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.

High temperatures are associated with reduced cognitive performance in wild southern pied babblers.

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.

Extra food provisioning does not affect behavioral lateralization in nestling lesser kestrels.

Costs and benefits of brain lateralization may depend on environmental conditions. Growing evidence indicates that the development of brain functional asymmetries is adaptively shaped by the environmental conditions experienced during early life. Food availability early in life could act as a proxy of the environmental conditions encountered during adulthood, but its potential modulatory effect on lateralization has received little attention. We increased food supply from egg laying to early nestling rearing in a wild population of lesser kestrels Falco naumanni, a sexually dimorphic raptor, and quantified the lateralization of preening behavior (head turning direction). As more lateralized individuals may perform better in highly competitive contexts, we expected that extra food provisioning, by reducing the level of intra-brood competition for food, would reduce the strength of lateralization. We found that extra food provisioning improved nestling growth, but it did not significantly affect the strength or direction of nestling lateralization. In addition, maternal body condition did not explain variation in nestling lateralization. Independently of extra food provisioning, the direction of lateralization differed between the sexes, with female nestlings turning more often toward their right. Our findings indicate that early food availability does not modulate behavioral lateralization in a motor task, suggesting limited phenotypic plasticity in this trait.

General cognitive performance declines with female age and is negatively related to fledging success in a wild bird.

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.

Periorbital temperature responses to natural air temperature variation in wild birds.

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.