Fused Thoracic Vertebrae in Birds: Their Occurrence and Possible Significance

Home , Juncitarsus, Notarium, Palaelodus

J. Yamashina Inst. Ornith., 14: 86-95, 1982

Robert W. Storer*

Abstract The notarium, a group of fused thoracic vertebrae, is characteristic of birds of five orders and is found in one or more families of five more orders of non-passerine birds . Sixteen patterns of variation in the number of vertebrae in the notarium and of unfused vertebrae between it and the synsacrum were found. The occurrence of these patterns in the groups having a notarium is tabulated. Selective factors favoring the evolution of fusion of these vertebrae may have included the shock induced by landing on hard substrates or of striking prey and the prevention of downward bending of the ends of the thoracic portion of vertebral column while the birds are in flight. Phylogenetic implications of the presence of a notarium in several groups are discussed.

The notarium of Os dorsale of birds is a group of fused thoracic vertebrae usually separated by one or more unfused vertebrae from the anteriormost vertebra of the synsacrum (Baumel 1979: 93, 112). Although it was described and figured as early as 1856 (Barkow 1856: pl. II), I have found little more than casual mention of it in the literature. It therefore seems worthwhile to survey the distribution of this structure among the orders and families of birds, to describe the variation in the numbers of vertebrae in the notarium and between it and the synsacrum, to speculate on its possible adaptive significance, and to discuss phylogenetic implications of its presence. This study is based on examination of skeletons in the U. S. National Museum of Natural History, the Field Museum of Natural History, and the University of Michigan Museum of Zoology. Skeletons of all families of non-passerine birds, as well as those of all the suborders and superfamilies and most of the families of passerine birds, were examined. I am grateful to Dr. Richard L. Zusi for permitting me to use the first collection and for other assistance in the project, to Dr. John Fitzpatrick for permission to use the collection of the Field Museum, and for Steven M. Goodman for obtaining data from the Field Museum and the U.S. National Museum of Natural History, as well as for helpful criticism of the manuscript. It is an honor to offer this paper to the Journal of the Yamashina Institute for Ornithology for its Jubilee number and a pleasure to compliment the Institute on the fine morphological work done there.

In birds, the number of vertebrae varies both between and within species, ranging from 39 in some passerines to 63 in some swans (Portmann 1950: 79). This makes it all but impossible to determine homologies between thoracic vertebrae of different species,

* Museum of Zoology and Division of Biological Sciences , The University of Michigan, Ann Arbor, MI 48109, USA.

86 Fused Thoracic Vertebrae in Birds 87 and no such determination is attempted here. Instead, I have chosen to consider the different arrangements of fused and unfused vertebrae as units and to compare them as such. In doing this, I have adopted a simple notation in which "S" stands for the synsacrum (included as an aid in orientation) and is followed first by the number of unfused vertebrae and then by the number of fused vertebrae in the notarium. Thus a

Table 1. The Distribution of fused thoracic vertebrae. 88 R. W. Storer bird with four fused vertebrae in the notarium and one unfused vertebra between it and the synsacrum would have the formula "S-1-4." In the pelicans, there is a fusion of a few of the posterior thoracic vertebrae with the synsacrum (Barkow 1856: pl. III). This condition is not considered in this paper. The notarium, as considered here, is never fused with the synsacrum there being at least one articulation between it and the synsacrum. The presence or absence of the notarium in the various orders of birds and suborders of the Gruiformes is listed on Table 1. Unless otherwise indicated, the condition listed is the rule in adult birds of the order or suborder.

Variation Among and Within Groups

The range of variation in the formula is shown in Table 2. The number of unfused vertebrae ranges from 0 in some pigeons and tinamous to 4 in some cranes and that of the fused vertebrae from 2 in several groups to 6 in some Western Grebes (Aechmophorus). Tinamidae. The most common formula in the tinamous was S-1-4, comprising 75 percent of the specimens examined. Formulas involving a total of 6 vertebrae (S-1-5 and S-2-4) were found only 7 times in this family, 5 of them in species of Nothoprocta, which

Table 2. Distribution of numbers of fused and unfused thoracic vertebrae . Fused Thoracic Vertebrae in Birds 89 90 R. W. Storer were represented by 9 specimens. This is not related to the size of the birds because members of this genus are of medium size for the family and because the other two specimens with six involved vertebrae were in the genera Nothura and Rhynchotus, small and large birds, respectively. Furthermore, the three birds with but 4 involved vertebrae were in the genera Tinamus (large birds) and in Crypturellus soul, a small bird. Podicipedidae. The greatest number of patterns (nine) was found within this family. In the related genera Tachybaptus and Podilymbus, the most frequent arrangement (S-1-4) accounted for 92.5 percent of the individuals examined. In Rollandia the median was S-1-5 (55.6%) and in Podiceps it was S-2-4 (60.0%). In Aechmophorus occidentalis, the situation was more complex, three arrangements being frequent (S-1-5, 42.1%; S-2-5, 28.3%; and S-2-4, 23.8%). There also appeared to be a difference between the sexes (Table 3), S-1-5 being more frequent in males (45.9% to 35.5%) and S-2-4 more frequent in females (29.0% to 20.8%). The trend in the family is for an increase in the numbers both of fused and unfused vertebrae from large to small species (Table 3), although this effect is modified by relationships. For example, there are no significant differences within Podiceps in spite of the rather large range in size of the species, and the species of Podilymbus, which are larger than those of Tachybaptus differ but little from those of that genus. Phalacrocoracidae. The cormorants differ from all the other groups in that the fusion only occurs in approximately half of the species and individuals (42 out of 80 specimens examined) and when it occurs, always involves two vertebrae. In all other genera in which the notarium was found, all adults possessed it. Threskiornithidae. The most frequent arrangement is S-2-3 or 68.3% of the sample. The sample was too small to show trends in the number of fused vertebrae with size of the bird. Phoenicopteridae. S-1-4 was the most frequent formula in all five species examined and accounted for 86% of the total sample. It may be significant that this is not the most frequent formula found in the Threskiornithidae. Falconidae. Omitting the genera Herpetotheres and Micrastur, which lack the notarium, the falconids are nearly equally divided between the formulas S-1-5 and S-1-4, which account for 51 and 47 percent of the specimens, respectively. The remaining genera, except Falco, all have four fused vertebrae. In Falco, 5 species (naumanni, tinnunculus, rupicoloides, cenchroides, and vespertinus) also have four fused vertebrae. Of two specimens of F. biarmicus examined, one had 4 and one, 5 fused vertebrae. All the remaining 18 species of Falco examined had 5 fused vertebrae. This family is unusual in showing a nearly equal division between two arrangements and in having genera, or species of Falco showing a single arrangement. In view of this small variation within taxa it is surprising to find the New World Kestrel (F. sparverius, N = 20) differing from the Old World kestrels (F. tinnunculus, N = 2: F. naumanni, N = 1: and F. cenchroides, N = 1) and F. vespertinus (N = 1) from F. amurensis (N = 2), with which it is sometimes considered conspecific. Galliformes. This order is marked by small variation in the formula, 95 percent being S-1-4. Gruidae. The cranes proved highly variable in the pattern of fusion of the thoracic Fused Thoracic Vertebrae in Birds 91 vertebrae and had, on the average, the most unfused vertebrae between the notarium and the synsacrum (67 percent had 3 and 11.5 percent had 4 such unfused vertebrae). In no other group was the latter condition found. Aramidae. The six Limpkins examined all had S-3-3, the most frequent arrangement in the Gruidae. Psophiidae. The most frequent formula in the trumpeters was S-2-4, accounting for 71% of the sample. This formula was uncommon (3.8%) in the Gruidae and was not found in the Aramidae, both families considered close to the Psophiidae. Rhinochetidae, Eurypygidae, and Mesoenatidae. The small samples of these three isolated families showed some overlap in arrangements with each other and the Gruidae. Pteroclididae. The small sample of sandgrouse was divided between the two commonest arrangements of found in the Columbidae (S-1-4 and S-1-3) but in the reverse order of frequency. Columbidae. Except for 13 specimens of Columbinae in which the notarium articulated directly with the synsacrum, there appeared to be little difference between that subfamily and the Treroninae. Of the 13 specimens without free vertebrae, 7 were found as variants in 6 different genera, but in Staroenas and Leucosarcia all specimens examined (4 and 2, respectively) had the formula S-0-4. Of the genera represented by samples of ten or more specimens, only Zenaida (including Zenaidura) had a majority which differed from the commonest formula in the family (S-1-3), in that genus, 15 of 21 were S-1-4 and one was S-1-5, the only dove with that formula. Opisthocomus. Four specimens examined all had the formula S-2-4 and one had S-1-4. This genus is discussed below in the phylogenetic section. Steatornis. The two specimens examined had the formula S-1-3. This is the only caprimulgiform bird known to have a notarium.

Possible Adaptive Significance

The adaptive value of the notarium is by no means clear. The following speculations are offered in the hope that others may pursue the problem in greater depth. The ribs articulating with this structure also articulate with the sternum, the whole acting as part of the unit which moves like a bellows in breathing. If fusion of a group of thoracic vertebrae were an advantage in breathing, why did this structure not become universal among birds? And why are there free thoracic vertebrae between the notarium and the synsacrum? The answer to the latter probably lies in the lack of flexibility that would accompany such fusion. The adaptive value of the notarium is more probably related to aspects of locomotion than to breathing. The notarium is not related to the type of articulation between thoracic vertebrae. In most birds, including both those with and those without notaria, these articulations are heterocoelous, in the penguins, which lack notaria, and in the cormorants, some of which have notaria, they are opisthocoelous. Fusion of vertebrae adds strength and rigidity at the expense of flexibility to the 92 R. W. Storer

part of the vertebral column involved and thus may reduce the likelihood of dislocation when this part is jarred. Such an explanation may account for the remarkable similarity of the arrangements in the unrelated Tinamiformes and Galliformes. Birds of both of these groups are heavy bodied and small winged, and the shock of landing must be great. But if this is the case, why do the heavy-bodied bustards lack a notarium? Long-legged, long-necked birds that hold both legs and neck outstretched in flight present another problem. The weight and distance from the center of gravity of these parts would tend to pull the ends of the thoracic part of the vertebral column downward. This could explain why the notarium is present in the Threskiornithidae, Phoenicopteridae, Gruidae, and Aramidae. But if this is so, why hasn't it evolved in the Ciconiidae and other birds with long legs and necks? Possibly the storks' back-paddling with their wings before landing makes the evolution of a notarium less advantageous than in the ibises and other groups which have it. The presence of a notarium in other gruiform groups (Psophia, Rhinochetos, Eurypyga, and the Mesoenatidae) is difficult to explain. Possibly it is a carry-over from crane-like ancestors. The situation in diving birds is also complex. The Podicipedidae and Phalacrocoracidae are the only divers which possess a notarium. Both are foot- propelled while under water and have very heavy leg musculature that in flight tends to cause flexion of the spine as in long-legged birds. Yet the Gaviidae, which are similarly adapted, lack a notarium. Wing-propelled diving birds have not evolved a notarium. This is not surprising because these birds probably steer, at least in part, by a lateral bending of the body which would be lessened by fusion of vertebrae, whereas foot-propelled divers can steer more easily by differential propulsive foot movements. Some Falconidae, for example the Peregrine Falcon (Falco peregrinus), strike their prey in the air with closed talons. Others strike their prey on the ground. In both instances, the shock at impact must be great, and this may have provided the selective pressure for the evolution of a notarium in this group. The adaptive significance of the notarium in Opisthocomus is not immediately apparent. These birds spend most of their lives in tall shrubs or small trees, where flexible branches cushion the shock of landing. If these birds were derived from cuckoos, it is difficult to imagine what selective pressure might have favored fusion of thoracic vertebrae. On the other hand, if they were derived from galliform birds, this fusion could be a retention of an ancestral character. Pigeons (Columbidae) and sandgrouse (Pteroclididae) are heavy-bodied birds with longer, more pointed wings than galliform birds. Their flight is swift and direct, and they frequently land on the ground, where most of them feed. Thus, as in the tinamous and galliform birds, evolution of the notarium may have been related to the shock of landing on the ground. On the average, fewer vertebrae are included in the notarium of pigeons and sandgrouse than of tinamous and galliform birds. This can be explained by the smaller number of ribs in the former groups. Steatornis, alone among the Caprimulgiformes, has a notarium. Unlike other members of this order, these birds live in caves, where they navigate by echo-location. Here again, the shock of landing on a hard substrate may have provided the selective Fused Thoracic Vertebrae in Birds 93 pressure for a notarium. In summary, notaria have arisen independently in at least ten phyletic lines of birds. I believe that the selective factors involved in their evolution have been related to locomotion. In the Tinamiformes, Galliformes, Columbiformes, and Steatornis, the shock of landing on a hard substrate seems to be the most likely factor. In the Threskiornithidae, Phoenicopteridae, Gruidae, and Aramidae, the factor may have been pressure from the long legs and necks to flex the thoracic part of the vertebral column while the birds are in flight, although shock on landing cannot be ruled out. In the Falconidae, the shock of striking prey on the ground or at high velocity in the air may have been the factor. In the Podicipedidae and Phalacrocoracidae, the weight of the hind limbs and their musculature may have been a factor much as may have been the long legs of the Gruidae and similar birds. I find the presence of the notarium in the remaining groups even more difficult to explain, except as a retention of an ancestral character.

Possible Phylogenetic Significance

In order to assess the phylogenetic significance of a character state it is important to determine whether it is primitive or derived. Several lines of evidence indicate that fusion of thoracic vertebrae is a derived condition. There was no such fusion in the earliest known bird, Archaeopteryx, although that bird already had some fusion in the synsacrum, a condition found to an even greater degree in all later birds. More orders and families of birds lack this fusion than have it. Finally, this fusion appears later in the ontogeny of the individual, in grebes at least, appearing complete at approximately the same time as the complete ossification of the tarsometatarsus (five to six month of age). While it is unwise to base classifications on single-character analyses, such analyses can and do yield clues to the relationships among groups. Given that fusion is derived and that none of the five orders in which fusion is the rule (Tinamiformes, Podicipediformes, Phoenicopteriformes, Galliformes, and Columbiformes) is more closely related to another in this group than to others outside it, the notarium presumably arose independently in each. Assuming further that lack of fusion was the primitive condition in the five orders in which both conditions are found (Pelecaniformes, Ciconiiformes, Falconiformes, Gruiformes, and Caprimulgiformes), fusion must have arisen independently in each. Thus, there have been at least ten independent derivations of this character. The presence of a notarium in Opisthocomus, is at odds with Sibley and Ahlquist's (1972: 181-182) placement of this bird in the Cuculidae near the Crotophaginae. No cuckoos, including the Crotophaginae, are known to have this structure. On the other hand, the most frequent arrangement of fused thoracic vertebrae in Opisthocomus (S-2- 4, four of five individuals) is rare in the Galliformes and was not found in any cracid, the Galliform group to which Opisthocomus has been thought closest (Miller 1953). If Opisthocomus is a cuckoo, it must have evolved the notarium independently. The sandgrouse, Pteroclididae, have been thought closer to the Charadriiformes than the Columbiformes (Sibley & Ahlquist 1972:158), but the presence of the notarium 94 R. W. Storer in these birds indicates either a common ancestry with the Columbidae or an independent evolution of fusion in a charadriiform ancestor. The two arrangements in the sandgrouse (S-1-4 and S-1-3) are the two commonest in the Columbidae although in a reverse order of frequency (83% of sandgrouse have S-1-4 and 82% of columbids have s-1-31. In the Falconidae, members of the genera Herpetotheres and Micrastur differ from others of the family and resemble the Accipitridae in lacking fusion of the thoracic vertebrae. Either they represent an early offshoot of the falconid line, or they are incorrectly placed in that family. (As Brodkorb [1960] pointed out in supporting the transferral of Gampsonyx from the Falconidae to the Accipitridae, that genus lacks fusion of the thoracic vertebrae.) Among the true falcons, the differences between the formulas of Falco sparverius and the Old World kestrels (F. tinnunculus and F. naumanni) and between F. vespertinus and F. amurensis could be used as arguments that F. sparverius does not form a superspecies with these Old World forms and that the last two forms are specifically distinct. According to Sibley & Ahlquist (1972: 86), the Phoenicopteridae should be included in the Ciconiiformes. More recently, Olson & Feduccia (1980) have argued that the flamingos were derived from the shorebirds (Charadrii). If the flamingos are ciconiiform, either they shared a common ancestor with the Threskiornithidae after the common ancestor split off from the rest of the Ciconiiformes, none of which have notaria, or the notarium was evolved independently in both the Phoenicopteridae and the Threskiornithidae. According to Olson & Feduccia (1980: 68),"There is, as yet, no evidence to indicate whether Palaelodus diverged from the more typical flamingos before or after the evolution of Juncitarsus." The last form is from the earliest middle Eocene, and according to Olson & Feduccia (op. cit.: 57), its thoracic vertebrae were not fused. If this is true and if Juncitarsus is indeed a flamingo, the presence of a notarium in Palaelodus (Milne-Edwards 1869-1871: 66) of late Oligocene or early Miocene age, can be considered evidence that either Palaelodus diverged from the line of the Recent flamingos subsequent to the time of Juncitarsus or that the notarium evolved independently in both the Palaelodus and the modern flamingo line. The relationships among the different groups in the Gruiformes have long been debated. Evidence from the notarium adds little to the solution of this problem. Perhaps the most significant idea is that the presence of fused thoracic vertebrae in the Gruidae, Aramidae, and Psophiidae and its absence in the Rallidae supports the idea of an early divergence of a common ancestor of the first three from that of the Rallidae. The similarity of the patterns of the Gruidae and the Aramidae suggests that these two groups are closer to each other than either is to the Psophiidae. In the presence of notaria in the remaining orders and families I see no obvious phylogenetic significance. These points are not presented as arguments in support of particular phylogenetic arrangements. Instead, they are intended to show the ways in which the presence of the notarium in particular groups of birds affects our thinking about the arrangements of these groups. Similar analyses of enough other characters should together lead to better understanding of the phylogenetic relationships among the higher taxa of birds. Fused Thoracic Vertebrae in Birds 95

References

Barkow, H. K. L. 1856. Syndesmologie der Vogel. Koniglichen Universitat, Breslau. Baumel, J. J. et al. Eds. 1979. Nomina Anatomica Avium. Academic Press, New York. Brodkorb, P. 1960. The skeleton and systematic postion of Gampsonyx. Auk 77: 88-89. Miller, A. H. 1953. A fossil hoatzin from the Miocene of Colombia. Auk 70: 484-489. Milne-Edwards, A. 1869-1871. Recherches anatomique et paleontologiques pour servir a l'histoire des oiseaux fossiles de la France. Vol. 2. Victor Masson and Sons, Paris. Olson, S. L. & Feduccia, A. 1980. Relationships and evolution of flamingos (Aves: Phoenicopteridae). Smithsonian Contrib. Zool. 316. Portmann, A., in Grasse, P-P. 1950. Traite de Zoologie, XV, Oiseaux. Masson et Cie, Paris. Sibley, C. G. & Ahlquist, J. E. 1972. A comparative study of the egg white proteins of non-passerine birds. Peabody Mus. Nat. Hist. Bull. 39: 1-276.