The glucocorticoid response in a free-living bird predicts whether long-lasting memories fade or strengthen with time

Jones, Blake Carlton; Bebus, Sara E.; Ferguson, Stephen M.; Bateman, Philip W.; Schoech, Stephan J.

doi:10.1016/j.anbehav.2016.10.009

Cited by 13 publications

(6 citation statements)

References 133 publications

(179 reference statements)

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“…While such differences might be influenced by previous experience with predators [ 46 , 47 ], it is also possible that individual differences in agitation (possibly linked to variation in stress reactivity or coping styles; [ 48 ]) could affect the potential for individuals to learn about novel predators, both in experimental and natural contexts. While a hormonally mediated stress response is known to be necessary to promote aversion learning [ 49 , 50 ], there is some evidence that acute levels of stress can inhibit learning [ 51 ]. Moreover, highly anxious individuals may be faster to flee upon hearing conspecific alarm calls, thus reducing their potential for learning to associate the calls with the presence of a novel predator.…”

Section: Discussionmentioning

confidence: 99%

Testing social learning of anti-predator responses in juvenile jackdaws: the importance of accounting for levels of agitation

McIvor¹,

Lee²,

Thornton³

2018

R. Soc. open sci.

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Social learning is often assumed to help young animals respond appropriately to potential threats in the environment. We brought wild, juvenile jackdaws briefly into captivity to test whether short exposures to conspecific vocalizations are sufficient to promote anti-predator learning. Individuals were presented with one of two models—a stuffed fox representing a genuine threat, or a toy elephant simulating a novel predator. Following an initial baseline presentation, juveniles were trained by pairing models with either adult mobbing calls, indicating danger, or contact calls suggesting no danger. In a final test phase with no playbacks, birds appeared to have habituated to the elephant, regardless of training, but responses to the fox remained high throughout, suggesting juveniles already recognized it as a predator before the experiment began. Training with mobbing calls did seem to generate elevated escape responses, but this was likely to be a carry-over effect of the playback in the previous trial. Overall, we found little evidence for social learning. Instead, individuals' responses were mainly driven by their level of agitation immediately preceding each presentation. These results highlight the importance of accounting for agitation in studies of anti-predator learning, and whenever animals are held in captivity for short periods.

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Section: Discussionmentioning

confidence: 99%

Testing social learning of anti-predator responses in juvenile jackdaws: the importance of accounting for levels of agitation

McIvor¹,

Lee²,

Thornton³

2018

R. Soc. open sci.

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“…It is still unclear, however, whether the increased enzymatic activities observed are due to the "fear" directly caused by the presence of the predator itself (as suggested by the predation stress hypothesis; Boonstra et al 1998;Clinchy et al 2004). The risk perceived by the prey can, for example, lead to increased glucocorticoid levels (e.g., Cockrem and Silverin 2002;Sheriff et al 2009) even when predator encounters are very short (up to a few seconds; Jones et al 2016b), and it can have long-term consequences on prey response to threat (Jones et al 2016a). On the other hand, variation in the cellular antioxidant metabolism could also be a consequence of behavioral antipredator responses, which could, for example, reduce foraging efficiency (the predatorsensitive food hypothesis; e.g., Sinclair and Arcese 1995;Zanette et al 2011;Zanette et al 2014).…”

Section: Discussionmentioning

confidence: 99%

“…Predation risk is known to induce a physiological stress response in prey in response to both acute and chronic stress events (e.g., Cockrem and Silverin 2002;Butler et al 2009;Sheriff et al 2009Sheriff et al , 2011Clinchy et al 2011;Zanette et al 2014;Jones et al 2016b) that can affect animals' physiology and fitness even long after the pred-ator encounter (Sheriff et al 2009(Sheriff et al , 2011Jones et al 2016a). Our results suggest that predation risk could also modify animal antioxidant enzyme activities, although the effect may be enhanced by cold temperatures.…”

Section: Discussionmentioning

confidence: 99%

Antioxidant Enzyme Activities Vary with Predation Risk and Environmental Conditions in Free-Living Passerine Birds

Morosinotto

Rainio

Ruuskanen

et al. 2018

Physiological and Biochemical Zoology

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Prolonged physiological stress response may lead to an excessive production of reactive oxygen species (ROS) and ultimately to oxidative stress and severe fitness costs. We investigated whether natural variation in predation risk, induced by pygmy owls (Glaucidium passerinum), modifies the oxidative status of two free-living food-supplemented passerine bird species-the great tit (Parus major) and the willow tit (Poecile montanus)-in March 2012 and 2013. Predation risk significantly affected antioxidant enzyme activities of willow tits. Antioxidant enzyme activities (principal component factor 2 [PC2] representing glutathione-S-transferase and superoxide dismutase activities) were higher in high predation risk areas in 2013 than in low predation risk areas in the same year. Higher enzyme activities may suggest higher ROS production in birds living under high predation risk. In addition, antioxidant enzyme activities (PC2) were also higher in high predation risk areas in 2013 than in high predation risk areas in the previous year, 2012. This may represent variation in the risk represented by pygmy owls, which is probably inversely related to the natural fluctuations in the densities of their main prey, voles. In willow tits, PC1 (representing catalase, total glutathione, the ratio of reduced to oxidized glutathione, and protein carbonylation) was not affected by perceived predation risk, nor were antioxidant levels or enzyme activities in great tits. Higher enzyme activities observed in willow tits suggest that predator presence can modify the antioxidant status of avian prey, but the response also seem to be influenced by other environmental characteristics, like harsh winter conditions.

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“…Corticosterone is an important glucocorticoid in vertebrates, being part of the complex physiological stress response and promoting behaviors that directly or indirectly enhance survival (e.g., decreased reproductive activity [Belliure, Smith, & Sorci, ], increased locomotor activity [Clobert et al, ]). Experimental data (mainly on avian species) indicate that stress‐induced corticosterone affects cognitive abilities (Bebus, Small, Jones, Elderbrock, & Schoech, ; Bókony et al, ; Jones, Bebus, Ferguson, Bateman, & Schoech, ; Ruiz‐Gomez, Huntingford, Øverli, Thörnqvist, & Höglund, ). In addition, bold behavioral types (i.e., risk‐prone, active, superficial explorer) seem to be associated with low, while shy behavioral types (i.e., risk‐averse, less active, thorough explorer) with high basal levels of corticosterone (see Carere et al, ; Cockrem, ; Koolhaas et al, ).…”

Section: Introductionmentioning

confidence: 99%

Maternal diet affects juvenile Carpetan rock lizard performance and personality

Horváth

Rodríguez‐Ruiz

Martı́n

et al. 2019

Ecology and Evolution

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Differences in both stable and labile state variables are known to affect the emergence and maintenance of consistent interindividual behavioral variation (animal personality or behavioral syndrome), especially when experienced early in life. Variation in environmental conditions experienced by gestating mothers (viz. nongenetic maternal effects) is known to have significant impact on offspring condition and behavior; yet, their effect on behavioral consistency is not clear. Here, by applying an orthogonal experimental design, we aimed to study whether increased vitamin D3 content in maternal diet during gestation (vitamin‐supplemented vs. vitamin control treatments) combined with corticosterone treatment (corticosterone‐treated vs. corticosterone control treatments) applied on freshly hatched juveniles had an effect on individual state and behavioral consistency of juvenile Carpetan rock lizards (Iberolacerta cyreni). We tested the effect of our treatments on (a) climbing speed and the following levels of behavioral variation, (b) strength of animal personality (behavioral repeatability), (c) behavioral type (individual mean behavior), and (d) behavioral predictability (within‐individual behavioral variation unrelated to environmental change). We found higher locomotor performance of juveniles from the vitamin‐supplemented group (42.4% increase), irrespective of corticosterone treatment. While activity personality was present in all treatments, shelter use personality was present only in the vitamin‐supplemented × corticosterone‐treated treatment and risk‐taking personality was present in corticosterone control treatments. Contrary to our expectations, behavioral type was not affected by our treatments, indicating that individual quality can affect behavioral strategies without affecting group‐level mean behavior. Behavioral predictability decreased in individuals with low climbing speed, which could be interpreted as a form of antipredator strategy. Our results clearly demonstrate that maternal diet and corticosterone treatment have the potential to induce or hamper between‐individual variation in different components of boldness, often in interactions.

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The glucocorticoid response in a free-living bird predicts whether long-lasting memories fade or strengthen with time

Cited by 13 publications

References 133 publications

Testing social learning of anti-predator responses in juvenile jackdaws: the importance of accounting for levels of agitation

Testing social learning of anti-predator responses in juvenile jackdaws: the importance of accounting for levels of agitation

Antioxidant Enzyme Activities Vary with Predation Risk and Environmental Conditions in Free-Living Passerine Birds

Maternal diet affects juvenile Carpetan rock lizard performance and personality

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