Functional and Behavioral Responses of the Natural Enemy Anthocoris nemoralis to Cacopsylla pyri, at Different Temperatures

J Insect Behav (2023) 36:222–238 https://doi.org/10.1007/s10905-023-09836-5 RESEARCH Functional and Behavioral Responses of the Natural Enemy Anthocoris nemoralis to Cacopsylla pyri, at Different Temperatures Laura A. Reeves · Michael P. D. Garratt Michelle T. Fountain · Deepa Senapathi · Received: 17 January 2023 / Revised: 20 June 2023 / Accepted: 30 June 2023 / Published online: 7 July 2023 © The Author(s) 2023 Abstract Anthocoris nemoralis is the dominant predator of pear sucker (Cacopsylla pyri) in the UK. Anthocoris nemoralis migrates into orchards in spring or is introduced as a biocontrol agent, reaching peak population levels in July-August, contributing to effective control of summer pear sucker populations. However, due to temperature dependent development and metabolism there are concerns that C. pyri populations or feeding rates may increase due to changing climatic conditions. Thus, how A. nemoralis responds to temperature, impacts its ability as a biocontrol agent. Functional response assays, monitoring attack rate and handling time of A. nemoralis and behavioral assays, using Ethovision tracking software occurred, to assess the impact of temperature on predation. Experiments were conducted at current and future July-August mean temperatures, predicted using RCP4.5 and RCP8.5 (medium and high, representative concentration pathway) emissions scenarios, using 2018 UK Climate Projections Supplementary Information The online version contains supplementary material available at https://doi. org/10.1007/s10905-023-09836-5. L. A. Reeves (*) · M. P. D. Garratt · D. Senapathi Centre for Agri‑Environmental Research, School of Agriculture, Policy and Development, University of Reading, Reading, Berkshire RG6 6AR, UK e-mail: M. T. Fountain NIAB, New Road, East Malling, Kent ME19 6BJ, UK Vol:. (1234567890) 13 (UKCP18). All treatments demonstrated a Type II functional response, with female anthocorids demonstrating shorter handling times and higher attack rates than males. Males showed longer prey handling times at 18 °C compared to 23 °C and more time was spent active at lower temperatures for both sexes. Females did not show significant differences in attack rate or handling time in response to temperature. Overall prey consumption was also not significantly affected by temperature for either sex. This study suggests that anthocorids are likely to remain effective natural enemies under future predicted temperatures, due to nonsignificant differences in prey consumption. Keywords Anthocoris nemoralis · anthocorids · pear sucker · temperature · functional response · behavioral assays. Introduction The anthocorid, Anthocoris nemoralis (Fabricius), is the main natural enemy of pear sucker (Cacopsylla pyri L.) in the UK and Europe (Solomon et al. 2000; Nagy et al. 2008; Sigsgaard 2010). The estimated cost of pear sucker to the UK pear industry is £5 million per annum in damage and control costs (AHDB 2012). These phloem feeding insects damage pear trees in three main ways: nymphs produce honeydew, a sugary secretion that encourages the growth of black sooty mold (Daniel et al. 2005; Salvianti et al. J Insect Behav (2023) 36:222–238 2008; Montanari et al. 2015), adult C. pyri are a vector of pear decline disease (Candidatus Phytoplasma pyri); which reduces shoot and fruit growth in pear and can lead to tree death (Carraro et al. 2001; Kucerová et al. 2007; Süle et al. 2007) and high numbers of C. pyri can cause ‘psylla shock’; toxic saliva is injected into pear leaves, resulting in defoliation and fruit drop (Erler 2004; Saour et al. 2010; Oz and Erler 2021). With a high resistance to commonly available pesticides (Erler 2004; Sek Kocourek and Stará 2006) many growers currently practice integrated pest management (IPM) of pear sucker, focusing on maximizing natural enemy populations, to control pear sucker (Shaw et al. 2021). Natural migrations of anthocorids can reduce pear sucker populations during the summer (Nagy et al. 2008). Adult A. nemoralis often overwinter in hedgerows or on unmanaged vegetation, migrating into orchards in April-May to lay eggs, when pear sucker populations are increasing (Shaltiel and Coll 2004; Nagy et al. 2008). Anthocoris nemoralis populations usually peak during JulyAugust, helping to control C. pyri numbers (Fields and Beirne 1973; Scutareanu et al. 1999). However, anthocorids can also be released artificially into orchards as a biocontrol agent, to reduce pear sucker populations more rapidly (Beninato and Morella 2000; Gajski and Pekár 2021). Nymphs and adult A. nemoralis predate upon pear sucker eggs and nymphs (Sigsgaard 2010) and have a pierce-sucking stylet to feed (Bulgarini et al. 2021). A single anthocorid is estimated to consume almost 5000 eggs during its lifetime (Yanik and Ugur 2004), with no significant preference shown between eggs and nymphs based on biomass (Sigsgaard 2010). There is increasing concern that rising temperatures may impact pest populations (Barford 2013; Sable and Rana 2016; Zidon et al. 2016). Insects are poikilothermic, this means they have a body temperature that fluctuates with their environment (May 1979; Sable and Rana 2016; Wojda 2017). Therefore, rising temperatures could impact pest development (Ratte 1984; Campolo et al. 2014), fecundity (Kindlmann et al. 2001; Boggs 2016), number of generations per year (Tobin et al. 2008), overwintering times (Ladányi and Horváth 2010) and behavior (Mellanby 1939). Pear sucker have temperature dependent development (Kapatos and Stratopoulou 1999; Schaub et al. 2005); faster development rates at warmer temperatures could lead to shorter generation 223 times, potentially increasing pest populations. There is concern that warmer temperatures could alter the feeding behavior, activity and fecundity of phloem feeders (McMullen and Jong 1972; Liu et al. 2021). One explanation for increased feeding rate under high temperatures is due to altered metabolism (Yuan et al. 2009), as metabolic rate increases exponentially with temperature up to a certain threshold, increasing demand for energy and nutrients (Schmitz and Barton 2014; Frances and McCauley 2018). Furthermore, the scale of metabolic increase is largely dependent on body size, with smaller species having higher increases in metabolism than larger species (Frances and McCauley 2018). Thus, as prey species are often smaller than their predators, their metabolism may increase at a faster rate with respect to warming, leading to an enhanced feeding rate. For example, C. pyri adults are less than 3 mm and nymphs in their 5th instar are 1.9 mm in length (Chireceanu 1998), compared to A. nemoralis adults which have a body length of 3.5–4 mm (BPDB 2022). Therefore, feeding rates of pear sucker prey may increase more than their anthocorid predators due to body size. It is important, therefore, to establish whether the feeding rate of A. nemoralis increases with temperature, to understand if it will be an effic (...truncated)