polyphenol oxidase activity gradually increased. However, S. litura survival rate and adult body weight showed an initial increase, followed by a decrease, and then remained steady. Soil phosphatase activity initially increased and then stabilized, while M. pulchricornis cocoon emergence rate and fecundity showed an initial increase, followed by a decrease. Spodoptera litura adults preferred to oviposit on soybean at the 10 g/kg biochar level, whereas the parasitoids preferred the hosts at the 20 g/kg biochar level. Our results indicate that the biochar amendment of soils increased soil enzymes activity and soybean defenses, which had a positive effect on S. litura and M. pulchricornis at low levels, but became detrimental at high levels. The bottom-up effects triggered by biochar seemingly affected the second and third trophic levels, resulting in increased defense potential against herbivorous insects. Thus, biochar showed potential to enhance direct plant defenses against pests and indirectly influenced defenses mediated by natural enemies.
Temperature affects the outcome of competition between two sympatric endoparasitoids
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Temperature is a major driver of species interactions as it determines many physiological and behavioural parameters of ectothermic organisms such as insects. Examining the effects of elevated temperature and extreme temperature events within and between different trophic levels is crucial for understanding their broader implications for community and ecosystem level processes. We compared parasitism success of two hymenopteran parasitoid species, Diadegma semiclausum and Cotesia vestalis, under different temperature regimes when foraging intra- and interspecifically. Both parasitoid species can be found in the same habitat and are important biological control agents of the cosmopolitan lepidopteran pest Plutella xylostella, the host species in this study. Because parasitoid density may influence parasitism success through interference competition, we first investigated the effect of parasitoid density (one to four females of the same species) on parasitism success at 22 °C. In all assays, parasitoid females were released in cages with a single plant infested with 30 hosts placed in a greenhouse or climate cabinets set at 22, 27 or 33 °C and removed after 3 h. All cages were returned to 22 °C until pupation of the parasitoids or hosts, which were then counted. When females of the same species foraged together, parasitism success increased with parasitoid density. However, when both species were foraging together, parasitism success of D. semiclausum decreased with increasing temperature at both tested densities, whereas the opposite was found for C. vestalis. Nevertheless, parasitism success of D. semiclausum was always higher than that of C. vestalis, irrespective of parasitoid density or temperature, but competitive superiority of D. semiclausum decreased with increasing temperature. Increases in the magnitude and frequency of extreme temperature events under climate change are likely to have differential effects on species involved in intimate interactions, depending on community species composition, as species may differ in thermal resilience.
Sensitivity of forest phenology in China varies with proximity to forest edges
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Shifts in forest phenological events serve as strong indicators of climate change. However, the sensitivity of phenology events to climate change in relation to forest origins has received limited attention. Moreover, it is unknown whether forest phenology changes with the proximity to forest edge.
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Our results reveal that PF had earlier green-up dates, later dormancy dates, and higher LiNDVI than NF. However, green-up sensitivities to temperature were higher at the edges of NF, whereas no such pattern was observed in PF. Conversely, the sensitivity of dormancy dates remains relatively stable from the inner to the edge of both NF and PF, except for a quadratic change in dormancy date sensitivity to precipitation found in NF. Additionally, we found that the green-up sensitivity to temperature increased with decreasing proximity to edge in NF evergreen forests, while it showed the opposite trend in PF evergreen forests. Furthermore, we observed that the precipitation impact on green-up dates shifts from postponing to advancing from the inner to the edge of NF, whereas precipitation dominantly postpones PF's green-up dates regardless of the proximity to edge. The LiNDVI exhibits higher sensitivity to precipitation at the edge areas, a phenomenon observed in NF but not in PF.
These results suggest that the responses of forests to climate change vary with the distance to the edge. With increasing edge forests, which results from fragmentation caused by global changes, we anticipate that desynchronized phenological events along the distance to the edge could alter biogeochemical cycles and reshape ecosystem services such as energy flows, pollination duration, and the tourism industry. Therefore, we advocate for further investigations of edge effects to improve ecosystem modelling, enhance forest stability, and promote sustainable tourism.
Feeding guild determines strength of top-down forces in multitrophic system experiencing bottom-up constraints
2021, Science of the Total Environment
Citation Excerpt :
Nitrogen and water are important macronutrients in plants, crucial for a plethora of processes and suboptimal supply can affect their primary and secondary metabolism (English-Loeb et al., 1997; Chaves et al., 2002; Liu et al., 2010; Han et al., 2016). Such changes in plant chemistry can have bottom-up effects on higher trophic levels (see Han et al., 2022 for a thorough review), mediated by nutritional and/or defense compounds (Coqueret et al., 2017; English-Loeb et al., 1997; Huberty and Denno, 2004; Han et al., 2014; Han et al., 2016; Han et al., 2019) or their interaction (Le Bot et al., 2009; Couture et al., 2010) but the effects vary between plant species and cultivars (Rivelli et al., 2013; Han et al., 2016) and with insect species and their feeding guild (Huberty and Denno, 2004; Gutbrodt et al., 2011; Stam et al., 2014). Quantitatively, the main defense compounds in tomato are glycoalkaloids and phenolics (Awmack and Leather, 2002; Cataldi et al., 2005; Larbat et al., 2014; Larbat et al., 2016).
Nitrogen (N) and water are crucial in crop production but increasingly scarce environmental resources. Reducing their inputs can affect the whole plant-arthropod community including biocontrol agents. In a multitrophic system, we studied the interaction of the bottom-up effects of moderately reduced N concentration and/or water supply as well as the top-down effects of pests of different feeding guilds on plant nutritional quality (N and carbon concentration), direct defense (alkaloids and phenolics), and indirect defense (plant volatile organic compounds); on herbivore performance and host quality (N and carbon) to parasitoids and the latter's performance. Studied organisms were tomato plants, the sap feeders Macrosiphum euphorbiae and Bemisia tabaci, the leaf chewers Tuta absoluta and Spodoptera littoralis, and the parasitic wasps Aphelinus abdominalis and Necremnus tutae. Resource limitation affected plant quality, triggering bottom-up effects on herbivore and parasitoid performance, except for T. absoluta and N. tutae. Feeding guild had a major influence: bottom-up effects were stronger on sap feeders; N effects were stronger on sap feeders while water effects were stronger with leaf chewers (S. littoralis). Top-down effects of leaf chewer herbivory partly attenuated bottom-up effects and partly suppressed plant defenses. Bottom-up effects weakened when cascading up trophic levels. In summary, the interaction between plants, pests, and beneficial insects was modulated by abiotic factors, affecting insect performance. Simultaneous abiotic and biotic impact shaped plant biochemistry depending on the feeding guild: the biotic top-down effect of leaf chewer herbivory attenuated the bottom-up effects of plant nutrition and hence dominated the plant biochemical profile whereas in sap feeder infested leaves, it corresponded to the abiotic impact. This study highlights the plant's finely tuned regulatory system facilitating response prioritization. It offers perspectives on how smart manipulation of plant nutrient solutions might save resources while maintaining efficient biocontrol in crop production.
Forecasting impacts of biological control under future climates: mechanistic modelling of an aphid pest and a parasitic wasp
2021, Ecological Modelling
Citation Excerpt :
In addition to temperature, terrestrial insects are sensitive to other interacting stressors including altered rainfall patterns (Todgham and Stillman, 2013), increasing CO2 (Johns and Hughes, 2002), and more frequent extreme weather events (Ma et al., 2015). Pest insects may also be indirectly impacted by the responses of their host plants, competitors and natural enemies (Dáder et al., 2015; DeLucia et al., 2012; Holton et al., 2003; Han et al., 2019). With this myriad of processes in mind, it is perhaps not surprising that observed insect pest responses to climate change are complex; dependent on the species, the crop, and geographic location (Lehmann et al., 2020).
Climate change impacts agricultural pests in complicated ways, and accounting for these responses should form an integral part of pest management programmes. Process-based models are often used in agriculture to forecast population dynamics of pests within a growing season, however these are often constrained to assessing the impacts of temperature in isolation of other factors. These models are therefore unable to fully explore species’ responses to climate change, which may be driven by multiple abiotic and biological stressors. Here, we build a mechanistic model of a globally distributed agricultural aphid pest (Myzus persicae (Sulzer)), and an associated parasitic wasp (Diaeretiella rapae (M'Intosh)) that is known to biologically control the aphid. We simulate temporal dynamics of the crop with a well-established canola growing degree-day model (APSIM) and incorporate the impacts of temperature and rainfall on insect survival. The model was parameterised with laboratory-measured datasets from around the globe, and we have calibrated and validated the model to Australian broadacre cropping systems using regional observation records. We then ran the validated models with future temperature and rainfall scenarios to reveal that suppression of aphid populations by the wasp is enhanced under stressful abiotic conditions, which are predicted to occur more frequently in the future. The process-based modelling approach affords valuable and novel insights into physiological traits that influence population dynamics of both species and highlights gaps in our current understanding of the system. In the future, farmers could have greater confidence in the bio-control potential of D. rapae under different conditions, and be in a position to adjust their M. persicae management programmes accordingly. This is the first model to explore the interaction of these two cosmopolitan species in the field, which is applicable across broad geographic regions, while also providing insights as to how both species could be better managed on a local scale.

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Global change-driven modulation of bottom–up forces and cascading effects on biocontrol services

Highlights

Introduction

Section snippets

Agricultural intensification, bottom–up forces and biocontrol services

Climate change, bottom–up forces, and biocontrol services

Interactions between ‘agricultural intensification’ and ‘climate change’

Conclusions and future research priorities

Conflict of interest statement

References and recommended reading

Acknowledgements

Ecol Econ

Biol Control

J Pest Sci

Environ Exp Bot

J Appl Entomol

Ecol Appl

Sci Rep

Proc Natl Acad Sci U S A

Glob Change Biol

Nature

Science

Entomol Exp Appl

Ecol Lett

Entomol Gen

Biomed Res Int

Entomol Gen

Biodiversity loss and its impact on humanity

Nature

Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies

Annu Rev Ecol Systemat

What is a trophic cascade?

Trends Ecol Evol

Evolutionary trade-offs in plants mediate the strength of trophic cascades

Science

Climate change, nutrition, and bottom-up and top-down food web processes

Trends Ecol Evol

A novel framework for linking functional diversity of plants with other trophic levels for the quantification of ecosystem services

J Veg Sci

Plant water stress and its consequences for herbivorous insects: a new synthesis

Ecology

Effects of nitrogen fertilization on tritrophic interactions

Arthropod Plant Interact

Climate change and its effects on terrestrial insects and herbivory patterns

Neotrop Entomol

Drought effects on damage by forest insects and pathogens: a meta‐analysis

Glob Change Biol

Climate change: resetting plant-insect interactions

Plant Physiol

Concepts for biocontrol in marine environments: is there a way forward?

Manag Biol Invasions

Global food demand and the sustainable intensification of agriculture

PNAS

Increased nitrogen availability influences predator-prey interactions by altering host-plant quality

Chemoecology

Nitrogen and water limitations in tomato plants trigger negative bottom-up effects on the omnivorous predator Macrolophus pygmaeus

J Pest Sci

Nitrogen fertilization increases the nutritional quality of Aphis gossypii (Hemiptera: Aphididae) as prey for Hippodamia variegata (Coleoptera: Coccinellidae) and alters predator foraging behavior

J Econ Entomol

Nitrogen deficiency affects bottom-up cascade without disrupting indirect plant defense

J Chem Ecol

Nitrogen-mediated interaction: a walnut-aphid-parasitoid system

Environ Entomol

Nitrogen and water inputs to tomato plant do not trigger bottom-up effects on a leafminer parasitoid through host and non-host exposures

Pest Manag Sci

Nitrogen and water affect direct and indirect plant systemic induced defense in cotton

Biol Control

Crops for a salinized world

Science

Increased water salinity applied to tomato plants accelerates the development of the leaf miner Tuta absoluta through bottom-up effects

Sci Rep

Effects of environmental stress cascade up through four trophic levels in a salt marsh study system

Ecol Entomol

Behavioral effects of insect-resistant genetically modified crops on phytophagous and beneficial arthropods: a review

J Pest Sci

Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services

Nature

The sublethal effects of pesticides on beneficial arthropods

Ann Rev Entomol

Impacts of sublethal insecticide exposure on insects — facts and knowledge gaps