Geologically oldest evidence of ‘lumpy jaw’ (Macropod Progressive Periodontal Disease) in kangaroos of Australia: implications for conservation management

Abstract

At a time of widespread concern over the prevalence of viruses and infectious diseases in global ecosystems, it is helpful to consider the history of afflictions in the geological record. Amongst captive species of Australian kangaroos, one of the most common pathological conditions observed is the occurrence of ‘lumpy jaw’, or Macropod Progressive Periodontal Disease (MPPD). Macropods (including both kangaroos and wallabies) affected by the disease commonly exhibit osteological swellings in either the mandible or maxilla, or both, including in areas surrounding the cheek teeth. Diseased individuals struggle to eat, often resulting in death. The specific cause of MPPD is unclear, although it may be multifactorial. When present in wild populations, the condition is more likely to occur in situations that result in the mass-gathering of individuals around critical resources such as drying waterholes. Here we report a case of MPPD in a Pliocene (ca 3 Ma) kangaroo, the geologically oldest record of this condition within macropods. The fossil is identified as Osphranter ?pan and was excavated from a deposit in the Chinchilla Sand, southeast Queensland. The osteomyelitis is expressed by a noticeable lateral mandibular swelling on the horizontal ramus; this is clearly pathological and has not been observed in any other member of the species. The specific circumstance that led to the development of MPPD in this individual likely reflects palaeoenvironmental stress, principally drought, in the Pliocene ecosystem. Lumpy jaw is evidently a geologically young disease, with its higher incidence through the late Cenozoic closely tied to long-term shifts towards progressively drier and more arid conditions. Given predictions that future climate change will follow such trajectories across many regions of Australia, MPPD is expected to become an increasingly important pathology for management in extant populations. This includes conservation projects that may lead to resource-limited settings such as fenced (including re-wilding) and translocated island populations.

Gilbert J. Price [[email protected]], School of Earth and Environmental Sciences, The University of Queensland, Brisbane, Queensland 4072, Australia; Julien Louys [[email protected]], Australian Research Centre for Human Evolution, Griffith University, Brisbane, Queensland 4101, Australia; Joanne E. Wilkinson [[email protected]], Queensland Museum Geosciences, 122 Gerler Road, Hendra, Queensland 4011 Australia.

Keywords:

• Lumpy jaw
• macropod progressive periodontal disease
• kangaroo
• fossil
• palaeopathology
• conservation management

KANGAROOS, WALLABIES, AND RAT-KANGAROOS, or ‘macropods’ (broadly regarded here as any member of Macropodiformes), have an extensive and diverse record in both modern and palaeo-ecosystems of mainland Australia, Tasmania, and New Guinea (Sahul; Black et al. 2012). Following emergence at least 25 million years ago, their subsequent evolution and diversification as the now dominant endemic herbivores of these landmasses has been shaped by climatic changes, ecosystem perturbations, and extinctions. Early macropods were quadrupedal and mostly browsers within mid-Cenozoic forests (Butler et al. 2021). Many distinct lineages independently evolved towards larger body sizes through time, adopting either a saltorial or even bipedal mode of locomotion (Janis et al. 2014), with a long-term dietary shift towards more grass-based foods. These evolutionary changes were likely driven by the overall trend of a reduction of closed forests to open savannah grasslands over the mid–late Cenozoic.

The largest-bodied macropod species occurred during the Pliocene and Pleistocene, although these were dwarfed by the herbivorous diprotodontoids (Hocknull et al. 2020). The apparent rise of macropods as the largest-bodied herbivores did not occur until after the extinction of the diprotodontoids in the Late Pleistocene (Price & Piper 2009); however, they do not fill the ecological role of the diprotodontoids (e.g., Price et al. 2017), with modern ecosystems clearly non-analogous with most, if not all, Pleistocene ecosystems (Black et al. 2012).

Several extant macropod species are threatened by a range of factors including habitat clearing, over-predation by non-native predators (e.g., foxes and cats), as well as the emerging threat of climate change (Woinarski et al. 2012). Some species are particularly rare in the wild, but with various ‘insurance’ populations surviving in captive environments such as zoos (Blessington et al. 2021). Among the challenges of conserving and protecting macropods is the close monitoring and management of disease. One of the most common pathologies reported is Macropod Progressive Periodontal Disease (MPPD), colloquially known as ‘lumpy jaw’ (McLelland 2019), a progressive osteomyelitic condition that results in swellings of either the mandible, maxilla, or both. The precise cause of MPPD in captive populations is uncertain. However, cases are far more prevalent in zoo populations than in the wild, although MPPD is recorded in both environments (Borland et al. 2012; Rendle et al. 2020a). Several factors have been hypothesized to lead to MPPD, ranging from faecal contamination of pastureland, to intentional and/or unintentional coprophagia among others (Borland et al. 2012; McLelland 2019). Stress-induced immunosuppression may also lead to elevated rates of mortality in affected individuals (Sotohira et al. 2018).

During a time of universal concern regarding pathogens that may affect the persistence of various species, it is critical to recognize and document cases of diseases in the fossil record. Identification of diseases through deep time can provide important information on the biology, health, and environmental conditions of ancient organisms and their populations (Poinar 2014). Within macropods, some pathologies have been reported in the fossil record, including cases of bony lesions (Garvey & Sandy 2009) and specifically MPPD (Horton & Samuel 1978), but not previously in individuals older than Late Pleistocene.

Here we report a case of MPPD in an individual from a pre-Quaternary deposit. The specimen was collected in June 2021 during fieldwork at the Chinchilla Rifle Range, southeast Queensland. Fossils have long been known from this locality, and they include many collected during dedicated palaeontological surveying in the 1970s by Michael Archer (see Wilkinson et al. 2021), whose contributions to vertebrate palaeontology are honoured in this festschrift. Given Archer’s investigations in the region, as well as his seminal contributions to understanding pathologies in marsupials (e.g., Archer 1975), our study here builds on his foundational work. The aim of this paper is to describe the MPPD-affected fossil kangaroo specimen and the deposit from which it was derived, including associated palaeoclimate inferences.

Geographic and geologic settings

Discoveries of fossils from the Pliocene Chinchilla Sand (ca 3 Ma) of southeast Queensland have been regularly reported since the mid–late-1800s (Wilkinson et al. 2021). The Chinchilla Sand crops out across an area between Nangram Lagoon and Warra, mostly adjacent to the modern Condamine River, a major drainage basin that forms the headwaters of the modern Darling River Catchment (Fig. 1). The Pliocene sequence is ca 30 m thick and includes mostly unconsolidated fluviatile sands and silts, and the occasional lithified conglomerate (Louys & Price 2013). The sediments are most likely derived from the Orallo Formation (Bartholomai & Woods 1976).

Figure 1. Map of Queensland showing study location at Chinchilla.

Although fossils have been reported widely across the area, most specimens accessioned into the collections of the Queensland Museum were collected from various deposits at, or in the vicinity of, the Chinchilla Rifle Range. Wilkinson et al. (2021) recently mapped the occurrence of known Pliocene fossil localities there, describing the history of collecting and prevalence of Pliocene deposits or ‘sites’ adjacent to the type section of the Chinchilla Sand. A significant stratigraphic layer represented by a well-lithified conglomeratic horizon is present throughout the Rifle Range deposits and may represent a clear marker of the Pliocene. Sediments yielding Pliocene taxa are known both below, in, and immediately above this layer, mostly in unconsolidated sands.

The fossil assemblages of the Chinchilla Rifle Range are particularly diverse, and they include a range of vertebrates, including small-bodied taxa such as skinks, rodents, bandicoots and koalas through to large-bodied crocodiles and diprotodontoids (e.g., Godthelp 1990, Hutchinson & Mackness 2002, Mackness et al. 2002, Hocknull et al. 2009, Price & Piper 2009, Price et al. 2009, Louys 2015, Travouillon et al. 2017, Ristevski et al. 2020, Ristevski et al. 2021). Palaeopathology in a crocodile femur was previously reported from the Chinchilla Sand, and likely represents a puncture wound (Mackness et al. 2010).

Results

Deposit

The pathological macropod specimen reported here is from a previously undescribed fossil-bearing locality at the Chinchilla Rifle Range, here dubbed ‘Diprotodon Site’ (Fig. 2). Fossils from the site were originally reported by citizen scientist Mr Robert Knezour. Subsequent investigations have revealed a deposit that is somewhat geologically unusual in comparison to other deposits at the Chinchilla Rifle Range. Diprotodon Site contains the stratigraphically highest fossil-bearing stratum currently recorded at the Chinchilla Rifle Range, the base of which is at least 1 m higher than the uppermost, fossil-rich, coarse, unconsolidated sands, and approximately 2 m higher than the conglomerate marker horizon (i.e., Wilkinson et al. 2021). Given the necessity to protect the deposit from unauthorized collectors, specific geographic location details are not provided here, but are available to bona fide researchers upon request to the Queensland Museum.

Figure 2. Stratigraphic log of Diprotodon Site at the Chinchilla Rifle Range, Chinchilla, southeast Queensland. Letters in circles (A–G) refer to the named stratigraphic horizons.

From the base of Diprotodon Site (Fig. 2), the deposit passes upwards through various grey clays (Horizon A) that somewhat resemble younger Pleistocene deposits of the eastern Darling Downs (cf. Price et al. 2005; Price & Sobbe 2005, Price & Webb 2006). A distinct hardpan calcrete horizon (Horizon B) ca 100 mm thick occurs just above these clays; such weathered crusts typically occur in arid and semiarid environments (Haldar 2018).

Upwards, a thin stratigraphic horizon (Horizon C) up to ca 50 mm thick is present and dominated by coarse sands with a basal erosional contact; this is the only known fossil-bearing stratum within Diprotodon Site. This layer has yielded not only the pathological macropod specimen, but also an additional broken macropod mandible, a lungfish tooth plate and associated maxilla, as well as isolated and less taxonomically useful marsupial tooth fragments that we have not been able to identify to family level or below.

Further upwards, the deposit passes into a clay unit (Horizon D) up to ca 50 mm thick that contains occasional carbonate concretions. These clasts reflect pedogenic processes and are clearly in situ, as they are mostly horizontal and randomly distributed (e.g., Dixon 2013). Their presence is typically associated with grassland soils (Mikhailova et al. 2006).

The deposit then passes upwards to fine grey muds (Horizon E), followed by a comparatively thick unit up to 500 mm (Horizon F) of moderately to poorly sorted unlithified sands with weak planar lamination and an erosional basal contact. The stratigraphically youngest stratum (Horizon G) is represented by fine dark clays enriched by organics. Indeed, this uppermost layer in the exposed section comprises the primary substrate of modern vegetative rooting systems.

Pathological specimen and other fossils

The pathological kangaroo specimen (Queensland Museum Fossil; QMF61053, Brisbane, Queensland, Australia), along with other vertebrate fossils from the deposit, are thus far known only from the sand lens (Horizon D) immediately above the hardpan calcrete layer (Horizon C) at the site (Fig. 2). The pathological specimen is represented by a partial left mandible that possesses the M₃ and M₄ (Fig. 3). We have taxonomically identified the individual as Osphranter ?pan de Vis, 1895 (Macropus pan of Bartholomai 1975; generic level taxonomy revised following Jackson & Groves 2015), on the basis of the following features: (1) comparatively large size of the molars (Table 1); (2) molars are bilophodont and rectangular-shaped in occlusal view; (3) molars are particularly high-crowned with inward rotated lophids; (4) fore- and mid-links are well-developed and are positioned high on the crown; and (5) the posterior faces of the hypolophids exhibit an oblique groove that extend downwards towards the alveoli. There are some minor differences to O. pan as described by Bartholomai (1975), including a ca 10% longer M₃ and a deeper oblique groove on the posterior lophid of M₃. This latter feature somewhat resembles the condition seen in the closely related O. ferragus (a species known only from the Pleistocene, although it lacks firm geochronological control; Wroe et al. 2013). Other features present in QMF61053 express the condition seen in other specimens referred to O. pan (e.g., Bartholomai 1975). The species is the largest-bodied member of the macropod fauna of the Chinchilla Sand.

Figure 3. Left mandible of Osphranter ?pan (QMF61053) from Diprotodon Site at the Chinchilla Rifle Range showing expression of MPPD (indicated by large arrows). A, Occlusal view; B, lingual view; C, buccal view. Abbreviations (lowercase): a, anterior; b, buccal; d, dorsal. For comparison to non-pathological mandibular specimens of O. pan, see plates 17 and 18 in Bartholomai (1975). A digital 3D photogrammetric model (https://doi.org/10.17602/M2/M515488) and associated image series of the specimen is available on Morphosource (https://doi.org/10.17602/M2/M515485).

Table 1. Measurements of the cheek teeth of Osphranter ?pan (QMF61053), the pathological specimen at Diprotodon Site, Chinchilla Rifle Range, southeast Queensland.

Tooth	Length	Anterior width	Posterior width
LM3	22.1	12.3	11.6
LM4	20.0	12.4	10.8

All measurements are in mm. For a comparison of dental measurements with other individuals of O. pan, see Bartholomai (1975).

The pathology occurs as a large lateral swelling on the horizontal ramus. The mandibular body is smooth and rounded. The swelling is widest at the position ventral to the M₂ alveoli (ca 31.1 mm measured laterally at that point). The swelling is strongest laterally, and is more gently expressed medially. The ventral margin of the horizontal ramus is strongly convex. The outer surface of the bone of the horizontal ramus is intact and undistorted, demonstrating that the swelling is not taphonomic.

Regarding ontogeny, the specimen has M₃ in occlusion, and M₄ partly erupted at the time of death. These teeth are relatively unworn (the dentine–enamel junction has not been breached in either tooth). Collectively, this suggests that it may have been a young adult when it died.

In terms of both osteological expression and ontogenetic age, the condition in QMF61053 is similar to a recent case in a zoo-housed wallaby (Gerras et al. 2022) also affected by MPPD. Upon euthanization and examination, the osteomyelitis in that individual is thought to have been caused by a species of bacteria in Actinomyces (Gerras et al. 2022). In the absence of soft tissues, we cannot be certain of the aetiological agent that caused MPPD in QMF61053.

In addition to the MPPD-affected specimen, the same stratum has also yielded specimens of a subadult Protemnodon sp. (forest wallaby) and Neocertatodus fosteri (modern lungfish). Species of Protemnodon are known from the Pliocene and Pleistocene (Bartholomai 1975), whilst N. forsteri has a temporal range from the Cretaceous to Recent, so is less biostratigraphically useful (Kemp & Molnar 1981). Given the occurrence of QMF61053 proximal to the Pliocene deposits of the Chinchilla Rifle Range, and identification of the specimen as O. ?pan (or at least an Osphranter species close to O. pan), we suggest that the deposit is middle Pliocene.

Discussion

Although the species reported here is extinct, other species in Osphranter are extant. This fossil record represents one of the oldest occurrences of the genus in Australia, in addition to having been an individual also clearly afflicted by MPPD. Geologically younger members of the genus include extant species such as the Red Kangaroo (O. rufus), Common Wallaroo (O. robustus), Black Wallaroo (O. berardus), and Antilopine Kangaroo (O. antilopinus). Cases of MPPD have also been reported in at least some of these taxa (e.g., Tomlinson & Gooding 1954).

In modern natural ecosystems, MPPD is rare in unstressed populations (Rendle et al. 2020b) but occurs markedly more frequently in those affected by droughts (Borland et al. 2012). At Lancefield Swamp, Victoria, the site of the previous geologically oldest known occurrence of MPPD (late Quaternary), up to 10% of the population of Macropus giganteus titan were recognized to have been afflicted by a range of pathologies, including MPPD (Horton & Samuel 1978). Independent evidence from that assemblage indicates that most individuals succumbed because of environmental stresses induced by drought (Dortch et al. 2016). It is likely that the congregation of individuals around drying waterholes at Lancefield Swamp was sufficient to lead to high-density aggregations of macropods within a resource-limited ecosystem. This may have been compounded by the devastating effect of drought in the region, and contributed to elevated rates of mortality.

Evidence presented here suggests that similarly stressful conditions may have been prevalent at Chinchilla during the mid-Pliocene although we acknowledge that the sample size is very small. However, the fact that the fossil-bearing stratum immediately overlies a hardpan calcrete layer, a geological feature associated with arid and semi-arid environments (Haldar 2018), provides independent palaeoclimate evidence that the assemblage accumulated during, or soon after, a period of locally drier conditions. Furthermore, the immediate stratum (Horizon D) overlying the fossil-bearing unit (Horizon C) at Diprotodon Site also has characteristics that resemble sedimentological features of semi-arid or arid grassland soils (e.g., Mikhailova et al. 2006). This is unlike geological and palaeontological interpretations of fossils contained in lower (=older) strata that clearly indicate deposition under fluvial regimes with local faunas dominated by forest and semi-aquatic taxa (e.g., Montanari et al. 2013, Louys & Price 2013). Thus, the strata at Diprotodon Site suggest an extended and sustained shift towards drier climates and more open vegetation. Both macropod specimens from the fossil-bearing stratum were breeding-age individuals at the time of their death, rather than juvenile or senile; such a mortality profile is also seen in late-stage drought-affected modern macropod populations (Horton 1984). This scenario bears resemblance to both Lancefield Swamp and modern, drought-stressed natural populations where MPPD has been recorded (e.g., Borland et al. 2012). Future investigations at Diprotodon Site will aim to test this hypothesis.

Noting that palaeoclimate conditions across Australia before the mid-Pliocene were wetter (Martin 2006), and that MPPD has not been reported in older deposits despite the thousands of macropod specimens now recovered (e.g., Butler et al. 2017), these data suggest that the disease is geologically young and may have become more prevalent closer to today. The apparent trend towards increased macropod mortality during drought conditions since the mid-Pliocene is likely reflective of local (Price 2012), regional (Price 2013), and global (Ehlers et al. 2018, Rustic et al. 2020, Kaboth-Bahr & Mudelsee 2022) shifts towards progressively drier and more arid conditions across the late Cenozoic, coupled with enhanced El Niño–Southern Oscillation and greater climatic variability.

The incidence of MPPD is likely to increase in the future, making management of MPPD more challenging in some circumstances, and potentially threatening the perseverance of extant macropod populations. Indeed, predictions from the Intergovernmental Panel on Climate Change (Lawrence et al. 2022) suggest that many regions of Australia will continue to experience enhanced aridity and climate variability into the future, thus mirroring the deep-time trajectory of climate change in Australia but at a significantly accelerated rate. Although some macropod species today persist in large numbers, such as Macropus fuliginosus (Western Grey Kangaroo), and MPPD is apparently rare in some of their extant populations (Rendle et al. 2020b), it can be extremely common in closely related species. For example, Borland et al. (2012) reported that more than 50% of individuals in a drought-stressed population of Macropus giganteus (Eastern grey kangaroos) in Victoria were afflicted with MPPD. Such high occurrence rates may have the potential to extirpate populations. That scenario would be even more devastating for species already within resource-limited ecosystems, including those closely related to the Chinchilla kangaroo, such as Osphranter robustus isabellinus (Barrow Island Wallaroo), a subspecies today restricted only to a single small island off the Pilbara coast of Western Australia, and one whose conservation status is already listed as Vulnerable (Threatened Species Scientific Committee 2008). Similarly, MPPD will likely be an increasingly important factor to manage in conservation projects (including re-wilding) that concern the construction of fenced enclosures that protect native taxa (including macropods) to the exclusion of exotic predators and herbivores, and those that translocate individuals to islands to establish ‘insurance’ populations (e.g., Short & Smith 1994; Clayton et al. 2014; Legge et al. 2018; Smith et al. 2023). Both of these measures can create resource-limited conditions that mirror settings in some natural and artificial environments in which high rates of MPPD occur, and in which climate change may further exacerbate the frequency of cases.

Future excavations at Diprotodon Site and other stratigraphically younger deposits will be critical to determine the incidence of MPPD amongst macropod species in the region, and to reveal additional evidence for locally challenging palaeoenvironmental conditions. Such work has the potential to provide further information about the origin of the disease, including when it first affected macropod populations, and to offer critical insights into the long-term survival of populations at local and regional levels through time. The results of such investigations are likely to have benefits for conservation management of extant species in which this disease will likely become increasingly prevalent.

Acknowledgments

We dedicate this paper to the late Dr Bernard N. Cooke (1944–2020), a field assistant at Chinchilla in the 1970s to, and later PhD student of, Michael Archer. In addition to his remarkable contributions towards understanding macropod biology, palaeontology and evolution, Bernie played the role of supervisor, mentor and friend to the authors of this paper. We are also perpetually gratefully to Peter Dougall and the Chinchilla branch of the Sporting Shooters’ Association of Australia for access to, and management of, the Chinchilla Rifle Range Nature Reserve. We thank Robert Knezour for introducing us to the study site, Doug Boyer for support at Morphosource, as well as the numerous volunteers who have assisted in the field and laboratory on the broader Chinchilla Sand palaeontology project. Finally, we appreciate the constructive feedback from three anonymous reviewers whose suggestions greatly improved this paper.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Additional information

Funding

This work was supported by The University of Queensland, Griffith University, and Queensland Museum.