RESUMO
For over a century, the evolution of animal play has sparked scientific curiosity. The prevalence of social play in juvenile mammals suggests that play is a beneficial behavior, potentially contributing to individual fitness. Yet evidence from wild animals supporting the long-hypothesized link between juvenile social play, adult behavior, and fitness remains limited. In Western Australia, adult male bottlenose dolphins (Tursiops aduncus) form multilevel alliances that are crucial for their reproductive success. A key adult mating behavior involves allied males using joint action to herd individual females. Juveniles of both sexes invest significant time in play that resembles adult herding-taking turns in mature male (actor) and female (receiver) roles. Using a 32-y dataset of individual-level association patterns, paternity success, and behavioral observations, we show that juvenile males with stronger social bonds are significantly more likely to engage in joint action when play-herding in actor roles. Juvenile males also monopolized the actor role and produced an adult male herding vocalization ("pops") when playing with females. Notably, males who spent more time playing in the actor role as juveniles achieved more paternities as adults. These findings not only reveal that play behavior provides male dolphins with mating skill practice years before they sexually mature but also demonstrate in a wild animal population that juvenile social play predicts adult reproductive success.
Assuntos
Golfinho Nariz-de-Garrafa , Reprodução , Comportamento Sexual Animal , Comportamento Social , Animais , Masculino , Golfinho Nariz-de-Garrafa/fisiologia , Feminino , Reprodução/fisiologia , Comportamento Sexual Animal/fisiologia , Austrália Ocidental , Vocalização Animal/fisiologia , Jogos e BrinquedosRESUMO
Extensive research has investigated the relationship between the social environment and cognition, suggesting that social complexity may drive cognitive evolution and development. However, evidence for this relationship remains equivocal. Group size is often used as a measure of social complexity, but this may not capture intraspecific variation in social interactions. Social network analysis can provide insight into the cognitively demanding challenges associated with group living at the individual level. Here, we use social networks to investigate whether the cognitive performance of wild Western Australian magpies (Gymnorhina tibicen dorsalis) is related to group size and individual social connectedness. We quantified social connectedness using four interaction types: proximity, affiliative, agonistic and vocal. Consistent with previous research on this species, individuals in larger groups performed better on an associative learning task. However, social network position was also related to cognitive performance. Individuals receiving aggressive interactions performed better, while those involved in aggressive interactions with more group members performed worse. Overall, this suggests that cognitive performance is related to specific types of social interaction. The findings from this study highlight the value of considering fine-grained metrics of sociality that capture the challenges associated with social life when testing the relationship between the social environment and cognition.
Assuntos
Agressão , Cognição , Comportamento Social , Animais , Austrália Ocidental , Masculino , Passeriformes/fisiologia , FemininoRESUMO
Despite considerable research into the structure of cognition in non-human animal species, there is still much debate as to whether animal cognition is organised as a series of discrete domains or an overarching general cognitive factor. In humans, the existence of general intelligence is widely accepted, but less work has been undertaken in animal psychometrics to address this question. The relatively few studies on non-primate animal species that do investigate the structure of cognition rarely include tasks assessing social cognition and focus instead on physical cognitive tasks. In this study, we tested 36 wild Western Australian magpies (Gymnorhina tibicen dorsalis) on a battery of three physical (associative learning, spatial memory, and numerical assessment) and one social (observational spatial memory) cognitive task, to investigate if cognition in this species fits a general cognitive factor model, or instead one of separate physical and social cognitive domains. A principal component analysis (PCA) identified two principal components with eigenvalues exceeding 1; a first component onto which all three physical tasks loaded strongly and positively, and a second component onto which only the social task (observational spatial memory) loaded strongly and positively. These findings provide tentative evidence for separate physical and social cognitive domains in this species, and highlight the importance of including tasks assessing both social and physical cognition in cognitive test batteries.
Assuntos
Cognição , Passeriformes , Animais , Masculino , Feminino , Passeriformes/fisiologia , Memória Espacial , Cognição SocialRESUMO
The social intelligence hypothesis states that the demands of social life drive cognitive evolution. This idea receives support from comparative studies that link variation in group size or mating systems with cognitive and neuroanatomical differences across species, but findings are contradictory and contentious. To understand the cognitive consequences of sociality, it is also important to investigate social variation within species. Here we show that in wild, cooperatively breeding Australian magpies, individuals that live in large groups show increased cognitive performance, which is linked to increased reproductive success. Individual performance was highly correlated across four cognitive tasks, indicating a 'general intelligence factor' that underlies cognitive performance. Repeated cognitive testing of juveniles at different ages showed that the correlation between group size and cognition emerged in early life, suggesting that living in larger groups promotes cognitive development. Furthermore, we found a positive association between the task performance of females and three indicators of reproductive success, thus identifying a selective benefit of greater cognitive performance. Together, these results provide intraspecific evidence that sociality can shape cognitive development and evolution.
Assuntos
Evolução Biológica , Cognição/fisiologia , Aptidão Genética , Passeriformes/fisiologia , Comportamento Social , Animais , Animais Selvagens/fisiologia , Austrália , Feminino , Inteligência/fisiologia , Masculino , Densidade Demográfica , Reprodução/fisiologiaRESUMO
Global temperatures are increasing rapidly. While considerable research is accumulating regarding the lethal and sublethal effects of heat on wildlife, its potential impact on animal cognition has received limited attention. Here, we tested wild southern pied babblers (Turdoides bicolor) on three cognitive tasks (associative learning, reversal learning and inhibitory control) under naturally occurring heat stress and non-heat stress conditions. We determined whether cognitive performance was explained by temperature, heat dissipation behaviours, individual and social attributes, or proxies of motivation. We found that temperature, but not heat dissipation behaviours, predicted variation in associative learning performance. Individuals required on average twice as many trials to learn an association when the maximum temperature during testing exceeded 38°C compared with moderate temperatures. Higher temperatures during testing were also associated with reduced inhibitory control performance, but only in females. By contrast, we found no temperature-related decline in performance in the reversal learning task, albeit individuals reached learning criterion in only 14 reversal learning tests. Our findings provide novel evidence of temperature-mediated cognitive impairment in a wild animal and indicate that its occurrence depends on the cognitive trait examined and individual sex.
Assuntos
Passeriformes , Humanos , Animais , Feminino , Temperatura , Cognição , Animais Selvagens , Reversão de AprendizagemRESUMO
Anthropogenic noise is a pollutant of growing concern, with wide-ranging effects on taxa across ecosystems. Until recently, studies investigating the effects of anthropogenic noise on animals focused primarily on population-level consequences, rather than individual-level impacts. Individual variation in response to anthropogenic noise may result from extrinsic or intrinsic factors. One such intrinsic factor, cognitive performance, varies between individuals and is hypothesised to aid behavioural response to novel stressors. Here, we combine cognitive testing, behavioural focals and playback experiments to investigate how anthropogenic noise affects the behaviour and anti-predator response of Western Australian magpies (Gymnorhina tibicen dorsalis), and to determine whether this response is linked to cognitive performance. We found a significant population-level effect of anthropogenic noise on the foraging effort, foraging efficiency, vigilance, vocalisation rate and anti-predator response of magpies, with birds decreasing their foraging, vocalisation behaviours and anti-predator response, and increasing vigilance when loud anthropogenic noise was present. We also found that individuals varied in their response to playbacks depending on their cognitive performance, with individuals that performed better in an associative learning task maintaining their anti-predator response when an alarm call was played in anthropogenic noise. Our results add to the growing body of literature documenting the adverse effects of anthropogenic noise on wildlife and provide the first evidence for an association between individual cognitive performance and behavioural responses to anthropogenic noise.
Assuntos
Ecossistema , Passeriformes , Humanos , Animais , Austrália , Ruído/efeitos adversos , Animais Selvagens , CogniçãoRESUMO
A robust understanding of cognitive variation at the individual level is essential to understand selection for and against cognitive traits. Studies of animal cognition often assume that within-individual performance is highly consistent. When repeated tests of individuals have been conducted, the effects of test order (the overall sequence in which different tests are conducted) and test number (the ordinal number indicating when a specific test falls within a sequence)-in particular the potential for individual performance to improve with repeated testing-have received limited attention. In our study, we investigated test order and test number effects on individual performance in three inhibitory control tests in Western Australian magpies (Cracticus tibicen dorsalis). We presented adult magpies with three novel inhibitory control tasks (detour-reaching apparatuses) in random order to test whether experience of cognitive testing and the order in which the apparatuses were presented were predictors of cognitive performance. We found that neither test number nor test order had an effect on cognitive performance of individual magpies when presenting different variants of inhibitory control tasks. This suggests that repeated testing of the same cognitive trait, using causally identical but visually distinct cognitive tasks, does not confound cognitive performance. We recommend that repeated testing effects of cognitive performance in other species be studied to broadly determine the validity of repeated testing in animal cognition studies.
Assuntos
Passeriformes , Animais , Austrália , CogniçãoRESUMO
Identifying the causes and fitness consequences of intraspecific variation in cognitive performance is fundamental to understand how cognition evolves. Selection may act on different cognitive traits separately or jointly as part of the general cognitive performance (GCP) of the individual. To date, few studies have examined simultaneously whether individual cognitive performance covaries across different cognitive tasks, the relative importance of individual and social attributes in determining cognitive variation, and its fitness consequences in the wild. Here, we tested 38 wild southern pied babblers (Turdoides bicolor) on a cognitive test battery targeting associative learning, reversal learning and inhibitory control. We found that a single factor explained 59.5% of the variation in individual cognitive performance across tasks, suggestive of a general cognitive factor. GCP varied by age and sex; declining with age in females but not males. Older females also tended to produce a higher average number of fledglings per year compared to younger females. Analysing over 10 years of breeding data, we found that individuals with lower general cognitive performance produced more fledglings per year. Collectively, our findings support the existence of a trade-off between cognitive performance and reproductive success in a wild bird.
Assuntos
Animais Selvagens , Passeriformes , Humanos , Animais , Feminino , Cruzamento , Reprodução , CogniçãoRESUMO
With global temperatures rapidly increasing, biologists require tools to assess how wild animals are responding to heat. Thermal imaging of the eye region offers a potential non-invasive alternative to traditional techniques to study thermoregulation and stress responses in wild animals. However, we currently have a poor understanding of how the temperature of the eye region is regulated under increasing temperature and whether this regulation differs among individuals. Here, we use thermal imaging to repeatedly measure the maximum temperature of the eye region (periorbital temperature) in 42 wild pied babblers (Turdoides bicolor) under natural air temperatures ranging from 14.3 to 42.5 °C. Our aim was to determine the relationship between periorbital temperature and air temperature, whether this relationship is repeatable, and whether it differs according to individual attributes. Periorbital temperature showed a non-linear increase with air temperature, becoming independent of air temperature above 38 °C. Above 38 °C, periorbital temperature was not explained by any individual attributes. Below 38 °C, periorbital temperature increased more steeply in individuals with low body mass and it was lower in older compared to younger females. However, the effect of these individual attributes was small compared to the effect of wind speed, air temperature and head tilt. Additionally, the repeatability of individual periorbital temperature was low (R < 0.25) and non-significant both below and above 38 °C. Our findings warrant caution in the use of periorbital temperature to infer individual thermoregulatory responses to increasing temperatures, especially in the wild, where control over confounding non-physiological factors is limited.
Assuntos
Animais Selvagens , Regulação da Temperatura Corporal , Animais , Aves/fisiologia , Temperatura Corporal , Feminino , Temperatura Alta , TemperaturaRESUMO
Relatively little effort has been directed towards elucidating the role of physiological stress pathways in mediating avian responses to global heating. For free-ranging southern pied babblers, Turdoides bicolor, daily maximum air temperatures (Tmax) between â¼35 and â¼40°C result in reduced foraging efficiency, loss of body mass and compromised breeding success. We tested the hypothesis that very hot days are experienced as stressors by quantifying relationships between Tmax and faecal glucocorticoid metabolite (fGCM) levels in naturally excreted droppings. On days when Tmax<38°C, fGCM levels were independent of Tmax (mean±s.d. 140.25±56.92â ng g-1 dry mass). At Tmax>38°C, however, fGCM levels increased linearly with Tmax and averaged 190.79±70.13â ng g-1 dry mass. The effects of Tmax on fGCM levels did not carry over to the following morning, suggesting that very hot days are experienced as acute stressors.
Assuntos
Passeriformes , Animais , Regulação da Temperatura Corporal , Glucocorticoides , Temperatura Alta , Estresse Fisiológico , TemperaturaRESUMO
Climate change is affecting animal populations around the world and one relatively unexplored aspect of species vulnerability is whether and to what extent responses to environmental stressors might be mitigated by variation in group size in social species. We used a 15-year data set for a cooperatively breeding bird, the southern pied babbler Turdoides bicolor, to determine the impact of temperature, rainfall and group size on body mass change and interannual survival in both juveniles and adults. Hot and dry conditions were associated with reduced juvenile growth, mass loss in adults and compromised survival between years in both juveniles (86% reduction in interannual survival) and adults (60% reduction in interannual survival). Individuals across all group sizes experienced similar effects of climatic conditions. Larger group sizes may not buffer individual group members against the impacts of hot and dry conditions, which are expected to increase in frequency and severity in future.
Assuntos
Secas , Passeriformes , Animais , Cruzamento , Mudança Climática , HumanosRESUMO
An improved understanding of life-history responses to current environmental variability is required to predict species-specific responses to anthopogenic climate change. Previous research has suggested that cooperation in social groups may buffer individuals against some of the negative effects of unpredictable climates. We use a 15-year dataset on a cooperative breeding arid zone bird, the southern pied babbler Turdoides bicolor, to test (i) whether environmental conditions and group size correlate with survival of young during three development stages (egg, nestling, fledgling) and (ii) whether group size mitigates the impacts of adverse environmental conditions on survival of young. Exposure to high mean daily maximum temperatures (mean Tmax) during early development was associated with reduced survival probabilities of young in all three development stages. No young survived when mean Tmax > 38°C, across all group sizes. Low survival of young at high temperatures has broad implications for recruitment and population persistence in avian communities given the rapid pace of advancing climate change. Impacts of high temperatures on survival of young were not moderated by group size, suggesting that the availability of more helpers in a group is unlikely to buffer against compromised offspring survival as average and maximum temperatures increase with rapid anthropogenic climate change.
Assuntos
Mudança Climática , Temperatura Alta , Passeriformes , Animais , Aves , CruzamentoRESUMO
Using faecal matter to monitor stress levels in animals non-invasively is a powerful technique for elucidating the effects of biotic and abiotic stressors on free-living animals. To validate the use of droppings for measuring stress in southern pied babblers (Turdoides bicolor) we performed an ACTH challenge on captive individuals and determined the effect of temporary separation from their social group on their faecal glucocorticoid metabolite (fGCM) concentration. Additionally, we compared fGCM concentrations of captive babblers to those of wild conspecifics and examined the effects of dominance rank on fGCM concentration. We found droppings to be a suitable matrix for measuring physiological stress in babblers and that individual separation from the group caused an increase in fGCM levels. In addition, babblers temporarily held in captivity had substantially higher fGCM concentrations than wild individuals, indicating that babblers kept in captivity experience high levels of stress. In wild, free-living individuals, dominant males showed the highest levels of stress, suggesting that being the dominant male of a highly territorial social group is stressful. Non-invasive sampling allows field-based researchers to reduce disturbance related to monitoring adrenocortical function, thereby avoiding artificially increasing circulating corticosterone concentration as it is not necessary to physically restrain study animals.
Assuntos
Passeriformes/fisiologia , Estresse Fisiológico , Clima Tropical , Hormônio Adrenocorticotrópico/farmacologia , Animais , Corticosterona/sangue , Fezes/química , Feminino , Glucocorticoides/metabolismo , Técnicas Imunoenzimáticas , Masculino , Metaboloma , Passeriformes/sangueRESUMO
We recently identified a strong, positive relationship between group size and individual cognitive performance, and a strong, positive relationship between female cognitive performance and reproductive success (Ashton, Ridley, Edwards, & Thornton in Nature, 554, 364-367, 2018). An opinion piece by Smulders (Learning & Behavior, https://doi.org/10.3758/s13420-018-0335-0, 2018) raised the interesting notion that these patterns may be underlined by motivational factors. In this commentary, we highlight why none of the available data are consistent with this explanation, but instead support the argument that the demands of group living influence cognitive development, with knock-on consequences for fitness.
Assuntos
Cognição , Motivação , Animais , FemininoRESUMO
Language's expressive power is largely attributable to its compositionality: meaningful words are combined into larger/higher-order structures with derived meaning. Despite its importance, little is known regarding the evolutionary origins and emergence of this syntactic ability. Although previous research has shown a rudimentary capability to combine meaningful calls in primates, because of a scarcity of comparative data, it is unclear to what extent analog forms might also exist outside of primates. Here, we address this ambiguity and provide evidence for rudimentary compositionality in the discrete vocal system of a social passerine, the pied babbler (Turdoides bicolor). Natural observations and predator presentations revealed that babblers produce acoustically distinct alert calls in response to close, low-urgency threats and recruitment calls when recruiting group members during locomotion. On encountering terrestrial predators, both vocalizations are combined into a "mobbing sequence," potentially to recruit group members in a dangerous situation. To investigate whether babblers process the sequence in a compositional way, we conducted systematic experiments, playing back the individual calls in isolation as well as naturally occurring and artificial sequences. Babblers reacted most strongly to mobbing sequence playbacks, showing a greater attentiveness and a quicker approach to the loudspeaker, compared with individual calls or control sequences. We conclude that the sequence constitutes a compositional structure, communicating information on both the context and the requested action. Our work supports previous research suggesting combinatoriality as a viable mechanism to increase communicative output and indicates that the ability to combine and process meaningful vocal structures, a basic syntax, may be more widespread than previously thought.
Assuntos
Passeriformes/fisiologia , Vocalização Animal/fisiologia , AnimaisRESUMO
There is a large body of research on conflict in nonhuman animal groups that measures the costs and benefits of intergroup conflict, and we suggest that much of this evidence is missing from De Dreu and Gross's interesting article. It is a shame this work has been missed, because it provides evidence for interesting ideas put forward in the article.
Assuntos
Conflito Psicológico , Processos Grupais , Animais , Humanos , PesquisaRESUMO
Many cooperatively breeding societies are characterized by high reproductive skew, such that some socially dominant individuals breed, while socially subordinate individuals provide help. Inbreeding avoidance serves as a source of reproductive skew in many high-skew societies, but few empirical studies have examined sources of skew operating alongside inbreeding avoidance or compared individual attempts to reproduce (reproductive competition) with individual reproductive success. Here, we use long-term genetic and observational data to examine factors affecting reproductive skew in the high-skew cooperatively breeding southern pied babbler (Turdoides bicolor). When subordinates can breed, skew remains high, suggesting factors additional to inbreeding avoidance drive skew. Subordinate females are more likely to compete to breed when older or when ecological constraints on dispersal are high, but heavy subordinate females are more likely to successfully breed. Subordinate males are more likely to compete when they are older, during high ecological constraints, or when they are related to the dominant male, but only the presence of within-group unrelated subordinate females predicts subordinate male breeding success. Reproductive skew is not driven by reproductive effort, but by forces such as intrinsic physical limitations and intrasexual conflict (for females) or female mate choice, male mate-guarding and potentially reproductive restraint (for males). Ecological conditions or "outside options" affect the occurrence of reproductive conflict, supporting predictions of recent synthetic skew models. Inbreeding avoidance together with competition for access to reproduction may generate high skew in animal societies, and disparate processes may be operating to maintain male vs. female reproductive skew in the same species.
Assuntos
Passeriformes/fisiologia , Reprodução , Comportamento Sexual Animal , Animais , Cruzamento , Feminino , Hierarquia Social , Endogamia , Masculino , Caracteres SexuaisRESUMO
Delayed dispersal is a key step in the evolution of familial animal societies and cooperative breeding. However, no consensus has been reached on the ecological and social circumstances driving delayed dispersal. Here, we test predictions from the ecological constraints and benefits of philopatry hypotheses as well as the recently proposed dual benefits hypothesis to better understand the evolution of group-living and cooperative breeding. Furthermore, we consider how individual social circumstances within groups affect dispersal decisions. We examine 11 years of life-history information on a wild population of cooperatively breeding southern pied babblers Turdoides bicolor. We investigate the effects of ecological conditions, natal-group membership and individual social context on male and female dispersal delays, disperser survival and acquisition of dominance. Female dispersal decisions are generally unconstrained by ecological or social circumstances. In contrast, males disperse in response to relaxed ecological constraints, decreases in nepotistic tolerance or when low social rank in the queue for dominance decreases their likelihood of gaining a dominant breeding position. Early dispersal by end-of-queue males often leads to a head-of-queue subordinate position in a non-natal group, thereby increasing access to dominant breeding positions. However, males and females remaining in natal groups gain benefits of philopatry via increased survival and, for head-of-queue males, very high likelihood of acquisition of a breeding position. Overall, predictions from the dual benefits hypothesis best describe these results, while some predictions from each of the ecological constraints and benefits of philopatry hypotheses were supported. The benefits of living and working together (collective action benefits) in large stable groups are of central importance in shaping dispersal delays in southern pied babbler societies. In addition, position in the subordinate social queue for dominance is the key in determining access to reproduction, particularly for males. This research highlights the importance of considering the costs and benefits of individual social circumstances in dispersal decisions and illustrates how the dual benefits hypothesis offers new perspectives in understanding delayed dispersal.
Assuntos
Cruzamento , Passeriformes , Animais , Ecologia , Feminino , Masculino , ReproduçãoRESUMO
Human language is a recombinant system that achieves its productivity through the combination of a limited set of sounds. Research investigating the evolutionary origin of this generative capacity has generally focused on the capacity of non-human animals to combine different types of discrete sounds to encode new meaning, with less emphasis on meaning-differentiating mechanisms achieved through potentially simpler temporal modifications within a sequence of repeated sounds. Here we show that pied babblers (Turdoides bicolor) generate two functionally distinct vocalisations composed of the same sound type, which can only be distinguished by the number of repeated elements. Specifically, babblers produce extended 'purrs' composed of, on average, around 17 element repetitions when drawing young offspring to a food source and truncated 'clucks' composed of a fixed number of 2-3 elements when collectively mediating imminent changes in foraging site. We propose that meaning-differentiating temporal structuring might be a much more widespread combinatorial mechanism than currently recognised and is likely of particular value for species with limited vocal repertoires in order to increase their communicative output.
Assuntos
Passeriformes/fisiologia , Vocalização Animal/fisiologia , Acústica , Animais , Comportamento ApetitivoRESUMO
In many cooperatively breeding societies, subordinate individuals delay dispersal and independent breeding. The length of time that subordinates delay dispersal (subordinate tenure) is likely to have important implications for both subordinate and dominant fitness. However, quantitative comparisons of the subordinate tenure of males and females are rare, especially with respect to the presence of same- versus opposite-sex close kin. Here, we investigate subordinate tenure and how it is affected by the genetic relationship between subordinates and dominants in the cooperatively breeding southern pied babbler (Turdoides bicolor). We find that for males, longer subordinate tenures result in increased likelihood of attaining dominance. In the presence of an unrelated dominant male, tenure of subordinate males is significantly shorter, indicating nepotism among males. Female tenures are unaffected by the genetic relationship to either the dominant male or female. These results are some of the first to demonstrate that the sex of both the dominants and subordinates, and the genetic relationship between them, can have significant impacts on subordinate tenure and dispersal delays. Nepotism has likely played a vital role in the evolution of cooperative breeding in this species.