RT26: Energetic consequences of human disturbances

Hüppop, O. & Gabrielsen, G.W. 1999. Energetic consequences of human disturbances. In: Adams, N.J. & Slotow, R.H. (eds) Proc. 22 Int. Ornithol. Congr., Durban: 3209-3210. Johannesburg: BirdLife South Africa.

Although there are a remarkable number of studies emphasising more or less severe effects of human disturbances on free-living birds (see reviews by Götmark, F. 1992. Curr. Ornithol. 9: 63-104; Keller, V. 1995. Beob. 92: 3-38; Kempf, N. & Hüppop, O. 1998 Nat. und Land.30: 17-28.) the mechanisms responsible for these effects remain uncertain in most cases. Hence, the questions how and to what extend human disturbances may affect the energy demands of birds can be answered in a very few cases only.

At least theoretically, human disturbances may have impact on energetics: (1) by increasing the energy expenditure through additional activities such as fight or flight repsonses; (2) by stress hormones acting on the intermediary metabolism; (3) by a higher muscular tension; (4) by thermoregulatory effects; or (5) by reducing the energy expenditure during ‘freezing responses’.

Most obviously, activities such as fight or flight are extremely energy consuming. Several authors compiled data on the costs of (horizontal) flight over a variety of species and these were used to estimate the energetic consequences of disturbances (e.g. Bélanger, L. & Bédard, J. 1990. J. Wildl. Mgmt. 54: 36 – 4; Yalden, D.W. 1992. Biol. Conserv. 61: 41-49; Stock, M. & Hofeditz, F. 1997. J. Ornithol. 138: 387-411). However, there are strong effects of the methods used to measure flight cost on the results. In general, estimates derived from wind tunnel measurements render higher values than measurements carried out with doubly labelled water (Flint, E.N. & Nagy, K.A. 1984. Auk 101: 288 – 294; Masman, D. & Klaassen, M. 1987. Auk 104: 603 - 616). Even worse, flight activities during fight or flight responses are everything else but horizontal flight. The energetic costs for these are virtually unknown (S. Ward pers. comm.) and urgently need further investigations. The present knowledge allows any estimate between five and over 25 times BMR for fight or flight responses. Of course, this has severe consequences for estimates of artificially induced changes of the energy consumption based on time-energy-budgets.

This raises the question of methods to measure energy consumption in free-living birds with as few investigator effects as possible. Karasov and co-workers (pers. comm.) recently have shown that both doubly labelled water and observations of food consumption are suited to estimate energetics of Bald Eagles Haliaeetus leucocephalus under different environmental conditions. Both methods may therefore be used to estimate energetic costs of human disturbances, too. Heart rates are not only useful to indicate excitement in free-living birds (e.g. Jungius, H. & Hirsch, U. 1979. J. Ornithol. 120: 299-310; Hüppop, O. & Hagen, K. 1990. Vogelwarte 35: 301-310). They can further serve as indicators of a bird’s instantaneous energy consumption during activities (Bevan, R.M., Woakes, A.J., Butler, P.J. & Croxall, J.P. 1995. Physiol. Zool. 68: 855 – 877; Hüppop, O. in press. Proc. 5th Eur. Conf. Wildl. Telem. Strasbourg (France), Aug. 1996.) and presumably as well under excitement (Hüppop unpubl. data).

A very few studies have shown that excitement per se can severely affect the energy consumption of birds and mammals, too (Hayes, J.P., Speakman, J.R. & Racey, P.A. 1992. Physiol. Zool. 65: 604 – 619; Hubert, B. & Hüppop, O. 1993. Proc. Int. Congr. Appl. Ethology, Berlin 1993: 541 - 543). Again, the mechanisms responsible are pretty speculative. ‘Stress hormones’ such as corticosterone may effect the energy consumption. The result can be, depending on the situation, both an increase or a decrease of the energy metabolism (Buttemer, W.A., Astheimer, L.B. & Wingfield, J.C. 1991. J. Comp. Physiol. B 161: 427-431.). However, the very fast response in heart rate and oxygen consumption towards excitement make neuronal mechanisms more likely at least in short-term reactions.

Despite direct hormonal effects on the energy consumption, there are manifold interactions between hormones (cathecholamins, corticosterone, endorphins) and, for example, reproduction, foraging behaviour, activity, immunosystem, muscle mobilisation, growth, and neuronal cell death. This means that human disturbance or other stress can have indirect effects on other important systems of the organism as well (Wingfield, J. 1994. In: Davey, K.G., Peter, R.E. & Tobe, S.S. (eds) Perspectives in comparative endocrinology. Nat. Res. Coun. of Canada, Ottawa: 520-528; and pers. comm.).

Besides general differences throughout the year or throughout different phases of the breeding season, birds in poorer body condition seem be even more susceptible to stress (e.g. Fowler, G.S. in press. Biol. Cons.; Hood, L.C., Boersma, P.D. & Wingfield, J.C. 1998. Auk 115: 76-84). If the adrenocortical response is influenced by artificial stress such as human disturbances this may interact with its natural response profiles that changes with the changing demands of reproduction, migration and overwintering. For example, during migration, birds can maintain elevated corticosterone levels to facilitate hyperphagia and fattening. Migrants are able to mobilise corticosterone above these already elevated levels in response to ‘emergency’ situations (Holberton, R.L., Marra, P.P. & Moore, F. 1999. Proc. 22^nd Int. Ornithol. Congr., Durban). These can be natural (e.g. storms or bad food conditions) but also might be a consequence of human disturbances. In both cases, impacts on body condition and hence on migratory behaviour, reproduction and survival are likely. Ebbinge (1989) could show that the reproductive success of Arctic geese is dependent on their body condition when leaving the wintering grounds in central Europe.

In conclusion it can be expected that, at least in some cases, human disturbances could reduce body condition and influence endocrinological regulations and hence reduce survival, fitness and reproduction. However, the knowledge about these effects of human disturbances is still pretty scarce, mainly due to methodical problems with measuring or estimating the energetic costs instantaneously in free-living birds without investigator induced stress. Nevertheless, a few case studies may give an impression on the extent of these effects.

In penguins body condition and survival to the next year was reduced by the application of wing tags (Le Maho pers. comm.). In general, the reproductive success is dependent on the energy reserves during the breeding period (Drent, R.H. & Daan, S. 1980. Ardea 68: 225-252.). This means that any reduction of the body condition should result in a reduction in the number of offspring. Indeed, Madsen (Masman, D. & Klaassen, M. 1987. Auk 104: 603 - 616.) observed that Pink-footed Geese Anser brachyrhynchos in areas with agricultural disturbances were not able to build up sufficient fat deposits prior to incubation. In these geese, only 17% of the pairs reproduced successfully compared to 46% of the pairs from undisturbed sites. Stock & Hofeditz (Stock, M. & Hofeditz, F. 1997. J. Ornithol. 138: 387-411.) investigated the impact of human disturbances on the energy budget of Brent Geese Branta bernicla during spring migration in the German Wadden Sea. Human disturbances had a severe influence on the daily metabolizable energy. Due to physiological constraints the birds reached their compensatory abilities. As a consequence, the proportion of young birds in the next autumn was lower in the more disturbed one of the two study sites. Energetic constraints on reproductive success are further confirmed by a laboratory study on Zebra Finches Taeniopygia guttata. Lemon (Lemon, W.C. 1993. Physiol. Zool. 66: 946- 963.) could substantially reduce their survival and their reproductive success by artificially increasing the energy consumption for foraging.

We are especially grateful to G. Fowler, R. Holberton, W. Karasov, Y. Le Maho, J. Wingfield and numerous other colleagues for contributing with own data and experience to this RTD and thus laying the basis for a vital and fruitful discussion.