Global change-driven modulation of bottom–up forces and cascading effects on biocontrol services
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+
References (88)
- et al.
Ecosystem services and dis-services to agriculture
Ecol Econ
(2007) - et al.
Effects of global environmental changes on parasitoid–host food webs and biological control
Biol Control
(2014) - et al.
Bottom-up effects of irrigation, fertilization and plant resistance on Tuta absoluta: implications for integrated pest management
J Pest Sci
(2019) - et al.
Salinity stress effects on direct and indirect defence metabolites in maize
Environ Exp Bot
(2016) - et al.
Non-target risk assessment of Bt crops—cry protein uptake by aphids
J Appl Entomol
(2011) - et al.
The relationship between agricultural intensification and biological control: experimental tests across Europe
Ecol Appl
(2011) - et al.
Effects of agricultural intensification on ability of natural enemies to control aphids
Sci Rep
(2017) - et al.
Crop pests and predators exhibit inconsistent responses to surrounding landscape composition
Proc Natl Acad Sci U S A
(2018) - et al.
Consequences of simultaneous elevation of carbon dioxide and temperature for plant–herbivore interactions: a meta-analysis
Glob Change Biol
(2006) - et al.
Environmental warming alters food-web structure and ecosystem function
Nature
(1999)
Environmental correlates of food chain length
Science
Impacts of elevated CO2 on Bemisia tabaci infesting Bt cotton and its parasitoid Encarsia formosa
Entomol Exp Appl
Temperature-size responses alter food chain persistence across environmental gradients
Ecol Lett
Bottom-up effect of water stress on the aphid parasitoid Aphidius ervi
Entomol Gen
Effects of abiotic factors on HIPV-mediated interactions between plants and parasitoids
Biomed Res Int
Impact of nitrogen and potassium fertilization regimes on the biology of the tomato leaf miner Tuta absoluta
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
Basic Appl Ecol
Persistent negative effects of pesticides on biodiversity and biological control potential on European farmland
Basic Appl Ecol
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2021, Science of the Total EnvironmentCitation 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).
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2021, Ecological ModellingCitation 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).