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Perceived risk and obstacle avoidance in flying birds
188
Short Communications Perceived Risk and Obstacle Avoidance in Flying Birds
The aerodynamics of vertebrate flight manoeuvrability have been well studied (see reviews in Norberg & Rayner 1987; Rayner 1988), as have the perceptual limits of obstacle detection in bats (e.g. Griffin 1986). Clearly, flying animals must avoid colliding with obstacles during flight, for collisions are likely to be costly, or even fatal (e.g. Avery et al. 1978). Yet, perhaps because under natural conditions serious collisions are apparently rare, their influence on decision-making has received neither theoretical nor empirical consideration. Since the opportunity for colliding with obstacles (such as trees, other flying animals or the substrate) is a constant feature of a flying bird or bat's daily life, it seems likely that collision risks will influence behaviour. However, whilst the fitness costs of some actions may be quantified (in terms of lifetime reproductive success) or approximated (e.g. in terms of energy loss) by direct measurement, this is not true for all. Measuring costs may be particularly difficult for actions that bring an increased risk of a very rare, but nevertheless serious, danger. We argue that through natural selection rare dangers should leave their imprint on behaviour in the form of perceived risks. The quantification of perceived risks may be regarded as difficult because they are part of private experience, but subjective estimates of risk can be studied quantitatively if their effects on behaviour can be titrated against other known fitness components. Here we test the possibility that the risk of collision associated with flying close to obstacles is integrated as a 'currency component' (sensu McNamara & Houston 1986) in decisionmaking by seeing whether birds trade off this risk against foraging profitability in a graded fashion. The alternative possibility is that obstacles constrain choice of flight routes in an all-or-none fashion as, perhaps, most workers have implicitly assumed. The subjects, three male and two female wildcaught, adult starlings, Sturnus vulgaris L., were colour-ringed and kept individually in outdoor aviaries adjacent to a large testing room (3 x 4.4 • 2.5 m high). This uniformly lit room contained a raised central perch, equidistant from raised perch-operated feeders at each end (feeder design in Krebs et al. 1978). Vertical wood-framed netting barriers stood midway between each feeder and the central perch. Each barrier contained a central flight gap, from roof to floor, of precisely variable width, but was otherwise physically impenetrable. The netting ensured that the birds could see through the barriers clearly. The feeders delivered aliquots of turkey starter crumbs inde-
pendently under the control of standard logic circuits. Landing on the central perch primed both feeders. Subsequently landing on the left feeder perch delivered a single food reward at the left feeder, and inhibited the right feeder (and vice; versa). Both feeders then became disabled, requil ing the subject to fly back to the central perch to reset the system. Central perch and feeder availability was cued by lights, also operated by perch landings. The birds were trained progressively to use the set-up, were exposed to all experimental treatments in training trials, and entered testing only after showing frequent use of both feeders in trials where sides offered identical rewards (2-3 weeks training in total). Testing consisted of four 5-min trials on each of 8 consecutive days. After food deprivation, the subject was allowed access to the testing room, with trials starting on the first central perch landing. There were four experimental treatments (A, B, C, D; with all but A having a left/right asymmetry), and every bird received every treatment on every day, in a design balanced for time of day, order and side bias. Trial duration, deprivation time, gap widths, reward sizes and flight distances were decided during pilot trials with birds not used in this experiment. Relatively short flight distances (1-4 m) were chosen to ensure active flapping in the accelerating phase of flight, with no opportunity for gliding. In treatment A, both feeders delivered small rewards ()?+__sn = 22.0 __.0.7 rag), deprivation was short (30min), and the flight gaps were wide (400mm) relative to a starling's wingspan (ca. 270 mm). N o feeder preference was predicted. For treatment B, deprivation was short, both ga_pswere wide, but one feeder offered large rewards ( X + SE= 77'0+2"4mg), the other small, as in A. We predicted that subjects should prefer the high-reward feeder. Treatment C was equivalent to treatment B except that the high-reward feeder now had a narrow flight gap (250 mm). We predicted that subjects should show less preference for the highreward feeder than in treatment B. The key treatment was D, which was the same as C except that subjects now had long food deprivation (115 min). Because they were hungrier, we predicted that if birds genuinely assess and trade off the risk of collision in a graded fashion, they should now increase their preference for the high-reward side despite the heightened risk due to the narrower gap. All predictions were fulfilled (Fig. 1). In short, this experiment demonstrates that the tendency to avoid the narrow gap was inversely related to the importance of gathering food at a high rate. Because birds could easily see behind the barriers, other potential differences between narrow and
189
Short Communications 1-00
0"75
"!0"50 0.25
0.00 A
8
C
D
Treatment
Figure 1. Mean proportion of choices allocated to the high-reward side in a 5-min trial (+ upper 95% condidence limit, N= 8 days in all cases) for subjects S 1-$5. For the symmetrical treatment A, bars arbitrarily depict the proportion to the left feeder. A two-way ANOVA on arcsine-square-root-transfomled proportions reveals significant treatment (F3.14o=48.45, P<0.001), subject (F4.140=6"24, P<0.001) and interaction (F~2.a4o=l.93, P=0.036) effects. Contrasts between treatment pairs reveal highly significant differences between B and A (t = 7.17, P < 0.001), C and B (t= 10.70, P<0.001) and D and C (t = 8.94, P<0.001). See text for details of treatments. I1: SI; ~: $2; @: $3; []: $4; IS]:$5. wide gap treatments, such as the fear of a lurking predator, were eliminated, so that it is only the perceived risks associated with the gaps themselves that are likely to influence behaviour. The dangers associated with flying close to obstacles may take many forms, of which impact death will be the worst, and bone fracture, feather loss, feather damage, muscle damage, bruising and, less obviously, reduced attention to other incoming stimuli (such as an approaching predator or rival; Milinski & Heller 1978), may be others, arranged, perhaps, in a hierarchy of decreasing seriousness all ultimately driven by the need to avoid serious collision. Our results suggest that birds do not merely avoid obstacles, they continually assess the risks associated with different flight manoeuvres. Furthermore, rather than treating them as fixed constraints, these risks enter decision-making trade-offs as a currency component. Although birds occasionally brushed the barriers with their wingtips, there were no serious impacts, indicating that birds respond flexibly to assessed risks even outside the domain in which serious injury is likely. Therefore, simply measuring the incidence of injury in nature would underestimate its significance in bird biology (c.f. predation; McNamara & Houston 1987).
Our finding has clear implications both within and beyond behavioural ecology. For example, many optimality models invoke flight costs to explain adaptive decision-making. These include food patch exploitation (see Stephens & Krebs 1986), flight speed (Norberg 1981 a; Houston 1986), route choice (Norberg 1983) and fat accumulation (Norberg 1981 b; Houston 1986). Only the energetic costs of flight are considered in these models, yet we demonstrate here that flight has at least one other cost which influences behaviour, and we provide an experimental system for assessing its importance. For example, the 'cost of being fat' is invoked in several dynamic models of optimal decisionmaking (e.g. McNamara & Houston 1987): enhanced collision risk is likely to be an important component of such costs. Animals moving through physically complex environments (e.g. forests) or airways congested by unpredictably moving objects (e.g. socially foraging swallows) should incur particularly high costs. More widely, studies on the dynamics of locomotion are unlikely to give genuinely comparable data when different species respond similarly to perceived risks of collision. For example, even if different organisms are maximally efficient using the same locomotor pattern, they may still move
190
Short Communications
differently if collision carries different costs (e.g. bats versus birds versus insects). Furthermore, if collision risks can be traded off against other currency components, then differences between species in the importance of these may themselves appear as differences in the locomotor dynamics even under apparently standard conditions. This problem also applies when using locomotor changes to investigate the limits of non-visual perception, such as bat and cetacean sonar (Moore 1980; Griffin 1986). Successful obstacle avoidance is not simply a function of obstacle perception, but also the accepted collision risk which is in turn a function of hunger. Whilst this complexity may prove difficult to unravel, at the very least it is now evident that hunger level needs to be standardized, even in tests of a single species. More generally, we show that the task of quantifying the effects on fitness of rare but potentially catastrophic dangers may not be intractable if such dangers leave their imprint on behaviour in the form of perceived risks, and if these can be titrated against known and potentially measurable components of fitness such as food. Order of authorship conveys no information. For financial assistance we thank ASAB, St John's and Brasenose Colleges and the Zoology Department, Oxford. Paul Harvey, John Krebs, Marian Dawkins, Alasdair Houston, Sue Healy, Jim Bull, Andrew Read, Jeremy Rayner and anonymous referees provided valuable comments.
McNamara, J. M. & Houston, A. I. 1987. Starvation and predation as factors limiting population size. Ecology, 68, 1515-1519. Milinski, M. & Heller, R. 1978. Influence of a predator on optimal foraging behaviour of sticklebacks Gasterosteus aculeatus. Nature, Lond., 275, 642-644. Moore, P. W. B. 1980. Cetacean obstacle avoidance. In: Animal Sonar Systems (Ed. by R.-G. Busnel& J. F. Fish), pp. 97-108. New York: Plenum Press. Norberg, R. A. 1981a. Optimal flight speed in birds when feedingyoung. J. Anim. Ecol., 50, 473-477. Norberg, R. A. 1981b. Temporary weight decrease in breeding birds may result in more fledged young. Am. Nat., 118, 838-850. Norberg, R. A. 1983. Optimal locomotion modes of birds foraging in trees. Ibis, 125, 172-180. Norberg, U. M. & Rayner, J. M, V. 1987.Ecologicalmorphology and flight in bats (Mammalia; Chiroptera): wingadaptations, flightperformance, foraging strategy and echolocation. Phil. Trans R. Soc. Ser. B, 316, 335-427. Rayner, J. M. V. 1988. Form and function in avian flight. In: Current Ornithology. Vol. 5 (Ed. by R. F. Johnston), pp. 1-66. New York: Plenum Press. Stephens, D. W. & Krebs, J. R. 1986. Foraging Theory. Princeton, New Jersey: Princeton University Press.
(Received 10 May 1989; initial acceptance 18 September 1989;final acceptance 19 December 1989; MS. number: sc-536)
Male-biased Dispersal in Australian Magpies
INNESCUTHILL* TIra GULFORDt
*Department of Zoology, Br&tol University, Woodland Road, Bristol BS8 lUG, U.K. ~fDepartment o f Zoology, Oxford University, Oxford OX1 3PS, U.K.
References Avery, M, L., Springer, P. F. & Dailey, N. S. 1978.Avian mortality at man-made structures: an annotated bibliography. U.S. Dept Interior, Fish Wildl. Serv. OBS-78,
58. Griffin, D. R. 1986. Listening in the Dark. Ithaca: Cornel1 University Press. Houston, A. I. 1986.The optimal flight velocityfor a bird exploitingpatches of food. J. theor. Biol., 119, 345-362. Krebs, J. R., Kaeelnik, A. & Taylor, P. 1978. Test of optimal sampling by foraging great tits. Nature, Lond., 275, 27-31. McNamara, J. M. & Houston, A. I. 1986. The common currency for behavioral decisions. Am. Nat., 127, 358-378.
Australian magpies, Gymnorhina tibicen, are large passerines which breed in permanent territories defended by monogamous pairs or groups varying in size and composition. Within the groups, however, there is no cooperative breeding (Veltman 1989a). Most young birds disperse from their parental territories when their parents begin their next breeding effort, and form non-territorial nonbreeding flocks. After a variable period of time in the flock, they either establish a territory of their own or are recruited into an established territory. Most settle within a mile of their birthplace, giving rise to negligible dispersal distances (Carrick 1972). In this paper, we examine the timing of dispersal by Australian magpies in the light of their unusual social system. Life histories were constructed from sightings between 1953 and 1965 of birds colour-ringed as nestlings from 1953 to 1959. Birds were sexed from breeding observations or, when these were not available, from plumage sketches and measurements of retrapped individuals. Their partial life histories varied from 6 to 12 years, being the interval from the year of birth to 1965 when
Short Communications Perceived Risk and Obstacle Avoidance in Flying Birds
The aerodynamics of vertebrate flight manoeuvrability have been well studied (see reviews in Norberg & Rayner 1987; Rayner 1988), as have the perceptual limits of obstacle detection in bats (e.g. Griffin 1986). Clearly, flying animals must avoid colliding with obstacles during flight, for collisions are likely to be costly, or even fatal (e.g. Avery et al. 1978). Yet, perhaps because under natural conditions serious collisions are apparently rare, their influence on decision-making has received neither theoretical nor empirical consideration. Since the opportunity for colliding with obstacles (such as trees, other flying animals or the substrate) is a constant feature of a flying bird or bat's daily life, it seems likely that collision risks will influence behaviour. However, whilst the fitness costs of some actions may be quantified (in terms of lifetime reproductive success) or approximated (e.g. in terms of energy loss) by direct measurement, this is not true for all. Measuring costs may be particularly difficult for actions that bring an increased risk of a very rare, but nevertheless serious, danger. We argue that through natural selection rare dangers should leave their imprint on behaviour in the form of perceived risks. The quantification of perceived risks may be regarded as difficult because they are part of private experience, but subjective estimates of risk can be studied quantitatively if their effects on behaviour can be titrated against other known fitness components. Here we test the possibility that the risk of collision associated with flying close to obstacles is integrated as a 'currency component' (sensu McNamara & Houston 1986) in decisionmaking by seeing whether birds trade off this risk against foraging profitability in a graded fashion. The alternative possibility is that obstacles constrain choice of flight routes in an all-or-none fashion as, perhaps, most workers have implicitly assumed. The subjects, three male and two female wildcaught, adult starlings, Sturnus vulgaris L., were colour-ringed and kept individually in outdoor aviaries adjacent to a large testing room (3 x 4.4 • 2.5 m high). This uniformly lit room contained a raised central perch, equidistant from raised perch-operated feeders at each end (feeder design in Krebs et al. 1978). Vertical wood-framed netting barriers stood midway between each feeder and the central perch. Each barrier contained a central flight gap, from roof to floor, of precisely variable width, but was otherwise physically impenetrable. The netting ensured that the birds could see through the barriers clearly. The feeders delivered aliquots of turkey starter crumbs inde-
pendently under the control of standard logic circuits. Landing on the central perch primed both feeders. Subsequently landing on the left feeder perch delivered a single food reward at the left feeder, and inhibited the right feeder (and vice; versa). Both feeders then became disabled, requil ing the subject to fly back to the central perch to reset the system. Central perch and feeder availability was cued by lights, also operated by perch landings. The birds were trained progressively to use the set-up, were exposed to all experimental treatments in training trials, and entered testing only after showing frequent use of both feeders in trials where sides offered identical rewards (2-3 weeks training in total). Testing consisted of four 5-min trials on each of 8 consecutive days. After food deprivation, the subject was allowed access to the testing room, with trials starting on the first central perch landing. There were four experimental treatments (A, B, C, D; with all but A having a left/right asymmetry), and every bird received every treatment on every day, in a design balanced for time of day, order and side bias. Trial duration, deprivation time, gap widths, reward sizes and flight distances were decided during pilot trials with birds not used in this experiment. Relatively short flight distances (1-4 m) were chosen to ensure active flapping in the accelerating phase of flight, with no opportunity for gliding. In treatment A, both feeders delivered small rewards ()?+__sn = 22.0 __.0.7 rag), deprivation was short (30min), and the flight gaps were wide (400mm) relative to a starling's wingspan (ca. 270 mm). N o feeder preference was predicted. For treatment B, deprivation was short, both ga_pswere wide, but one feeder offered large rewards ( X + SE= 77'0+2"4mg), the other small, as in A. We predicted that subjects should prefer the high-reward feeder. Treatment C was equivalent to treatment B except that the high-reward feeder now had a narrow flight gap (250 mm). We predicted that subjects should show less preference for the highreward feeder than in treatment B. The key treatment was D, which was the same as C except that subjects now had long food deprivation (115 min). Because they were hungrier, we predicted that if birds genuinely assess and trade off the risk of collision in a graded fashion, they should now increase their preference for the high-reward side despite the heightened risk due to the narrower gap. All predictions were fulfilled (Fig. 1). In short, this experiment demonstrates that the tendency to avoid the narrow gap was inversely related to the importance of gathering food at a high rate. Because birds could easily see behind the barriers, other potential differences between narrow and
189
Short Communications 1-00
0"75
"!0"50 0.25
0.00 A
8
C
D
Treatment
Figure 1. Mean proportion of choices allocated to the high-reward side in a 5-min trial (+ upper 95% condidence limit, N= 8 days in all cases) for subjects S 1-$5. For the symmetrical treatment A, bars arbitrarily depict the proportion to the left feeder. A two-way ANOVA on arcsine-square-root-transfomled proportions reveals significant treatment (F3.14o=48.45, P<0.001), subject (F4.140=6"24, P<0.001) and interaction (F~2.a4o=l.93, P=0.036) effects. Contrasts between treatment pairs reveal highly significant differences between B and A (t = 7.17, P < 0.001), C and B (t= 10.70, P<0.001) and D and C (t = 8.94, P<0.001). See text for details of treatments. I1: SI; ~: $2; @: $3; []: $4; IS]:$5. wide gap treatments, such as the fear of a lurking predator, were eliminated, so that it is only the perceived risks associated with the gaps themselves that are likely to influence behaviour. The dangers associated with flying close to obstacles may take many forms, of which impact death will be the worst, and bone fracture, feather loss, feather damage, muscle damage, bruising and, less obviously, reduced attention to other incoming stimuli (such as an approaching predator or rival; Milinski & Heller 1978), may be others, arranged, perhaps, in a hierarchy of decreasing seriousness all ultimately driven by the need to avoid serious collision. Our results suggest that birds do not merely avoid obstacles, they continually assess the risks associated with different flight manoeuvres. Furthermore, rather than treating them as fixed constraints, these risks enter decision-making trade-offs as a currency component. Although birds occasionally brushed the barriers with their wingtips, there were no serious impacts, indicating that birds respond flexibly to assessed risks even outside the domain in which serious injury is likely. Therefore, simply measuring the incidence of injury in nature would underestimate its significance in bird biology (c.f. predation; McNamara & Houston 1987).
Our finding has clear implications both within and beyond behavioural ecology. For example, many optimality models invoke flight costs to explain adaptive decision-making. These include food patch exploitation (see Stephens & Krebs 1986), flight speed (Norberg 1981 a; Houston 1986), route choice (Norberg 1983) and fat accumulation (Norberg 1981 b; Houston 1986). Only the energetic costs of flight are considered in these models, yet we demonstrate here that flight has at least one other cost which influences behaviour, and we provide an experimental system for assessing its importance. For example, the 'cost of being fat' is invoked in several dynamic models of optimal decisionmaking (e.g. McNamara & Houston 1987): enhanced collision risk is likely to be an important component of such costs. Animals moving through physically complex environments (e.g. forests) or airways congested by unpredictably moving objects (e.g. socially foraging swallows) should incur particularly high costs. More widely, studies on the dynamics of locomotion are unlikely to give genuinely comparable data when different species respond similarly to perceived risks of collision. For example, even if different organisms are maximally efficient using the same locomotor pattern, they may still move
190
Short Communications
differently if collision carries different costs (e.g. bats versus birds versus insects). Furthermore, if collision risks can be traded off against other currency components, then differences between species in the importance of these may themselves appear as differences in the locomotor dynamics even under apparently standard conditions. This problem also applies when using locomotor changes to investigate the limits of non-visual perception, such as bat and cetacean sonar (Moore 1980; Griffin 1986). Successful obstacle avoidance is not simply a function of obstacle perception, but also the accepted collision risk which is in turn a function of hunger. Whilst this complexity may prove difficult to unravel, at the very least it is now evident that hunger level needs to be standardized, even in tests of a single species. More generally, we show that the task of quantifying the effects on fitness of rare but potentially catastrophic dangers may not be intractable if such dangers leave their imprint on behaviour in the form of perceived risks, and if these can be titrated against known and potentially measurable components of fitness such as food. Order of authorship conveys no information. For financial assistance we thank ASAB, St John's and Brasenose Colleges and the Zoology Department, Oxford. Paul Harvey, John Krebs, Marian Dawkins, Alasdair Houston, Sue Healy, Jim Bull, Andrew Read, Jeremy Rayner and anonymous referees provided valuable comments.
McNamara, J. M. & Houston, A. I. 1987. Starvation and predation as factors limiting population size. Ecology, 68, 1515-1519. Milinski, M. & Heller, R. 1978. Influence of a predator on optimal foraging behaviour of sticklebacks Gasterosteus aculeatus. Nature, Lond., 275, 642-644. Moore, P. W. B. 1980. Cetacean obstacle avoidance. In: Animal Sonar Systems (Ed. by R.-G. Busnel& J. F. Fish), pp. 97-108. New York: Plenum Press. Norberg, R. A. 1981a. Optimal flight speed in birds when feedingyoung. J. Anim. Ecol., 50, 473-477. Norberg, R. A. 1981b. Temporary weight decrease in breeding birds may result in more fledged young. Am. Nat., 118, 838-850. Norberg, R. A. 1983. Optimal locomotion modes of birds foraging in trees. Ibis, 125, 172-180. Norberg, U. M. & Rayner, J. M, V. 1987.Ecologicalmorphology and flight in bats (Mammalia; Chiroptera): wingadaptations, flightperformance, foraging strategy and echolocation. Phil. Trans R. Soc. Ser. B, 316, 335-427. Rayner, J. M. V. 1988. Form and function in avian flight. In: Current Ornithology. Vol. 5 (Ed. by R. F. Johnston), pp. 1-66. New York: Plenum Press. Stephens, D. W. & Krebs, J. R. 1986. Foraging Theory. Princeton, New Jersey: Princeton University Press.
(Received 10 May 1989; initial acceptance 18 September 1989;final acceptance 19 December 1989; MS. number: sc-536)
Male-biased Dispersal in Australian Magpies
INNESCUTHILL* TIra GULFORDt
*Department of Zoology, Br&tol University, Woodland Road, Bristol BS8 lUG, U.K. ~fDepartment o f Zoology, Oxford University, Oxford OX1 3PS, U.K.
References Avery, M, L., Springer, P. F. & Dailey, N. S. 1978.Avian mortality at man-made structures: an annotated bibliography. U.S. Dept Interior, Fish Wildl. Serv. OBS-78,
58. Griffin, D. R. 1986. Listening in the Dark. Ithaca: Cornel1 University Press. Houston, A. I. 1986.The optimal flight velocityfor a bird exploitingpatches of food. J. theor. Biol., 119, 345-362. Krebs, J. R., Kaeelnik, A. & Taylor, P. 1978. Test of optimal sampling by foraging great tits. Nature, Lond., 275, 27-31. McNamara, J. M. & Houston, A. I. 1986. The common currency for behavioral decisions. Am. Nat., 127, 358-378.
Australian magpies, Gymnorhina tibicen, are large passerines which breed in permanent territories defended by monogamous pairs or groups varying in size and composition. Within the groups, however, there is no cooperative breeding (Veltman 1989a). Most young birds disperse from their parental territories when their parents begin their next breeding effort, and form non-territorial nonbreeding flocks. After a variable period of time in the flock, they either establish a territory of their own or are recruited into an established territory. Most settle within a mile of their birthplace, giving rise to negligible dispersal distances (Carrick 1972). In this paper, we examine the timing of dispersal by Australian magpies in the light of their unusual social system. Life histories were constructed from sightings between 1953 and 1965 of birds colour-ringed as nestlings from 1953 to 1959. Birds were sexed from breeding observations or, when these were not available, from plumage sketches and measurements of retrapped individuals. Their partial life histories varied from 6 to 12 years, being the interval from the year of birth to 1965 when