High temperatures during early development reduce adult cognitive performance and reproductive success in a wild animal population.

Global warming is rapidly changing the phenology, distribution, behaviour and demography of wild animal populations. Recent studies in wild animals have shown that high temperatures can induce short-term cognitive impairment, and captive studies have demonstrated that heat exposure during early development can lead to long-term cognitive impairment. Given that cognition underpins behavioural flexibility and can be directly linked to fitness, understanding how high temperatures during early life might impact adult cognitive performance in wild animals is a critical next step to predict wildlife responses to climate change. Here, we investigated the relationship between temperatures experienced during development, adult cognitive performance, and reproductive success in wild southern pied babblers (Turdoides bicolor). We found that higher mean daily maximum temperatures during nestling development led to long-term cognitive impairment in associative learning performance, but not reversal learning performance. Additionally, a higher number of hot days (exceeding 35.5 °C, temperature threshold at which foraging efficiency and offspring provisioning decline) during post-fledging care led to reduced reproductive success in adulthood. We did not find evidence that low reproductive success was linked to impaired associative learning performance: associative learning performance was not related to reproductive success. In contrast, reversal learning performance was negatively related to reproductive success in breeding adults. This suggests that reproduction can carry a cost in terms of reduced performance in cognitively demanding tasks, confirming previous evidence in this species. Taken together, these findings indicate that naturally occurring high temperatures during early development have long-term negative effects on cognition and reproductive success in wild animals. Compounding effects of high temperatures on current nestling mortality and on the long-term cognitive and reproductive performance of survivors are highly concerning given ongoing global warming.

Helpers don't help when it's hot in a cooperatively breeding bird, the Southern Pied Babbler.

Cooperative breeding, where more than two individuals invest in rearing a single brood, occurs in many bird species globally and often contributes to improved breeding outcomes. However, high temperatures are associated with poor breeding outcomes in many species, including cooperative species. We used data collected over three austral summer breeding seasons to investigate the contribution that helpers make to daytime incubation in a cooperatively breeding species, the Southern Pied Babbler Turdoides bicolor, and the ways in which their contribution is influenced by temperature. Helpers spent a significantly higher percentage of their time foraging (41.8 ± 13.7%) and a significantly lower percentage of their time incubating (18.5 ± 18.8%) than members of the breeding pair (31.3 ± 11% foraging and 37.4 ± 15.7% incubating). In groups with only one helper, the helper's contribution to incubation was similar to that of breeders. However, helpers in larger groups contributed less to incubation, individually, with some individuals investing no time in incubation on a given observation day. Helpers significantly decrease their investment in incubation on hot days (>35.5°C), while breeders tend to maintain incubation effort as temperatures increase. Our results demonstrate that pied babblers share the workload of incubation unequally between breeders and helpers, and this inequity is more pronounced during hot weather. These results may help to explain why recent studies have found that larger group size does not buffer against the impacts of high temperatures in this and other cooperatively breeding species.

Dehydration risk is associated with reduced nest attendance and hatching success in a cooperatively breeding bird, the southern pied babbler Turdoides bicolor.

High air temperatures have measurable negative impacts on reproduction in wild animal populations, including during incubation in birds. Understanding the mechanisms driving these impacts requires comprehensive knowledge of animal physiology and behaviour under natural conditions. We used a novel combination of a non-invasive doubly labelled water (DLW) technique, nest temperature data and field-based behaviour observations to test effects of temperature, rainfall and group size on physiology and behaviour during incubation in southern pied babblers Turdoides bicolor, a cooperatively breeding passerine endemic to the arid savanna regions of southern Africa. The proportion of time that clutches were incubated declined as air temperatures increased, a behavioural pattern traditionally interpreted as a benefit of ambient incubation. However, we show that (i) clutches had a <50% chance of hatching when exposed to daily maximum air temperatures of >35.3°C; (ii) pied babbler groups incubated their nests almost constantly (99% of daylight hours) except on hot days; (iii) operative temperatures in unattended nests frequently exceeded 40.5°C, above which bird embryos are at risk of death; (iv) pied babblers incubating for long periods of time failed to maintain water balance on hot days; and (v) pied babblers from incubating groups lost mass on hot days. These results suggest that pied babblers might leave their nests during hot periods to lower the risk of dehydration associated with prolonged incubation at high operative temperatures. As mean air temperatures increase and extreme heat events become more frequent under climate change, birds will likely incur ever greater thermoregulatory costs of incubation, leading to compromised nest attendance and increased potential for eggs to overheat, with implications for nest success and, ultimately, population persistence.

Hot days are associated with short-term adrenocortical responses in a southern African arid-zone passerine bird.

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 ∼35 and ∼40°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±56.92 ng g-1 dry mass). At Tmax>38°C, however, fGCM levels increased linearly with Tmax and averaged 190.79±70.13 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.

High temperatures drive offspring mortality in a cooperatively breeding bird.

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.

Hot droughts compromise interannual survival across all group sizes in a cooperatively breeding bird.

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.

Non-invasive monitoring of physiological stress in an afrotropical arid-zone passerine bird, the southern pied babbler.

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.