Haldanodon exspectatus

Martin, Thomas, 2005, Postcranial anatomy of Haldanodon exspectatus (Mammalia, Docodonta) from the Late Jurassic (Kimmeridgian) of Portugal and its bearing for mammalian evolution, Zoological Journal of the Linnean Society 145 (2), pp. 219-248 : 241-243

LIFESTYLE OF HALDANODON EXSPECTATUS

Fossorial adaptations are rare among Mesozoic mammals, and they generally have rather unspecialized postcranial skeletons. Therefore for most taxa with known postcranium either a more scansorial [e.g. Henkelotherium, Eomaia and Sinodelphis ( Krebs, 1991; Vázquez-Molinero et al., 2001; Ji et al., 2002; Luo et al., 2003)] or more terrestrial [e.g. Repenomamus , Sinobaatar and Zhangheotherium ( Hu et al. 1997, 1998, 2005; Hu & Wang, 2002)] lifestyle is assumed. A stout humerus with prominent deltopectoral crest and comparatively wide distal end has been interpreted as fossorial adaptation in a Cretaceous and two early Palaeogene taeniolabidoid multituberculates ( Miao, 1988; Kielan-Jaworowska, 1989; Kielan-Jaworowska & Qi, 1990). A remarkable exception is the recently described Late Jurassic basal mammal Fruitafossor windscheffeli with strong fossorial adaptations in forelimb and manus ( Luo & Wible, 2005) that are strikingly similar to those of modern scratch diggers and Haldanodon . Due to the incomplete fossil record of early stem-mammals, particularly from the Middle Jurassic, it is difficult to say if these fossorial adaptations at least partially represent a retention of the plesiomorphic condition observed in many eucynodonts or a secondary specialization.

The humerus of Haldanodon , with its very broad proximal and distal heads and the enlarged trochanters, immediately evokes comparison with talpids (e.g. Talpa and Scapanus ) or monotremes ( Tachyglossus , Ornithorhynchus ). Based on these similarities, Krusat (1991) postulated a fossorial lifestyle for Haldanodon , and also referred to the wedge-like shape of the skull of Haldanodon which probably was used like a shovel lifting loose soil away over its back.

In talpids (e.g. Talpa , Scapanus , Galemys , Desmana ) and the chrysochlorid Amblysomus hottentotus the scapula is strongly elongated and narrow which is interpreted as an adaptation to their fossorial lifestyle ( Reed, 1951: 539). The scapulocoracoid of Haldanodon only with limitations can be compared to the scapula of therian mammals. However, it exhibits a striking similarity to the scapula of the Oligocene palaeanodont Xenocranium ( Rose & Emry, 1983) , even if the relevant structures may not be homologous. In the Xenocranium scapula, apart from the scapular spine, a ‘secondary spine’ at the posterior margin of the scapular blade is developed, that functionally corresponds to the laterally bent posterior margin of the Haldanodon scapula. A ‘secondary spine’ characterizes also the scapula of digging xenarthrans and some fossorial rodents such as the Spalacidae ( Gambaryan, 1960; Lehmann, 1963). Compared to the fossorial monotreme Tachyglossus , the scapulocoracoid of Haldanodon appears rather long and narrow; it more closely resembles in shape the scapulocoracoid of the semiaquatic and semifossorial Ornithorhynchus , but has a shorter wing-like posterior extension at the dorsal side. Fossorial talpids and Tachyglossus and Ornithorhynchus have an oval glenoid facet limiting the movements of the humerus. In the semicursorial Sorex the glenoid fossa is a segment of a spherical surface and allows movements of the spherical head of the humerus in all directions ( Reed, 1951: 536). The oval shape of the glenoid fossa of Haldanodon points to a fossorial adaptation.

The humerus of Haldanodon is very similar in shape and proportions to that of Tachyglossus and Ornithorhynchus . In Ornithorhynchus , the twist of the proximal and distal head is 90°, which is much greater than in Haldanodon and Tachyglossus . The humerus of Talpa , which is almost as broad as long with its greatly enlarged deltopectoral crest, represents an extreme fossorial adaptation, while Desmana and Galemys exhibit only moderate expansion of the deltopectoral crest and other muscle insertion planes.

The proximal humeral head of fossorial talpids, chrysochlorids (e.g. Amblysomus ), and palaeanodonts ( Epoicotherium , Xenocranium ; Rose & Emry, 1983) is elliptical while it is spherical in semicursorial soricids ( Reed, 1951). Haldanodon has an elliptical humeral head. This shape represents the plesiomorphic mammalian condition but also can be interpreted as an adaptation towards a fossorial lifestyle. Together with the oval glenoid facet a hinge-like shoulder joint is formed that limits the range of movement of the humerus to a mainly antero-posterior direction. This is typical for fossorial taxa. In specialized fossorial mammals such as monotremes and various fossil and extant therians that abduct their forelimbs during digging, the distal end of the humerus, and especially the entepicondyle, is strongly expanded ( Gambaryan & Kielan-Jaworowska, 1997: 33). Haldanodon also possesses an enlarged entepicondyle.

Like in talpids and chrysochlorids, which mainly use their front limbs for digging, in Haldanodon the humerus is considerably stronger than the femur. Therefore it can be postulated that Haldanodon mainly used its front limbs for digging and that the hind limbs fixed the body while burrowing (see below).

A large olecranon as present in the ulna of Haldanodon is another indicator for a fossorial lifestyle because it acts as in-lever of the triceps muscle. Hildebrand (1995) determined a range of relative length of the olecranon compared to the entire ulna length between 20 and 75% for fossorial taxa; the olecranon (with semilunear notch) of Haldanodon is 47% of the ulnar length and falls well within this range.

The very short first and second phalanges of Haldanodon are typical for scratch-digging mammals such as armadillos, fossil and extant pangolins (e.g. Manis javanica , Necromanis franconica ; Koenigswald & Martin, 1990), and palaeanodonts ( Epoicotherium , Xenocranium ; Rose & Emry, 1983). The two terminal phalanges which were found in association with other footbones and a maxilla of Haldanodon are pointed, only slightly curved and moderately laterally compressed. Morphologically, they resemble the claws of pangolins ( Manis ) except for the median slit that is not present in Haldanodon ; instead of the median slit, Haldanodon has a groove on each side of the claw for attachment of the horn claw. Manis is a typical scratch-digger ( Hildebrand, 1995), in contrast to Talpa which digs in soft soil and has broad and flattened terminal phalanges. All strongly fossorial talpids have bifid terminal phalanges, and ‘the grooved and bifid phalanx is an obvious adaptation for strengthening the union of phalanx and claw, and the distribution of this modification within the Talpidae is in correlation with the fossorial activities of the genera’ ( Reed, 1951: 556). Furthermore, in all fossorial talpids (except Uropsilus ; Reed, 1951: 555; further references therein) the claws of the hand are spatulate, which is a very characteristic feature and easy to recognize. The two claws of Gui Mam 132/74 are not spatulate (however, it is not possible to attribute them to a pes or manus), and among several hundred isolated probable mammalian phalanges from the Guimarota coal, which were recovered by screen-washing, no spatulate phalanges were been detected. This makes it very probable that the hand of Haldanodon was adapted to scratch digging rather than to the shovel digging style of Talpa and other fossorial talpids. The lateral and dorsal shapes of the terminal phalanges of Haldanodon correspond closely to those that are typical for fossorial small mammals as demonstrated by McLeod & Rose (1993) by eigenshape analysis. After McLeod & Rose (1993), fossorial taxa are distinguished by shallower (= dorso-ventrally compressed) ungual phalanges with a distinctive broadly curving dorsal margin and a relatively undifferentiated extensor tubercle.

The claws of the hands of Ornithorhynchus are moderately flattened (claws of feet are not flattened) and, like Haldanodon , have a groove on each side for attachment of the horn claw. In Tachyglossus the claws of hands and feet are flattened but have no median slit or lateral grooves.

Stout and comparatively short ilia that are strongly fused to a high number of sacral vertebrae are typical for fossorial mammals such as Manis and Tachyglossus . ( Hildebrand, 1995).

In talpids the hind legs are not used for digging, but for fixing the body when the soil is scratched loose with the hand. Nevertheless, digging adaptations are also evident in the shape of the femur, as the proximal end of the femur is wider and the three trochanters are more strongly developed in the talpids Scapanus and Neurotrichus than in the soricid Sorex ( Reed, 1951: 573) . The femur of Ornithorhynchus like that of Haldanodon has enlarged wing-shaped trochanters at the proximal head and a broad distal head. This is also in accordance with a fossorial and possibly semiaquatic lifestyle of Haldanodon .

Another adaptation for a fossorial lifestyle of Haldanodon is the short and comparatively stout tibia. A short tibia (and resulting short hind leg) is an adaptation towards powerful locomotion with a corresponding loss of speed, and the shorter hind leg can be manipulated more easily during burrowing ( Reed, 1951: 575). Therefore it can be concluded that Haldanodon most probably was a fossorial and possibly semiaquatic animal, comparable to the habits of Ornithorhynchus and desmans. This kind of lifestyle appears more suitable for the swampy environment of the Guimarota ecosystem ( Martin & Krebs, 2000; Kielan-Jaworowska, Cifelli & Luo, 2004) than that of a talpid with a permanent life in subterranean burrows as postulated by Krusat (1991).