The systematic position of Hoplitomerycidae (Ruminantia) revisited

Geobios 46 (2013) 33–42

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Original article

The systematic position of Hoplitomerycidae (Ruminantia) revisited§ Paul Peter Anthony Mazza Department of Earth Sciences, University of Florence, via La Pira 4, 50121 Florence, Italy

A R T I C L E I N F O

A B S T R A C T

Article history: Received 26 November 2011 Accepted 11 October 2012 Available online 20 January 2013

Hoplitomeryx Leinders was originally described only on cranial characters. The type specimens were found during the 1970’s in karstic fissure fillings, most likely of Messinian age, in Gargano (Apulia, southeastern Italy), between Poggio Imperiale (418490 300 N, 158210 580 E) and Apricena (418470 060 N, 158260 410 E). During the 1990’s, Hoplitomeryx remains were also discovered in the lower Tortonian layered calcarenites near Scontrone (Abruzzo, central Italy; 418450 15.550 N, 148020 13.230 E). The skull fragments, teeth, and jawbones from both localities have been examined. The dental characters had never been described before, and also some maxillaries and jawbones were not part of the original sample that was analyzed to establish the genus. Because they possess two lacrimal orifices and closed metatarsal gulley, hoplitomerycids have been linked more closely with Cervids, and accommodated in Cervoidea. A cladistic analysis of a character-taxon matrix of 121 morphological features (48 cranial, 51 dental and 22 postcranial characters) is performed. The analysis shows that hoplitomerycids stem either between antilocaprids and bovids, or antilocaprids and giraffids. They are not linked directly with cervids. Hoplitomerycids likely stemmed from a primitive ruminant stock, perhaps around 29 Ma when a land bridge connected the Abruzzo-Apulia platform with the Balkans across the Adriatic Sea. In the new land, hoplitomerycids developed a mosaic of apomorphic and homoplastic (convergent) character states that recall those found in other higher ruminants. ß 2013 Elsevier Masson SAS. All rights reserved.

Keywords: Hoplitomerycidae Ruminantia Phylogeny Miocene Central-Southeastern Italy

1. Introduction 1.1. Original classification of Hoplitomeryx 1.1.1. Horncores, lacrimal orifices, and metatarsals On the basis of only two features, Leinders (1983) classified the Hoplitomerycidae, i.e., the weird Ruminants from Scontrone (Abruzzo, central Italy) and Gargano (southeastern Italy) (Fig. 1), in the Cervoidea. Like cervids, but also like antilocaprids, Moschus, and some palaeomerycids, hoplitomerycids possess two lacrimal orifices and closed metatarsal gulleys. For this reason, Leinders (1983) considered Hoplitomerycidae as the sister family of Cervidae, linking them more closely to the Cervidae than to the Bovidae, the same as Leinders (1979) and Leinders and Heintz (1980) had done with Antilocapridae. Hoplitomericids, however, do not possess the most characteristic feature of cervids: antlers. Their cranial appendages are unbranched and have a heavily ridged texture; they never show burrs, nor have naturally shed cranial appendages. Hence, Hoplitomeryx Leinders, 1983, had unbranched, non-deciduous horns, covered by an unbranched, non-deciduous keratine sheath. These cranial appendages are therefore the opposite of antlers, and are quite similar, in contrast,

§

Corresponding editor: Giorgio Carnevale.

E-mail addresses: pmazza@unifi.it, [email protected] 0016-6995/$ – see front matter ß 2013 Elsevier Masson SAS. All rights reserved. http://dx.doi.org/10.1016/j.geobios.2012.10.009

to bovid horns (Leinders, 1983; Janis and Scott, 1987). To explain this oddity, Leinders (1983) proposed parallel evolution within the Cervoidea. The cranial appendages of Hoplitomerycids are actually quite baffling also for other aspects. Unlike true bovids, hoplitomerycids were said to possess a full set of five horns, i.e., two pairs of suprapostorbital frontal appendages and a single median nasal horn (Leinders, 1983). This very distinctive characteristic, however, is not present in the type skull of Hoplitomeryx matthei Leinders, 1983, RGM 260.965 (Fig. 2(A)), which still preserves the two paired orbital horns, but shows no scar, rugosity or any other sign proving the former presence of the nasal horn core, nor did Leinders (1983) mention any evidence of this kind in his original description of the specimen. Five horncores are present only in the fragmental skull roof RGM 260.944 (Fig. 2(B,C)), which is also assigned to Hoplitomeryx matthei. RGM 260.944 is actually a compilation of two different skull fragments, i.e, nasal bones bearing an unpaired horn, and a fragmental forehead with paired orbital horns. The two fragments are glued together, but the fracture margins between them do not fit. Moreover, the two specimens seem to be fossilized somewhat differently. Mazza and Rustioni (2008) challenged the originality of this specimen, supposing it to be an artificial reconstruction, hence questioning the supposed association of five horns all in one animal. Freudenthal and Martı´n-Sua´rez (2010: p. 97) replied that ‘‘. . . the material was extracted from a small block of matrix and the fragments fitted perfectly. Unfortunately,

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Fig. 1. Map showing the location of the sites of Scontrone and Gargano. Scale bar: 100 km.

at the time, the Leiden Museum had a new and not yet expert preparator; the specimen became damaged, but there can be no doubt on its authenticity: the lateral horns on skull RGM 260.944 and the nasal horn belong to one single individual’’. 1.1.2. Sabre-like upper canines Hoplitomerycids possess also large sabre-like upper canines of moschid type. Scontrone and Gargano yielded many isolated sabre-like canines; two fragmentary maxillary bones from Gargano (RGM 260.951 and RGM 260.941), which are kept in the Museum of Leiden, still preserve such teeth in place. The association of cranial appendages with large upper canines in Hoplitomeryx has drawn the attention of ruminant specialists. Muntiacinae have upper canines matched with antlers mounted on long pedicles, but these cranial appendages are small, thus contributing to the opinion that the size of cranial appendages is inversely proportional to that of upper canines. The Miocene cervids Pliocervus and Cervavitus have long upper canines associated with short antlers and short pedicles. Procervulus and Heteroprox are other Miocene cervids with long protoantlers and very large upper canines. Also, the Early Pliocene Procapreolus wenzensis has antlers similar to those of modern Capreolus associated with large upper canines (Lister et al., 1998), which however are considered not a primitive, but rather a derived character in the direction of the antlerless Hydropotes (Groves, 2007). Hassanin and Douzery (2003) stressed that males of Moschus and Hydropotes are armed with large upper canines but lack cranial appendages. Molecular analyses, reported both by Randi et al. (1998) and Hassanin and Douzery (2003), show that Hydropotes secondarily lost cranial appendages. Hassanin and Douzery (2003) suspect that the same occurred also in Moschus, which would have derived from a bovid-like ancestor with horns but without large upper canines. Also, protoceratid horns are associated with long upper canines, but although protoceratids imitate Pecorans in many respects, they are Tylopods (Janis and Scott, 1987). Supposed male palaeomerycids possessed long upper canines associated with giraffid-like, keratine-free cranial appendages. Hoek Ostende et al. (2009) assume a relationship between hoplitomerycids and palaeomerycids. Leinders (1983) believed

that hoplitomerycids developed their formidable set of weapons because of their insularity, to protect themselves against large birds of prey, an opinion apparently shared by Hassanin and Douzery (2003). Mazza and Rustioni (2011) revised the remains of Hoplitomeryx described by Leinders (1983), together with other cranial and dental material from Gargano and Scontrone. It is unfortunate that an unskilled preparator caused the loss of the crucial piece of evidence that could certify the genuinity of the skull roof RGM 260.944, which would prove that Hoplitomeryx is actually the only known five-horned ruminant (no past or living ruminant possesses five horns, not even the Rothschild Giraffe (Giraffa camelopardalis rothschildi), which has distinct, paired, hair-covered ossicones behind each ear, and a horn-like bump in the forehead region, which makes it appear having five horns). The cranial appendages in giraffes and hoplitomerycids are by no means comparable, neither structurally/morphologically nor topographically on the skull. Ossicones are unbranched, non-deciduous, and hair-covered, quite different from the horns of Hoplitomeryx. Moreover, the posterior paired ones issue from the frontal bone and nuchal crest, in a very backward position over the ear region; the unpaired anterior ossicone issues from the frontal bone as well. Hoplitomerycids, in contrast, have their paired horns towering over the orbital rims, and the unpaired nasal horn located at the rear end of the nasal bones. Although many skull fragments of Hoplitomeryx have been recovered over the past years in Gargano and Scontrone, not a single one bears solid evidence of the alleged five horns. Awaiting to find a complete skull-roof of Hoplitomeryx, Mazza and Rustioni (2011) supposed the existence of distinct single- and pairedhorned Hoplitomeryx species, and perhaps even hornless representatives. In this perspective, Hoplitomerycidae would have radiated so widely to generate more than a single genus, or maybe even more than a single family. In the whole sample they analyzed, Mazza and Rustioni (2011) could not find any evidence bearing out the supposed coexistence of five horns and saber-like upper canines. None of the horned specimens shows the alveoli of these teeth. Protoantlers, antlers and giraffid ossicones are indeed found associated with large upper

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Fig. 2. A–C. Prominent skulls of Hoplitomeryx matthei mentioned in the text. A. Hoplitomeryx matthei (RGM 260.965) holotype, right lateral view. Arrows indicate two lacrimal orifices. B, C. Hoplitomeryx matthei (RGM 260.944), dorso-lateral view. Arrow shows the margin between the two skull fragments that compose the specimen. D. Left tarsometatarsal. Arrow shows closed dorsal gully. Scale bars: 5 cm.

canines, but these cranial appendages are by no means comparable to the bovid-like horns of hoplitomerycids. Bovid-like horns, in contrast, are never associated with large upper fangs. Hence, as Hoplitomeryx would be the only ruminant ever known to have five horns, it would also be the only one to possess a combination of bovid-like horns and saber-like upper canines, another uniqueness of Hoplitomeryx. Mazza and Rustioni (2011) concluded that in Hoplitomeryx, like they are in all other ruminants, horns, in contrast to antlers and giraffid-like appendages, seem to be incompatible with large upper canines. 1.1.3. Horn use in Hoplitomeryx The behaviour supposed by Leinders (1983) to explain the high protection of Hoplitomeryx finds no correspondent in today’s ruminants and seems untenable. Ruminants, as all other polygy-

nous mammals, use their horns either for sexual display or for intraspecific confrontations. Intrasexual aggression typically differs between the sexes, with males coming into conflict over breeding opportunities and females over resources such as food and space. Horns are seldom used against predators and primarily for defending the offspring, in intrasexual competition for mates, or in social interactions by both sexes (Geist, 1966, 1967; Alvarez, 1990; Locati and Lovari, 1990). Moreover, predatory birds do not attack their victims directly at the throat. When assaulting a victim exceeding its own size, a predatory bird lands on the victim’s back or hind quarters, rides it until it falls from exhaustion, and only then finishes it off by striking the back of the head or ripping the throat, when the victim is totally helpless (Wiley and Bolen, 1971). Horns are totally ineffective against such predatory tactics. Rather than for defence, the structure of the nuchal area in Hoplitomeryx

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suggests a different use of the horns. The arrangement of the occiput, with its condyles and foramen magnum inclined obliquely downwards and backwards together with its quite prominent nuchal crest, indicates that the animal bore its head uplifted and had fairly strong neck muscles. These anatomical characters, matched with the few cervical vertebrae we know about, indicate a fairly mobile neck. It seems that Hoplitomeryx could freely swoop down its head and swing it laterally. This suggests movements similar to those of extant giraffes in male conflicts: the rivals bludgeon each other, swinging their necks and striking into each other’s torso. If so, the horns of hoplitomerycids might therefore be related to confrontations between males. This would explain the use of the laterally projected orbital horns. 1.1.4. Controversies in the classification of Hoplitomeryx Phylogenetic relationships of even-toed ungulates have been proposed by numerous authors using either morphological (e.g., Webb and Taylor, 1980; Janis, 1987; Janis and Scott, 1987, 1988; Gentry and Hooker, 1988; Webb, 1998) or molecular data (e.g., Hassanin and Douzery, 2003; Marcot, 2007), or both (e.g., Herna´ndez Ferna´ndez and Vrba, 2005), often with conflicting results. In their most influential paper on the interrelationships of higher ruminant families, Janis and Scott (1987) substantially followed Leinders (1983), classifying hoplitomerycids in the Cervoidea (Janis and Scott’s Eucervoidea), alongside Antilocapridae, Palaeomerycidae and Cervidae. Janis and Scott (1987) acritically accepted Leinders’s (1983) original description of Hoplitomeryx and of Hoplitomerycidae, which is most detailed on cranial features, but very sketchy, or sometimes even inaccurate, on dental and postcranial traits. Whereas Leinders (1983) supposed that Amphimoschus could be a potential ancestor of Hoplitomeryx, Janis and Scott (1987) accommodated Amphimoschus in the Hoplitomerycidae. More recently, Amphimoschus has been placed near the origin of Bovidae (Solounias, 2007). Hassanin and Douzery (2003) disagreed about placing hoplitomerycids within Cervoidea, finding that the double lacrimal orifice and the closed metatarsal gully are highly variable characters, which can be found in taxa other than cervids. Moschus, for instance, may possess either one or two lacrimal orifices, together with either open or closed gully on the dorsal side of metatarsal III/ IV. Hassanin and Douzery (2003) could not find any evidence of parallel evolution of bovid-like horns and concluded considering Hoplitomerycidae closer to Bovidae than to Cervidae, though admitting that the presence of four or five horns actually distinguishes Hoplitomeryx from most bovids. 1.2. Aims of the study Mazza and Rustioni’s (2011) detailed description of the dental features of hoplitomerycids permits a reappraisal of the relationships of this still poorly known taxon. This improved knowledge helps clarifying many doubtful and even contradictory concepts on the interrelationships and systematic position of this family. Contributing to a more accurate classification of Hoplitomerycidae is the intended task of the present study. A cladistic analysis is performed based on a combination of cranial, dental and postcranial characters of hoplitomerycids, set against those of past and living artiodactyls. The works of Webb and Taylor (1980), Janis and Scott (1987), O’Leary and Geisler (1999), Hassanin and Douzery (2003), Geisler et al. (2007), and Me´tais and Vislobokova (2007) form the background knowledge to the investigation, providing also the necessary input to the discussion of the findings from this study. The results confirm the faraway phylogenetic origin of hoplitomerycids and show how much the superficial knowledge of these animals weighed on their misclassification.

2. Analized characters and methods Janis and Scott (1987) proposed a classification of the ruminants based on a list of characters. Referring to those characters, which will be reported enclosed in square brackets, hoplitomerycids show the following suite of features:  mesostyles in upper molars and ectostylids in lower molars [1a];  traces of a mesial cingulum on lower molars [2b];  unbranched, non-deciduous horns with unbranched non-deciduous keratin sheath [7b];  double lacrimal orifice [9];  sabre-like ‘‘moschid’’-type upper canine [11b];  brachyodont cheek teeth [12a] (hoplitomerycids include also mesodont representatives, but this character was not contemplated by Janis and Scott, 1987);  cingulum absent on upper molars [13c];  protocone in P3 centrally-situated and lingually-directed [14b];  incipient entostyle in upper molars [15a];  generally small metastyle in upper molars [16b];  large P4 metacone [17a];  large M3 metaconule [18b];  presence of metastylids in lower molars [21];  complete postentocristid in lower molars [22b];  vertical groove on posterolingual region of p4 [25];  double distal lobe either closed [26a] or partially opens [26b] distally on m3;  complete distal metapodial keels [27];  closed metatarsal gully [28b];  side toes completely lost [29c].

2.1. Cranial characters Cranially, hoplitomerycids are most characterized by their horns, but also by their two lacrimal orifices. The supposed five horns do not have the same weight than all the other features: they are so exclusive to have the potential to draw the family out obscuring any relationship based on other traits. For this reason, and because of the uncertainties described above, the character ‘‘number of cranial appendages’’ has been excluded from the analysis. Janis and Scott (1987) accommodated the hornless Amphimoschus in the Hoplitomerycidae because of its cranial and dental affinities with Hoplitomeryx, but Amphimoschus is now considered near the origin of Bovidae (Solounias, 2007), as mentioned above. Hence, hoplitomerycids and bovids must be somehow related to one another. The double lacrimal orifices have been considered one of the most distinctive traits of the cervoid ruminants. Janis and Scott (1987), however, advise that this character should be used with caution. Actually, two lacrimal orifices are not exclusive of Cervoidea, as they are also possessed by some bovids (Bovini and Tragelaphini), as well as antilocaprids and palaeomerycids. 2.2. Dental characters Dentally, Hoplitomeryx mixes derived pecoran characters (e.g., moschid-type upper canines, the absence of a Palaeomeryx fold already in the brachyodont representatives of the genus, the complete postentocristid, the incipient entostyle in the mesodont cheek teeth, the absence of cingula on the upper molars) with other more primitive traits (e.g., the lack of an entostyle on the brachyodont upper molars, the weak to absent labial rib of the metacone, the presence of a still reduced metastyle in upper molars, the large metacone in P4, p4 with well-developed

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metaconid, the presence of metastylid and ectostylid in lower molars). Janis and Scott (1987) write ‘‘Amphimoschus, unlike Hoplitomeryx, has [. . .] the retention of p2 and a strongly developed [. . .] ectostylid’’. They also affirm that increasing hypsodonty leads to the loss of entostyle and ectostylid. In contrast to Janis and Scott’s statement, the Scontrone specimens show that older hoplitomerycids do retain p2 (Mazza and Rustioni, 2011). Moreover, the present analysis shows that small entostyles are present in the relatively higher-crowned, mesodont species H. apruthiensis and H. magnus, and that ectostylids may be variably developed, from very robust (e.g., H. falcidens, H. magnus, H. minutus) to tiny (e.g., H. apruthiensis, H. apulicus, H. matthei), with no apparent relation to crown height. Hoplitomerycids share a number of dental characters with several other ruminants: the large metaconule in M3 characterizes also the giraffoid Propalaeoryx, as well as Antilocapridae; the vertical groove in the posterolingual region of p4, plus the metastylids of the lower molars, can be observed in Giraffinae and Sivatheriinae; the centrally-situated and lingually-directed protocone is also found in Bovidae. With giraffoids, hoplitomerycids share strong metastylids. Hoplitomerycids have a distinct bi-lophed posterior lobe in m3. Janis and Scott (1987) observe that it is ‘‘a unique feature among the Pecora’’ and state that this same character is observed in most dromomerycids, in Parablastomeryx, possibly in Prolibytherium, and also in Zarafa from Gebel Zelten, as well as in living giraffid species. Gobiomeryx adds a distinct entoconulid in m3 (Me´tais and Vislobokova, 2007), and a bi-lophed m3 is also present in Amphimoschus, but Janis and Scott (1987) include this genus in the Hoplitomerycidae, as mentioned above. Janis and Scott (1987) assert that the distal margins of the two cristids are not fused in hoplitomerycids (their character 26b), as opposed to all other possessors of bi-lophed third lower molars in which the two cristids are distally fused together (their character 26a). This, however, is not correct: the two cristids remain unfused only in H. magnus and rarely also in H. matthei and H. apulicus. In the other species, the two lophs do not meet only in unworn or poorly worn third lower molars, whereas they do fuse as wear progresses. Hence, in hoplitomerycids this character is changing from one state to another, the family indisputably deriving from an ancestor with fused distal cristids.

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On the basis of the evidence seen so far, hoplitomerycids are dentally reminiscent of the Paleogene Archaeomerycidae and Leptomerycidae, but also, and more convincingly, of some Gelocidae, such as Prodremotherium and Gobiomeryx. Similarities include the low-crowned dentition, the presence of parastyle and mesostyle, the weak to absent labial rib of the metacone, the absence of upper cingula, the retention of the paraconid, and p4 with a well-developed metaconid. With Prodremotherium and Gobiomeryx, hoplitomerycids also share the entostyle, metastylid, ectostylid, p4 with strong metaconid, as well as the lack of the ‘‘Palaeomeryx fold’’ and ‘‘Dorcatherium fold’’. Strong metastylids are also possessed by giraffoids. 2.3. Postcranial characters The suite of taxonomically most significant postcranial features shown by hoplitomerycids includes the astragalus with not parallel trochleae (Fig. 3), the closed metatarsal gully (Janis and Scott’s character [28b]), the complete distal metapodial keels [27], and the side toes completely lost [29c]. Archaeomerycids and leptomerycids also possess non-parallel sided astragali, but hoplitomerycids may have likely developed such a feature independently, living over the rough terrains of their homeland. Quite more significant is the closed metatarsal gully (Fig. 2(D)), which is considered one of the most typical characters of Cervoidea. Closed metatarsal gullies, in contrast, are possessed also by: Tragulus and the living Hyemoschus (Tragulina); Eumeryx and Prodremotherium (Gelocidae); Walangania, Dremotherium, Blastomeryx, Parablastomeryx, Moschus, and Micromeryx (Moschina of Webb and Taylor, 1980, or Sinecornua of Bubenik, 1990); Sivatherium (primitive giraffid: Geraads, 1996); Antilocapridae (Bovoidea according to Matthew, 1904; Pilgrim, 1941; Stirton, 1944; Simpson, 1945; Romer, 1966; Gentry and Hooker, 1988; Vislobokova, 1990; Bovidae for O’Gara and Matson, 1975; Antilocapridea for Thenius, 1969; Cervoidea according to Leinders and Heintz, 1980; Ginsburg, 1985; Janis and Scott, 1987; Gentry, 2000); and most Palaeomerycidae. 2.4. Character-taxon matrix Of the array of characters listed by Webb and Taylor (1980), Janis and Scott (1987), O’Leary and Geisler (1999), Hassanin and

Fig. 3. Astragali of Hoplitomeryx. A, B. Specimens from Scontrone. C–J. Specimens from Gargano. Scale bars: 5 cm.

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Douzery (2003), Geisler et al. (2007), and Me´tais and Vislobokova (2007), only those that can actually be observed in the hoplitomerycid material currently available has been selected for the study. Hence, there are no missing characters (‘‘-’’ in Table S1; features that are not preserved or whose state is unclear are indicated by a ‘‘?’’ in this supplementary table) for hoplitomerycids in the character-taxon matrix used for the analysis. A few new characters or character states have been added, which were not considered in the cited studies. This led to the scoring of 121 features: 48 cranial, 51 dental and 22 postcranial characters, which have been analyzed to infer the interrelationships between Hoplitomerycidae and an ingroup of 12 past and six living ruminant taxa (the character-taxon matrix and its legend are provided as supplementary materials and are available as an electronic appendix to this study; see Tables S1 and S2). Excluding hoplitomerycids for the reasons explained before, the missing characters range from 0.8% to 6.6% (average 2.2%). Binary characters are dominant (88, i.e., 73%), whereas 33 (27%) are multistate. Trees were rooted with Diacodexidae and Leptictidae as outgroup. These taxa did not have state 0 for every character already in the original matrices contained in the papers cited above. All characters have been equally weighted. Twelve characters are ordered; these were drawn from Me´tais and Vislobokova (2007; their characters 37, 38, 42, 51, 55, 58, 61, 70), O’Leary and Geisler (1999), and Geisler et al. (2007) (the same ordered characters are numbered differently in the last two papers: 52 = 121, 53 = 117, and 60 = 114, respectively), hypothesizing the hierarchical transformations already supposed by the authors. Ordered features sum up to 9% of the total analyzed characters. This has been the only constraint applied on the analysis. Because using ordered features introduces preconceived hierarchy to morphological changes, analyses have been performed both including and excluding ordered characters. It is well known that the astragalus is one of the most characterizing bones of arctiodactyls. Basalmost ruminants, e.g., Diacodexidae, Leptictidae, Hypertragulidae, Praetragulidae, Leptomerycidae and Archaeomerycidae, notoriously have a non-parallel-sided astragalus, in contrast to more advanced Pecora, over the level of Tragulidae (Janis and Scott, 1987), in which the bone is parallel-sided. Yet protoceratids, the present-day Tragulus and Hyemoschus, but also suids, besides ruminants, have an asymmetric astragalus. An astragalus with non-aligned trochleae is possessed also by the endemic Hoplitomerycids and Miotragus of the Balearic Islands. The exclusive occurrence of non-parallelsided astragali in earlier representatives in contrast to the two alternatives in later taxa, indicates that the former is the plesiomorphic condition of the bone, whereas more recent, nonparallel-sided astragali likely result from secondary convergence. Van der Geer (1999, 2005) supposed that, by reducing their size because of their living on islands, hoplitomerycids developed a larger abdomen. Hence, their hindlimbs deviated outwards causing the deformation of the astragali, which became asymmetrical. Yet not all hoplitomerycids were tiny: the lengths of their astragali, for example, range from 1.7–1.8 to 4.2–4.6 mm, suggesting that the largest known hoplitomerycids approximated the size of a present-day fallow deer. This seems ruling out van der Geer’s (1999, 2005) hypothesis of an enlarged abdomen. Nonetheless, all the astragali of hoplitomerycids, including the largest ones, from both Scontrone and Gargano, are non-parallel-sided. This suggests either that their unique astragalus helped hoplitomerycids bound over the rough terrain of the insular settings where they lived, or that it may actually be an ancestral reminiscence, in the hypothesis that the stock from which these odd ruminants derived colonized the Abruzzo-Apulian land before the separation of higher ruminants. Because of this uncertainty, analyses have

been performed both including and excluding this trait of the astragalus to test how central this bone is to establishing the relationships of hoplitomerycids with the other analyzed ruminants. The character-taxon matrix was analyzed by using the heuristic search algorithms in PAST 1.99 (Hammer et al., 2001). Nonpreserved characters are distinct from inapplicable character states; nonetheless both have been treated as missing by PAST. All searches were heuristic, using 100 reorderings, 1000 bootstrap replicates, tree-bisection and reconnection (TBR) branch-swapping, random addition sequence, and exclusion of uninformative characters. Fitch optimization was performed. All tree lengths reported are calculated in PAST 1.99. The character-taxon matrix has been subjected to maximum parsimony analysis using the following parameters:    

run run run run

1, 2, 3, 4,

both ordered and astragalus features included; ordered features included, astragalus excluded; ordered features excluded, astragalus included; both ordered features and astragalus excluded.

3. Results In all four runs (Fig. 4), the clade formed by Hypertragulidae and Praetragulidae (i.e., Hypertraguloidea) is sister taxon to all other Ruminantia. Within the latter, a clade including Achaeomerycidae and Lophiomerycidae is sister taxon to the rest of the families analyzed here. Run 1 (Fig. 4(A)) produced 13 most-parsimonious trees of 260 steps each (consistency index CI = 0.5903, retention index RI = 0.9420). The clade of Achaeomerycidae and Lophiomerycidae is followed by Tragulidae, Leptomerycidae, Bachitheriidae, Gelocidae, and Pecora. Within Pecora, Giraffoidea (Giraffidae and Climacoceridae, i.e., Cantumeryx, Zarafa, Climacoceras, Nyanzameryx) is sister taxon to Antilocapridae, Hoplitomerycidae, Bovidae, Cervidae, Palaeomerycidae, and Moschidae. Hoplitomerycids therefore stem between Antilocapridae and Bovidae. Removing the astragalus features and maintaining the ordered characters (run 2) gives 11 most-parsimonious trees of 257 steps each (CI = 0.5957, RI = 0.9437; Fig. 4(B)). Sister taxa of Achaeomerycidae and Lophiomerycidae are now Tragulidae and all other families. Leptomerycidae and Bachitheriidae stem between Tragulidae and Gelocidae, and the latter are the sister group of higher ruminants, which include two separate clades: one formed by Cervidae, Moschidae and Palaeomerycidae, the other by Bovidae, Antilocapridae, Hoplitomerycidae, Giraffidae, and Climacoceridae. Hoplitomerycids now stem between antilocaprids and giraffids. Run 3 (Fig. 4(C)), in which ordered characters are removed, maintaining the astragalus features, gives 17 trees of 240 steps each (CI = 0.5940; RI = 0.9452). Tragulidae are the sister taxon of two clades, one represented by Gelocidae, Leptomerycidae, and Bachitheriidae, the other by higher ruminants. Hoplitomerycidae follow as sister group of two more clades, one formed by Bovidae, Cervidae, Moschidae, and Palaeomerycidae, the other by Antilocapridae, Giraffidae, and Climacoceridae. The removal of both ordered and astragalus characters (run 4) produces 13 trees of 237 steps each (CI = 0.5854; RI = 0.9470; Fig. 4(D)). The sister taxa of Achaeomerycidae and Lophiomerycidae are Tragulidae, Leptomerycidae, Bachitheriidae, Gelocidae, and Pecora. Giraffoidea (Giraffidae and Climacoceridae) are now the sister taxon of Antilocapridae, Hoplitomerycidae, Bovidae, Cervidae, Palaeomerycidae, and Moschidae. Once again, as in run 1, hoplitomerycids stem between Antilocapridae and Bovidae.

P.P.A. Mazza / Geobios 46 (2013) 33–42

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Fig. 4. Results of the cladistic analysis. A. Run 1, both ordered and astragalus features included. B. Run 2, ordered features included, astragalus excluded. C. Run 3, ordered features excluded, astragalus included. D. Run 4, ordered features excluded, astragalus excluded. Heuristic searches with 100 reorderings, 1000 bootstrap replicates, treebisection and reconnection (TBR) branch-swapping, and Fitch optimization. See text for details.

4. Discussion and conclusions The parsimony analyses of 121 morphological characters from 13 extinct (hoplitomerycids included) and six extant higher-level artiodactyl taxa contradict the opinion, set off by Leinders (1983), and perhaps too acritically accepted in the following years with only rare exceptions (e.g., Hassanin and Douzery, 2003), that among Ruminantia, Hoplitomerycidae are more closely related to cervoids. Actually, three of the four alternative results from the cladistic analyses performed here group hoplitomerycids with bovids and antilocaprids (runs 1 and 4), or with giraffids (run 2), whereas the fourth, i.e., the one (run 3) without ordered features

and with the astragalus traits maintained, shows hoplitomerycids as the stem taxon to the higher ruminant clades. The run 1 and run 4 tree topologies are fairly similar: in both, hoplitomerycids stem between bovids and antilocaprids. Yet both trees were obtained using opposite character-taxon matrices: ordered characters and the astragalus features are either included or excluded, respectively. The run 4 tree was found removing the non-parallel sided astragalus of hoplitomerycids from the charactertaxon matrix used for run 3. The run 3 result is in line with Mazza and Rustioni’s (1996, 2008, 2011) opinion that hoplitomerycids are related to a stock of basal ruminants that established in the AbruzzoApulian land some time before the birth of higher ruminants.

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4.1. An origin far-away in time? Solid geological evidence confirms that at 29 Ma the AbruzzoApulian platform was connected with the Balkans across the Adriatic Sea, approximately where now are the Tremiti islands (Patacca et al., 2008). Soon after, the connection sank and the Abruzzo-Apulian land remained cut out from the mainland for several million years. Mazza and Rustioni (1996, 2008, 2011) believe that the ensuing vicariant isolation led to the endemization of the new residents, which diversified developing a range of homoplasies with bovids, antilocaprids, giraffids, and cervids. The simple presence/absence of the non-parallel-sided astragalus of hoplitomerycids in the character-taxon matrix used here was sufficient to change the tree topologies from those produced by runs 1 and 4, into the one found by run 3. Hence, including or excluding ordered characters makes no substantial difference: only the asymmetrical astragalus seems to play a key-role in classifying Hoplitomerycidae. Deciding whether the nonparallel-sided astragalus is rather a plesiomorphic or an autoapomorphic trait is a matter of opinion. It is a fact, however, that hoplitomerycids diversified extensively, generating a variety of larger- and smaller-sized species, either brachyodont or mesodont, which demonstrates that they occupied several different niches. In spite of this, all hoplitomerycids have nonparallel-sided astragali. If a character is shared so widely, it must have been inherited by a common ancestor, rather than being an autoapomorphic acquisition. For this reason, hoplitomerycids are here believed to be ruminants of archaic origin, which developed a full range of homoplasies with many other higher ruminants by living in isolation on the protected Abruzzo-Apulian recess. They are very difficult to place in the pigeonholes of established classifications, such as those proposed by Leinders and Heintz (1980), Webb and Taylor (1980), Moya´-Sola´ (1986, 1988), Groves and Grubb (1987), Janis and Scott (1987, 1988), Carroll (1988), Vislobokova (1990), Gentry (2000), Janis (2000), Hassanin and Douzery (2003), Herna´ndez Ferna´ndez and Vrba, 2005 and Prothero and Foss (2007 and articles therein). In fact, the array of characters they show permits to classify them indifferently well as bovids, cervids, antilocaprids, giraffids, or even palaeomerycids. 4.2. Hoplitomerycids, highly improbable Cervoids The ruminant family Hoplitomerycidae was originally based on the single species Hoplitomeryx matthei by Leinders (1983). The author linked the family more closely to the Cervidae than to other ruminants because of its possessing of two lacrimal orifices and closed metatarsal gulleys, and hence classified it within the Cervoidea. Despite Leinders (1983) had described almost exclusively the cranial features of hoplitomerycids, most later authors accepted quite acritically his classification. Mazza and Rustioni’s (2011) revision of the family and description of the dental and jawbone features, which Leinders (1983) had failed to analyze, led not only to the description of five new species, either brachyodont or mesodont and of considerably different size, but it also cast doubts on the appropriateness of classifying hoplitomerycids within the Cervoidea. Hoplitomeryx is surely not a cervid, because it lacks the paired, deciduous, branched frontal appendages typical of the members of that family. Leinders (1983) acknowledged this and suitably created the new family of the Hoplitomerycidae, in which to accommodate this genus. However, Leinders (1983) went a step too far, in my opinion, including this family in Cervoidea. This conclusion, in Mazza and Rustioni’s (1996) view, is disputable. And this is my position still today. Hoplitomeryx has a me´lange of characters:

 keratine-covered horns like bovids;  two lacrimal orifices on the orbital rim and rear cannon bones with distally closed gullies, like cervids;  a nasal horn core, which is not comparable, but which can be paralleled, to the unpaired forehead protuberance of Giraffa;  non-deciduous, unbranched, laterally compressed and fairly backward-bent horn cores;  teeth with styles(-ids) relatively more developed than in cervids;  humeri with deep trochlear troughs;  and cannon bones with flat volar surfaces, like giraffids (Ginsburg and Heintz, 1966). Like cervids, bovids and giraffids, hoplitomerycids have small, roundish anteorbital cavities. Like tragulids and Late Oligocene gelocids, Hoplitomeryx shows a tendency towards the fusion of the tarsal elements, although this might be a consequence of its living on rough insular settings. Like bachitheriids, hoplitomerycids have the orbits placed relatively distally, with their mesial border situated above M2. 4.3. Convergence of geological and paleontological evidence Geological evidence ascertains that a land bridge crossed the Adriatic Sea at 29 Ma (Patacca et al., 2008). Mazza and Rustioni (2008) claim that this land bridge was the most parsimonious and reasonable way the ancestors of Hoplitomerycidae could use to reach the Apulian Platform from the Balkans. If so, this represents a very strong chronological constraint in any search for the ancestry of this peculiar group of ruminants. The land bridge then gradually sank and the connections between the Apulian Platform and the Balkans progressively dropped until 14 Ma, when the AbruzzoApulian land was finally isolated. By then, the hoplitomerycids attained their peculiar endemic characters. The ancestral stock of colonizers radiated, diversifying widely and originating several species, similar morphologically to one another, but quite different in size and proportions. Each was likely the result of the adaptation to a variety of sub-environments, which indicates that the Abruzzo-Apulian Platform had high habitat heterogeneity. Hoek Ostende et al. (2009) sketch a thoroughly different story. Their reconstruction is based on the fact that hoplitomerycids derived from some palaeomerycid representative that swam across the Adriatic Sea, without the need of any land bridge, i.e., later than the 29–14 Ma interval. This interpretation is untenable for a number of reasons, I cite only three:  hoplitomerycids, for reasons detailed above, are not related to palaeomerycids;  a later incomer would have been some higher ruminant, because after the 29–14 Ma time period the major lines of higher ruminants had already diverged;  a land bridge, whose existence is attested to by very solid geological evidence (Patacca et al., 2008), is a far more parsimonious and realistic way of immigration than sweepstake swimming. Cervids have often been hypothesized swimming through the sea to reach islands (Macpherson, 1981; Held, 1989a, 1989b; Serjeantson, 1990; Masseti and Zava, 2002; Reimchen et al., 2003; Brown, 2005a, 2005b; Crouchley et al., 2007; Godwin, 2008; Leslie, 2009). Their supposed swimming performances, however, seem rather overestimated. Empirical observations attest that deer can swim up to a maximum of about 7 km (Whitehead, 1993). In my opinion, it is far easier for a land mammal to cross a land bridge than to be disposed to venture into an environment so different from that of life.

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From all of this, hoplitomerycids can be thought having a quite ancient ancestry. Such an assumption is in line with Mazza and Rustioni’s (1996, 2008, 2011) and Van der Geer’s (2008) conclusions. The latter author analyzed some of the characters of Hoplitomeryx mentioned by Mazza and Rustioni (1996), together with another set of features shared, or not, with other higher ruminants. She concluded (Van der Geer, 2008: p. 151) that ‘‘for the present, [. . .] Hoplitomerycidae indeed constitute a family on its own, as an early member of the Cervoidea. However, this is by no means certain, and also a lower phylogenetic position, as holdover of a primitive ruminant stock is possible (Mazza and Rustioni, 1996).’’ She also observed (Van der Geer, 2008: p. 149) that ‘‘Hoplitomerycidae [. . .] differ from [. . .] Palaeomerycidae by a nonmolarized lower p4’’ and ‘‘from Palaeomeryx von Meyer, 1851, by the absence of a lower p2 and the absence of pli-Palaeomeryx in lower molars.’’ The present cladistic analysis confirms that hoplitomerycids cannot be easily accommodated in any of the superfamilies of higher ruminants. In contrast, they bear characters that can easily place their ancestors somewhere at the basal divergence of Pecora, according to the classifications that enjoy a general consensus. In other words, the ancestry of hoplitomerycids can be traced back to the late Oligocene-early Miocene, i.e., to a time when artiodactyls underwent the strong phylogenetic instability and rapid diversification that gave birth to higher ruminants. Acknowledgments I thank the following people and institutions for giving me access to the specimens and collections under their care: A. Rossi and S. Agostini, of the Soprintendenza Archeologica dell’Abruzzo, Chieti, who administer the Centro di Documentazione ‘‘Hoplitomeryx’’ at Scontrone, L’Aquila; M. Freudenthal and L.W. van den Hoek Ostende, at the National Museum of Natural History Naturalis, Leiden. Many thanks to D. Ventra, who recovered some of the specimens from Scontrone, as well as to P.M. Rinaldi, who made some of the photographs. I am especially indebted to P. Melone, Mayor of Scontrone, for her long collaboration and assistance. I owe special thanks to both reviewers of the early version of the manuscript, I.A. Vislobokova and D.R. Prothero, but also to both editors, G. Carnevale and especially G. Escarguel, whose assistance greatly increased the quality of this study. This research was financially supported by PRIN (Research Projects of National Interest) 2009 MIUR (Ministry of Education, University and Research) grants. Appendix A. Supplementary data Supplementary data (Tables S1, S2) associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/ j.geobios.2012.10.009. References Alvarez, E., 1990. Horns and fighting in male Spanish ibex, Capra pyrenaica. Journal of Mammalogy 71, 608–616. Brown, D., 2005a. Secretary Island deer Eradication – Scoping document. DOC Southland Conservancy (unpublished). Brown, D., 2005b. A summary of responses to the Secretary Island deer Eradication – Scoping document. DOC Te Anau Area (unpublished). Bubenik, A.B., 1990. Epigenetical, morphological, physiological, and behavioral aspects of evolution of horns, pronghorns, and antlers. In: Bubenik, G.A., Bubenik, A.B. (Eds.), Horns, pronghorns, and antlers. Springer-Verlag, New York, pp. 3–113. Carroll, R.L., 1988. Vertebrate paleontology and evolution. W.H. Freeman and Company, New York. Crouchley, D., Brown, D., Edge, K.-A., McMurtrie, P., 2007. Secretary Island Operational Plan deer Eradication. Department of Conservation, PO Box 29, Te Anau, New Zealand.

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