J. Avian Biol. 38: 536 540, 2007 doi: 10.1111/j.2007.0908-8857.04253.x # 2007 The Authors. J. Compilation # 2007 J. Avian Biol. Received 24 April 2007, accepted 14 July 2007
Twofold seasonal variation in the supposedly constant, species-specific, ratio of upstroke to downstroke flight muscles in red knots Calidris canutus Theunis Piersma and Maurine W. Dietz T. Piersma (correspondence) and M.W. Dietz, Animal Ecology Group, Centre for Ecological and Evolutionary Studies, University of Groningen, P.O. Box 14, 9750 AA Haren, The Netherlands; and Department of Marine Ecology and Evolution, Royal Netherlands Institute for Sea Research (NIOZ), P.O. Box 59, 1790 AB Den Burg, Texel, The Netherlands. E-mail:
[email protected]
We show that in a long-distance migrant shorebird species with outspoken seasonal changes in body mass and composition, the red knot Calidris canutus , the ratio between the masses of the small flight muscle (musculus supracoracoideus , powering twists and active upstrokes of the wings) and the larger flight muscle (musculus pectoralis , for the downstrokes) is far from constant. During an annual cycle the supracoracoideus /pectoralis ratio varied more than twofold between values of 0.058 (90.005 SE) in early winter period and of 0.124 (90.01 SE) on the High Arctic tundra breeding grounds. The ratios thus spanned a range from those typical of soaring raptors and seabirds to those of fast and agile fliers and birds with rapid take-offs. The overall average ratio was 0.102 (90.001 SE, for non-starved knots, and 0.10390.001 SE including starved knots) and did not differ between males and females. As predicted from the known functions of supracoracoideus and pectoralis , the ratio was a negative function of body mass. However, after arrival on the breeding grounds (0.124) and during winter starvation (0.135) particularly high ratios were reached: these may be times when wing-manoeuvrability (in flight display and during the evasive ‘rodent run’ away from predators at the nest) and an ability for rapid takeoff and active up-strokes (from near the nest, and in times of depletion of flight muscle mass during winter starvation) may be at premium. The particularly low ratio of 0.06 in early winter is puzzling. Many aspects of avian phenotypes have recently been shown to be intraindividually variable. To a twofold seasonal variation in flight muscle mass (Dietz et al. 2007), we can now add the twofold variation in the ratio between the muscles for the upstroke and the downstroke.
In birds, but not bats, the muscles responsible for the combined down- and upstrokes of the wings are both attached to the sternum (Sy 1936, Norberg 1990, Proctor and Lynch 1993, Videler 2005). There is no doubt that the relatively large flight muscle, the musculus pectoralis, powers the downstroke (e.g. Dial et al. 1988). Clarifying the function of the smaller flight muscle, the musculus supracoracoideus, situated in the fold of the keel and the base of the sternum and surrounded by the pectoralis, has been more difficult. It powers the rapid twisting of the upper arm (humerus ) at the end of the upstroke to reposition the wing for the subsequent downstroke (Poore et al. 1997a,b), and it may power the upstrokes, particularly during low flight speeds and rapid take-offs (Rayner 1988, Warrick and
536
Dial 1998). That the supracoracoideus can act its opposite forces from the same position as the pectoralis, is due to a pulley system by which a long tendon from the supracoracoideus along the coracoid bone and through the ‘trisosseal canal’ is attached on the dorsal side of the humerus , right across the ventral location where the tendon from the pectoralis is attached (Poore et al. 1997a). Depending on flight style, the ratios between the mass of the supracoracoideus and the pectoralis vary between taxa (e.g. Greenewalt 1962, Lack 1973, Rayner 1988, Norberg 1990). Perhaps unintentionally, supracoracoideus /pectoralis ratios (henceforth called s/p ratios) have been portrayed as species-specific constants. For example, in hummingbirds (Trochilidae),
so wonderfully specialised in making stationary hovering flights during which considerable aerodynamic power is generated during both down- and upstroke (Warrick et al. 2005), the supracoracoideus may weigh up to half as much as the pectoralis. In underwater fliers and relatively large ground-living species like tinamous (Tinamidae), grouse (Tetraonidae) and pheasants (Phasianidae) that make steep take-off flights to escape predators, the supracoracoideus weighs as much as one third to one fourth of the pectoralis (Rayner 1988). In agile fliers like swifts (Apodidae), the supracoracoideus measures one fifth of the pectoralis , in fast-forward fliers such as shorebirds one-ninth or one-tenth, and in soaring raptors, storks and seabirds one-twentieth. Given the close correspondence between flight style, skeletal and external morphology and muscular features between species, it may not be surprising that, to the best of our knowledge, no author has examined intraspecific variation in s/p ratios. However, in view of the rather different functions of the two flight muscles, such variations would perhaps be expected in species and individuals that find themselves in a variety of ecological, including aerodynamic, contexts over space and time. Long-distance migrant shorebirds with stark seasonal changes in body mass and composition and ecological conditions such as red knots Calidris canutus (see Piersma and Davidson 1992, Piersma et al. 2005) would be interesting candidate species. Red knots show considerable seasonal and context-specific intraindividual variation in flight muscle size (Piersma 1998, Dietz et al. 1999, 2007, Lindstro¨m et al. 2000). When we examined their s/p ratios, these ratios appeared to be far from constant, but to vary more than twofold in the course of a year. Apart from reporting our findings, we here present and entertain various explanatory correlates of these seasonal s/p ratio variations that may help us understand this intriguing new axis of phenotypic variation.
Material and methods Body composition data from freshly dead, free-living adult knots were accumulated between 1981 and 2002 (dataset overlaps with that used by Dietz and Piersma 2007, Dietz et al. 2007). Most of the dissected specimens were victims of lighthouses and poachers or died during capture (Battley and Piersma 2005); some were collected on purpose (Iceland, Piersma et al. 1999, Delaware Bay, Baker et al. 2004, Arctic Canada, Morrison et al. 2005), and there were victims of winter starvation incidents (for the latter, see Dietz and Piersma 2007). Birds of the islandica subspecies (n 152) were available for much of the annual cycle, but for some of the other subspecies, samples for limited
periods were available (C. c. rufa : n 98; C. c. canutus: n 11; C. c. piersmai : n 3; C. c. rogersi : n 10). The birds were dissected following the procedures described in Piersma et al. (1999), and Battley and Piersma (2005). Briefly, after the skin was removed, the two pectoral muscles, musculus pectoralis and musculus supracoracoideus were excised of both sides of the sternum. To avoid any biases due to variable dehydration of the two sets of muscles (e.g. Piersma and van Brederode 1990), we here use the dry mass values to calculate s/p ratios. To obtain these, the muscles were dried to constant mass at 608 C. Sex was determined by visual inspection of the gonads in most red knots.
Results The distinct seasonal variation in body mass in the islandica and rufa subspecies (Fig. 1A) is reflected by similar changes in flight muscle mass (Fig. 1B), except for starved birds that had catabolized much of their flight muscle when they die. However, the masses of supracoracoideus and pectoralis did not vary in parallel. Winter-starved islandica knots had a much higher s/p ratio (0.13590.01 SE) than birds in good condition, which at that time had s/p ratios close to the overall average of 0.102 (90.001 SE, subspecies combined; Fig. 1C). Similar values were found in other subspecies (Fig. 1D, E and F). No sexual differences in the s/p ratios in islandica and rufa knots were apparent (Student t -test, subspecies combined, t259 0.573, P 0.567, excluding starved knots, males 0.1039 0.016, n 131; and females 0.10190.018, n 130). Nevertheless, in islandica knots (no data for rufa ; Fig. 1C) particularly low s/p ratios occurred during wing moult (0.07690.004, n 12, August-September) and in early winter (0.05890.005, n 4, October-December). A particularly high s/p ratio (0.12490.005, n 11) was found after arrival on the breeding grounds. Indeed, the variation over time was significant in islandica (ANOVA with time category as fixed factor: time category significant, F9,142 17.5, P B0.01, n 152; R2 0.526), but not in the more restricted time series in rufa (F5,92 1.1, P 0.386, n 97). Consistent with a published allometric interspecific comparison (Rayner 1988), the s/p ratio was a clear negative function of body mass (Fig. 2). For the islandica samples, an analysis of covariance with time category as a fixed factor and body mass as a covariate, the effect of body mass was F10,141 3.7, P 0.056, n 152 (note that the analysis initially included a nonsignificant interaction term between time and the covariate). The s/p ratio was more strongly negatively correlated with overall dry flight muscle mass than with body mass (final model for islandica including time category and dry flight muscle mass, non-significant
537
Body mass (g)
220
A
D
B
E
C
F
180 140 100
Dry flight muscle mass (g)
60 12 10 8 6 4 2 0 0.18 0.16 S/p ratio
0.14
10
0.10 0.08 0.06
1
11
0.12 17 51
21
12
19
19
8
17 11
12 12
11
14
2
10
12 4
(1) W
inte r Ja n-A pril Net herl and s& Arg (3) F enti (4) u na e Arri l l e r s Ap val (5) May ril B Ear rasil Icel ly fu and elle &D rs M (6) L e a la y Ic ate war elan fuel e d& lers (7) Del May Pre awa Icel dep re and artu &D re M (8) A elaw ay I rriva cela are l on nd & bree Del ding a w grou are (9) nds Mig Jun (10) ratio e nS W in Aler outh gm t oult July (11) Aug I c elan -Se Ear d pt W ly w inte add r Oc en S t-De ea cW add (1) W en S ea inte r Ja n-A pril Mau ritan (2) L ia & ate NW fuel Aus lers tralia Mar ch N (3) e Fue w Z llers eala nd Apr il NW Aus trali a
0.04
Fig. 1. Seasonal variation in (A, D) body mass and (B, E) associated changes in the total flight muscle mass, and (C, F) the ratio between supracoracoideus and pectoralis mass in red knots of the islandica and rufa , and the other subspecies. Time categories are numbered in chronological order. A, B and C: islandica black circles; rufa gray triangles down; islandica winter starved open circles. D, E and F: canutus black squares; piersmai gray triangles up; rogersi white diamonds. Dotted lines indicate ranges around the means (connecting minimum and maximum values). N-values are indicated in bottom panel, but apply to all panels, and to Fig. 2.
538
0.14 8 1
0.12
1 1
5
9
All subspecies
2
3
7
S/p ratio
6 4 3
0.10
1
4
7 6
1 5
0.08
islandica only 10
0.06 11
0.04 80
100
120
140 160 180 Body mass (g)
200
220
Fig. 2. The supracoracoideus /pectoralis ratio (averages with SE) as a function of body mass (mb ) for all subspecies per time category as defined in Fig. 1. The solid line represents the linear regression for islandica only: s/p ratio 0.12626 (90.00818 SE) 0.00018 (90.00005 SE) mb , n 152, R2 0.067, PB0.01. The dotted line represents the linear regression for all subspecies combined: s/p ratio 0.12358 (90.00500 SE) 0.00014 (90.00003 SE) mb, n 273, R2 0.061, PB0.001. Subspecies and time categories (here indicated by numbers adjacent to the symbols) follow Fig. 1. N-values as indicated in Fig. 1C and F.
interaction term, F10,141 20.3, P B0.01, n 152, R2 0.601).
Discussion It is increasingly clear that many aspects of an animal’s phenotype including morphology, in birds as well as in other species, are variable in seasonal and other ecological contexts (e.g. Piersma and Lindstro¨m 1997, Piersma and Drent 2003, van den Hout et al. 2006, van Gils et al. 2006). This phenotypic flexibility is interesting, because it gives us a direct way to look at environment-design matching, unhindered by the complications of genetic constraints. How to interpret the strong seasonal variation in s/p ratios? If all the work necessary to maintain level flight at any speed would come from the pectoralis, pectoralis mass would be expected to increase with body mass as predicted from power requirements (see Dietz et al. 2007), but the mass of the supracoracoideus should vary less, if at all. On this basis one predicts the s/p ratio to be a negative function of body mass (and of total flight muscle mass), and this is precisely what we found. After arrival on their high Arctic breeding grounds, red knots engage in song flights during which birds (probably males only) rise to a height of several 10s to several 100s of m, often in ever decreasing circles with rapid wing beats, followed by a shallow glide with wings held horizontally or slightly upraised (Whitfield and
Brade 1991). The height lost in the glide is regained by a flight with rapidly quivering wing beats in a shallow arc, and a song flight is completed by a plunge to the ground with upraised wings. It is unclear whether a relatively large supracoracoideus is necessary to accomplish these song flights, although the absence of a difference between the sexes during this time (t9 0.148, P 0.885; males 0.12590.018, n 6; and females 0.12390.017, n 5) suggests that it isn’t. Still, any context that requires a rapid flapping and pronation and supination (‘turning’) of the wings would be expected to place high demands on the supracoracoideus (Poore et al. 1997a,b). As this seems to be the case of the aerial displays of red knots, we suggest that s/p ratios represent a trait that would be moulded by sexual selection. Only a little later, both sexes of knots attend the nest and when a nest is approached by predators such as Arctic foxes Alopex lagopus or ermines Mustela erminea, the birds first secretively leave it but then try to lurk the predators away from the nest with the so-called ‘rodent run’, during which the birds run low with rapidly flapping wings that may well call both flight muscles into action. If the predators go after the parent bird, ability for rapid take-off will be at premium. High ratios are also reached during winter starvation (0.135), a situation when, even relative to body mass, the flight muscle mass is depleted (Dietz and Piersma 2007). At such times a relatively large supracoracoideus may help speed up any take-offs when starving birds are faced with surprise attacks. The low s/p ratios during wing moult and in early winter, and the subsequent doubling of the ratio toward the average values between the first and the second half of the winter period are puzzling. Would the low s/p ratio during wing moult occur because gaps in the wing make slow flight and rapid take-offs from the ground (see Rayner 1988) impossible anyway? The doubling of the s/p ratio in midwinter does not seem to correlate with temporal variation in the likelihood of encountering aerial predators such as peregrines Falco peregrinus (Bijlsma et al. 2001). Descriptive work on s/p ratio variation in other birds is now called for to establish whether the striking variation in red knots, and the seasonal pattern of this variation is more common, and which factors such variation is correlated with. Such analyses, and dedicated experimental wind tunnel studies on flight performance during periods with low and high s/p ratios, could further help interpretations of this striking case of variability in a morphological trait that was supposed to be an invariant characteristic of a species. Acknowledgements This analysis was inspired by rereading the writings of David Lack on (the flight of) swifts (Lack 1973). We thank Anne Dekinga, Phil Battley, Guy Morrison,
539
Nick Davidson and many others who helped carrying out red knot dissections in the past, and Anne Dekinga and Anders Hedenstro¨m for discussing interpretations. We benefited from helpful expert criticisms made by Andrew Biewener and two anonymous reviewers.
References Baker, A. J., Gonza´lez, P. M., Piersma, T., Niles, L. J., de Lima Serrano do Nascimento, I., Atkinson, P. W., Clark, N. A., Minton, C. D. T., Peck, M. K. and Aarts, G. 2004. Rapid population decline in red knots: fitness consequences of decreased refuelling rates and late arrival in Delaware Bay. Proc. R. Soc. B 271: 875 882. Battley, P. F. and Piersma, T. 2005. Adaptive interplay between feeding ecology and features of the digestive tract in birds. In: Starck, J. M. and Wang, T. (eds). Physiological and ecological adaptations to feeding in vertebrates. Science Publications, Enfield, New Hampshire, pp. 201 228. Bijlsma, R. G., Hustings, F. and Camphuysen, C. J. 2001. Algemene en schaarse vogels van Nederland (Avifauna van Nederland 2). GMB Uitgeverij/KNNV Uitgeverij, Haarlem/Utrecht. Dial, K. P., Kaplan, S. R., Goslow, G. E., Jr and Jenkins, F. A., Jr. 1988. A functional analysis of the primary upstroke and downstroke muscles in the domestic pigeon (Columba livia ) during flight. J. Exp. Biol. 134: 1 16. Dietz, M. W. and Piersma, T. 2007. Red knots give up escape flight capacity but defend digestive capacity during winter starvation. Funct. Ecol. 21: in press. Dietz, M. W., Piersma, T. and Dekinga, A. 1999. Bodybuilding without power training: endogenously regulated muscle hypertrophy in confined shorebirds. J. Exp. Biol. 202: 2831 2837. Dietz, M. W., Piersma, T., Hedenstro¨m, A. and Brugge, M. 2007. Intraspecific variation in avian pectoral muscle mass: constraints on maintaining maneouvrability with increasing body mass. Funct. Ecol. 21: 317 326. Greenewalt, C. H. 1962. Dimensional relationships for flying animals. Smithsonian Misc. Coll. 144: 1 46. Lack, D. 1973. Swifts in a tower. Chapman & Hall, London. Lindstro¨m, A˚., Kvist, A., Piersma, T., Dekinga, A. and Dietz, M. W. 2000. Avian pectoral muscle size rapidly tracks body mass changes during flight, fasting and fuelling. J. Exp. Biol. 203: 913 919. Morrison, R. I. G., Davidson, N. C. and Piersma, T. 2005. Transformations at high latitudes: why do red knots bring body stores to the breeding grounds? Condor 107: 449 457. Norberg, U. M. 1990. Vertebrate flight. Springer, Berlin. Piersma, T. 1998. Phenotypic flexibility during migration: optimization of organ size contingent on the risks and rewards of fuelling and flight? J. Avian Biol. 29: 511 520.
540
Piersma, T. and Davidson, N. C. 1992. The migrations and annual cycles of five subspecies of knots in perspective. Wader Study Group Bull. 64, Suppl.: 187 197. Piersma, T. and Drent, J. 2003. Phenotypic flexibility and the evolution of organismal design. Trends Ecol. Evol. 18: 228 233. Piersma, T. and Lindstro¨m, A˚. 1997. Rapid reversible changes in organ size as a component of adaptive behaviour. Trends Ecol. Evol. 12: 134 138. Piersma, T. and van Brederode, N. E. 1990. The estimation of fat reserves in coastal waders before their departure from northwest Africa in spring. Ardea 78: 221 236. Piersma, T., Gudmundsson, G. A. and Lilliendahl, K. 1999. Rapid changes in the size of different functional organ and muscle groups during refuelling in a long-distance migrating shorebird. Physiol. Biochem. Zool. 72: 405 415. Piersma, T., Rogers, D. I., Gonza´lez, P. M., Zwarts, L., de Lima Serrano do Nascimento, I., Minton, C. D. T. and Baker, A. J. 2005. Fuel storage rates before northward flights in red knots worldwide. Facing the severest ecological constraints in tropical intertidal environments? In: Greenberg, R. and Marra, P. P. (eds). Birds of two worlds: Ecology and evolution of migration. Johns Hopkins Univ. Press, Baltimore, pp. 262 273. Poore, S. O., Ashcroft, A., Sa´nchez-Haiman, A. and Goslow, G. E., Jr. 1997a. The contractile properties of the M. supracoracoideus in the pigeon and the starling: a case for long-axis rotation of the humerus. J. Exp. Biol. 200: 2987 3002. Poore, S. O., Sa´nchez-Haiman, A. and Goslow, G. E., Jr. 1997b. Wing upstroke and the evolution of flapping flight. Nature 387: 799 802. Proctor, N. S. and Lynch, P. J. 1993. Manual of ornithology. Avian structure and function. Yale Univ. Press, New Haven. Rayner, J. M. V. 1988. Form and function in avian flight. Curr. Ornithol. 5: 1 66. Sy, M. 1936. Funktionell-anatomische Untersuchungen am Vogelflu¨gel. J. Ornithol. 84: 253 267. van Gils, J. A., Piersma, T., Dekinga, A. and Battley, P. F. 2006. Modelling phenotypic flexibility: an optimality analysis of gizzard size in red knots (Calidris canutus ). Ardea 94: 409 420. van den Hout, P. J., Piersma, T., Dekinga, A., Lubbe, S. K. and Visser, G. H. 2006. Ruddy turnstones rapidly build pectoral muscle after raptor scares. J. Avian Biol. 37: 425 430. Videler, J. J. 2005. Avian flight. Oxford Univ. Press, Oxford. Warrick, D. R. and Dial, K. P. 1998. Kinematic, aerodynamic and anatomical mechanisms in the slow, maneuvering flight of pigeons. J. Exp. Biol. 201: 655 672. Warrick, D. R., Tobalske, B. W. and Powers, D. R. 2005. Aerodynamics of the hovering hummingbird. Nature 435: 1094 1097. Whitfield, D. P and Brade, J. J. 1991. The breeding behaviour of the knot Calidris canutus . Ibis 133: 246 255.
