Correction: Does Environmental Enrichment Reduce Stress? An Integrated Measure of Corticosterone from Feathers Provides a Novel Perspective

Abstract

Enrichment is widely used as tool for managing fearfulness, undesirable behaviors, and stress in captive animals, and for studying exploration and personality. Inconsistencies in previous studies of physiological and behavioral responses to enrichment led us to hypothesize that enrichment and its removal are stressful environmental changes to which the hormone corticosterone and fearfulness, activity, and exploration behaviors ought to be sensitive. We conducted two experiments with a captive population of wild-caught Clark's nutcrackers (Nucifraga columbiana) to assess responses to short-(10-d) and long-term (3-mo) enrichment, their removal, and the influence of novelty, within the same animal.Variation in an integrated measure of corticosterone from feathers, combined with video recordings of behaviors, suggests that how individuals perceive enrichment and its removal depends on the duration of exposure. Short-and long-term enrichment elicited different physiological responses, with the former acting as a stressor and birds exhibiting acclimation to the latter. Non-novel enrichment evoked the strongest corticosterone responses of all the treatments, suggesting that the second exposure to the same objects acted as a physiological cue, and that acclimation was overridden by negative past experience. Birds showed weak behavioral responses that were not related to corticosterone. By demonstrating that an integrated measure of glucocorticoid physiology varies significantly with changes to enrichment in the absence of agonistic interactions, our study sheds light on potential mechanisms driving physiological and behavioral responses to environmental change.

Feather Corticosterone Measurements of Greater Flamingos Living under Different Forms of Flight Restraint

“…As predicted, in the two zoos in which cranes were observed to intentionally attack the flamingos (i.e., zoos K and L) the highest CORTf values were measured. This supports the hypothesis that repetitive and/or severe stressful events can have a measurable influence on CORTf [32,33].…”

“…However, results have consistently led to the conclusion that CORTf is a useful measure to show HPA-axis reactions to stimuli in order to predict an alteration in allostatic load. Fairhurst et al [33] were able to show a short-term increase of CORTf followed by a long-term decrease in Clark's Nutcrackers (Nucifraga columbiana) in response to enrichment. Will et al [46] measured elevated CORTf levels in food-deprived Rhinoceros Auklet (Cerorhinca moncerata) chicks.…”

“…Measuring CORT concentrations in feathers (CORTf) is a rather new but increasingly used method in the field of stress research in birds [31]. Compared to the conventional measurement of plasma CORT, the assessment of CORTf has some advantages: (1) it is minimally or even noninvasive-feathers can be plucked both from live [32][33][34] or dead birds [35] or even collected from molting individuals without capturing them [31]; (2) it enables a retrospective, integrated measure of HPA-axis activity for the time period of feather growth and cannot be distorted by capture as long as feather growth is finished at the time of collection [35]; and (3) feathers are a stable matrix that apart from being stored dry and clean do not require additional storage conditions or processing [31,[36][37][38][39]. These advantages are especially useful in wild animals and in field work when (repeated) access to birds is difficult and equipment is limited.…”

Comparison of Two Different Feather Sampling Methods to Measure Corticosterone in Wild Greater Flamingos (Phoenicopterus roseus) and Wild Mallards (Anas platyrhynchos)

“…As described in a study by Bortolotti et al and then confirmed in other studies, increased plasma CORT levels during feather growth result in elevated CORTf levels [11][12][13][14]. To determine CORTf, the feathers are sampled by plucking them from live or dead birds or even by collecting the ones dropped by molting birds [10,11,13,15]. Depending on the scientific context, the aspect of a long-term and retrospective view on the activity of the HPA axis could be a clear benefit compared to other corticosterone measurement methods.…”

Casting the Net Widely for Change in Animal Welfare: The Plight of Birds in Zoos, Ex Situ Conservation, and Conservation Fieldwork

“…A year after Burden et al’s paper [ 172 ], Zemanova [ 176 ] published a paper bringing together copious examples of available and innovative alternative methods, i.e., showing the principle of the three Rs at work, be this in genetic or behavioral studies. Zemanova demonstrated convincingly that methods are already available that are non-invasive and superior in producing reliable data [ 176 ]: For example, instead of capturing birds and taking blood samples (both highly invasive and stressful strategies for mammals and birds alike [ 177 ]), various studies have found that excrements [ 178 , 179 ] and feathers [ 180 , 181 ] can produce reliable results without subjecting the bird to invasive procedures [ 182 ]. In foxes it was demonstrated that DNA could be extracted from their footprints in the snow and, thus, did not require trapping and handling them [ 183 , 184 ].…”