Osphranter rufus ( Desmarest, 1822 )

Freedman, Calli R, Rothschild, Daniel, Groves, Colin & Newman, Amy E M, 2020, Osphranter rufus (Diprotodontia: Macropodidae), Mammalian Species 52 (998), pp. 143-164 : 143-151

Osphranter rufus ( Desmarest, 1822)

Red Kangaroo

Kangurus rufus Desmarest, 1822:541 . Type locality “West of the Blue Mountains, New South Wales, Australia.”

Kangurus lanigeri Gaimard, 1823:138 . Type locality “Port Macquarie, New South Wales, Australia.”

Kangurus griseo-lanosus Quoy and Gaimard, 1825: 482 . Type locality “Blue Mountains, New South Wales, Australia.”

Macropus lanigerus Gray, 1826: 49 ; plate. Type locality “Bathurst Plains, New South Wales, Australia.”

K [angurus]. Lanosus Gray, 1827:202 . As of Gaimard, in synonymy.

Kangurus lanosus Gray, 1843:88 . Nomen nudum as of Gaimard.

Macropus rufus: Bennett, 1837:6 . Name combination.

H [almaturus]. Laniger: Wagner, 1843:110. Name combination.

Macropus (Halmaturus) rufus: Waterhouse, 1846:95 . Name combination.

Macropus (Osphranter) pictus Gould, 1861:373 . Nomen nudum; error vide Gould (1845 –1863).

M [acropus]. ruber Crisp, 1862:135. Incorrect subsequent spelling of M. rufa Bennett, 1837 .

Macropus (Boriogale) magnus Owen, 1874:247 . Type locality “Far north of South Australia, Australia.” Preoccupied by Macropus magnus Rothschild, 1905b .

Macropus rufus dissimulatus Rothschild, 1905a:508 . Type locality “North West Australia [= Gascoyne River, Western Australia, Australia].” Established from Iredale and Troughton (1934:53).

Macropus rufus dissimulator Lydekker, 1906:47 . Incorrect subsequent spelling of M. rufus dissimulatus Rothschild, 1905a .

M [acropus]. rufus occidentalis Cahn, 1906: 381 . Type locality “Murchison River, Western Australia, Australia.”

Macropus rufus pallidus Schwarz, 1910: 89 . Type locality “Shaw River, Western Australia, Australia.”

Megaleia rufa: Iredale and Troughton, 1934:52 . Name combination.

Macropus (Osphranter) rufus: Dawson and Flannery, 1985:488 . Name combination.

Osphranter rufus: Jackson and Groves, 2015:164 . First use of current name combination (see “Nomenclatural Notes”).

CONTEXT AND CONTENT. Order Diprotodontia , family Macropodidae , subfamily Macropodinae ( Gray, 1821) , genus Osphranter ( Gould 1842; Jackson and Groves 2015). O. rufus is monotypic.

NOMENCLATURAL NOTES. Historically, Osphranter rufus has been placed within the genus Macropus ( Shaw, 1790, in Shaw and Nodder 1790) and the subgenus Osphranter ( Gould, 1842) . However, there is evidence to suggest that the three subgenera Macropus , Notamacropus , and Osphranter separated 8–9 million years ago, shortly after the genus Macropus separated from its closest relatives, Lagorchestes and Setonix ( Meredith et al. 2008) . Considering this divergence time, Jackson and Groves (2015) split the three subgenera of Macropus ( Macropus , Notamacropus , and Osphranter ) into distinct genera. The genus Osphranter includes three extant species in addition to O. rufus : the antilopine wallaroo ( Osphranter antilopinus Gould, 1842 ), the black wallaroo ( Osphranter bernardus Rothschild, 1904 ), and four subspecies of the common wallaroo ( Osphranter robustus Gould, 1841 ).

DIAGNOSIS

Osphranter rufus ( Fig. 1 ) is the largest macropod and can be distinguished from most macropodines based on body size. For example, an adult O. bernardus (black wallaroo) is typically one-half the size of an adult O. rufus . It is, however, more difficult to distinguish O. rufus from O. antilopinus , O. robustus , M. giganteus (eastern grey kangaroo), and M. fuliginosus (western grey kangaroo) based on size, as there is considerable overlap in body measurements among these species (Eldridge and Coulson 2015). Instead, these species are typically distinguished from O. rufus based on fur patterns, pattern of skin and fur on the rhinarium, shape and groove patterns on the third upper incisor, and posture and movement patterns. Also, O. rufus has a distinct white and black pattern on the sides of the muzzle, which is absent in all other species of Osphranter and Macropus ( Fig. 1 ; Dawson 1995; Strahan 1995; Menkhorst and Knight 2011; Eldridge and Coulson 2015).

Compared to O. rufus , O. robustus tends to be stockier with shaggier fur, a shorter muzzle, less pointed ears, proportionally shorter hind limbs, and a larger area of bare black rhinarium. O. antilopinus lacks bold facial markings and occupies a different range (tropical monsoonal woodlands—Menkhorst and Knight 2011). In O. rufus , the fur of the muzzle extends about one-half of the way down between the nostrils in a V-shaped pattern, while in species of Macropus the muzzle is completely haired between the nostrils, which are ringed with black skin ( Troughton 1966). In other species of Osphranter , the muzzle is naked and scaly between the nostrils, similar to a canid nose pad ( Troughton 1966). Both sexes of O. rufus also have a series of four or more distinct bands of fur on the distal part of the tail, which is unlike other kangaroos or large wallabies (Sharman and Pilton 1964).

Osphranter rufus is characterized by molars which lack a forelink ( Hope et al. 1977). The third upper incisor is also noticeably larger than in other species of kangaroo and is nearly equally wide as long (when viewed from the side), with the hind margin sloping inward and a faint groove that is difficult to see ( Troughton 1966). Macropus species have oblong third incisors with two clearly visible grooves on the front half, while other Osphranter species have oblong third incisors that are nearly twice as wide as they are long with a single groove on the front half ( Troughton 1966; Dawson 1995; Menkhorst and Knight 2011).

In the field, O. rufus can be distinguished from Macropus at a distance based on posture and movement. Macropus species hop with the back relatively flat, the forelegs low down, and the head held up. The tail is also curved up and swings up and down when hopping quickly. In contrast, O. rufus hops with a flatter back and the head held lower. The tail is also not as curved and moves less than in Macropus ( Dawson 1995) .

GENERAL CHARACTERS

Osphranter rufus is the largest extant marsupial, and the largest of the Australian mammals. It has a short coat, the hair of which is similar to soft wool in texture; small head; large, pointed ears; large, black eyes; and a pointed tail that is used as a prop and for balance ( Nowak 1999).

As with all species of Osphranter , O. rufus exhibits sexual dimorphism in pelage color ( Russell 1974). In New South Wales and in adjacent areas of Queensland and South Australia, males are mainly a rich reddish-brown, whereas females are bluishgray. This is in contrast to Western Australia, where males are a lighter reddish tan. Additionally, in the northern part of the species’ distribution, males are primarily a pale sandy-red and, in Central Australia, along with some parts of Western Australia, the majority of O. rufus are the same red color, regardless of sex ( Dawson 1995). Reversals of dimorphic coloring may also occur in up to 30% of individuals ( Oliver 1986). Females are generally white on their ventral surface, while males are often paler on their ventral surface than on their dorsum, especially in the areas of the throat, upper chest, and inguinal region ( Russell 1974; Dawson 1995). In males, the limbs and tail are also paler than the body, whereas, in females, these appendages are most often white ( Russell 1974). Unlike the other kangaroos, the distal part of the tail of O. rufus displays four or more faint but distinct dark bands of fur (Sharman and Pilton 1964). In both sexes, the muzzle is mostly white with a conspicuous black patch in the area of the whiskers, and a broad white stripe reaching from the corner of the mouth to the ear. The nose is mostly hairless, and the skin is dusky-black in color ( Dawson 1995). Black hair covers the paws and toes (Frith and Calaby 1969).

Sexual size dimorphism is prominent in O. rufus . Males range from 45 to 85 kg, whereas females are commonly 18–36 kg ( Dawson 1995; Moss and Croft 1999). Males are typically 94–160 cm in length, excluding the tail, which may add an additional 70–115 cm. Females are 75–110 cm in length, with their tails adding 65–90 cm, on average (Yom-Tov and Nix 1986; Tyndale-Biscoe and Renfree 1987). The hind foot length is 30–38 cm in males and 26–33 cm in females (Yom-Tov and Nix 1986). The ears are about 13–16 cm in males and 12–15 cm in females (Yom-Tov and Nix 1986). The greatest skull length is 15–21 cm in males and 15–17 cm in females (Yom-Tov and Nix 1986). Additionally, males have significantly broader shoulders than females, and proportionally larger forelimbs ( Newsome 1995). Geographic body-size variation is also present, with individuals being larger, on average, in southeastern Australia than in the rest of the continent ( Correll et al. 2018). This variation is significantly correlated with mean annual precipitation, which is used as a measure of food supply or biomass productivity (Yom-Tov and Nix 1986; Moss and Croft 1999). There is also geographic variation in skull size, adhering to Bergmann’s rule, which predicts smaller measurements with increasing temperature (Yom-Tov and Nix 1986).

Osphranter rufus also displays the skeletal adaptations characteristic of the macropodines. In all macropods, the hind limbs are adapted for hopping and are considerably longer than the forelimbs. The narrow foot of O. rufus is the longest of all macropods and bears five digits. Additionally, the large, heavy tail of this group is used as a balancing organ during hopping or fighting, and as a form of auxiliary limb during quadrupedal locomotion. All macropod marsupials exhibit molar progression, whereby the teeth slowly move forward in the jaws, and possess a wide diastema between the incisors and cheek teeth (Frith and Calaby 1969). Common features between O. rufus and other members of the order Diprotodontia include the possession of a pair of procumbent incisors on the lower jaw and syndactyly of the second and third digits of the hind limb ( Russell 1974). The skull of O. rufus is an average of 14.6 cm in length, 7.4 cm in width, and 7.1 cm in height ( Nowak 1999; Fig. 2 ).

DISTRIBUTION

Osphranter rufus is endemic to Australia, where it occupies arid and semiarid regions ( Caughley et al. 1987), and it is the most widely distributed of all kangaroos, with a range of roughly 5 million square kilometers (Frith and Calaby 1969). It can be found in about two-thirds of the continent, and prefers open plains, open desert, grassland, woodland, or shrubland habitats, where scattered trees can be used for shade and shelter ( Caughley et al. 1985).

Osphranter rufus is mostly distributed in the drier part of mainland Australia ( Fig. 3 ), with the humid boundary lying between 400 and 700 mm of mean annual rainfall according to the level of mean annual temperature ( Caughley et al. 1987). Unlike the eastern and western grey kangaroos ( Macropus giganteus and Macropus fuliginosus , respectively), the distribution of O. rufus is unrelated to seasonality of rainfall but is defined in terms of mean annual precipitation and mean annual temperature ( Caughley et al. 1987). It generally inhabits areas that receive a mean annual precipitation of 277 ± 138 mm (mean ± SD) and is found in areas that have a higher mean annual temperature (21.6 ± 2.8°C, mean ± SD) than are members of Macropus ( Caughley et al. 1987) . Summer temperatures in these habitats average 36.6 ± 2.4°C (mean ± SD — Caughley et al. 1987), while temperatures average 6.3 ± 2.6°C (mean ± SD) in winter months ( Caughley et al. 1987). Human activities, especially agricultural practices, have permitted O. rufus to increase its range since the 1800s ( Tyndale-Biscoe 2005).

FOSSIL RECORD

A minimum of three red kangaroos ( Osphranter ) were identified from molar fragments in late Pleistocene deposits in the Seton Rock Shelter (Kangaroo Island, South Australia — Hope et al. 1977). In general, species of the genus Osphranter are not well-represented in the fossil record as few characters of the teeth and jaws can be reliably diagnosed (Dawson and Flannery 1985). The presence of Osphranter in the Pliocene (5.3–2.6 million years ago) has been established by specimens of O. pavana from the Bow fauna, and in the Pleistocene (2.6 million–11,700 years ago) by O. robustus altus , along with another, larger species (Dawson and Flannery 1985). These specimens were discovered in the Wellington Caves (New South Wales, Australia), and this larger species has also been found in early Pleistocene deposits from eastern Darling Downs (Queensland), Bingara (New South Wales), and possibly Lake Victoria (New South Wales), but is yet to be formally described (Dawson and Dawson 1982).

FORM AND FUNCTION

Form.— The skin of Osphranter rufus is almost entirely composed of the papillary layer, while the reticular layer is nearly absent (Mykytowycz and Nay 1964). Hair follicles are paired with sebaceous and sweat glands and are separated from cutaneous muscle by a thin layer of connective tissue (Mykytowycz and Nay 1964). The fine fur coat is composed of 62 fibers/mm, and effectively insulates O. rufus against both hot and cold temperatures ( Tyndale-Biscoe 2005). Hair density is highest in the mid-dorsal regions of the body, on the shoulders, and on the thighs, at an average of 119 hair follicles/ mm 2 (Mykytowycz and Nay 1964). Unlike the fur of other kangaroos, the fur of O. rufus is similar to soft wool in texture and is generally molted twice each year ( Staker 2006). The dense, soft fur of O. rufus reflects incident solar radiation, which prevents heat loss in the winter and protects from solar radiation in the summer. Red coats, present in approximately 78% of males and 12% of females, reflect more solar radiation (32–58%) than blue coats (27–55%), which are present in approximately 6% of males and 68% of females (Dawson and Brown 1970). Red-blue coats, present in about 15% of males and 20% of females, are similar in reflectance to blue coats (Dawson and Brown 1970).

Female O. rufus rear their young within a pouch which, in this species, opens horizontally on the ventral surface of the body and contains four teats ( Russell 1974). Male O. rufus lack teats. The mammae of O. rufus are the most complex, with respect to morphology and physiology, of all mammals; their structure and function has been described in detail ( Griffiths et al. 1969, 1972). Briefly, the four mammary glands and their respective teats can independently exhibit the anatomical and biochemical characteristics of different stages of lactation. In an immature, nonreproductive female, all four teats are embryonic in structure and teats only develop fully once stimulated by the suckling of offspring. Each teat is located within a pit on the dorsal surface of the pouch and a separate mammary gland is associated with each teat. There are 24–26 mammary ducts or galactophores in each teat ( Griffiths et al. 1972). A single O. rufus will often simultaneously exhibit one developing gland associated with a pouch young and another in a state of full lactation, supplying a young-at-foot ( Griffiths et al. 1972). During lactation, despite existing in the same endocrine environment, the two suckled glands also vary biochemically (see “Function”) to supply milk of different composition to young at different stages of development ( Griffiths et al. 1972).

Osphranter rufus has long, narrow feet and hind limbs adapted for hopping. The femur, tibia, fibula, and pes are elongated ( Hume et al. 1989). The tendons that extend the ankle are able to withstand large stresses and store large amounts of elastic strain energy, which allows for the hind limbs to act like springs during hopping (Alexander and Vernon 1975; Bennett and Taylor 1995). The patella is absent, while the calcaneum is well-developed and elongated ( Hume et al. 1989). Due to the articulations of the astragalus with the tibia and calcaneum, the foot can only move back and forth, but cannot twist sideways ( Hume et al. 1989). The first digit is absent, while the fourth is very large and carries a heavy claw; the fifth toe is similar, but smaller ( Nowak 1999). O. rufus exhibits syndactyly of the second and third digits, whereby they are reduced and unified within a fold of skin and possess a single claw ( Nowak 1999). These syndactylous toes are used for grooming (Frith and Calaby 1969). The vertebral formula is 7 C, 13 T, 6 L, 2 S, 21–25 Ca, total 49–53 ( Hume et al. 1989).

Macropods share many unique adaptations of the masticatory apparatus which allow for more efficient cropping and chewing of plant material (Frith and Calaby 1969). The dental formula for macropods is i3/1, c0/0, p2/2, and m4/4, total 32 ( Kirkpatrick 1978; Poole 1982; Sanson 1989; Ungar 2010). All of the macropodine kangaroos exhibit molar progression, whereby the teeth move forward slowly in the jaws. O. rufus has a total of four molars and, when worn, the anterior two molars are shed, while the remaining posterior molars shift forward. In young kangaroos, the first teeth to appear in the cheek row are the sectorial premolar (P3) followed by the deciduous molariform milk premolar (dP4) which, in turn is followed by the first true molar (M1—Sharman et al. 1964). Molars continue to erupt as the kangaroo ages, until the full complement of four (occasionally five) is attained (Sharman et al. 1964). The first two teeth (P3 and dP4) are eventually shed, at about the same time, and replaced by a sectorial premolar (P4), causing the entire toothrow to shift forward in the jaw line (Sharman et al. 1964; Frith and Calaby 1969). The toothrow continues to move forward in the jaw line even after the last molar (M4) has erupted (Sharman et al. 1964). Adults have a total of three incisors in the upper and lower jaws, and one pair of procumbent incisors with sharp lateral edges ( Russell 1974). In addition to a wide diastema between the incisors and cheek teeth, O. rufus has a true mandibular symphysis, which allows some independent movement of the jaws (Frith and Calaby 1969). This adaptation allows for close shearing of the sharp edges of the lower incisors against the upper ( Russell 1974). O. rufus possesses a masseteric canal, a large opening through the lower jaw, with an associated downward projection of the masseteric fossa (Frith and Calaby 1969).

The dominant senses of O. rufus are vision and olfaction. Its visual capacity is similar to that of rodents and ungulates, and its eyes are positioned high on the skull, affording a wide field of vision, while still maintaining approximately 50° of binocular vision ( Wimborne et al. 1999; Tyndale-Biscoe 2005). It has a prominent olfactory bulb and vomeronasal organ ( Russell 1985) and is capable of odor recognition and avoidance ( Hunt et al. 1999). Additionally, these animals possess large ears that are capable of independent movement through 180° ( Tyndale-Biscoe 2005).

The digestive system of O. rufus is adapted for the poorquality foods found in its habitat ( Russell 1974). It is a foregut fermenter, meaning the forestomach is expanded into the principal site of microbial fermentation. The salivary glands consist of parotid, sublingual, and submandibular glands ( Hume 1982). The esophagus is made up of smooth muscle with longitudinal folds of stratified epithelium and is devoid of glands ( Smith 2009). The long, tubular stomach contains distinct regions with specialized digestive functions, and is divided into the forestomach, where most microbial fermentation occurs, and the hindstomach, which is the acid-secreting region ( Hume 1982). The forestomach is further divided into the sacciform region, the anterior blind sac known as the fermentation chamber; and the tubiform region, the region between the sacciform region and hindstomach (Stonehouse and Gilmore 1977; Hume 1982). A gastric sulcus is present in O. rufus and extends caudally along the tubiform forestomach ( Hume 1982). It is presumed that this sulcus allows milk to bypass the fermentation areas of the stomach and pass directly to the hindstomach, the site of peptic digestion ( Hume 1982). The dense population of cellulytic bacteria found within the fermentation chamber produces volatile fatty acids (acetic, propionic, and n-butyric acid), ammonia, and gas ( Russell 1974; Hume 1982). The dominant phyla found in the gastrointestinal tract of O. rufus are Actinobacteria, Bacteroidetes, and Firmicutes ( Li et al. 2016). The fermentation chamber is lined by a mucus-secreting epithelium, which produces a high pH buffer after feeding ( Russell 1974).

The reproductive system of female O. rufus consists of paired ovaries, uterine tubes, and uteri, which open by separate cervices into the vaginal cul-de-sac (Sharman 1964; TyndaleBiscoe and Renfree 1987). Two separate lateral vaginal canals arise from the cul-de-sac and open into the urogenital sinus. In nonparous females, a median septum within the cul-de-sac partially separates the right and left vaginal canals, but this may disappear in parous females (Sharman 1964). A median pseudovaginal (birth) canal connects the vaginal cul-de-sac and urogenital sinus to allow passage of the fetus (Sharman 1964; Tyndale-Biscoe and Renfree 1987). In contrast to other marsupial species, the median vaginal canal does not regress and reform at each birth but remains open after the first birth (Sharman 1964). The vaginal cul-de-sac and anterior vaginal canals are lined by stratified epithelium, while their posterior ends are lined by columnar epithelium, with numerous crypts branching off the main canal (Sharman 1964).

The reproductive system of the male is similar to other marsupials and eutherian mammals. One major difference with marsupials is that the scrotum is located in front of the penis, as opposed to behind it, and it has been proposed that the marsupial scrotum is not homologous to the eutherian (Stonehouse and Gilmore 1977; Renfree et al. 1995; Watson and Cooper 1995). The penis is bifid, having right and left prongs that correspond to the lateral vaginal canals of the female (TyndaleBiscoe and Renfree 1987). The only accessory reproductive glands found in male O. rufus are the prostate and Cowper’s gland. Differentiation of the prostate accommodates for this lack of accessory organs (Tyndale-Biscoe and Renfree 1987). N-acetylglucosamine, the major sugar in O. rufus semen, is present at 339 mg % (Rodger and White 1975) and is secreted by all segments of the prostate but is most concentrated in the central segment (Rodger and White 1976). The semen also contains glucose at 111 mg % as well as small amounts of fructose. Glucose is contained within all segments of the prostate but is most concentrated in the posterior segments (Rodger and White 1974, 1976). An approximate 2.5–5°C temperature difference between the body and the testes ( Setchell 1977) is established by the rete mirabile (Setchell and Waites 1969), which, in O. rufus , contains about 95 arteries and 75 veins ( Hume et al. 1989). In the testicular vein, testosterone concentrations are approximately 80 ng /ml, corresponding to testosterone secretion rates of 2.6 ng min−1 g−1 testis (Carrick and Cox 1973). Its relative testes mass is considered average for its body mass, while its relative sperm tail length is considered large at approximately 119 µm (Tyndale-Biscoe and Renfree 1987). The semen of male O. rufus coagulates to form a copulatory plug shortly after ejaculation to prevent other males from copulating with the same female (Tyndale-Biscoe and Renfree 1987).

The general form and function of the endocrine glands are similar to those of other metatherians ( Hume et al. 1989). In O. rufus , the adrenal gland resembles that of the human, and has a pyriform shape (as opposed to the oval shape in other mammals) and exhibits a distinct yellowish coloration on the cut face of the cortex ( McDonald and Martin 1989). There is also evidence that adrenal structure can be affected by environmental conditions ( Myers et al. 1976). Severe drought causes a reduction in adrenal size, cortical folding and nodulation; and shrinkage of the three zones of the adrenal cortex, associated with lipid accumulation in the cortical cells ( Myers et al. 1976). Associated with these alterations is a significant change in the size of the pituitary ( Myers et al. 1976).

Function. —The milk of Osphranter rufus is composed of water, sugars, fats, and proteins, and is also rich in antibodies that confer passive immunity to immunologically incompetent neonates ( Russell 1974; Stonehouse and Gilmore 1977). Neonates receive milk that is high in carbohydrates and low in lipid content (Lemon and Barker 1967; Griffiths et al. 1972), as the young are unable to metabolize large quantities of lipids at this stage (Stonehouse and Gilmore 1977). The milk increases in lipid and protein content from day 1–4 to day 360 of lactation and may contain up to 20% fat (Lemon and Barker 1967; Griffiths et al. 1972), allowing developing young (joeys) to meet increasing energy and protein demands associated with increased growth rate and muscle growth (Stonehouse and Gilmore 1977). The fatty acid content of the milk also changes from mostly palmitic acid to mostly oleic acid ( Griffiths et al. 1972). Palmitic acid is important early in lactation, when it is required for the production of surfactants in the developing lung (Stonehouse and Gilmore 1977). Later, oleic acid becomes important as it is required for the production of nervonic acid, which is the major fatty acid component of myelin (Stonehouse and Gilmore 1977).

In the mouth of O. rufus , a bolus of food is mixed with large amounts of saliva, mainly from the parotid glands which secrete a serous saliva containing a high concentration of bicarbonate and phosphate ions ( Russell 1974). The maximum flow rate for parotid gland saliva is approximately 125 µl/kg/min ( Beal 1989). The maximum flow rate for mandibular saliva is approximately 128 µl/kg/min ( Beal 1989). The saliva also contains high concentrations of amylase, which begins carbohydrate digestion in the mouth ( Russell 1974). Although fermentation occurs throughout the forestomach, it is most rapid in the sacciform region, and declines along the length of the tubiform region as the concentration of soluble components in the digesta decreases (Stonehouse and Gilmore 1977; Hume 1982). Secondary fermentation occurs in the cecum and in the proximal colon but makes a much smaller contribution to the animal’s digestible energy intake (Stonehouse and Gilmore 1977; Stevens and Hume 1995). O. rufus does not ruminate, but merycism may occur, where a bolus of semi-digested food is regurgitated and reingested without chewing (Stonehouse and Gilmore 1977; Hume 1982; Vendl et al. 2017). This behavior does not appear to be under voluntary control but may be an adaptation to stimulate saliva production, which helps to buffer the pH of the forestomach, or it may serve to further grind insufficiently chewed food particles ( Smith 2009; Vendl et al. 2017). Regurgitation is not often seen, however, as O. rufus chews its food more thoroughly than do ruminants ( Hume 1982). Digestive efficiency when selecting from arid, rangeland forage is about 52.1% ( Munn et al. 2010). Its average bite size is 0.16 g dry matter and it grazes at 18 bites min−1 while feeding on chenopod shrubs ( Belovsky et al. 1991; Munn et al. 2010).

Osphranter rufus is an efficient homeotherm and maintains an internal body temperature of approximately 36°C (Dawson and Hulburt 1970; Needham et al. 1974; McCarron et al. 2001) using a combination of morphological and behavioral adaptations. These include the possession of soft, dense fur as well as assuming a nocturnal lifestyle ( Russell 1974). To conserve energy, it is generally inactive, and, during hot periods, it spends much of its day lying under trees and avoiding the sun to prevent heat gain ( Caughley 1964). It is generally active only from late afternoon to early morning ( Russell 1974). Although the primary method of heat loss is by panting, in extreme heat (around 40°C), O. rufus will engage in saliva spreading as a method of thermoregulation ( Needham et al. 1974), where a hypotonic solution of sodium chloride and potassium chloride, produced by the mandibular and parotid glands, is spread via the tongue onto the forearms and acts as a cooling mechanism ( Needham et al. 1974; Smith 2009). At the onset of saliva spreading, mandibular saliva flow rises rapidly to a maximum of approximately 1.12 ml min−1 over 10 min. Parotid saliva flow increases at a slower rate, reaching a level comparable to the maximum for mandibular saliva after 40 min of saliva spreading, and continues to rise over a period of over 90 min ( Beal 2017). A dense network of blood vessels is located on the region of the forearm that is licked, allowing for significant heat loss ( Needham et al. 1974).

Osphranter rufus lives in hot, arid areas and therefore also possesses a variety of physiological adaptations that allow it to thrive in its natural habitat, especially with respect to avoiding water loss in this desert environment. Due to low water availability, especially during the summer, O. rufus has a low rate of water turnover at approximately 70–120 ml kg−0.8 day−1 ( Dawson et al. 1975; Denny and Dawson 1975a; Munn et al. 2008) and a low glomerular filtration rate (Denny and Dawson 1977). On average, the kidneys reabsorb 69% of urea from glomerular filtrate when dehydrated (Denny and Dawson 1977). In comparison to other desert-dwelling species, O. rufus has a high plasma osmolality at approximately 320–407 mOsm/kg as well as a high urine osmolality at approximately 1,800 –2,120 mOsm/kg depending on climatic conditions (Dawson and Denny 1969; Dawson et al. 1975; Munn et al. 2010). Moreover O. rufus has adapted to tolerate dehydration by maintaining plasma volume when dehydrated, despite up to 20% decreases in body weight (Denny and Dawson 1975b).

Osphranter rufus also has a low level of oxygen metabolism compared with equivalent-sized eutherians, resulting in lower metabolic heat production, such that less water is needed to cool down ( Russell 1974). The basal metabolic rate of O. rufus is approximately 0.12 ml O 2 kg−1 s−1, while the metabolic rate is approximately 1.25 ml O 2 kg−1 s−1 while hopping, regardless of speed (Kram and Dawson 1998). The resting metabolic rate of a juvenile O. rufus is 1.5–1.6 times higher than predicted for adults of equivalent body mass, due to the additional energy needed for growth (Munn and Dawson 2003). O. rufus has the highest aerobic capacity of all the marsupials, at 4.7 ml O 2 min−1 ml−1 of mitochondria (Kram and Dawson 1998; Dawson et al. 2004). Under field conditions, its average minimum heart rate is 39 ± 3 bpm (mean ± SE — McCarron et al. 2001).

In O. rufus , as in all kangaroos, locomotion is primarily bipedal and saltatory. However, these animals rely on different movement patterns depending on their speed (Frith and Calaby 1969; Dawson and Taylor 1973). At the low speeds used for grazing (averaging 6 km /h), locomotion is primarily via a pentapedal crawl, with the tail serving as a crutch when the hind feet are off the ground (Frith and Calaby 1969; Dawson and Taylor 1973). In this gait, the forelimbs are first moved forward together, then the hind limbs are swung forward, together, to rest outside them (Dawson and Taylor 1973). At high speeds (averaging 7–18 km /h), it adopts a graceful bipedal hop (Dawson and Taylor 1973). In this gait, the body is inclined forward and the tail acts as a balance while the animal springs forward on the tips of the toes (Frith and Calaby 1969). The hop of O. rufus averages 1 m when the animal is moving slowly, but is lengthened with speed, up to 3–4 m (Frith and Calaby 1969). At speeds greater than 18 km /h, less energy is required, and less heat is produced to sustain the bipedal locomotion, as compared to a four-legged animal running at the same speed (Dawson and Taylor 1973). This is a result of the achilles tendon and ligaments in the foot storing and returning mechanical energy with each hop (Alexander and Vernon 1975; Bennett and Taylor 1995; Biewener et al. 1998). O. rufus has been reported to reach speeds greater than 40 km /h, but this speed cannot be sustained for more than short bursts (Dawson and Taylor 1973).

ONTOGENY AND REPRODUCTION

Ontogeny. —In Osphranter rufus , only embryogenesis occurs in utero, while primary growth and development takes place inside the pouch ( Tyndale-Biscoe 1973). Pouch life lasts an average of 235 days and, during the final 30 days, a dormant blastocyst completes development in utero, such that the final emergence of a pouch young may be followed within 24–48 h by another birth ( Russell 1974). As a result, when conditions are favorable, it is possible for a female to be suckling both a young-at-foot and a pouch young while carrying a dormant blastocyst in her uterus ( Russell 1974).

Female O. rufus give birth to live young which complete development in the pouch. The neonate weighs about 750 mg at birth but will weigh about 900 mg by the end of its first day (Sharman and Pilton 1964). At this time, some neural systems in the brain and spinal cord have limited functional capacity, but many remain embryonic ( Ashwell 2010). Generally, the hindbrain is more developed than the midbrain or forebrain ( Ashwell 2010). Some functional organs are present, but most are embryonic ( Russell 1974). Additionally, the newborn lacks a functional immune system and the immune tissues must mature in the pouch, which may contain a number of potentially pathogenic bacteria ( Edwards et al. 2012).

At parturition, the young passes through the urogenital opening while still enclosed in the fluid-filled amniotic sac ( Sharman 1970). After breaking free, the blind, hairless neonate then crawls from the sinus to the pouch by grasping the mother’s fur with its forelimbs (Sharman and Pilton 1964). Neonates have well-developed and active forelimbs with digits and claws, jaw muscles, and tongues, to crawl to the pouch and commence suckling (Sharman and Calaby 1964; Sharman and Pilton 1964). In contrast, the hind limbs are generally very poorly developed at birth, as they are not involved in the climb to the pouch (Sharman and Calaby 1964; Sharman and Pilton 1964). Neonates do not have functional eyes or ears but do have large nostrils and are presumed to possess a well-developed sense of smell, which may play a major role in their ability to locate the pouch and teat (Sharman and Pilton 1964). Attachment to the teat occurs within 5–10 min of birth, and suckling commences immediately (Sharman and Calaby 1964; Sharman and Pilton 1964). Suckling will then continue, uninterrupted, for about 40 days, after which the young is intermittently free of the teat for progressively longer periods (Merchant and Sharman 1966). Body hair begins to appear at 90 days, and by 160 days the joey is usually completely furred (Frith and Calaby 1969).

The head of the neonate is large, with an elliptical mouth at the tip (Sharman and Pilton 1964; Frith and Calaby 1969). The mouth begins to open along the sides at 40 days and is completely open by 115 days (Sharman and Pilton 1964; Frith and Calaby 1969). The stomach of the pouch young does contain peptic activity, due to the secretion of acid and pepsin, but it is not yet differentiated into distinct regions (Griffiths and Barton 1966; Russell 1974). The definitive form of the stomach is achieved between day 16 and 35, and by day 200, the stomach begins to transition to adult morphology and histology and has generally attained its final structure by 236 days, at which time, all peptic activity is restricted to the posterior gastric pouch region (Griffiths and Barton 1966; Russell 1974).

The growth rate of females begins to slow at about 2 years of age, and most are considered fully grown by approximately 5 years (Frith and Calaby 1969). Females grow at a slower rate than males, and this rate is maintained until they reach their full size, at about 10 years (Frith and Calaby 1969). Similarly, males continue to increase in weight until about 10 years of age, but do not increase in total length after 8 years (Frith and Calaby 1969). After this time, their weight and length remain constant for the remainder of their lives (Frith and Calaby 1969). One can distinguish the sex of a joey once it is 14–20 days old (Sharman and Pilton 1964). The pouch appears after about 14 days, while the scrotum does not appear until day 17–20 (Sharman and Pilton 1964). Males generally reach sexual maturity between 2 and 4 years of age, when they weigh about 20–30 kg, while females reach sexual maturity between 1 and 3 years of age, when they weigh 15–25 kg ( Newsome 1964; Sharman and Pilton 1964). In captivity, females become sexually mature earlier, following eruption of second and third molars (Sharman et al. 1964) or at about 15–20 months of age (Sharman and Calaby 1964; TyndaleBiscoe and Renfree 1987). Captive males generally reach sexual maturity between 24 and 36 months of age (Tyndale-Biscoe and Renfree 1987). This being said, poor conditions can delay the onset of sexual maturity, and it has been estimated that severe drought will cause a delay of about 6 months ( Newsome 1965a). This delay is usually attributed to poor nutrition in drought ( Newsome 1965a).

Reproduction.— Osphranter rufus exhibits a continuous breeding cycle and is thus capable of successful copulation throughout the year ( Russell 1974). It is essentially an opportunistic breeder. Female O. rufus generally have 1–2 bouts of reproduction per year, with approximately 236 days between births (Stonehouse and Gilmore 1977). Litters usually consist of only one young, although twins have been reported (Grzimek and Ganslosser 1990). Compared with monotocous eutherian mammals, O. rufus has a fairly high reproductive efficiency, with 82% of females becoming pregnant and giving birth to a young after having access to a male for 1 day ( Sharman 1970).

Female O. rufus are mono-ovular and polyestrous, and the estrous cycle lasts, on average, 35 days, but may vary in length from 22 to 42 days (Sharman and Pilton 1964). In O. rufus , conception after fertilization does not vary the estrous cycle, and it is not suppressed until after parturition, via the suckling stimulus from the young (Sharman and Pilton 1964; Russell 1974). Therefore, the next estrus and mating will occur at the same time, regardless of whether the female becomes pregnant ( Russell 1974). Although O. rufus has a short gestation period as compared to placental mammals, its gestation period is longer than in other marsupials. The gestation period is often shorter than the estrous cycle, and lasts, on average, 33 days (Sharman and Pilton 1964). The gestation period is followed within 2 days by a postpartum estrus and subsequent fertilization (Sharman and Pilton 1964). Although conception can occur at this time, if lactation proceeds normally, the embryo that results from this fertilization develops to the blastocyst phase of about 85 cells within 40 days, and subsequently enters a dormant stage, as long as the previous young is retained in the pouch and suckled ( Clark 1966). This phenomenon is referred to as embryonic diapause ( Tyndale-Biscoe 1963). The corpus luteum of postpartum estrus and subsequent fertilization are also inhibited, a condition referred to as ovarian or lactational quiescence (Tyndale-Biscoe and Renfree 1987). When a pouch young reaches about 200 days, or anytime earlier if the young is lost or otherwise removed from the pouch for an extended period of time, the estrous cycle will resume, and the development of the dormant blastocyst will continue ( Sharman 1963). This appears to be a result of a decline in prolactin levels allowing the undeveloped corpus luteum to increase in size, causing progesterone levels to rise and resuming blastocyst growth and development (Tyndale-Biscoe and Hinds 1981). The resulting fetus will be born 1–2 days after the pouch young permanently leaves the pouch, at about 235 days (Sharman and Pilton 1964).

The growth of the oocyte and follicle in the ovaries of marsupials has been studied by Lintern-Moore et al. (1976). Briefly, oocyte growth in relation to follicular growth conforms to the uniform biphasic pattern characteristic of eutherian mammals but the marsupial oocyte and follicle are larger ( Lintern-Moore et al. (1976). Additionally, the hormonal control of pregnancy and parturition, and estrus and ovulation have been described in most detail for the tammar wallaby ( Macropus eugenii ) and reviewed for marsupials by Hinds (1990) and Hinds et al. (1996). Briefly, estrus is regulated, as in eutherians, by both estrogen and luteinizing hormone, while progesterone is the primary hormone produced during the luteal phase, following ovulation and formation of the corpus luteum. At parturition, there is a rapid decline in progesterone, an increase in peripheral estradiol concentrations, and a release of prostaglandin and prolactin ( Hinds et al. 1996).

During prolonged drought, anestrous females may be found, which is thought to result from poor nutrition ( Newsome 1964). In anestrous, the uteri are very small, the endometrial glands are short and straight with closed lumina, and the ovaries do not contain corpora lutea or tertiary Graafian follicles ( Newsome 1964; Clarke and Poole 1967). This phenomenon may be of adaptive significance, offering the embryos and pouch young of anestrous females a better chance of surviving the drought ( Newsome 1964). Testicular function may also be impaired during periods of severe drought, the severity of which is determined by the synergistic interaction between heat and poor nutrition ( Newsome 1973). However, O. rufus is able to maintain normal spermatogenesis at much higher environmental temperatures as compared to other herbivorous mammals of similar body size (Frith and Sharman 1964; Newsome 1965a).

Development of the mammary glands of the female begins during the first one-half of pregnancy, or the equivalent stage of the nonpregnant cycle, and secretion begins to accumulate in the lumena of alveoli toward the end of pregnancy or equivalent postestrus state ( Griffiths et al. 1972). Enlargement of the mammary gland and the histological changes associated with lactation occur regardless of if the female is pregnant; however, only the glands to which a young becomes attached enlarge and lactate, while the others quickly regress within 10 days ( Griffiths et al. 1972; Tyndale-Biscoe and Renfree 1987). For effective lactogenesis to occur, an active corpus luteum must be present at the end of pregnancy ( Clark 1968a).

Figures

Fig. 1.—An adult male (left) and female (right) Osphranter rufus from Broken Hill, New South Wales, Australia taken in 2004. Photograph by Nicholas Walker used with permission.

Fig. 2.—Dorsal, ventral, and lateral views of skull and lateral view of mandible of an adult female red kangaroo (Osphranter rufus; NMV [Museums Victoria] C9623) from Fowlers Gap, New South Wales, Australia. Greatest skull length is 159.08 mm. Photographed by Alistair Evans used with permission.

Fig. 3.—Geographic distribution of Osphranter rufus. Map redrawn from Ellis et al. (2016) with modifications.