- Email: [email protected]
Swallows unhandicapped by long tails?
NEWS
&
COMMENT
Swallows unhandicapped
by long tails?
cut and rejoined using a splint of tail feather) reduced the amount of time spent flyinglo.
Dawn for aerodynamics n a series of well-known tail manipulation experiments, Anders Pape Moller demonstrated female preferences for long tails in the swallow (/fir-undo rustica)iS*;the swallow is now a model species of sexual selection (Ref. 3). However, as the swallow is an aerial forager, catching flying insects by precise manoeuvres, it is very dependent on the control and stability functions of the deep-forked tai14. So, what is the function of the elongated outermost tail feathers in the swallow? Are they the outcome of sexual selection (which is the orthodox view) or do they possess an aero dynamic function? Two years ago, Adrian Thomas and co-workers applied delta-wing theory to estimate the aerodynamic costs of different types of tail elongatior@ (reported in TREE by Jennionsr). In this perspective the optimal shape of a bird tail is when the tail has triangular shape when spread and shallow forked when closed. This is because the lift generated by the tail is proportional to the maximum continuous span squared, while the drag is proportional to the area of the tails. Therefore, the area protruding beyond the maximum continuous width of the tail when spread only adds drag without generating lift. Hence, this model supports the accepted view that the outermost tail feathers in the swallow (the so-called streamers, which are elongated beyond the point of maximum continuous span) should be the outcome of sexual rather than natural selection. However, shallow-forked tails as observed in house martins (Defichon urbicu) and swifts (Apus upus) are aerodynamically optimal and probably shaped by natural selection since they give maximum lift-to-drag ratios. A detailed comparative analysis confirmed most predictions from the delta-wing approachs. However, in a new study by ,&ke Norbergs it emerges that the tail streamers in the swallow may have a novel aerodynamic function after all.
I
Aeroelastic properties Norberg took a close look at how the tail actually is used during foraging manoeuvres, by shooting high-speed motionpicture film of free-flying swallows. The way in which the tail is elevated, lowered and twisted during turning manoeuvres, and the bending of the outermost tail feathers, suggested an aerodynamic function for the streamers. During a manoeuvre, the tail is spread at approximately 120” and the whole tail is lowered, hence generating lift through a positive angle of attack relative to the incident airflow. 140
0 1995, Elsevier
Science
Ltd
Because of the positive angle of attack, the tail streamers are bent upwards, thus aligning with the airflow. This bending force on the streamer acts on a relatively long pitching moment arm; by the aeroelastic properties of the swallow tail feather, the force translates through the base of the outermost tail feather. The next step to study this mechanism was to get a swallow into a wind tunnel. A male swallow was placed in a wind tunnel with the wings folded and the angle of tail spread and angle of attack were controlled by a rake made of thin piano wire. Then tail feather bending and twisting were studied in different positions to mimic the behaviour during manoeuvring flight. Because feathers on live birds are slightly mobile in their sockets, the loaded tail streamer causes the proximal parts of the outermost tail feather to twist in the nosedown sense and rotate nose-down at its attachment (Fig. 1). Aerodynamically this creates a drooped leading edge, which in turn enhances the lift force of the tail and consequently improves manoeuvrability. The drooped outermost tail feather acts in a way similar to the Kruger flaps on the leading edges of aircraft wings, which are lowered at take-off and landing when high lift is required.
How do these new ideas on the aerodynamic function of elongated tail streamers bear on our view of the evolution of exaggerated tails in birds? Clearly, Norberg has demonstrated a novel function of the tail streamers in swallows that should be favoured by natural selection. However, he does not predict the optimal length of the protruding streamers in swallows. If we assume that streamer length in the female swallow represents the optimal design from an aerodynamic point of view, then the extra length in males (when controlling for allometry) could be the outcome of sexual selection. Alternatively, if the male represents the aerodynamic optimum, the shorter streamer length in the female could be the result of a different breeding role involving incubation and brooding. Without doubt,
Natural versus sexual selection We may draw two conclusions from Norberg’s study. First, since the tail streamers seem to have an aerodynamic function, they may have evolved through natural rather than sexual selection. Secondly, Norberg argues that the entire tail is a finely tuned co-adapted aerodynamic instrument and any experimental changes are likely to disrupt its original function. Hence, both elongation and shortening of the outermost tail feathers would lead to decreased performance. Interestingly, Mollerg found that elongated males brought back smaller insects (less profitable) to the nest than did controls, but shortened males did not do better than controls, However, new studies involving larger sample sizes revealed that male swallows (particularly those with naturally short tails) captured more profitable prey if their tails had been shorteneds. These results indicate a need for caution when manipulating aerodynamically functional structures in birds, although the treatment effects are not so obvious in the swallow as in the scarlet-tufted malachite sunbird (Nectarirza johnsoni), where even sham-manipulated control birds (birds which had their tail streamers
Fig. 1. Male swallow held in a wind tunnel to illustrate the tail feather bending, twisting and rotation under aerodynamic loads. Here the swallow is seen from obliquely behind and above (upper) and from behind and below (lower). As the streamer part of the outermost tail feather is bent upwards by the incident air flow, the consequence is a nose-down rotation of the entire feather. This drooping enhances the aero dynamic efficiency of the entire tail, especially during tight manoeuvres. Reproduced, with permission, from Ref. 8.
TREE
vol.
IO,
no.
4 April
1995
NEWS long-tailed males are preferred over shorttailed males, especially if their streamers are equally long, and they seem to enjoy a set of fitness advantage&ll. There is a negative correlation between tail length and degree of fluctuating asymmetry in swallows, and both length and low asymmetry seem to be rewarded by the females233. As already reported in TREE’*, Moller manipulated the apparent length and asymmetry of male tails using dyes, presumably without affecting the aerodynamic propertiesl3. Again, males with apparent long and symmetric tails enjoyed early and recurrent sex. In conclusion, Norberg has demonstrated a new function of a character that we believed only indicated viability. Hence, nature is a little more complicated and the life of experimentalists a little more difficult than we thought. Inevitably, aerodynamic considerations are now seriously entering
the scene of behavioural ecoIogy5+j~8.Tail form and function in birds are so variable6 and to study them all and explain their adaptive significance will occupy researchers for years. Can the sexually monomorphic deep-forked tails in terns and frigate birds be explained by Norberg’s aeroelastic mechanism? Why do females in an Australian Cisticolu species prefer short-tailed males? We are still at the beginning.
he relevance of chaos theory to population ecology is still a matter of some controversy1,2. Some believe that the irregular fluctuations characteristic of many natural populations can be attributed to chaotic motion; others suggest that these irregularities can be explained by observation error and other ‘noise’ in the system. There are analytical methods that can distinguish between these two possible explanation+‘. However, these methods are handicapped by the small number of data points and wide confidence intervals that are typical of natural population time series. Although robust new methods are being developed to counter these problems3, at present there is no data set that can show unequivocally the existence of chaos in a natural population. In tandem with tests on empirical data, the likelihood of chaotic population changes has been investigated by analysis of mathematical models designed to simulate the mechanisms behind fluctuations in populations. Early work on models of a single species with non-overlapping generations commonly predicted chaotic dynamicsg. Similarly, chaos has also been shown to be a common occurrence in models of interacting species and species with overlapping generationss. Another logical extension to this suite of models is the introduction of spatial factors. This is commonly achieved by TREE
ool.
10,
no.
4 April
1995
COMMENT
References Msller, A.P. (1988) Nature 322,640-642 Moller, A.P. (1992) Nature 357,238-240 Moller, A.P. (1994) Sexual Selection and the Born Swallour, Oxford University Press 4 Hummel, D. (1992) Z. Flugwiss. Weltraumforsch. 16,159-168 5 Thomas, A.L.R. (1993) Philos. Trans. R. Sot. 1 2 3
London
Ser. B 340,361-380
Balmford, A., Thomas, A.L.R. and Jones, I.L. (1993) Nature 361,628-631 7 Jennions, M.D. (1993) Trends Ecol. Euol. 8, 6
230-232
Acknowledgements
Norberg, R.A. (1994) PIKX.R. Sot. London Ser.
9 10
Moller, A.P. (1989) Nature 339, 132-135 Evans, M.R. and Hatchwell, B.J. (1992) Behao. Ecol. Sociobiol.
29,421-427
Smith, H.G. and Montgomerie, R. (1991) Behau. Ecol. Sociobiol. 28, 195-201 12 Brookes, M. and Pomiankowski, A. (1994) 11
Anders Hedenstriim Dept of Theoretical Ecology Building,
8
t3 257,227-233
I am grateful to Thomas Alerstam, Henrik Smith and Erik Svensson for comments on an early draft of this paper.
13
Ecoiogv, Lund Universily, S-223 62 Lund, Sweden
Temporal scales and the occurrence chaos in coupled populations
T
&
Trends Ecol. Evol. 9,201-202 Moller, A.P. (1993) Eehao. Ecol. Sociobiol.
32,
371-376
of
modelling a large system of populations with non-overlapping generations. The populations are arranged on the nodes of a square lattice. The size of the next generation of each population is determined by a function of the current population size. Traditionally, this function has been the same for all populations. Additionally, at each generation, immigration of individuals to neighbouring populations can occur, normally by simple diffusion, with a fixed fraction of each generation dispersing to each neighbouring site. Such models are termed ‘coupled map lattices’ (CMLs). Several recent papers in the ecological literature examine the predicted behaviour of CMLs of one or more specie&-‘2. These papers commonly report chaotic behaviour and spatial organization (i.e. correlation between the behaviour of sites that are close together on the lattice). Further studies have generalized these models to overlapping generations and continuous distribution of individuals in spacel3,14.These models again commonly predict chaos and spatial organization. The consensus view of this research can be summarized by the interpretation of Mercedes Pascual? ‘These results suggest that complex temporal dynamics in natural populations may arise through the spatial dimension. Spatially induced chaos may have an important role in spatial pat-
tern generation’. However, a recent paper in the physics literature, by Csilling and collaborator+, analyses a CML and observes completely the opposite behaviour. They report that the time evolution of their collective system was always ‘strictly periodic or shows a stable fixed equilib rium’. That is, the system finally settles down to a state where further iterations either cause the total population to follow a fixed sequence of values that form a finite set, or cause it to remain at one unchanging value. They were unable to find any parameter values for which the system would show chaotic behaviour. Furthermore, they report that ‘there is no sign of spatial organisation, even when the system settled down to a strictly periodic oscillatory state’. Some previous papers have reported that the ensemble dynamics of a system of chaotically varying populations can resemble a steady state with added noise. This occurs even in models, like that of Csilling et al., that are completely deterministic. However, the amplitude of the fluctuations appears always to be sufficiently high that it is unlikely that even the most casual observer would describe the signal as ‘strictly stable’ -as Csilling et al. commonly do. There can be little doubt that their model does make predictions that are greatly different from those made by a wide variety of recent papers which use similar models. The question is: why? Interestingly, the model of Csilling et al. is very similar to the CML in one of the other above-mentioned papers, by Jordi Bascompte and Richard SolC6. The two models differ in only two respects. Csilling et al. assume that immigration of a fixed
0 1995, Elsevier
Science
Ltd
141
&
COMMENT
Swallows unhandicapped
by long tails?
cut and rejoined using a splint of tail feather) reduced the amount of time spent flyinglo.
Dawn for aerodynamics n a series of well-known tail manipulation experiments, Anders Pape Moller demonstrated female preferences for long tails in the swallow (/fir-undo rustica)iS*;the swallow is now a model species of sexual selection (Ref. 3). However, as the swallow is an aerial forager, catching flying insects by precise manoeuvres, it is very dependent on the control and stability functions of the deep-forked tai14. So, what is the function of the elongated outermost tail feathers in the swallow? Are they the outcome of sexual selection (which is the orthodox view) or do they possess an aero dynamic function? Two years ago, Adrian Thomas and co-workers applied delta-wing theory to estimate the aerodynamic costs of different types of tail elongatior@ (reported in TREE by Jennionsr). In this perspective the optimal shape of a bird tail is when the tail has triangular shape when spread and shallow forked when closed. This is because the lift generated by the tail is proportional to the maximum continuous span squared, while the drag is proportional to the area of the tails. Therefore, the area protruding beyond the maximum continuous width of the tail when spread only adds drag without generating lift. Hence, this model supports the accepted view that the outermost tail feathers in the swallow (the so-called streamers, which are elongated beyond the point of maximum continuous span) should be the outcome of sexual rather than natural selection. However, shallow-forked tails as observed in house martins (Defichon urbicu) and swifts (Apus upus) are aerodynamically optimal and probably shaped by natural selection since they give maximum lift-to-drag ratios. A detailed comparative analysis confirmed most predictions from the delta-wing approachs. However, in a new study by ,&ke Norbergs it emerges that the tail streamers in the swallow may have a novel aerodynamic function after all.
I
Aeroelastic properties Norberg took a close look at how the tail actually is used during foraging manoeuvres, by shooting high-speed motionpicture film of free-flying swallows. The way in which the tail is elevated, lowered and twisted during turning manoeuvres, and the bending of the outermost tail feathers, suggested an aerodynamic function for the streamers. During a manoeuvre, the tail is spread at approximately 120” and the whole tail is lowered, hence generating lift through a positive angle of attack relative to the incident airflow. 140
0 1995, Elsevier
Science
Ltd
Because of the positive angle of attack, the tail streamers are bent upwards, thus aligning with the airflow. This bending force on the streamer acts on a relatively long pitching moment arm; by the aeroelastic properties of the swallow tail feather, the force translates through the base of the outermost tail feather. The next step to study this mechanism was to get a swallow into a wind tunnel. A male swallow was placed in a wind tunnel with the wings folded and the angle of tail spread and angle of attack were controlled by a rake made of thin piano wire. Then tail feather bending and twisting were studied in different positions to mimic the behaviour during manoeuvring flight. Because feathers on live birds are slightly mobile in their sockets, the loaded tail streamer causes the proximal parts of the outermost tail feather to twist in the nosedown sense and rotate nose-down at its attachment (Fig. 1). Aerodynamically this creates a drooped leading edge, which in turn enhances the lift force of the tail and consequently improves manoeuvrability. The drooped outermost tail feather acts in a way similar to the Kruger flaps on the leading edges of aircraft wings, which are lowered at take-off and landing when high lift is required.
How do these new ideas on the aerodynamic function of elongated tail streamers bear on our view of the evolution of exaggerated tails in birds? Clearly, Norberg has demonstrated a novel function of the tail streamers in swallows that should be favoured by natural selection. However, he does not predict the optimal length of the protruding streamers in swallows. If we assume that streamer length in the female swallow represents the optimal design from an aerodynamic point of view, then the extra length in males (when controlling for allometry) could be the outcome of sexual selection. Alternatively, if the male represents the aerodynamic optimum, the shorter streamer length in the female could be the result of a different breeding role involving incubation and brooding. Without doubt,
Natural versus sexual selection We may draw two conclusions from Norberg’s study. First, since the tail streamers seem to have an aerodynamic function, they may have evolved through natural rather than sexual selection. Secondly, Norberg argues that the entire tail is a finely tuned co-adapted aerodynamic instrument and any experimental changes are likely to disrupt its original function. Hence, both elongation and shortening of the outermost tail feathers would lead to decreased performance. Interestingly, Mollerg found that elongated males brought back smaller insects (less profitable) to the nest than did controls, but shortened males did not do better than controls, However, new studies involving larger sample sizes revealed that male swallows (particularly those with naturally short tails) captured more profitable prey if their tails had been shorteneds. These results indicate a need for caution when manipulating aerodynamically functional structures in birds, although the treatment effects are not so obvious in the swallow as in the scarlet-tufted malachite sunbird (Nectarirza johnsoni), where even sham-manipulated control birds (birds which had their tail streamers
Fig. 1. Male swallow held in a wind tunnel to illustrate the tail feather bending, twisting and rotation under aerodynamic loads. Here the swallow is seen from obliquely behind and above (upper) and from behind and below (lower). As the streamer part of the outermost tail feather is bent upwards by the incident air flow, the consequence is a nose-down rotation of the entire feather. This drooping enhances the aero dynamic efficiency of the entire tail, especially during tight manoeuvres. Reproduced, with permission, from Ref. 8.
TREE
vol.
IO,
no.
4 April
1995
NEWS long-tailed males are preferred over shorttailed males, especially if their streamers are equally long, and they seem to enjoy a set of fitness advantage&ll. There is a negative correlation between tail length and degree of fluctuating asymmetry in swallows, and both length and low asymmetry seem to be rewarded by the females233. As already reported in TREE’*, Moller manipulated the apparent length and asymmetry of male tails using dyes, presumably without affecting the aerodynamic propertiesl3. Again, males with apparent long and symmetric tails enjoyed early and recurrent sex. In conclusion, Norberg has demonstrated a new function of a character that we believed only indicated viability. Hence, nature is a little more complicated and the life of experimentalists a little more difficult than we thought. Inevitably, aerodynamic considerations are now seriously entering
the scene of behavioural ecoIogy5+j~8.Tail form and function in birds are so variable6 and to study them all and explain their adaptive significance will occupy researchers for years. Can the sexually monomorphic deep-forked tails in terns and frigate birds be explained by Norberg’s aeroelastic mechanism? Why do females in an Australian Cisticolu species prefer short-tailed males? We are still at the beginning.
he relevance of chaos theory to population ecology is still a matter of some controversy1,2. Some believe that the irregular fluctuations characteristic of many natural populations can be attributed to chaotic motion; others suggest that these irregularities can be explained by observation error and other ‘noise’ in the system. There are analytical methods that can distinguish between these two possible explanation+‘. However, these methods are handicapped by the small number of data points and wide confidence intervals that are typical of natural population time series. Although robust new methods are being developed to counter these problems3, at present there is no data set that can show unequivocally the existence of chaos in a natural population. In tandem with tests on empirical data, the likelihood of chaotic population changes has been investigated by analysis of mathematical models designed to simulate the mechanisms behind fluctuations in populations. Early work on models of a single species with non-overlapping generations commonly predicted chaotic dynamicsg. Similarly, chaos has also been shown to be a common occurrence in models of interacting species and species with overlapping generationss. Another logical extension to this suite of models is the introduction of spatial factors. This is commonly achieved by TREE
ool.
10,
no.
4 April
1995
COMMENT
References Msller, A.P. (1988) Nature 322,640-642 Moller, A.P. (1992) Nature 357,238-240 Moller, A.P. (1994) Sexual Selection and the Born Swallour, Oxford University Press 4 Hummel, D. (1992) Z. Flugwiss. Weltraumforsch. 16,159-168 5 Thomas, A.L.R. (1993) Philos. Trans. R. Sot. 1 2 3
London
Ser. B 340,361-380
Balmford, A., Thomas, A.L.R. and Jones, I.L. (1993) Nature 361,628-631 7 Jennions, M.D. (1993) Trends Ecol. Euol. 8, 6
230-232
Acknowledgements
Norberg, R.A. (1994) PIKX.R. Sot. London Ser.
9 10
Moller, A.P. (1989) Nature 339, 132-135 Evans, M.R. and Hatchwell, B.J. (1992) Behao. Ecol. Sociobiol.
29,421-427
Smith, H.G. and Montgomerie, R. (1991) Behau. Ecol. Sociobiol. 28, 195-201 12 Brookes, M. and Pomiankowski, A. (1994) 11
Anders Hedenstriim Dept of Theoretical Ecology Building,
8
t3 257,227-233
I am grateful to Thomas Alerstam, Henrik Smith and Erik Svensson for comments on an early draft of this paper.
13
Ecoiogv, Lund Universily, S-223 62 Lund, Sweden
Temporal scales and the occurrence chaos in coupled populations
T
&
Trends Ecol. Evol. 9,201-202 Moller, A.P. (1993) Eehao. Ecol. Sociobiol.
32,
371-376
of
modelling a large system of populations with non-overlapping generations. The populations are arranged on the nodes of a square lattice. The size of the next generation of each population is determined by a function of the current population size. Traditionally, this function has been the same for all populations. Additionally, at each generation, immigration of individuals to neighbouring populations can occur, normally by simple diffusion, with a fixed fraction of each generation dispersing to each neighbouring site. Such models are termed ‘coupled map lattices’ (CMLs). Several recent papers in the ecological literature examine the predicted behaviour of CMLs of one or more specie&-‘2. These papers commonly report chaotic behaviour and spatial organization (i.e. correlation between the behaviour of sites that are close together on the lattice). Further studies have generalized these models to overlapping generations and continuous distribution of individuals in spacel3,14.These models again commonly predict chaos and spatial organization. The consensus view of this research can be summarized by the interpretation of Mercedes Pascual? ‘These results suggest that complex temporal dynamics in natural populations may arise through the spatial dimension. Spatially induced chaos may have an important role in spatial pat-
tern generation’. However, a recent paper in the physics literature, by Csilling and collaborator+, analyses a CML and observes completely the opposite behaviour. They report that the time evolution of their collective system was always ‘strictly periodic or shows a stable fixed equilib rium’. That is, the system finally settles down to a state where further iterations either cause the total population to follow a fixed sequence of values that form a finite set, or cause it to remain at one unchanging value. They were unable to find any parameter values for which the system would show chaotic behaviour. Furthermore, they report that ‘there is no sign of spatial organisation, even when the system settled down to a strictly periodic oscillatory state’. Some previous papers have reported that the ensemble dynamics of a system of chaotically varying populations can resemble a steady state with added noise. This occurs even in models, like that of Csilling et al., that are completely deterministic. However, the amplitude of the fluctuations appears always to be sufficiently high that it is unlikely that even the most casual observer would describe the signal as ‘strictly stable’ -as Csilling et al. commonly do. There can be little doubt that their model does make predictions that are greatly different from those made by a wide variety of recent papers which use similar models. The question is: why? Interestingly, the model of Csilling et al. is very similar to the CML in one of the other above-mentioned papers, by Jordi Bascompte and Richard SolC6. The two models differ in only two respects. Csilling et al. assume that immigration of a fixed
0 1995, Elsevier
Science
Ltd
141