Tuatara: Volume 14, Issue 3, December 1966
In New Zealand the Australian phalanger Trichosurus vulpecula is common, and the wallabies Protemnodon rufogrisea, P. eugenii, and Petrogale penicillata, although of restricted distribution, are readily available (Appendix). Since these animals offer valuable biological material and zoological textbooks devote little space to marsupials, the following supplementary notes have been compiled.
For many years marsupials were regarded as being relatively ill-equipped for modern conditions. This view largely resulted from the premature grouping of monotremes, marsupials, and placentals into the sub-classes Prototheria, Metatheria, and Eutheria*, with implied relative progression along a single line of evolution instead of specialisation along three divergent lines. The separation of placentals and marsupials (during some 50 million years of the Cretaceous) is largely unexplained, since the very small early mammals are represented almost exclusively by fossilised teeth and jaws, but palaeontological data can be supplemented by evidence derived from existing animals, and from the varying stages of viviparity found in modern reptiles.
* Simpson (1945) stated: ‘Although these terms have poor authority in the light of original definitions, they are so widely accepted and so generally understood in these [literal] senses that it would be puristic to reject them or to attempt to maintain their forgotten original significations.’ (Metatheria was originally a grade, not a sub-class). He recommended for existing mammals, sub-class Prototheria (Gill 1872), and sub-class Theria (Parker and Haswell 1897) containing the infra-classes Metatheria (Huxley 1880), Eutheria (Gill 1872), and the extinct Pantotheria (Simpson 1929). Vandebroek (1961) rejected Theria in favour of sub-class Eutheria in Gill's original sense (including the marsupials), with infra-classes Marsupialia (Illiger 1811) and Placentalia (Owen 1837). He raised Simpson's infra-class Pantotheria to a sub-class containing the orders Symmetrodonta, Dryolestoiidae, and Docodonta, on the grounds that these extinct mammals, according to tooth characters, formed a relatively homogeneous group, from which placentals and marsupials were excluded by their more advanced dentition.
Kermack (1963) also reverted to Gill's Eutheria, but on different grounds. Teeth had reached an advanced level even in the Upper Jurassic and, in taxonomy, it has been assumed that equal advance had been made in other mammalian characters; but examination of skull fragments indicated little change from the therapsid condition, and Kermack considered that the gap separating the marsupials and eutherians from the extinct orders was too wide to be bridged within one sub-class.
In the present paper Gill's specifications are followed for a third reason: placentals and marsupials have common reproductive features which are not shared by any other existing amniotes. Since it is not known whether the early mammals possessed these features or even whether they showed any degree of uniformity, the definition ‘therian reproduction’ is too vague to have any value.
Kermack pointed out that there is need for a term which distinguishes modern mammals, and ‘eutherian’ is the only one which does this. ‘Therian’ remains a useful designation for the wider group.
Since it is now uncommon for marsupials to be considered second grade placentals, they are here regarded as efficient and well adapted mammals. An alternative view in respect of reproduction has been presented by Sharman (1959a, 1959b, 1965a).
It is generally accepted that placentals and marsupials diverged from a common mammalian stock and it should be assumed first, unless contrary evidence is found, that each infra-class shares attributes which are a common inheritance, and secondly that each infra-class, under the compulsion of natural selection, would have evolved along its divergent path until each of its component species reached an optimum state of adaptation to its habitat. From this point rate of change would fall to a low level, but regression and advance would occur, within the limits set by natural selection, according to the differing requirements of species.
Adult anatomy and ontogeny give some indication of phyletic sequence, but the prototype of the sub-class requires to be defined before deductions can be made concerning the derived infra-classes.
Matthew (1904) suggested that progressive elevation of land accompanied by cold, arid, and highly variable climates led to the development of more active and adaptable land vertebrates, which by re-adaptation to a moist warm environment during the opposite page 107 phase of the climatic cycle, became the dominant types of new fauna in which survivors of the old tropical fauna had only a subordinate place.*
Unquestionably, a strong unidirectional selective pressure was applied to land vertebrates during the Mesozoic, since the Mammalia, which evolved during this era, are considered to be polyphyletic, with parallel evolution resulting from similar adaptations (Simpson 1959a). (The class would have been monophyletic within the Reptilia, but the advance to mammalian status appears to have been made independently by a number of reptilian groups (Simpson 1959b, 1960).
Olson (1959) and Brink (1963) stated that explanation of parallel evolution could be found in the advantage of speed — in movement, in the senses, and in metabolism — which could be sustained at a high level in either hot or cold climates only through endothermy.
Temperature regulation can be maintained by heliothermy, as probably occurred during the lower Permian in pelycosaurs such as Dimetrodon (Romer 1959), which could have facilitated both heating and cooling by exposure or orientation of the large dorsal fin; but in a cold climate such a system would be far less effective than endothermy. Although the results of the two forms of heat regulation (exothermy and endothermy) are in many respects similar, there is a fundamental difference between the two in that exothermy precludes the development of effective insulation. Heliothermic reptiles lack subcutaneous fat, and they store reserves in depots, usually in the abdominal cavity (Bogert 1949); not until endothermy had been achieved could fur, feathers, or subcutaneous fat be used for conservation of heat.
The pro-mammals almost unquestionably produced hairs which supplemented the reptilian scales and then replaced them by suppression, not by conversion (Spearman 1963). Associated with the pelage were sweat glands** which paved the way for development of mammary glands (Olson 1959).
* Dissension was expressed by Darlington (1959) who cited the abundance of tropical species as evidence of the tropics being the major region for evolution, but it is doubtful whether the tropics would have permitted strong selective pressure for the endothermic regulations of body heat which appears to have been essential for the evolution of mammals.
** Sweat glands would seem, superficially, to have constituted a cooling system, but this is unlikely. The Cretaceous mammals, from which recent therians evolved, appear to have been no larger than small rats, of a size too small in recent mammals (Schmidt-Nielson 1964) for toleration of the water loss required for cooling by perspiration. Sweat glands can be classed loosely as independent eccrine glands, or as apocrine glands and sebaceous glands associated with hair follicles. Eccrine glands in most mammals are restricted to paws or to bare surfaces where they maintain pliant skin texture. Their role of evaporative temperature reduction appears to be a late evolutionary trend, characteristic of man, in which they respond to heat as well as to emotional stress.
The apocrine glands have been considered the most primitive, because of their prevalence and their specialisations as scent, cerumineous (wax secreting) and mammary glands, but antiquity of both eccrine and apocrine glands is shown by their occurrence in primitive mammals (Weiner and Hellman 1960; Montagna and Ellis 1960; Montagna 1965). Sebaceous glands also had a probable early origin; Brink (1956) suggested that they were associated with vibrissae of the snout in the Permian cyanodont Diamodon.
Lactation was not of primary significance; the major reproductive advance of the Mesozoic was increased parental care (Romer 1959) and it is evident that milk would have evolved as a late consequence of this. But long association of mother and young is only one aspect of social behaviour, and nurture may have been either a cause or an effect of communal life.
Most of the existing species of mammals rely on scent for recognition, sexual attraction, trail marking and definition of territories. Urine and faeces are often utilised, but dermal scent glands (reviewed by Boulière 1954) are often of more than one type, and are most commonly used for recognition of individuals and their tracks. Such glands produce local concentrations of secretions held in hair, and it is possible that primitive aggregation of skin glands, of social importance, led on to lactation.
Milk would have consolidated an antecedent association of mother and young, increased potential growth rates, and permitted the birth of incompletely developed young, but it would not have induced a change from oviparity to viviparity.
Viviparity in present day lizards and snakes is an adaptation of cold-blooded animals, which has permitted extension of breeding range into cool climates (Weekes 1935), since free eggs are more subject to variations of temperature than are embryos or intra-uterine eggs, which benefit from the search for warmth or shelter by an active adult.
Weekes (1935) suggested that the relative failure of oviparous reptiles in the inland plain of south eastern Australia indicated desiccation of eggs by heat, but concluded that invasion of a hot dry area would not bring about viviparity. Neill (1964) largely agreed in this, and added that ovoviviparous snakes, because of adaptations, thrive in the arid south-western United States. He considered that, both in United States and Australia, viviparity among snakes and lizards was associated with descent from viviparous or viviparously adapted stock which expanded without competition from some advanced Old World species, which had been unable to cross either Bering Bridge or Torres Strait. He found viviparity in snakes often associated with ability to defend young, or with specialisation as for arboreal life or swimming. Evidence such as the repeated occurrence of oviparity and viviparity with the one genus page 109 led Weekes (1935) to conclude: ‘… that among reptiles placentation has arisen independently many times in the course of evolution, and that the phenomenon of parallel development of similar types of placentas is common.’ The evidence from reptiles indicates that viviparity probably appeared independently many times in the mammalian stock also, but it cannot be assumed that the earliest viviparous pro-mammals necessarily gave rise to the later therians; most probably they did not, because general advance seems more important in ultimate progress than specialisation of one character.*
Mammals and birds unquestionably evolved from reptiles, but they differ from all known reptiles in that they have not retained a completely double vaginal system. The abortion of the right side of the avian reproductive system and lack of reproductive function in the apparently full sized right oviduct of the monotreme (Wood Jones 1923) is commonly accepted as being a means of preventing the co-incidence of laterally placed large eggs in the restricted space of the pelvic girdle. Marsupials and placentals each give birth through a single vaginal passage, formed from union of the Müllerian ducts with infundibula which extends anteriorly from the cloaca. Such union has the same result as the unilateral suppression of birds and monotremes, but, while large therian embryos in a bipartite reproductive system could be subject to mutual obstruction during parturition, no such complications could occur in present day marsupials. It seems that either marsupial embryos were formerly of much larger relative size or that marsupials produced large hard-shelled eggs when they first developed a mammalian-type of pelvic girdle. Monotremes, by example, support the latter possibility, oviparity being retained until after mammalian status had been reached. The marsupial has a long-persisting shell membrane (Sharman 1959b), small amounts of albumen and yolk (Flynn 1938-39) and, in the embryo a vestigial egg tooth together with an ascending premaxilliary process which, by monotreme analogy, indicates the former presence of the caruncle for cracking a hard shelled egg (Hill and de Beer 1950). These features, absent from placentals, show oviparous affinities which suggest that the marsupials became viviparous later than the placentals, although it is equally possible that these functionless vestiges indicate only a slower rate of reduction in marsupials.
* This principle of mosaic evolution is illustrated by Docodon which, among Upper Jurassic mammals, combined the most advanced teeth with the most primitive jaw (Kermack 1963). Apparently highly efficient teeth permitted retention of archaic jaws. Possibly the metabolic rate had to rise before further improvement in mastication would have been of selective advantage.
In recapitulation: the Theria (or Eutheria) were advanced mammals before their separation into placentals and marsupials. Irrespective of viviparity in reptiles, the probable early development of endothermy would reduce the likelihood of viviparity in pro-mammals, and the change from the reptilian type of female reproductive system suggests that the therians approached mammalian status while they were still oviparous, since extant marsupials, with minute young, would have less need than reptiles for a single birth passage. Unlike that of exothermous reptiles, the breeding range of endothermic mammals would not long have been restricted by oviparity, but, on the limited evidence relating to snakes, cited by Neill (1964), viviparity could have resulted from arboreal life or from efficiency in the care of young.
A good deal of information is now available on the first mammals of the Upper Triassic, and on the relatively advanced ones of the Palaeocene, but between the two groups there is a gap of more than a hundred million years, a span of time considerably greater than from the Palaeocene to the present day (Kermack 1963). The Triassic mammals showed no division into placentals and marsupials, but in the Palaeocene the two groups were well established and already differentiated into lines which showed a long evolutionary history (Simpson 1929).
The placentals and marsupials of the Cretaceous were largely generalised; neither group being clearly separated into herbivores or carnivores. Most dentitions were of the piercing kind which we nowadays associated with an insectivorous diet, although some mammals possessed much broader crushing teeth of the kind we would now view as indicating an omnivorous diet. During the Palaeocene, the South American and Old World continental groups were separated. At that time placentals and marsupials seem to have represented a basic dichotomy of the main mammalian stock and to have been about equally progressive and adaptively efficient. Primitive forms of these two major branches apparently lived together in ecological equilibrium, and when carnivores evolved, there does not appear to have been any clash between placentals and marsupials as such; probably there was only marginal competition, with parcelling out of the various ecological zones which happened to receive different occupants (Simpson 1950). Placental carnivores page 111 became dominant in the Old World, and marsupial ones in South America. In the Miocene, when the Central American land bridge was re-established, unrestricted entry of the Old World mammals into South America did not result in selective discrimination between placentals and marsupials; the South American mammals as a whole were largely displaced by the invading placentals (Simpson 1950).
The South American marsupials have a relatively clear history, but in the Old World marsupials have been largely obscured by placental dominance. There the most successful marsupials were of the insectivore-like didelphoid stock, and Peratherium which was widely distributed and present in North America, remained in Europe until the Miocene (Simpson 1929). The southern limits of the Old World penetration by marsupials are uncertain. This may be due simply to lack of fossils, but the extent to which the Tethys Sea imposed a barrier is unknown (Ride 1964).
Marsupials probably entered Australia during the Palaeocene, and absence of early placentals is best explained by the sweepstake hypothesis which postulates one marsupial, or several, reaching Australia because of an improbable chance which did not fall to any placental however well endowed (Ride 1962; Simpson 1961). The hypothesis requires, instead of land bridges, island chains extending to Australia, either from Asia or from South America.
The northern route has been the one supported by most zoologists (Simpson 1961; Keast 1963) but it has not been established. Ride (1964) pointed out that the Torres Strait floral discontinuity, a subject of dissension among botanists (Keast 1963), is greater than would be expected from long term proximity of Australia and New Guinea. Further, the fossil marsupials so far found in New Guinea are late, of Upper Pliocene and Pleistocene, while the modern marsupials of New Guinea and the adjacent islands have a distribution that is entirely consistent with it being the product of alterations in Pleistocene sea level (Ride 1964). Continental drift and botanical evidence show with reasonable certainty that Australia reached its present latitude only during the late Tertiary, and that since the Mesozoic it has been moving slowly northwards across what is now the Southern Ocean (Ride 1964).
The fossil vegetation of Antarctica (Keast 1963) indicates a previously warmer climate for that continent, and unlike Asia, South America unquestionably could have provided migrant marsupials, although close affinity between America and Australasian marsupials has not been established.
The northern route to Australia would be the more likely one for an unspecified mammal, but the undoubted presence in Asia, during the early Tertiary, of such highly efficient short water-barrier crossers as Primates, Insectivora, Sciuromorpha, Hystricomorpha, etc. (Ride 1964), reduces the probability of successful migration by a page 112 marsupial which was not known to have been present. On available evidence, neither of the alternative routes can be rejected.
Marsupials have been placed in two sub-orders as Polyprotodonta and Diprotodonta, Didactyla and Syndactyla or Simplici-commissurala and Duplicommissurala. These classifications were each based on a single criterion and they were rejected by Simpson (1945). Ride (1962) showed that whereas dichotomous branching failed to indicate clearly defined taxa, dendritic branching could produce an unequivocal phylogeny. His illustration of this is reproduced in Figs. 1 and 2. The evolutionary sequence indicated would permit radiation of the Australasian marsupial from an ancestral marsupicarnivore type.
The traditional lumping of marsupials into one order implies an unwarranted degree of homogeneity in a group of animals which has evolved for just as long as have the placentals which are currently divided into twenty six orders. This was stated by Ride (1964) who raised Marsupialia to a super-order (corresponding to the infra-class of Vandebroek 1961) and divided it into the following orders:
Order 1: Marsupicarnivora Ride, 1964.
I. Didelphoidea, II. *Borhyaenoidea, III Dasyuroidea Families:
(III) 1. Dasyuridae, 2. Thylacinidae
Order 2: Paucituberculata Ameghino, 1894.
1. Caenolestidae, 2. *Polydolopidae
Order 3: Peramelina Gray, 1825.
Marsupialia incertae sedis Family Notoryctidae
Marsupials and placentals show evidence of descent from arboreal ancestors (Huxley 1880; Matthew 1904), but they differ in tending to modify the hallux or the pollex respectively for prehension.
* Taxa comprising extinct forms only.
Fig. 1: The sequence of morphological differentiation in the evolution of marsupial orders (from Ride 1964).
Specialisation of hind and fore limbs respectively suggests differences in locomotion. In most arboreal marsupials the grasping hind foot leaves the fore limbs free for manipulation of food or for fighting, but the firm stance suggests relatively slow progress in trees. The opposable pollex of the placentals also gives firm prehension, but it is functional during movement rather than when static, and lends itself to acceleration of progress by leaping or by brachiation.
Differences from the bones of placentals are slight and not readily explainable, but the epipubes are of some interest. Irrespective of the question of reptilian affinities, they are apparently associated with the pouch though they do not support it, and they are present in the pouchless males. They are hinged to the pubes, and so do not restrain the abdominal movement which results from elevation and depression of the diaphragm. They provide attachment for the pyramidalis muscles of the abdomen, for part of the external oblique, and, in some species, for part of the rectus abdominis. The cremaster, from the anterior superior iliac spine, bends around the epipubis and is inserted in the tunica vaginalis testis or spreads over the mammary glands at the back of the pouch, in the male and female respectively (Owen 1841; Barbour 1963). The epipubes are probably present in the male because their absence would require different arrangement of abdominal muscles in males and females. The same consideration would be relevant to pouchless marsupials.
The pouch in the Dasyuridae is exceptional in that it may open backwards or be absent, but never opens forwards (Troughton 1965). Epipubic bones are present in the pouchless forms but in Thylacinus they are only vestigial despite the presence of a pouch. Such reduction is apparently one of many convergences between Thylacinidae and the extinct and phyletically separated Borhyaenidae in which the epipubes are unknown (Ride 1964, and personal communication). The Thylacinidae and Borhyaenidae differ from the daysurid pattern in being large and carnivorous, and in being mainly cursorial. It appears that sustained pursuit and capture of large prey produced a selective force with which was not faced by the small pouchless dasyurids, and which was greater than that which maintained the epipubes and their supporting musclature.
Gregory (1951) listed the main skeletal features, which distinguish extant marsupials, largely as follows:
The dentary has an inflected angular process.
The jugal (malar) extends posteriorly, beneath the zygomatic process of the squamosal, to the glenoid articular surface, where it participates in forming the anterior limit for the movement of condyle of the lower paw.
The bony palate is usually fenestrated (in the adult).page 115
The auditory bulla, usually present, is formed by the alisphenoid instead of by the tympanic (except in Phascolomis [van Kampen 1905]).
The basisphenoid is pierced by paired foramina for the internal carotids.
The optic foramen of each side is fused with the foramen lacerum anterius.
The proximal ends of the nasals, as seen from above, are spreading.
The adult dental formula, excepting the Diprotodonta, is typically 5/4, 1/1, 3/3, 4/4 or a reduction of it, never 3/3, 1/1. 4/4. 3/3, or a reduction of this (except for Myrmecobius 4/1, 1/1, 3/3 5/6, with the total number ranging from 50-56 [Wood Jones 1923]).
The adult dental formula of the Diprotodonta is 3/1, 1/0, 3/3, 4/4 or a reduction of this. One or two vestigial lower incisors also may appear in the Phalangeridae.
The adult dental formula of the Notoryctidae is 4/3, 1/1, 2/3, 4/4 or a reduction of this.
Only premolars have deciduous precessors and only the posterior premolar is replaced by a permanent tooth. (Deciduous teeth of some marsupials are not known.)
In the vertebral column the atlas intercentrum of mammal-like reptiles is retained, and the centrum of the atlas forming the the epistrophus or odontoid of the atlas usually remains suturally separate from the axis.
The inferior arch of the atlas is often incomplete or cartilaginous in the mid-line.
Epipubic bones are usually present. They are vestigial in Thylacinus and unknown in Borhyaenidae.
The fibula sometimes bears a dorso-posterior process or flabellum proximally.
The lower ends of the astralagus are usually narrow and not expanded transversely as in many placentals.
Temperature Regulation and Sweat Glands
Text books state that body temperatures of marsupials are lower than those of placentals, but this is somewhat misleading. In many mammals resting temperatures require to be distinguished from active ones, and frequently this has not been done.
Among placentals, in health, temperature range (C) is: man. 35.5°-37.5°; horse, donkey, ox. 37.5°-38°: dog, cat, 38.5°-39°: sheep, rabbit, 38°-39°; mouse 37.5°; rat, 37.9° (McDowall 1944); camel 34°-40° (Schmidt-Nielsen 1964); micropteran bat 22.7°-41.7° (Morrison 1959).page 116
Examples of the marsupial temperature range (C) are Peramelidae: Macrotis lagotis 34.2°-37.0° (Morrison 1962); Dasyuridae: Sminthopsis 36.6°-38.6°; Antechinus 37.1°-38.7°; Dasycercus 33.9°-37.9°; Phascogale 36.7°-38.8°; Satanellus 35.1°-37.6°; Sarcophilus 36.1°-37.1° (Morrison 1965); Didelphidae: Marmosa 32.2°-35.7° (Morrison and McNab 1962) Didelphis and Metachirus 34°-37° (Morrison 1946); Macropodidae: Setonix 36.7°-38.3° (Bartholomew 1956). In some individuals among the Dasyuridae and in Marmosa, Morrison and McNab (1962) and Morrison (1965) recorded lower minimum temperatures than those quoted, indicating some degree of aestivation, as found in micropteran bats (Morrison 1959) and in a number of rodents (Schmidt-Nielsen 1964).
Marsupials do not differ greatly from placentals in range of temperature, but all for which adequate data are readily available appear to have experienced tropical or seasonally arid climates at some stage of their evolution in Central America or in Australia. Such conditions are not likely either to have raised or lowered the body temperatures maintained during phases of maximum activity, but they could have had considerable influence on methods of temperature regulation.
Adaptations to a hot climate are discussed by Schmidt-Nielsen (1964). They are mostly concerned with water conservation. Some moisture loss, with resulting cooling, unavoidably occurs through the skin irrespective of sweating. Small mammals have few sweat glands* on the general body surface and though in large mammals apocrine glands may be numerous their function in temperature regulation is usually small. Watery eccrine glands are frequently restricted to unfurred areas and to feet. Panting can be highly effective in cooling, and by this method the dog reduces temperature as effectively as does man, who is copiously supplied with eccrine glands. Panting prevents depletion of salt by sweating, but excessive aeration of the blood can result in alkalosis (to which the dog has high tolerance) through excessive reduction of carbon dioxide. Sheltering gives a high degree of protection from heat at little physiological cost, but water can still be dissipated involuntarily through respiration, in which loss is largely proportional to the difference between body and ambient temperature. In aestivation, when heat dissipation exceeds production, body temperature falls, lowering the saturation point of air expelled from the lungs, and further reduction of water loss results from the depressed breathing rate.
* Sebaceous glands and specialised apocrine glands, as those of the ear and eye, although coming within the general classification of sweat glands are excluded from present consideration.
Temperature regulation in marsupials is based mainly on metabolism, panting or accelerated respiration, and wetting of fur or bare skin with saliva (Robinson and Lee 1946; Robinson 1954). Setonix wets its fur, but the effectiveness of its temperature regulation does not appear to depend on this (Bentley 1960), which casts some doubt on the importance of fur wetting by marsupials.* Both Setonix and Sarcophilus seem to regulate with high efficiency by sweating alone.
Sweat glands on the body surface of marsupials are associated with pelage. In general, a central hair follicle has a sebaceous gland and an apocrine one. It is bordered by two or three lateral follicles with one or more sebaceous glands in the group, but no apocrine glands. Some central follicle and lateral follicle clusters may lack both apocrine and sebaceous glands respectively. As far as is known, eccrine glands are restricted to the pads and interdigital areas of the paws and to the bare under surface of the tail (Bolliger and Hardy 1945; Hardy 1947; Green 1963; Mykytowycz and Nay 1964).
The precise functions of apocrine glands are uncertain, but since Mykytowycz and Nay (1964) distinguished five basic types together with intermediates, it is likely that these glands have varied functions. In most cases, apocrine glands do not appear to be important in cooling, but these authors stated that the red kangaroo, after prolonged chasing, shows obvious signs of sweating, indicating at least an emergency utilisation. However, seasonal development of the glands and their aggregation on the neck and breast of males and in the pouch region of females suggest social functions also, as are certainly served by the sternal glands of Trichosurus.
* Bentley (1960) pointed out that salivation might be a sympton of hyperpyrexia, and Green (1961) suggested that the purpose of licking may be to recover salt deposited in the fur as a result of sweating.
Schmidt-Nielsen (1964) summed up, in part, as follows:
Marsupials have erroneously been accredited with a primitive type of heat regulation. Actually some marsupials are poor heat regulators, others are excellent and this is exactly as among placental mammals… The conclusion to be drawn from these diverse observations [largely covered in these notes] is that marsupials display a wide variety in their heat and water metabolism. This reflects the multitude of biological forms which have evolved in the Australian fauna. The characteristic demands of the environment have been adequately met by responses comparable to those of placental mammals, and there is no reason to consider marsupials as physiologically primitive in these respects.
Marsupials are not unlike placentals in their range of temperature during a 24 hour day, but they tend to have a more distinct differentiation of active and resting temperatures. Aestivation definitely occurs in the American Marmosa (Morrison and McNab 1962), and in the dormouse phalangers Cercaertus and Eudromica (Hickman and Hickman 1960). Some marsupials show no distinct signs of aestivation, but others have unexplained variations of resting temperatures which suggest effects of aestivation.
The new-born marsupial is very small. It seems to be only partly formed. This is certainly true of the hind limbs and some internal organs but the apparent absence of lips, eyes and ears is illusory. These parts are obvious in the late embryo, but before birth they are overlaid by thickening of epithelium anteriorly. The whole neonatus is covered by epitrichium, a thin keratinised impermeable membrane which gives protection against desiccation (Hill and Hill 1955).
The neonatus makes its own way to the pouch. There have been a few records of macropods using their lips to place young in the pouch, and though the accuracy of these observations has been questioned, they cannot be definitely rejected, because occasional variations in maternal behaviour would not be exceptional. Pelage between the vent and the pouch may be dampened with saliva, which appears to facilitate progress by the neonatus. The pouch can be reached across dry hair (Sharman 1964), although in Trichosurus (Lyne et al. 1959), in the absence of a prepared track, the neonatus fell from the mother. After replacement it reached the pouch, but it failed to attach to a teat. Sharman (1964) found that in the red kangaroo licking of the fur could occur both before and after establishment within the pouch, and he suggested that it might result simply from cleaning of the pouch and vent; but if the track has functional value, causation of fur wetting would be difficult to determine.page 119
Actual weights of young show a positive correlation with increase in size of adult females but, as indicated by ratios, relative weights of young have a negative correlation. Size of young is probably determined by the needs of the neonatus in traversing the distance between the vent and the pouch; since this distance varies more or less in proportion to cube roots of adult body weights and the potential energy of the neonatus increases according to weight, a three dimensional relationship, the progressive reduction of the neonatus with increasing adult size (Table 1) would be expected.
|Genus||Adult (g)||Young (g)||Ratio||Reference|
|Pseudocheirus||300-800||.3||1:2,400||Thomson and Owen 1964|
|Dasyurus||600||.0125||1:48,00||Hill and Hill 1955; Marlow 1961|
|Isoodon||2045||.18||1:11,000||Mackerras and Smith 1960|
|Setonix||3000||<.45||1:7,000||Waring et al. 1955|
|Macropus||=Megaleia||.828||1:30,000||Poole and Pilton 1964; Pilton 1961|
|Megaleia||27500||.745||1:36,000||Sharman and Calaby 1964|
Dasyurus, with the smallest known neonatus and a ratio of 1:48,000, is a marked exception. The evident specialisation for minute size might be associated with the surplus production of young, 10 and 18 being recorded for two females despite the presence of only six teats (Hill and O'Donoghue 1913), but the the backwardly opening pouch of the Dasyuridae could also be a factor. The other exception is Setonix which has large young for no apparent reason.
Parturition varies among individuals or species. Young may be delivered free or enclosed in the amnion, but opinions differ as to the function of the mother in removing impeding membranes (Sharman 1964; Sharman et al. 1966).
Hind limbs are not functional, and the pouch is reached by use of the fore limbs only. The head is moved to one side, followed by forward movement of the opposite fore limb. The head then changes to the opposite side, and the digits of the advanced limb are flexed and the limb is bent, pulling the neonatus forward. As the other fore limb and the digits straighten they are moved forward in turn and the cycle is repeated (McCrady 1938). Guidance may result from a sense of smell, since the olfactory apparatus is well developed, and distribution of branches of the Vth cranial nerve suggests response to tactile stimulae also (Hill and Hill 1955). Lips are fused laterally to a variable extent initially.page 120
The persistent belief that pouch young are force fed is not supported by evidence, and milk is not known to have been voluntarily expressed. Lamina of the cremaster muscle pass above and below the mammary glands in a manner which would render compression of the glands mechanically possible, but the more obvious function of the muscle fibres appears to be support for the hypertrophied glandular tissue (Hill and Hill 1955).
The respiratory and alimentary tracts are separated. The epiglottis, as a relatively large conical structure, projects upwards and slightly forwards into the pharyngeal cavity, and the posterior margin of the velum palati is produced downwards as a thin tapering lamina which projects into a well marked groove situated between the base of the tongue and that of the epiglottis. Laryngo-pharyngeal grooves, continuous with the glosso-epiglottic sulcus in front, pass back below and laterally to the glottis, then continue along the posterior prolongation of the pharynx and so finally merge into the lumen of the oesophagus. Two distinct palato-pharyngeal folds project down from the lateral pharyngeal wall into the laryngo-pharyngeal grooves. Apposition of the velum palati and the epiglottis forms a continuous respiratory tract, and the palato-pharyngeal folds convert the laryngo-pharyngeal grooves into lateral tubes for the conduction of milk to the oesophagus (Hill and Hill, 1955). This arrangement would permit the pouch marsupial to breathe and drink simultaneously, but it is neither known that it does so nor certain that such action would serve any necessary function. However, the teat is extremely flaccid; its tip is at first extended into the mouth by suction and then expanded to assume the form of the buccal cavity. Because the aperture of the mouth is small, this expansion (which can be reduced by continued gentle traction) tethers the young by the teat which lengthens as a thin cord during the first two weeks of pouch life. This facile teat expansion could conceivably obstruct both breathing and drinking, but such risk is obviated by the provision of channels for these purposes.
The neonatus sucks strongly, and the large muscular tongue may function in this respect, since it could exert considerably greater force than could be derived from the diaphragm; but by pressure against the palate anteriorly, the tongue may also serve to anchor the young to the teat, particularly in the early stages before fusion of the lips anteriorly has reduced the opening to a relatively small circular orifice (Hill and Hill 1955).
To Be Continued.