TY - JOUR
T1 - High temperatures during early development reduce adult cognitive performance and reproductive success in a wild animal population
AU - Soravia, Camilla
AU - Ashton, Benjamin J.
AU - Thornton, Alex
AU - Bourne, Amanda R.
AU - Ridley, Amanda R.
N1 - Funding Information:
We thank the Kuruman River Reserve managers and the families at the surrounding farms (Van Zylsrus, South Africa) for making this work possible. We thank Lina Peña-Ramirez, Grace Blackburn, Amy Hunter, Samantha Wagstaff and Mara Zali for fieldwork assistance and all the researchers that contributed to the long-term life history database. We thank the Hot Birds Research Project for the weather station data and the FitzPatrick Institute of African Ornithology for logistical support. We thank Grace Blackburn for helpful discussions and Prof. Leigh Simmons for his support as co-supervisor to CS. We also thank Nicholas Pattinson for taking the photographs used in the graphical abstract. This work was supported by the Australian Government (RTP scholarship awarded to CS and grant DP220103823 awarded to ARR, BJA and AT) and by the Rotary Club of Melville and The University of Western Australia (two awards to CS). The KRR was financed by the Universities of Cambridge and Zurich, the MAVA Foundation and the European Research Council (grant 294494 to Tim Clutton-Brock) and received logistical support from the University of Pretoria. This research was approved by the Animal Ethics Committee, UWA (RA/3/100/1619 and 2021/ET000414) and the Department of Environment and Nature Conservation, Northern Cape Province, South Africa (permit n. 0024.2022)
Funding Information:
We thank the Kuruman River Reserve managers and the families at the surrounding farms (Van Zylsrus, South Africa) for making this work possible. We thank Lina Peña-Ramirez, Grace Blackburn, Amy Hunter, Samantha Wagstaff and Mara Zali for fieldwork assistance and all the researchers that contributed to the long-term life history database. We thank the Hot Birds Research Project for the weather station data and the FitzPatrick Institute of African Ornithology for logistical support. We thank Grace Blackburn for helpful discussions and Prof. Leigh Simmons for his support as co-supervisor to CS. We also thank Nicholas Pattinson for taking the photographs used in the graphical abstract. This work was supported by the Australian Government (RTP scholarship awarded to CS and grant DP220103823 awarded to ARR, BJA and AT) and by the Rotary Club of Melville and The University of Western Australia (two awards to CS). The KRR was financed by the Universities of Cambridge and Zurich , the MAVA Foundation and the European Research Council (grant 294494 to Tim Clutton-Brock) and received logistical support from the University of Pretoria . This research was approved by the Animal Ethics Committee, UWA (RA/3/100/1619 and 2021/ET000414) and the Department of Environment and Nature Conservation, Northern Cape Province, South Africa (permit n. 0024.2022)
Publisher Copyright:
© 2023 The Authors
PY - 2024/2/20
Y1 - 2024/2/20
N2 - 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.
AB - 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.
KW - Climate change
KW - Cognition
KW - Early development
KW - Fitness
KW - Heat stress
KW - Pied babblers
UR - http://www.scopus.com/inward/record.url?scp=85179882282&partnerID=8YFLogxK
U2 - 10.1016/j.scitotenv.2023.169111
DO - 10.1016/j.scitotenv.2023.169111
M3 - Article
C2 - 38070557
AN - SCOPUS:85179882282
SN - 0048-9697
VL - 912
JO - Science of the Total Environment
JF - Science of the Total Environment
M1 - 169111
ER -
