flipper development in the mediterranean striped dolphin (stenella coeruleoalba)

THE ANATOMICAL RECORD 2451708-714 (1996)

Flipper Development in the Mediterranean Striped Dolphin . .

(Stenella coeruleoalba) NURIA CALZADA AND ALEX AGUILAR

University of Barcelona, Faculty of Biology, Department of Animal Biology (Vertebrates), Barcelona, Spain

ABSTRACT Background: Studies of population biology are scarce in Mediterranean striped dolphins (Stenella coeruleoalba) mostly because of the lack of samples. Until now, studies of physical maturity, growth, and development of the flipper bones were not available for this species in the Mediterranean.

Methods: The osteological features and metric characters of the pectoral limbs of Mediterranean striped dolpins were analyzed with radiological techniques. Measurements were made directly on the radiographic films.

Results and Conclusions: We found five carpal bones arranged in a proximal row of three and a distal row of two, although one or two additional osseous elements were occasionally observed. The phalangeal formula (excluding metacarpals) was established as 1-28-9-106-5-7:3-2:l-2. In metacarpals, epiphyseal ossification centers matured at the same time at both ends. As a general rule, the ossification of the epiphyses in the flipper bones showed a decreasing gradient in the proximodistal direction, confirming the pattern previously described in other species. Phalangeal epiphyses were not useful as indicators of skeletal maturity, and grading epiphyseal maturation of the distal radius and ulna is proposed as the more straight- forward and precise method for assessing bone maturation. In females, maturity of the flipper was achieved between 5 and 6 years of age and 160-175 cm of body length, whereas this maturation occurred between 8 and 9 years of age and 170-181 cm in length in males. Prediction of gender through examination of flipper structure was not feasible. 0 1996 Wiley-Liss, Inc.

Key words: Mediterranean striped dolphin, Skeletal maturation, Epiphy- seal ossification, Pectoral limb

The striped dolphin Stenella coeruleoalba is the most common cetacean in the Mediterranean Sea (Viale, 1985; Duguy et al., 1988). It is gregarious and inhabits pelagic waters. Females attain sexual maturity at about 187 cm and 12 years of age, whereas males do so at about 187 cm and 9 years of age (Calzada et al., in press). Until a morbillivirus epizootic affected the Med- iterranean striped dolphin (Aguilar and Raga, 1993), few samples were available to allow reliable studies on its population biology. To date, neither physical maturity nor variability in structure, growth, or development of the flipper has been investigated in this population. In contrast, the striped dolphins off the coast of Japan has been thoroughly studied, and their population biology is largely known. In particular, studies on flipper structure and development based on radiographs have been carried out by Ito and Miyazaki (1 990).

Radiographic technology is a useful tool for the study of skeletons. It is a noninvasive technique and can be used efficiently in dead and live specimens. This technique can be used to document and assess osteological

0 1996 WILEY-LISS, INC.

variation within and between cetacean populations. Moreover, measures of the osseous elements may be obtained from successive stages of development of the skeletons as seen in radiographs and used throughout the growth period to assess bone age. In addition, bones often survive the process of decay in stranded dolphins and provide the main evidence for the study of species after the death of the individual.

Because few studies of skeletal aging are available in marine mammals, this paper describes the osteological features and metric characteristics of the flipper of the striped dolphin based on radiographic techniques. Moreover, this paper considers the different stages of maturation of the secondary (epiphyeal) ossification centers in the different osseous elements, thus corre- lating the degree of maturation with the body length and chronologic age of the specimens. Intraspecific

Received July 25, 1995; accepted January 25, 1996. Address reprint requests to Nuria Calzada, Department of Animal

Biology (Vertebrates), Faculty of Biology, University of Barcelona, Diagonal 645, 08028 Barcelona, Spain.

FLIPPER DEVELOPMENT IN STRIPED DOLPHIN 709

Fig. 1. Metric characters and skeletal elements of the pectoral limb. FL, flipper length; HL, humeral length; HD, humeral diameter; RL, radial length; RD, radial diameter; UL, ulnar length; UD, ulnar di-

variability in bone components and the difference between males and females are also examined.

MATERIAL AND METHODS Most of the specimens used for the present study

come from animals that died during the 1990 striped dolphin morbillivirus epizootic in the Mediterranean Sea, although additional specimens from the same area found stranded in previous years were also examined. A total of 98 striped dolphins (54 males and 44 females) of various ages were studied, including five fetuses from 81 to 99 cm long. Body length was measured to the nearest centimeter in a straight line from the tip of the snout to the notch between the flukes. Age was determined by counting growth layer groups in decal- cified and stained longitudinal sections of tooth dentine (Myrick et al., 1983; Calzada et al., 1994).

To study the bone structure, the right flipper was detached from the glenohumeral joint in each specimen and stored frozen. Bilateral asymmetry has not been found in this species (Ito and Miyazaki, 1990). Radio- graphs were made with an X-ray machine capable of 100 kVp, 30 mA, and variable time by using Kodak 100 X-ray film. Flippers were placed directly on the film cassette to avoid magnification and radiographed at 55 KVP and 250 mAs; the time of exposure was 12 sec. These standards were established by trial and error and maintained throughout the study.

ameter; BL, braquial length; DL, length of the second digit; r, radiale; i, intermedium; u, ulnare; c, capitatum (c3); un, unciform (c4+c5) (terms taken from Eales, 1954).

To describe the proportions of the skeletal elements of the flipper, measurements of different metric characters were taken with a slicing caliper to the nearest millimeter directly on the radiographic films. Mea- sures taken in this study (Fig. l) were length and mid- shaft transversal diameter of the humerus radius and ulna, braquial (humerus + radius) length, length of the flipper, and length of the second digit. With the quoted measurements, the following proportions were estimated: humeroradial or braquial ratio, radial length to the length of the second digit, humeral length to its transversal diameter, radial length to its transversal diameter, and body length to flipper length. Sta- tistical comparisons between males and females were performed with t-tests in all the variables except for the ratio between humeral and radial length to transversal diameter, variables that were observed to depart from normality; in these two cases, a Kruskal-Wallis test was performed. Because each measurement varied throughout development and growth, only specimens with complete epiphyseal closure were included in the analysis of metrical variation. Moreover, carpal, metacarpal, and phalangeal bones were counted to study variation in number of ossification centers according to age, sex, and body length.

The development of the epiphyses and their fusion to the diaphyses on the different bones was graded according to Ogden et al. (1981), whose rating scheme is as

710 N. CALZADA AND A. AGUILAR

follows: stage 0 = no secondary ossification center present; stage 1 = the secondary ossification center is present but occupies less than 50% of the width of the adjacent bone, stage 2 = the secondary ossification center occupies 50-100% of the adjacent bone, stage 3 = the distance between the epiphysis and the metaphysis of bone begins to diminish, stage 4 = physis (epiphyseal or growth plate) begins to close, stage 5 = physis is completely closed and a radiodense physeal line traverses the width of the bone, stage 6 = remodeling of the physeal region, essentially consisting in replacement of the physeal line by mature bone tissue, occurs at this stage; as a consequence, less than 50% to no evidence of the physeal line remains.

RESULTS Congenital abnormalities were not found in the dol-

phins examined. None of the bones of the flipper presented marrow cavity, and all bones were totally filled with spongy material, a characteristic, as discussed by Felts and Spurrell (19651, that is considered to be an adaptation to aquatic habitats (Fig. 2). Tables 1 and 2 detail the indices and measurements of the different bone components. Fetuses had a body 1engtWflipper length ratio between 5.2 and 5.7, and neonates had ratios of 5.8 to 6.5, suggesting initial rapid growth of the flipper during the fetal stage that becomes propor- tionally smaller in neonates. During the postnatal stage, the correlation between flipper length and body length, by using the least squares method, was high, and the relation between both lengths was linear, indicating that flippers grow at the same rate as body length (r = 0.90, y = 0.114 x + 5.7 for males and r = 0.95, y = 0.118 x + 5.4 for females). The mean length of the flippers in mature dolphins was 28 cm, and no significant differences were found between males and females (t = 1.32, P > 0.05). Moreover, the ratio between body length and flipper length was 6.9 in males and 6.8 in females, a difference that proved to be significant (t = 2.16, P < 0.05). However, the difference could be due to sexual dimorphism in relation to body length because differences between sexes in the length of the flipper were not found. Moreover, the ratio between the braquial length and the length of the second digit (the longest) was 0.47 for males and 0.45 for females; this difference was statistically significant (t = 3.25, P < 0.05).

Humerus The humerus is short and compact, with no marrow

cavity. It is almost twice as long as it is wide, and the ratio between its length and transversal diameter reached 1.9. Humeral length at birth ranges from 3 to 3.3 cm and increases rapidly until it reaches an adult length of around 5.5 cm by 6 years of age (Fig. 3). In all specimens including fetuses, the proximal epiphysis of the humerus was found at an advanced stage of development, reaching epiphyseodesis in the fetal stage. Nevertheless, this portion of the humerus was difficult to visualize and not always possible to assess in every individual because of the different orientation versus the rest of the osseous structures of the flipper. In the distal humerus, according to the classification scheme described earlier, the grading in fetuses was between stage 3 and stage 4, whereas neonates presented stage

4. Complete fusion (stage 5) and remodeling of the metaphysis (stage 6) was reached rapidly between 1 and 2 years of age.

Radius and Ulna The ratio of radius length to that of the humerus

(humeroradial ratio) was 1.3 (SD = *0.06), indicating that, in this species, as in other delphinids (Benke, 19931, the radius is longer than the humerus. Radius and ulna were located in the same plane and were not fused to one another, although in older animals, as seen radiographically, the radius, the ulna, or both may be fused with the humerus. In these cases, measurements of the bones were not taken. The radius, located at the frontal edge of the flipper, is longer than the ulna. Its length at birth ranged between 4.2 and 5.8 cm, rapidly increasing until it reached an average adult length of 7 cm (SD = k0.37) (Fig. 3) and a radial lengthhadial diameter ratio of 2.4 (SD 5.43). At birth, the ulna measured between 3.9 and 5 em; its mean length in adults was 6.2 cm (SD = 50.35). T tests failed to show significant differences between males and females for any of these lengths.

Proximal and distal radioulnar epiphyseal ossification centers fused quite simultaneously. Therefore, data for age and length of physiological epiphyseodesis were the same for both bones. Moreover, proximal radioulnar closure occurred at a rate similar to that of the distal humerus. Proximal secondary ossification centers in fetuses and neonates were found at an advanced stage of development, particularly in stage 3. Their fusion to the metaphysis began during the second year, and physiological epiphyseodesis was completed by the third. In relation to the maturation of the distal epiphysis, substantial variability was found in neonates. Thus, although some animals were born with cartilag- inous epiphysis (stage 01, most were at stage 2. Physi- ological epiphyseodesis a t the distal ends was achieved earlier in females than in males (Table 3). Thus, physical maturity, stage 5, was reached in females between 5 and 6 years of age and at body lengths between 160 and 175 cm. In males, stage 5 was achieved between 8 and 9 years of age and at lengths of 170-181 cm (Fig. 4).

Carpals All the ossification centers of the carpal bones were

already present in fetuses. In general, each bone had only one ossification center. The number of carpals was usually five with a proximal row of three and a distal row of two. This disposition remained the same until adulthood, and the only variation was an increase in size of the bones. The most constant and largest elements of the carpus were arranged in the following way: the proximal row consisted of one radiale (sca- phoid), which was the smallest bone; one intermedium (lunar), which was the largest; and one ulnare (cunei- form); the distal row was composed by the third carpal (capitatum), and the fourth and fifth carpals fused to form the unciform (Eales, 1954; Rommel, 1990). How- ever, in about 20% of specimens, additional bones were found so that the carpus consisted of six or seven bones. Occasionally, the proximal row presented a separate bone on the ulnar side, which could be the accessory carpal (pisiform) or a secondary ossification center of

FLIPPER DEVELOPMENT IN STRIPED DOLPHIN 711

Fig. 2. Radiographs of flippers of two Mediterranean striped dolpins showing the amedullary bones. The process of epiphyseal ossification can be observed in the different bone components. A Distal radioulnar epiphyses are still open (stage 3), indicating this 4-year-old fe-

male was not physically mature. B Twenty-five-year-old physically mature male. Stage 6 can be observed in the secondary ossification centers of all bones.

TABLE 1. Mean lengths (cm) and standard deviations of bone components in physically mature specimens

Bone Males (n) Females (n)

could be the second carpal, which may be absent, or the first carpal, which fuses to metacarpal I in early development (Eales, 1954).

Flipper 28.0 (21.25) (39) 28.3 (kO.91) (33)

Radius 7.05 (k0.456) (32) 7.02 (k0.280) (23)

Humerus + radius 2.15 (20.665) (38) 12.17 (k0.530) (33)

Humerus 5.39 (20.302) (32) 5.38 (k0.237) (23)

Ulna 6.24 (20.390) (29) 6.17 (20.306) (22)

Digit I1 14.97 (k0.852) (38) 15.50 (k0.664) (33)

the ulnare because it was sometimes fused to this bone in older animals. In two specimens, a small bone was found between the intermedium and the radiale; which may be the centrale carpal. In the distal row, variability was limited to the radial side in which one bone of varying size was found between the radiale and the first metacarpalia, sometimes fusing to it. This bone

Metacarpals and Phalanges There are five metacarpals, and each one supports a

digit. MII, MIII, and MIV were relatively long and cy- lindrical; MI was rounded in neonates and young specimens, becoming triangular in adult specimens. MV was round. The second and third digits exhibited hy- perphalangism, thus giving an elongated form to the flipper. Metacarpals and phalanges had two epiphyseal ossification centers except for the most distal epiphysis of the phalanges, where secondary centers were always absent.

In the fetuses available in the sample, the primary ossification centers in all metacarpals were present except for the smallest specimen, 81 cm long, in which MI

712 N. CALZADA AND A. AGUILAR

TABLE 2. Mean indices and standard deviations of bone components in physically mature specimens

Index Males (n) Females (n) Body 1ength:flipper length 6.99 (20.344) (37) 6.83 (t0.259) (30) Radius 1ength:humerus length 1.31 (k0.068) (31) 1.30 (t0.052) (23) Braquial 1ength:length of digit I1 0.449 (t0.024) (23) Humeral 1ength:humeral width 1.96 (k0.196) (29) 1.99 (20.211) (23) Radial 1ength:radial width 2.42 (20.434) (29) 2.45 (e0.424) (23)

0.470 (t0.023) (32)

Ulna

4 i i q , , , , , , , , , , , , , , Radius , , ,

0 2 4 6 8 10121416182022242630323436

Age (years)

Fig. 3. Size increase of the humerus, ulna, and radius in relation to age.

was still absent. Phalanges of digits I and V were only present in the two largest fetuses (94 and 99 cm). In older specimens, secondary ossification centers in distal and proximal epiphysis of MI1 and MI11 and in the proximal one of MIV follow the same rate of maturation as the distal radius, although the union of the proximal epiphysis appeared to proceed slightly more rapidly than the proximal epiphysis.

Phalanges can be rectangular to round, depending on the stage of development of the animal and the position of the phalanx. In general, the shape in mature specimens was rectangular, similar to that of the metacarpals, and became progressively smaller toward the distal end of a digit, where the phalanges were round. Regarding phalangeal count, digit I had no phalanges, or one phalange which may be already ossified at birth. Occasionally, two ossified phalanges could be found in adult individuals. The first phalanx sometimes fused to MI and, on some occasions, fusion between the two phalanges was also seen. Digit I1 had six, seven, or, most often, eight phalanges at birth. Adult specimens usually had eight, but sometimes nine or 10 phalanges. Digit I11 had five or six phalanges at birth, and adults may have seven. Digit IV had two and rarely three phalanges at birth, and adults usually had three and

TABLE 3. Age (years) and length (cm) at physiological epiphyosedesis of the radioulnar distal eDiDhvses

Age and length Males Females

Oldest age at physical maturity 9 6 Shortest length at physical maturity 170 160 Longest lendh at Dhvsical maturitv 181 175

Youngest age at physical maturity 8 5

d 3- Ij 4l 2 / m 1 - I Females O L - 1 I I 1 - 1 , I "

0 2 4 6 8 101214 16 182022242628303234

Age (years)

Fig. 4. Status of radioulnar epiphysis in relation to age.

ocassionally two. At birth, digit V had no ossified phalanges; in older animals, there is only one #phalanx and rarely two or none. Clearly, there was large variability in the number of phalangeal bones so that an overall picture of maturation and order to appearance was difficult to ascertain from all the possible combinations. However, the phalangeal formula for the Mediterra- nean striped dolphin (excluding metacarpals) can be established as 1-2%-9-10:6-5-7:3-2:l-2.

In the flipper, phalangeal epiphyses are the last to

FLIPPER DEVELOPMENT I N STRIPED DOLPHIN

TABLE 4. Epiphyseal fusion of the different bone components

713

Epiphssis Beginning Active Fused Proximal humerus Fetus Fetus Fetus Distal humerus Fetus Fetus to neonate 1 year Proximal radius and ulna Fetus Fetus to neonate Neonates to 1 year Distal radius and ulna 2-3 vears 3-8 vears 6-8 vears

fuse and are normally one maturation stage behind that of the distal epiphysis of the radius and ulna. Glo- bally, epiphyseal centers in the phalanges appear in a proximal4istal direction, but a great deal of variability between specimens is found in the sequence of appearance and the number of secondary centers present in the phalanges. Moreover, stage 0 cannot be distin- guished reliably in the radiographs from stage 6 , espe- cially in the distal phalanges, and epiphysis may never form in some individuals.

DISCUSSION Externally, the flipper of the striped dolphin has the

typical delphinid shape. It is longer than it is wide, and its distal end is narrow and pointed. Humeral, radial, and ulnar lengths develop rapidly after birth, reaching adult size by the age of 6 in both sexes, and little or no increase in size is apparent afienvard (Fig. 3). When these measurements are compared with those of striped dolphins inhabiting the North Western Pacific, it is observed that the length of the humerus and other osseous elements in the Mediterranean striped dolphins reach adult size a t the age of 6 , 4 years earlier than in the conspecific population off Japan (Ito and Miyazaki, 1990).

The carpal region showed considerable variability. In general, there were five carpal bones arranged in a proximal row of three and a distal row of two, although one or two additional osseous elements were occasionally observed. Variation in the carpal region is not un- common in cetaceans and has been documented in other species (Pilleri and Ghir, 1976; Casinos and Filella, 1981; Gihr et al., 1982). Distal to the carpus, there were five metacarpals with adjacent phalanges in each digit. The usual number of phalanges, from the first to the fifth digits, was one, eight, six, three, and one, although, again, substantial variation among individuals was found, and these numbers differed by one, two, and even three phalanges per digit. This variation was also no- ticed in Japanese striped dolphins, although the basic phalangeal formula in this population was found to be 2:9:7:4:2 (Ito and Miyazaki, 1990). Therefore, striped dolphins from Japanese waters appear to have, on average, one phalanx more in each of the digits. Minor differences were also found when comparing these counts to the congeneric Stenella attenuata and Stenella longirostris, the phalangeal formula of which is 1:7-8: 5:2:1 and 0%-9:6:3:1, respectively (Perrin, 1975).

Estimation of sex from the examination of bones in other species is usually based on differences in the length and the diameter in bone components between males and females. In our sample, significant variation between sexes was only detected in the length of the second digit and in its proportion to the braquial length. However, the variation was too small to be used for a clear identification of sex. Obvious sexual differ-

ences in the other metric characters described in this study were not observed, so prediction of sex based on osseous traits of the flipper was not feasible.

The appearance and degree of fusion of growth centers of bones during the growing period offers a relative indication of the age of the individual. Nevertheless, because few growth processes continue during the adult stage, assessment of chronologic age in adult specimens becomes more difficult as the individuals become old. Table 4 summarizes the progress of ossification as evidence by serial analyses of radiographs. The sequence of appearance of the secondary ossification centers is as follows: complete physeal closure is first achieved in the proximal epiphysis of the humerus; the distal epiphysis of the humerus and the proximal epiphysis of the radius and ulna follow; then, the distal epiphysis of the radius and ulna and the last to fuse are metacarpals and phalanges. In metacarpals, epiphyseal ossification centers mature a t the same time at both ends. As a general rule, the ossification of the epiphyses in the flipper bones showed a decreasing gradient in the proximodistal direction, thus confirming the pattern already described for other species in previous studies (Felts, 1966). Nevertheless, the epiphyseal centers in the phalanges show a great deal of variability in appearance and number, so a basic pattern of maturation for the species could not be established.

The results of the present study indicate that phalangeal epiphyses are not reliable indicators of skeletal maturity. Grading epiphyseal maturation at the distal epiphysis of the radius and ulna is a more straightfor- ward and precise method. Thus, variability in the chro- nology of appearance of the distal epiphysis of radius and ulna is quite constant, and its pattern of maturation is more regular than that of phalangeal epiphysis. This finding contradicts the method for measuring skeletal maturation proposed by Hui (19791, where maturation scores were calculated from the ossification stage of the distal ends of the radius, ulna, and phalanges. However, the grading of the secondary ossification centers in radius and ulna presented sexual dimorphism; ossification centers appeared earlier in females and epiphyseal closure occurred at an earlier age and at smaller body size in females than in males (Fig. 4).

ACKNOWLEDGMENTS We thank Dr. A. Casinos for advice on this manu-

script. E. Grau, A. Borrell, J. Forcada (Department of Animal Biology, University of Barcelona), J.A. Raga, M. Fernandez, J. Salinas, J.A. Balbuena (Department of Animal Biology, University of Valencia), M. Dom- ingo, J . Visa, M. Pumarola (Department of Anatomic Pathology Autonomous, University of Barcelona), and Rosa Mejias (SECONA, Palma de Mallorca) assisted in

714

the necropsies and in the collection of some of the material analyzed. Nuria Calzada was supported by an FPI fellowship from the Ministry ofEducation and sci- ence of Spain. Funds for this research were provided by CICYT projects Nat-1255-E and Nat91-1128-C04-02.

N. CALZADA AND A. AGUILAR

K. Norris, ed. University of California Press, Berkeley, Los An-

Felts, W., and F. Spurrell 1965 Structural orientation and density in cetacean humerii. Am. J. Anat., 116:172-203.

Gihr, M., C. Kraus, and G. Pilleri 1982 The manus ofPseudorca cras- d e n s (Owen): A studv of variabilitv. Invest. Cetacea. 23:lOl-24.

g e h PP. 255-276.

-~

LITERATURE CITED Aguilar, A,, and J.A. Raga 1993 The striped dolphin epizootic in the

Mediterranean sea. Ambio, 22:524-528. Benke, H. 1993 Investigations on the osteology and the functional

morphology of the flipper of whales and dolphins (cetacea). In- vest. Cetacea, 24:9-52.

Calzada, N., C. Lockyer, and A. Aguilar 1994 Age and sex composition of the striped dolphin die-off in the western Mediterranean. Mar. Mammal. Sci., 10.299-301.

Calzada, N., A. Aguilar, T.B. arensen, and C. Lockyer 1996 Repro- ductive parameters of the female Mediterranean striped dolphin. J . Zool. In Press.

Casinos, A,, and S. Filella 1981 Notes on cetaceans of the Iberian coasts: IV. A specimen of Mesoplodon densirostris (Cetacea, Hy- peroodontidae) stranded on the Spanish Mediterranean littoral. Saugetierk. Mttlg., 4:61-67.

Duguy, R., A. Aguilar, A. Casinos, E. Grau, and J.A. Raga 1988 fitude comparative des echouages de cetaces sur les c6tes MBditerra- n6ennes de France et d'Espagne. Misc. Zool., 12339-345.

Eales, N.B. 1954 The manus of the Narwhal, Monodon monoceros. L. Proc. 2001. Soc. London, 124:ZOl-211.

Felts, W. 1966 Some functional and structural characteristics of cetacean flippers and flukes. In: Whales, Dolphins and Porpoises.

Hui, C.A. 1979 Correlates of maturity-in the common dolphin, Del- phinus delphis. Fish. Bull., 77.295-300.

Ito, H., and N. Miyazaki 1990 Skeletal development of the striped dolphin (Stenella coeruleoalba) in Japanese waters. J . Mammal. SOC. Japan, 14:79-96.

Myrick, A.C., A.A. Hohn, P.A. Sloan, M. Kimura, and D.D. Stanley 1983 Estimating Age of Spotted and Spinner Dolphins (Stenella attenuata) and (Stenella longirostris) From Teeth. NOAA Tech. Mem. NMFS, SWFS-30.

Ogden, J.A., G.J. Conlongue, M.H.S. Rhodin, and A.G.J. Rhodin 1981 Roentgenographic indicators of skeletal maturity in marine mammals. Skeletal Radiol., 7:119-123.

Perrin, W.F. 1975 Variation of spotted and spinner porpoise (genus Stenella) in the eastern Pacific and Hawaii. Bull. Scripps Inst. Oceanogr., 2l:l-206.

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Rommel, S. 1990 Osteology of the bottlenose dolphin. In: The Bottle- nose Dolphin. S. Leatherwood and R. Reeves, eds. Academic Press, New York. Pp 29-49.

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flipper development in the mediterranean striped dolphin (stenella coeruleoalba)

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