Forelimb joint mobility and the evolution of wing-propelled diving in birds

-We measured wing joint mobility in penguins, alcids, diving-petrels, and nondiving fliers. Great reduction in mobility of the intrinsic wing joints was found in penguins, but not in alcids or diving-petrels. This reduction is correlated with simplification of the intrinsic wing musculature. In contrast, alcids and diving-petrels, which use their wings in both air and water, retain the full functional capacities for flight. Movement through the air probably requires a capability for subtle and varied motions, forces, and shape changes that preclude stiffening and simplification of the wing. Hence, the conversion of an aerial wing to a flipper, as in penguins, must be possible only after the evolutionary loss of flight. Received 23 September 1987, accepted 2 February 1988. WING-PROPELLED diving has evolved at least five times in birds: in the penguins (Spheniscidae), auks (Alcidae), diving-petrels (Pelecanoididae), the extinct Plotopteridae (Olson and Hasegawa 1979), and the dippers (Cinclidae; Goodge 1959). The penguins are flightless, as were the plotopterids, the Miocene Lucas auks (Mancallinae), and the recent great auks (Pinguinus). The diving-petrels and all living alcids, however, practice both aerial and underwater locomotion. Simpson (1946: 84-92) maintained that living alcids and diving-petrels represent a stage in the evolution of flightlessness and wing-propelled diving through which the ancestor of penguins passed. Storer (1960) suggested further that flying auks and diving-petrels represent a "compromise" stage between birds well adapted for locomotion in air and in water. Because the optimum design of the propulsive organs is different for the two media, which differ substantially in density and buoyancy, an intermediate adaptive stage probably would involve a loss of efficiency in each medium as the price of adequacy in the other. Neither Simpson nor Storer elaborated on the anatomical correlates of a "compromise" wing. If their views are correct, one might expect intermediate stages to approach some of the anatomical features of submarine specialists. The extreme of underwater adaptation occurs in penguins. The limb and its skeleton are flattened, and the wing is reduced in surface area by the loss of differentiated flight feathers, patagia, and the alula. The shoulder joint and the extrinsic muscles of the wing are functionally specialized (Bannasch 1986a, b, 1987), and the limb is relatively rigid because joint mobility is restricted. In all, the wing is converted to a "flipper" similar in external form to those of other aquatic tetrapods. No detailed analyses of the relationship between wing structure and the idea of compromise has been made for forms such as the diving-petrels and volant alcids. Hudson et al. (1969) described the wing muscles of alcids and suggested (without functional explanation) that some features might be related to diving. Spring (1971) described underwater swimming in two species of the alcid genus Uria. Storer (1960: fig. 4) used illustrations of wing skeletons of a gull (Larus), Razorbill (Alca), Great Auk (Pinguinus), Lucas Auk (Mancalla), and penguin (Spheniscus) to represent stages in the evolution of the extreme aquatic specialization, showing a trend for increased flattening of the bones and loss of the alula. Pennycuick (1987) suggested that auks and diving-petrels have reduced wing areas as adaptations for propulsion through media of greatly different densities. Storer did not address a concomitant specialization, the stiffening of the wing through a 446 The Auk 105: 446-451. July 1988 This content downloaded from 157.55.39.164 on Thu, 07 Jul 2016 06:03:24 UTC All use subject to http://about.jstor.org/terms July 1988] Forelimb Joint Mobility 447 reduction in the ranges of motion of the joints. Stiffening may prevent distortion of the wing during movement through the dense aquatic medium. That this is a problem is suggested by the observation that dippers and auks keep their wings partly folded when swimming (Goodge 1959, Spring 1971). Studies of underwater propulsion indicate that alcids employ a different method from that of penguins. In alcids the manus stays in the flexed position during the propulsive stroke, in which the wing moves down and backward in a rowing action (Spring 1971). In penguins the manus is extended, the wing is rotated so that the leading edge is lower than the trailing edge in the downstroke, which entails little caudal movement of the wing, and the upstroke is used to generate thrust as well (Clark and Bemis 1979). Thus, with regard to method of underwater propulsion, alcids and penguins can be considered convergent only in the most general sense. We attempted to determine whether species capable of both flight and wing-propelled diving show attributes of wing structure convergent to those of penguins. We measured and compared wing-joint mobility in penguins, other wing-propelled divers, and nondiving fliers, and related these findings to differences in the wing musculature. The results are discussed in relation to the evolutionary transformation from aerial to submarine propulsion. MATERIALS AND METHODS The range of motion was measured at the shoulder; elbow, wrist, and major digit of specimens that were frozen while freshly dead and subsequently thawed in a refrigerator 2-5 days (depending on size) before measurement. Each specimen was placed on its back on a table, and the right wing was extended flat over a sheet of paper. To measure motion at each joint, the proximal element was held securely in place, the position of the joint was marked, and the distal element was moved through the range of motion until the joint resisted further movement. These points were marked, and the arc thus circumscribed was measured with a protractor. This was taken as an estimate of the normal arc of motion. To reduce variation in technique, one person (the senior author) moved the element through the range of motion while the other workers maintained the specimen in place and marked the positions. Replicate estimates varied, and each measurement was repeated 10 times and a mean arc of motion was calculated. Although the tissues were compliant, we observed no pattern of increase in the estimated arc during a series of replicates, indicating that deformation through stretching of the tissues did not occur during measurement.