Learned predation risk management by spider mites

Abstract

Predation is a prime selective force shaping prey behavior. Investment in anti-predator behavior is traded-off against time and energy for other fitness-enhancing activities such as foraging or reproduction. To optimize this benefit/cost trade-off, prey should be able to innately and/or by experience modulate their behavior to the level of predation risk. Here, we assessed learned predation risk management in the herbivorous two-spotted spider mite Tetranychus urticae. We exposed spider mites coming from benign (naïve) or high immediate predation risk (experienced) environments to latent and/or no risk and assessed their site choice, activity and oviposition. Benign environments were characterized by the absence of any predator cues, high immediate risk environments by killed spider mites, physical presence of the predatory mite Phytoseiulus persimilis and associated chemosensory traces left on the surface, and latent risk environments by only predator traces. In the no-choice experiment both naïve and experienced spider mites laid their first egg later on leaves with than without predator traces. Irrespective of predator traces presence/absence, experienced mites laid their first egg earlier than naïve ones did. Naïve spider mites were more active, indicating higher restlessness, and laid fewer eggs on leaves with predator traces, whereas experienced mites were less active and laid similar numbers of eggs on leaves with and without predator traces. In the choice experiment both naïve and experienced spider mites preferentially resided and oviposited on leaves without predator traces but experienced mites were less active than naïve ones. Overall, our study suggests that spider mites experienced with high predation risk behave bolder under latent risk than naïve spider mites. Since predator traces alone do not indicate immediate risk, we argue that the attenuated anti-predator response of experienced spider mites represents adaptive learned risk management.

Within‐patch oviposition site shifts by spider mites in response to prior predation risks decrease predator patch exploitation

“…Moreover, Hirayama and Kasuya () found that predator‐experienced water striders oviposit at deeper positions underwater not to avoid current risks, but rather, to avoid future egg parasitism (i.e., precautionary antipredator behavior). Our findings confirmed spider mites’ potential for adaptive learning (e.g., Agrawal, Vala & Sabelis, ; Egas & Sabelis, ; Hackl & Schausberger, ), and suggest that the potential influences of predators on parental care for offspring in many other organisms may have been underestimated and require further study.…”

“…Censored Experienced Naïve behavior). Our findings confirmed spider mites' potential for adaptive learning (e.g., Agrawal, Vala & Sabelis, 2002;Egas & Sabelis, 2001;Hackl & Schausberger, 2014), and suggest that the potential influences of predators on parental care for offspring in many other organisms may have been underestimated and require further study.…”

Maternal intraguild predation risk affects offspring anti-predator behavior and learning in mites

“…They avoided overreaction and saved energy by being less restless in presence of predator traces alone. We argue that the observed behavioral changes represent optimized risk management, as has been shown for various animals including fish, salamanders and spider mites 26 27 28 , i.e. an attenuated response to alarm and/or predator traces following physical predator experience.…”

“…During the learning phase, larvae and early protonymphs were exposed to high IGP risk (physical presence of predator females, their eggs and traces) whereas, in the choice situation, late protonymphs were exposed to sites with and without predator traces, indicating latent risk. Since the predator-experienced protonymphs acted bolder towards predator traces than the naïve ones did, our experiment suggests that learning allowed the protonymphs to distinguish between immediate and latent IGP risks 1 7 8 26 . Since every anti-predator behavior has costs, misjudging the risks associated with a given predator or cue would have negative consequences for prey.…”

Behavioural flexibility in spider mites: oviposition site shifts based on past and present stimuli from conspecifics and predators

“…they respond less actively to predators. For example, predator-experienced spider mites attenuated their anti-predator responses to predator cues [ 5 ].…”