Richard A. Peters

Lizards speed up visual displays in noisy motion habitats

Extensive research over the last few decades has revealed that many acoustically communicating animals compensate for the masking effect of background noise by changing the structure of their signals. Familiar examples include birds using acoustic properties that enhance the transmission of vocalizations in noisy habitats. Here, we show that the effects of background noise on communication signals are not limited to the acoustic modality, and that visual noise from windblown vegetation has an equally important influence on the production of dynamic visual displays. We found that two species of Puerto Rican lizard, Anolis cristatellus and A. gundlachi, increase the speed of body movements used in territorial signalling to apparently improve communication in visually ‘noisy’ environments of rapidly moving vegetation. This is the first evidence that animals change how they produce dynamic visual signals when communicating in noisy motion habitats. Taken together with previous work on acoustic communication, our results show that animals with very different sensory ecologies can face similar environmental constraints and adopt remarkably similar strategies to overcome these constraints.

Signaling against the Wind: Modifying Motion-Signal Structure in Response to Increased Noise

Animal signals are optimized for particular signaling environments [1-3]. While signaling, senders often choose favorable conditions that ensure reliable detection and transmission [4-8], suggesting that they are sensitive to changes in signal efficacy. Recent evidence has also shown that animals will increase the amplitude or intensity of their acoustic signals at times of increased environmental noise [9-11]. The nature of these adjustments provides important insights into sensory processing. However, only a single piece of correlative evidence for signals defined by movement suggests that visual-signal design depends on ambient motion noise [12]. Here we show experimentally for the first time that animals communicating with movement will adjust their displays when environmental motion noise increases. Surprisingly, under sustained wind conditions, the Australian lizard Amphibolurus muricatus changed the structure and increased the duration of its introductory tail flicking, rather than increasing signaling speed. The way these lizards restructure the alerting component of their movement-based aggressive display in the presence of increased motion noise highlights the challenge we face in understanding motion-detection mechanisms under natural operating conditions.

Measuring the structure of dynamic visual signals

Correspondence: R. Peters, Department of Psychology, Macquarie University, Sydney, NSW 2109, Australia (email: richard@ galliform.psy.mq.edu.au). C. W. G. Clifford is at the School of Psychology, University of Sydney, Sydney, NSW 2006, Australia. The evolutionary significance of perceptual processes is well documented (Endler 1991; Guilford & Dawkins 1991; Pagel 1993; Dawkins & Guilford 1996; Endler & Basolo 1998). Signals must be designed to stimulate the sense organs of intended receivers (e.g. social companions, opponents, or potential mates) and this effect must typically be achieved without attracting the attention of ‘eavesdroppers’ such as parasites and predators. Signals must also be memorable (Bernard & Remington 1991; Rowe & Guilford 1996; Speed 2000), so that nuances of structure are learned quickly amongst a welter of competing stimuli impinging upon the receiver. Analysis of structure is an essential prerequisite for any exploration of signal design. The long history of successful work on acoustic communication can be traced to the development of the sound spectrograph in the 1950s (for a review see Hopp et al. 1998). Similarly, rapid advances have been made in recent years since spectral analysis (Endler 1990) has been applied in studies of static visual signals, such as ornaments and colour patterns. In contrast, much less is known about signals that are defined by movement, such as courtship and aggressive displays. Such dynamic visual signals are ubiquitous: they are used in contexts as diverse as opponent assessment (Ord et al. 2001), female mate choice (where they may act synergistically with morphology; Rosenthal et al. 1996), pursuit deterrence (e.g. Hasson 1991; Caro 1995), alarm signalling (Hennessy et al. 1981) and even camouflage (e.g. Fleishman 1985). Motion is also an important component of many multimodal signals (Partan & Marler 1999), often in combination with sound (Evans & Marler 1994). The design of these motor patterns is a classic problem in evolutionary biology (Darwin 1871) and

Claw waving display changes with receiver distance in fiddler crabs, Uca perplexa

Effective communication is critically dependent on the successful transfer of information and, because environmental and social conditions can affect signal transmission, animals should be able to adjust their signals to optimize reliability. We show, apparently for the first time in a movement-based signal, that visual displays are adjusted with respect to the distance of signal receivers. Not only does this show the ability of the fiddler crab to judge distance, but this also shows that signalling is context dependent on surprisingly fine spatial and temporal scales. We elicited courtship behaviour in the crabs with tethered females and simultaneously recorded the displays of males from above and from crab-eye level. As females approached, males increased signal intensity by shortening display duration and altered signal form by reducing the lateral movement component of the waving signal. We suggest that males tune their waving display depending on receiver distance (a) to balance energetic costs with reproductive benefits, (b) to alter the information content of the signal and (c) to avoid signal misinterpretation. Such fine-scale context sensitivity is likely to be far more widespread in animal communication than hitherto recognized from similar signal modifications in auditory communication.

Caste-specific visual adaptations to distinct daily activity schedules in Australian Myrmecia ants

Animals are active at different times of the day and their activity schedules are shaped by competition, time-limited food resources and predators. Different temporal niches provide different light conditions, which affect the quality of visual information available to animals, in particular for navigation. We analysed caste-specific differences in compound eyes and ocelli in four congeneric sympatric species of Myrmecia ants, with emphasis on within-species adaptive flexibility and daily activity rhythms. Each caste has its own lifestyle: workers are exclusively pedestrian; alate females lead a brief life on the wing before becoming pedestrian; alate males lead a life exclusively on the wing. While workers of the four species range from diurnal, diurnal-crepuscular, crepuscular-nocturnal to nocturnal, the activity times of conspecific alates do not match in all cases. Even within a single species, we found eye area, facet numbers, facet sizes, rhabdom diameters and ocelli size to be tuned to the distinct temporal niche each caste occupies. We discuss these visual adaptations in relation to ambient light levels, visual tasks and mode of locomotion.

Image motion environments: background noise for movement-based animal signals.

Understanding the evolution of animal signals has to include consideration of the structure of signal and noise, and the sensory mechanisms that detect the signals. Considerable progress has been made in understanding sounds and colour signals, however, the degree to which movement-based signals are constrained by the particular patterns of environmental image motion is poorly understood. Here we have quantified the image motion generated by wind-blown plants at 12 sites in the coastal habitat of the Australian lizard Amphibolurus muricatus. Sampling across different plant communities and meteorological conditions revealed distinct image motion environments. At all locations, image motion became more directional and apparent speed increased as wind speeds increased. The magnitude of these changes and the spatial distribution of image motion, however, varied between locations probably as a function of plant structure and the topographic location. In addition, we show that the background motion noise depends strongly on the particular depth-structure of the environment and argue that such microhabitat differences suggest specific strategies to preserve signal efficacy. Movement-based signals and motion processing mechanisms, therefore, may reveal the same type of habitat specific structural variation that we see for signals from other modalities.

Environmental motion delays the detection of movement-based signals

Animal signals are constrained by the environment in which they are transmitted and the sensory systems of receivers. Detection of movement-based signals is particularly challenging against the background of wind-blown plants. The Australian lizard Amphibolurus muricatus has recently been shown to compensate for greater plant motion by prolonging the introductory tail-flicking component of its movement-based display. Here I demonstrate that such modifications to signal structure are useful because environmental motion lengthens the time lizard receivers take to detect tail flicks. The spatio-temporal properties of animal signals and environmental motion are thus sufficiently similar to make signal detection more difficult. Environmental motion, therefore, must have had an influence on the evolution of movement-based signals and motion detection mechanisms.

Detection of a looming stimulus by the Jacky dragon: selective sensitivity to characteristics of an aerial predator

Rapidly looming objects are highly salient to most animal visual systems. The sensory processing of such stimuli is now well understood in birds and insects. We conducted the first analogous study in lizards, concentrating on the ecologically realistic challenge posed by an approaching aerial predator. In an initial experiment, video footage of a trained raptor flying towards the camera produced flight responses in Jacky dragons, Amphibolurus muricatus, but control sequences showing a retreating or stationary stimulus were ineffectual. Two additional experiments then explored the processing of motion and of morphological attributes separately. We presented a series of expanding disks, systematically manipulating area/time characteristics to test looming sensitivity in the absence of other cues. Lizards oriented significantly more frequently to a sequence matching the area change of the approaching predator than to any other. Comparisons show that this response was specific to an exponential increase following a period of slow change, a pattern remarkably similar to those described in other taxa. In the final experiment, we presented a range of stimulus shapes, all with identical area and movement. Lizards were most responsive to a realistic raptor silhouette. Controls allowed us to exclude the possibility that this result was attributable to looming rate, size or the axis of asymmetric expansion. We conclude that response to an approaching aerial predator depends upon a hierarchical series of cues, including area/time profile, edge length, shape and orientation. The integration of this information will be an important problem for future work.

Motion sensitivity of the Jacky dragon, Amphibolurus muricatus: random-dot kinematograms reveal the importance of motion noise for signal detection

The evolution of movement-based signals is constrained by the successful segmentation of relevant movements from motion noise by the visual system of receivers. We tested five Jacky dragons, Amphibolurus muricatus, a species characterized by stereotyped movement-based social signals, for their ability to discriminate the direction of drifting dots against simulated background motion noise of varying angular speeds. Results from trials with artificial (dot) backgrounds suggested that Jacky dragons are most sensitive to high-speed movement, while background movement of similar angular speeds to target stimuli reduced performance. We also found differences in accuracy between natural backgrounds comprising footage of plant motion at two independent sites. We argue that detecting salient movement depends on the particular characteristics of the surrounding motion noise, and discuss its implications for movement-based signal design.

Movement signal choreography unaffected by receiver distance in the Australian Jacky lizard, Amphibolurus muricatus

Theory explains the structure of animal signals in the context of the receiver sensory systems, the environment through which signals travel and their information content. The influence of signalling context on movement-based signalling strategies is becoming clearer. Building upon recent findings that demonstrated changing environmental plant motion conditions resulted in a change of signalling strategy by the Australian lizard Amphibolurus muricatus, we examined whether receiver distance also influences signalling strategies. We found that signalling lizards did not modify their introductory tail flicking in response to distant viewers in the absence of competing, irrelevant plant image motion despite significant reductions in signal structure at the eye of the viewer. The magnitude of resultant effect sizes strongly suggests that receiver distance does not contribute to signalling strategies as much as the presence of motion noise in the environment.