The sensory ecology of adaptive landscapes

Abstract

In complex environments, behavioural plasticity depends on the ability of an animal to integrate numerous sensory stimuli. The multidimensionality of factors interacting to shape plastic behaviour means it is difficult for both organisms and researchers to predict what constitutes an adaptive response to a given set of conditions. Although researchers may be able to map the fitness pay-offs of different behavioural strategies in changing environments, there is no guarantee that the study species will be able to perceive these pay-offs. We thus risk a disconnect between our own predictions about adaptive behaviour and what is behaviourally achievable given the umwelt of the animal being studied. This may lead to erroneous conclusions about maladaptive behaviour in circumstances when the behaviour exhibited is the most adaptive possible given sensory limitations. With advances in the computational resources available to behavioural ecologists, we can now measure vast numbers of interactions among behaviours and environments to create adaptive behavioural surfaces. These surfaces have massive heuristic, predictive and analytical potential in understanding adaptive animal behaviour, but researchers using them are destined to fail if they ignore the sensory ecology of the species they study. Here, we advocate the continued use of these approaches while directly linking them to perceptual space to ensure that the topology of the generated adaptive landscape matches the perceptual reality of the animal it intends to study. Doing so will allow predictive models of animal behaviour to reflect the reality faced by the agents on adaptive surfaces, vastly improving our ability to determine what constitutes an adaptive response for the animal in question.

Keywords: adaptive landscape; behavioural plasticity; fitness surface; perception; sensory ecology.

Figure 1.

A visual nutrient space of autumn leaves. The colour of autumn leaves has been suggested to signal either their toxicity (aposematism) or nutrient value to herbivores (e.g. green leaves are higher in nitrogen than yellow or red leaves). (a) Feeding on greener leaves with a higher probability (y-axis) than yellow or red leaves (x-axis) therefore leads to higher fitness pay-offs. (b) To the visual system of aphids, however, yellow leaves appear as a super-normal green stimulus, and will potentially be fed on with greater probability than other leaves. The fitness surface according to the aphid (b) is therefore very different from the actual fitness surface (a). (Online version in colour.)

Figure 2.

(a) The distribution of a hypothetical predator across space. The presence of predators can create a ‘landscape of fear’ [8], altering the behaviour of prey. The landscape of fear, however, will vary with the ability of prey to perceive the presence of predators, but not all prey and not all sensory modalities sense predators in the same way. (b) The perceived presence of predators by prey that detect predators through the visual modality. Vision gives accurate information about the presence of a predator when it is seen. It relies on direct line of sight, so detection rate can be lower than in other modalities (the prey might not see all the predators in its visual field) and the size of the detection field is typically smaller than in other modalities, but the information about spatial location is more accurate. Note that compared with (a) the peaks in (b) are lower (fewer predators are detected than are actually present), the area of the base of the peaks is smaller (the visual field does not encompass the entire landscape), but the gradient is still steep (i.e. greater accuracy of information). (c) The perceived presence of predators by prey that detect predators through the auditory modality. Sound gives less accurate information about location than visual cues, but because a direct line of sight is not required predators can be detected by acoustic cues over a larger distance than visual cues. Sound is only emitted by the predator when it moves and when it voluntarily makes sound, such as in acoustic communication. Thus, compared with (b) the height of the peaks (predators detected) could be lower if predators tend to be silent, the areas around the peaks are larger (the acoustic detection field is larger than the visual detection field), and the peaks are less steep (the accuracy of localization information is lower). (d) The perceived presence of predators by prey that detect predators through the olfactory modality. Here, we assume that odours are deposited by a predator to mark its territory or home range and thus are non-volatile. Odours provide accurate information about where an individual was but almost no information as to where it is, and this information cannot be detected at any substantial distance from the odour source when odours are used for marking (unlike long-distance olfactory communication in moths and some other animals). Thus, compared with (c) the peaks are high (many prey are detected), the area over which prey can be detected is small and restricted to be within the actual range of the predator (unlike with visual and especially auditory cues when a predator can be detected from a prey outside of its range), and the peaks are not at all steep since the information about the where a predator is at the time the odour cue is sensed in not very accurate. (Online version in colour.)