Coping with continuous human disturbance in the wild: insights from penguin heart rate response to various stressors

Abstract

BackgroundA central question for ecologists is the extent to which anthropogenic disturbances (e.g. tourism) might impact wildlife and affect the systems under study. From a research perspective, identifying the effects of human disturbance caused by research-related activities is crucial in order to understand and account for potential biases and derive appropriate conclusions from the data.ResultsHere, we document a case of biological adjustment to chronic human disturbance in a colonial seabird, the king penguin (Aptenodytes patagonicus), breeding on remote and protected islands of the Southern ocean. Using heart rate (HR) as a measure of the stress response, we show that, in a colony with areas exposed to the continuous presence of humans (including scientists) for over 50 years, penguins have adjusted to human disturbance and habituated to certain, but not all, types of stressors. When compared to birds breeding in relatively undisturbed areas, birds in areas of high chronic human disturbance were found to exhibit attenuated HR responses to acute anthropogenic stressors of low-intensity (i.e. sounds or human approaches) to which they had been subjected intensely over the years. However, such attenuation was not apparent for high-intensity stressors (i.e. captures for scientific research) which only a few individuals experience each year.ConclusionsHabituation to anthropogenic sounds/approaches could be an adaptation to deal with chronic innocuous stressors, and beneficial from a research perspective. Alternately, whether penguins have actually habituated to anthropogenic disturbances over time or whether human presence has driven the directional selection of human-tolerant phenotypes, remains an open question with profound ecological and conservation implications, and emphasizes the need for more knowledge on the effects of human disturbance on long-term studied populations.

Modulation of heart rate responses to acute stressors throughout the breeding season in a colonial seabird, the king penguin

“…The models including those variables explained substantial and similar amounts of variation in the HR response to stressors. Consistent with previous results, HR excess was also affected by the specific nature (intensity/risk) of acute disturbances (Viblanc et al, 2012) (see similar findings in other bird species; Wascher et al, 2011, including penguins;Giese, 1998;Holmes et al, 2005;Ellenberg et al, 2006Ellenberg et al, , 2013, but the decrease in HR excess with advancement of breeding was not stressor dependent. Stress responses may vary according to the energy demands of various reproductive stages.…”

“…The starting model included all two-way interactions between independent variables. Colony area and stressor order were entered as a covariates in the model to control for area related differences in stress responses (see Viblanc et al, 2012) and potential habituation or sensitization effects. Bird identity was specified as a random factor.…”

“…Heart rate (HR) has been shown to increase with increased sympathetic input , and can be used to investigate the fine tuning of 'fight-or-flight' responses to acute stressors of various nature. For instance, we recently found that the HR response of colonial king penguins (Aptenodytes patagonicus) to acute experimental stressors increases with stressor intensity (Viblanc et al, 2012). Similarly, several studies have documented stimuli-dependent modulations of HR responses to stress in other species Tarlow and Blumstein, 2007;Wascher et al, 2011), including other penguins (Giese, 1998;Holmes et al, 2005;Ellenberg et al, 2006Ellenberg et al, , 2013.…”

“…The data collected on brooding birds in 2011 (see Viblanc et al, 2012) was supplemented with additional data collected on both incubating and brooding birds during the 2009-2010 breeding season. Three different stressors were applied to the birds (see below).…”

“…We used the same experimental stress protocols as previously described by Viblanc et al (2012). Penguins were submitted to (1) a distant (10 m) pedestrian approach; (2) a capture; or (3) a sound stress.…”