Uncertainty about old information results in differential predator memory in tadpoles

Abstract

As information ages, it may become less accurate, resulting in increased uncertainty for decision makers. For example, chemical alarm cues (AC) are a source of public information about a nearby predator attack, and these cues can become spatially inaccurate through time. These cues can also degrade quickly under natural conditions, and cue receivers are sensitive to such degradation. Although numerous studies have documented predator-recognition learning from fresh AC, no studies have explored learning from aged AC and whether the uncertainty associated with this older information contributes to shortening the retention of learned responses (i.e. the ‘memory window’). Here, we found that wood frog tadpoles, Lithobates sylvaticus , learned to recognize a novel odour as a predator when paired with AC aged under natural conditions for up to 1 h. However, only tadpoles conditioned with fresh AC were found to retain this learned response when tested 9 days after conditioning. These results support the hypothesis that the memory window is shortened by the uncertainty associated with older information, preventing the long-term costs of a learned association that was based on potentially outdated information.

Uncertainty about predation risk: a conceptual review

“…Other studies have corroborated these findings, revealing that neophobia is a phenotypically plastic trait (Crane & Ferrari, 2017b). Such behaviour benefits prey by improving their odds of surviving initial encounters with novel predators, thus allowing prey to cope with uncertainty until the threat is identified and/or the environment becomes familiar and stable (Crane et al, 2020). The fitness costs of such actions include energetic losses due to increased vigilance and lost opportunities for foraging and mating.…”

“…Chemical cues indicating risk should thus become less reliable as they age. This appears true for wood frog tadpoles that were conditioned to recognise the odour of a novel predator via a pairing with old, rather than fresh, alarm cues (Crane et al, 2023). While tadpoles learned from both types of alarm cues, exposure to the older cues resulted in a shorter retention of the learned response, suggesting that tadpoles were uncertain about whether the older information was relevant.…”

“…Although it was not tested, we would expect the retention of this neophobic response to be shorter than that of their more certain response to the conditioned odour (as in Abudayah & Mathis, 2016). Similar to alarm cues, many species also release chemical 'disturbance cues' (often pulses of waste products) when attacked by a predator (Crane et al, 2022a). However, prey do not need to be injured to release effective concentrations of these cues, which can occur in response to any form of biotic or abiotic disturbance (i.e.…”

“…The psychology literature focuses on uncertainty as a perceptual state, where sensory data and prior knowledge are used to generate beliefs based on incomplete knowledge of the environment, one's relationship to the environment, and the conditional relationships between behavioural action and environmental variables (Downey & Slocum, 1975;Battaglia, 2008). In short, uncertainty is an animal's perception of unpredictability and unknowns (Crane et al, 2020) and can be thought of mathematically as an animal's inability to estimate accurately the probability of an event (Milliken, 1987;Downey & Slocum, 1975). One source of confusion in the literature has arisen from terms like 'environmental uncertainty' being used to describe both the perceptual state of the decision-maker and the variability in the environment (Milliken, 1987).…”

“…This suggests that, at least in some cases, the retention of learned responses (i.e. the 'memory window'; Ferrari et al, 2010a) may be a better proxy for measuring uncertainty than an animal's initial response (Crane et al, 2023).…”