Australia: The Land Where Time Began

A biography of the Australian continent 

Australian Aboriginal People - Prehistoric Assisted Migration of a Rainforest Tree

The dispersal of many plants that are culturally important has been contributed to by human activities. The way the natural distribution and dynamics of species and communities are perceived can be altered by the study of these traditional interactions. The way in which native populations influenced their distribution is revealed by comprehensive evolutionary and anthropological data. Empirical evidence for the deliberate dispersal of native crops by prehistoric peoples remains limited, though also included in traditional diets were a suite of plants that were not cultivated, and which necessitated in some places the development of culturally important technical advances such as the treatment of toxic seeds. In this study Rossetto et al. integrated historic and biocultural research that involved Aboriginal people, with chloroplast and nuclear genomic data to demonstrate Aboriginal-mediated dispersal of a non-cultivated rainforest tree.

Rossetto et al. assembled new anthropological evidence of the use and deliberate dispersal of Castanospermum australe (Fabaceae), a non-cultivated riparian tree that produces toxic, though highly nutritious, seeds that are distributed by water, that are culturally significant.  Rossetto et al. validated cultural evidence of recent dispersal that was mediated by humans by revealing genomic homogeneity across habitat that was extensively dissected, multiple catchments and uneven topography in the southern range of this species. They excluded the potential contribution of other dispersal mechanisms based on the absence of suitable vectors and current distributional patterns at higher elevations and not near watercourses, as well as comparing a comparative sample from northern Australia.

Previous studies of the influence of prehistoric humans on the Australian vegetation have centred primarily around broad-scale change that was associated with the practice and cessation of burning by Aboriginals (Bowman, 1998; Ens, Walsh & Clarke, 2017) and the accumulative effects that have been hypothesised of human–induced decline of megafauna (Miller et al., 2005). The role of humans within a broader context has been considered to have been an integral factor in the geographical spread of crops and agriculture. It is suggested by evidence that has been obtained from Amazonian forests that pre-Columbian dispersal of domesticated plants had an unforeseen role of the way in which species are distributed in rainforest assemblages of the present (Shepard & Ramirez, 2011; Thomas et al., 2015; Levis et al., 2017). Evolutionary studies based on DNA that have been carried out in the Pacific region have documented the link between long distance dispersal of seed by Indigenous people and the current distribution of native crops (Zerega et al., 2004; Clarke & Burtenshaw, 2006; Roullier & Benoit, 2013). Investigators have been able to investigate the prehistoric human settlement of the Pacific through evolutionary history of traditional domestication by integrating genetics, linguistics and archaeobotany (Perrier & Langhe, 2011). In regards to the dispersal of non-cultivated plants by prehistoric Indigenous peoples evidence has remained limited, however, to ecological and archaeological circumstantial evidence (Perrier & Langhe, 2011; Atchison, 2009). There is now the potential to innovate in the field as the result of the new technological advances and the integration of multi-disciplinary data sources.

The influence in Australia of assisted migration or human dispersal is now included in lists of possible explanations for the genetic patterns in landscapes that have been detected for Livistona mariae in central Australia (Kondo, 2012) and Adansonia gregorii in the Kimberley region (Bell et al., 2014). The corroboration of dispersal hypotheses that is human-mediated and the exclusion of alternative mechanisms require that further ethnographic and cultural research be linked directly to the interpretations that have been derived from genetic patterns. A follow-up study on A. gregorii, for instance, identified overlap between genetic connectivity at population level and regional linguistic variation (Rangan et al., 2015), and local traditional beliefs of Indigenous dispersal where reported with historical accounts that are related to current distribution of L. mariae (Bowman, 2015). These interpretative frameworks lack, however, corroboration from other sources and ethnographic information derived from Indigenous collaborators. The study by Rossetto et al. integrated from the start the onset, anthropological, molecular and ecological research to test if dispersal by Aboriginal people can explain the distribution of a variable, though non-cultivated resource tree, Castanospermum australe A. Cunn. Ex Mudie (black bean, Fabaceae). Hydrochory (water-dispersal) is the usual method of migration of Castanospermum, instead of ingestion and deposition in faeces that is used by many other species of tree to migrate (Smith et al., 1990). The seed pods of C. australe are large and buoyant, and the germination of the seed is not affected by seawater (Smith et al., 1990), and so neither the seeds nor pods provide rewards for dispersal. The reliance on water of C. australe for dispersal is reflected in the distribution of this tree along riparian habitats close to the coast (Swanborough, 1998). However there are multiple populations located among rainforest vegetation inland from the coast and at considerable elevation, which implies dispersal by alternative means.

Australian Aboriginal people have traditionally used the seeds, which are highly nutritious, as a staple food source (Birtles, 1997; Dixon, 1983) following extensive treatment to neutralise the toxins (Birtles, 1997; Dixon, 1983). The seeds ripen in May-June, and these were often stored underground for several months (Coyyan, 1018; Mjöberg, 1918). Also, when the ground meal of C. australe was prepared it could be stored for later use (Maiden, 1899). It had previously been identified that there were strong links between the application of techniques for detoxifying the seeds and the more intensive habitation of rainforests in northern Queensland between 2,500 BP and 1,000 BP (Cosgrave, field & Ferrier, 2007; Ferrier & Cosgrove, 2012), though the dispersal by Aboriginal people had not been investigated previously. In this study Rossetto et al. used an integrative framework that was exclusion-based to show that the prehistoric dispersal by Aboriginal people explains the distribution at the present of C. australe within northern New South Wales (NNSW). They focused their attention on this geographically well-defined area because of the paucity of local fauna that could disperse the seeds (an absence of megafauna [Rossetto et al., 2015]), their understanding of local rainforest dynamic and biogeographic processes (Rossetto et al., 2015; Kooyman et al., 2011), and because dispersal by Aboriginal people had been proposed as a speculative explanation for the inland distribution of the species in NNSW (Maiden, 1899).

In order to determine if deliberate dispersal by local Aboriginal People influenced the contemporary patterns of distribution of C. australe they aimed to:

1.     reveal prehistoric, historic, linguistic and ethnographic cultural evidence of use and deliberate dispersal;

2.     analyse chloroplast and nuclear (ribosomal) genetic data to detect the genetic signature of recent, rapid expansion within NNSW;

3.     exclude alternative explanatory scenarios through the integration of complementary sources of evidence, and by comparing the findings from NNSW to a representative sample from the Australian Wet Tropics (AWT), where ecological (Rossetto et al., 2015) and prehistoric cultural circumstances differ (Cosgrove, Field & Ferrier, 2007; Ferrier & Cosgrove, 2012).

Results and discussion

Anthropological evidence for the use and dispersal of black bean seeds

Anthropological evidence was revealed by Rossetto et al. for prehistoric dispersal by Aboriginal people by verifying that Aboriginal people used the species; and several sources that included Songlines (Dreaming tracks) that describe deliberate movement of this species by Aboriginal people. Linguistic evidence could neither support nor negate the hypothesis of human dispersal and lateral languages transfer.

This study found many historical records from the colonial period (Maiden, 1899; Ferrier & Cosgrove, 2012) that described detoxification and food preparation methods of C. australe seeds by Aboriginal people in NNSW. There are also many ethnographic records that describe other uses of C. australe by Aboriginal people from the AWT (Birtles, 1997; Dixon, 1983; Coyyan, 1918) including:

·        The use of bark fibre for fish and animal traps, nets and baskets;

·        wood for spear throwers; 

·        seed pods as toy boats; and

·        as a seasonal cue for jungle fowl hunting.

The study corroborated the usefulness of black bean as a food resource through ethnographic interviews with 5 NNSW Aboriginal knowledge custodians in 2016 (S1 and S2 Appendices).

It has been revealed by mtDNA studies that Aboriginal people have inhabited Australia in consistent geographic arrangements for up to 50,000 [Recent dating 65,000 years (Tobler et al., 2017) see Australian Occupation of Northern Australia by Humans 65,000 years ago]. The strong connection to country by local Aboriginal communities, who, over time, maintained knowledge via oral transmissions, was facilitated by continuous regional persistence. Physical pathways are associated with traditional Aboriginal Songlines (Dreaming stories/tracks) that were traversed by Aboriginal people and for which specific songs and stories were told to pass on and maintain knowledge.

Rossetto et al. recovered 3 Dreaming stories that relayed the movement, maintenance and sign significance of C. australe in NNSW (S1 Appendix), of which the Nguthungulli Songline told by Ngarakbal woman Charlotte Brown and recorded by Roland Robinson in the 1950s (Robinson, 1989) is the most pertinent. According to this story Nguthungulli (an ancestral spirit that likely represents a real person) carried and left “bean tree” (C. australe is the only local species being commonly referred to as “bean tree”) seeds as he journeyed inland from the east coast to the western Ranges (S1 Appendix point 1.2). In this study, the Songline was traced for the first time on a topographic map by a local Aboriginal man, Oliver Costello, and traditional pathway expert, Ian Fox). They believe, based on their intimate cultural and migration knowledge of the region, that like many Aboriginal pathways which followed points of high elevation for ease of access and vision, the Nguthungulli Songline traverses the ridges of the Nightcap, Border and McPherson ranges which divide New south Wales from Queensland. The relevance of this pathway is that the ridges of the Nightcap ranges coincide with the top of the drainage basin for the Tweed River, and the southern face of the Border and McPherson ranges coincide with the top of the drainage basins for the Richmond and Clarence Rivers. The sampling sites of this study for the genomic analyses are represented by these catchments. From the perspective of Aboriginal knowledge, these stories confirm that Aboriginal people used black bean seeds as food in prehistoric times and moved them around the landscape deliberately, including along ridgelines of NNSW.

Vertical inheritance, language-internal replacements, sound mutations that accumulate slowly, shifts in meanings, or lateral transfer, shape histories of individual words. The geographic range of C. australe coincides with Pama-Nyungan language family (Bowen & Atkinson, 2012). Rossetto et al. identified linguistic terms for C. australe in 8 linguistic subgroups of the eastern clade of the Pama-Nyungan language family (S3 Appendix).

Included within the Bandjalangic clade are the languages of NNSW, and the most common ancestors (MMCA) of which is likely to be close to 1,500 years old  (C. Bowens pers, comm.). Common inheritance from the MRCA results in Bandjalangic vocabulary being inherited with only a few sound changes (45), and the word for C. australe is uniformly bugam. This contrasts with the rest of the distribution of C. australe where little homology is exhibited by the terms, even within members of the same low-level clade such as the Djirbalic languages from the (AWT) (S3 Appendix).

Positive diagnosis of inheritance with modifications by the absence of mutation of any of the phonemes in bugam, though it is also in line with a scenario of locally recent dispersal of black bean. It is suggested by the divergence with words for C. australe from both neighbouring and more distant language clades, that lateral transfer of bugam into post-MRCA Bandjalangic from external sources is not probable. Therefore, while alternatives are possible it is most likely that as the Bandjalangic languages expanded into their current territory, or diversified in situ, they inherited bugam continuously from their MRCA.

Genomic evidence of rapid, recent and widespread expansion from their MRCA

It was confirmed by the combination of ethnographic data and first-hand corroboration by Aboriginal custodians of traditional knowledge from NNSW that C. australe was a valuable local traditional resource plant and was likely to have been moved intentionally by Aboriginal people across the focus area of the study. The distribution of this tree within the framework of dispersal by Aboriginal people was interpreted further by sampling the local genomic variation.

Rossetto et al. used genomic analyses to search for a signature of the rapid local expansion expected from the human-mediated timeline that was set by archaeological evidence by the use of techniques to detoxify the seeds (Cosgrove, field & Ferrier, 2007). The detection of single nucleotide polymorphism (SNP) from low-coverage genomic sequencing can reveal small amounts of variation within- and between-population variation that enables the exploration of fine-scale patterns of dispersal even in non-model species with low diversity (McPherson et al., 2013; Rossetto et al., 2015).

This study analysed a total of 1224,678bp of chloroplast DNA (cpDNA) and 5,813bp of nuclear ribosomal DNA (nrDNA) and compared the results with C. australe sites, comprising 8 individuals each, catchments and regions. 987 cpDNA SNPs (0.749% of sequence analysed) and 29 nrDNA SNPs (0.50% of sequence analysed), were yielded by analyses of sequence data across 96 individual trees from 12 distinct sites. Between 4 and 12 heterozygotic variants across 5,813bp, which confirmed a pattern of low diversity within the population. 

In species that are dispersed by water, the results of landscape restraints can be local patterns of localised relatedness and population level cpDNA uniformity that is observed across the distribution of C. australe (Kondo, Nakagoshi & Isagi, 2009). In NNSW, however, genomic homogeneity extended across entire catchments, with every site sampled from within each catchment belonging to the same lineage, regardless of geographic distances and topography. A single, unique, fixed SNP was found in the Big Scrub site within the catchment of the Richmond River. Conditions of the landscape need to be favourable for long-distance and directed dispersal of seeds along water bodies for Hydrochory to generate patterns of cpDNA within catchments (Nilsson et al., 2010). The altitudinal heterogeneity and geographic scale that is typical of the southern distribution of C. australe is, however, not likely to favour rapid inland expansion that is mediated by water.

Spatial aggregation of individuals that are genetically related can also be reduced by Hydrochory with the result that high levels of genetic divergence between catchments (Nilsson et al., 2010; Kondo, Nakagoshi & Isagi, 2009). Though the samples from the northern AWT distribution of C. australe fit the pattern that is expected of high differentiation between catchments, the sites in NNSW do not. In the north high diversity was detected, where there were considerably more unique SNPs across 3 AWT sites (509 in cpDNA, and 3 in nrDNA) than across 9 NNSW sites (6 in cpDNA, and none in nrDNA. In NNSW, genomic homogeneity extended across 3 catchments covering a large area (30,604 km²) that was topographically complex, from sea level to an elevation of 1,166 m, across multiple ranges that are dissected, crossing the Clarence River Corridor into the Orara catchment, which was an important biogeographic barrier that can restrict genetic connectivity even in species that are easily dispersed (Rossetto et al., 2015).

It is implied by this that, unlike the comparative sample from the AWT, that exhibits a high level of diversity among 3 adjacent catchments that cover a smaller area, 6,550 km²; from sea level to an altitude of 783 m; all NNSW populations that have been sampled are derived from recent dispersal events that were sourced from 1 or a very small number of maternal lineages that were closely related. Rapid expansion within the southern range of the species is further supported by the non-accrual of unique, catchment-specific nrDNA variation, as it is expected from ancient processes, that there would be accumulation of detectable distinctive mutations (Ossowski et al., 2010). These findings match the expectations of population genetics from the recent Aboriginal dispersal scenario that is suggested by anthropological, cultural and linguistic evidence.

Exclusion of alternative rapid, southern expansion scenarios

According to Rossetto et al. when their findings are combined with recent Aboriginal dispersal as the most parsimonious explanation for the current distribution in NNSW, though there are other interpretations that could be proposed for some aspects of the data that is presented. Recent, rapid population expansions have also been observed in natural post-glacial settings (Hewitt, 2000), are suggested by landscape genetics patterns. C. australe would have been restricted to a small refugial population within NNSW during the Last Glacial Maximum (LGM) in a natural post glacial expansion, and a single founder lineage would have expanded rapidly to its current distribution as habitat became increasingly available. It is suggested by environmental niche models that represent the availability of climatic conditions suitable for C. australe during the LGM that there is likely to have been an increase in habitat that is available in the current interglacial period, and the environmental suitability in the south remains marginal compared to the north. The increase in suitable habitat that was modelled fits with the proposed recent dispersal that was mediated by humans, following the pursuit of resources that were newly available (Cosgrove, Field & Ferrier, 2007), and the scenario of natural expansion that was also proposed for other local trees (McPherson et al., 2013; Rossetto et al., 2004). The latter processes, however, invariably rely on dispersal mechanisms that are efficient and that are not available to C. australe in NNSW.

The contribution of rapid, recent geographic expansion, which was mediated by water, along coastal areas and along waterways that were low lying (potentially even derived from a northern source) cannot be excluded. Oceanic currents, tidal processes, extreme weather events or the capture of rivers cannot, however, explain the location of multiple inland sites, as well as above current and historical sea level (Helman et al., 2010). Secondary movement of species that are water-dispersed inland away from the riparian zone, to upland areas, or between catchments is often performed by animals (Nilsson et al., 2010).

Within Australian rainforests the movement of species that have large seeds is restricted by the limited number of functional classes of fauna that disperse fruit irrespective of the availability of habitat (Rossetto et al., 2015). As a consequence the distribution and assembly of Australian rainforest plants is impacted by the type and size of fruit. Significantly larger geographical ranges are occupied by species that produce small, palatable fleshy fruits than species that produce fruits that are poorly dispersible, and landscapes that are recolonised lack the component of the flora that produce large fruit (Rossetto et al., 2015). A zoochory (animal dispersal) hypothesis for the current distribution of C. australe is therefore at odds with the large, toxic seeds that have no reward for the fauna to disperse them.  Even within the AWT, where the highest diversity of frugivorous animals persists, which includes the cassowary, the remaining representative of the rainforest megafauna, the high genetic diversion that has been measured between neighbouring catchments suggests that zoochory does not play a critical role in maintaining a connectivity among populations of C. australe. An alternative scenario that involves the potential contribution of megafauna that are now extinct is also doubtful, as the timeframes that are involved in the loss of large rainforest vertebrates are too extended (Johnson, 2006) to justify the genomic homogeneity that has been detected in NNSW.

Conclusions

The new combined evidence that is presented supports deliberate dispersal by prehistoric Aboriginal People as this is the interpretation that is the most parsimonious for the distribution of the species in NNSW. It has been suggested (Furrier & Cosgrove, 2012) that in the AWT, the expansion of aboriginal dwellers in rainforest during the Late Holocene, 2,500-1,000 BP, could have been facilitated by the development of techniques for the detoxifying rainforest nuts such as C. australe, which became critical technologies that aided survival in areas where these resources were available. It was demonstrated by Rossetto et al. that the inverse was also true: Food preparation technologies were developed by local Aboriginal communities that had a deliberate impact on the distribution of culturally important rainforest species. Aboriginal influence on the distribution and assembly of species was largely ignored by early European colonists in Australia, apart from obvious fire-related impacts. The studies of Rossetto et al., as well as those of other researchers, can help to expand cultural heritage management practices by promoting the need to maintain living biotic heritage, in this case, groves of C. australe in collaboration with Aboriginal custodians of knowledge.

Evidence of dispersal of plant propagules by prehistoric Australian Aboriginal people for their direct need and benefit also significantly challenges assumptions of “natural” distributions of plants, requires reassessment of distribution interpretations that do not include the possible impact of prehistoric intervention by humans (Levis, 2017). Rossetto et al. suggest that current debates on the role of migration that was human assisted (Corlett, 2016) and other active management options could also benefit from the acceptance, from practitioners of conservation as well as the general public, that in the past species were deliberately dispersed by Aboriginal people. As current measures of the success are often based on historical (pre-European) reference systems, this is particularly relevant.

Now that the role of Aboriginal dispersal has been established regionally for C. australe, studies in the future can explore the broader biogeographic questions, such as possible routes along eastern Australia and across the pacific islands. Aboriginal knowledge custodian Uncle Ron Heron proposed independently a scenario of long-distance dispersal by ancestors from the north. (S1 Appendix, point 1.7).

Rossetto, M., et al. (2017). "From Songlines to Genomes: Prehistoric Assisted Migration of a Rain Forest Tree by Australian Aboriginal People." PLoS ONE 12: e0186663.