Tim Guilford

Receiver psychology and the evolution of animal signals

Abstract Despite decades of interest, the adaptive significance of the extraordinary diversity in the design of animal signals remains elusive. It is suggested that signal design consists of two components: ‘strategic design’ and ‘efficacy’. Strategic design is concerned with how a signal is constructed by natural selection to provide the information necessary to make a receiver respond (e.g. by being good at displaying underlying quality), whilst efficacy is concerned with how a signal is designed to get that information across to the receiver (e.g. by being easily measured). It is argued that an important but neglected evolutionary force on animal signals is therefore the psychology of the signal receiver, and that three aspects of receiver psychology (what a receiver finds easy to detect, easy to discriminate and easy to remember) constitute powerful selective forces in signal design. Greatest emphasis is given to memorability because this has been least considered by previous authors. It is argued that learning and memory are involved in a wide range of signals, and numerous hypotheses as to how signals may be adapted to be more memorable to receivers are suggested. The relationship of this analysis to earlier attempts at understanding signals is explored, particularly with reference to the concepts of honesty, manipulation and mind-reading.

The corruption of honest signalling

Abstract It is argued that recent analyses of the evolution of animal signals, which claim that signalling systems must be honest indicators of underlying quality, have neglected a vital consideration: the costs receivers pay in assessment. Where the costs of fully assessing a signaller are high, in terms of energy, time, or risk, and the value of the extra information gained is low, then it will pay receivers to settle for cheaper, but less reliable, indicators of quality instead. Thus, it is argued, honest assessment will be replaced by conventional signalling. Conventional signals are open to cheating, but cheating will be kept at low frequencies by the frequency-dependent benefits of occasional assessment (or ‘probing’), so dishonest signalling remains stable. The concept of ‘honesty’ is discussed.

Migration and stopover in a small pelagic seabird, the Manx shearwater Puffinus puffinus: insights from machine learning

The migratory movements of seabirds (especially smaller species) remain poorly understood, despite their role as harvesters of marine ecosystems on a global scale and their potential as indicators of ocean health. Here we report a successful attempt, using miniature archival light loggers (geolocators), to elucidate the migratory behaviour of the Manx shearwater Puffinus puffinus, a small (400 g) Northern Hemisphere breeding procellariform that undertakes a trans-equatorial, trans-Atlantic migration. We provide details of over-wintering areas, of previously unobserved marine stopover behaviour, and the long-distance movements of females during their pre-laying exodus. Using salt-water immersion data from a subset of loggers, we introduce a method of behaviour classification based on Bayesian machine learning techniques. We used both supervised and unsupervised machine learning to classify each birds daily activity based on simple properties of the immersion data. We show that robust activity states emerge, characteristic of summer feeding, winter feeding and active migration. These can be used to classify probable behaviour throughout the annual cycle, highlighting the likely functional significance of stopovers as refuelling stages.

The Evolution of Multimodal Warning Displays

Multimodal warning displays combine visual signals with components produced in other sensory modalities, for instance, aposematically coloured insects often produce a pungent odour or harsh sound when they are attacked. Recent research has focussed upon a particular odour, pyrazine, which is commonly associated with warning coloration. Our experiments have shown that pyrazine elicits hidden unlearned biases against particular visual aspects of food in foraging domestic chicks. Here we asses the current state of our knowledge about these biases, reviewing our results using pyrazine and other odours, and also presenting new data showing that sound can produce similar effects. We will discuss potential psychological mechanisms by which these foraging biases are achieved in avian predators, and potential pathways for their evolution.

Search images not proven: A reappraisal of recent evidence

Abstract It is commonly agreed that predators hunting for cryptic prey have been demonstrated to adopt search images (involving perceptual specialization) for particular prey types. However, a simple alternative strategy, that of an appropriate reduction in search rate, may in many cases have the same effect as adopting a search image. The search image and search rate hypotheses are examined, and a series of critical predictions are proposed to distinguish them. Briefly, the search rate hypothesis predicts: (1) that adjusting search rate for one cryptic prey type will enhance the ability to detect other equally cryptic types (the search image hypothesis predicts that this will interfere with the ability to detect other equally cryptic types); (2) that adjusting search rate for cryptic prey will be achieved by learning to spend longer looking at each patch of the environment, and that the more cryptic the prey the longer will be the viewing time required to effect accurate detection (the search image hypothesis makes no such predictions). Four recent studies purporting to demonstrate search images are re-examined in the light of these predictions, and it is found that the published data fail to distinguish the two hypotheses. In addition, some evidence that is better explained by the search rate hypothesis is discussed. A brief examination of the ecological consequences of the search rate hypothesis shows that, unlike the search image hypothesis, it does not predict apostatic selection. It is therefore argued that the distinction between the two mechanisms explaining how predators ‘learn to see’ cryptic prey is important, but that the critical tests have not yet been made. The existence of search images remains not proven.

What are conventional signals

Abstract Confusion over the validity of ‘conventional signalling’ may have resulted at least in part because it has been used to refer to different concepts. The main aim of this paper is to expose the source of this confusion, not to prescribe a particular solution. Two key current senses of conventional signals are identified: (1) as strategic correlates of quality (or, more generally, of the parameter about which information is contained in the signals message); (2) as signals whose design is arbitrarily related to their message. The sometimes difficult relationships between these two senses and other concepts in the signalling literature (assessment signals, strategic choice handicaps, direct indicators, revealing handicaps) are explored. It is concluded that two separate but important distinctions have been used to characterize conventional signals (first, whether or not signals allow strategic choice, and, second, whether signalling costs are intrinsic to the signals production), and that these remain of significance to the understanding of signal design. The paper concentrates mainly on signalling between parties with conflicting evolutionary interests, but briefly shows how these concepts may relate to signalling systems with no conflict of interest.

Homing pigeons develop local route stereotypy.

The mechanisms used by homing pigeons (Columba livia) to navigate homeward from distant sites have been well studied, yet the mechanisms underlying navigation within, and mapping of, the local familiar area have been largely neglected. In the local area pigeons potentially have access to a powerful navigational aid--a memorized landscape map. Current opinion suggests that landmarks are used only to recognize a familiar start position and that the goalward route is then achieved solely using compass orientation. We used high-resolution global positioning system (GPS) loggers to track homing pigeons as they became progressively familiar with a local homing task. Here, we demonstrate that birds develop highly stereotyped yet individually distinctive routes over the landscape, which remain substantially inefficient. Precise aerial route recapitulation implies close control by localized geocentric cues. Magnetic cues are unlikely to have been used, since recapitulation remains despite magnetic disruption treatment, and olfactory cues would have been positionally unstable under the variable wind conditions, making visual landmarks the most likely cues used.

A dispersive migration in the Atlantic Puffin and its implications for migratory navigation.

Navigational control of avian migration is understood, largely from the study of terrestrial birds, to depend on either genetically or culturally inherited information. By tracking the individual migrations of Atlantic Puffins, Fratercula arctica, in successive years using geolocators, we describe migratory behaviour in a pelagic seabird that is apparently incompatible with this view. Puffins do not migrate to a single overwintering area, but follow a dispersive pattern of movements changing through the non-breeding period, showing great variability in travel distances and directions. Despite this within-population variability, individuals show remarkable consistency in their own migratory routes among years. This combination of complex population dispersion and individual route fidelity cannot easily be accounted for in terms of genetic inheritance of compass instructions, or cultural inheritance of traditional routes. We suggest that a mechanism of individual exploration and acquired navigational memory may provide the dominant control over Puffin migration, and potentially some other pelagic seabirds, despite the apparently featureless nature of the ocean.

Pigeons combine compass and landmark guidance in familiar route navigation

How do birds orient over familiar terrain? In the best studied avian species, the homing pigeon (Columba livia), two apparently independent primary mechanisms are currently debated: either memorized visual landmarks provide homeward guidance directly, or birds rely on a compass to home from familiar locations. Using miniature Global Positioning System tracking technology and clock-shift procedures, we set sun-compass and landmark information in conflict, showing that experienced birds can accurately complete their memorized routes by using landmarks alone. Nevertheless, we also find that route following is often consistently offset in the expected compass direction, faithfully reproducing the shape of the track, but in parallel. Thus, we demonstrate conditions under which compass orientation and landmark guidance must be combined into a system of simultaneous or oscillating dual control.

What are leaders made of? The role of individual experience in determining leader–follower relations in homing pigeons

Negotiating joint routes during group travel is one of the challenges faced by collectively moving animals, on spatial scales ranging from daily foraging trips to long-distance migrations. Homing pigeons, Columba livia, provide a useful model system for studying the mechanisms of group decision making in the context of navigation, owing to the combination of their gregarious nature and the depth of our understanding of their individual orientational strategies. Previous work has shown that during paired flight, if two birds’ individually preferred routes are sufficiently different, one bird will emerge as leader whom the other follows. What determines the identity of a leader has important implications for the efficiency of a moving collective, since leaders with higher navigational certainty can increase the accuracy of the group. We examined factors contributing to the establishment of leadership/followership, focusing on the role of previous navigational experience. We tested, on a homing task, pairs of pigeons in which the two partners had relatively greater and lesser prior experience, generated through individual training. Analysis of the GPS-tracked routes taken by such pairs revealed a negative correlation between homing experience and the probability that a pigeon would follow a co-navigating partner. Thus, the larger the difference in experience between two partners, the higher the likelihood the more experienced bird would emerge as leader. Our results contribute to a better understanding of the mechanisms and potential payoffs of collective navigational decision making in species that travel in mixed-experience groups.