Habituation in anuran tadpoles and the role of risk uncertainty

Abstract

The ability to learn in the context of predation allows prey to respond to threats by adjusting their behavior based on specific information acquired from their current environment. Habituation is a process that allows animals to adapt to environmental changes. Very little is known about habituation in wild animals in general and there are no studies on habituation in anuran tadpoles in particular. Here, we performed three experiments to investigate the behavioral response of predator naïve Pleurodema thaul tadpoles to repeated stimulation with two predation risk cues (injured conspecific and predator fed cues) which a priori provide different information regarding risk. Experiment 1 showed that P. thaul tadpoles habituate the antipredator response when undergo predation risk chemical cues from injured conspecific and that response is long term. Experiment 2 showed that P. thaul tadpoles did not habituate their antipredator response when exposed to cues derived from an event of nymph odonate preying on P. thaul tadpoles (predator fed cues). Experiment 3 specifically evaluated the risk imposed by each of the risk cues used in Experiment 1 and Experiment 2 and showed that the degree of perceived risk in tadpoles appear to be similar in a single experience with any risk stimuli. We suggest that the behavioral habituation of tadpoles in the context of predation could be modulated by the level of uncertainty associated with risk stimuli.

Habituation to a predatory stimulus in a harvester (Arachnida, Opiliones)

“…We used a highly threatening stimulus that resembled a predator, since no stimulus other than a predator would pinch and lift the harvester´s body. Moreover, as explained above, we applied a force similar to a bird bite, although we did not provide other putative relevant sensory cues such as shade or olfactory cues of a predator (see Pueta et al 2021 ). We were not expecting habituation to occur based on examples from previous work (Prestrude and Crawford 1970 ; Zangrossi and File 1992 ; Masini et al 2006 ; Ardiel et al 2017 ; Pueta et al 2021 ).…”

“…If animals can remember information about a dangerous event, such learning may positively influence future behavior (Shettleworth 2010 ). After experiencing a predatory attack, being able to maintain a long-term memory could improve not only the defensive behavior itself, but also help avoiding future encounters with such predators by using cues released by the predator in the environment (Pueta et al 2021 ).…”

“…However, regardless of the explanation, the unambiguity of the stimulus per se has not been specifically addressed or studied, that is, there has been no comparison of reactions towards ambiguous and unambiguous stimuli. Previous papers that have reported the absence of habituation (and/or sensitization) are cases in which the stimuli used happened to be unambiguous (Prestrude and Crawford 1970 ; Zangrossi and File 1992 ; Hemmi and Zeil 2003 ; Masini et al 2006 ; but see: Pueta et al 2021 ).…”

Predatory invertebrates indirectly impact leaf‐litter breakdown by different foragers in temporary wetlands

“…We consider activity (time active) as any movement. A tadpole was active when moving its tail, swimming, or generating movement similar to feeding behavior (Pueta et al., 2016, 2022). In the case of caddisfly larvae, we considered an active individual when it was outside the case moving any part of the body or walking.…”

Uncertainty about predation risk: a conceptual review

“…In one example, Chilean four‐eyed frog ( Pleurodema thaul ) tadpoles stopped responding to alarm cues when repeatedly presented alone but not when alarm cues were paired with a predator kairomone, suggesting they were more certain about the paired (i.e. more complete) information (Pueta, Ardanaz & Tallone, 2022). In another example, repeated background exposure to alarm cues, both alone and when paired with a different odour each time, induced subsequent neophobia in wood frog tadpoles (Ferrari et al ., 2018).…”