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Phenological Responses in a Sycamore‐Aphid‐Parasitoid System and Consequences for Aphid Population Dynamics: a 20‐Year Case Study

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Phenological Responses in a Sycamore‐Aphid‐Parasitoid System and Consequences for Aphid Population Dynamics: a 20‐Year Case Study This is a repository copy of Phenological responses in a sycamore‐aphid‐parasitoid system and consequences for aphid population dynamics: a 20‐year case study. White Rose Research Online URL for this paper: http://eprints.whiterose.ac.uk/156683/ Version: Accepted Version Article: Senior, V.L., Evans, L.C., Leather, S.R. et al. (2 more authors) (2020) Phenological responses in a sycamore‐aphid‐parasitoid system and consequences for aphid population dynamics: a 20‐year case study. Global Change Biology. ISSN 1354-1013 https://doi.org/10.1111/gcb.15015 This is the peer reviewed version of the following article: Senior, V.L., Evans, L.C., Leather, S.R., Oliver, T.H. and Evans, K.L. (2020), Phenological responses in a sycamore‐aphid‐ parasitoid system and consequences for aphid population dynamics: a 20‐year case study. 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[email protected] https://eprints.whiterose.ac.uk/ 1 Phenological responses in a sycamore-aphid-parasitoid system and consequences for 2 aphid population dynamics: a 20-year case study 3 Climate change and species interactions. 4 Vicki L. Senior1, Luke C. Evans2, Simon R. Leather3, Tom H. Oliver2, Karl L. Evans1 5 1. Animal and Plant Sciences Department, University of Sheffield 6 2. School of Biological Sciences, University of Reading 7 3. Centre for Integrated Pest Management, Harper Adams University 8 9 [email protected] 10 ABSTRACT 11 Species interactions have a spatio-temporal component driven by environmental cues, which 12 if altered by climate change can drive shifts in community dynamics. There is insufficient 13 understanding of the precise time-windows during which inter-annual variation in weather 14 drives phenological shifts and the consequences for mismatches between interacting species 15 and resultant population dynamics – particularly for insects. We use a 20-year study on a tri- 16 trophic system: sycamore Acer pseudoplatanus, two associated aphid species Drepanosiphum 17 platanoidis and Periphyllus testudinaceus, and their hymenopteran parasitoids. Using a sliding 18 window approach, we assess climatic drivers of phenology in all three trophic levels. We 19 quantify the magnitude of resultant trophic mismatches between aphids and their plant hosts 20 and parasitoids, and then model the impacts of these mismatches, direct weather effects and 21 density dependence on local-scale aphid population dynamics. Warmer temperatures in mid- 22 March to late-April were associated with advanced sycamore budburst, parasitoid attack and 23 (marginally) D. platanoidis emergence. The precise time-window during which spring weather 24 advances phenology varies considerably across each species. Crucially, warmer temperatures 1 25 in late winter delayed the emergence of both aphid species. Seasonal variation in warming rates 26 thus generate marked shifts in the relative timing of spring events across trophic levels and 27 mismatches in the phenology of interacting species. Despite this, we found no evidence that 28 aphid population growth rates were adversely impacted by the magnitude of mismatch with 29 their host plants or parasitoids, or direct impacts of temperature and precipitation. Strong 30 density dependence effects occurred in both aphid species and probably buffered populations, 31 through density dependent compensation, from adverse impacts of the marked inter-annual 32 climatic variation that occurred during the study period. These findings explain the resilience 33 of aphid populations to climate change and uncover a key mechanism, warmer winter 34 temperatures delaying insect phenology, by which climate change drives asynchronous shifts 35 between interacting species. 36 37 Key Words – emergence, pests, phytophagous insects, population size, Hymenopteran 38 parasitoids, woodland 39 INTRODUCTION 40 Climate change can influence species populations through direct and indirect mechanisms 41 (Cahill et al. 2013; Ockendon et al. 2014) although indirect mechanisms arising from climate- 42 induced alterations in species interactions frequently appear to be the principal factors driving 43 demographic responses to climate change (Cahill et al. 2013; Ockenden et al. 2014; Ogilvie et 44 al. 2017). The ectothermic physiology of insects means that their fitness is strongly influenced 45 by their surrounding microclimate (Bale et al. 2002). Warmer temperatures during spring and 46 summer may thus directly enhance growth and reproductive rates (Deutsch et al. 2008) but also 47 increase the possibility of heat stress (Kingolver, Diamond and Buckley 2013) leading to 48 increased mortality. Heat stress in temperate insect populations occupying closed habitats, such 49 as woodland, are likely to be limited though as these insects typically experience conditions 2 50 that are within their thermal tolerances (Deutch et al. 2008; Diamond et al. 2012; Sunday et al. 51 2014). 52 The direct effects of changes in precipitation and winter temperatures on insect demography 53 are less well understood than the direct impacts of temperature during spring and summer (Bale 54 & Hayward 2010). Droughts can increase insect mortality through desiccation (Torode et al. 55 2016), whilst heavy rainfall can remove phytophagous insects from their host plants and 56 increase mortality rates (Alford 2000; Rosenzweig, Iglesias, Yang, Epstien & Chivian 2001; 57 Walker, Nault & Simonet 1984). This risk of mortality probably explains why rainy conditions 58 reduce mating behaviour of aphids and other insects – which could thus slow down population 59 growth rates in years of high precipitation (Pellegrino et al 2013). Whilst future changes in 60 spring and summer precipitation in temperate regions, including the UK, are uncertain (with 61 potential for droughts, increased rainfall and more intense rainfall events; Lowe et al. 2018) 62 these changes could influence insect demography. 63 Winter temperature in the UK is predicted to increase by 2-3°C by 2099 (Lowe et al. 2018) 64 which could influence insect demography through a number of mechanisms. Warmer winter 65 conditions can reduce nutritional reserves during the dormant diapause period, leading to 66 increased mortality (Xiao, Chen, Chen, Chen & Wu 2017), and reduced reproductive potential 67 following diapause termination (Irwin & Lee Jr 2000). Warmer winter temperatures may also 68 delay diapause termination (Lehmann, Van Der Bijl, Nylin, Wheat & Gotthard 2017). Some 69 insects do, however, require a certain amount or duration of chilling in order to respond to 70 warming spring temperatures that ultimately terminate diapause (Bosch & Kemp 2003; Chuche 71 & Thiéry 2009, Stålhandske et al. 2015). Warmer conditions experienced during diapause 72 could thus reduce both diapause incidence and duration exposing insects to unfavourable 73 conditions that further increase mortality (Bale & Hayward 2010; Tougeron et al. 2017). 3 74 Indirect impacts are also likely to be a key determinant of insect response to climate change 75 and frequently arise due to changes in the timing of key events including diapause termination 76 and eclosion (Boggs & Inouye 2012; Høye, Post, Schmidt, Trojelsgaard & Forchammer 2013; 77 Kudo & Ida 2013). Earlier emergence and associated increased duration of the period suitable 78 for insect activity could enable multivoltine insects to complete more generations per year, thus 79 increasing population growth rates (Forrest 2016). Phenological shifts could also disrupt 80 interspecific interactions if interacting species exhibit differential responses to climate change 81 (Yang & Rudolph 2010). Changes in insect emergence date relative to host plant leaf burst may 82 affect the abundance and quality of plant material available to phytophagous insects (Dixon 83 1976; Singer & Parmesan 2010). Similarly, changes in the relative timings of insect emergence 84 and the phenology of their natural enemies could alter the duration and intensity of top-down 85 pressures (Godfray, Hassell & Holt 1994; Hicks, Aegerter, Leather & Watt 2007; Van Nouhuys 86 & Lei 2004), although experimentally simulated earlier aphid emergence did not result in 87 aphids escaping subsequent control from late arriving predators (Fuchs et al. 2017). 88 Variation in phenological responses between interacting species may arise frequently 89 (Thackeray et al. 2016) and will occur when species respond to different cues or respond at 90 different rates to the same cue. Spring temperature is clearly associated with advancing 91 phenology in temperate regions, with ectotherms and herbivores exhibiting the strongest 92 responses (Cohen et al. 2018). There is increasing evidence from laboratory studies, however,
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