Pruning of Small Fruit Crops Can Affect Habitat Suitability for Drosophila Suzukii
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Agriculture, Ecosystems and Environment 294 (2020) 106860 Contents lists available at ScienceDirect Agriculture, Ecosystems and Environment journal homepage: www.elsevier.com/locate/agee Pruning of small fruit crops can affect habitat suitability for Drosophila T suzukii Torsten Schöneberga,1, Arielle Arsenault-Benoita,1, Christopher M. Taylora, Bryan R. Butlerb, Daniel T. Daltonc, Vaughn M. Waltonc, Andrew Petrand, Mary A. Rogersd, Lauren M. Diepenbrocke, Hannah J. Burrackf, Heather Leachg, Steven Van Timmereng, Philip D. Fanningg, Rufus Isaacsg, Brian E. Gressh, Mark P. Boldai, Frank G. Zalomh, Craig R. Roubosj, Richard K. Evansj, Ashfaq A. Sialj, Kelly A. Hambya,* a Department of Entomology, University of Maryland, College Park, MD, 20742, USA b Department of Plant Science and Landscape Architecture, College Park, MD, 20742, USA c Department of Horticulture, Oregon State University, Corvallis, OR, 97331, USA d Department of Horticultural Science, University of Minnesota, Saint Paul, MN, 55108, USA e Entomology and Nematology Department, University of Florida, Lake Alfred, FL, 33850, USA f Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC, 27695, USA g Department of Entomology, Michigan State University, East Lansing, MI, 48824, USA h Department of Entomology and Nematology, University of California, Davis, CA, 95616, USA i University of California Cooperative Extension, Santa Cruz County, Watsonville, CA, 95076, USA j Department of Entomology, University of Georgia, Athens, GA 30602, USA ARTICLE INFO ABSTRACT Keywords: Insect activity, survival, and development are affected by climatic conditions that elicit effects at multiple scales. Spotted-wing drosophila Pruning small fruit crop canopies alters the microclimate, which in turn may influence insect pest activity. We Blackberry investigated the effect of three canopy density treatments (high, medium, low)on Drosophila suzukii Blueberry (Matsumura) (Diptera: Drosophilidae) fruit infestation in blueberries and caneberries using a two-year, multi- Raspberry state experiment. We quantified the effect of canopy density on canopy microclimate, fruit quality (total soluble Canopy microclimate solids, fruit firmness), and yield. To better understand heterogeneity in canopy microclimate, parameters were Cultural management further separated by canopy location (exterior vs. interior) in Maryland. In both crops, meta-analyses reveal small magnitude effects of the plant canopy on microclimate, whereas analysis of variance did not separate these effects, with mean canopy differences of 0.1–0.7 °C and 0.5–1.3 % relative humidity (RH) between caneberry canopy densities and locations. In caneberry multi-state trials, 0.14 fewer D. suzukii larvae (g fruit)−1 occurred on average in the low canopy density treatment, and 0.2 fewer D. suzukii larvae (g fruit)−1 occurred in exterior raspberries in Maryland compared with the canopy interior. Artificially infested blueberry fruit indicated im- mature D. suzukii survival within fruit can vary across canopy densities and locations. Although lower total yield was produced in low density canopies, canopy density did not influence berry quality or marketable yield. Microhabitats provide important shelter from extreme environmental conditions; the availability of shelter and ability to locate it affects insect pest populations and distributions. Understanding how crop canopy micro- climate affects D. suzukii infestation can inform efforts to develop habitat manipulation tactics and improve the efficiency of fruit production. 1. Introduction Rinehart et al., 2000; Henderson and Roitberg, 2006). Temperature and relative humidity (RH) influence development rate, phenology, fitness, As poikilothermic organisms, insects are particularly sensitive to population size, distribution, activity, and habitat selection (Bach, fluctuations and extremes in climatic conditions (Ferro et al., 1979; 1993; Drake, 1994; Henderson and Roitberg, 2006; Cui et al., 2008; Li ⁎ Corresponding author at: Department of Entomology, 4112 Plant Sciences, College Park, MD, 20742, USA. E-mail address: [email protected] (K.A. Hamby). 1 Torsten Schöneberg and Arielle Arsenault-Benoit contributed equally to this work. https://doi.org/10.1016/j.agee.2020.106860 Received 1 September 2019; Received in revised form 2 February 2020; Accepted 7 February 2020 Available online 02 March 2020 0167-8809/ © 2020 Elsevier B.V. All rights reserved. T. Schöneberg, et al. Agriculture, Ecosystems and Environment 294 (2020) 106860 et al., 2011; Zhang et al., 2013). To avoid climate stress and thermo- range expansion into new geographic regions has disrupted integrated regulate, insects seek optimal microhabitats (Larmuth, 1979; Leimar pest management (IPM) programs, increasing insecticide sprays in et al., 2003; Henderson and Roitberg, 2006; Adar et al., 2016) in their susceptible crops (Beers et al., 2011; Asplen et al., 2015; Diepenbrock mobile life stages. The availability and accessibility of heterogenous et al., 2017). Insecticides are currently the primary and most efficacious microhabitats underlies ectotherms’ ability to behaviorally buffer management approach in both conventional (Haye et al., 2016) and against climate extremes (Roslin et al., 2009; Scheffers et al., 2014; organic (Sial et al., 2019) systems, and alternative strategies that are Sears et al., 2016). Microclimate heterogeneity occurs at the scale of a economically and environmentally sustainable are needed. In organic single leaf (Ferro et al., 1979; Pincebourde and Casas, 2019), within the production systems where chemical control options are limited, it is plant canopy (Pincebourde et al., 2007), and within a habitat (Suggitt particularly important to implement cultural controls, such as pruning, et al., 2011; Ulyshen, 2011). While scale and time can reduce the to minimize D. suzukii populations. magnitude of climate differences (Faye et al., 2014; Pincebourde and Drosophila suzukii is sensitive to abiotic conditions, and adult ac- Casas, 2019), a wide range of microclimates may occur at distances less tivity within crops correlates with time of day, temperature, and re- than 40 cm (Faye et al., 2017). In agroecosystems, crop microclimate lative humidity. In hot, dry climates D. suzukii captures peak in spring contributes to insect pest distributions and abundances (Saxena and and fall, with less activity during the summer (Wang et al., 2016). Even Saxena, 1975; Ferro et al., 1979; Willmer et al., 1996; Henderson and during the summer when unfavorably hot weather occurs, cooler per- Roitberg, 2006), and affects the success of biological control agents iods of the day (morning and evening hours) are often favorable for (Suh et al., 2002; Shipp et al., 2003). Plant size, architecture, growth activity (Wang et al., 2016; Swoboda-Bhattarai and Burrack, 2020). pattern, and canopy porosity determine canopy microclimate char- Drosophila suzukii adult activity usually occurs in the early morning and acteristics including light penetration, aeration, temperature, humidity, around twilight, during mild temperature and high humidity conditions leaf wetness, and capacity for buffering climate fluctuations (Huber and (Evans et al., 2017; Van Timmeren et al., 2017b; Jaffe and Guédot, Gillespie, 1992; Willaume et al., 2004; Pincebourde et al., 2007; 2019; Tait et al., 2019; Swoboda-Bhattarai and Burrack, 2020). Droso- McDonald et al., 2013); these plant characteristics can be manipulated phila suzukii exhibits optimal development between 22–28 °C, with the through breeding and cultural practices, and can be exploited for pest highest reproductive rate at approximately 23 °C (Ryan et al., 2016). In management (Altieri, 1983; Simon et al., 2006, 2007). a laboratory experiment, Ryan et al. (2016) showed that D. suzukii adult Cultural modification of crop architecture can directly remove in- life span is lowered, no oviposition occurs, and no adults emerge from sect pests as well as reduce their recruitment and survival. For example, eggs exposed to constant temperatures above 30 °C, with no pupation leaf removal in grape (Vitis vinifera L.) vineyards can simultaneously occurring above 31 °C. Simulated “heat waves” with fluctuating tem- remove leafhopper nymphs (Stapleton et al., 1990), and thinning cuts perature and relative humidity also reduce D. suzukii survival and dis- of fruiting spurs may remove aphids in apples (Malus x domestica Borkh) rupt egg production (Eben et al., 2018). Relative humidity in- (Simon et al., 2006). Summer pruning and growth regulators reduce dependently influences D. suzukii survival and habitat preferences. In Lobesia botrana (Denis and Schiffermüller) (Lepidoptera: Tortricidae) the laboratory, female D. suzukii could survive more than 20 days at infestation relative to untreated grapevines (V. vinifera)(Vartholomaiou 71–94 %RH, whereas survival was less than three days between 20–33 et al., 2008), and looser clusters are less favorable to larvae (Fermaud, %RH (Tochen et al., 2016). Drosophila suzukii adults sense humidity, 1998; Vartholomaiou et al., 2008). Canopy complexity and number of favoring high humidity over low humidity in laboratory bioassays branching points also influence dispersal of pests (Simon et al., 2012) as (Fanning et al., 2019). In the field, adults appear to seek areas of high well as host finding by biological control agents (Gingras and Boivin, humidity and low temperature for refuge from unfavorable climatic 2002; Riihimäki et al., 2006). Canopy