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1.  Within-group behavioural consequences of between-group conflict: a prospective review 
Conflict is rife in group-living species and exerts a powerful selective force. Group members face a variety of threats from extra-group conspecifics, from individuals looking for reproductive opportunities to rival groups seeking resources. Theory predicts that such between-group conflict should influence within-group behaviour. However, compared with the extensive literature on the consequences of within-group conflict, relatively little research has considered the behavioural impacts of between-group conflict. We give an overview of why between-group conflict is expected to influence subsequent behaviour among group members. We then use what is known about the consequences of within-group conflict to generate testable predictions about how between-group conflict might affect within-group behaviour in the aftermath. We consider the types of behaviour that could change and how the role of different group members in the conflict can exert an influence. Furthermore, we discuss how conflict characteristics and outcome, group size, social structure and within-group relationship quality might modulate post-conflict behavioural changes. Finally, we propose the need for consistent definitions, a broader range of examined behaviours and taxa, individual-focused data collection, complementary observational and experimental approaches, and a consideration of lasting effects if we are to understand fully the significant influence of between-group conflict on social behaviour.
doi:10.1098/rspb.2016.1567
PMCID: PMC5136580  PMID: 27903869
conflict; social evolution; behavioural consequences; group living; aggression
2.  Repeated exposure reduces the response to impulsive noise in European seabass 
Global Change Biology  2016;22(10):3349-3360.
Abstract
Human activities have changed the acoustic environment of many terrestrial and aquatic ecosystems around the globe. Mounting evidence indicates that the resulting anthropogenic noise can impact the behaviour and physiology of at least some species in a range of taxa. However, the majority of experimental studies have considered only immediate responses to single, relatively short‐term noise events. Repeated exposure to noise could lead to a heightened or lessened response. Here, we conduct two long‐term (12 week), laboratory‐based exposure experiments with European seabass (Dicentrarchus labrax) to examine how an initial impact of different sound types potentially changes over time. Naïve fish showed elevated ventilation rates, indicating heightened stress, in response to impulsive additional noise (playbacks of recordings of pile‐driving and seismic surveys), but not to a more continuous additional noise source (playbacks of recordings of ship passes). However, fish exposed to playbacks of pile‐driving or seismic noise for 12 weeks no longer responded with an elevated ventilation rate to the same noise type. Fish exposed long‐term to playback of pile‐driving noise also no longer responded to short‐term playback of seismic noise. The lessened response after repeated exposure, likely driven by increased tolerance or a change in hearing threshold, helps explain why fish that experienced 12 weeks of impulsive noise showed no differences in stress, growth or mortality compared to those reared with exposure to ambient‐noise playback. Considering how responses to anthropogenic noise change with repeated exposure is important both when assessing likely fitness consequences and the need for mitigation measures.
doi:10.1111/gcb.13352
PMCID: PMC5006868  PMID: 27282635
anthropogenic noise; Dicentrarchus labrax; European seabass; growth; habituation; hearing threshold; pollution; stress; tolerance; ventilation rate
3.  Dominance-related seasonal song production is unrelated to circulating testosterone in a subtropical songbird 
Highlights
•Whether testosterone (T) regulates song in subtropical birds is poorly known.•Subtropical white-browed sparrow weavers show seasonal profiles in T and song.•Dominant males sang more than subordinate males, despite comparable T.•Dominant male song production was not correlated with circulating T.•We highlight the need to consider the role of alternative neuroendocrine mechanisms.
Circulating testosterone (T) is widely considered to play a key role in the production of sexual displays by male vertebrates. While numerous studies support a role for circulating T in promoting the production of song in male birds, this understanding is based primarily on evidence from seasonally breeding northern temperate species, leaving it unclear whether this mechanism generalizes to other regions of the world. Here we investigate whether variation in circulating levels of T can explain the marked within- and among-individual variation in male song performance observed in a subtropical population of the year-round territorial white-browed sparrow weaver (Plocepasser mahali mahali). Our findings reveal that both circulating T and male song production peaked at a similar time point, halfway through the population-level breeding season. However, while dominant males were more likely to sing and sang for longer than subordinate males, within-group paired comparisons revealed no dominance-related differences in circulating T. Moreover, comparisons both among and within individual dominant males revealed that song duration, syllable rate and proportion of time spent singing were all unrelated to circulating T. Together, our findings suggest that natural variation in male song production, at least in this population of white-browed sparrow weavers, is achieved principally through mechanisms other than variation in circulating T concentration. More widely, our results are in line with the view that male song production is not exclusively regulated by gonadally synthesized steroids.
doi:10.1016/j.ygcen.2016.05.011
PMCID: PMC4920672  PMID: 27179883
Tropical endocrinology; Sexual signalling; Circulating testosterone; Seasonality; Dominance
4.  Routine handling methods affect behaviour of three-spined sticklebacks in a novel test of anxiety 
Behavioural Brain Research  2016;306:26-35.
Highlights
•We develop a new combined diving and scototaxis test of anxiety in fish.•We compare box (in water) and net (out of water) transfer between tanks.•Net transfer results in less anxiety like-behaviour. Explanations are considered.•Novel-object and open-field tests fail to detect these differences.•The combined diving and scototaxis test is a promising biologically-meaningful test.
Fish are increasingly popular subjects in behavioural and neurobiological research. It is therefore important that they are housed and handled appropriately to ensure good welfare and reliable scientific findings, and that species-appropriate behavioural tests (e.g. of cognitive/affective states) are developed. Routine handling of captive animals may cause physiological stress responses that lead to anxiety-like states (e.g. increased perception of danger). In fish, these may be particularly pronounced when handling during tank-to-tank transfer involves removal from water into air. Here we develop and use a new combined scototaxis (preference for dark over light areas) and novel-tank-diving test, alongside conventional open-field and novel-object tests, to measure the effects of transferring three-spined sticklebacks (Gasterosteus aculeatus) between tanks using a box or net (in and out of water respectively). Preference tests for dark over light areas confirmed the presence of scototaxis in this species. Open-field and novel-object tests failed to detect any significant differences between net and box-handled fish. However, the combined diving and scototaxis detected consistent differences between the treatments. Net-handled fish spent less time on the dark side of the tank, less time in the bottom third, and kept a greater distance from the ‘safe’ bottom dark area than box-handled fish. Possible explanations for this reduction in anxiety-like behaviour in net-handled fish are discussed. The combined diving and scototaxis test may be a sensitive and taxon-appropriate method for measuring anxiety-like states in fish.
doi:10.1016/j.bbr.2016.03.015
PMCID: PMC4850245  PMID: 26965568
Stickleback; Anxiety; Handling; Scototaxis; Novel tank diving test; Relief
5.  Anthropogenic noise increases fish mortality by predation 
Nature Communications  2016;7:10544.
Noise-generating human activities affect hearing, communication and movement in terrestrial and aquatic animals, but direct evidence for impacts on survival is rare. We examined effects of motorboat noise on post-settlement survival and physiology of a prey fish species and its performance when exposed to predators. Both playback of motorboat noise and direct disturbance by motorboats elevated metabolic rate in Ambon damselfish (Pomacentrus amboinensis), which when stressed by motorboat noise responded less often and less rapidly to simulated predatory strikes. Prey were captured more readily by their natural predator (dusky dottyback, Pseudochromis fuscus) during exposure to motorboat noise compared with ambient conditions, and more than twice as many prey were consumed by the predator in field experiments when motorboats were passing. Our study suggests that a common source of noise in the marine environment has the potential to impact fish demography, highlighting the need to include anthropogenic noise in management plans.
Little evidence exists on whether human-generated noise directly affects survival of wildlife. Here, Simpson et al. show that damselfish exposed to motorboat noise have elevated metabolic rates, reduced responses to predatory attacks, and suffer increased predation compared to fish in ambient conditions.
doi:10.1038/ncomms10544
PMCID: PMC4748250  PMID: 26847493
6.  Dominant male song performance reflects current immune state in a cooperatively breeding songbird 
Ecology and Evolution  2016;6(4):1008-1015.
Abstract
Conspicuous displays are thought to have evolved as signals of individual “quality”, though precisely what they encode remains a focus of debate. While high quality signals may be produced by high quality individuals due to “good genes” or favourable early‐life conditions, whether current immune state also impacts signalling performance remains poorly understood, particularly in social species. Here, we experimentally demonstrate that male song performance is impaired by immune system activation in the cooperatively breeding white‐browed sparrow weaver (Plocepasser mahali). We experimentally activated the immune system of free‐living dominant males via subcutaneous injection of phytohemagglutinin (PHA) and contrasted its effects with those of a control (phosphate buffered saline) injection. PHA‐challenged males showed significant reductions in both the duration and the rate of their song performance, relative to controls, and this could not be readily attributed to effects of the challenge on body mass, as no such effects were detected. Furthermore, male song performance prior to immune‐challenge predicted the scale of the inflammatory response to the challenge. Our findings suggest that song performance characteristics are impacted by current immune state. This link between current state and signal performance might therefore contribute to enforcing the honesty of signal performance characteristics. Impacts of current state on signaling may be of particular importance in social species, where subordinates may benefit from an ability to identify and subsequently challenge same‐sex dominants in a weakened state.
doi:10.1002/ece3.1938
PMCID: PMC4719765  PMID: 26811745
Behavioral plasticity; cooperative breeder; dominance; handicap hypothesis; resource‐allocation trade‐offs; sociality; state‐dependent signaling
7.  Rapid recovery following short-term acoustic disturbance in two fish species 
Royal Society Open Science  2016;3(1):150686.
Noise from human activities is known to impact organisms in a variety of taxa, but most experimental studies on the behavioural effects of noise have focused on examining responses associated with the period of actual exposure. Unlike most pollutants, acoustic noise is generally short-lived, usually dissipating quickly after the source is turned off or leaves the area. In a series of experiments, we use established experimental paradigms to examine how fish behaviour and physiology are affected, both during short-term (2 min) exposure to playback of recordings of anthropogenic noise sources and in the immediate aftermath of noise exposure. We considered the anti-predator response and ventilation rate of juvenile European eels (Anguilla anguilla) and ventilation rate of juvenile European seabass (Dicentrarchus labrax). As previously found, additional-noise exposure decreased eel anti-predator responses, increased startle latency and increased ventilation rate relative to ambient-noise-exposed controls. Our results show for the first time that those effects quickly dissipated; eels showed rapid recovery of startle responses and startle latency, and rapid albeit incomplete recovery of ventilation rate in the 2 min after noise cessation. Seabass in both laboratory and open-water conditions showed an increased ventilation rate during playback of additional noise compared with ambient conditions. However, within 2 min of noise cessation, ventilation rate showed complete recovery to levels equivalent to ambient-exposed control individuals. Care should be taken in generalizing these rapid-recovery results, as individuals might have accrued other costs during noise exposure and other species might show different recovery times. Nonetheless, our results from two different fish species provide tentative cause for optimism with respect to recovery following short-duration noise exposure, and suggest that considering periods following noise exposures could be important for mitigation and management decisions.
doi:10.1098/rsos.150686
PMCID: PMC4736948  PMID: 26909193
anthropogenic noise; behaviour; residual effect; physiology; environmental pollutant; sound
8.  Dominant male song performance reflects current immune state in a cooperatively breeding songbird 
Ecology and Evolution  2016;10.1002/ece3.1938.
Abstract
Conspicuous displays are thought to have evolved as signals of individual “quality”, though precisely what they encode remains a focus of debate. While high quality signals may be produced by high quality individuals due to “good genes” or favourable early‐life conditions, whether current immune state also impacts signalling performance remains poorly understood, particularly in social species. Here, we experimentally demonstrate that male song performance is impaired by immune system activation in the cooperatively breeding white‐browed sparrow weaver (Plocepasser mahali). We experimentally activated the immune system of free‐living dominant males via subcutaneous injection of phytohemagglutinin (PHA) and contrasted its effects with those of a control (phosphate buffered saline) injection. PHA‐challenged males showed significant reductions in both the duration and the rate of their song performance, relative to controls, and this could not be readily attributed to effects of the challenge on body mass, as no such effects were detected. Furthermore, male song performance prior to immune‐challenge predicted the scale of the inflammatory response to the challenge. Our findings suggest that song performance characteristics are impacted by current immune state. This link between current state and signal performance might therefore contribute to enforcing the honesty of signal performance characteristics. Impacts of current state on signaling may be of particular importance in social species, where subordinates may benefit from an ability to identify and subsequently challenge same‐sex dominants in a weakened state.
doi:10.1002/ece3.1938
PMCID: PMC4719765  PMID: 26811745
Behavioral plasticity; cooperative breeder; dominance; handicap hypothesis; resource‐allocation trade‐offs; sociality; state‐dependent signaling
9.  Impacts of regular and random noise on the behaviour, growth and development of larval Atlantic cod (Gadus morhua) 
Anthropogenic noise impacts behaviour and physiology in many species, but responses could change with repeat exposures. As repeat exposures can vary in regularity, identifying regimes with less impact is important for regulation. We use a 16-day split-brood experiment to compare effects of regular and random acoustic noise (playbacks of recordings of ships), relative to ambient-noise controls, on behaviour, growth and development of larval Atlantic cod (Gadus morhua). Short-term noise caused startle responses in newly hatched fish, irrespective of rearing noise. Two days of both regular and random noise regimes reduced growth, while regular noise led to faster yolk sac use. After 16 days, growth in all three sound treatments converged, although fish exposed to regular noise had lower body width–length ratios. Larvae with lower body width–length ratios were easier to catch in a predator-avoidance experiment. Our results demonstrate that the timing of acoustic disturbances can impact survival-related measures during development. Much current work focuses on sound levels, but future studies should consider the role of noise regularity and its importance for noise management and mitigation measures.
doi:10.1098/rspb.2015.1943
PMCID: PMC4633878  PMID: 26468248
anthropogenic noise; regularity; developmental stages; tank experiments; fish
10.  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.
doi:10.7717/peerj.594
PMCID: PMC4178459  PMID: 25276507
Cichlidae; Anthropogenic noise; Growth; Development; Offspring survival; Long-term noise exposure; Sound; Teleost; Fitness; Vertebrates; Lake Tanganyika
11.  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.
doi:10.1371/journal.pone.0102946
PMCID: PMC4109949  PMID: 25058618
12.  Effect of reward downshift on the behaviour and physiology of chickens 
Animal Behaviour  2015;105:21-28.
When a reward is downgraded in quantity or quality from that which is expected, one of two possible outcomes can result. Acquisition responses may decline gradually, owing to a strong stimulus–response reinforcement history, and thus follow the Thorndikian law of effect. Alternatively, there may be an exaggerated reaction to a downgraded reward when it is initially altered, compared to the behaviour of individuals that have always been trained to receive the lower magnitude reward; this is known as successive negative contrast (SNC). While behavioural SNC effects have been commonly demonstrated in mammals, evidence that they occur in other taxa is more equivocal. Additionally, studies demonstrating immediate physiological reactions during reward downshifts are limited. We investigated the reaction of chickens, Gallus gallus domesticus, to a downshift in the quality of a food reward that they had been trained to expect in a runway apparatus. During a preshift phase, 16 chickens (control) were given food that was flavoured to make it less preferred, while the other 16 (contrast) were fed the same food but without flavouring. During trial 7, unflavoured food was substituted by flavoured food for contrast hens and all birds were fed the flavoured food during a postshift phase. In the contrast group, food consumption immediately decreased and heart rate increased when the reward was downshifted from unflavoured to flavoured food, but there was no evidence of SNC effects, which could stem from methodological or taxonomic differences from previous studies. The latency to reach the food appeared to follow the Thorndikian law of effect, gradually increasing following the downshift. We suggest that the disparity between the pattern shown by the latency results and other measures could relate to the time period in which measures were taken, as acquisition responses are more likely to follow the law of effect.
Highlights
•We investigated the reactions of chickens to an unexpected downshift in reward.•Food consumption decreased and heart rate increased immediately after the downshift.•Latency to reach food followed the Thorndikian law of effect by increasing gradually.•There was no evidence of successive negative contrast effects.
doi:10.1016/j.anbehav.2015.04.005
PMCID: PMC4510205  PMID: 26257402
bird; chicken; contrast; expectation; heart rate; latency to reach food; reward; temperature
13.  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.
doi:10.1098/rsbl.2013.0970
PMCID: PMC3917340  PMID: 24429683
lunar cycle; moon phase; twilight; light pollution; song; dawn chorus
14.  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.
doi:10.1371/journal.pone.0108809
PMCID: PMC4183509  PMID: 25275440
15.  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.
doi:10.1038/srep05891
PMCID: PMC4118180  PMID: 25080997
16.  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.
doi:10.1098/rsbl.2012.1194
PMCID: PMC3639773  PMID: 23445945
anthropogenic noise; habituation; tolerance; pollution; global change; interindividual variation
17.  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.
doi:10.1098/rspb.2013.2683
PMCID: PMC3871318  PMID: 24335986
environmental change; fitness; hearing; insect; noise quantification; pollution
18.  Negotiating a stable solution for vigilance behaviour 
doi:10.1098/rspb.2012.1210
PMCID: PMC3415925  PMID: 22787028
19.  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.
doi:10.1098/rsbl.2011.0559
PMCID: PMC3259957  PMID: 21795264
affiliation; cooperation; grooming; group-living; stress
20.  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.
doi:10.1098/rsbl.2010.0455
PMCID: PMC3030868  PMID: 20573617
law of brevity; Neotropical primates; vocal repertoire; signalling
21.  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.
doi:10.1098/rsbl.2010.0507
PMCID: PMC3030875  PMID: 20610419
cooperation; grooming; sociality; primates; group-living; cooperative breeding
22.  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.
doi:10.1371/journal.pone.0025010
PMCID: PMC3184948  PMID: 21984898
23.  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.
doi:10.1371/journal.pone.0017478
PMCID: PMC3046255  PMID: 21386909
24.  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.
doi:10.1371/journal.pone.0016625
PMCID: PMC3033890  PMID: 21326604
25.  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.
doi:10.1098/rspb.2009.0187
PMCID: PMC2690466  PMID: 19364740
public information; reliability; anti-predator vigilance; foraging efficiency; vocalizations; cooperative breeding

Results 1-25 (27)