Predator‐ and killed prey‐induced fears bear significant cost to an invasive spider mite: Implications in pest management

Abstract

BACKGROUND The success of biological control using predators is normally assumed to be achieved through direct predation. Yet it is largely unknown how the predator‐ and killed prey‐induced stress to prey may contribute to biological control effectiveness. Here, we investigate variations in life‐history traits and offspring fitness of the spider mite Tetranychus ludeni in response to cues from the predatory mite Phytoseiulus persimilis and killed T. ludeni, providing knowledge for evaluation of the nonconsumptive contribution to the biological control of T. ludeni and for future development of novel spider mite control measures using these cues. RESULTS Cues from predators and killed prey shortened longevity by 23–25% and oviposition period by 35–40%, and reduced fecundity by 31–37% in T. ludeni females. These cues significantly reduced the intrinsic rate of increase (rm) and net population growth rate (R0), and extended time to double the population size (Dt). Predator cues significantly delayed lifetime production of daughters. Mothers exposed to predator cues laid significantly smaller eggs and their offspring developed significantly more slowly but these eggs had significantly higher hatch rate. CONCLUSION Predator‐ and killed prey‐induced fears significantly lower the fitness of T. ludeni, suggesting that these nonconsumptive effects can contribute to the effectiveness of biological control to a great extent. Our study provides critical information for evaluation of biological control effectiveness using predators and paves the way for identification of chemical odors from the predator and killed prey, and development of new materials and methods for the control of spider mite pests. © 2022 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Pest management of postharvest potatoes: lethal, sublethal and transgenerational effects of the ectoparasitic mite Pyemotes zhonghuajia on the potato worm Phthorimaea operculella

“…We further reveal that PTM adults that developed from the fourth‐instar larvae that were exposed to parasitism/predation risk during feeding (Experiment 3) or parasitized by P. zhonghuajia females for a short period of time (i.e., 30 or 60 min in Experiment 4) had significantly lower fecundity and/or shorter adult longevity compared to the controls (Tables 1 and 2), supporting the finding that sublethal stress reduces host survival and reproduction, as reported in many studies 58,75–79 . As reported in other ectophagous idiobiont parasitoids, 47–54 P. zhonghuajia females inject venom to paralyze hosts and suppress their immune responses 29,31 .…”

“…Nutrients used for host feeding by parasitoids will not be available for the survival and reproduction of hosts. We further showed that PTM females also had significantly lower reproductive output when their mothers experienced predation risk (Table 2), indicating that nonconsumptive impacts on prey may be transgenerational 78–81 …”

“…74 We further reveal that PTM adults that developed from the fourth-instar larvae that were exposed to parasitism/predation risk during feeding (Experiment 3) or parasitized by P. zhonghuajia females for a short period of time (i.e., 30 or 60 min in Experiment 4) had significantly lower fecundity and/or shorter adult longevity compared to the controls (Tables 1 and 2), supporting the finding that sublethal stress reduces host survival and reproduction, as reported in many studies. 58,[75][76][77][78][79] As reported in other ectophagous idiobiont parasitoids, [47][48][49][50][51][52][53][54] P. zhonghuajia females inject venom to paralyze hosts and suppress their immune responses. 29,31 Becchimanzi et al demonstrate that in Bracon nigricans Szépligeti, a generalist ectophagous idiobiont parasitoid of lepidopteran larvae, the injected venom induces the formation of macrogranulocytes, which trigger a rapid histolysis of host fat body and the mobilization of stored nutrients to make them suitable and available for host feeding by parasitoids.…”

“…We further showed that PTM females also had significantly lower reproductive output when their mothers experienced predation risk (Table 2), indicating that nonconsumptive impacts on prey may be transgenerational. [78][79][80][81] Insects may slow down 69,78,79,82,83 or accelerate development 77,84,85 in response to nonconsumption effects or predation stress. However, the development of different life stages of PTM was not significantly different between treatments in the parental (Table 2) and offspring generations (Tables 1 and 2), regardless of the mature fourth-instar larvae being exposed to sublethal stress (i.e., exposed to mites of various densities, Experiment 3) or lethal stress (i.e., parasitized for various durations, Experiment 4).…”

Predator densities alter the influence of non‐consumptive effects on the population dynamics of an agricultural pest

“…In biocontrol, more generally, the ways in which risk-induced trait responses might mitigate or amplify management practices are being increasingly recognised (Culshaw-Maurer et al, 2020), and NCEs have now been observed in many agricultural pest species. For example, effects of risk-induced trait responses on pest demographic rates have been demonstrated in aphids (Bannerman et al, 2011;Fievet et al, 2008;Nelson, 2007), spider mites (Gyuris et al, 2017;Ristyadi et al, 2022), planthoppers (Wen & Ueno, 2021) and lepidopterans (Griffin & Thaler, 2006;Xiong et al, 2015). Risk-induced stress responses, and predator avoidance behaviours in particular, can be leveraged to reduce pest populations by deploying predator cues (e.g., pheromones) rather than predators themselves (Aflitto & Thaler, 2020).…”