Available online at www.sciencedirect.com
ScienceDirect Insect responses to interacting global change drivers in managed ecosystems Christoph Scherber1,2 Insects are facing an increasingly stressful combination of global change drivers such as habitat fragmentation, agricultural intensification, pollution, or climatic changes. While single-factor studies have yielded considerable insights, multifactor manipulations have gained momentum recently. Nevertheless, most work to date has remained within particular domains of research, such as ‘habitat destruction’ or ‘climate change’, and linkages among subdisciplines within the ecological literature have remained scarce. Here, I provide an overview of the most recent developments in the field, with a focus on main functional groups of insects, but also their interactions with other organisms. All major global change drivers (landscape modification, climate change, agricultural management) are covered both singly and in interaction. The manuscript concludes with concepts on how to statistically and conceptually deal with interactions in experimental and observational work. Addresses 1 Agroecology, Department of Crop Science, Georg-August-University Go¨ttingen, Grisebachstr. 6, 37077 Go¨ttingen, Germany 2 Institute of Landscape Ecology, University of Mu¨nster, Heisenbergstr. 2, 48149 Mu¨nster, Germany Corresponding author: Scherber, Christoph ([email protected]
, [email protected]
Current Opinion in Insect Science 2015, 11:56–62 This review comes from a themed issue on Global change biology Edited by Steven L Chown For a complete overview see the Issue and the Editorial Available online 6th November 2015
just beginning to be explored. In this review, I cover the key concepts necessary to understand insect responses to interacting drivers, show recent experimental progress, and provide approaches to predict the outcome of interacting drivers for insect populations and communities.
Biotic and abiotic drivers of global change Global and anthropogenic environmental changes (GEC) affect what has been termed ‘drivers’ , most of which are directly or indirectly related to human population growth . Classes of drivers important for insects can be grouped by compartments and/or biogeochemical cycles. The most important drivers currently recognized (e.g. ) are land-use change (including habitat loss), climatic changes, pollution, biological invasion, anthropogenic exploitation of resources, and diseases.
The concept of interacting drivers Consider two GEC drivers, for example drought and elevated CO2, dynamic over time. If both drought and elevated CO2 act independently, the outcome (e.g. insect growth) will equal the sum of the impacts of both processes (e.g. negative growth ). However, if both drivers are correlated, the result will be a coupled time series . Recent research  has shown that coupled nonlinear time series can appear uncorrelated, positively or negatively correlated (so-called mirage correlations). While there are methods to reconstruct cause-effect relationships from multiple interacting ecological variables [12,13], applications in the field of GEC research have so far been limited.
http://dx.doi.org/10.1016/j.cois.2015.10.002 2214-5745/# 2015 Elsevier Inc. All rights reserved.
Introduction Human activities are increasingly altering all major components of the Earth system, affecting ecosystem flux rates, biodiversity, and community structure [1,2]. Because many different drivers of global change act simultaneously , the outcome for particular species or communities may be difficult to predict. Insects are the most species-rich group of organisms on Earth [4,5], inhabiting major parts of terrestrial and aquatic ecosystems. Their responses to interacting global change drivers in a multi-factor world  are Current Opinion in Insect Science 2015, 11:56–62
Another approach to multiple interacting GEC drivers is to look at temporally aggregated data, for example by calculating central tendency or working with log-response ratios . In these studies, it has become common practice to classify effects as synergistic, neutral or antagonistic. Recently, the concept of ‘synergism’ versus ‘antagonism’ among drivers was extended  to include terms such as ‘double positive’, ‘positive neutral’ or similar. However, this concept falls short if there are more than two interacting drivers. Other studies  have differentiated additive from synergistic effects, but usually disregarded antagonistic interactions. Overall, three main questions remain to be answered in the context of multiple interacting drivers: (1) Which are the most important individual drivers for insect performance? www.sciencedirect.com
Global change responses in insects Scherber 57
(2) Does the number of drivers per se influence insect performance? (3) Which are the most commonly observed combinations of drivers, and how do they affect insect performance?
Insect responses to single global change drivers Clearly, habitat destruction and conversion from natural to managed systems are among the most important drivers of changes in insect abundance and diversity , affecting agriculturally important processes such as biological control . For example, in a study in 45 Swedish grassland fragments strong negative effects of habitat loss on pollinating insects were reported . Resource consumption in general  has been shown to be negatively affected by habitat fragmentation, especially in specialist species. Conversion from (semi-)natural to managed systems often coincides with changes in farming practices, such as organic versus conventional farming , or increased pesticide use . A particularly recent development is the study of multiple interacting pesticides such as neonicotinoids [23,24,25]. Biotic exchange and biological invasions may affect insects in a variety of ways, depending on the trophic level at which alien taxa enter local communities. For example, invasive alien plants may provide additional resources to herbivores or pollinators, altering the structure of interaction networks . By contrast, invasive insects can dramatically alter top-down control in ecosystems . In the context of climate change research, many studies have focused on altered temperature . For example, Ref.  presented a meta-analysis of responses of insect herbivores to individual drivers and concluded that temperature (but not CO2 or UV radiation) strongly affected key parameters of insect performance. Rapid climate warming may disrupt life-cycle regulation, leading to developmental traps (lost generation hypothesis ). Water availability, which is often closely linked to other climatic changes, can also have profound effects on insect herbivores [31–33], with particularly adverse effects on sap-sucking taxa. In dryland ecosystems, shifts in the trophic position of some insect taxa may be expected, depending on local water availability (reviewed in ). Other drivers, such as nitrogen deposition or elevated CO2 [7,35], have been shown to act indirectly via changes in primary producer abundance, diversity or physiology (but see ). In unfertilized systems, increased CO2 may result in progressive nitrogen limitation [37,38], negatively affecting insect herbivores . www.sciencedirect.com
Number of drivers In classical biodiversity experiments, the number of species present in a system is manipulated . By analogy, one could imagine experiments that explicitly manipulate the number of global change drivers (e.g. ). As more and more drivers are combined, insect performance may be expected to decrease. This would be an example of a sampling effect, where an increasing number of drivers would increase the chance that a particularly adverse driver is present.
Interactions of drivers Increasingly, global change experiments incorporate combinations of GEC drivers [14,40,41] and explicitly test for interactions. In the simplest possible scenario, the interaction among several drivers can be summarized as the sum of individual effects, assuming these effects are additive . However, effects of an interaction may also become stronger over time. For example, growth of insect larvae exposed to combinations of drivers may show complex dynamics over time (Figure 1). Future experiments therefore need to investigate longer-term responses to combined GEC drivers . Several key ingredients are needed to understand interactions among drivers. First, full-factorial manipulations of several factors in experiments are required; that is, we need to move away from experiments manipulating only one or two drivers. Such combined experiments are best done using split-plot or nested designs . Second, interaction terms of sufficient order need to be incorporated in statistical models. Third, it is notoriously difficult to interpret interactions on the basis of numerical model output alone , and interactions should be plotted using twodimensional graphs, preferably showing the individual data points instead of using bar graphs (Figure 2).
Recent developments in the study of interacting drivers Most studies so far focused on two or three interacting global change drivers. For pollinators, a recent analysis showed that global change pressures tend to interact in an additive way ; that is, the result of the interaction is equal to the sum of the individual effect sizes. For example, human-modified landscapes are often characterized by higher abundances of non-native plants and pollinators [46,47]. Several important interactions have remained little explored, such as those between climatic changes and landscape modification , or between agricultural intensification and landscape modification . One of the currently most pressing research questions is the interaction between pesticides and other stressors , including parasites and pathogens affecting pollinators. In addition, interacting global change drivers may unexpectedly affect attractiveness of flowers to pollinators  (Figure 3), reducing globally important pollination services. Current Opinion in Insect Science 2015, 11:56–62
58 Global change biology
Additive vs. non-additive
Number of drivers
Ctrl. Ctrl. Ctrl. Ctrl. 0
T D H C
TD HT CT HD CH DC
Type of effect
TDH CDH THC TDC
TDHC TDHC TDHC TDHC
Number of drivers Current Opinion in Insect Science
Theoretical concepts showing insect responses to (a) additive versus non-additive effects and (b) number of global change drivers. In (a), an additive effect means that the response equals the mean across all treatments (dashed grey line); a positive effect indicates that combinations result in a more positive effect than expected from single drivers; a negative effect indicates that the result is more negative than expected; (b) shows a hypothetical example of four drivers temperature (T), drought (D), habitat fragmentation (H) and increased CO2 (C), where an increased number of drivers leads to a stronger response; (b) is partly on the basis of .
No Drought Drought
Time (weeks) Current Opinion in Insect Science
An example of how to visualize a three-way interaction in global change experiments. The response variable is the weight of beetle larvae (in mg) measured over time (x axis). The two lines in each graph show drought versus ambient treatments, and the two panels show ambient versus elevated CO2. Own figure, on the basis of data from Ref. . Current Opinion in Insect Science 2015, 11:56–62
Global change responses in insects Scherber 59
+ _ eCO2
+ N deposition
Current Opinion in Insect Science
An example showing how the effects of interacting climate change drivers on performance of insect pollinators, herbivores or parasitoids may be visualized as a conceptual structural equation metamodel. While elevated CO2 (eCO2) often reduces plant quality (tissue, nectar), other drivers such as warming or nitrogen deposition increase it; in addition, effects may be direct (dotted arrows) or plant-mediated (solid arrows). Performance may include behavioural aspects (visitation, consumption) or fitness correlates (reproduction, survival). Own figure, synthesized from [10,51,70] and Box S1 in .
For insect herbivores, a wide range of interacting drivers has been studied so far, including land-use intensity and landscape context [52,53,54,55], biodiversity and agricultural management , or climate change components such as altered temperature, CO2, rain, ozone, photoperiod or ultraviolet radiation  (Figure 3), sometimes over long time scales . Many climate change studies have concentrated on warming, altered precipitation or increased CO2 [14,58,59,60,61,62], and only few studies have investigated more than two drivers (but see ). Similar to the findings reported for pollinators, insect herbivores also tend to be affected in a multiplicative way in most cases; that is, the effects of interacting drivers often equals the product of their individual effect sizes . Management of phytophagous agricultural pests in response to global change drivers may require multi-species management approaches . Higher trophic levels, such as carnivores or omnivores (e.g. Carabid beetles , trap-nesting taxa ), or parasitoids [49,67,68], have received fewer attention. A recent study on host-parasitoid interactions in 30 landscapes  found that higher trophic levels were more negatively affected by land-use change (insecticides, annual crop cover) than lower trophic levels. Similar effects were reported for climate change drivers , where herbivore biomass was increased relative to www.sciencedirect.com
parasitoid biomass in response to interacting climate change. Some of these effects may additionally be modified by altered patterns in plant volatile organic compounds or chemistry . Herbivore control by higher trophic levels in agroecosystems may be modified by biotic interactions and landscape complexity . Finally, a large body of literature reports interactive effects of global change drivers on belowground communities [72–75], in which insects or their larval stages act as predators, herbivores, or decomposers. For example, a study manipulating plant biodiversity, atmospheric CO2, and nitrogen deposition found that plant communities of 1, 4 or 9 species had increasingly higher abundances of Thysanoptera, while other belowground insects were only weakly affected by plant diversity, CO2 or nitrogen (with no significant interactions). Understanding interactive global change effects in belowground systems will be considerably improved when traditional analyses are paired with molecular approaches such as next-generation sequencing, allowing more rapid assessments of belowground insect diversity .
Outlook and future directions Recently, interactive effects of global change drivers have been studied in a wide range of insect groups, such as Current Opinion in Insect Science 2015, 11:56–62
60 Global change biology
received funding from the Deutsche Forschungsgemeinschaft (DFG FOR1451/2 ‘The Jena Experiment’), the DFG Graduiertenkolleg 1644 ‘Scaling Problems in Statistics’ and the EU-infrastructure project ‘Increase’. The Danish ‘Climaite’ Experiment consortium is thanked for their support.
Parasitism Predation rates
Barnosky A, Hadly E, Bascompte J, Berlow E, Brown J, Fortelius M, Getz W, Harte J, Hastings A, Marquet P et al.: Approaching a state shift in Earth’s biosphere. Nature 2012, 486:52-58.
Ellis EC: Anthropogenic transformation of the terrestrial biosphere. Philos Transact A Math Phys Eng Sci 2011, 369:1010-1035.
Steffen W, Sanderson A, Tyson PD, Ja¨ger J, Matson PA, Iii BM, Oldfield F, Richardson K, Schellnhuber HJ, Wasson RJ: Global Change and the Earth System: A Planet Under Pressure. Berlin/ Heidelberg/New York: Springer; 2004.
Caley MJ, Fisher R, Mengersen K: Global species richness estimates have not converged. Trends Ecol Evol 2014, 29:187-188.
Mora C, Tittensor DP, Adl S, Simpson AGB, Worm B: How many species are there on earth and in the ocean? PLoS Biol 2011, 9:1-8.
Norby RJ, Luo Y: Evaluating ecosystem responses to rising atmospheric CO2 and global warming in a multi-factor world. New Phytol 2004, 162:281-293.
Hooper DU, Adair EC, Cardinale BJ, Byrnes JEK, Hungate BA, Matulich KL, Gonzalez A, Duffy JE, Gamfeldt L, O’Connor MI: A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 2012, 486:105-U129.
Nelson GC, Bennett E, Berhe AA, Cassman K, DeFries R, Dietz T, Dobermann A, Dobson A, Janetos A, Levy M et al.: Anthropogenic drivers of ecosystem change: an overview. Ecol Soc 2006:11.
Hautier Y, Tilman D, Isbell F, Seabloom EW, Borer ET, Reich PB: Anthropogenic environmental changes affect ecosystem stability via biodiversity. Science 2015, 348:336-340.
Pollination Flower visitation
Major global change drivers Current Opinion in Insect Science
Network thinking in global change research. Major interacting global change drivers affect plant communities; these changes are passed on to higher trophic levels, affecting ecosystem process rates (parasitism, herbivory, etc.) and, ultimately, ecosystem services such as productivity or agricultural yield.
herbivores, pollinators, or predatory insects. Nevertheless, both insects  and global change drivers  interact to form complex networks. Unravelling relationships in such complex networks, and disentangling cause and effect of individual and interacting drivers, will require novel statistical and methodological approaches such as structural equation modelling [10,53,78] (Figure 4), or molecular analyses of trophic interactions . Last but not least, novel experimental facilities are needed, such as next-generation biodiversity  and climate change experiments , where both stochastic and deterministic components of global change are manipulated with sufficient replication. Small-scale, highly controlled experiments need to be combined with largerscale, landscape-wide manipulations  of both global change drivers and trophic interactions . Eventually, novel experiments will allow us to predict and respond to pressures of the future to come.
10. Scherber C, Gladbach DJ, Stevnbak K, Karsten RJ, Schmidt IK, Michelsen A, Albert KR, Larsen KS, Mikkelsen TN, Beier C et al.: Multi-factor climate change effects on insect herbivore performance. Ecol Evol 2013, 3:1449-1460. 11. Crawley MJ: The R Book. edn 2. 2012. 12. Sugihara G, May R, Ye H, Hsieh C-h, Deyle E, Fogarty M, Munch S: Detecting causality in complex ecosystems. Science 2012, 338:496-500. 13. Ma HF, Aihara K, Chen LN: Detecting causality from nonlinear dynamics with short-term time series. Sci Rep 2014:4. 14. Rosenblatt AE, Schmitz OJ: Interactive effects of multiple climate change variables on trophic interactions: a metaanalysis. Clim Change Responses 2014:1. A review paper on interacting climate change drivers and multitrophic interactions. 15. Piggott JJ, Townsend CR, Matthaei CD: Reconceptualizing synergism and antagonism among multiple stressors. Ecol Evol 2015, 5:1538-1547. This paper introduced new terms within the framework of interacting global change drivers. However, interactions were limited to two-way interactions. 16. Brook BW, Sodhi NS, Bradshaw CJ: Synergies among extinction drivers under global change. Trends Ecol Evol 2008, 23:453-460. 17. Sala OE: Global Biodiversity Scenarios for the Year 2100. 2000.
18. Tylianakis JM, Binzer A: Effects of global environmental changes on parasitoid–host food webs and biological control. Biol Control 2014, 75:77-86.
I thank David Gladbach, Karen Stevnbak, Søren Christensen, Claus Beier, and colleagues from the Danish ‘Climaite’ Experiment for help with data collection and field site management (Figure 2 of this manuscript). C.S.
19. Bommarco R, Lindborg R, Marini L, O¨ckinger E: Extinction debt for plants and flower-visiting insects in landscapes with contrasting land use history. Divers Distrib 2014, 20:591-599.
Current Opinion in Insect Science 2015, 11:56–62
Global change responses in insects Scherber 61
20. Martinson HM, Fagan WF: Trophic disruption: a meta-analysis of how habitat fragmentation affects resource consumption in terrestrial arthropod systems. Ecol Lett 2014, 17:1178-1189. 21. Batary P, Baldi A, Kleijn D, Tscharntke T: Landscape-moderated biodiversity effects of agri-environmental management: a meta-analysis. Proc Biol Sci 2011, 278:1894-1902. 22. Geiger F, Bengtsson J, Berendse F, Weisser WW, Emmerson M, Morales MB, Ceryngier P, Liira J, Tscharntke T, Winqvist C: Persistent negative effects of pesticides on biodiversity and biological control potential on European farmland. Basic Appl Ecol 2010, 11:97-105. 23. Gill RJ, Ramos-Rodriguez O, Raine NE: Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature 2012, 491:105-108. 24. Kessler SC, Tiedeken EJ, Simcock KL, Derveau S, Mitchell J, Softley S, Stout JC, Wright GA: Bees prefer foods containing neonicotinoid pesticides. Nature 2015, 521:74-U145. 25. Rundlof M, Andersson GKS, Bommarco R, Fries I, Hederstrom V, Herbertsson L, Jonsson O, Klatt BK, Pedersen TR, Yourstone J et al.: Seed coating with a neonicotinoid insecticide negatively affects wild bees. Nature 2015, 521:77-U162. This paper reported on the effects of neonicotinoid insecticides on pollinator density, growth and reproduction. 26. Bezemer TM, Harvey JA, Cronin JT: Response of native insect communities to invasive plants. Annu Rev Entomol 2014, 59:119-U740.
limited nitrogen availability. Proc Natl Acad Sci U S A 2010, 107:19368-19373. 39. Johnson SN, McNicol JW: Elevated CO2 and abovegroundbelowground herbivory by the clover root weevil. Oecologia 2010, 162:209-216. 40. Rustad LE: The response of terrestrial ecosystems to global climate change: towards an integrated approach. Sci Total Environ 2008, 404:222-235. 41. Tylianakis JM, Didham RK, Bascompte J, Wardle DA: Global change and species interactions in terrestrial ecosystems. Ecol Lett 2008, 11:1351-1363. 42. Sternberg M, Yakir D: Coordinated approaches for studying long-term ecosystem responses to global change. Oecologia 2015, 177:921-924. 43. Schielzeth H, Nakagawa S: Nested by design: model fitting and interpretation in a mixed model era. Methods Ecol Evol 2013, 4:14-24. 44. Jaccard J, Turrisi R: Interaction Effects in Multiple Regression. edn 2. Thousand Oaks (California)/London/New Delhi: Sage Publications; 2003. 45. Gonzalez-Varo JP, Biesmeijer JC, Bommarco R, Potts SG, Schweiger O, Smith HG, Steffan-Dewenter I, Szentgyorgyi H, Woyciechowski M, Vila M: Combined effects of global change pressures on animal-mediated pollination. Trends Ecol Evol 2013, 28:524-530.
27. Snyder WE, Evans EW: Ecological effects of invasive arthropod generalist predators. Annu Rev Ecol Evol Syst 2006, 37:95-122.
46. Williams NM, Cariveau D, Winfree R, Kremen C: Bees in disturbed habitats use, but do not prefer, alien plants. Basic Appl Ecol 2011, 12:332-341.
28. Andrew NR, Hill SJ, Binns M, Bahar MH, Ridley EV, Jung MP, Fyfe C, Yates M, Khusro M: Assessing insect responses to climate change: what are we testing for? Where should we be heading?. PeerJ 2013, 1:e11.
47. Grass I, Berens DG, Peter F, Farwig N: Additive effects of exotic plant abundance and land-use intensity on plant–pollinator interactions. Oecologia 2013, 173:913-923.
29. Bale JS, Masters GJ, Hodkinson ID, Awmack C, Bezemer TM, Brown VK: Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Global Change Biol 2002, 8:1-16. 30. Van Dyck H, Bonte D, Puls R, Gotthard K, Maes D: The lost generation hypothesis: could climate change drive ectotherms into a developmental trap? Oikos 2015, 124:54-61. The authors showed how increased temperatures under climate change affect insect development. 31. Zhu H, Wang DL, Wang L, Fang J, Sun W, Ren BZ: Effects of altered precipitation on insect community composition and structure in a meadow steppe. Ecol Entomol 2014, 39:453-461. 32. Lenhart PA, Eubanks MD, Behmer ST: Water stress in grasslands: dynamic responses of plants and insect herbivores. Oikos 2015, 124:381-390. 33. Huberty A, Denno R: Plant water stress and its consequences for herbivorous insects: a new synthesis. Ecology 2004, 85:1383-1398. 34. McCluney KE, Belnap J, Collins SL, Gonza´lez AL, Hagen EM, Nathaniel Holland J, Kotler BP, Maestre FT, Smith SD: Wolf BO: Shifting species interactions in terrestrial dryland ecosystems under altered water availability and climate change. Biol Rev 2012, 87:563-582. 35. Smith MD, Knapp AK, Collins SL: A framework for assessing ecosystem dynamics in response to chronic resource alterations induced by global change. Ecology 2009, 90:3279-3289. 36. Kerr ED, Phelan C, Woods HA: Subtle direct effects of rising atmospheric CO2 on insect eggs. Physiol Entomol 2013, 38:302-305. 37. Luo Y, Su B, Currie WS, Dukes JS, Finzi AC, Hartwig U, Hungate B, McMurtrie RE, Oren R, Parton WJ et al.: Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. Bioscience 2004, 54:731-739. 38. Norby RJ, Warren JM, Iversen CM, Medlyn BE, McMurtrie RE: CO2 enhancement of forest productivity constrained by www.sciencedirect.com
48. Parsche S, Fru¨nd J, Tscharntke T: Experimental environmental change and mutualistic vs. antagonistic plant flower–visitor interactions. Perspect Plant Ecol Evol System 2011, 13:27-35. 49. Jonsson M, Buckley HL, Case BS, Wratten SD, Hale RJ, Didham RK: Agricultural intensification drives landscapecontext effects on host-parasitoid interactions in agroecosystems. J Appl Ecol 2012, 49:706-714. 50. Goulson D, Nicholls E, Botias C, Rotheray EL: Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 2015, 347:1255957. This paper shows pollinator responses to combined biotic and abiotic global change drivers. 51. Hoover SE, Ladley JJ, Shchepetkina AA, Tisch M, Gieseg SP, Tylianakis JM: Warming, CO2, and nitrogen deposition interactively affect a plant–pollinator mutualism. Ecol Lett 2012, 15:227-234. 52. Liu YH, Rothenwo¨hrer C, Scherber C, Bata´ry P, Elek Z, Steckel J, Erasmi S, Tscharntke T, Westphal C: Functional beetle diversity in managed grasslands: effects of region, landscape context and land use intensity. Landsc Ecol 2014, 29:529-540. 53. Beduschi T, Tscharntke T, Scherber C: Using multi-level generalized path analysis to understand herbivore and parasitoid dynamics in changing landscapes. Landsc Ecol 2015, 30:1975-1986. 54. Kormann U, Ro¨sch V, Bata´ry P, Tscharntke T, Orci KM, Samu F, Scherber C, Ku¨hn I: Local and landscape management drive trait-mediated biodiversity of nine taxa on small grassland fragments. Divers Distrib 2015, 21:1204-1217. Multi-taxa study on insects along several orthogonal gradients in agricultural landscapes. 55. Ro¨sch V, Tscharntke T, Scherber C, Bata´ry P, Osborne J: Landscape composition, connectivity and fragment size drive effects of grassland fragmentation on insect communities. J Appl Ecol 2013, 50:387-394. 56. Everwand G, Rosch V, Tscharntke T, Scherber C: Disentangling direct and indirect effects of experimental grassland management and plant functional-group manipulation on plant and leafhopper diversity. BMC Ecol 2014:14. Current Opinion in Insect Science 2015, 11:56–62
62 Global change biology
57. Ouyang F, Hui C, Ge SY, Men XY, Zhao ZH, Shi PJ, Zhang YS, Li BL: Weakening density dependence from climate change and agricultural intensification triggers pest outbreaks: a 37-year observation of cotton bollworms. Ecol Evol 2014, 4:3362-3374.
70. Jamieson MA, Trowbridge AM, Raffa KF, Lindroth RL: Consequences of climate warming and altered precipitation patterns for plant–insect and multitrophic interactions. Plant Physiol 2012, 160:1719-1727.
58. Robinson EA, Ryan GD, 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 2012, 194:321-336.
71. Martin EA, Reineking B, Seo B, Steffan-Dewenter I: Natural enemy interactions constrain pest control in complex agricultural landscapes. Proc Natl Acad Sci U S A 2013, 110:5534-5539.
59. Zvereva EL, Kozlov MV: Consequences of simultaneous elevation of carbon dioxide and temperature for plant– herbivore interactions: a metaanalysis. Global Change Biol 2006, 12:27-41. A detailed review on the combined effects of elevated CO2 and warming on plants and herbivores.
72. Eisenhauer N, Cesarz S, Koller R, Worm K, Reich PB: Global change belowground: impacts of elevated CO2, nitrogen, and summer drought on soil food webs and biodiversity. Global Change Biol 2012, 18:435-447.
60. Wu Z, Dijkstra P, Koch GW, Pen˜uelas J, Hungate Ba: Responses of terrestrial ecosystems to temperature and precipitation change: a meta-analysis of experimental manipulation. Global Change Biol 2011, 17:927-942. Meta-analysis showing combined effects of warming and precipitation changes on ecosystem variables. 61. Facey SL, Ellsworth DS, Staley JT, Wright DJ, Johnson SN: Upsetting the order: how climate and atmospheric change affects herbivore–enemy interactions. Curr Opin Insect Sci 2014, 5:66-74. A concise overview of how insects at different trophic levels are affected by combinations of climate change drivers. 62. Ryalls JMW, Moore BD, Riegler M, Gherlenda AN, Johnson SN: Amino acid-mediated impacts of elevated carbon dioxide and simulated root herbivory on aphids are neutralized by increased air temperatures. J Exp Bot 2015, 66:613-623. 63. Stevnbak K, Scherber C, Gladbach DJ, Beier C, Mikkelsen TN, Christensen S: Interactions between above- and belowground organisms modified in climate change experiments. Nat Clim Change 2012, 2:805-808. 64. Keren IN, Menalled FD, Weaver DK, Robison-Cox JF: Interacting agricultural pests and their effect on crop yield: application of a Bayesian decision theory approach to the joint management of Bromus tectorum and Cephus cinctus. PLOS ONE 2015:10. A study showing how interacting agricultural pests (insects and invasive weeds) can be managed.
73. Eisenhauer N, Dobies T, Cesarz S, Hobbie SE, Meyer RJ, Worm K, Reich PB: Plant diversity effects on soil food webs are stronger than those of elevated CO2 and N deposition in a long-term grassland experiment. Proc Natl Acad Sci U S A 2013, 110:6889-6894. 74. Xu GL, Kuster TM, Gunthardt-Goerg MS, Dobbertin M, Li MH: Seasonal exposure to drought and air warming affects soil collembola and mites. PLoS ONE 2012:7. 75. McKenzie SW, Hentley WT, Hails RS, Jones TH, Vanbergen AJ, Johnson SN: Global climate change and above-belowground insect herbivore interactions. Front Plant Sci 2013:4. 76. Pompanon F, Deagle BE, Symondson WOC, Brown DS, Jarman SN, Taberlet P: Who is eating what: diet assessment using next generation sequencing. Mol Ecol 2012, 21: 1931-1950. 77. Pocock MJ, Evans DM, Memmott J: The robustness and restoration of a network of ecological networks. Science 2012, 335:973-977. 78. Eisenhauer N, Bowker MA, Grace JB, Powell JR: From patterns to causal understanding: structural equation modeling (SEM) in soil ecology. Pedobiologia 2015, 58:65-72. An overview and introduction to structural equation modelling; though on belowground food webs, it is also of interest for insect ecologists in general.
65. Pozsgai G, Littlewood NA: Ground beetle (Coleoptera: Carabidae) population declines and phenological changes: is there a connection? Ecol Indic 2014, 41:15-24.
79. Ebeling A, Pompe S, Baade J, Eisenhauer N, Hillebrand H, Proulx R, Roscher C, Schmid B, Wirth C, Weisser WW: A traitbased experimental approach to understand the mechanisms underlying biodiversity–ecosystem functioning relationships. Basic Appl Ecol 2014, 15:229-240.
66. Steckel J, Westphal C, Peters MK, Bellach M, Rothenwo¨hrer C, Erasmi S, Scherber C, Tscharntke T, Steffan-Dewenter I: Landscape composition and configuration differently affect trap-nesting bees, wasps and their antagonists. Biol Conserv 2014, 172:56-64.
80. Mikkelsen TN, Beier C, Jonasson S, Holmstrup M, Schmidt IK, Ambus P, Pilegaard K, Michelsen A, Albert K, Andresen LC et al.: Experimental design of multifactor climate change experiments with elevated CO2, warming and drought: the CLIMAITE project. Funct Ecol 2008, 22:185-195.
67. Stangler ES, Hanson PE, Steffan-Dewenter I: Interactive effects of habitat fragmentation and microclimate on trap-nesting Hymenoptera and their trophic interactions in small secondary rainforest remnants. Biodivers Conserv 2015, 24:563-577.
81. Fischer J, Lindenmayer DB: Landscape modification and habitat fragmentation: a synthesis. Global Ecol Biogeogr 2007, 16:265-280.
68. Dyer LA, Richards LA, Short SA, Dodson CD: Effects of CO2 and temperature on tritrophic interactions. PLOS ONE 2013:8. 69. de Sassi C, Tylianakis JM: Climate change disproportionately increases herbivore over plant or parasitoid biomass. PLoS ONE 2012, 7:e40557.
Current Opinion in Insect Science 2015, 11:56–62
82. Legrand D, Guillaume O, Baguette M, Cote J, Trochet A, Calvez O, Zajitschek S, Zajitschek F, Lecomte J, Benard Q et al.: The Metatron: an experimental system to study dispersal and metaecosystems for terrestrial organisms. Nat Methods 2012, 9:828. This paper describes a new experimental facility to study habitat fragmentation and metapopulation ecology.