Jonathan A. Green

Space Partitioning Without Territoriality in Gannets

This Is the Place Bats, bees, seals, and many seabirds practice central-place foraging, leaving a central home site, such as a hive or a rookery, to forage in a specific territory. Such species also share the challenge of competing for local resources with individuals from separate colonies. Using satellite tags, Wakefield et al. (p. 68, published online 6 June; see the Perspective by Weimerskirch) followed over 180 northern gannets to determine potential drivers of foraging territory division. Boundaries among colonial territories arose as a result of competition with individuals from other territories. Individuals from the same colony appeared to share information about foraging sites, presumably contributing to the establishment and maintenance of specific, long-term colonial territories. Gannets establish foraging territory boundaries in colonies through local competition and information exchange. [Also see Perspective by Weimerskirch] Colonial breeding is widespread among animals. Some, such as eusocial insects, may use agonistic behavior to partition available foraging habitat into mutually exclusive territories; others, such as breeding seabirds, do not. We found that northern gannets, satellite-tracked from 12 neighboring colonies, nonetheless forage in largely mutually exclusive areas and that these colony-specific home ranges are determined by density-dependent competition. This segregation may be enhanced by individual-level public information transfer, leading to cultural evolution and divergence among colonies.

Estimating energy expenditure of animals using the accelerometry technique: activity, inactivity and comparison with the heart-rate technique

SUMMARY Several methods have been used to estimate the energy expenditure of free-ranging animals. A relatively new technique uses measures of dynamic body acceleration as a calibrated proxy for energy expenditure and has proved an excellent predictor of energy expenditure in active animals. However, some animals can spend much of their time inactive and still expend energy at varying rates for a range of physiological processes. We tested the utility of dynamic body acceleration to estimate energy expenditure during a range of active (locomotion, eating) and inactive (digesting, thermoregulating) behaviours exhibited by domestic chickens. We also compared this technique with the more established heart-rate method for estimating energy expenditure. During activity, the error of estimation using body acceleration was very similar to that from the heart-rate method. Importantly, our results also showed that body acceleration can be used to estimate energy expenditure when birds are inactive. While the errors surrounding these estimates were greater than those during activity, and those made using the heart-rate method, they were less than those made using interspecific allometric equations. We highlight the importance of selecting a methodology that is appropriate for the life-history of the subject animal. We suggest that, to achieve the greatest possible accuracy and precision when estimating energy expenditure in free-ranging animals, the two techniques should be combined, and both heart rate (fH) and dynamic body acceleration could be included as covariates in predictive models. Alternatively, measures of acceleration can be used to ascertain which behaviour is being exhibited at each moment and hence which predictive model should be applied.

The heart rate method for estimating metabolic rate: review and recommendations.

Under most circumstances heart rate (f(H)) is correlated with the rate of oxygen consumption (VO(2)) and hence the rate of energy expenditure or metabolic rate (MR). For over 60 years this simple principle has underpinned the use of heart rate to estimate metabolic rate in a range of animal species and to answer questions about their physiology, behaviour and ecology. The heart rate method can be applied both quantitatively and qualitatively. The quantitative approach is a two-stage process where firstly f(H) and MR are measured simultaneously under controlled conditions and a predictive calibration relationship derived. Secondly, measurements of heart rate are made and converted to estimates of MR using the calibration relationship. The qualitative approach jumps directly to the second stage, comparing estimates of f(H) under different circumstances and drawing conclusions about MR under the assumption that a relationship exists. This review describes the range of studies which have adopted either the quantitative or qualitative approach to estimating the MR of birds, mammals and reptiles. Studies have tended to focus on species, states and questions which are hard to measure, control or define using other techniques. For example, species studied include large, wide-ranging species such as ungulates, marine predators, and domestic livestock while research questions have concerned behaviours such as flight, diving and the effects of stress. In particular, the qualitative approach has applied to circumstances and/or species where it may be hard or impossible to derive a calibration relationship for practical reasons. The calibration process itself can be complex and a number of factors such as body mass, activity state and stress levels can affect the relationship between f(H) and VO(2). I recommend that a quantitative approach be adopted wherever possible but that this may entail deriving a calibration relationship which is practical and applicable, rather than the most accurate possible. I conclude with a series of recommendations for the application and development of this method.

Accelerometry to Estimate Energy Expenditure during Activity: Best Practice with Data Loggers

Measurement of acceleration can be a proxy for energy expenditure during movement. The variable overall dynamic body acceleration (ODBA), used in recent studies, combines the dynamic elements of acceleration recorded in all three dimensions to measure acceleration and hence energy expenditure due to body movement. However, the simplicity of ODBA affords it limitations. Furthermore, while accelerometry data loggers enable measures to be stored, recording at high frequencies represents a limit to deployment periods as a result of logger memory and/or battery exhaustion. Using bantam chickens walking at different speeds in a respirometer while wearing an accelerometer logger, we investigated the best proxies for rate of oxygen consumption (V̇o2) from a range of different models using acceleration. We also investigated the effects of sampling acceleration at different frequencies. The best predictor of V̇o2 was a multiple regression including individual measures of dynamic acceleration in each of the three dimensions. However, R2 was relatively high for ODBA as well and also for certain measures of dynamic acceleration in single dimensions. The aforementioned are single variables, therefore easily derived onboard a data logger and from which a simple calibration equation can be derived. For calibrations of V̇o2 against ODBA, R2 was consistent as sampling number decreased down to 600 samples of each acceleration channel per ODBA data point, beyond which R2 tended to be considerably lower. In conclusion, data storage can be maximized when using acceleration as a proxy for V̇o2 by consideration of reductions in (1) number of axes measured and (2) sampling frequency.

Annual changes in body mass and resting metabolism in captive barnacle geese (Branta leucopsis): the importance of wing moult.

SUMMARY Many different physiological changes have been observed in wild waterfowl during the flightless stage of wing moult, including a loss of body mass. We aimed to determine whether captive barnacle geese (Branta leucopsis) would show the characteristic decrease in body mass during their wing moult, even though they had unlimited and unrestricted access to food. Fourteen captive geese were weighed at 1–2-week intervals for two complete years. During the flightless period of the moult, body mass decreased by approximately 25% from the pre-moult value. To understand the basis of this change, the rate of oxygen consumption was measured during daytime and nighttime at six points in the second year, and at three points (before, during and after wing moult) behavioural observations were made. Measurements of the rate of oxygen consumption showed an 80% increase above that of the nonmoulting periods of the year. We propose that metabolism was increased during moult because of the cost of feather synthesis. Although food was available, the captive birds chose not to forage and instead increased the proportion of time spent resting. It is likely that this behaviour in response to wing moult is a strategy to avoid predation in the wild. Thus, the innate nature of this behaviour has potential survival value for wild birds of this species. We conclude that the increase in metabolism led to the use of endogenous energy reserves because the birds reduced rather than increased their food intake rates, and as a result, the barnacle geese lost body mass during wing moult.

Energetics of diving in macaroni penguins.

SUMMARY Heart rate (fH), abdominal temperature (Tab) and diving depth were measured in thirteen free-ranging breeding female macaroni penguins. Measurement of these variables allowed estimation of the mass-specific rate of oxygen consumption (V̇O2) while diving and investigation of the physiological adjustments that might facilitate the diving behaviour observed in this species. In common with other diving birds, macaroni penguins showed significant changes in fH associated with diving, and these variables accounted for 36% of the variation in dive duration. When V̇O2 was calculated for dives of different durations, 95.3% of dives measured were within the calculated aerobic dive limit (cADL) for this species. Mean fH for all complete dive cycles was 147±6 beats min-1. When this fH is used to estimate V̇O2 of 26.2±1.4 ml min-1 kg-1 then only 92.8% of dives measured were within the cADL. Significant changes in abdominal temperature were not detected within individual dives, though the time constant of the measuring device used may not have been low enough to record these changes if they were present. Abdominal temperature did decline consistently during bouts of repeated diving of all durations and the mean decrease in Tab during a diving bout was 2.32±0.2°C. There was a linear relationship between bout duration and the magnitude of this temperature drop. There was no commensurate increase in dive duration during dive bouts as Tab declined, suggesting that macaroni penguins are diving within their physiological limits and that factors other than Tab are important in determining the duration of dives and dive bouts. Lowered Tab will in turn facilitate lower metabolic rates during diving bouts, but it was not possible in the present study to determine the importance of this energy saving and whether it is occurs actively or passively.

Fasting metabolism in Antarctic fur seal (Arctocephalus gazella) pups.

The metabolism of 52-73-day old Antarctic fur seal pups from Bird Island, South Georgia, was investigated during fasting periods of normal duration while their mothers were at sea foraging. Body mass decreased exponentially with pups losing 3.5-3.8% of body mass per day. Resting metabolic rate also decreased exponentially from 172-197 ml (O2) x min(-1) at the beginning of the fast and scaled to M(b)(0.74) at 2.3 times the level predicted for adult terrestrial mammals of similar size. While there was no significant sex difference in RMR, female pups had significantly higher (F(1,18)=6.614, P<0.019) mass-specific RMR than male pups throughout the fasting period. Fasting FMR was also significantly (t(15)=2.37, P<0.035) greater in females (823 kJ x kg(-1) x d(-1)) than males (686 kJ x kg(-1) x d(-1)). Average protein turnover during the study period was 19.3 g x d(-1) and contributed to 5.4% of total energy expenditure, indicating the adoption of a protein-sparing strategy with a reliance on primarily lipid catabolism for metabolic energy. This is supported by observed decreases in plasma BUN, U/C, glucose and triglyceride concentrations, and an increase in beta-HBA concentration, indicating that Antarctic fur seals pups adopt this strategy within 2-3 days of fasting. Mean RQ also decreased from 0.77 to 0.72 within 3 days of fasting, further supporting a rapid commencement of protein-sparing. However, RQ gradually increased thereafter to 0.77, suggesting a resumption of protein catabolism which was not substantiated by changes in plasma metabolites. Female pups had higher TBL (%) than males for any given mass, which is consistent with previous findings in this and other fur seal species, and suggests sex differences in metabolic fuel use. The observed changes in plasma metabolites and protein turnover, however, do not support this.

How many seabirds do we need to track to define home-range area?

1. In recent years, marine predator and seabird tracking studies have become ever more popular. However, they are often conducted without first considering how many individuals should be tracked and for how long they should be tracked in order to make reliable predictions of a population’s home-range area. 2. Home-range area analysis of two seabird-tracking data sets was used to define the area of active use (where birds spent 100% of their time) and the core foraging area (where birds spent 50% of their time). Analysis was conducted on the first foraging trip undertaken by the birds and then the first two, three and four foraging trips combined. Appropriate asymptotic models were applied to the data, and the calculated home-range areas were plotted as a function of an increasing number of individuals and trips included in the sample. Data were extrapolated from these models to predict the area of active use and the core foraging area of the colonies sampled. 3. Significant variability was found in the home-range area predictions made by analysis of the first foraging trip and the first four foraging trips combined. For shags, the first foraging trip predicted a 56% smaller area of active use when compared to the predictions made by combining the first four foraging trips. For kittiwakes, a 43% smaller area was predicted when comparing the first foraging trip with the four combined trips. 4. The number of individuals that would be required to predict the home range area of the colony depends greatly on the number of trips included in the analysis. This analysis predicted that 39 (confidence interval 29–73) shags and 83 (CI: 109–161) kittiwakes would be required to predict 95% of the area of active use when the first four foraging trips are included in the sample compared with 135 (CI 96–156) shags and 248 (164–484) kittiwakes when only the first trip is included in the analysis. 5. Synthesis and applications. Seabird and marine mammal tracking studies are increasingly being used to aid the designation of marine conservation zones and to predict important foraging areas. We suggest that many studies may be underestimating the size of these foraging areas and that better estimates could be made by considering both the duration and number of data logger deployments. Researchers intending to draw conclusions from tracking data should conduct a similar analysis of their data as used in this study to determine the reliability of their home-range area predictions.

Implantation reduces the negative effects of bio-logging devices on birds

SUMMARY Animal-borne logging or telemetry devices are widely used for measurements of physiological and movement data from free-living animals. For such measurements to be relevant, however, it is essential that the devices themselves do not affect the data of interest. A recent meta-analysis reported an overall negative effect of these devices on the birds that bear them, i.e. on nesting productivity, clutch size, nest initiation date, offspring quality, body condition, flying ability, foraging behaviours, energy expenditure and survival rate. Method of attachment (harness, collar, glue, anchor, implant, breast-mounted or tailmount) had no influence on the strength of these effects but anchored and implanted transmitters had the highest reported rates of device-induced mortality. Furthermore, external devices, but not internal devices, caused an increase in ‘device-induced behaviour’ (comfort behaviours such as preening, fluffing and stretching, and unrest activities including unquantifiable ‘active’ behaviours). These findings suggest that, with the exception of device-induced behaviour, external attachment is preferable to implantation. In the present study we undertake a meta-analysis of 183 estimates of device impact from 39 studies of 36 species of bird designed to explicitly compare the effects of externally attached and surgically implanted devices on a range of traits, including condition, energy expenditure and reproduction. In contrast to a previous study, we demonstrate that externally attached devices have a consistent detrimental effect (i.e. negative influences on body condition, reproduction, metabolism and survival), whereas implanted devices have no consistent effect. We also show that the magnitude of the negative effect of externally attached devices decreases with time. We therefore conclude that device implantation is preferable to external attachment, providing that the risk of mortality associated with the anaesthesia and surgery required for implantation can be mitigated. We recommend that studies employing external devices use devices that can be borne for long periods, and, wherever possible, deploy devices in advance of the time period of interest.

Do seasonal changes in metabolic rate facilitate changes in diving behaviour

SUMMARY Macaroni penguins were implanted with data loggers to record heart rate (fh), abdominal temperature (Tab) and diving depth during their pre-moult trip (summer) and winter migration. The penguins showed substantial differences in diving behaviour between the seasons. During winter, mean and maximum dive duration and dive depth were significantly greater than during summer, but the proportion of dives within the calculated aerobic dive limit (cADL) did not change. Rates of oxygen consumption were estimated from fh. As winter progressed, the rate of oxygen consumption during dive cycles (sV̇O2DC) declined significantly and mirrored the pattern of increase in maximum duration and depth. The decline in sV̇O2DC was matched by a decline in minimum rate of oxygen consumption (sV̇O2min). When sV̇O2min was subtracted from sV̇O2DC, the net cost of diving was unchanged between summer and winter. We suggest that the increased diving capacity demonstrated during the winter was facilitated by the decrease in sV̇O2min. Abdominal temperature declined during winter but this was not sufficient to explain the decline in sV̇O2min. A simple model of the interactions between sV̇O2min, thermal conductance and water temperature shows how a change in the distribution of fat stores and therefore a change in insulation and/or a difference in foraging location during winter could account for the observed reduction in sV̇O2min and hence sV̇O2DC.