Application of the two-sample doubly labelled water method alters behaviour and affects estimates of energy expenditure in black-legged kittiwakes

Abstract

SUMMARYDespite the widespread use of the doubly labelled water (DLW) method in energetic studies of free-ranging animals, effects of the method on study animals are rarely assessed. We studied behavioural effects of two alternative DLW protocols. During two consecutive breeding seasons, 42 parent black-legged kittiwakes received either the commonly used two-sample (TS) or the less invasive single-sample (SS) DLW treatment. A third group served as a non-treated control. We evaluated the effect of treatment with respect to the time birds took to return to their nest after treatment and recaptures, and the nest attendance during DLW measurement periods. We found that TS kittiwakes took on average 20 times longer to return to their nest than SS kittiwakes after initial treatment, and nest attendance was reduced by about 40% relative to control birds. In contrast, nest attendance did not differ between control and SS kittiwakes. Estimates of energy expenditure of SS kittiwakes exceeded those of TS kittiwakes by 15%. This difference was probably caused by TS birds remaining inactive for extended time periods while at sea. Our results demonstrate that the common assumption that the TS DLW method has little impact on the behaviour of study subjects is in some circumstances fallacious. Estimates of energy expenditure derived by the SS approach may thus more accurately reflect unbiased rates of energy expenditure. However, the choice of protocol may be a trade-off between their impact on behaviour, and hence accuracy, and their differences in precision. Adopting procedures that minimize the impact of TS protocols may be useful.

Counting calories in cormorants: dynamic body acceleration predicts daily energy expenditure measured in pelagic cormorants

“…Given that extensive restraint alters birds' behaviour, and consequently daily energy expenditure (Schultner et al, 2010;Hinsley et al, 2011), we attempted a modified two-sample technique. To reduce disturbance and associated possibility of abandonment with a costly accelerometer attached, we injected the DLW intravenously and our second sample was taken only 12 min after injection to reduce the impact of extended restraint on behaviour.…”

“…Daily energy expenditure has seldom been reported in the order Suliformes (Shaffer, 2011; referred to there as 'Pelecaniformes' from which Suliformes has recently been split), only once in cormorants (Keller and Visser, 1999), and never in a small cormorant species, presumably because many cormorants are very sensitive to disturbance. The two-sample DLW method requires holding large animals for over an hour, and that lengthy period of restraint can cause abandonment of offspring or altered behaviour (Schultner et al, 2010;Hinsley et al, 2011). Obtaining direct estimations of daily energy expenditure would be useful for validating estimates from bioenergetic models used to quantify the impact of cormorants on fisheries (Ridgway, 2010).…”

Effects of the doubly labelled water procedure on Great TitsParus majorfeeding young

“…The practical difficulties (and costs) of the use of DLW in free-living animals has undoubtedly contributed to problems with small sample sizes, and hence low statistical power, in assessments of behavioural effects (Zurowski & Brigham 1994, Wilson & Culik 1995. The recent study by Schultner et al (2010) was designed to address these problems and showed an effect of the two-sample procedure on both behaviour and estimates of energy expenditure in Black-legged Kittiwakes. The authors suggested that the initial period of restraint required for equilibration by this method may have been a major factor, acting through stress and/or by increasing time required for plumage maintenance.…”

“…Whatever the mechanism, an effect of stress seems likely in that Schultner et al (2010) found stronger negative effects in a year of unfavourable foraging conditions; thus the Kittiwakes may have had less tolerance to the stress imposed by the procedure during a year when environmental stress was already high. Experience from our work with both Great Tits and Blue Tits using a two-sample DLW method concurs with this.…”

“…There have been relatively few attempts to test this assumption in the field and most studies have found little or no effect (Obst & Nagy 1992, Uttley et al 1994, Zurowski & Brigham 1994, Wilson & Culik 1995, review in Speakman 1997. However, in a recent comprehensive study of Black-legged Kittiwakes Rissa tridactyla (Schultner et al 2010), the time taken to return to the nest increased (20 times) and nest attendance decreased (40%) in experimental birds compared with controls following the initial procedures of the two-sample method (i.e. capture, injection, equilibration period, © 2011 British Trust for Ornithology, Bird Study, 58, 151-159 blood sampling, release).…”