Is Preening Behaviour Sexually Selected? An Experimental Approach

Elaborate or colourful feathers are important traits in female mate choice in birds but little attention has been given to potential costs of maintaining these traits in good condition with preening behaviour. Recent studies indicate that the time and energy required to maintain ornamental plumage in good condition reinforces the honesty of plumage trait. It has been proposed that some behaviours, whose primary function is not to transfer information, can also evolve as signalling components. Here we investigate whether the preening behaviour intensity has a signalling component: we hypothesized that if only high quality males can invest a lot of time in preening, this behaviour may be used by females as a quality signal (attractive preening hypothesis). We tested this hypothesis by using female budgerigars in mate‐choice tests in captivity. We tried to experimentally manipulate the preening behaviour of two groups of budgerigar males (treatment and control group). The proportion of time in which treated males preened in front of females was statistically higher than for control males, however, females spent similar amounts of time with treated males and control males. Moreover, males did not show significant quantitative changes in preening (for both groups) when females were present, suggesting that male budgerigars did not use this behaviour to convey information. These results are inconsistent with the ‘attractive preening’ hypothesis which predicts that preening behaviour itself provides information on condition and is used in female choice.     

Does access to open water affect the behaviour of Pekin ducks (Anas platyrhynchos)?

Ducks show a wide range of water-related behaviours but commercial production often involves access to water that allows drinking only. In this study we evaluated effects of four water resource (WR) treatments on water related behaviours of Pekin ducks. Ducks (n = 2800) were kept in one of four water provision treatments (7 replicate groups of 100 ducks per treatment) from 20 days of age: a bath that allowed full access to water; a trough in which the head could be dipped but without body access; turkey bell drinkers; chicken bell drinkers. The turkey and chicken bells provided easy access for drinking but less opportunity for interaction with the water. The behaviour of the ducks was video recorded, then analysed using scan sampling at 7.5 min intervals between 10:00 and 22:00 at 21, 32, 42 and 45 days. As might be expected, as birds grew, fewer were observed in the bath and over all treatments the amount of preening behaviour increased as ducks aged. Although ducks with access to a bath spent less time in or near the bath, this does not indicate lack of importance to the birds. Fewer ducks were observed standing or resting idle at the bath, and they performed proportionately more water-related preening behaviours than ducks in the other treatments. Moreover, as access to water increased (i.e. from beak only, through to entire body access) higher proportion of preening ducks performed head-dipping behaviour, and a lower proportion performed feather manipulation. This work shows that provision of a water resource that permits full body access appears to promote efficiency of drinking-related behaviours and preening behaviour. This helps to explain improvements in feather hygiene reported in other studies where the birds had full access to, or greater access to water.     

The vocal expression of feeding motivation and frustration in the domestic laying hen, Gallus gallus domesticus

Thwarting of feeding behaviour in the laying hen results in an increase in stereotyped pacing, displacement preening, and the gakel-call. These behaviours therefore reflect the frustration arousal caused by the thwarting of feeding behaviour. This raises the question whether the level of frustration also varies with the intensity of the motivation to perform the thwarted behaviour. This study investigated the relationship between the intensity of the motivation and level of frustration on the one hand and the gakel-call on the other hand. In Experiment 1, the strength of the motivation to feed was varied by thwarting hens in their feeding behaviour in an operant procedure after different durations of food deprivation (0, 8, 23 and 47 h). Trend analysis showed that with increasing hunger state, an increasing number of gakel-calls was given. No effect of treatments on temporal characteristics of the gakel-call was found. In Experiment 2, the level of frustration was varied by reducing or increasing the duration of access to food for food-deprived hens compared to the duration of access during training. It was assumed that a shorter duration of access to food compared to training would elicit frustration, which in turn would affect the performance of behaviours indicative of thwarting. However, we found neither a relation between the number of gakel-calls nor the temporal features of the gakel-call and the duration of access to food. Possibly, the differences between treatments were not large enough to induce differences in frustration level. Also, other factors that might have influenced the motivation are discussed.     

Plumage maintenance affects ultraviolet colour and female preference in the budgerigar

Elaborate or colourful feathers are important traits in female-mate choice in birds but little attention has been given to the potential costs of maintaining these traits in good condition via preening behaviour. While preening is known to be an important component of plumage maintenance, it has received little attention with respect to colouration. We investigated whether preening can influence plumage reflectance and whether females show a preference for plumage cleanliness in captive-bred, wild-type budgerigars, Melopsittacus undulatus. To do this, we compared the spectral colour of birds that were allowed to preen their plumage and individuals that were prevented from preening. The plumage of birds that were prevented from preening showed a significant lower reflectance in the UV range (300-400 nm). Subsequently, we measured females’ preferences for preened and unpreened males using a two-choice test. In a second experiment we allowed females to choose between an unpreened male and a male smeared with UV-absorbing chemicals (UV-blocked male). The proportion of time that females stayed near preened males was statistically higher than for unpreened males, but females spent similar amounts of time with unpreened males and UV-blocked males. These results are consistent with the idea that female budgerigars are able to discriminate between preened and unpreened males, and that UV colours, mediated by preening, can convey information about a bird's current condition.     

Effects of experience and object complexity on exploration in garden warblers (Sylvia borin)

Animals are increasingly exposed to novel environmental conditions because of human activities. An organism's ability to cope with these challenges is critical to its survival. The decision of whether or not an animal should investigate environmental changes involves a trade-off between the risk and the potential benefit of a novel resource. Novelty often elicits approach (exploratory) as well as avoidance behaviour in animals, and the extent of each of these behaviours may influence learning about the environment. We formulated and tested several hypotheses to determine how external factors (complexity of a novel stimulus) and internal factors (experience with objects) might influence exploration latencies to touch a novel object based on either cost or benefit considerations. Garden warblers were confronted with a simple and a complex novel object in their familiar cages, and latencies until first touch were measured. Additionally, corticosterone levels before and after the experiment were measured to assess whether differences in baseline levels might explain variations in latency to approach and whether presentation of novel objects is stressful. The complex object was touched significantly later than the simple object. Experienced birds investigated both types of objects later than inexperienced birds. Although birds showed marked approach–avoidance behaviour with the complex object, none of the objects elicited a corticosterone stress response. The results indicate that garden warblers consider both costs and benefits when exploring novel objects, and that the relative influence of costs and benefits varies with external and internal factors.     

How effective is preening against mobile ectoparasites? An experimental test with pigeons and hippoboscid flies

Birds combat ectoparasites with many defences but the first line of defence is grooming behaviour, which includes preening with the bill and scratching with the feet. Preening has been shown to be very effective against ectoparasites. However, most tests have been with feather lice, which are relatively slow moving. Less is known about the effectiveness of preening as a defence against more mobile and evasive ectoparasites such as hippoboscid flies. Hippoboscids, which feed on blood, have direct effects on the host such asanaemia, as well as indirect effects as vectors of pathogens. Hence, effective defence against hippoboscid flies is important. We used captive Rock Pigeons (Columba livia) to test whether preening behaviour helps to control pigeon flies (Pseudolynchia canariensis). We found that pigeons responded to fly infestation by preening twice as much as pigeons without flies. Preening birds killed twice as many flies over the course of our week-long experiment as birds with impaired preening; however, preening did not kill all of the flies. We also tested the role of the bill overhang, which is critical for effective preening against feather lice, by experimentally removing the overhang and re-measuring the effectiveness of preening against flies. Birds without overhangs were as effective at controlling flies as were birds with overhangs. Overall, we found that preening is effective against mobile hippoboscid flies, yet it does not eliminate them. We discuss the potential impact of preening on the transmission dynamics of blood parasites vectored by hippoboscid flies.     

Coccidial infection does not influence preening behavior in American goldfinches

Preening behavior in birds is important for the maintenance of thermoregulatory and ornamental functions of plumage. It has been repeatedly demonstrated that birds trade off time between plumage maintenance and other activities. However, the condition-dependent constraints of preening remain virtually unstudied. Here, we present the first experimental test of the hypothesis that intestinal parasite infection impairs preening activity. We studied male American goldfinches (Spinus tristis), a species with carotenoid-based plumage coloration. Following pre-alternate (spring) molt, we manipulated the health of males by infecting some birds with Isospora spp. coccidia and keeping others free of the infection. Although the goldfinches increased preening throughout the captive period, we found no significant effect of coccidial treatment on preening behavior. The effect of coccidia on plumage maintenance may be more pronounced under natural conditions where birds have limited access to food and engage in more activities that might limit time available for preening.     

Toxins induce ‘malaise’ behaviour in the honeybee (Apis mellifera)

To avoid poisoning and death when toxins are ingested, the body responds with a suite of physiological detoxification mechanisms accompanied by behaviours that in mammals often include vomiting, nausea, and lethargy. Few studies have characterised whether insects exhibit characteristic ‘malaise-like’ behaviours in response to intoxication. Here, we used the honeybee to investigate how intoxication produced by injection or ingestion with three toxins with different pharmacological modes of action quinine, amygdalin, and lithium chloride affected behaviour. We found that toxin-induced changes in behaviour were best characterised by more time spent grooming. Bees also had difficulty performing the righting reflex and exhibited specific toxin-induced behaviours such as abdomen dragging and curling up. The expression of these behaviours also depended on whether a toxin had been injected or ingested. When toxins were ingested, they were least 10 times less concentrated in the haemolymph than in the ingested food, suggesting that their absorption through the gut is strongly regulated. Our data show that bees exhibit changes in behaviour that are characteristic of ‘malaise’ and suggest that physiological signalling of toxicosis is accomplished by multiple post-ingestive pathways in animals.     

Functions of an unreported “rocking-embrace” gesture between female Japanese Macaques (Macaca fuscata) in Kinkazan Island,Japan

Recently, research has focused on the effects of the concurrence of multimodal signals and their efficacy and meaning. We observed an unreported behaviour, a ventro-ventral “rocking-embrace” gesture that is always accompanied by lip smacking as the facial expression and sometimes by a girney call, in wild Japanese macaques (Macaca fuscata) living in Kinkazan Island, northern Japan. This study examined the form and contexts of the occurrence of such multimodal signals in order to elucidate its functions. Eighty-eight cases of rocking embrace were recorded during 183 h of observation over 22 days. Adult females were involved in all of the cases. Of the 71 cases between adult females in which behaviours prior to the rocking embrace could be identified, 13 cases were allogrooming interruptions, 11 were aggression, and 42 were approaches, most of which occurred between non-kin grooming partners. The rocking embrace was often followed by allogrooming. This suggests that rocking embraces occur under stressful conditions and may function to reduce tensions. This conclusion is consistent with the contexts and functions of lip smacking and girneys shown in previous studies. In contrast with lip smacking and girneys, neither a rocking embrace nor a ventro-ventral embrace (without rocking) between anoestrous adult females has been previously shown in Japanese macaques. In other macaque species, however, the latter gesture is often observed as an affiliative behaviour that immediately follows conflict; it functions to reconcile or as a greeting when it occurs immediately after an approach. Rocking embraces among the Kinkazan macaques occur in contexts similar to, and have a similar function to, the ancestral gesture of ventro-ventral embracing (which is hidden in Japanese macaques) and the ancestral display of lip smacking (which is still observed in Japanese macaques). The ventro-ventral embrace as a tactile signal might have been hidden since it was made redundant by the visual signal of lip smacking in ancestral macaques.     

四川宝兴笼养绿尾虹雉的繁殖期行为观察

2003年和2006年的繁殖季节,对笼养条件下绿尾虹雉的行为进行了详细的观察.在48 480次行为记录中,非繁殖行为主要以走动(32.34%)、站立(12.78%)、静卧(16.32%)和静栖(16.52%)行为为主,理羽(2.65%)、进食(8.01%)和观望(9.56%)行为较少发生.绿尾虹雉的求偶炫耀行为独特,交配行为历时一般不超过5 s,雌鸟产卵过程甚短,只有几秒钟的时间.繁殖期笼养绿尾虹雉与野生个体之间在行为方面存在较大差异.     

Correlational selection does not explain the evolution of a behavioural syndrome

Correlated suites of behaviours, or behavioural syndromes, appear to be widespread, and yet few studies have explored how they arise and are maintained. One possibility holds that correlational selection can generate and maintain behavioural syndrome if certain behavioural combinations enjoy greater fitness than other combinations. Here we test this correlational selection hypothesis by comparing behavioural syndrome structure with a multivariate fitness surface based on reproductive success of male water striders. We measured the structure of a behavioural syndrome including dispersal ability, exploration behaviour, latency to remount and sex recognition sensitivity in males. We then measured the relationship between these behaviours and mating success in a range of sex ratio environments. Despite the presence of some significant correlational selection, behavioural syndrome structure was not associated with correlational selection on behaviours. Although we cannot conclusively reject the correlational selection hypothesis, our evidence suggests that correlational selection and resulting linkage disequilibrium might not be responsible for maintaining the strong correlations between behaviours. Instead, we suggest alternative ways in which this behavioural syndrome may have arisen and outline the need for physiological and quantitative genetic tests of these suggestions.     

A unified mechanism for innate and learned visual landmark guidance in the insect central complex

Insects can navigate efficiently in both novel and familiar environments, and this requires flexiblity in how they are guided by sensory cues. A prominent landmark, for example, can elicit strong innate behaviours (attraction or menotaxis) but can also be used, after learning, as a specific directional cue as part of a navigation memory. However, the mechanisms that allow both pathways to co-exist, interact or override each other are largely unknown. Here we propose a model for the behavioural integration of innate and learned guidance based on the neuroanatomy of the central complex (CX), adapted to control landmark guided behaviours. We consider a reward signal provided either by an innate attraction to landmarks or a long-term visual memory in the mushroom bodies (MB) that modulates the formation of a local vector memory in the CX. Using an operant strategy for a simulated agent exploring a simple world containing a single visual cue, we show how the generated short-term memory can support both innate and learned steering behaviour. In addition, we show how this architecture is consistent with the observed effects of unilateral MB lesions in ants that cause a reversion to innate behaviour. We suggest the formation of a directional memory in the CX can be interpreted as transforming rewarding (positive or negative) sensory signals into a mapping of the environment that describes the geometrical attractiveness (or repulsion). We discuss how this scheme might represent an ideal way to combine multisensory information gathered during the exploration of an environment and support optimal cue integration.     

Neural mechanisms underlying the evolvability of behaviour

The complexity of nervous systems alters the evolvability of behaviour. Complex nervous systems are phylogenetically constrained; nevertheless particular species-specific behaviours have repeatedly evolved, suggesting a predisposition towards those behaviours. Independently evolved behaviours in animals that share a common neural architecture are generally produced by homologous neural structures, homologous neural pathways and even in the case of some invertebrates, homologous identified neurons. Such parallel evolution has been documented in the chromatic sensitivity of visual systems, motor behaviours and complex social behaviours such as pair-bonding. The appearance of homoplasious behaviours produced by homologous neural substrates suggests that there might be features of these nervous systems that favoured the repeated evolution of particular behaviours. Neuromodulation may be one such feature because it allows anatomically defined neural circuitry to be re-purposed. The developmental, genetic and physiological mechanisms that contribute to nervous system complexity may also bias the evolution of behaviour, thereby affecting the evolvability of species-specific behaviour.     

Behavioural adjustment in response to increased predation risk: a study in three duck species

Predation directly triggers behavioural decisions designed to increase immediate survival. However, these behavioural modifications can have long term costs. There is therefore a trade-off between antipredator behaviours and other activities. This trade-off is generally considered between vigilance and only one other behaviour, thus neglecting potential compensations. In this study, we considered the effect of an increase in predation risk on the diurnal time-budget of three captive duck species during the wintering period. We artificially increased predation risk by disturbing two groups of 14 mallard and teals at different frequencies, and one group of 14 tufted ducks with a radio-controlled stressor. We recorded foraging, vigilance, preening and sleeping durations the week before, during and after disturbance sessions. Disturbed groups were compared to an undisturbed control group. We showed that in all three species, the increase in predation risk resulted in a decrease in foraging and preening and led to an increase in sleeping. It is worth noting that contrary to common observations, vigilance did not increase. However, ducks are known to be vigilant while sleeping. This complex behavioural adjustment therefore seems to be optimal as it may allow ducks to reduce their predation risk. Our results highlight the fact that it is necessary to encompass the whole individual time-budget when studying behavioural modifications under predation risk. Finally, we propose that studies of behavioural time-budget changes under predation risk should be included in the more general framework of the starvation-predation risk trade-off.     

Beyond the phenotypic gambit: molecular behavioural ecology and the evolution of genetic architecture

Most studies of behaviour examine traits whose proximate causes include sensory input and neural decision-making, but conflict and collaboration in biological systems began long before brains or sensory systems evolved. Many behaviours result from non-neural mechanisms such as direct physical contact between recognition proteins or modifications of development that coincide with altered behaviour. These simple molecular mechanisms form the basis of important biological functions and can enact organismal interactions that are as subtle, strategic and interesting as any. The genetic changes that underlie divergent molecular behaviours are often targets of selection, indicating that their functional variation has important fitness consequences. These behaviours evolve by discrete units of quantifiable phenotypic effect (amino acid and regulatory mutations, often by successive mutations of the same gene), so the role of selection in shaping evolutionary change can be evaluated on the scale at which heritable phenotypic variation originates. We describe experimental strategies for finding genes that underlie biochemical and developmental alterations of behaviour, survey the existing literature highlighting cases where the simplicity of molecular behaviours has allowed insight to the evolutionary process and discuss the utility of a genetic knowledge of the sources and spectrum of phenotypic variation for a deeper understanding of how genetic and phenotypic architectures evolve.     

Effect of restricted preen-gland access on maternal self maintenance and reproductive investment in mallards

Background

As egg production and offspring care are costly, females should invest resources adaptively into their eggs to optimize current offspring quality and their own lifetime reproductive success. Parasite infections can influence maternal investment decisions due to their multiple negative physiological effects. The act of preening – applying oils with anti-microbial properties to feathers – is thought to be a means by which birds combat pathogens and parasites, but little is known of how preening during the reproductive period (and its expected disease-protecting effects) influences maternal investment decisions at the level of the egg.

Methodology/Principal Findings

Here, we experimentally prevented female mallards (Anas platyrhynchos) from accessing their preen gland during breeding and monitored female immunoresponsiveness (e.g., plasma lysozyme concentration) as well as some egg traits linked to offspring quality (e.g., egg mass, yolk carotenoid content, and albumen lysozyme levels). Females with no access to their preen gland showed an increase in plasma lysozyme level compared to control, normally preening females. In addition, preen-gland-restricted females laid significantly lighter eggs and deposited higher carotenoid concentrations in the yolk compared to control females. Albumen lysozyme activity did not differ significantly between eggs laid by females with or without preen gland access.

Conclusion/Significance

Our results establish a new link between an important avian self-maintenance behaviour and aspects of maternal health and reproduction. We suggest that higher yolk carotenoid levels in eggs laid by preen-gland-restricted females may serve to boost health of offspring that would hatch in a comparatively microbe-rich environment.     

Social molecular pathways and the evolution of bee societies

Bees provide an excellent model with which to study the neuronal and molecular modifications associated with the evolution of sociality because relatively closely related species differ profoundly in social behaviour, from solitary to highly social. The recent development of powerful genomic tools and resources has set the stage for studying the social behaviour of bees in molecular terms. We review 'ground plan' and 'genetic toolkit' models which hypothesize that discrete pathways or sets of genes that regulate fundamental behavioural and physiological processes in solitary species have been co-opted to regulate complex social behaviours in social species. We further develop these models and propose that these conserved pathways and genes may be incorporated into 'social pathways', which consist of relatively independent modules involved in social signal detection, integration and processing within the nervous and endocrine systems, and subsequent behavioural outputs. Modifications within modules or in their connections result in the evolution of novel behavioural patterns. We describe how the evolution of pheromonal regulation of social pathways may lead to the expression of behaviour under new social contexts, and review plasticity in circadian rhythms as an example for a social pathway with a modular structure.     

Psychophysiological correlates of aggression and violence: an integrative review

This paper reviews existing psychophysiological studies of aggression and violent behaviour including research employing autonomic, electrocortical and neuroimaging measures. Robust physiological correlates of persistent aggressive behaviour evident in this literature include low baseline heart rate, enhanced autonomic reactivity to stressful or aversive stimuli, enhanced EEG slow wave activity, reduced P300 brain potential response and indications from structural and functional neuroimaging studies of dysfunction in frontocortical and limbic brain regions that mediate emotional processing and regulation. The findings are interpreted within a conceptual framework that draws on two integrative models in the literature. The first is a recently developed hierarchical model of impulse control (externalizing) problems, in which various disinhibitory syndromes including aggressive and addictive behaviours of different kinds are seen as arising from common as well as distinctive aetiologic factors. This model represents an approach to organizing these various interrelated phenotypes and investigating their common and distinctive aetiologic substrates. The other is a neurobiological model that posits impairments in affective regulatory circuits in the brain as a key mechanism for impulsive aggressive behaviour. This model provides a perspective for integrating findings from studies employing different measures that have implicated varying brain structures and physiological systems in violent and aggressive behaviour.     

Effects of food supplementation on behavioural decisions of hoopoe-larks in the Arabian Desert: balancing water, energy and thermoregulation

Patterns of time allocation to different activities can help reveal how natural selection has solved optimality problems that involve simultaneous environmental constraints. To investigate how time budgets of desert birds are affected by ambient temperature, lack of drinking water and low food availability, we provided food and water to hoopoe-larks,Alaemon alaudipes , in the Arabian Desert during years in which no larks reared young. We followed birds continuously from sunrise to sunset on unsupplemented and supplemented days, and recorded their behaviour every 15 s. Taking into account the variation in temperature between days, hoopoe-larks decreased foraging time by 13-29% of total daytime, and increased resting and preening time by 7-16 and 8%, respectively, when they had access to supplemental food. When birds had access to extra food, they began and ended their midday resting period when shade temperature was on average 2.2°C lower, and operative temperature was on average 3.1°C lower, than on unsupplemented days, a significant effect of food supplementation. We concluded that birds optimized time spent on foraging and thermoregulating based on a combination of physiological state variables, including body temperature, hydration state and level of energy reserves. Our results do not support a previous hypothesis that activity budgets of desert birds are dictated by thermal constraints alone.     

Fox Odour Increases Vigilance in European Rabbits: A Study under Semi-Natural Conditions

The recognition of predator odours is a well‐known mechanism in many prey species which may lead to various behavioural and physiological responses. This has been shown for many mammal species under laboratory conditions, but efforts to validate the results in the field often have led to inconclusive results. We investigated the behavioural reactions and the physiological stress response of European rabbits (Oryctolagus cuniculus) to the odour of a mammalian predator (red fox, Vulpes vulpes) under semi‐natural conditions. The study was conducted on a rabbit population living in an outdoor enclosure of 2 ha. We compared the rates of vigilance and exploration, the time allocated to self‐directed behaviours, the home range sizes and the physiological responses of an experimental and a control group. Only animals from the experimental group were confronted with fox faeces. These animals increased their vigilance rate whereas the control animals did not respond. The increase did not differ between adult and subadult individuals. Furthermore, the experimental animals frequently approached the odour of the predator which might indicate an increase in investigative behaviour. Home‐range size, feeding and other self‐directed behaviours did not change in response to fox odour. Moreover, the animals of the experimental and the control group did not differ in serum corticosterone concentrations (measured after adrenocorticotrophic hormone challenge) that we determined in the beginning and in the end of the experiment. We suggest that the observed behavioural responses represent a low‐cost strategy for lowering the individual risk of predation.