FORELIMB JOINT MOBILITY AND THE EVOLUTION OF WING-PROPELLED DIVING IN BIRDS ROBERTJ. RAIKOW? 2 LESLEYBICANOVSKY, • AND ANTHONY H. BLEDSOE •'2 1Departmentof BiologicalSciences, University of Pittsburgh,Pittsburgh, Pennsylvania 15260 USA, and 2TheCarnegie Museum of NaturalHistory, 4400 ForbesAvenue, Pittsburgh, Pennsylvania 15213 USA ABSTRACT.--Wemeasured wing joint mobility in penguins,alcids, diving-petrels, and non- diving fliers.Great reduction in mobility of the intrinsicwing jointswas found in penguins, but not in alcids or diving-petrels.This reduction is correlatedwith simplificationof the intrinsicwing musculature.In contrast,alcids and diving-petrels,which usetheir wings in both air and water, retain the full functional capacitiesfor flight. Movement through the air probably requiresa capability for subtleand varied motions,forces, and shapechanges that precludestiffening and simplificationof the wing. Hence, the conversionof an aerial wing to a flipper,as in penguins,must be possibleonly after the evolutionaryloss of flight. Received 23 September1987, accepted 2 February1988. WING-PROPELLEDdiving has evolved at least in penguins. The limb and its skeleton are flat- five times in birds: in the penguins (Sphenis- tened, and the wing is reduced in surface area cidae), auks (Alcidae), diving-petrels (Pelecan- by the lossof differentiated flight feathers,pa- oididae), the extinct Plotopteridae (Olson and tagia, and the alula. The shoulder joint and the Hasegawa 1979), and the dippers (Cinclidae; extrinsicmuscles of the wing are functionally Goodge 1959). The penguins are flightless, as specialized (Bannasch1986a, b, 1987), and the were the plotopterids,the Miocene Lucasauks limb is relatively rigid becausejoint mobility is (Mancallinae), and the recent great auks (Pin- restricted. In all, the wing is converted to a guinus).The diving-petrelsand all living alcids, "flipper" similar in external form to those of however, practice both aerial and underwater other aquatic tetrapods. locomotion. Simpson (1946: 84-92) maintained No detailed analysesof the relationship be- that living alcids and diving-petrels represent tween wing structure and the idea of compro- a stage in the evolution of flightlessnessand mise has been made for forms such as the div- wing-propelled diving through which the ing-petrels and volant alcids. Hudson et al. ancestorof penguins passed.Storer (1960) sug- (1969) describedthe wing musclesof alcidsand gestedfurther that flying auks and diving-pe- suggested(without functional explanation)that trels represent a "compromise" stage between somefeatures might be related to diving. Spring birds well adapted for locomotion in air and in (1971) describedunderwater swimming in two water. speciesof the alcid genusUria. Storer (1960:fig. Becausethe optimum design of the propul- 4) used illustrationsof wing skeletonsof a gull sire organsis differentfor the two media,which (Larus),Razorbill (Alca), Great Auk (Pinguinus), differ substantiallyin densityand buoyancy,an LucasAuk (Mancalla),and penguin (Spheniscus) intermediateadaptive stage probably would in- to represent stagesin the evolution of the ex- volve a lossof efficiencyin eachmedium as the treme aquatic specialization,showing a trend priceof adequacyin the other.Neither Simpson for increasedflattening of the bones and loss nor Storer elaborated on the anatomical corre- of the alula. Pennycuick(1987) suggestedthat latesof a "compromise"wing. If their views are auksand diving-petrelshave reduced wing areas correct, one might expect intermediate stages asadaptations for propulsion through media of to approach some of the anatomical features of greatly different densities. submarine specialists. Storer did not addressa concomitantspecial- The extreme of underwater adaptation occurs ization, the stiffening of the wing through a 446 The Auk 105:446-451. July 1988 July1988] ForelimbJoint Mobility 447 reduction in the ranges of motion of the joints. that deformation through stretchingof the tissuesdid Stiffening may prevent distortion of the wing not occur during measurement. during movement through the dense aquatic medium. That this is a problem is suggestedby RESULTS the observationthat dippersand aukskeep their wings partly folded when swimming (Goodge Jointmobility.--We obtained arcsof motion at 1959, Spring 1971). four joints for 11 volant speciesthat do not use Studies of underwater propulsion indicate their wings underwater, 2 speciesof diving- that alcidsemploy a different method from that petrels,9 of alcids,and 7 of penguins (Table 1). of penguins. In alcids the manus stays in the For all four motions the values in alcids,diving- flexed position during the propulsivestroke, in petrels, and nondiving fliers were similar and which the wing movesdown and backward in overlappedbroadly. In penguinsthe mean val- a rowing action (Spring 1971). In penguins the uesfor flexion of the forearm,manus, and major manus is extended, the wing is rotated so that digit were substantiallylower than those for the leading edge is lower than the trailing edge alcids,diving-petrels, and nondiving fliers, and in the downstroke, which entails little caudal did not overlap the values for these groups. For movement of the wing, and the upstrokeis used protraction of the humerus, the values for pen- to generatethrust as well (Clark and Bemis1979). guins overlappedthe lowest three valuesamong Thus,with regardto methodof underwater pro- the nondiving fliers and the lowestvalue of the pulsion, alcids and penguins can be considered set of alcids. The penguin average values, how- convergent only in the most general sense. ever, were lower than the values for these We attempted to determine whether species groups.Bannasch (1986a) reported a lower es- capableof both flight and wing-propelled div- timate (45ø ) for this motion but, unlike our ing show attributes of wing structure conver- method, limited the fully protractedposition to gent to those of penguins. We measured and a line perpendicular to the body axis. comparedwing-joint mobility in penguins,oth- The mean arc and 95% confidence limits of er wing-propelled divers, and nondiving fliers, the mean for flexion of the forearm, protraction and related thesefindings to differencesin the of the humerus, flexion of the manus, and flex- wing musculature. The results are discussedin ion of the major digit for each speciesare de- relationto the evolutionarytransformation from picted in Figs. 1-4. The reduction in forearm aerial to submarine propulsion. flexion of penguins differed dramatically from the other species(Fig. 1). This pattern was typ- MATERIALS AND METHODS ical of flexion of the manusand major digit as well (Figs. 3 and 4). The values for flexion of The range of motion was measuredat the shoulder,. the forearm in alcids and diving-petrels ap- elbow, wrist, and major digit of specimensthat were peared slightly larger on average than for the frozen while freshly dead and subsequentlythawed nondiving fliers (Fig. 1). The penguinsalso had in a refrigerator 2-5 days (depending on size) before a slightly reduced protraction of the humerus measurement.Each specimenwas placed on its back comparedwith the other species(Fig. 2). on a table, and the right wing was extendedflat over a sheet of paper. To measuremotion at eachjoint, the To test for these and other possible differ- proximal element was held securely in place, the po- encesin the arcsof movement, the species(Ta- sition of the joint was marked,and the distal element ble 1) were allocatedto three categories:diving was moved through the range of motion until the nonfliers (penguins), diving fliers (alcids and joint resisted further movement. These points were diving-petrels), and nondiving fliers (remain- marked, and the arc thus circumscribed was measured ing species,including Melanitta nigra, a foot- with a protractor. This was taken as an estimate of propelled diver). For eachmeasurement a group the normal arc of motion. To reduce variation in tech- mean was calculated(Table 2), and a one-way nique, one person (the senior author) moved the ele- analysis of variance was performed. For pro- ment through the range of motion while the other traction of the humerus and flexion of the ma- workersmaintained the specimenin placeand marked the positions. Replicate estimates varied, and each nus, the difference between the mean for pen- measurementwas repeated 10 times and a mean arc guins and that for each other category was of motion was calculated.Although the tissueswere statisticallysignificant (P < 0.05). For flexion of compliant,we observedno pattern of increasein the the forearm and major digit the variancesof the estimatedarc during a seriesof replicates,indicating means were heteroscedastic(Bartlett's box F test 448 R•Kow, B•c^•ovsK¾,^•D BLEDSOE [Auk, Vol. 105 T^BLE1. Range of motion in avian wing joints.a Protraction of Flexion of Flexion of Speciesno. humerus forearm Flexion of manus majordigit Spheniscidae I Aptenodytespatagonica 103 (97-106) 23 (17-34) 22 (18-26) 12 (11-15) 2 Aptenodytesforsteri 92 (88-102) 14 (13-18) 13 (10-15) 14 (12-19) 3 Pygoscelispapua 65 (57-72) 26 (20-34) 29 (24-34) 25 (20-31) 4 Pygoscelisadeliae I 100 (91-106) 25 (20-32) 25 (22-29) 17 (13-21) 5 Pygoscelisadeliae 2 27 (20-32) 23 (19-26) 19 (11-23) 6 Pygoscelisantarctica 73 (67-82) 25 (20-30) 21 (19-22) 21 (16-27) 7 Eudyptescrestatus 92 (83-106) 34 (28-37) 30 (25-35) 26 (22-30) 8 Eudypteschrysolophus 62 (57-68) 26 (22-31) 27 (24-31) 16 (14-20) Pelecanoididae 9 Pelecanoidesurinatrix 144 (120-155)