Laura A. Kelley

Explanations for variation in cognitive ability: Behavioural ecology meets comparative cognition

Sara Shettleworth has played a defining role in the development of animal cognition and its integration into other parts of biology, especially behavioural ecology. Here we chart some of that progress in understanding the causes and importance of variation in cognitive ability and highlight how Tinbergens levels of explanation provide a useful framework for this field. We also review how experimental design is crucial in investigating cognition and stress the need for naturalistic experiments and field studies. We focus particularly on the example of the relationship among food hoarding, spatial cognition and hippocampal structure, and review the conflicting evidence for sex differences in spatial cognition. We finish with speculation that a combination of Tinbergen and Shettleworth-style approaches would be the way to grapple with the as-yet unanswered questions of why birds mimic heterospecifics.

Illusions promote mating success in great bowerbirds.

Trick of the Eye of the Beholder Male bowerbirds build elaborate bowers, or display areas, that consist of an avenue where the female stands and an arena where the male displays. Males decorate their arenas meticulously with stones, flowers, and found objects. Previous work has shown that these bowers induce forced perspective illusions in the observing females. Now Kelley and Endler (p. 335; see the Perspective by Anderson) show that mating success is based on components of the illusion, rather than the physical nature of the bower. Thus, females choose their mates based on a visual illusion painstakingly constructed and maintained by the displaying male. Males that are more successful at tricking female senses mate more often. Sexual selection studies normally compare signal strengths, but signal components and sensory processing may interact to create misleading or attention-capturing illusions. Visual illusions can be produced by altering object and scene geometry in ways that trick the viewer when seen from a particular direction. Male great bowerbirds actively maintain size-distance gradients of objects on their bower courts that create forced-perspective illusions for females viewing their displays from within the bower avenue. We show a significant relationship between mating success and the female’s view of the gradient; this view explains substantially more variance in mating success than the strength of the gradients. Illusions may be widespread in other animals because males of most species display to females with characteristic orientation and distance, providing excellent conditions for illusions.

Visual effects in great bowerbird sexual displays and their implications for signal design

It is often assumed that the primary purpose of a males sexual display is to provide information about quality, or to strongly stimulate prospective mates, but other functions of courtship displays have been relatively neglected. Male great bowerbirds (Ptilonorhynchus nuchalis) construct bowers that exploit the females predictable field of view (FOV) during courtship displays by creating forced perspective illusions, and the quality of illusion is a good predictor of mating success. Here, we present and discuss two additional components of male courtship displays that use the females predetermined viewpoint: (i) the rapid and diverse flashing of coloured objects within her FOV and (ii) chromatic adaptation of the females eyes that alters her perception of the colour of the displayed objects. Neither is directly related to mating success, but both are likely to increase signal efficacy, and may also be associated with attracting and holding the females attention. Signal efficacy is constrained by trade-offs between the signal components; there are both positive and negative interactions within multicomponent signals. Important signal components may have a threshold effect on fitness rather than the often assumed linear relationship.

Male great bowerbirds create forced perspective illusions with consistently different individual quality.

Males often produce elaborate displays that increase their attractiveness to females, and some species extend their displays to include structures or objects that are not part of their body. Such “extended phenotypes” may communicate information that cannot be transmitted by bodily signals or may provide a more reliable signal than bodily signals. However, it is unclear whether these signals are individually distinct and whether they are consistent over long periods of time. Male bowerbirds construct and decorate bowers that function in mate choice. Bower display courts constructed by male great bowerbirds (Ptilonorhynchus nuchalis) induce a visual illusion known as forced perspective for the female viewing the male’s display over the court, and the quality of illusion is associated with mating success. We improved the quality of the forced perspective to determine whether males maintained it at the new higher level, decreased the perspective quality back to its original value, or allowed it to decay at random over time. We found that the original perspective quality was actively recovered to individual original values within 3 d. We measured forced perspective over the course of one breeding season and compared the forced perspective of individual males between two successive breeding seasons. We found that differences in the quality of visual illusion among males were consistent within and between two breeding seasons. This suggests that forced perspective is actively and strongly maintained at a different level by each individual male.

The mimetic repertoire of the spotted bowerbird Ptilonorhynchus maculatus

Although vocal mimicry in songbirds is well documented, little is known about the function of such mimicry. One possibility is that the mimic produces the vocalisations of predatory or aggressive species to deter potential predators or competitors. Alternatively, these sounds may be learned in error as a result of their acoustic properties such as structural simplicity. We determined the mimetic repertoires of a population of male spotted bowerbirds Ptilonorhynchus maculatus, a species that mimics predatory and aggressive species. Although male mimetic repertoires contained an overabundance of vocalisations produced by species that were generally aggressive, there was also a marked prevalence of mimicry of sounds that are associated with alarm such as predator calls, alarm calls and mobbing calls, irrespective of whether the species being mimicked was aggressive or not. We propose that it may be the alarming context in which these sounds are first heard that may lead both to their acquisition and to their later reproduction. We suggest that enhanced learning capability during acute stress may explain vocal mimicry in many species that mimic sounds associated with alarm.

Vocal mimicry in male bowerbirds: who learns from whom?

Vocal mimicry is one of the more striking aspects of avian vocalization and is widespread across songbirds. However, little is known about how mimics acquire heterospecific and environmental sounds. We investigated geographical and individual variation in the mimetic repertoires of males of a proficient mimic, the spotted bowerbird Ptilonorhynchus maculatus. Male bower owners shared more of their mimetic repertoires with neighbouring bower owners than with more distant males. However, interbower distance did not explain variation in the highly repeatable renditions given by bower owners of two commonly mimicked species. From the similarity between model and mimic vocalizations and the patterns of repertoire sharing among males, we suggest that the bowerbirds are learning their mimetic repertoire from heterospecifics and not from each other.

Visual effects in great bowerbird sexual displays and their implications for signal design (vol 281, 20140235, 2014)

We inadvertently left out one acknowledgement in our paper [1] and we add it now in this addendum: We thank Natalie Doerr for an excellent job of setting up and running the bowerbird cameras and other aspects of fieldwork during the 2012 season. In addition, we neglected to reduce the number of significant figures in table 1 from the original R output. If interested, please round off each number to three significant figures.

How do great bowerbirds construct perspective illusions

Many animals build structures to provide shelter, avoid predation, attract mates or house offspring, but the behaviour and potential cognitive processes involved during building are poorly understood. Great bowerbird (Ptilinorhynchus nuchalis) males build and maintain display courts by placing tens to hundreds of objects in a positive size–distance gradient. The visual angles created by the gradient create a forced perspective illusion that females can use to choose a mate. Although the quality of illusion is consistent within males, it varies among males, which may reflect differences in how individuals reconstruct their courts. We moved all objects off display courts to determine how males reconstructed the visual illusion. We found that all individuals rapidly created the positive size–distance gradient required for forced perspective within the first 10 objects placed. Males began court reconstruction by placing objects in the centre of the court and then placing objects further out, a technique commonly used when humans lay mosaics. The number of objects present after 72 h was not related to mating success or the quality of the illusion, indicating that male skill at arranging objects rather than absolute number of objects appears to be important. We conclude that differences arise in the quality of forced perspective illusions despite males using the same technique to reconstruct their courts.

California scrub-jays reduce visual cues available to potential pilferers by matching food colour to caching substrate

Some animals hide food to consume later; however, these caches are susceptible to theft by conspecifics and heterospecifics. Caching animals can use protective strategies to minimize sensory cues available to potential pilferers, such as caching in shaded areas and in quiet substrate. Background matching (where object patterning matches the visual background) is commonly seen in prey animals to reduce conspicuousness, and caching animals may also use this tactic to hide caches, for example, by hiding coloured food in a similar coloured substrate. We tested whether California scrub-jays (Aphelocoma californica) camouflage their food in this way by offering them caching substrates that either matched or did not match the colour of food available for caching. We also determined whether this caching behaviour was sensitive to social context by allowing the birds to cache when a conspecific potential pilferer could be both heard and seen (acoustic and visual cues present), or unseen (acoustic cues only). When caching events could be both heard and seen by a potential pilferer, birds cached randomly in matching and non-matching substrates. However, they preferentially hid food in the substrate that matched the food colour when only acoustic cues were present. This is a novel cache protection strategy that also appears to be sensitive to social context. We conclude that studies of cache protection strategies should consider the perceptual capabilities of the cacher and potential pilferers.