Mini-review Received: 29 July 2013
Revised: 30 September 2013
Accepted article published: 4 November 2013
Published online in Wiley Online Library: 19 November 2013
(wileyonlinelibrary.com) DOI 10.1002/ps.3678
Can we forecast the effects of climate change on entomophagous biological control agents? Ernestina Aguilar-Fenollosa and Josep A Jacas∗ Abstract The worldwide climate has been changing rapidly over the past decades. Air temperatures have been increasing in most regions and will probably continue to rise for most of the present century, regardless of any mitigation policy put in place. Although increased herbivory from enhanced biomass production and changes in plant quality are generally accepted as a consequence of global warming, the eventual status of any pest species will mostly depend on the relative effects of climate change on its own versus its natural enemies’ complex. Because a bottom-up amplification effect often occurs in trophic webs subjected to any kind of disturbance, natural enemies are expected to suffer the effects of climate change to a greater extent than their phytophagous hosts/preys. A deeper understanding of the genotypic diversity of the populations of natural enemies and their target pests will allow an informed reaction to climate change. New strategies for the selection of exotic natural enemies and their release and establishment will have to be adopted. Conservation biological control will probably become the keystone for the successful management of these biological control agents. c 2013 Society of Chemical Industry Keywords: conservation; genotypic diversity; global warming; natural enemy; parasitoid; pest; predator
1
INTRODUCTION
Pest Manag Sci 2014; 70: 853–859
∗
Correspondence to: Josep A Jacas, Universitat Jaume I (UJI), Unitat Associada d’Entomologia Agr´ıcola UJI-IVIA (Institut Valenci`a d’Investigacions Agr`aries), Departament de Ci`encies Agr`aries i del Medi Natural, Campus del Riu Sec, E-12071, Castell´o de la Plana, Spain. E-mail: [email protected] Universitat Jaume I (UJI), Unitat Associada d’Entomologia Agr´ıcola UJI-IVIA (Institut Valenci`a d’Investigacions Agr`aries), Departament de Ci`encies Agr`aries i del Medi Natural, Castell´o de la Plana, Spain
www.soci.org
c 2013 Society of Chemical Industry
853
The Intergovernmental Panel on Climate Change (IPCC) defined the climate as a highly complex system consisting of five major components: the atmosphere, the hydrosphere, the cryosphere, the land surface and the biosphere, and the interactions between them.1 This system evolves in time under the influence of its own internal dynamics and because of external forcings including persistent anthropogenic modifications. These differences can result in changes in the mean and/or the variability of climate properties that persist for an extended period, typically decades or longer, which constitute climate change.2 Climate trends over the past few decades have been fairly rapid and ubiquitous around the world.3 Atmospheric carbon dioxide (CO2 ) concentrations have been rising rapidly since the start of the industrial era.4 In May 2013, for the first time since accurate measurements of atmospheric CO2 began, a daily value of 400 ppm was observed.5 This value is more than 40% higher than the level at the start of the Industrial Revolution.6 Global average tropospheric ozone (O3 ) concentrations have also increased relative to the preindustrial era owing to emissions of O3 precursors associated with industrial activity.1 As a consequence of these increases, air temperatures have been rising in most regions around the world. The average model-projected rates of warming are similar to the mean observed rates since 1980 of roughly 0.3 ◦ C per decade.7 Regardless of any climate change mitigation that may occur in the future to reduce the release of greenhouse gases, even the most optimistic scenarios mean that there is the inevitability of future warming for most of the present century.8 In contrast to temperature, historical changes in rainfall have been more mixed and generally not significant relative to natural variability.9 However, the intensity of rainfall has increased significantly in many parts of the world,10 and since 1970 significant increases in drought extent and severity have been observed for Africa, southern Europe, east and south Asia and eastern Australia.11,12
Climate change can significantly shape living communities directly and indirectly. On the one hand it can affect the physiology, phenology and distribution of any living species independently of its position in the trophic chain. On the other hand it can produce further changes in composition and diversity of communities, as all trophic levels are intimately coupled. Consequently, climate change can dramatically affect agricultural systems and their productivity. Herbivore populations are regulated by ‘top-down’ and ‘bottom-up’ forces. In biological control, the ‘top-down’ control concept13,14 is integrated into the management of agricultural communities by using natural enemies that will cause a higher crop productivity by consuming herbivores, a phenomenon known as a trophic cascade. On the other hand, ‘bottom-up’ control strategies focus on the management of the first trophic level to impair the performance of herbivores, thus reducing pest impact on crop yield. Differential responses to climate change within15 and between16 trophic groups may lead to a rearrangement of communities through asymmetric changes in competitive, ‘bottom-up’ and ‘top-down’ control effects. Foden et al.17 proposed a set of characteristics that would make a species more vulnerable to climate change. These include species with (1) specialised habitat and/or microhabitat requirements, (2) narrow environmental tolerances or thresholds that are likely to be exceeded owing to climate change at any stage in the life cycle,
www.soci.org
E Aguilar-Fenollosa, JA Jacas
(3) dependence on specific environmental triggers or cues that are likely to be disrupted by climate change, (4) dependence on interspecific interactions that are likely to be disrupted by climate change and (5) poor ability or limited opportunity to disperse to, or colonise, a new or more suitable range. Therefore, those species with the highest specialisations in terms of lifestyle or habitat are typically most at risk. Climate change may trigger farmers to change crops for better adaptation to new climatic conditions. In the case of arthropods, it is predicted that a warmer climate will induce increased activity18 – 20 and an enlarged geographical range.21 – 25 If natural enemies cannot follow herbivores, climate change could lead to an intensification of pesticide use, with increasingly important social, environmental and economic costs that could compromise the sustainability of agricultural systems26 and food security.27 In this mini-review the authors will focus on the effects of the main components of climate on the three most relevant trophic levels for agriculture and their interactions and consequences for biological control (BC) of arthropod pests.
under elevated CO2 may modulate the intensity of the impact of herbivores in all possible ways, either by direct or indirect plant defence mechanisms,43,44,49,50 and therefore predictions are difficult.
2 DIRECT EFFECTS OF CLIMATE CHANGE ON CROPS Changes in plant physiology, morphology, phenology and chemistry in response to climate change have been reviewed by different authors.28,29 While the individual mechanisms by which the main climatic factors affect crops are well understood, the interactions between them under real field conditions create substantial complexity that has not been fully appraised. Moreover, validating these effects is challenging because they are sometimes non-specific and may vary with environmental conditions and plant genotype.3,30,31 In agricultural systems, the change in rootstock/cultivar or even crop species in response to climate change will affect their response to pest attack. From the point of view of BC, it will be crucial to understand how this replacement can affect the performance not only of pests and pathogens but also of their natural enemies.32 – 36
854
2.1 Effects of CO2 Enhanced photosynthesis, increased water use efficiency and reduced damage from O3 have been reported under higher CO2 concentrations.37 Furthermore, plant organs (e.g. leaves, branches) may increase in number and size when plants are exposed to increased CO2 amounts.38 Likewise, elevated CO2 can affect the chemical composition of leaves, including increased C:N ratios, altered concentrations of allelochemicals and non-structural carbohydrates, starch and fibre contents and increased concentrations of substances involved in pest resistance, including jasmonic acid among others.39,40 As a consequence, increased biomass and changes in plant architecture and nutritional quality are expected under elevated CO2 levels.41 These changes may result in higher crop productivity and denser plant growth, which may lead, all else being equal, to increased herbivory.41 – 44 Increased water use efficiency increases leaf temperature,45 and this may affect arthropod dwellers of the phylloplane (e.g. leafminers, scales, mites, aphids, etc., and their natural enemies). The decrease in the nutritional quality of foliage may also result in increased herbivory by compensatory feeding.46,47 Moreover, increased herbivory can also result from the phagostimulant effects of increased sugar content in plants.48 However, the nature of the secondary metabolites produced
wileyonlinelibrary.com/journal/ps
2.2 Effects of O3 O3 enters leaves through the stomata, generating reactive oxygen species and causing oxidative stress, which results in premature senescence of leaves and decreased photosynthesis, plant growth and biomass accumulation.51 Additionally, O3 may activate the jasmonic acid signalling pathway,52 which constitutes a direct defence response of plants. This mechanism may also trigger the production of plant volatile organic compounds (VOCs), which constitutes an indirect defence response of plants.49 However, under controlled conditions, O3 has also been demonstrated to increase plant susceptibility to frost, pests and pathogens.31 2.3 Effects of temperature and drought When exposed to high temperatures, plants respond with changes in their RNA metabolism and protein, enzyme and plant hormone synthesis.28,29 Depending on the season and the latitude, the expected effects of these changes can differ greatly. In temperate areas, warming may relieve plant stress during the coldest parts of the year and enlarge the window of plant development.28,29 However, the opposite is expected during the summer, and symptoms such as wilting, leaf burn, leaf folding and abscission can appear.44,53 These changes can affect plant productivity, phenology and susceptibility to herbivorous arthropods, although the wide range of changes may make interactions difficult to predict. Heat and water stress often appear simultaneously, and their symptoms are similar. Both factors have a positive relationship with leaf temperature, with the same consequences on arthropods living in close association with the leaves as with increased CO2 .54 – 57
3 DIRECT EFFECTS OF CLIMATE CHANGE ON ARTHROPODS Modifications in life-history parameters of arthropods, such as development times and voltinism, resulting from direct effects of climate change on physiology, behaviour and phenology, have been described.58 These effects can ultimately result in changes in species abundance and distribution.59 – 61 However, most evidence of these changes has been obtained from experiments where climate variables have been manipulated and the arthropod response has been measured after a limited time period, especially if compared with the timeframe in which climate change is occurring.62,63 Therefore, these assays may overestimate the effects, as species can exhibit phenotypic plasticity and evolutionary responses, which may alter the predicted effects of climate change.64 – 70 In general, it is expected that arthropod performance can be enhanced under conditions of global warming.64,65 Furthermore, for herbivores, consumption of plant foliage altered at elevated temperatures71 could lead to changes in their quality (e.g. chemical defences or body size) and phenology, and these changes might, in turn, affect the fitness, abundance and activity of their natural enemies.66,67 In agricultural systems, populations of both pests and natural enemies will be subjected to these changes, which could ultimately result in a change of pest
c 2013 Society of Chemical Industry
Pest Manag Sci 2014; 70: 853–859
Climate Change and Biological Control
www.soci.org
status, from non-economic phytophagous to key pest species, or vice versa, depending on the balance between the impact on any particular pest relative to its natural enemies.72 3.1 Effect of CO2 Increased insect mortality has been associated with elevated CO2 concentrations compared with those in air (2–3% versus 0.03% v/v respectively).73 – 75 However, these concentrations are much higher than the levels associated with climate change. At these concentrations, direct and indirect effects have been described. On the one hand, insects using CO2 to detect their food source or oviposition site (such as moths, fruit flies or hematophagous insects) can be directly affected.76,77 On the other hand, as described before, altered leaf chemistry and temperature can affect second and higher trophic levels in all possible ways.43,44,78 For instance, in aphids, even a single clone has been reported to display different responses to high CO2 content, depending on the host plant.79 – 81 As a consequence, in spite of the many studies carried out on this subject, it is not possible to establish general rules or to predict the effects of elevated CO2 concentrations on arthropods and their pest status. 3.2 Effect of O3 In general, the effects of O3 on insect development and growth are counteracted by elevated CO2 .82 All types of response have been observed, depending on the interaction considered, from positive83 – 86 to negative85,87,88 and, most frequently, neutral.82 3.3 Effect of temperature As poikilothermic organisms, arthropods have a body temperature that is highly dependent on the ambient temperature. Many of the key processes of arthropods, such as metabolism, behaviour, growth, reproduction, development and survival, are mediated by temperature.89 – 92 Therefore, in temperate climates, global warming is expected to enlarge the window for development (i.e. the period when temperature lies between lower and upper development thresholds) and voltinism. However, if temperatures rise above the upper development threshold, a negative impact would be expected. In that case, even assuming that animals have behaviours providing some thermoregulation (seeking shelter, for example), a negative effect would be anticipated, as these behaviours have fitness costs in terms of lost foraging and reproduction opportunities.93 Most of the processes mentioned govern species interactions in food webs.93 – 96 As a consequence, divergence in thermal preferences of the species involved, which may lead to different spatiotemporal distribution, could disrupt the equilibrium of interactions relevant for BC.97 These mismatches could lead to the extinction of part of the system98 and thereby seriously affect BC.
4 EFFECTS OF CLIMATE CHANGE ON ECOLOGICAL INTERACTIONS: BIOLOGICAL CONTROL Although all trophic levels can be altered by climate change, it is widely recognised that, the higher the level, the stronger the impact,99 as a bottom-up amplification effect often occurs to trophic webs subjected to any kind of disturbance.100 Therefore, climate change is likely to result in a higher impact on natural enemies than on herbivores. However, not all natural enemies are expected to be affected to the same extent. According to Foden et al.,17 species with highest specialisations would be most at risk. Hence, within a continuum of increasing risk, omnivorous predators, which can switch their feeding preferences in response to the relative availability of alternative food types,101,102 would be the most robust, whereas koinobiont endoparasitoids, which have the most intimate relationship with their hosts, would be the most susceptible species.97 Likewise, tropical species, which are adapted to a fairly steady climate that never gets extremely hot or cold, may be particularly vulnerable to climate change.103,104 In natural ecosystems, the tritrophic interactions between plants, herbivorous insects and their natural enemies are the result of long coevolutionary processes specific to particular environments and relatively stable climatic conditions.98 However, in agricultural systems, these interactions have been deeply altered by humans, and coevolution cannot always be taken for granted.105,106 Many crop plants are grown far away from their area of origin, and therefore new associations with both herbivorous and entomophagous indigenous arthropods have appeared. This situation can be further complicated when exotic arthropods get into the system. According to the origin of target pest and natural enemy, different types of BC can be defined (Table 1),107,108 and origin is a key feature to predict the robustness of these associations and, therefore, how they may respond to climate change. These predictions should take into account the potential of invertebrates to adapt to changing climate on the basis of existing genotypic diversity.109 Figure 1 shows an adaptation of Lewis et al.,110 which illustrates the importance of genotypic diversity to the response of a hypothetical species when exposed to a different environment. Under the genotypic diversity heading, the response potential for two representative individual genotypes (G1 and G2) belonging to one particular population (P4) of the same hypothetical species is shown. This response potential consists of the genetically fixed maximum range of suitable environmental conditions to which the species could respond (the total white area plus the shaded area). This maximum level of response to the array of environmental conditions is shown as a curve, which indicates that the maximum response level varies with different environmental conditions in its range. As reflected by the different range and curve configuration for G1 and G2, the response potential may vary substantially among individuals within a population. The activated response potential of
Table 1. Types of biological control (BC) strategies based on the geographical origins of pest and natural enemy and the history of their association Origin of target pest
Origin of natural enemy (NE)
New environment
Coevolution
Classical New association, classical Fortuitous Neoclassical Natural
Exotic Exotic Exotic Indigenous Indigenous
Exotic (same as pest) Exotic (different from pest) Indigenous Exotic Indigenous
For both For both For pest only For NE only No
Yes No No No Yes
Pest Manag Sci 2014; 70: 853–859
c 2013 Society of Chemical Industry
wileyonlinelibrary.com/journal/ps
855
Type of BC
www.soci.org
E Aguilar-Fenollosa, JA Jacas
Figure 1. Factors determining the eventual response of populations to climate change (see text for explanation).
856
G1 and G2 (shaded area) that could be realised at any given time is somewhat less than the overall potential (white area) and depends on the actual environment encountered by these genotypes. Under the new environment heading, five different environments (E1 to E5) are proposed. The interaction of the two genotypes with these environments can have different outputs included under the phenotypic plasticity heading. For instance, new environment E5 would result in the disappearance of G1. The same would happen with G2 under E1, E2 and E3, whereas E4 would allow the conservation of both genotypes. Because the response potential to environmental change of individuals determines the response potential of the whole population that they make up, and the populations in turn determine the response potential of a species,110 the genetic diversity of herbivorous insects and their natural enemies will ultimately define their response to climate change. Individuals that colonise a new habitat are, by definition, a genetic subset of their source population, representing a genetic bottleneck relative to the source population.111,112 Therefore, indigenous pests and their natural enemies will have highest genotypic diversity and potential to respond to climate change when at their native ranges. Given the time pace at which this phenomenon is occurring, indigenous species may have the ability to respond and successfully adapt and coevolve in a warmer climate. However, whether the extent of the genotypic diversity of natural enemies, particularly that of specialists, will allow them to adapt successfully remains to be seen.113 Future studies will have to consider genotypic diversity of natural enemies and their hosts/preys and assess the ability of these enemies to track their hosts/preys through evolutionary changes113 to predict the effect of climate change on BC. Because higher tropic levels, especially predators and parasitoids, are more sensitive than herbivores to habitat fragmentation and connectivity,114 – 116 conservation BC practices, providing shelter or alternative food sources, especially when applied at a higher scale (landscape), may offer tools to alleviate the negative impact of global warming on BC.117 – 119 In the case of exotic invasive pest species, as most of them are originally from warmer climates than that occurring at the new habitat,120 even with limited genotypic diversity in this new location, they may be favoured by climate change relative to their
wileyonlinelibrary.com/journal/ps
natural enemies.17,121,122 For instance, introductions of tropical species of spider mites into Europe have increased 50% in the last 30 years.123 Moreover, warmer conditions in temperate areas may create new possibilities not only for invasive species to become established but also for pest outbreaks. Indeed, recent studies have attributed herbivore control disruption in some agroecosystems to severe environmental conditions.56,122,124 In the case of BC strategies exploiting exotic natural enemies, either classical, inoculative or inundative108 (Table 1), it is widely known that the practices used in collection, importation, quarantine, rearing and release phases of an introduction may lead to reduced fitness, or at least to reduced genetic variation.111,125 In fact, de Boer et al.126 illustrated how bottlenecks associated with BC could be particularly detrimental in parasitoid Hymenoptera. The numbers of individuals eventually introduced for BC are typically small, resulting in reduced genotypic diversity of the initial founding population.105,112 This reduced genetic variation may seriously hamper the response of exotic natural enemies to new environmental conditions. In these cases, it may be possible to respond to climate change by selecting in their areas of origin and releasing in the target region natural enemies better adapted to these new environmental conditions. Genetic diversity and phenotypic plasticity to different environmental conditions have been demonstrated for several natural enemies. For example, White et al.127 successfully selected for tolerance to extreme temperatures various populations of Aphytis lingnanensis Compere (Hymenoptera: Aphelinidae) derived from a large gene pool in California. Similarly, evidence for genetic variation in populations of Lysiphlebus testaceipes (Cresson) (Hymenoptera: Aphidiidae) with different thermal requirements was demonstrated by Shufran et al.128 Walzer et al.129,130 found natural variation in response to dry conditions for Neoseiulus californicus (McGregor) (Acari: Phytoseiidae) strains collected in different geographic areas. Even more complex traits, such as generation time in Trichogramma aurosum Sugonjaev and Sorokina (Hymenoptera: Trichogrammatidae),131 or the ability to synthesise lipids in Leptopilina boulardi (Barbotin et al.) (Hymenoptera: Figitidae),132 have been shown to change between populations subjected to different environmental conditions. As before, once identified, successfully reared and released,
c 2013 Society of Chemical Industry
Pest Manag Sci 2014; 70: 853–859
Climate Change and Biological Control
www.soci.org
conservation BC may help these recently introduced genotypes to persist in the new environment and show their full potential.
5
CONCLUSION
It is difficult to forecast the effect of climate change on the interactions between trophic levels, as these interactions are generally complex. For the practice of BC, new strategies for selecting exotic natural enemies and their release and establishment will need to be adopted. A thorough understanding of the genotypic diversity of the populations of natural enemies and their target pests will be necessary to adequately react to global warming. Furthermore, conservation BC techniques will have to be put in place to facilitate populations of natural enemies to endure in our changing world.
ACKNOWLEDGEMENTS A Tena and A Urbaneja (IVIA, Montcada, Spain) made valuable comments on an early draft of this manuscript. While working on the manuscript, the authors received financial support from the Spanish Plan Nacional R+D (AGL2011-30538-C03-01) and European FP7 (KBBE.2011.1.2-12).
REFERENCES
Pest Manag Sci 2014; 70: 853–859
c 2013 Society of Chemical Industry
wileyonlinelibrary.com/journal/ps
857
1 Baede APM, Appendix I: Glossary. Intergovernmental Panel on Climate Change, IPCC Third Assessment Report – Climate Change 2001, Working Group I: The Scientific Basis. [Online]. Available: http://www.grida.no/publications/other/ipcc_tar/?src=/climate/ ipcc_tar/wg1/518.htm [17 July 2013]. 2 Field CB, Barros V, Stocker TF, Qin D, Dokken DJ, Ebi KL, et al, Managing the risks of extreme events and disasters to advance climate change adaptation. IPCC Special Reports. [Online]. Cambridge University Press (2012). Available: http://www.ipcc.ch/pdf/specialreports/srex/SREX_Full_Report.pdf [17 July 2013]. 3 Lobell DB and Gourdji SM, The influence of climate change on global crop productivity. Plant Physiol 160:1686–1697 (2012). ´ e´ C, Boden T, Canadell JG and Raupach 4 Peters GP, Marland G, Le Quer MR, Rapid growth in CO2 emissions after the 2008–2009 global financial crisis. Nat Clim Change 2:2–4 (2011). 5 Now what? The Keeling Curve, a Daily Record of Atmospheric Carbon Dioxide. [Online]. Scripps Institution of Oceanography, UC San Diego, La Jolla, CA (2013). Available: http://keelingcurve. ucsd.edu/now-what/ [17 July 2013]. 6 Peters GP, Andrew R, Boden T, Canadell J, Ciais P, Le Qu´ere´ C, et al, The challenge to keep global warming below two degrees. Nat Clim Change 3:4–6 (2013). 7 Lobell DB, Bonfils C and Duffy PB, Climate change uncertainty for daily minimum and maximum temperatures: a model inter-comparison. Geophys Res Lett 34:L05715 (2007). 8 Hill JK, Griffiths HM and Thomas CD, Climate change and evolutionary adaptations at species’ range margins. Annu Rev Entomol 56:143–159 (2011). 9 Lobell DB, Schlenker WS and Costa-Roberts J, Climate trends and global crop production since 1980. Science 333:616–620 (2011). 10 Alexander LV, Zhang X, Peterson TC, Caesar J, Gleason B, Klein Tank A, et al, Global observed changes in daily climate extremes of temperature and precipitation. J Geophys Res 111:D05109 (2006). 11 Sheffield J and Wood EF, Global trends and variability in soil moisture and drought characteristics, 1950–2000, from observation-driven simulations of the terrestrial hydrologic cycle. J Clim 21:432–458 (2008). 12 Dai A, Drought under global warming: a review. Wires Clim Change 2:45–65 (2011). 13 Hairston NG, Smith FE and Slobodkin LS, Community structure, population control, and competition. Am Nat 94:421–425 (1960). 14 Oksanen L, Fretwell SD, Arruda J and Niemela P, Exploitation ecosystems in gradients of primary productivity. Am Nat 118:240–261 (1981).
15 Thomas CD, Cameron A, Green RE, Bakkenes M, Beaumont LJ, Collingham YC, et al, Extinction risk from climate change. Nature 427:145–148 (2004). 16 Vinebrooke RD, Schindler DW, Findlay DL, Turner KH, Paterson MA and Milis M, Trophic dependence of ecosystem resistance and species compensation in experimentally acidified Lake 302S (Canada). Ecosystems 6:101–113 (2003). 17 Foden W, Mace G, Vie´ JC, Angulo A, Butchart SHM, DeVantier L, et al, Species susceptibility to climate change impacts, in Wildlife in a Changing World: an Analysis of the 2008 IUCN Red List of Threatened Species, ed. by Vi´e JC, Hilton-Taylor C and Stuart SN. IUCN, Gland, Switzerland, pp. 77–88 (2008). 18 DeLucia EH, Casteel CL, Nabity PD and O’Neill BF, Insects take a bigger bite out of plants in a warmer, higher carbon dioxide world. Proc Natl Acad Sci USA 105:1781–1782 (2008). 19 Johnson SN and McNicol JW, Elevated CO2 and aboveground–belowground herbivory by the clover root weevil. Oecologia 162:209–216 (2010). 20 Stiling P, Forkner R and Drake B, Long-term exposure to elevated CO2 in a Florida scrub-oak forest increases herbivore densities but has no effect on other arthropod guilds. Insect Conserv Diver 3:152–156 (2010). 21 Parmesan C, Ryrholm N, Stefanescu C, Hill JK, Thomas CD, Descimon H, et al, Poleward shifts in geographical ranges of butterfly species associated with regional warming. Nature 399:579–583 (1999). 22 Bale JS, Masters GJ, Hodkinson ID, Awmack C, Bezemer TM, Brown VK, et al, Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Glob Change Biol 8:1–16 (2002). 23 Hickling R, Roy DB, Hill JK, Fox R and Thomas CD, The distributions of a wide range of taxonomic groups are expanding polewards. Glob Change Biol 12:450–455 (2006). 24 Musolin DL and Fujisaki K, Changes in ranges: trends in distribution of true bugs (Heteroptera) under conditions of the current climate warming. Russ Entomol J 15:175–179 (2006). 25 Berg MP, Kiers ET, Driessen G, van der Heijden M, Kooi BW, Kuenen F, et al, Adapt or disperse: understanding species persistence in a changing world. Glob Change Biol 16:587–598 (2010). 26 Rosenzweig C, Iglesias A, Yang XB, Epstein PR and Chivian E, Climate change and extreme weather events: implications for food production, plant diseases, and pests. Glob Change Hum Hlth, 2:90–104 (2001). 27 Wheeler T and von Braun J, Climate change impacts on global food security. Science 341:508–513 (2013). 28 Garrett KA, Dendy SP, Frank EE, Rouse MN and Travers SE, Climate change effects on plant disease: genomes to ecosystems. Annu Rev Phytopathol 44:489–509 (2006). 29 Fuhrer J, Agroecosystem responses to combinations of elevated CO2 , ozone, and global climate change. Agric Ecosyst Environ 97:1–20 (2003). 30 Harmens H and Mills G, Review of the influence of climate change on the impacts of ozone on vegetation. The UNECE International Cooperative Programme on Vegetation. [Online]. Natural Environment Research Council CEH Project No. C02309, Centre for Ecology and Hydrology, Bangor, UK (2005). Available: http://uk-air.defra.gov.uk/reports/cat10/0510100939_EPG_1-3205_Final_Report.pdf [17 July 2013]. 31 Battisti A, Masutti L, Paoletti E and Ragazzi A, Silviculture: forest protection. Ital J For Mount Environ 65:239–244 (2010). 32 Mattson WJ and Haack RA, The role of drought in outbreaks of plant eating insects. Bioscience 37:110–118 (1987). 33 Berryman AA, What causes population cycles of forest Lepidoptera? Trends Ecol Evol 11:28–32 (1996). 34 Ode PJ, Plant chemistry and natural enemy fitness: effects on herbivore and natural enemy interactions. Annu Rev Entomol 51:163–185 (2006). 35 Bruessow F, Asins MJ, Jacas JA and Urbaneja A, Replacement of CTV-susceptible sour orange rootstock by CTV-tolerant ones may have triggered outbreaks of Tetranychus urticae in Spanish citrus. Agric Ecosyst Environ 137:93–98 (2010). 36 Jamieson MA, Trowbridge AM, Raffa KF and Lindroth RL, Consequences of climate warming and altered precipitation patterns for plant–insect and multitrophic interactions. Plant Physiol 160:1719–1727 (2012).
858
www.soci.org
E Aguilar-Fenollosa, JA Jacas
37 von Tiedemann A and Firsching KH, Interactive effects of elevated ozone and carbon dioxide on growth and yield of leaf rust-infected versus non-infected wheat. Environ Pollut 108:357–363 (2000). 38 Pritchard SG, Rogers HH, Prior SA and Peterson CM, Elevated CO2 and plant structure: a review. Glob Change Biol 5:807–837 (1999). 39 Bezemer TM and Jones TH, Plant–insect herbivore interactions in elevated CO2 : quantitative analyses and guild effects. Oikos 82:212–222 (1998). 40 Ballhorn DJ, Reisdorff C and Pfanz H, Quantitative effects of enhanced CO2 on jasmonic acid induced plant volatiles of lima bean (Phaseolus lunatus L.). J Appl Bot Food Qual 84:65–71 (2011). 41 Robinson EA, Ryan GD and Newman JA, A meta-analytical review of the effects of elevated CO2 on plant–arthropod interactions highlights the importance of interacting environmental and biological variables. New Phytol 194:321–336 (2012). 42 Gurenstein PG and Hildebrand JG, Roles and effects of environmental carbon dioxide in insect life. Annu Rev Entomol 53:161–178 (2008). 43 Dyer LA, Richards LA, Short SA and Dodson CD, Effects of CO2 and temperature on tritrophic interactions. PLoS One 8:e62528 (2013). 44 Zavala JA, Nabity PD and DeLucia EH, An emerging understanding of mechanisms governing insect herbivory under elevated CO2 . Annu Rev Entomol 58:79–97 (2013). 45 O’Neill BF, Zangerl AR, DeLucia EH, Casteel C, Zavala JA and Berenbaum MR, Leaf temperature of soybean grown under elevated CO2 increases Aphis glycines (Hemiptera: Aphididae) population growth. Insect Sci 18:419–425 (2011). 46 Lincoln DE, Couvet D and Sionit N, Response of an insect herbivore to host plants grown in carbon dioxide enriched atmospheres. Oecologia 69:556–560 (1986). 47 Sch¨adler M, Roeder M, Brandl R and Matthies D, Interacting effects of elevated CO2 , nutrient availability and plant species on a generalist invertebrate herbivore. Glob Change Biol 13:1005–1015 (2007). 48 Hamilton JG, Dermody OC, Aldea M, Zangerl AR, Rogers A, Berenbaum MR, et al, Anthropogenic changes in tropospheric composition increase susceptibility of soybean to insect herbivory. Environ Entomol 34:479–485 (2005). 49 Yuan JS, Himanen SJ, Holopainen JK, Chen F and Stewart CNJ, Smelling global climate change: mitigation of function for plant volatile organic compounds. Trends Ecol Evol 24:323–331 (2009). 50 DeLucia EH, Nabity PD, Zavala JA and Berenbaum MR, Climate change: resetting plant–insect interactions. Plant Physiol 160:1677–1685 (2012). 51 Ainsworth AA, Yendrek CR, Sitch S, Collin WJ and Emberson LD, The effects of tropospheric ozone on net primary productivity and implications for climate change. Annu Rev Plant Biol 63:637–661 (2012). 52 Rao MV, Lee H, Creelman RA, Mullet JE and Davis KR, Jasmonic acid signaling modulates ozone-induced hypersensitive cell death. Plant Cell 12:1633–1646 (2000). 53 van Zyl JL, Canopy temperature as a water stress indicator in vines. S Afr J Enol Vitic 7:53–60 (1986). 54 Holtzer TO, Norman JM, Perring TM, Berry JS and Heintz JC, Effects of microenvironment on the dynamics of spider-mite populations. Exp Appl Acarol 4:247–264 (1988). 55 Leinonen I and Jones HG, Combining thermal and visible imagery for estimating canopy temperature and identifying plant stress. J Exp Bot 55:1423–1431 (2004). 56 Stavrinides MC, Daane KM, Lampinen BD and Mills NJ, Plant water stress, leaf temperature, and spider mite (Acari: Tetranychidae) outbreaks in California vineyards. Environ Entomol 39:1232–1241 (2010). 57 Chaves MM, Flexas J and Pinheiro C, Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560 (2009). 58 Romo CM and Tylianakis JM, Elevated temperature and drought interact to reduce parasitoid effectiveness in suppressing hosts. PLoS One 8:e58136 (2013). 59 Bale JS, Masters GJ, Hodkinson ID, Awmack C, Bezemer TM, Brown VK, et al, Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Glob Change Biol 8:1–16 (2002). 60 Parmesan C, Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669 (2006). 61 Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, et al, Ecological responses to recent climate change. Nature 416:389–395 (2002).
62 Walther GR, Tackling ecological complexity in climate impact research. Science 315:606–607 (2007). 63 Barton BT, Local adaptation to temperature conserves top-down control in a grassland food web. Proc R Soc B 278:3102–3107 (2011). 64 Deutsch CA, Tewksbury JJ, Huey RB, Sheldon KS, Ghalambor CK, Haak DC, et al, Impacts of climate warming on terrestrial ectotherms across latitude. Proc Natl Acad Sci USA 105:6668–6672 (2008). 65 Gienapp P, Teplitsky C, Alho JS, Mills JA and Meril¨a J, Climate change and evolution: disentangling environmental and genetic responses. Mol Ecol 17:167–178 (2008). 66 Skelly DK, Joseph LN, Possingham HP, Freidenburg LK, Farrugia TJ, Kinnison MT, et al, Evolutionary responses to climate change. Conserv Biol 21:1353–1355 (2007). 67 Clark CM and Tilman D, Loss of plant species after chronic low-level nitrogen deposition to prairie grasslands. Nature 451:712–715 (2008). 68 Suttle KB, Thomsen MA and Power ME, Species interactions reverse grassland responses to changing climate. Science 315:640–642 (2007). 69 Chapin FS, Shaver GR, Giblin AE, Nadelhoffer KJ and Laundre JA, Responses of Arctic tundra to experimental and observed changes in climate. Ecology 76:694–711 (1995). ¨ 70 Korner C, Plant CO2 responses: an issue of definition, time and resource supply. New Phytol 172:393–411 (2006). 71 Harrington R, Woiwod I and Sparks T, Climate change and trophic interactions. Trends Ecol Evol 14:146–150 (1999). 72 Quesada-Moraga E, Plagas de insectos y cambio clim´atico. Phytoma 232:1–9 (2011). 73 Nicolas G and Sillans D, Immediate and latent effects of carbon dioxide on insects. Annu Rev Entomol 34:97–116 (1989). 74 Carpenter A and Potter M, Controlled atmospheres, in Quarantine Treatments for Pests of Fruit Plants, ed. by Sharp JL and Hallman GJ. Westview Press, Boulder, CO, pp. 171–198 (1994). 75 Lehmann FO, Dickinson M and Staunton J, The scaling of carbon dioxide release and respiratory water loss in flying fruit flies (Drosophila spp.). J Exp Biol 203:1613–1624 (2000). 76 Guerenstein PG, Christensen TA and Hildebrand JG, Sensory processing of ambient CO2 information in the brain of the moth Manduca sexta. J Comp Physiol 190:707–725 (2004). 77 Guerenstein PG and Hildebrand JG, Roles and effects of environmental carbon dioxide in insect life. Annu Rev Entomol 53:161–178 (2008). 78 Holopainen JK, Himanen SJ and Poppy GM, Climate change and its effects on the chemical ecology of insect parasitoids, in Chemical Ecology of Insect Parasitoids, ed. by Wajnberg E and Colazza S. John Wiley & Sons, Ltd, Chichester, UK, pp. 169–190 (2013). 79 Awmack CS, Harrington R and Leather SR, Host plant effects on the performance of the aphid Aulacorthum solani (Kalt.) (Homoptera: Aphididae) at ambient and elevated CO2 . Glob Change Biol 3:545–549 (1997). 80 Mondor E, Tremblay MN, Awmack CS and Lindroth RL, Altered genotypic and phenotypic frequencies of aphid populations under enriched CO2 and O3 atmospheres. Glob Change Biol 11:1990–1996 (2005). 81 Hulle´ M, d’Acier AC, Bankhead-Dronnet S and Harrington R, Aphids in the face of global changes. C R Biol 333:497–503 (2010). 82 Valkama E, Koricheva J and Oksanen E, Effects of elevated O3 , alone and in combination with elevated CO2 , on tree leaf chemistry and insect herbivore performance: a meta-analysis. Glob Change Biol 13:184–201 (2007). 83 Jackson DM, Heagle AS and Eckel RVW, Ovipositional response of tobacco hornworm moths (Lepidoptera: Sphingidae) to tobacco plants grown under elevated levels of ozone. Environ Entomol 28:566–571 (1999). 84 Holton MK, Lindroth RL and Nordheim EV, Foliar quality influences tree herbivore–parasitoid interactions: effects of elevated CO2 , O3 , and plant genotype. Oecologia 137:233–244 (2003). 85 Mondor EB, Tremblay MN, Awmack CS and Lindroth RL, Divergent pheromone mediated insect behavior under global atmospheric change. Glob Change Biol 10:1820–1824 (2004). 86 Freiwald V, Haikio E, Julkunen-Tiitto R, Holopainen JK and Oksanen E, Elevated ozone modifies the feeding behavior of the common leaf weevil on hybrid aspen through shifts in developmental, chemical, and structural properties of leaves. Entomol Exp Appl 128:66–72 (2008).
wileyonlinelibrary.com/journal/ps
c 2013 Society of Chemical Industry
Pest Manag Sci 2014; 70: 853–859
Climate Change and Biological Control
www.soci.org
87 Kopper BJ and Lindroth RL, Effects of elevated carbon dioxide and ozone on the phytochemistry of aspen and performance of an herbivore. Oecologia 134:95–103 (2003). 88 Agrell J, Kopper B, McDonald EP and Lindroth RL, CO2 and O3 effects on host plant preferences of the forest tent caterpillar (Malacosoma disstria). Glob Change Biol 11:588–599 (2005). 89 Campbell A, Frazer BD, Gilbert N, Gutierrez AP and Mackauer M, Temperature requirements of some aphids and their parasites. J Appl Ecol 11:431–438 (1974). 90 Clarke A, Costs and consequences of evolutionary temperature adaptation. Trends Ecol Evol 18:573–581 (2003). 91 Trudgill DL, Honek A, Li D and Straalen NMV, Thermal time – concepts and utility. Ann Appl Biol 146:1–14 (2005). 92 Beveridge OS, Humphries S and Petchey OL, The interacting effects of temperature and food chain length on trophic abundance and ecosystem function. J Anim Ecol 79:693–700 (2010). 93 Gillespie DR, Nasreen A, Moffat CE, Clarke P and Roitberg BD, Effects of simulated heat waves on an experimental community of pepper plants, green peach aphids and two parasitoid species. Oikos 121:149–159 (2012). 94 Almeda R, Augustin CB, Alcaraz M, Calbet A and Saiz E, Feeding rates and gross growth efficiencies of larval developmental stages of Oithona davisae (Copepoda, Cyclopoida). J Exp Mar Biol Ecol 387:24–35 (2010). 95 Jalali MA, Tirry L and De Clercq P, Effect of temperature on the functional response of Adalia bipunctata to Myzus persicae. BioControl 55:261–269 (2010). 96 Petchey OL, Brose U and Rall BC, Predicting the effects of temperature on food web connectance. PhilTransRSocB 365:2081–2091 (2010). 97 Hance T, van Baaren J, Vernon P and Boivin G, Impact of extreme temperatures on parasitoids in a climate change perspective. Annu Rev Entomol 52:107–126 (2007). 98 van der Putten WH, de Ruiterb PC, Bezemera TM, Harvey JA, Wassen M and Wolters V, Trophic interactions in a changing world. Basic Appl Ecol 5:487–494 (2004). 99 Voigt W, Perner J, Davis AJ, Eggers T, Schumacher J, Bahrmann R, et al, Trophic levels are differentially sensitive to climate. Ecology 84:2444–2453 (2003). 100 Cagnolo L, Molina SI and Valladares GR, Diversity and guild structure of insect assemblages under grazing and exclusion regimes in a montane grassland from Central Argentina. Biodivers Conserv 11:407–420 (2002). 101 Begon M, Harper JL and Townsend CR, Ecology. Individuals, Populations and Communities. Blackwell Science, Taunton, MA (1990). 102 Singer MS and Bernays EA, Understanding omnivory needs a behavioral perspective. Ecology 84:2532–2537 (2003). 103 Janzen DH, Why mountain passes are higher in the tropics. Am Nat 101:233–249 (1967). 104 Rosner H, Survival of the flexible. Nature 494:22–23 (2013). 105 Roderick GK and Navajas M, Genes in new environments: genetics and evolution in biological control. Nat Rev Genet 4:889–899 (2003). 106 Roderick GK, Hufbauer R and Navajas M, Evolution and biological control. Evol Appl 5:419–423 (2012). 107 DeBach P and Rosen D, Biological Control by Natural Enemies. Cambridge University Press, Cambridge, UK (1991). 108 Eilenberg J, Hajek A and Lomer C, Suggestions for unifying the terminology in biological control. BioControl 46:387–400 (2001). 109 Cock MJ, Biesmeijer JC, Cannon RJ, Gerard PJ, Gillespie D, Jimenez JJ, et al, The implications of climate change for positive contributions of invertebrates to world agriculture. CAB Rev 8:028 (2013). 110 Lewis WJ, Vet LEM, Tumlinson JH, van Lenteren JC and Papaj DR, Variations in parasitoid foraging behavior: essential elements of a sound biological control theory. Environ Entomol 19:1183–1193 (1990). 111 Roderick GK, Tracing the origin of pests and natural enemies: genetic and statistical approaches, in Genetics, Evolution and Biological Control, ed. by Ehler LE, Sforza R and Mateille TT. CABI Publishing, Wallingford, Oxon, UK, pp. 97–112 (2004).
112 Fauvergue X, Vercken E, Malausa T and Hufbauer R, The biology of small, introduced populations, with special reference to biological control. Evol Appl 5:424–443 (2012). 113 Thomson LJ, Macfadyen S and Hoffmann AA, Predicting the effects of climate change on natural enemies of agricultural pests. Biol Control 52:296–306 (2010). 114 Kruess A and Tscharntke T, Habitat fragmentation, species loss, and biological control. Science 264:1581–1584 (1994). 115 Kruess A and Tscharntke T, Species richness and parasitism in a fragmented landscape: experiments and field studies with insects on Vicia sepium. Oecologia 122:129–137 (2000). 116 Hunter MD, Landscape structure, habitat fragmentation, and the ecology of insects. Agric For Entomol 4:159–166 (2002). 117 Boller EF, H¨ani F and Poehling HM, Ecological Infrastructures: Ideabook on Functional Biodiversity at the Farm Level Temperate Zones of Europe. IOBC/WPRS, LBL, Lindau, Switzerland (2004). 118 Fielder KA, Landis DA and Wratten DS, Maximizing ecosystem services from conservation biological control: the role of habitat management. Biol Control 45:254–271 (2008). 119 Mitsch WJ, What is ecological engineering? Ecol Eng 45:5–12 (2012). 120 Parmesan C and Yohe G, A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42 (2003). 121 Mainka SA and Howard GW, Climate change and invasive species: double jeopardy. Integr Zool 5:102–111 (2010). 122 Montserrat M, Guzm´an C, Sahun ´ RM, Belda JE and Hormaza JI, Pollen supply promotes, but high temperatures demote, predatory mite abundance in avocado orchards. Agric Ecosyst Environ 164:155–161 (2013). 123 Navajas M, Migeon A, Estrada-Pena A, Mailleux AC, Servigne P and Petanovic R, Mites and ticks (Acari). BioRisk 4:149–192 (2010). 124 Montserrat M, Sahun ´ RM and Guzm´an C, Can climate change jeopardize predator control of invasive herbivore species? A case study in avocado agro-ecosystems in Spain. Exp Appl Acarol 59:27–42 (2013). 125 Unruh TR and Woolley JB, Molecular methods in classical biological control, in Handbook of Biological Control: Principles and Applications of Biological Control, ed. by Bellows TS, Fisher TW, Caltagirone LE, Dahlsten DL, Gordh G and Huffaker CB. Academic Press, San Diego, CA, pp. 57–85 (1999). 126 de Boer JG, Kuijper B, Heimpel GE and Beukeboom LW, Sex determination meltdown upon biological control introduction of the parasitoid Cotesia rubecula? Evol Appl 5:444–454 (2012). 127 White EB, DeBach P and Garber MJ, Artificial selection for genetic adaptation to temperature extremes in Aphytis lingnanensis Compere (Hymenoptera: Aphelinidae). Hilgardia 40:161–192 (1970). 128 Shufran KA, Weathersbee AA, Jones DB and Elliot NC, Genetic similarities among geographic isolates of Lysiphlebus testaceipes (Hymenoptera: Aphidiidae) differing in cold temperature tolerances. Environ Entomol 33:776–778 (2004). 129 Walzer A, Castagnoli M, Simoni S, Liguori M, Palevsky E and Schausberger P, Intraspecific variation in humidity susceptibility of the predatory mite Neoseiulus californicus: survival, development and reproduction. Biol Control 41:42–52 (2007). 130 Walzer A, Castagnoli M, Simoni S, Liguori M, Palevsky E and Schausberger P, Identification of a drought-adapted Neoseiulus californicus strain: egg hatchability, juvenile survival and oviposition at low humidities, in Trends in Acarology, ed. by Sabelis MW and Bruin J. Springer, Dordrecht, The Netherlands, pp. 279–283 (2010). 131 Samara RY, Monje JC and Zebitz CPW, Comparison of different European strains of Trichogramma aurosum (Hymenoptera: Trichogrammatidae) using fertility life tables. Biocontrol Sci Technol 18:75–86 (2008). 132 Moiroux J, Lann CL, Seyahooei MA, Vernon P, Pierre JS, van Baaren J, et al, Local adaptations of life-history traits of a Drosophila parasitoid, Leptopilina boulardi: does climate drive evolution? Ecol Entomol 35:727–736 (2010).
859
Pest Manag Sci 2014; 70: 853–859
c 2013 Society of Chemical Industry
wileyonlinelibrary.com/journal/ps
Revised: 30 September 2013
Accepted article published: 4 November 2013
Published online in Wiley Online Library: 19 November 2013
(wileyonlinelibrary.com) DOI 10.1002/ps.3678
Can we forecast the effects of climate change on entomophagous biological control agents? Ernestina Aguilar-Fenollosa and Josep A Jacas∗ Abstract The worldwide climate has been changing rapidly over the past decades. Air temperatures have been increasing in most regions and will probably continue to rise for most of the present century, regardless of any mitigation policy put in place. Although increased herbivory from enhanced biomass production and changes in plant quality are generally accepted as a consequence of global warming, the eventual status of any pest species will mostly depend on the relative effects of climate change on its own versus its natural enemies’ complex. Because a bottom-up amplification effect often occurs in trophic webs subjected to any kind of disturbance, natural enemies are expected to suffer the effects of climate change to a greater extent than their phytophagous hosts/preys. A deeper understanding of the genotypic diversity of the populations of natural enemies and their target pests will allow an informed reaction to climate change. New strategies for the selection of exotic natural enemies and their release and establishment will have to be adopted. Conservation biological control will probably become the keystone for the successful management of these biological control agents. c 2013 Society of Chemical Industry Keywords: conservation; genotypic diversity; global warming; natural enemy; parasitoid; pest; predator
1
INTRODUCTION
Pest Manag Sci 2014; 70: 853–859
∗
Correspondence to: Josep A Jacas, Universitat Jaume I (UJI), Unitat Associada d’Entomologia Agr´ıcola UJI-IVIA (Institut Valenci`a d’Investigacions Agr`aries), Departament de Ci`encies Agr`aries i del Medi Natural, Campus del Riu Sec, E-12071, Castell´o de la Plana, Spain. E-mail: [email protected] Universitat Jaume I (UJI), Unitat Associada d’Entomologia Agr´ıcola UJI-IVIA (Institut Valenci`a d’Investigacions Agr`aries), Departament de Ci`encies Agr`aries i del Medi Natural, Castell´o de la Plana, Spain
www.soci.org
c 2013 Society of Chemical Industry
853
The Intergovernmental Panel on Climate Change (IPCC) defined the climate as a highly complex system consisting of five major components: the atmosphere, the hydrosphere, the cryosphere, the land surface and the biosphere, and the interactions between them.1 This system evolves in time under the influence of its own internal dynamics and because of external forcings including persistent anthropogenic modifications. These differences can result in changes in the mean and/or the variability of climate properties that persist for an extended period, typically decades or longer, which constitute climate change.2 Climate trends over the past few decades have been fairly rapid and ubiquitous around the world.3 Atmospheric carbon dioxide (CO2 ) concentrations have been rising rapidly since the start of the industrial era.4 In May 2013, for the first time since accurate measurements of atmospheric CO2 began, a daily value of 400 ppm was observed.5 This value is more than 40% higher than the level at the start of the Industrial Revolution.6 Global average tropospheric ozone (O3 ) concentrations have also increased relative to the preindustrial era owing to emissions of O3 precursors associated with industrial activity.1 As a consequence of these increases, air temperatures have been rising in most regions around the world. The average model-projected rates of warming are similar to the mean observed rates since 1980 of roughly 0.3 ◦ C per decade.7 Regardless of any climate change mitigation that may occur in the future to reduce the release of greenhouse gases, even the most optimistic scenarios mean that there is the inevitability of future warming for most of the present century.8 In contrast to temperature, historical changes in rainfall have been more mixed and generally not significant relative to natural variability.9 However, the intensity of rainfall has increased significantly in many parts of the world,10 and since 1970 significant increases in drought extent and severity have been observed for Africa, southern Europe, east and south Asia and eastern Australia.11,12
Climate change can significantly shape living communities directly and indirectly. On the one hand it can affect the physiology, phenology and distribution of any living species independently of its position in the trophic chain. On the other hand it can produce further changes in composition and diversity of communities, as all trophic levels are intimately coupled. Consequently, climate change can dramatically affect agricultural systems and their productivity. Herbivore populations are regulated by ‘top-down’ and ‘bottom-up’ forces. In biological control, the ‘top-down’ control concept13,14 is integrated into the management of agricultural communities by using natural enemies that will cause a higher crop productivity by consuming herbivores, a phenomenon known as a trophic cascade. On the other hand, ‘bottom-up’ control strategies focus on the management of the first trophic level to impair the performance of herbivores, thus reducing pest impact on crop yield. Differential responses to climate change within15 and between16 trophic groups may lead to a rearrangement of communities through asymmetric changes in competitive, ‘bottom-up’ and ‘top-down’ control effects. Foden et al.17 proposed a set of characteristics that would make a species more vulnerable to climate change. These include species with (1) specialised habitat and/or microhabitat requirements, (2) narrow environmental tolerances or thresholds that are likely to be exceeded owing to climate change at any stage in the life cycle,
www.soci.org
E Aguilar-Fenollosa, JA Jacas
(3) dependence on specific environmental triggers or cues that are likely to be disrupted by climate change, (4) dependence on interspecific interactions that are likely to be disrupted by climate change and (5) poor ability or limited opportunity to disperse to, or colonise, a new or more suitable range. Therefore, those species with the highest specialisations in terms of lifestyle or habitat are typically most at risk. Climate change may trigger farmers to change crops for better adaptation to new climatic conditions. In the case of arthropods, it is predicted that a warmer climate will induce increased activity18 – 20 and an enlarged geographical range.21 – 25 If natural enemies cannot follow herbivores, climate change could lead to an intensification of pesticide use, with increasingly important social, environmental and economic costs that could compromise the sustainability of agricultural systems26 and food security.27 In this mini-review the authors will focus on the effects of the main components of climate on the three most relevant trophic levels for agriculture and their interactions and consequences for biological control (BC) of arthropod pests.
under elevated CO2 may modulate the intensity of the impact of herbivores in all possible ways, either by direct or indirect plant defence mechanisms,43,44,49,50 and therefore predictions are difficult.
2 DIRECT EFFECTS OF CLIMATE CHANGE ON CROPS Changes in plant physiology, morphology, phenology and chemistry in response to climate change have been reviewed by different authors.28,29 While the individual mechanisms by which the main climatic factors affect crops are well understood, the interactions between them under real field conditions create substantial complexity that has not been fully appraised. Moreover, validating these effects is challenging because they are sometimes non-specific and may vary with environmental conditions and plant genotype.3,30,31 In agricultural systems, the change in rootstock/cultivar or even crop species in response to climate change will affect their response to pest attack. From the point of view of BC, it will be crucial to understand how this replacement can affect the performance not only of pests and pathogens but also of their natural enemies.32 – 36
854
2.1 Effects of CO2 Enhanced photosynthesis, increased water use efficiency and reduced damage from O3 have been reported under higher CO2 concentrations.37 Furthermore, plant organs (e.g. leaves, branches) may increase in number and size when plants are exposed to increased CO2 amounts.38 Likewise, elevated CO2 can affect the chemical composition of leaves, including increased C:N ratios, altered concentrations of allelochemicals and non-structural carbohydrates, starch and fibre contents and increased concentrations of substances involved in pest resistance, including jasmonic acid among others.39,40 As a consequence, increased biomass and changes in plant architecture and nutritional quality are expected under elevated CO2 levels.41 These changes may result in higher crop productivity and denser plant growth, which may lead, all else being equal, to increased herbivory.41 – 44 Increased water use efficiency increases leaf temperature,45 and this may affect arthropod dwellers of the phylloplane (e.g. leafminers, scales, mites, aphids, etc., and their natural enemies). The decrease in the nutritional quality of foliage may also result in increased herbivory by compensatory feeding.46,47 Moreover, increased herbivory can also result from the phagostimulant effects of increased sugar content in plants.48 However, the nature of the secondary metabolites produced
wileyonlinelibrary.com/journal/ps
2.2 Effects of O3 O3 enters leaves through the stomata, generating reactive oxygen species and causing oxidative stress, which results in premature senescence of leaves and decreased photosynthesis, plant growth and biomass accumulation.51 Additionally, O3 may activate the jasmonic acid signalling pathway,52 which constitutes a direct defence response of plants. This mechanism may also trigger the production of plant volatile organic compounds (VOCs), which constitutes an indirect defence response of plants.49 However, under controlled conditions, O3 has also been demonstrated to increase plant susceptibility to frost, pests and pathogens.31 2.3 Effects of temperature and drought When exposed to high temperatures, plants respond with changes in their RNA metabolism and protein, enzyme and plant hormone synthesis.28,29 Depending on the season and the latitude, the expected effects of these changes can differ greatly. In temperate areas, warming may relieve plant stress during the coldest parts of the year and enlarge the window of plant development.28,29 However, the opposite is expected during the summer, and symptoms such as wilting, leaf burn, leaf folding and abscission can appear.44,53 These changes can affect plant productivity, phenology and susceptibility to herbivorous arthropods, although the wide range of changes may make interactions difficult to predict. Heat and water stress often appear simultaneously, and their symptoms are similar. Both factors have a positive relationship with leaf temperature, with the same consequences on arthropods living in close association with the leaves as with increased CO2 .54 – 57
3 DIRECT EFFECTS OF CLIMATE CHANGE ON ARTHROPODS Modifications in life-history parameters of arthropods, such as development times and voltinism, resulting from direct effects of climate change on physiology, behaviour and phenology, have been described.58 These effects can ultimately result in changes in species abundance and distribution.59 – 61 However, most evidence of these changes has been obtained from experiments where climate variables have been manipulated and the arthropod response has been measured after a limited time period, especially if compared with the timeframe in which climate change is occurring.62,63 Therefore, these assays may overestimate the effects, as species can exhibit phenotypic plasticity and evolutionary responses, which may alter the predicted effects of climate change.64 – 70 In general, it is expected that arthropod performance can be enhanced under conditions of global warming.64,65 Furthermore, for herbivores, consumption of plant foliage altered at elevated temperatures71 could lead to changes in their quality (e.g. chemical defences or body size) and phenology, and these changes might, in turn, affect the fitness, abundance and activity of their natural enemies.66,67 In agricultural systems, populations of both pests and natural enemies will be subjected to these changes, which could ultimately result in a change of pest
c 2013 Society of Chemical Industry
Pest Manag Sci 2014; 70: 853–859
Climate Change and Biological Control
www.soci.org
status, from non-economic phytophagous to key pest species, or vice versa, depending on the balance between the impact on any particular pest relative to its natural enemies.72 3.1 Effect of CO2 Increased insect mortality has been associated with elevated CO2 concentrations compared with those in air (2–3% versus 0.03% v/v respectively).73 – 75 However, these concentrations are much higher than the levels associated with climate change. At these concentrations, direct and indirect effects have been described. On the one hand, insects using CO2 to detect their food source or oviposition site (such as moths, fruit flies or hematophagous insects) can be directly affected.76,77 On the other hand, as described before, altered leaf chemistry and temperature can affect second and higher trophic levels in all possible ways.43,44,78 For instance, in aphids, even a single clone has been reported to display different responses to high CO2 content, depending on the host plant.79 – 81 As a consequence, in spite of the many studies carried out on this subject, it is not possible to establish general rules or to predict the effects of elevated CO2 concentrations on arthropods and their pest status. 3.2 Effect of O3 In general, the effects of O3 on insect development and growth are counteracted by elevated CO2 .82 All types of response have been observed, depending on the interaction considered, from positive83 – 86 to negative85,87,88 and, most frequently, neutral.82 3.3 Effect of temperature As poikilothermic organisms, arthropods have a body temperature that is highly dependent on the ambient temperature. Many of the key processes of arthropods, such as metabolism, behaviour, growth, reproduction, development and survival, are mediated by temperature.89 – 92 Therefore, in temperate climates, global warming is expected to enlarge the window for development (i.e. the period when temperature lies between lower and upper development thresholds) and voltinism. However, if temperatures rise above the upper development threshold, a negative impact would be expected. In that case, even assuming that animals have behaviours providing some thermoregulation (seeking shelter, for example), a negative effect would be anticipated, as these behaviours have fitness costs in terms of lost foraging and reproduction opportunities.93 Most of the processes mentioned govern species interactions in food webs.93 – 96 As a consequence, divergence in thermal preferences of the species involved, which may lead to different spatiotemporal distribution, could disrupt the equilibrium of interactions relevant for BC.97 These mismatches could lead to the extinction of part of the system98 and thereby seriously affect BC.
4 EFFECTS OF CLIMATE CHANGE ON ECOLOGICAL INTERACTIONS: BIOLOGICAL CONTROL Although all trophic levels can be altered by climate change, it is widely recognised that, the higher the level, the stronger the impact,99 as a bottom-up amplification effect often occurs to trophic webs subjected to any kind of disturbance.100 Therefore, climate change is likely to result in a higher impact on natural enemies than on herbivores. However, not all natural enemies are expected to be affected to the same extent. According to Foden et al.,17 species with highest specialisations would be most at risk. Hence, within a continuum of increasing risk, omnivorous predators, which can switch their feeding preferences in response to the relative availability of alternative food types,101,102 would be the most robust, whereas koinobiont endoparasitoids, which have the most intimate relationship with their hosts, would be the most susceptible species.97 Likewise, tropical species, which are adapted to a fairly steady climate that never gets extremely hot or cold, may be particularly vulnerable to climate change.103,104 In natural ecosystems, the tritrophic interactions between plants, herbivorous insects and their natural enemies are the result of long coevolutionary processes specific to particular environments and relatively stable climatic conditions.98 However, in agricultural systems, these interactions have been deeply altered by humans, and coevolution cannot always be taken for granted.105,106 Many crop plants are grown far away from their area of origin, and therefore new associations with both herbivorous and entomophagous indigenous arthropods have appeared. This situation can be further complicated when exotic arthropods get into the system. According to the origin of target pest and natural enemy, different types of BC can be defined (Table 1),107,108 and origin is a key feature to predict the robustness of these associations and, therefore, how they may respond to climate change. These predictions should take into account the potential of invertebrates to adapt to changing climate on the basis of existing genotypic diversity.109 Figure 1 shows an adaptation of Lewis et al.,110 which illustrates the importance of genotypic diversity to the response of a hypothetical species when exposed to a different environment. Under the genotypic diversity heading, the response potential for two representative individual genotypes (G1 and G2) belonging to one particular population (P4) of the same hypothetical species is shown. This response potential consists of the genetically fixed maximum range of suitable environmental conditions to which the species could respond (the total white area plus the shaded area). This maximum level of response to the array of environmental conditions is shown as a curve, which indicates that the maximum response level varies with different environmental conditions in its range. As reflected by the different range and curve configuration for G1 and G2, the response potential may vary substantially among individuals within a population. The activated response potential of
Table 1. Types of biological control (BC) strategies based on the geographical origins of pest and natural enemy and the history of their association Origin of target pest
Origin of natural enemy (NE)
New environment
Coevolution
Classical New association, classical Fortuitous Neoclassical Natural
Exotic Exotic Exotic Indigenous Indigenous
Exotic (same as pest) Exotic (different from pest) Indigenous Exotic Indigenous
For both For both For pest only For NE only No
Yes No No No Yes
Pest Manag Sci 2014; 70: 853–859
c 2013 Society of Chemical Industry
wileyonlinelibrary.com/journal/ps
855
Type of BC
www.soci.org
E Aguilar-Fenollosa, JA Jacas
Figure 1. Factors determining the eventual response of populations to climate change (see text for explanation).
856
G1 and G2 (shaded area) that could be realised at any given time is somewhat less than the overall potential (white area) and depends on the actual environment encountered by these genotypes. Under the new environment heading, five different environments (E1 to E5) are proposed. The interaction of the two genotypes with these environments can have different outputs included under the phenotypic plasticity heading. For instance, new environment E5 would result in the disappearance of G1. The same would happen with G2 under E1, E2 and E3, whereas E4 would allow the conservation of both genotypes. Because the response potential to environmental change of individuals determines the response potential of the whole population that they make up, and the populations in turn determine the response potential of a species,110 the genetic diversity of herbivorous insects and their natural enemies will ultimately define their response to climate change. Individuals that colonise a new habitat are, by definition, a genetic subset of their source population, representing a genetic bottleneck relative to the source population.111,112 Therefore, indigenous pests and their natural enemies will have highest genotypic diversity and potential to respond to climate change when at their native ranges. Given the time pace at which this phenomenon is occurring, indigenous species may have the ability to respond and successfully adapt and coevolve in a warmer climate. However, whether the extent of the genotypic diversity of natural enemies, particularly that of specialists, will allow them to adapt successfully remains to be seen.113 Future studies will have to consider genotypic diversity of natural enemies and their hosts/preys and assess the ability of these enemies to track their hosts/preys through evolutionary changes113 to predict the effect of climate change on BC. Because higher tropic levels, especially predators and parasitoids, are more sensitive than herbivores to habitat fragmentation and connectivity,114 – 116 conservation BC practices, providing shelter or alternative food sources, especially when applied at a higher scale (landscape), may offer tools to alleviate the negative impact of global warming on BC.117 – 119 In the case of exotic invasive pest species, as most of them are originally from warmer climates than that occurring at the new habitat,120 even with limited genotypic diversity in this new location, they may be favoured by climate change relative to their
wileyonlinelibrary.com/journal/ps
natural enemies.17,121,122 For instance, introductions of tropical species of spider mites into Europe have increased 50% in the last 30 years.123 Moreover, warmer conditions in temperate areas may create new possibilities not only for invasive species to become established but also for pest outbreaks. Indeed, recent studies have attributed herbivore control disruption in some agroecosystems to severe environmental conditions.56,122,124 In the case of BC strategies exploiting exotic natural enemies, either classical, inoculative or inundative108 (Table 1), it is widely known that the practices used in collection, importation, quarantine, rearing and release phases of an introduction may lead to reduced fitness, or at least to reduced genetic variation.111,125 In fact, de Boer et al.126 illustrated how bottlenecks associated with BC could be particularly detrimental in parasitoid Hymenoptera. The numbers of individuals eventually introduced for BC are typically small, resulting in reduced genotypic diversity of the initial founding population.105,112 This reduced genetic variation may seriously hamper the response of exotic natural enemies to new environmental conditions. In these cases, it may be possible to respond to climate change by selecting in their areas of origin and releasing in the target region natural enemies better adapted to these new environmental conditions. Genetic diversity and phenotypic plasticity to different environmental conditions have been demonstrated for several natural enemies. For example, White et al.127 successfully selected for tolerance to extreme temperatures various populations of Aphytis lingnanensis Compere (Hymenoptera: Aphelinidae) derived from a large gene pool in California. Similarly, evidence for genetic variation in populations of Lysiphlebus testaceipes (Cresson) (Hymenoptera: Aphidiidae) with different thermal requirements was demonstrated by Shufran et al.128 Walzer et al.129,130 found natural variation in response to dry conditions for Neoseiulus californicus (McGregor) (Acari: Phytoseiidae) strains collected in different geographic areas. Even more complex traits, such as generation time in Trichogramma aurosum Sugonjaev and Sorokina (Hymenoptera: Trichogrammatidae),131 or the ability to synthesise lipids in Leptopilina boulardi (Barbotin et al.) (Hymenoptera: Figitidae),132 have been shown to change between populations subjected to different environmental conditions. As before, once identified, successfully reared and released,
c 2013 Society of Chemical Industry
Pest Manag Sci 2014; 70: 853–859
Climate Change and Biological Control
www.soci.org
conservation BC may help these recently introduced genotypes to persist in the new environment and show their full potential.
5
CONCLUSION
It is difficult to forecast the effect of climate change on the interactions between trophic levels, as these interactions are generally complex. For the practice of BC, new strategies for selecting exotic natural enemies and their release and establishment will need to be adopted. A thorough understanding of the genotypic diversity of the populations of natural enemies and their target pests will be necessary to adequately react to global warming. Furthermore, conservation BC techniques will have to be put in place to facilitate populations of natural enemies to endure in our changing world.
ACKNOWLEDGEMENTS A Tena and A Urbaneja (IVIA, Montcada, Spain) made valuable comments on an early draft of this manuscript. While working on the manuscript, the authors received financial support from the Spanish Plan Nacional R+D (AGL2011-30538-C03-01) and European FP7 (KBBE.2011.1.2-12).
REFERENCES
Pest Manag Sci 2014; 70: 853–859
c 2013 Society of Chemical Industry
wileyonlinelibrary.com/journal/ps
857
1 Baede APM, Appendix I: Glossary. Intergovernmental Panel on Climate Change, IPCC Third Assessment Report – Climate Change 2001, Working Group I: The Scientific Basis. [Online]. Available: http://www.grida.no/publications/other/ipcc_tar/?src=/climate/ ipcc_tar/wg1/518.htm [17 July 2013]. 2 Field CB, Barros V, Stocker TF, Qin D, Dokken DJ, Ebi KL, et al, Managing the risks of extreme events and disasters to advance climate change adaptation. IPCC Special Reports. [Online]. Cambridge University Press (2012). Available: http://www.ipcc.ch/pdf/specialreports/srex/SREX_Full_Report.pdf [17 July 2013]. 3 Lobell DB and Gourdji SM, The influence of climate change on global crop productivity. Plant Physiol 160:1686–1697 (2012). ´ e´ C, Boden T, Canadell JG and Raupach 4 Peters GP, Marland G, Le Quer MR, Rapid growth in CO2 emissions after the 2008–2009 global financial crisis. Nat Clim Change 2:2–4 (2011). 5 Now what? The Keeling Curve, a Daily Record of Atmospheric Carbon Dioxide. [Online]. Scripps Institution of Oceanography, UC San Diego, La Jolla, CA (2013). Available: http://keelingcurve. ucsd.edu/now-what/ [17 July 2013]. 6 Peters GP, Andrew R, Boden T, Canadell J, Ciais P, Le Qu´ere´ C, et al, The challenge to keep global warming below two degrees. Nat Clim Change 3:4–6 (2013). 7 Lobell DB, Bonfils C and Duffy PB, Climate change uncertainty for daily minimum and maximum temperatures: a model inter-comparison. Geophys Res Lett 34:L05715 (2007). 8 Hill JK, Griffiths HM and Thomas CD, Climate change and evolutionary adaptations at species’ range margins. Annu Rev Entomol 56:143–159 (2011). 9 Lobell DB, Schlenker WS and Costa-Roberts J, Climate trends and global crop production since 1980. Science 333:616–620 (2011). 10 Alexander LV, Zhang X, Peterson TC, Caesar J, Gleason B, Klein Tank A, et al, Global observed changes in daily climate extremes of temperature and precipitation. J Geophys Res 111:D05109 (2006). 11 Sheffield J and Wood EF, Global trends and variability in soil moisture and drought characteristics, 1950–2000, from observation-driven simulations of the terrestrial hydrologic cycle. J Clim 21:432–458 (2008). 12 Dai A, Drought under global warming: a review. Wires Clim Change 2:45–65 (2011). 13 Hairston NG, Smith FE and Slobodkin LS, Community structure, population control, and competition. Am Nat 94:421–425 (1960). 14 Oksanen L, Fretwell SD, Arruda J and Niemela P, Exploitation ecosystems in gradients of primary productivity. Am Nat 118:240–261 (1981).
15 Thomas CD, Cameron A, Green RE, Bakkenes M, Beaumont LJ, Collingham YC, et al, Extinction risk from climate change. Nature 427:145–148 (2004). 16 Vinebrooke RD, Schindler DW, Findlay DL, Turner KH, Paterson MA and Milis M, Trophic dependence of ecosystem resistance and species compensation in experimentally acidified Lake 302S (Canada). Ecosystems 6:101–113 (2003). 17 Foden W, Mace G, Vie´ JC, Angulo A, Butchart SHM, DeVantier L, et al, Species susceptibility to climate change impacts, in Wildlife in a Changing World: an Analysis of the 2008 IUCN Red List of Threatened Species, ed. by Vi´e JC, Hilton-Taylor C and Stuart SN. IUCN, Gland, Switzerland, pp. 77–88 (2008). 18 DeLucia EH, Casteel CL, Nabity PD and O’Neill BF, Insects take a bigger bite out of plants in a warmer, higher carbon dioxide world. Proc Natl Acad Sci USA 105:1781–1782 (2008). 19 Johnson SN and McNicol JW, Elevated CO2 and aboveground–belowground herbivory by the clover root weevil. Oecologia 162:209–216 (2010). 20 Stiling P, Forkner R and Drake B, Long-term exposure to elevated CO2 in a Florida scrub-oak forest increases herbivore densities but has no effect on other arthropod guilds. Insect Conserv Diver 3:152–156 (2010). 21 Parmesan C, Ryrholm N, Stefanescu C, Hill JK, Thomas CD, Descimon H, et al, Poleward shifts in geographical ranges of butterfly species associated with regional warming. Nature 399:579–583 (1999). 22 Bale JS, Masters GJ, Hodkinson ID, Awmack C, Bezemer TM, Brown VK, et al, Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Glob Change Biol 8:1–16 (2002). 23 Hickling R, Roy DB, Hill JK, Fox R and Thomas CD, The distributions of a wide range of taxonomic groups are expanding polewards. Glob Change Biol 12:450–455 (2006). 24 Musolin DL and Fujisaki K, Changes in ranges: trends in distribution of true bugs (Heteroptera) under conditions of the current climate warming. Russ Entomol J 15:175–179 (2006). 25 Berg MP, Kiers ET, Driessen G, van der Heijden M, Kooi BW, Kuenen F, et al, Adapt or disperse: understanding species persistence in a changing world. Glob Change Biol 16:587–598 (2010). 26 Rosenzweig C, Iglesias A, Yang XB, Epstein PR and Chivian E, Climate change and extreme weather events: implications for food production, plant diseases, and pests. Glob Change Hum Hlth, 2:90–104 (2001). 27 Wheeler T and von Braun J, Climate change impacts on global food security. Science 341:508–513 (2013). 28 Garrett KA, Dendy SP, Frank EE, Rouse MN and Travers SE, Climate change effects on plant disease: genomes to ecosystems. Annu Rev Phytopathol 44:489–509 (2006). 29 Fuhrer J, Agroecosystem responses to combinations of elevated CO2 , ozone, and global climate change. Agric Ecosyst Environ 97:1–20 (2003). 30 Harmens H and Mills G, Review of the influence of climate change on the impacts of ozone on vegetation. The UNECE International Cooperative Programme on Vegetation. [Online]. Natural Environment Research Council CEH Project No. C02309, Centre for Ecology and Hydrology, Bangor, UK (2005). Available: http://uk-air.defra.gov.uk/reports/cat10/0510100939_EPG_1-3205_Final_Report.pdf [17 July 2013]. 31 Battisti A, Masutti L, Paoletti E and Ragazzi A, Silviculture: forest protection. Ital J For Mount Environ 65:239–244 (2010). 32 Mattson WJ and Haack RA, The role of drought in outbreaks of plant eating insects. Bioscience 37:110–118 (1987). 33 Berryman AA, What causes population cycles of forest Lepidoptera? Trends Ecol Evol 11:28–32 (1996). 34 Ode PJ, Plant chemistry and natural enemy fitness: effects on herbivore and natural enemy interactions. Annu Rev Entomol 51:163–185 (2006). 35 Bruessow F, Asins MJ, Jacas JA and Urbaneja A, Replacement of CTV-susceptible sour orange rootstock by CTV-tolerant ones may have triggered outbreaks of Tetranychus urticae in Spanish citrus. Agric Ecosyst Environ 137:93–98 (2010). 36 Jamieson MA, Trowbridge AM, Raffa KF and Lindroth RL, Consequences of climate warming and altered precipitation patterns for plant–insect and multitrophic interactions. Plant Physiol 160:1719–1727 (2012).
858
www.soci.org
E Aguilar-Fenollosa, JA Jacas
37 von Tiedemann A and Firsching KH, Interactive effects of elevated ozone and carbon dioxide on growth and yield of leaf rust-infected versus non-infected wheat. Environ Pollut 108:357–363 (2000). 38 Pritchard SG, Rogers HH, Prior SA and Peterson CM, Elevated CO2 and plant structure: a review. Glob Change Biol 5:807–837 (1999). 39 Bezemer TM and Jones TH, Plant–insect herbivore interactions in elevated CO2 : quantitative analyses and guild effects. Oikos 82:212–222 (1998). 40 Ballhorn DJ, Reisdorff C and Pfanz H, Quantitative effects of enhanced CO2 on jasmonic acid induced plant volatiles of lima bean (Phaseolus lunatus L.). J Appl Bot Food Qual 84:65–71 (2011). 41 Robinson EA, Ryan GD and Newman JA, A meta-analytical review of the effects of elevated CO2 on plant–arthropod interactions highlights the importance of interacting environmental and biological variables. New Phytol 194:321–336 (2012). 42 Gurenstein PG and Hildebrand JG, Roles and effects of environmental carbon dioxide in insect life. Annu Rev Entomol 53:161–178 (2008). 43 Dyer LA, Richards LA, Short SA and Dodson CD, Effects of CO2 and temperature on tritrophic interactions. PLoS One 8:e62528 (2013). 44 Zavala JA, Nabity PD and DeLucia EH, An emerging understanding of mechanisms governing insect herbivory under elevated CO2 . Annu Rev Entomol 58:79–97 (2013). 45 O’Neill BF, Zangerl AR, DeLucia EH, Casteel C, Zavala JA and Berenbaum MR, Leaf temperature of soybean grown under elevated CO2 increases Aphis glycines (Hemiptera: Aphididae) population growth. Insect Sci 18:419–425 (2011). 46 Lincoln DE, Couvet D and Sionit N, Response of an insect herbivore to host plants grown in carbon dioxide enriched atmospheres. Oecologia 69:556–560 (1986). 47 Sch¨adler M, Roeder M, Brandl R and Matthies D, Interacting effects of elevated CO2 , nutrient availability and plant species on a generalist invertebrate herbivore. Glob Change Biol 13:1005–1015 (2007). 48 Hamilton JG, Dermody OC, Aldea M, Zangerl AR, Rogers A, Berenbaum MR, et al, Anthropogenic changes in tropospheric composition increase susceptibility of soybean to insect herbivory. Environ Entomol 34:479–485 (2005). 49 Yuan JS, Himanen SJ, Holopainen JK, Chen F and Stewart CNJ, Smelling global climate change: mitigation of function for plant volatile organic compounds. Trends Ecol Evol 24:323–331 (2009). 50 DeLucia EH, Nabity PD, Zavala JA and Berenbaum MR, Climate change: resetting plant–insect interactions. Plant Physiol 160:1677–1685 (2012). 51 Ainsworth AA, Yendrek CR, Sitch S, Collin WJ and Emberson LD, The effects of tropospheric ozone on net primary productivity and implications for climate change. Annu Rev Plant Biol 63:637–661 (2012). 52 Rao MV, Lee H, Creelman RA, Mullet JE and Davis KR, Jasmonic acid signaling modulates ozone-induced hypersensitive cell death. Plant Cell 12:1633–1646 (2000). 53 van Zyl JL, Canopy temperature as a water stress indicator in vines. S Afr J Enol Vitic 7:53–60 (1986). 54 Holtzer TO, Norman JM, Perring TM, Berry JS and Heintz JC, Effects of microenvironment on the dynamics of spider-mite populations. Exp Appl Acarol 4:247–264 (1988). 55 Leinonen I and Jones HG, Combining thermal and visible imagery for estimating canopy temperature and identifying plant stress. J Exp Bot 55:1423–1431 (2004). 56 Stavrinides MC, Daane KM, Lampinen BD and Mills NJ, Plant water stress, leaf temperature, and spider mite (Acari: Tetranychidae) outbreaks in California vineyards. Environ Entomol 39:1232–1241 (2010). 57 Chaves MM, Flexas J and Pinheiro C, Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560 (2009). 58 Romo CM and Tylianakis JM, Elevated temperature and drought interact to reduce parasitoid effectiveness in suppressing hosts. PLoS One 8:e58136 (2013). 59 Bale JS, Masters GJ, Hodkinson ID, Awmack C, Bezemer TM, Brown VK, et al, Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Glob Change Biol 8:1–16 (2002). 60 Parmesan C, Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669 (2006). 61 Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, et al, Ecological responses to recent climate change. Nature 416:389–395 (2002).
62 Walther GR, Tackling ecological complexity in climate impact research. Science 315:606–607 (2007). 63 Barton BT, Local adaptation to temperature conserves top-down control in a grassland food web. Proc R Soc B 278:3102–3107 (2011). 64 Deutsch CA, Tewksbury JJ, Huey RB, Sheldon KS, Ghalambor CK, Haak DC, et al, Impacts of climate warming on terrestrial ectotherms across latitude. Proc Natl Acad Sci USA 105:6668–6672 (2008). 65 Gienapp P, Teplitsky C, Alho JS, Mills JA and Meril¨a J, Climate change and evolution: disentangling environmental and genetic responses. Mol Ecol 17:167–178 (2008). 66 Skelly DK, Joseph LN, Possingham HP, Freidenburg LK, Farrugia TJ, Kinnison MT, et al, Evolutionary responses to climate change. Conserv Biol 21:1353–1355 (2007). 67 Clark CM and Tilman D, Loss of plant species after chronic low-level nitrogen deposition to prairie grasslands. Nature 451:712–715 (2008). 68 Suttle KB, Thomsen MA and Power ME, Species interactions reverse grassland responses to changing climate. Science 315:640–642 (2007). 69 Chapin FS, Shaver GR, Giblin AE, Nadelhoffer KJ and Laundre JA, Responses of Arctic tundra to experimental and observed changes in climate. Ecology 76:694–711 (1995). ¨ 70 Korner C, Plant CO2 responses: an issue of definition, time and resource supply. New Phytol 172:393–411 (2006). 71 Harrington R, Woiwod I and Sparks T, Climate change and trophic interactions. Trends Ecol Evol 14:146–150 (1999). 72 Quesada-Moraga E, Plagas de insectos y cambio clim´atico. Phytoma 232:1–9 (2011). 73 Nicolas G and Sillans D, Immediate and latent effects of carbon dioxide on insects. Annu Rev Entomol 34:97–116 (1989). 74 Carpenter A and Potter M, Controlled atmospheres, in Quarantine Treatments for Pests of Fruit Plants, ed. by Sharp JL and Hallman GJ. Westview Press, Boulder, CO, pp. 171–198 (1994). 75 Lehmann FO, Dickinson M and Staunton J, The scaling of carbon dioxide release and respiratory water loss in flying fruit flies (Drosophila spp.). J Exp Biol 203:1613–1624 (2000). 76 Guerenstein PG, Christensen TA and Hildebrand JG, Sensory processing of ambient CO2 information in the brain of the moth Manduca sexta. J Comp Physiol 190:707–725 (2004). 77 Guerenstein PG and Hildebrand JG, Roles and effects of environmental carbon dioxide in insect life. Annu Rev Entomol 53:161–178 (2008). 78 Holopainen JK, Himanen SJ and Poppy GM, Climate change and its effects on the chemical ecology of insect parasitoids, in Chemical Ecology of Insect Parasitoids, ed. by Wajnberg E and Colazza S. John Wiley & Sons, Ltd, Chichester, UK, pp. 169–190 (2013). 79 Awmack CS, Harrington R and Leather SR, Host plant effects on the performance of the aphid Aulacorthum solani (Kalt.) (Homoptera: Aphididae) at ambient and elevated CO2 . Glob Change Biol 3:545–549 (1997). 80 Mondor E, Tremblay MN, Awmack CS and Lindroth RL, Altered genotypic and phenotypic frequencies of aphid populations under enriched CO2 and O3 atmospheres. Glob Change Biol 11:1990–1996 (2005). 81 Hulle´ M, d’Acier AC, Bankhead-Dronnet S and Harrington R, Aphids in the face of global changes. C R Biol 333:497–503 (2010). 82 Valkama E, Koricheva J and Oksanen E, Effects of elevated O3 , alone and in combination with elevated CO2 , on tree leaf chemistry and insect herbivore performance: a meta-analysis. Glob Change Biol 13:184–201 (2007). 83 Jackson DM, Heagle AS and Eckel RVW, Ovipositional response of tobacco hornworm moths (Lepidoptera: Sphingidae) to tobacco plants grown under elevated levels of ozone. Environ Entomol 28:566–571 (1999). 84 Holton MK, Lindroth RL and Nordheim EV, Foliar quality influences tree herbivore–parasitoid interactions: effects of elevated CO2 , O3 , and plant genotype. Oecologia 137:233–244 (2003). 85 Mondor EB, Tremblay MN, Awmack CS and Lindroth RL, Divergent pheromone mediated insect behavior under global atmospheric change. Glob Change Biol 10:1820–1824 (2004). 86 Freiwald V, Haikio E, Julkunen-Tiitto R, Holopainen JK and Oksanen E, Elevated ozone modifies the feeding behavior of the common leaf weevil on hybrid aspen through shifts in developmental, chemical, and structural properties of leaves. Entomol Exp Appl 128:66–72 (2008).
wileyonlinelibrary.com/journal/ps
c 2013 Society of Chemical Industry
Pest Manag Sci 2014; 70: 853–859
Climate Change and Biological Control
www.soci.org
87 Kopper BJ and Lindroth RL, Effects of elevated carbon dioxide and ozone on the phytochemistry of aspen and performance of an herbivore. Oecologia 134:95–103 (2003). 88 Agrell J, Kopper B, McDonald EP and Lindroth RL, CO2 and O3 effects on host plant preferences of the forest tent caterpillar (Malacosoma disstria). Glob Change Biol 11:588–599 (2005). 89 Campbell A, Frazer BD, Gilbert N, Gutierrez AP and Mackauer M, Temperature requirements of some aphids and their parasites. J Appl Ecol 11:431–438 (1974). 90 Clarke A, Costs and consequences of evolutionary temperature adaptation. Trends Ecol Evol 18:573–581 (2003). 91 Trudgill DL, Honek A, Li D and Straalen NMV, Thermal time – concepts and utility. Ann Appl Biol 146:1–14 (2005). 92 Beveridge OS, Humphries S and Petchey OL, The interacting effects of temperature and food chain length on trophic abundance and ecosystem function. J Anim Ecol 79:693–700 (2010). 93 Gillespie DR, Nasreen A, Moffat CE, Clarke P and Roitberg BD, Effects of simulated heat waves on an experimental community of pepper plants, green peach aphids and two parasitoid species. Oikos 121:149–159 (2012). 94 Almeda R, Augustin CB, Alcaraz M, Calbet A and Saiz E, Feeding rates and gross growth efficiencies of larval developmental stages of Oithona davisae (Copepoda, Cyclopoida). J Exp Mar Biol Ecol 387:24–35 (2010). 95 Jalali MA, Tirry L and De Clercq P, Effect of temperature on the functional response of Adalia bipunctata to Myzus persicae. BioControl 55:261–269 (2010). 96 Petchey OL, Brose U and Rall BC, Predicting the effects of temperature on food web connectance. PhilTransRSocB 365:2081–2091 (2010). 97 Hance T, van Baaren J, Vernon P and Boivin G, Impact of extreme temperatures on parasitoids in a climate change perspective. Annu Rev Entomol 52:107–126 (2007). 98 van der Putten WH, de Ruiterb PC, Bezemera TM, Harvey JA, Wassen M and Wolters V, Trophic interactions in a changing world. Basic Appl Ecol 5:487–494 (2004). 99 Voigt W, Perner J, Davis AJ, Eggers T, Schumacher J, Bahrmann R, et al, Trophic levels are differentially sensitive to climate. Ecology 84:2444–2453 (2003). 100 Cagnolo L, Molina SI and Valladares GR, Diversity and guild structure of insect assemblages under grazing and exclusion regimes in a montane grassland from Central Argentina. Biodivers Conserv 11:407–420 (2002). 101 Begon M, Harper JL and Townsend CR, Ecology. Individuals, Populations and Communities. Blackwell Science, Taunton, MA (1990). 102 Singer MS and Bernays EA, Understanding omnivory needs a behavioral perspective. Ecology 84:2532–2537 (2003). 103 Janzen DH, Why mountain passes are higher in the tropics. Am Nat 101:233–249 (1967). 104 Rosner H, Survival of the flexible. Nature 494:22–23 (2013). 105 Roderick GK and Navajas M, Genes in new environments: genetics and evolution in biological control. Nat Rev Genet 4:889–899 (2003). 106 Roderick GK, Hufbauer R and Navajas M, Evolution and biological control. Evol Appl 5:419–423 (2012). 107 DeBach P and Rosen D, Biological Control by Natural Enemies. Cambridge University Press, Cambridge, UK (1991). 108 Eilenberg J, Hajek A and Lomer C, Suggestions for unifying the terminology in biological control. BioControl 46:387–400 (2001). 109 Cock MJ, Biesmeijer JC, Cannon RJ, Gerard PJ, Gillespie D, Jimenez JJ, et al, The implications of climate change for positive contributions of invertebrates to world agriculture. CAB Rev 8:028 (2013). 110 Lewis WJ, Vet LEM, Tumlinson JH, van Lenteren JC and Papaj DR, Variations in parasitoid foraging behavior: essential elements of a sound biological control theory. Environ Entomol 19:1183–1193 (1990). 111 Roderick GK, Tracing the origin of pests and natural enemies: genetic and statistical approaches, in Genetics, Evolution and Biological Control, ed. by Ehler LE, Sforza R and Mateille TT. CABI Publishing, Wallingford, Oxon, UK, pp. 97–112 (2004).
112 Fauvergue X, Vercken E, Malausa T and Hufbauer R, The biology of small, introduced populations, with special reference to biological control. Evol Appl 5:424–443 (2012). 113 Thomson LJ, Macfadyen S and Hoffmann AA, Predicting the effects of climate change on natural enemies of agricultural pests. Biol Control 52:296–306 (2010). 114 Kruess A and Tscharntke T, Habitat fragmentation, species loss, and biological control. Science 264:1581–1584 (1994). 115 Kruess A and Tscharntke T, Species richness and parasitism in a fragmented landscape: experiments and field studies with insects on Vicia sepium. Oecologia 122:129–137 (2000). 116 Hunter MD, Landscape structure, habitat fragmentation, and the ecology of insects. Agric For Entomol 4:159–166 (2002). 117 Boller EF, H¨ani F and Poehling HM, Ecological Infrastructures: Ideabook on Functional Biodiversity at the Farm Level Temperate Zones of Europe. IOBC/WPRS, LBL, Lindau, Switzerland (2004). 118 Fielder KA, Landis DA and Wratten DS, Maximizing ecosystem services from conservation biological control: the role of habitat management. Biol Control 45:254–271 (2008). 119 Mitsch WJ, What is ecological engineering? Ecol Eng 45:5–12 (2012). 120 Parmesan C and Yohe G, A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42 (2003). 121 Mainka SA and Howard GW, Climate change and invasive species: double jeopardy. Integr Zool 5:102–111 (2010). 122 Montserrat M, Guzm´an C, Sahun ´ RM, Belda JE and Hormaza JI, Pollen supply promotes, but high temperatures demote, predatory mite abundance in avocado orchards. Agric Ecosyst Environ 164:155–161 (2013). 123 Navajas M, Migeon A, Estrada-Pena A, Mailleux AC, Servigne P and Petanovic R, Mites and ticks (Acari). BioRisk 4:149–192 (2010). 124 Montserrat M, Sahun ´ RM and Guzm´an C, Can climate change jeopardize predator control of invasive herbivore species? A case study in avocado agro-ecosystems in Spain. Exp Appl Acarol 59:27–42 (2013). 125 Unruh TR and Woolley JB, Molecular methods in classical biological control, in Handbook of Biological Control: Principles and Applications of Biological Control, ed. by Bellows TS, Fisher TW, Caltagirone LE, Dahlsten DL, Gordh G and Huffaker CB. Academic Press, San Diego, CA, pp. 57–85 (1999). 126 de Boer JG, Kuijper B, Heimpel GE and Beukeboom LW, Sex determination meltdown upon biological control introduction of the parasitoid Cotesia rubecula? Evol Appl 5:444–454 (2012). 127 White EB, DeBach P and Garber MJ, Artificial selection for genetic adaptation to temperature extremes in Aphytis lingnanensis Compere (Hymenoptera: Aphelinidae). Hilgardia 40:161–192 (1970). 128 Shufran KA, Weathersbee AA, Jones DB and Elliot NC, Genetic similarities among geographic isolates of Lysiphlebus testaceipes (Hymenoptera: Aphidiidae) differing in cold temperature tolerances. Environ Entomol 33:776–778 (2004). 129 Walzer A, Castagnoli M, Simoni S, Liguori M, Palevsky E and Schausberger P, Intraspecific variation in humidity susceptibility of the predatory mite Neoseiulus californicus: survival, development and reproduction. Biol Control 41:42–52 (2007). 130 Walzer A, Castagnoli M, Simoni S, Liguori M, Palevsky E and Schausberger P, Identification of a drought-adapted Neoseiulus californicus strain: egg hatchability, juvenile survival and oviposition at low humidities, in Trends in Acarology, ed. by Sabelis MW and Bruin J. Springer, Dordrecht, The Netherlands, pp. 279–283 (2010). 131 Samara RY, Monje JC and Zebitz CPW, Comparison of different European strains of Trichogramma aurosum (Hymenoptera: Trichogrammatidae) using fertility life tables. Biocontrol Sci Technol 18:75–86 (2008). 132 Moiroux J, Lann CL, Seyahooei MA, Vernon P, Pierre JS, van Baaren J, et al, Local adaptations of life-history traits of a Drosophila parasitoid, Leptopilina boulardi: does climate drive evolution? Ecol Entomol 35:727–736 (2010).
859
Pest Manag Sci 2014; 70: 853–859
c 2013 Society of Chemical Industry
wileyonlinelibrary.com/journal/ps
