Behavioral Ecology Vol. 10 No. 1: 112-114
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Sexual selection and tail streamers in the barn swallow: appropriate tests of the function of size-dimorphic long tails
Laboratoire d'Ecologie, CNRS URA 258, Université Pierre et Marie Curie, Bat. A, 7eme etage, 7 quai St. Bernard, Case 237, F-75252 Paris Cedex 05, France
Address correspondence to A. Barbosa, who is now at Departamento de Ecologia Evolutiva, Museo Nacional de Ciencias Naturales, Jose Gutierrez Abascal, 2, E-28006 Madrid, Spain.
Received 13 November 1997; accepted 8 May 1998.
In their recent forum paper, Thomas and Rowe
(1997)
question our tail manipulation
experiments used to test sexual selection theory
(Cuervo et al., 1996;
de Lope and Møller, 1993;
Møller, 1988,
1989,
1992b,
1994b;
Møller and de Lope, 1994;
Saino and Møller, 1996;
Saino et al., 1997a,
b). In summary, Thomas and Rowe claim
that manipulations shortening and elongating the outermost tail feathers of
barn swallows Hirundo rustica (see
Møller, 1988, for a description of
methods) are based on faulty logic and therefore cannot test the function of
long tails. Several of their statements are unclear, incorrect, or need
clarification for understanding the significance of tail manipulation
experiments, and we will discuss these statements here. Thomas and Rowe repeat
what has already been stated by Evans and Thomas
(1997). We have responded to that paper
elsewhere (Møller et al., 1998),
and here we concentrate on the aerodynamic issues.
Thomas and Rowe state that the manipulations we used (experimental
elongation or shortening of the base of the two outermost tail feathers by 20
mm, with two control groups; one sham treatment and another untreated)
do not affect the length of the tail streamer, but only affect the
aerodynamically functional part of the outermost tail feathers. Therefore,
their claim is that our experiments cannot be used to examine the role, if
any, of sexual selection in the evolution and the maintenance of the elongated
tail streamer of the barn swallow. What is the aerodynamically functional part
of the outermost feathers, and what is a tail streamer? Given that the
relationship between feather length and the so-called Norberg effect (the
aerodynamic function of tail streamers is to increase lift generated by the
tail through aeroelastic properties translated from the distal parts of the
feather, causing a rotation in their sockets;
Norberg, 1994) is unknown and might be
constant, the aerodynamically functional part of the feather can be considered
that which increases lift without increasing drag. This aerodynamically
functional part is the length equaling that of the central feather because it
provides the maximum span that determines the aerodynamical shape
(Thomas and Balmford, 1995). Feather
manipulations (where the feathers were cut and glued) were made at the level
of the proximal, aerodynamically functional part of the feather, and they
obviously increased or decreased feather length. The manipulations only
affected the outermost feathers, and without manipulating the central
feathers, the aerodynamically functional part of the feather will be the same
in all experimental groups (elongated, shortened, or control); that is,
the part of the feather less than the length of the central feathers does not
vary among treatments. The only modification made is that which affects the
relationship between the length of the non-functional part—that is, the
part of the feather beyond the maximum span, the so-called streamer, and the
length of the central feathers. The streamer does not provide lift but
increases costs, when the Norberg effect is independent of streamer length.
Therefore, manipulation of the proximal part does modify streamer length by
deplacing it forward or backward.
Female barn swallows select males based on the length of the part the
feather beyond the other feathers, but not based on the shape of the feather
(the streamer), according to the results of our experiments using basal
feather manipulations. The shape of the streamer seems to be a consequence of
the costs imposed by feather length (Møller et
al., 1995b), and it seems unrealistic that females select males on
the basis of the shape of the streamer. Elongated and shortened streamers
clearly have aerodynamical consequences, as Thomas and Rowe suggest in their
paper. On the other hand, manipulations have repeatedly been shown to affects
sexual selection in males, but not in females, as reported numerous times
(Cuervo et al., 1996;
de Lope and Møller, 1993;
Møller, 1988,
1989,
1992b,
1994b;
Møller and de Lope, 1994;
Saino and Møller, 1996;
Saino et al., 1997a,
b; Smith
and Montgomerie, 1991; Smith et
al., 1991). Therefore, the statement by Thomas and Rowe about the
inability of manipulations to examine the role of sexual selection in the
evolution and the maintenance of elongated tail streamers is misleading.
Thomas and Rowe state that manipulations should not destroy the mechanical integrity of the outermost tail feathers. However, the absence of such treatment effects has been demonstrated several times by comparing results of manipulated birds with proper control treatments.
One of the main concerns of manipulations raised by Thomas and Rowe is that
tail shortening will reduce the lift that the tail can generate because it
reduces the maximum continuous width of the tail. Tail shortening will
therefore be costly in energetic terms, affecting foraging performance and the
risk of crashing during maneuvers as predicted by aerodynamic theory
(Thomas, 1993). Their statement is based
on the assumption that the central tail feathers have the same length as the
proximal part of the outermost feathers. If that were true, shortening the
outermost feathers effectively would cause a gap between the manipulated
feather and the neighboring feather, displacing the point of maximum
continuous span backward, which would be shorter than in unmanipulated birds,
thereby causing a lift reduction. There are two questions that arise from
their statement. First, the length of the basal part of the outermost feather
seems to be rather variable. In fact, there is no relationship between the
length of the proximal part of the outermost feather and the length of the
central tail feather in males (r =.14, n = 14, p
=.63), although the relationship in females is significantly positive
(r =.58, n = 16, p =.01; samples from
Badajoz, Southern Spain). However, the more important observation is the
difference in length between these two feathers, on average being 12.85 mm
(range 2.0-20.5 mm) in males, and on average 10.50 mm (range 6.5-16.0 mm) in
females. This difference implies that the shortening treatment has effects
that differ among individuals as claimed by Thomas and Rowe. However, in some
individuals the gap does not exist, which indicates that their statement lacks
generality. A few individuals do show a gap, but in that case a second
question arises. The presence of such a gap in some individuals makes evident
the disparity between theory and empirical results. The disagreement could
arise because theory is oversimplified, or the few empirical results could be
achieved by chance. It is unlikely that theory is wrong because general
aerodynamic theory has been supported by empirical tests
(Evans and Thomas, 1992;
Pennycuick, 1968,
1971;
Tucker, 1987,
1992). On the other hand, the results
obtained by Møller and co-workers and by Smith et al. clearly support
sexual selection theory (de Lope and Møller,
1993; Møller,
1988; 1989,
1992b,
1994b;
Møller and de Lope, 1994;
Saino and Møller, 1996;
Saino et al., 1997a,
b; Smith
et al., 1991; Smith and
Montgomerie, 1991). We suggest an alternative explanation based on
the assumption that there is a negligible effect produced by the feather gap,
or even that the gap does not exist at all. Tail feathers overlap their
neighboring feathers (Norberg, 1994), and
the gap produced by the shortening manipulation could be closed by the
neighboring feather overlapping the manipulated feather. In this case the
magnitude of the shortening treatment would be the product of both
differential length between the basal outermost feather and the central
feather and the degree of overlap between outermost and second outermost
feather. In most cases the point of maximum continuous span would not change,
which implies no reduction in lift, but a reduction in drag improving flight
performance as the empirical results suggest
(Møller and de Lope, 1994;
Møller et al., 1995a;
Saino et al., 1997a). Our manipulations
might have affected the variance in morphology within treatment groups.
However, the standard errors of the different response variables measured
after manipulations did not differ between males with shortened and elongated
tails (e.g., de Lope and Møller,
1993; Møller,
1988, 1989,
1992b,
1994b;
Møller and de Lope, 1994;
Saino and Møller, 1996;
Saino et al., 1997a,
b), indicating that the few individuals
with a gap in the tail did not seriously affect the results.
Another point of interest is related to the comments on the performance of
muscles. Thomas and Rowe suggest that the neuromuscular system of the tail is
tuned to feather mass and claim that any change will impair performance. In
fact, the relation supposed by Thomas and Rowe has already been demonstrated
by Moreno and Møller (1996),
although we disagree with Thomas and Rowe's conclusion. In tail-shortened
individuals, there is a reduction in feather mass, and therefore tail muscles
would need to develop less force than before manipulation, lowering the
energetic costs of tail movements. The magnitude of the force developed by the
muscle is similar to the magnitude of drag produced by the bird, and feather
mass is three orders of magnitude lower than that of the bird. However, the
relationship between feather mass and length of the feather affects the lever
arm of tail muscles. A reduction in the lever arm reduces the force needed,
which therefore increases muscle efficiency. Moreover, mass affects the moment
of inertia of the tail, which could affect muscular force as well.
We agree with the effects of tail elongation suggested by Thomas and Rowe.
Tail elongation will increase feather mass. In barn swallows we calculated
that a change in mass caused by elongation affected the moment of inertia of
the tail by almost 35% (Barbosa et al., unpublished manuscript), with a
resultant decrease in foraging ability (Møller
et al., 1995a).
One of the more important points in the criticism by Thomas and Rowe is
based on Norberg's findings. Norberg
(1994) suggested that streamers in the
barn swallow could increase lift generated by the tail through aeroelastic
properties translated from the distal parts of the feather, causing a rotation
in their sockets, which would deflect the leading edge. However, there are at
least three pieces of evidence that raise questions about the relationship
between the mechanism described by Norberg
(1994) and streamer length.
First, why are there morphological differences in streamer length between
males and females? If natural selection is responsible for the evolution
of long streamers, and if the Norberg effect is related to streamer length, it
would be expected that individuals with the highest flight costs due to their
morphology (body mass and wingspan) will have the longest streamers to reduce
such costs and improve flight. In eight populations of barn swallows we
studied, females had larger calculated flight costs (using the software in
Pennycuick, 1989), at the most frequent
foraging speed (11 m/s), than males as predicted from aerodynamic theory
(Barbosa et al., unpublished manuscript). However, in all these populations,
fork depth of females remained constant at the optimal shape, independent of
flight costs (Barbosa and Møller, unpublished manuscript), as expected
if the Norberg effect was unrelated to streamer length. Moreover, in males,
fork depth increased latitudinally from southern to northern Europe
(Møller, 1995;
Møller et al., 1995b), while high
ambient temperature, which renders capture of insects more difficult,
decreased from south to north (Møller et al.,
1995a). If long tails improve flight through the Norberg effect,
fork depth would be expected to decrease from south to north, which is clearly
not the case.
Thomas and Rowe suggest that differences in reproductive roles explain
morphological differences between sexes, and we would thus expect that
individuals with long tails (males) to carry out most offspring provisioning,
if long streamers improve flight performance. On the contrary, long-tailed
males (both naturally or manipulated) provide less provisioning than
short-tailed males, with the lack of male parental care being compensated by
females (de Lope and Møller,
1993; Møller,
1992a, 1994a).
Vulnerability to damage of streamers in the nest while incubating, as
suggested by Thomas and Rowe, seems to be a factor of no relevance, as most
incubating females keep their streamers outside the nest, as males do in the
North American subspecies with male incubation (Barbosa and Møller,
personal observations). Comparison of tail length of American and European
male barn swallows does not support the damage hypothesis either because at
least males from Southern Spain and North Africa have tails of the same length
as American males, and males in Southern Spain do not incubate
(Møller, 1994a;
Smith and Montgomerie, 1992).
Furthermore, we would expect a cline in the role of incubation from north to
south if incubation depended on morphology. Such a cline does not exist.
The second question related to the Norberg effect and streamer length is
why most species of hirundines do not have long streamers? In a
comparative study of the evolution of tail morphology in hirundines, using the
phylogenetic information of Sheldon and Winkler
(1993), we have found that long streamers
are only present in 3 of 20 species, although most have a shallow, forked tail
(Barbosa and Møller, unpublished data). If long streamers improved
flight performance, we would expect such morphology to be widely distributed
among most aerial foragers such as hirundines. However, the most common
morphology is a shallow, forked tail, as expected if the Norberg effect was
unrelated to streamer length. In fact, Norberg
(1994) assumed that even without
streamers, it was possible to achieve a similar effect to improve flight.
The third question arises from the suggestions made by Norberg
(1994) and Evans and Thomas
(1997) about the aerodynamic properties of
the tail as a co-adapted deflecting mechanism. Most of these hypothetical
relations among feather traits, such as feather shaft, curvature, and flexion
stiffness, remain to be tested. However, we have tested the relationship
between streamer length and basal feather length. Our results show that there
is no relationship between these feather traits in either sex in five
different populations of barn swallows (Barbosa and Møller, unpublished
data). These results suggest that the deflecting leading edge mechanism is not
determined by the relation between basal feather length and streamer
length.
As we did not find any relation between streamer length and basal feather
length, the Norberg mechanism cannot be tested by basal manipulations or by
streamer manipulations. However, as we have discussed above, it is likely that
the mechanism proposed by Norberg (1994)
is unrelated to streamer length, being present even in very short outermost
feathers such as those of females. Therefore, in all manipulations the Norberg
effect would be acting to a similar degree. Thus both basal and streamer
manipulations would have the same consequences; shortening would reduce
drag and increase performance, and elongation would add drag and decrease
performance. Effects on moment of inertia of the tail would also be similar.
The only difference between manipulations would be in the magnitude of the
changes, but not their direction (Barbosa and Møller, unpublished
data).
Thomas and Rowe are contradictory in their statement that elongations are always costly and that only the shortening treatment can test the three possible functions of streamers. First, this would not be the case if the Norberg mechanism were related to streamer length and if this trait were under directional selection. But supposing that streamer length is under stabilizing selection and the Norberg effect is related to streamer length, the statement made by Thomas and Rowe is incorrect. They conclude that elongations are always costly whatever the mechanism of evolution generating long tails in males. However, this is only true if elongation is done in individuals with tails longer than the optimum under natural selection, but if we manipulate individuals with shorter tails, elongation will be beneficial if natural selection is acting. This implies that the direction of the change in costs will depend on tail length with respect to the optimal morphology. Under a model of sexual selection, the direction of the change in costs will always have the same directionality, with elongation effectively always being costly from an aerodynamic point of view, and shortening always improving flight. This fact is important as we have repeatedly obtained such results suggesting a role of sexual selection in several experiments (see references above). If natural selection were responsible for the evolution of tail streamers, it is likely that our results would be less clear.
In conclusion, we maintain that the manipulation experiments we carried out can very well test the functional significance of long streamers in barn swallows, in particular with respect to sexual selection. All the results obtained at the moment indicate that sexual selection is the mechanism responsible for the maintenance of longer tails in male than in female barn swallows, and they support the handicap theory for the evolution of secondary sexual characters.
ACKNOWLEDGEMENTS
A.B. was supported by a Marie Curie post-doctoral grant from the European Union and A.P.M. was supported by grants from the Swedish and Danish Natural Science Research Councils.
REFERENCES
Cuervo JJ, de Lope F, Møller AP, 1996. The
function of long tails in female barn swallows (Hirundo
rustica): an experimental study. Behav Ecol
7:132-136.
de Lope F, Møller AP, 1993. Female reproductive effort depends on the degree of ornamentation of their mates.Evolution 47:1152-1160.[Web of Science]
Evans MR, Thomas ALR, 1992. The aerodynamic and mechanical consequences of elongated tails in the scarlet tufted malachite sunbird: measuring the cost of a handicap. Anim Behav 43:337-347.
Evans MR, Thomas ALR, 1997. Testing the functional
significance of tail streamers. Proc R Soc Lond B
264:211-217.
Møller AP, 1988. Female choice selects for male sexual tail ornaments in the monogamous swallow. Nature 332:640-642.
Møller AP, 1989. Viability costs of male tail ornaments in a swallow. Nature 339:132-135.
Møller AP, 1992a. Sexual selection in the monogamous swallow (Hirundo rustica). II. Mechanisms of intersexual selection. J Evol Biol 5:603-624.[Web of Science]
Møller AP, 1992b. Female swallow preference for symmetrical male sexual ornaments. Nature 357:238-240.[Medline]
Møller AP, 1994a. Sexual selection and the barn swallow. Oxford: Oxford University Press.
Møller AP, 1994b. Symmetrical male sexual
ornaments, paternal care, and offspring quality. Behav Ecol
5:188-194.
Møller AP, 1995. Sexual selection in the barn swallow (Hirundo rustica). V. Geographic variation in ornament size.J Evol Biol 8:3-19.
Møller AP, Barbosa A, Cuervo JJ, de Lope F, Merino S, Saino
N, 1998. Sexual selection and tail streamers in the barn swallow.Proc R Soc Lond B
265:409-414.
Møller AP, de Lope F. 1994 Differential costs of a secondary sexual character: an experimental test of the handicap principle. Evolution 48:1676-1683.[Web of Science]
Møller AP, de Lope F, Lopez Caballero JM,1995a . Foraging costs of a tail ornament: experimental evidence from two populations of barn swallows Hirundo rustica with different degrees of sexual size dimorphism. Behav Ecol Sociobiol 37:289-295.[Web of Science]
Møller AP, de Lope F, Saino N, 1995b. Sexual selection in the barn swallow Hirundo rustica. VI. Aerodynamic adaptations. J Evol Biol 8:671-687.
Moreno E, Møller AP, 1996. Morphological aspects of avian tail movements: a functional approach in hirundines.Auk 113:647-654.[Web of Science]
Norberg R
, 1994.
Swallow tail streamer is a mechanical device for self-deflection of tail
leading edge, enhancing aerodynamic efficiency and flight manoeuvrability.Proc R Soc Lond B
257:227-233.
Pennycuick CJ, 1968. A wind-tunnel study of gliding
flight in the pigeon Columba livia. J Exp Biol
49:509-526.
Pennycuick CJ, 1971. Control of gliding angle in
Ruppell's griffon vulture Gyps rueppellii. J Exp Biol
55:39-46.
Pennycuick CJ, 1989. Bird flight performance. Oxford: Oxford University Press.
Saino N, Møller AP, 1996. Sexual ornamentation
and immunocompetence in the barn swallow. Behav Ecol
7:227-232.
Saino N, Bolzern AM, Møller AP, 1997a.
Immunocompetence, ornamentation and viability of male barn swallows
(Hirundo rustica). Proc Natl Acad Sci USA
94:549-552.
Saino N, Primmer CR, Ellegren H, Møller AP,1997b . An experimental study of paternity and tail ornamentation in the barn swallow (Hirundo rustica). Evolution 51:562-570.[Web of Science]
Sheldon FH, Winkler DW, 1993. Intergeneric relationships of swallows estimated by DNA-DNA hybridization.Auk 110:798-824.[Web of Science]
Smith HG, Montgomerie R, 1991. Sexual selection and the tail ornaments of North American barn swallows. Behav Ecol Sociobiol 28:195-201.[Web of Science]
Smith HG, Montgomerie R, 1992. Male incubation in barn swallows: the influence of nest temperature and sexual selection.Condor 94:750 -759.[Web of Science]
Smith HG, Montgomerie R, Poldmaa T, White BN, Boag PT,1991
. DNA fingerprinting reveals relation between tail ornaments
and cuckoldry in barn swallows, Hirundo rustica. Behav
Ecol
2:90-98.
Thomas ALR, 1993. On the aerodynamics of birds' tails.Phil Trans R Soc Lond B 340:361-380.
Thomas ALR, Balmford A, 1995. How natural selection shapes birds's tails. Am Nat 146:848-868.[Web of Science]
Thomas ALR, Rowe L, 1997. Experimental tests on tail
elongation and sexual selection in swallows (Hirundo rustica) do not
affect the tail streamer and cannot test its function. Behav
Ecol
8:580-581.
Tucker VA, 1987. Gliding birds: the effect of
variable wing span. J Exp Biol
133:33-58.
Tucker VA, 1992. Pitching equilibrium, wing span and
tail span in a gliding Harris' hawk, Parabuteo unicinctus. J
Exp Biol
165:21-43.
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