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1.  Singing in the moonlight: dawn song performance of a diurnal bird varies with lunar phase 
Biology Letters  2014;10(1):20130970.
It is well established that the lunar cycle can affect the behaviour of nocturnal animals, but its potential to have a similar influence on diurnal species has received less research attention. Here, we demonstrate that the dawn song of a cooperative songbird, the white-browed sparrow weaver (Plocepasser mahali), varies with moon phase. When the moon was above the horizon at dawn, males began singing on average 10 min earlier, if there was a full moon compared with a new moon, resulting in a 67% mean increase in performance period and greater total song output. The lack of a difference between full and new moon dawns when the moon was below the horizon suggests that the observed effects were driven by light intensity, rather than driven by other factors associated with moon phase. Effects of the lunar cycle on twilight signalling behaviour have implications for both pure and applied animal communication research.
PMCID: PMC3917340  PMID: 24429683
lunar cycle; moon phase; twilight; light pollution; song; dawn chorus
2.  Increased Noise Levels Have Different Impacts on the Anti-Predator Behaviour of Two Sympatric Fish Species 
PLoS ONE  2014;9(7):e102946.
Animals must avoid predation to survive and reproduce, and there is increasing evidence that man-made (anthropogenic) factors can influence predator−prey relationships. Anthropogenic noise has been shown to have a variety of effects on many species, but work investigating the impact on anti-predator behaviour is rare. In this laboratory study, we examined how additional noise (playback of field recordings of a ship passing through a harbour), compared with control conditions (playback of recordings from the same harbours without ship noise), affected responses to a visual predatory stimulus. We compared the anti-predator behaviour of two sympatric fish species, the three-spined stickleback (Gasterosteus aculeatus) and the European minnow (Phoxinus phoxinus), which share similar feeding and predator ecologies, but differ in their body armour. Effects of additional-noise playbacks differed between species: sticklebacks responded significantly more quickly to the visual predatory stimulus during additional-noise playbacks than during control conditions, while minnows exhibited no significant change in their response latency. Our results suggest that elevated noise levels have the potential to affect anti-predator behaviour of different species in different ways. Future field-based experiments are needed to confirm whether this effect and the interspecific difference exist in relation to real-world noise sources, and to determine survival and population consequences.
PMCID: PMC4109949  PMID: 25058618
3.  Behavioural and Physiological Effects of Finely Balanced Decision-Making in Chickens 
PLoS ONE  2014;9(10):e108809.
In humans, more difficult decisions result in behavioural and physiological changes suggestive of increased arousal, but little is known about the effect of decision difficulty in other species. A difficult decision can have a number of characteristics; we aimed to monitor how finely balanced decisions, compared to unbalanced ones, affected the behaviour and physiology of chickens. An unbalanced decision was one in which the two options were of unequal net value (1 (Q1) vs. 6 (Q6) pieces of sweetcorn with no cost associated with either option); a finely balanced decision was one in which the options were of equal net value (i.e. hens were "indifferent" to both options). To identify hens' indifference, a titration procedure was used in which a cost (electromagnetic weight on an access door) was applied to the Q6 option, to find the individual point at which hens chose this option approximately equally to Q1 via a non-weighted door. We then compared behavioural and physiological indicators of arousal (head movements, latency to choose, heart-rate variability and surface body temperature) when chickens made decisions that were unbalanced or finely balanced. Significant physiological (heart-rate variability) and behavioural (latency to pen) differences were found between the finely balanced and balanced conditions, but these were likely to be artefacts of the greater time and effort required to push through the weighted doors. No other behavioural and physiological measures were significantly different between the decision categories. We suggest that more information is needed on when best to monitor likely changes in arousal during decision-making and that future studies should consider decisions defined as difficult in other ways.
PMCID: PMC4183509  PMID: 25275440
4.  Chronic playback of boat noise does not impact hatching success or post-hatching larval growth and survival in a cichlid fish 
PeerJ  2014;2:e594.
Anthropogenic (man-made) noise has been shown to have a negative impact on the behaviour and physiology of a range of terrestrial and aquatic animals. However, direct assessments of fitness consequences are rare. Here we examine the effect of additional noise on early life stages in the model cichlid fish, Neolamprologus pulcher. Many fishes use and produce sounds, they are crucial elements of aquatic ecosystems, and there is mounting evidence that they are vulnerable to anthropogenic noise; adult N. pulcher have recently been shown to change key behaviours during playback of motor boat noise. Using a split-brood design to eliminate potential genetic effects, we exposed half of the eggs and fry from each clutch to four weeks of playbacks of noise originally recorded from small motor boats with the other half acting as a control (receiving no noise playback). There was no significant effect of additional noise on hatching success or fry survival, length or weight at the end of the exposure period. Although care should be taken not to generalize these findings on a single species from a laboratory study, our data suggest that moderate noise increases do not necessarily have direct negative impacts on early-life survival and growth. Further studies on a range of species in natural conditions are urgently needed to inform conservation efforts and policy decisions about the consequences of anthropogenic noise.
PMCID: PMC4178459  PMID: 25276507
Cichlidae; Anthropogenic noise; Growth; Development; Offspring survival; Long-term noise exposure; Sound; Teleost; Fitness; Vertebrates; Lake Tanganyika
5.  Anthropogenic noise playback impairs embryonic development and increases mortality in a marine invertebrate 
Scientific Reports  2014;4:5891.
Human activities can create noise pollution and there is increasing international concern about how this may impact wildlife. There is evidence that anthropogenic noise may have detrimental effects on behaviour and physiology in many species but there are few examples of experiments showing how fitness may be directly affected. Here we use a split-brood, counterbalanced, field experiment to investigate the effect of repeated boat-noise playback during early life on the development and survival of a marine invertebrate, the sea hare Stylocheilus striatus at Moorea Island (French Polynesia). We found that exposure to boat-noise playback, compared to ambient-noise playback, reduced successful development of embryos by 21% and additionally increased mortality of recently hatched larvae by 22%. Our work, on an understudied but ecologically and socio-economically important taxon, demonstrates that anthropogenic noise can affect individual fitness. Fitness costs early in life have a fundamental influence on population dynamics and resilience, with potential implications for community structure and function.
PMCID: PMC4118180  PMID: 25080997
6.  Size-dependent physiological responses of shore crabs to single and repeated playback of ship noise 
Biology Letters  2013;9(2):20121194.
Anthropogenic noise has fundamentally changed the acoustics of terrestrial and aquatic environments, and there is growing empirical evidence that even a single noise exposure can affect behaviour in a variety of vertebrate organisms. Here, we use controlled experiments to investigate how the physiology of a marine invertebrate, the shore crab (Carcinus maenas), is affected by both single and repeated exposure to ship-noise playback. Crabs experiencing ship-noise playback consumed more oxygen, indicating a higher metabolic rate and potentially greater stress, than those exposed to ambient-noise playback. The response to single ship-noise playback was size-dependent, with heavier crabs showing a stronger response than lighter individuals. Repeated exposure to ambient-noise playback led to increased oxygen consumption (probably due to handling stress), whereas repeated exposure to ship-noise playback produced no change in physiological response; explanations include the possibility that crabs exhibited a maximal response on first exposure to ship-noise playback, or that they habituated or become tolerant to it. These results highlight that invertebrates, like vertebrates, may also be susceptible to the detrimental impacts of anthropogenic noise and demonstrate the tractability for more detailed investigations into the effects of this pervasive global pollutant.
PMCID: PMC3639773  PMID: 23445945
anthropogenic noise; habituation; tolerance; pollution; global change; interindividual variation
7.  The importance of invertebrates when considering the impacts of anthropogenic noise 
Anthropogenic noise is now recognized as a major global pollutant. Rapidly burgeoning research has identified impacts on individual behaviour and physiology through to community disruption. To date, however, there has been an almost exclusive focus on vertebrates. Not only does their central role in food webs and in fulfilling ecosystem services make imperative our understanding of how invertebrates are impacted by all aspects of environmental change, but also many of their inherent characteristics provide opportunities to overcome common issues with the current anthropogenic noise literature. Here, we begin by explaining why invertebrates are likely to be affected by anthropogenic noise, briefly reviewing their capacity for hearing and providing evidence that they are capable of evolutionary adaptation and behavioural plasticity in response to natural noise sources. We then discuss the importance of quantifying accurately and fully both auditory ability and noise content, emphasizing considerations of direct relevance to how invertebrates detect sounds. We showcase how studying invertebrates can help with the behavioural bias in the literature, the difficulties in drawing strong, ecologically valid conclusions and the need for studies on fitness impacts. Finally, we suggest avenues of future research using invertebrates that would advance our understanding of the impact of anthropogenic noise.
PMCID: PMC3871318  PMID: 24335986
environmental change; fitness; hearing; insect; noise quantification; pollution
8.  Negotiating a stable solution for vigilance behaviour 
PMCID: PMC3415925  PMID: 22787028
9.  Post-allogrooming reductions in self-directed behaviour are affected by role and status in the green woodhoopoe 
Biology Letters  2011;8(1):24-27.
Allogrooming occurs in a wide range of species and can serve both hygienic and social functions. While the latter have long been thought to be underpinned by reductions in tension for recipients, recent work has suggested that donors may also benefit in this way. Here, I show that, in cooperatively breeding green woodhoopoes Phoeniculus purpureus, involvement in allogrooming is followed by a reduction in self-grooming by both recipients and donors, but that the former exhibit a greater decrease. Moreover, I demonstrate for the first time that the dominance status of the allogrooming participant is important, with subordinate group members reducing subsequent self-grooming to a greater extent than the dominant pair. If avian self-directed behaviour reflects current distress levels in the same way as found in various primates, my results would indicate that allogrooming benefits are not confined to mammals, and would have important implications both for accurate assessments of the true costs and benefits of affiliative behaviour and for our understanding of the evolution of sociality.
PMCID: PMC3259957  PMID: 21795264
affiliation; cooperation; grooming; group-living; stress
10.  Brevity is not always a virtue in primate communication 
Biology Letters  2010;7(1):23-25.
Semple et al. (Semple et al. in press, Biol. Lett. (doi:10.1098/rsbl.2009.1062)) argued that the ‘law of brevity’ (an inverse relationship between word length and frequency of use) applies not only to human language but also to vocal signalling in non-human primates, because coding efficiency is paramount in both situations. We analysed the frequency of use of signals of different duration in the vocal repertoires of two Neotropical primate species studied in the wild—the common marmoset (Callithrix jacchus) and the golden-backed uakari (Cacajao melanocephalus). The key prediction of the law of brevity was not supported in either species: although the most frequently emitted calls were relatively brief, they were not the shortest signals in the repertoire. The costs and benefits associated with signals of different duration must be appreciated to understand properly their frequency of use. Although relatively brief vocal signals may be favoured by natural selection in order to minimize energetic costs, the very briefest signals may be ambiguous, contain reduced information or be difficult to detect or locate, and may therefore be selected against. Analogies between human language and vocal communication in animals can be misleading as a basis for understanding frequency of use, because coding efficiency is not the only factor of importance in animal communication, and the costs and benefits associated with different signal durations will vary in a species-specific manner.
PMCID: PMC3030868  PMID: 20573617
law of brevity; Neotropical primates; vocal repertoire; signalling
11.  Preparing for battle? Potential intergroup conflict promotes current intragroup affiliation 
Biology Letters  2010;7(1):26-29.
Groups of human soldiers increase their affiliative behaviour when moving into combat zones. Despite numerous other species also competing as groups, little is known about how potential intergroup conflict might influence current intragroup affiliative behaviour in non-human animals. Here, I show that allopreening (when one individual preens another) increases in groups of cooperatively breeding green woodhoopoes (Phoeniculus purpureus) when they enter areas where conflicts with neighbours are more likely. Self-preening, which is an indicator of stress in other species, did not increase in conflict areas, suggesting that the change in affiliative behaviour is not the simple consequence of greater stress. Instead, because it is the dominant breeding pair that increase their preening of subordinate helpers, it is possible that current affiliative behaviour is being exchanged for agonistic support in any intergroup conflicts that might ensue. These results are important for our understanding of group dynamics, cooperation and the evolution of sociality, but also bring to mind the intriguing possibilities of social contracts and future planning in birds.
PMCID: PMC3030875  PMID: 20610419
cooperation; grooming; sociality; primates; group-living; cooperative breeding
12.  Calling by Concluding Sentinels: Coordinating Cooperation or Revealing Risk? 
PLoS ONE  2011;6(10):e25010.
Efficient cooperation requires effective coordination of individual contributions to the cooperative behaviour. Most social birds and mammals involved in cooperation produce a range of vocalisations, which may be important in regulating both individual contributions and the combined group effort. Here we investigate the role of a specific call in regulating cooperative sentinel behaviour in pied babblers (Turdoides bicolor). ‘Fast-rate chuck’ calls are often given by sentinels as they finish guard bouts and may potentially coordinate the rotation of individuals as sentinels, minimising time without a sentinel, or may signal the presence or absence of predators, regulating the onset of the subsequent sentinel bout. We ask (i) when fast-rate chuck calls are given and (ii) what effect they have on the interval between sentinel bouts. Contrary to expectation, we find little evidence that these calls are involved in regulating the pied babbler sentinel system: observations revealed that their utterance is influenced only marginally by wind conditions and not at all by habitat, while observations and experimental playback showed that the giving of these calls has no effect on inter-bout interval. We conclude that pied babblers do not seem to call at the end of a sentinel bout to maximise the efficiency of this cooperative act, but may use vocalisations at this stage to influence more individually driven behaviours.
PMCID: PMC3184948  PMID: 21984898
13.  Acoustic Noise Induces Attention Shifts and Reduces Foraging Performance in Three-Spined Sticklebacks (Gasterosteus aculeatus) 
PLoS ONE  2011;6(2):e17478.
Acoustic noise is known to have a variety of detrimental effects on many animals, including humans, but surprisingly little is known about its impacts on foraging behaviour, despite the obvious potential consequences for survival and reproductive success. We therefore exposed captive three-spined sticklebacks (Gasterosteus aculeatus) to brief and prolonged noise to investigate how foraging performance is affected by the addition of acoustic noise to an otherwise quiet environment. The addition of noise induced only mild fear-related behaviours - there was an increase in startle responses, but no change in the time spent freezing or hiding compared to a silent control - and thus had no significant impact on the total amount of food eaten. However, there was strong evidence that the addition of noise increased food-handling errors and reduced discrimination between food and non-food items, results that are consistent with a shift in attention. Consequently, noise resulted in decreased foraging efficiency, with more attacks needed to consume the same number of prey items. Our results suggest that acoustic noise has the potential to influence a whole host of everyday activities through effects on attention, and that even very brief noise exposure can cause functionally significant impacts, emphasising the threat posed by ever-increasing levels of anthropogenic noise in the environment.
PMCID: PMC3046255  PMID: 21386909
14.  Adaptive Avoidance of Reef Noise 
PLoS ONE  2011;6(2):e16625.
Auditory information is widely used throughout the animal kingdom in both terrestrial and aquatic environments. Some marine species are dependent on reefs for adult survival and reproduction, and are known to use reef noise to guide orientation towards suitable habitat. Many others that forage in food-rich inshore waters would, however, benefit from avoiding the high density of predators resident on reefs, but nothing is known about whether acoustic cues are used in this context. By analysing a sample of nearly 700,000 crustaceans, caught during experimental playbacks in light traps in the Great Barrier Reef lagoon, we demonstrate an auditory capability in a broad suite of previously neglected taxa, and provide the first evidence in any marine organisms that reef noise can act as a deterrent. In contrast to the larvae of species that require reef habitat for future success, which showed an attraction to broadcasted reef noise, taxa with a pelagic or nocturnally emergent lifestyle actively avoided it. Our results suggest that a far greater range of invertebrate taxa than previously thought can respond to acoustic cues, emphasising yet further the potential negative impact of globally increasing levels of underwater anthropogenic noise.
PMCID: PMC3033890  PMID: 21326604
15.  The higher the better: sentinel height influences foraging success in a social bird 
In all social species, information relevant to survival and reproduction can be obtained in two main ways: through personal interaction with the environment (i.e. ‘personal’ information) and from the performance of others (i.e. ‘public’ information). While public information is less costly to obtain than personal information, it may be inappropriate or inaccurate. When deciding how much to rely on public information, individuals should therefore assess its potential quality, but this possibility requires empirical testing in animals. Here, we use the sentinel system of cooperatively breeding pied babblers (Turdoides bicolor) to investigate how behavioural decisions of foragers are influenced by potential variation in the quality of anti-predator information from a vigilant groupmate. When sentinels moved to a higher position, from where their probability of detecting predators is likely to be greater, foragers reduced their vigilance, spread out more widely and were more likely to venture into the open. Consequently, they spent more time foraging and increased their foraging efficiency, resulting in a profound increase in biomass intake rate. The opposite behavioural changes, and consequent foraging outcomes, were found when sentinels moved lower. A playback experiment demonstrated that foragers can use vocal cues alone to assess sentinel height. This is the first study to link explicitly a measure of the potential quality of public information with a fitness measure from those relying on the information, and our results emphasize that a full understanding of the evolution of communication in complex societies requires consideration of the reliability of information.
PMCID: PMC2690466  PMID: 19364740
public information; reliability; anti-predator vigilance; foraging efficiency; vocalizations; cooperative breeding
16.  Duration and outcome of intergroup conflict influences intragroup affiliative behaviour 
Theoreticians have long suggested that the amount of intergroup conflict in which a group is involved could influence the level of cooperation or affiliation displayed by its members. Despite the prevalence of intergroup conflicts in many social animal species, however, few empirical studies have investigated this potential link. Here, I show that intragroup allopreening rates are highest in green woodhoopoe (Phoeniculus purpureus) groups that have the greatest involvement in intergroup conflict. One reason for this relationship is a post-conflict increase in allopreening, and I demonstrate for the first time that both conflict duration and outcome influence subsequent allopreening rates: group members allopreened more following long conflicts and those they lost compared with short conflicts and those they won, perhaps because the former are more stressful. The increase in affiliative behaviour was the result of more allopreening of subordinate helpers by the dominant breeding pair, which may be because the breeders are trying to encourage helpers to participate in future conflicts; relative group size influences conflict outcome and helpers contribute more to conflicts than do the breeding pair. These results emphasize that our understanding of cooperation and group dynamics can be enhanced by investigations of how intergroup interactions affect intragroup processes.
PMCID: PMC2605834  PMID: 18765344
allopreening; cooperation; intergroup conflict; reconciliation; social behaviour; stress
17.  Individuals in foraging groups may use vocal cues when assessing their need for anti-predator vigilance 
Biology Letters  2007;3(3):249-252.
Many studies of social species have reported variation in the anti-predator vigilance behaviour of foraging individuals depending on the presence and relative position of other group members. However, little attention has focused on how foragers assess these variables. It is commonly assumed that they do so visually, but many social species produce frequent calls while foraging, and these ‘close’ calls might provide valuable spatial information. Here, we show that foraging pied babblers (Turdoides bicolor) are less vigilant when in larger groups, in the centre of a group and in closer proximity to another group member. We then show that foragers are less vigilant during playbacks of close calling by more individuals and individuals on either side of them when compared with calls of fewer individuals and calls on one side of them. These results suggest that foragers can use vocal cues to gain information on group size and their spatial position within a group. Future studies of anti-predator vigilance should consider the relative importance of both visual and vocal monitoring of group members.
PMCID: PMC2464705  PMID: 17426006
close calling; anti-predator vigilance; vocal communication; social foraging; social monitoring; vocal cues

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