Kangaroos

PREFACE TO THE FIRST EDITION

My father was a railwayman and the family was moved around country New South Wales. As a consequence, I grew up wandering the bush around towns like Nyngan in western New South Wales and Albury on the Murray River. Seeing kangaroos was always special for me and because of my curiosity about them Ellis Troughton’s Furred Animals of Australia came as a Christmas present when I was 12. My scientific interest in kangaroos, however, had its origins in the United States. I was a postdoctoral fellow in Knut Schmidt-Nielsen’s comparative physiology group at Duke University, North Carolina in the mid-1960s, and I was often asked about kangaroos. Americans assumed that an Australian would know all about them. I didn’t and my curiosity was rekindled.

The 1960s was a time when you could fall on your feet. I got a lectureship in Zoology at the University of New South Wales, where Geoff Sharman was setting up a kangaroo research group. The university also recently had acquired Fowlers Gap Station and was developing it as an arid zone research station. To live in Sydney as well: what more could a New South Welshman ask for?

At that time there was a burst of interest in kangaroos, partly driven by conflict between conservation and pastoral interests. The initial focus was at the CSIRO Division of Wildlife, but it spread out to the universities and state organisations. As a result, an integrated understanding of the biology of kangaroos is now emerging. The biology of the large kangaroos is more complex and interesting than I ever could have imagined when I first watched them in the bush around Nyngan.

Many colleagues and students are thanked for their input into my work with kangaroos. In my early days at UNSW and Fowlers Gap Station, Eleanor Russell and Leon Hughes were fine colleagues; we learnt a lot together with Geoff and it was mostly fun. David Croft has been a great Fowlers Gap stalwart and I have relied much on his group’s studies of behavioural ecology. Thanks to my many good students for their contributions. Two of these particularly come to mind when I think about kangaroos, Martin Denny my first ‘kangaroo’ PhD and Glen Edwards, one of my most recent. Their efforts and dedication were far beyond what was necessary. For her skill at diet analysis and cheerful field assistance, Beverley Ellis is specially thanked.

Those who have helped with this book must also be thanked for their forbearance. There was always something else that needed to be done more urgently. Julia Collingwood and Rex Parry of the University of New South Wales Press have been very supportive of the whole Natural History Series and Kangaroos in particular. Dr Jill Hallam’s diagrams and Anne Musser’s drawings have added extra dimension to the text.

Without my wife Lyndall’s help, both scientific and editorial, this book would never have seen the light of day. She provided many ideas and removed much scientific jargon during her continuous editing. I especially thank her for her forbearance.

Additional comments for the second edition

When Kangaroos was completed in 1994 for the Australian Natural History Series, I had been surprised at how far our understanding of kangaroos had come since the 1960s. Researchers had broken down the notion that kangaroos, and other marsupials, were somewhat primitive mammals. Consequently, I was then able to present insights into unique and special features of kangaroos.

Now some 18 years later I am in the same situation. We know even more about kangaroos and their place in Australia and I have tried to make these stories accessible. New stories have come from many labs and field studies across Australia; however, one from my own group gives me special pleasure, instead of being metabolically limited, kangaroos are actually among the most superior of athletic mammals.

Again, I give much thanks to Lyndall Dawson as a very dedicated editor and reviewer; readers will be most thankful for her ‘war’ on jargon. Her patience with my long sessions at the computer during my retirement needs special commendation. We will get a life!

1

WHAT ARE KANGAROOS?

Kangaroos are among the strangest of all mammals, not only because they are marsupials and keep their young in a pouch, but because they hop. Many types of marsupial are spread throughout Australia and Central and South America and, apart from their distinctive reproductive systems, they are not really very different from other mammals. However, hopping is very uncommon among vertebrates, otherwise being used only by frogs and some small mammals, notably desert rodents. Apart from kangaroos and their relatives, no vertebrates larger than about 5 kg hop and there is no evidence in the fossil history of other large hopping animals.

Kangaroos and their hopping intrigued the earliest European visitors to Australia (Figure 1.1). Sir Joseph Banks wrote in the journal of his voyage with Captain James Cook on the Endeavour from 1768 to 1771:

Quadripeds we saw but few, and were able to catch few of them that we did see. The largest was called by the natives kangaroo. It is different from any European and indeed any animal I have heard or read of except the Gerbua of Egypt, which is not larger than a rat when this is as large as a middling Lamb; the largest we shot weighed 84lb. It may however be easily known from all other mammals by the singular property of running or rather hopping upon only its hinder legs carrying its fore bent close to its breast; in this manner however it hops so fast that in the rocky bad ground where it is commonly found it easily beat my grey hound, who tho he was fairly started at several killed only one, and that quite a young one.

The name kangaroo was one of the first Aboriginal words introduced into English. It came from the natives at Endeavour River (modern Cooktown) in the far north of Queensland. Cook’s party sighted and obtained their first kangaroos there when they put in to repair the Endeavour after it was almost wrecked on the Great Barrier Reef.

Kangaroos with their relatives in the suborder Macropodiformes (‘big foots’) comprise a most conspicuous group among the Australian marsupials. There are some 70 living species of macropodiforms in Australia and New Guinea, ranging from rat-sized species weighing less than 1 kg to species in which the males may weigh up to 90 kg. While relationships have been hotly debated in the past, these species are currently placed in three distinctive families: Hypsiprymnodontidae (the Musky Rat-kangaroo), Potoroidae (potoroos and bettongs) and Macropodidae (kangaroos, wallabies and pademelons). Further detail on the evolutionary relationships of the Macropodiformes to the rest of the marsupials and within the suborder is shown in Box 1.1. This discussion is based on recent studies of Robert Meredith and colleagues.

Figure 1.1. A reproduction of an early poster featuring a ‘Kanguroo from Botany Bay’. Londoners were informed of the amazing features of this unique animal from the new colony in the south seas. The features of the kangaroo were based on a painting by George Stubbs done in 1771 or 1772. Stubbs’ painting, in turn, was based on drawings by the Endeavour’s draughtsman, Sydney Parkinson. Unfortunately, Parkinson died on the voyage back to England and received little credit as the first European illustrator of a kangaroo.

What are kangaroos?

‘Kangaroo’ is at times used as a general term for members of the family Macropodidae, especially those within the large genus Macropus. This genus also contains species known as wallabies. So what are kangaroos? Early scientists defined kangaroos as those species having a hind foot more than 250 mm long. This definition encompassed the six largest species, but overlap between small female kangaroos and some large male wallabies caused problems. Today there is a clearer appreciation of the lineages of the large species within Macropus. A few years ago Lyndall Dawson and Tim Flannery, then at the University of New South Wales, recognised that there were subgroups among the large array of wallabies and kangaroos that are referrable to this genus.

Box 1.1. The phylogenetic relationships of the kangaroos with other marsupial groups and the evolution of the grazing kangaroos within the Macropodiformes

That the kangaroos are a group of evolutionarily advanced marsupials is clearly seen in Figure 1.2. They are the most recent lineage in the order Diprotodontia, which is itself the most recently evolved of the seven marsupial orders (three South American and four Australian). The nearest relatives (sister group) of the Macropodiformes are the arboreal Phalangeriformes, including the family Phalangeridae (cuscuses) and the Burramyidae (pygmy possums).

Figure 1.2. Timeline in millions of years for the evolution of marsupials as based on genetic studies of Meredith et al. (2008b). Grey bars indicate confidence intervals, solid rectangles indicate oldest fossils of a lineage and fossil constrained branch points are indicated by open circles. K-T indicates the Cretaceous–Tertiary boundary.

The diversification of the Macropodiformes and the evolution of their feeding strategies are seen in Figure 1.3. The potoroids are often considered ‘basal’ in their feeding, i.e. like ancestral types, but while there are elements of this, such as feeding on insects, roots, succulent plants and seeds, the preferred food of potoroids is fungi, particularly the fruiting bodies of underground fungus, i.e. types of truffles. The fungi are usually in a symbiotic relationship with trees; they help the tree roots take up nutrients and ‘get paid’ by getting other nutrients from the trees. Thus, reduction of forests and woodland throughout the past 10 million years has not favoured rat-kangaroos. The same applies with land clearing today. Among other Macropodiformes a range of feeding strategies is seen, from browsing on trees and woody shrubs to mixed feeding on soft grasses and shrubs. However, only the kangaroos have developed a true specialisation for feeding on grasses.

Figure 1.3. Ancestral reconstruction of grades of dental organisation by Meredith et al. (2008a). Posterior probability distributions for grades at each ancestral node are shown with pie graphs.

They proposed three subgenera for these groups: Macropus (Notomacropus) for an extensive group of wallabies, such as Agile and Redneck wallabies; Macropus (Macropus) for the group containing the Eastern Grey Kangaroo and the Western Grey

Figure 1.4. Limb proportions of a female Red Kangaroo showing the marked specialisation for hopping in the hind legs and tail. The forearms are much reduced for overall weight reduction. (Photo Mark Chappell)

Kangaroo; and Macropus (Osphranter), the group that includes the Red Kangaroo, the Antilopine Kangaroo and the Euro–wallaroo complex of species. Genetic studies now confirm these relationships for living species (Figure 1.2 and Figure 1.3 in Box 1.1). It is the latter two subgenera containing the six largest species that are accepted as comprising the ‘kangaroos’, while the Notomacropus group contains the wallabies. The kangaroos are distinctive in having highly specialised features for grazing (Figure 1.3) and their limb proportions also indicate the evolution of greater high-speed capability (Figure 1.4).

The specialised grazing lifestyle is crucial in uniting kangaroos as a group and distinguishes them from wallabies that are ‘mixed feeders’ (i.e. graze and browse). As grazers, grass is the main component of their diets; it can be widely available as a food source but is not very easy to digest. The evolution of the anatomical and physiological specialisations that permit grazing is complex and has not occurred in many mammal groups. While the use of forestomach fermentative digestion to utilise fibrous vegetation is a feature of the macropodiform radiation, the kangaroos have developed it further and matched it with specialised teeth for cropping rough grass (see Chapter 7). Parallel adaptations are found only among ruminants, such as bovids (sheep, cattle and antelope) and cervids (deer and elk), from Africa and the northern continents, respectively. Other mammalian herbivores, such as horses and rabbits, use hindgut fermentative digestion that lacks some of the advantages of the foregut system (see Chapter 7).

As the largest living marsupials, the grazing kangaroos are now unique. But through most of marsupial history there have been other larger macropod species. Before the arrival of humans in Australia, some 45–50 000 years ago, types of giant ‘kangaroos’, together with large wombats and their distant relatives the huge diprotodontids, featured in Australian landscapes. We are only now starting to understand why the characteristics of the modern kangaroos selectively facilitated their survival through the ecosystem collapse that followed the first arrival of the humans on this continent. This will be discussed further in Chapter 9.

Of the six living species of kangaroo – the two grey kangaroos, the Red Kangaroo, the Antilopine Kangaroo and the Euro–wallaroo group – none is in danger of extinction, unlike many of their smaller relatives, such as bettongs, hare-wallabies and some of the Notomacropus wallabies. Between them the kangaroos range over most of Australia and exist in large populations. In some areas, only one species may be found, but in other places several occur. Such is the case at my study area at Fowlers Gap Arid Zone Research Station in western New South Wales (see Plate 1). Here four species are found, namely the Red Kangaroo, the Euro, the Eastern Grey Kangaroo and the Western Grey Kangaroo. Although they all occur on this 40 000-ha station, there are obvious differences in each species’ microhabitat preferences. Locations throughout Australia in which significant studies of the biology of kangaroos have occurred are shown in Figure 1.5.

Figure 1.5. The sites of some major studies of the biology of kangaroos. Key: AS, Alice Springs; B, Bago State Forest; BH, Bakers Hill; C, Canberra; CY, Cape York; FG, Fowlers Gap; H, Hattah-Kulkyne NP; K, Kinchega; KI, Kangaroo Island; M, Mardi Station; T, Tibooburra; TC, Tero Creek; W, Wiluna; WC, Wallaby Creek.

Fossil history and evolution of kangaroos

The first appearance of hopping macropodiforms in Australia and their early evolutionary paths are still somewhat of a mystery. No fossils of Australian marsupials older than 55 million years ago (Mya) have yet been discovered. The earliest known mammal fossils are from the early Eocene Tingamarra Local Fauna (Murgon in south-eastern Queensland), the most common being Djarthia murgonensis, a small marsupial carnivore that Robin Beck and co-workers consider to approximate the ancestral morphotype of the Australian marsupial radiation. Tingamarra Local Fauna does not contain macropodiforms or even recognisable members of the order Diprotodontia (also including wombats, koalas and possums) to which macropodiforms belong. Unfortunately, there is a blank in the fossil record until 26 Mya and evidence about what transpired in relation to the macropodiforms through this time has been derived from ancestry trees established from recent genetic analyses, such as those of Robert Meredith and colleagues. These suggest that the earliest ancestors of kangaroos branched off from a small, tree-dwelling possum-like marsupial that left the trees of the rainforests that then covered most of Australia. Exactly when that occurred is uncertain and not recorded in the fossil record. To estimate when the living groups of macropodiforms arose we have to rely on genetic data. Apparently the Hypsiprymnodontidae, of which the Musky Rat-kangaroo (Hypsiprymnodon moschatus) (Plate 2) is the only living member, diverged from the ancestors of the Potoroidae and Macropodidae around 35 Mya, and then, by around 23 Mya the latter two families had separated. The structural changes that were associated with success on the forest floor are not well understood but the use of a hopping gait must have played a large role.

Hopping appears to be a phylogenetically old trait that arose only once in the suborder Macropodiformes. Estimation of the timing of its actual evolution is difficult because of the 30 million year gap in the fossil record through much of the Eocene and Oligocene. If we consider the gaits used within the range of living species in this order an answer is suggested. The Musky Rat-kangaroo seems not to hop and, if this was true of past members of this family, it could be that bipedal hopping arose after the divergence of the common ancestor of the families Macropodidae and Potoroidae from the Hypsiprymnodontidae, but before the macropodids and potoroids diverged (see Figure 1.2). If the above dates for the divergence of these families are correct, then hopping may have developed in a forested Australia during the Oligocene.

Doubts have arisen with this picture, however, due to recent work by Ben Kear and colleagues. This work has focused on the skull and partial skeleton of an Oligo–Miocene macropodiform Nambaroo gillespieae from the Riversleigh deposits in north Queensland. The limbs of N. gillespieae suggest it predominantly used a quadrupedal gait (as do some potoroids when moving at slower speeds), but they show some distinct hind leg adaptations compatible with hopping. This specimen, at 24 Mya, is one of the oldest macropodiform skeletons yet discovered and is attributable to the extinct family Balbaridae, which, importantly, is now seen as basal to all other macropodiform families. This means it predated the Hypsiprymnodontidae, so if Nambaroo gillespieae hopped then hopping presumably evolved back in the Eocene, i.e. much earlier than indicated from living species. Further analyses of early fossil macropodiforms by Kear and colleagues have supported the idea of an early evolution of bipedal locomotor strategies.

A full understanding of the evolution of hopping obviously must wait until we have a better fossil record. However, a modern scenario exists that may be a model for the evolution of hopping from small, arboreal forest-dwelling mammals. Bush babies, prosimian primates of the African rainforest and savanna, are small (~1 kg), agile and fast leaping animals that have highly developed hind legs. Most species are arboreal but the Northern Greater Galago, Otolemur garnettii, and the Brown Greater Galago, O. crassicaudatus, also spend time on the ground. Though they are morphologically very similar, one has become a habitual bipedal hopper, while the other employs a bounding gallop. Hopping, as we will see, is actually an extension of the gallop to achieve higher speeds. Marsupials inherently have high energetic capabilities and it is plausible to imagine an active, leaping ‘possum’ developing a hop to avoid predators on its excursions to the ground.

By the middle–late Miocene (25–15 Mya) all macropodiform fossils show an obvious bipedal morphology. While this early evolution of hopping was not associated with arid environments, the drying out of the continent and the spread of grasslands during the late Miocene gave the Macropodiformes scope for a major radiation and they became the dominant group of marsupial herbivores, with both Potoroidae and Macropodidae having many fast ‘athletic’ species.

The special characteristics of hopping

Continuous locomotion using the bipedal hop, also known as saltatory locomotion, is an unusual mammalian gait but it defines the macropodiforms (Plate 6). There is no reliable evidence from the fossil record that other large vertebrates (>5 kg) have hopped; suggestions that some dinosaurs hopped are now discounted. This indicates that there is something very special about the macropods. Saltatory locomotion is also found in four families of rodents, small animals often associated with arid habitats. An African hopping rodent Pedetes capensis (Springhare) reaches 3–4 kg, but other species are much smaller, with body masses typically below 200 g. The only other marsupial that hops is the Kultarr (Antechinomys laniger), a mouse-sized marsupial carnivore. Thus, the hopping of the macropodiforms is unique for large vertebrates.

The body shape of kangaroos, especially of the hindquarters and tail, is highly specialised. This is seen clearly from the skeleton (Figure 1.6 and also Figure 9.3). This leads us to ask whether the underlying principle of locomotion in kangaroos has similarities in other fast mammals. Also, if hopping is so special, what are its advantages? Over 40 years ago Richard Taylor and co-workers at Duke and Harvard universities were studying the energetics of normal walking and running among placental mammals and found that there is a relatively constant increase in the cost, or energy use, of locomotion as speed increases (Figure 1.7). This work provided a basis for examining the relative performance of hopping in kangaroos.

In 1973 I was able to take Red Kangaroos to Harvard University to work with Richard Taylor on this problem. We trained the kangaroos to walk or hop on a treadmill at speeds up to about 25 km per hour. The kangaroos were also trained to wear a mask while they exercised so that oxygen use could be measured. Oxygen use indicates how much metabolic fuel is being burnt and hence the energy cost of locomotion. Whereas in most walking and running mammals (both placental and marsupial) there was a relatively constant increase in the energy cost as speed increases, this was not so for the Red Kangaroos (Figure 1.7). When compared with the locomotory energetics of a similar sized quadruped, such as a dog, the kangaroos had a pattern of energy use with increasing speed that was quite uneven. Unlike in dogs, energy use patterns at different speeds were very different for the different gaits of the kangaroo, that is, for ‘pentapedal’ walking and hopping. The net result was, however, that kangaroos, when walking and hopping at slow speeds, had a relatively high energy use, but at higher hopping speeds they travelled at lower energy costs than a running quadruped.

Figure 1.6. The skeleton of a male Red Kangaroo showing the extreme specialisation for hopping in the hind legs, lower back and tail. The forearms in males are used in male-to-male fighting and are relatively more developed than in the female in Figure 1.4.

Figure 1.7. (A) Changes in stride frequency and length across a wide range of speeds for Red Kangaroo females (18 kg). Speeds up to and including 6 m per second are from treadmill studies; above 6 m per second data are from field observations. (B) Costs of locomotion for a Red Kangaroo female at differing speeds. The data below 6 m per second are from treadmill studies; above 6 m per second values were predicted from gait changes. Solid lines are predicted costs for quadrupedal mammals of equivalent weights. VO2 max. is maximum oxygen consumption, and Red Kangaroos should achieve higher aerobically sustained speeds than quadrupeds. From Dawson and Webster (2010).

The peculiar walk of kangaroos has been termed pentapedal because it involves the four legs plus the tail. It is used for speeds up to about 6 km per hour but is mostly used at slower speeds. This gait is energetically costly; a kangaroo walking uses double the energy at a particular speed than does a quadrupedal walking dog. The use of the tail at slow speeds is common in macropodiforms but extreme in the large kangaroos. Here the tail makes a significant contribution to forward propulsion, with the hind legs that move together providing the rest. The front legs act only as struts to support the body while the tail pushes it forward as the hind legs are lifted forward. The hind legs then push forward and the front legs are lifted forward. This understanding was established when kangaroos were trained to walk over force-measuring plates by Max Donelan, now of Simon Fraser University in Canada, when he visited my lab some years ago. Kangaroos apparently have accepted structural and/or functional limitations at slow speeds to achieve the advantages of hopping for faster movement. In the wild, kangaroos rarely walk fast. They use slow walking when feeding and relaxing but, not surprisingly, they quickly transition to hopping if they are to move far. Incidentally, kangaroos are good swimmers and, as they swim, they ‘dog paddle’ and their hind legs alternate, contrary to their normal hopping action.

What are the advantages of hopping? Hopping at slow speeds is still more energetically costly than quadrupedal running, such as by a dog. Kangaroos can hop at around 6–7 km per hour but it is only above 12 km per hour that hopping becomes more economic than running. At 22 km per hour, the highest speed when energy cost was measured, hopping provided a substantial benefit, using only 73% of the energy use calculated for a dog. The efficiencies of hopping are projected to increase further at even higher speeds and at 40 km per hour a kangaroo should require half the energy that a quadrupedal mammal would. This energy efficiency, together with their structural specialisations, allows kangaroos to go even faster. If given time to get moving they can out-speed quadrupedal predators, such as Dingoes!

Since our first findings, we have struggled to understand the mechanisms behind the benefits of hopping. Initially we considered that the spring-like characteristic of hopping was its distinctive feature, but this is not so. During hopping, elastic energy storage, as in a spring, is significant but we now know that it features also in galloping mammals. In hopping and galloping, substantial energy is stored in the tendons and muscles of the legs during the landing part of a stride and recovered during the subsequent take-off phase, like a bouncing ball. However, given that elastic energy recovery occurs in both hoppers and gallopers this does not explain the lower energy costs of hopping at higher speeds, relative to those of a galloping quadruped.

This lack of a clear explanation for the low energy costs of hopping has led to a reexamination of the specialised anatomy of the kangaroos, particularly the great locomotory muscles around the upper hind legs, the much elongated hind legs and the reduced forequarters. It seems that the key differences between kangaroos and quadrupeds in their locomotion is the differing connection between stride length, stride frequency and energy costs as speed is increased. Stride length is distance covered with each hop or step. Stride frequency is the number of hops or steps made in a period of time. Animals can increase speed by increasing either stride length or frequency or a combination of both. There is clear evidence that energy needs in locomotion are largely determined by the frequency of steps or hops, i.e. the fewer strides taken at a speed the less the energy used. The anatomical specialisations in kangaroos enable large increases in hop length (stride length), thereby reducing the need for increases in hop frequency as speed is raised. In kangaroos, frequency is largely unchanged until their highest speeds are reached and consequently energy needs are relatively lower than in quadrupeds, which increase both the number and length of their strides as speed is increased.

The precise functional reason for the close correlation between energy use and stride frequency is still debated. However, the volume of muscle activated per step, and