Punjab Univ. J. Zool., Vol. 30 (1), pp. 031-036, 2015 ISSN 1016-1597 (Print) ISSN 2313-8556 (online)

Review Article

Siwalik Giraffidae (Mammalia, Artiodactyla): A review

Khalid Mahmood*, Muhammad Akbar Khan, Muhammad Adeeb Babar and Muhammad Akhtar

Palaeontology laboratory, Department of Zoology, University of the Punjab, Lahore-54590, Pakistan.

(Article history: Received: March 18, 2015; Revised: May 29, 2015)

Abstract The article is based on the published literature regarding the family Giraffidae, particularly about the extinct Siwalik species. The provided information is collected from the previous published articles, aiming to produce the basic information of the Siwalik giraffids. The distribution of the Siwalik giraffid species is also briefly discussed.

Key words: Mammalia, Vertebrate, Giraffidae, Miocene, Siwaliks.

To cite this article: MAHMOOD, K., KHAN, M.A., BABAR, M. A. AND AKHTAR, M., 2015. Siwalik Giraffidae (Mammalia, Artiodactyla): A review. Punjab Univ. J. Zool., 30(1): 31-36.

INTRODUCTION related to the Antilocapridae and to the Saiga antelope based on the development of the horn ecora (horned ruminants) and Tragulina- cores. He stipulated that the connections Pecora are well-adapted ruminants. between Sivatherium and the modern giraffe are Fossils are recorded in Eurasia, North of minor importance. Although Murie did not P outline a classification for the fossil Giraffidae, America and Africa during Neogene but the remains are rare during Eocene. Cervoids and he present a sort of phylogenetic diagram in giraffoids could have had predominantly which he showed Sivatherium as being directly vicariant origins within the pecora, giraffoids related to Bramatherium, to the saiga and to the within Africa, Arabia and/or India and cervoids pronghorn antelope. He interposed further north in Eurasia. Undoubted cervids then Antilocapridae and Cervidae between appeared from among cervoids in the early Sivatherium and Giraffa (Colbert, 1935). Miocene of Europe and East (Khan et al., 2006). Rutimeyer, in his ‘Nattirliche Geschichte During the later portions of Tertiary der Hirsche,’ published in 1881, failed to realize times northern India was a great center for the the relationships existing between the large adaptive radiation of Giraffidae. In the Siwalik Siwalik giraffes and the modern giraffe, he deposits of Upper Miocene, Pliocene, and placed Giraffa among Cervina, as closely related Pleistocene age there is a considerable to elk. Helladotherium from Pikermi was assemblage of fossil giraffes of varied form, and considered as being related to giraffe, and a study of these Siwalik giraffes put great consequently it was placed with the giraffe information on the problem of the evolution and among the deer. Sivatherium, Bramatherium the classification of Giraffidae (Colbert, 1935). and Vishnutherium from the Siwaliks were Some of the important classification assigned to a position among the antelopes, schemes for Giraffidae are made by Murie contiguous to the Damilis group of South Africa (1871), Lydekker (1882), Von Zittel (1925), (Colbert, 1935). It remained for Lydekker to Pilgrim (1911), Bohlin (1927) and Matthew show, in his large monograph on the Siwalik (1929). In 1871,James Murie published a paper Camelopardalidae published in 1882, that the in the Geological Magazine entitled, “On the Siwalik genera, Sivatherium, Hydaspitherium, Systematic Position of Sivatherium giganteum of Bramatherium, etc., are true giraffes and they Falconer and Cautley, in which he discussed the directly related to the modern Giraffa and to relationship of Sivatherium to Bramatherium and such fossil forms as Helladotherium from to other artiodactyls. Murie was led to believe Pikermi. Lydekker's realization that these that Sivatherium and Bramatherium are closely several fossil forms are true giraffes, and that 0079-8045/15/0031-0036 $ 03.00/0 Copyright 2015, Dept. Zool., P.U., Lahore, Pakistan *Corresponding author: [email protected] 32 K. MAHMOOD ET AL.

they should be combined with the modern Bohlin's classification is the most giraffes in one family, is a distinct advance over comprehensive and perhaps the best of all the the views of previous authors. Lydekker did not proposed schemes of giraffid taxonomy. His divide the Camelopardalidae, as he called it, into creation of a separate subfamily for the okapi lesser groups or subfamilies, but he did arrange may be disputed (Colbert, 1935). Matthew the seven genera which he considered as (1929) in his 'Critical Observations upon Siwalik constituting the family in a certain order of their Mammals,' pointed out the desirability of relationship to one another, indicating a gradual including Okapia among Palaeotraginae, diminution in the length of the limbs and of the thereby making three subfamilies of Giraffidae neck from the giraffe to the sivathere (Colbert, instead of four (exclusive of "Progiraffinae"). 1935). Matthew's classification is given below: The The English translation of Von Zittel's subfamily Palaeotraginae includes 'Textbook of Palaeontology,' published in 1925, Palaeotragus, Samotherium, Giraffokeryx and includes the Giraffinae and the Sivatheriinae as Okapia. The subfamily Giraffinae includes the two separate subfamilies among the family genera Giraffa, Orasius and Honanotherium. Cervicornia. In 1911, Dr. Pilgrim published a The subfamily Sivatheriinae includes the genera memoir entitled 'The Fossil Giraffidae of India.' Sivatherium, Indratherium, Helladotherium, Although this work was based on with the Bramatherium and Hydaspitherium. Siwalik giraffes, it contained a supplementary A careful consideration of the problem of consideration of the evolution of the Giraffidae. a classification of Giraffidae will demonstrate the There is a phylogenetic diagram of the validity of Matthew's views as to the inclusion of Giraffidae which classifies the family in the Okapia in Palaeotraginae. Bohlin's separation of following manner (Colbert, 1935). The Giraffidae the okapi into a distinct subfamily is seemingly a shows in phylogenetic relationship that it has the flaw in his otherwise admirable classification of following members of the family Palaeotraginae, this group of artiodactyls. It would seem as if he Palaeotragus, Samotherium, Alcicephalus, has placed too much emphasis on minute and Okapia, Indratherium, and Libytherium in a for the most part unimportant characters, and in sequential way (Colbert, 1935). doing this he has disregarded the great The Giraffidae’s classification is marked preponderance of characters that typify Okapia by the multiplication of subfamilies, of which as a truly primitive palaeotragine. Okapia is, in one, Progiraffinae, is founded on rather scanty all of its essential characters, a structurally material, and another, Helladotheriinae, consists primitive Miocene giraffe (more primitive than of genera that might very well be placed within Palaeotragus or Samotherium) that has two different but well-established groups, persisted on to the present day in a region Palaeotraginae and Sivatheriinae. The family conducive to the continuation of such an early Helladotheriinae is classified at that time that form (Colbert, 1935). Bohlin has separated the includes the following genera Helladotherium, okapi from the Palaeotraginae in having: the Vishnutheriu, and Giraffokeryx. Progiraffinae frontals are narrow in the modern form as includes only the genus Progiraffa. Giraffinae compared to the fossil species, the horns are includes the genus Giraffa and Orasius. placed in a slightly different position in Okapia Sivatheriinae includes the genera Sivatherium, from the positions of the horns in Palaeotragus Hydaspitherium, Bramatherium and or Samotherium, the frontals in the okapi tend to Urmiatherium. develop pneumatic sinuses within them whereas Abel's classification of Giraffidae, the sinuses are not pronounced in Palaeotragus published in 1919 in his 'Stiimme der and related genera, there are minor differences Wirbeltiere,' is essentially the same as that of in the dentition, no outer cingulum on DM2 in the von Zittel. He divides the family into two okapi, whereas in Palaeotragus and subfamilies, Giraffinae and Sivatheriinae. In Samotherium the cingulum is present, and the 1927 Birger Bohlin published an elaborate skeleton of the okapi differs in small details, monograph, 'Die Familie Giraffidae,' a very especially those of proportions, from the thorough study of the giraffes, with the fossil skeleton of Palaeotragus. material collected by the Swedish expeditions in These are differences of minor North China serving as its basis (Colbert, 1935). importance. Now let us look at Okapia and the The family Giraffidae includes Palaeotraginae, fossil Palaeotraginae for the purpose of making Sivatheriinae, Giraffinae, and Progirafflnae. comparisons between major anatomical characters.The skull of Okapia is in most SIWALIK GIRAFFIDAE 33

respects more primitive than the skull of the The skeleton of the okapi is certainly fossil Palaeotraginae. The canine-premolar primitive. It shows little of the elongation of the diastema of the mandible is much shorter in the limbs, or of transverse growth of the skull and okapi than it is in the fossil forms, showing that skeletal elements that appear in the more the modern species has retained a short muzzle, advanced Giraffidae. Therefore, considering a primitive and a diagnostic heritage character. Okapia with regard to its major anatomical In the okapi the frontals are narrow, which is to characters, without special emphasis on small, be expected in a relatively primitive artiodactyl. single features, we see that it is a very primitive In Palaeotragus the frontals are wide, and this giraffid, more primitive even than Palaeotragus, may be considered as an habitus character, and that it is a satisfactory structural ancestor for subsequent to the narrow frontal region. An the Palaeotraginae. It has the diagnostic examination of various groups of ungulates will heritage characters of Palaeotraginae, but in this show that the skull tends to elongate first, after persistent genus very few of the advanced which it widens, if the tendency to widen exists habitus characters that characterize the fossil at all. That is, elongation precedes lateral genera have been developed (Colbert, 1935). expansion. The genus Giraffokeryx was created by Consequently, we may expect a Pilgrim in 1910, on the basis of upper and lower primitive giraffid, such as the okapi, to have a cheek teeth. Pilgrim (1911) in his monograph of narrower frontal region than a more advanced the Siwalik Giraffidae, placed Giraffokeryx along form in which the cranium has broadened out. with Helladotherium and Vishnutherium in a Of course, as Bohlin has shown, the frontals of separate subfamily, Helladotheriinae. Bohlin the okapi contain rather large sinus cavities, (1927) went to the other extreme and reduced which are lacking in Palaeotragus and the genus Giraffokeryx to synonymy with Samotherium. It may be quite probable that the Palaeotragus, including it, naturally, in the development of the frontal sinuses in the okapi subfamily Palaeotraginae. Both of these authors are of a secondary nature, and that they have were founding their conclusions on the evidence been acquired more or less independently in the of teeth alone. An almost complete skull of long period of time that has elapsed between Giraffokeryx in the American Museum gives Miocene and the present day. But this is no much evidence that helps to solve the question reason for excluding the okapi from a place as a of the taxonomic position of the genus. This skull relatively primitive palaeotragine. It is a primitive has been described by Colbert (1933), and it is genus that has developed certain specialized shown to be essentially a Palaeotragus-type characters during the passage of geologic time. with an extra pair of horn cores on the frontals. In Okapia the horn cores are rather Therefore the genusGiraffokeryx properly small, whereas in Palaeotragus they are much belongs in the subfamily Palaeotraginae, where larger. Thus we may regard the okapi as more it was placed by Bohlin and later by Matthew. It primitive in its horn development than is is, however, a separate genus, quite distinct Palaeotragus. Of course, one might argue that from Palaeotragus, but closely related to it. the small horns in the okapi are degenerate Bohlin and Matthew have both given conclusive structures, secondarily reduced from larger evidence to show that the genera horns, but in answer to this argument it might be Hellodotherium and Vishnutherium should be said that the horn cores in the okapi have included in one subfamily with Sivatherium, retained a primitive position over the orbit, and Hydaspitherium, Bramatherium, etc. (Colbert, this would favor their being truly primitive 1935). structures. This primitive position of the horn Consequently Pilgrim's subfamily cores is retained in Palaeotragus, but in Helladotheriinae would seem to be unnecessary. Samotherium the horn cores have shifted The subfamily Progiraffinae, created by Pilgrim somewhat to the rear, due to the elongation of (1911) is based on rather insufficient material. the skull. In Okapia the dentition is very The genus Progiraffa (Propalaeomeryx) may be brachyodont a primitive character. In perfectly valid, and it may deserve separation Palaeotragus and Samotherium the teeth are from the other Giraffidae as a distinct subfamily, considerably higher than is the case in the but at the present time the material is not modern genus, showing that the fossil forms are plentiful enough to prove this. Until further relatively advanced in the stage of their material is discovered it would seem best to phylogenetic development (Colbert, 1935). include this genus tentatively to Palaeotraginae (Colbert, 1935). 34 K. MAHMOOD ET AL.

Palaeotraginae includes primitive, shown, however, that the resemblances medium sized giraffids, having as a rule one pair between Protoceratidae and Giraffidae are due of supraorbital frontal horn cores. There may be to convergence, and that these two families are a second pair of horn cores at the anterior really separated from each other by differences extremities of the frontals. Horn cores in the of basic importance (Colbert, 1935). form of simple tines, well developed in the There are certain resemblances in the males, feebly developed or absent in the teeth between Protoceratidae and the more females. Skull usually elongated. Cheek teeth primitive Giraffidae, resemblances that may be brachyodont, with moderately coarse sculpture attributed to primitive heritage characters carried of the enamel. Limbs and neck slightly over from a common Eocene ancestor. The skull elongated (Colbert, 1935). resemblances, especially in the development of The giraffid species reported from the numerous pairs of horn cores in several genera above mentioned literature (many have become of these two families, are due entirely to a synonym) includes Palaeotragus rouenii Gaudry, convergence in evolutionary trends. Both Palaeotragus parvus (Weithofer) synonym of P. Protoceratidae and Giraffidae produced horn rouenii, Palaeotragus vetustus (Wagner) cores anterior to and posterior to the orbits. But synonym of P. rouenii, Palaeotragus microdon these horn cores are derived from different skull (Koken), Palaeotragus coelophrys (Rodler and elements in the two groups. This is well Weithofer), Palaeotragus decipiens Bohlin. illustrated by the anterior horn cores, which are Palaeotragus quadricornis Bohlin, Palaeotragus of premaxillary origin in Protoceratidae, and of expectans (Borissiak), Achtiariaex pectans frontal origin in Giraffidae (Colbert, 1935). (Borissiak), Giraffokeryx punjabiensis, Okapia Matthew (1929) made the following johnstoni (Sclater), Samotherium boisseri, remarks with regard to the origin of Giraffidae Samotherium neumeyeri (Rodler and Weithofer), and the relation of this family to the North Samotherium sinense (Schlosser), Samotherium American Protoceratidae that "the family tafeli (Killgus), Samotherium eminens appears to be a group of specialized survivals of (Alexejew), Alcicephalus neumeyeri Rodler and the Middle Miocene Palaeomerycinae, of which Weithofer, Chersonoterium Alexejew synonym Dromomeryx, the American genus, is the only of Samotherium, Chersonotherium eminens one known from complete skulls and associated Alexejew, Shianshithenrum Killgus, synonym of skeletons. The horns of Dromomeryx are of Samotherium, Shanshitherium tafeli Killgus, giraffoid type, long, straight, probably skin- Propalaeomeryx sivalensis Lydekker, Progiraffa covered, nondeciduous, supra-orbital, and with a exigua Pilgrim, Giraffa camelopardalis basal wing that suggests the later complications (Linnaeus), Giraffa sivalensis, Giraffa affinis in the sivatheriines. Teeth quite close to (Falconer and Cautley) synonym of G. Palaeotragus and Giraffokeryx. Schlosser sivalensis, Giraffa punjabiensis Pilgrim, Giraffa derives giraffes from Protoceratinae, but this priscilla Matthew, Giraffa nebrascensis Matthew does not seem to be a tenable phylogeny. The and Barbour, Orasius atticus (Gaudry and protoceratines are an early specialized group of Lartet), Orasius eximius Wagner, Orasius Traguloidea, with no approach to the Pecora in speciosus (Wagner), Honanotherium schlosseri foot characters. The Giraffidae are true Pecora, (Pilgrim), Sivatherium giganteum Falconer and fully developed as such in the feet, and nearly Cautley, Indratherium majori, Bramatherium related through Palaeomerycinae to the primitive perimense Falconer, Hydaspitherium Cervidae (cf. Eumeryx of the Stampian megacephalum Lydekker, Hydaspitherium Oligocene of Mongolia) (Colbert, 1935). grande, Hydaspitherium magnum Pilgrim, The evolutionary development of the Hydaspitherium birmanicum, Vishnutherium group took place in Europe and Asia. The okapi iravaticum Lydekker, Helladotherium duvernoyi and the giraffe, the one a persistent primitive Gaudry, Helladotherium gaudryi De genus and the other a genus that specialized Mecquenem. Griquatherium cingulaum early in the evolutionary history of the group, Haughton, Libytherium maurusicum Pomel. migrated to Africa from the Holarctic center of Protoceratidae of North America have origin. The survival of these two forms in Africa, been linked to Giraffidae by some authors, on far from the center of origin of the family, is what the basis of certain resemblances between the might be expected. members of the two groups. Schlosser, Matthew has shown, in his 'Climate and especially, would derive Giraffidae directly from Evolution,' that persistent primitive species Protoceratidae. Both Bohlin and Matthew have migrate away from the center of origin and their SIWALIK GIRAFFIDAE 35

place is taken by more specialized forms. Or, to 1910; Giraffa priscilla Pilgrim, 1911 (Matthew, put it in a different way, the primitive and in 1929; Colbert, 1933, 1935; Pilgrim, 1937, 1939; adaptive species are pushed out by the Raza, 1983; Akhtar 1992; Barry et al., 2002; specialized, adaptive species, so they must Badgley et al., 2008; Khan et al., 2008, 2009). needs find refuge in peripheral regions, far The family Giraffidae represents only two living distant from their place of origin (Colbert, 1935). species, Okapi (Okapiajohnstoni) and Giraffe (Girffacameloparadalis). Both species today are Siwalik Giraffids present in Africa (Ethiopian region). However, The Siwalik giraffid species are provided the Giraffidae have a rich fossil history in Table 1. The Kamlial Formation represents consisting of approximately thirty species Progiraffa exigua. The Chinji Formation throughout the Neogene of the Old World. indicates Giraffokeryx punjabiensis Pilgrim,

Table I: The Siwalik species of the family Giraffidae. The Siwalik species can be distinguished on the basis of their dentition and skull patterns. Species Appearance in the Siwalik Hills of Pakistan Giraffa sivalensis Falconer and Cautley, 1843 Upper Siwaliks Bramatherium geraadsi Falconer, 1845 Upper Siwaliks Sivatherium giganteum Falconer and Cautley, 1836 Upper Siwaliks Bramatherium perimense Falconer, 1845 Middle Siwliks Giraffa punjabiensis Pilgrim, 1910 Middle Siwaliks Helladotherium grande Gaudry, 1860 Middle Siwliks Hydaspitherium birmanicum Pilgrim, 1910 Middle Siwaliks Hydaspitherium grande Lydekker, 1878 Middle Siwaliks Hydaspitherium megacephalum Lydekker, 1876 Middle Siwaliks Hydaspitherium magnum Pilgrim, 1910 Middle Siwaliks Vishnutherium iravaticum Lydekker, 1876 Middle Siwaliks Giraffokeryx punjabiensis Pilgrim, 1910 Lower Siwaliks Giraffa priscilla Matthew, 1929 Lower Siwaliks Progiraffa sivalensis Pilgrim, 1911 Lower Siwaliks

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