Flowering plants had small beginnings in Gondwana during the Mid-Cretaceous (100 Ma) but the Proteaceae was abundant in Antarctic temperate rainforests by the Campanian (71−84 Ma)
]. However, our analysis shows that recurrent fire must already have been influencing the path of evolution among Proteaceae by the Mid-Upper Cretaceous (84−89 Ma) and has continued as a strong agent of selection ever since, based on the continual appearance of fire-tolerant clades (Figure
). The chronogram and trait assignment analysis indicate that ancestors to the dry indehiscent-fruited section of the family, the subfamilies Proteoideae and Symphionematoideae, were already present in fireprone habitats by that time.
Proliferation of lineages assigned to fireprone and non-fireprone habitats at 10 My intervals from the estimated time of origin of the Proteaceae (collated from Figurea).
Did these clades actually exist by then? The fossil record supports the existence of pollen with affinities to at least two extant genera in the Proteoideae, and 17 pollen types whose Proteaceae affinities are less prescribed, in eastern Gondwana (Zealandia, southern Australia – especially the Otway Basin,) during the Santonian-Campanian (86−71 Ma)
]. Dettmann and Jarzen
] concluded that the southern Australian/Antarctic vegetation in this period must have been a mosaic of rainforest (though the angiosperm element would not have been dominant) and sclerophyll communities, with the Proteaceae prominent in the latter (Sauquet et al.
] discredit most of their identifications at genus level but this does not invalidate their clear Proteaceae affinities that are not in dispute).
Did suitable habitats exist by then? By 90−85 Ma most of the current Australian portion of Eastern Gondwana had emerged due to sedimentation (high rainfall) and general elevation of the continent
], including the Otway, Eromanga and Murray Basins. The sedimentary basins: Eucla, Officer and Surat, were already exposed by 100−90 Ma. In addition, various metasediments were uplifted/downwarped in the lower-mid-Cretaceous (Stirling−Barren Ranges in SW Australia, Great Dividing Range, Victorian Southern Uplands
]). Heavy leaching due to the high but seasonal rainfall during the Upper Cretaceous created oligotrophic sands and ferricretes
]. There has even been the suggestion that the Proteaceae was a (mainly Cenozoic) driver in this process
]. Thus, well-drained, nutrient-poor substrates (sands, sandstones, quartzite, schists, laterites) of variable elevation and suitable for colonization by the evolving sclerophyll element were already widespread.
Were these habitats also fireprone? Not only were carbon dioxide levels and mean temperatures much higher than currently (favouring high productivity)
] but calculated oxygen levels 80−90 Ma were 25% higher (Figure
]), all greatly enhancing flammability. Bond and Scott
] note in addition strong seasonality, frequent lightning and charcoalified fossils peaking at 65–105 Ma, though these values are biased towards the Northern Hemisphere. The presence of indehiscent-fruited Proteaceae in fireprone habitats for the first time at 88 Ma coincides with the peak or just postpeak atmospheric levels of oxygen, carbon dioxide, temperature and burn probability in the presence of an ignition source over the last 150 My (Figure
]), bearing in mind that crown Angiosperms appeared about 135 Ma
]. The nutrient-impoverished substrates where sclerophyllous Proteaceae are favoured would have supported dense, shrubby evergreen vegetation with highly flammable foliage particularly vulnerable to lightning ignition at this time. The Proteoideae itself would have contributed to this flammability: small, acicular or highly divided isolateral leaves, finely divided foliage, highly sclerophyllous, long-lived leaves with low nutrient content and poorly decomposable litter
Figure 3 Mean atmospheric conditions over the last 150 million years. From top to bottom, oxygen and carbon dioxide concentrations, annual global temperature, and ignition probability of plant matter. Broken horizontal lines correspond to ambient levels. Shaded (more ...)
Is there direct evidence of fire at that time? Abundant charcoal is recorded in the Eromanga Basin, SW Queensland, at 100–94 Ma
]. Charcoal was noted among pollen samples in Zealandia at 94–85 Ma
], together with other evidence “suggesting a generally broad occurrence of fire in the mid-Cretaceous across middle to high latitudes in the Southern Hemisphere” that the authors attributed in part to the high atmospheric oxygen. Charcoalified fragments (‘black wood’) made up 40% of the microsamples that contained pollen of > 7 Proteaceae species (including several with suggested Proteoideae affinities) in Zealandian sandstones at 88–71 Ma
] indicating that “wildfires were part of the Late Cretaceous ecosystem”. Eklund et al.
] studied 83-My-old charcoalified mesofossils of Angiosperms between Antarctica and Australia that they attributed to fires caused by volcanism near the collection site.
Was there selection against the fire-sensitive ancestors that might have biased the assignments? Figure
shows that net lineage proliferation at the generic level has continued steadily and in parallel for both fireprone and non-fireprone groups. This means that fire-sensitive clades did not become extinct at the expense of fire-tolerant clades that might have distorted the analysis – this is consistent with both being accommodated in different vegetation types through time preventing their extinction
]. If extinction was recent
it would have to be on a massive scale to delete all trace of the non-fire-tolerant lineage. It seems that even during the last glacial maximum, rainforest species in eastern Australia, including Proteaceae, were able to survive in moister lowland refugia
]. Further, if (unrecorded) extinction of fire-sensitive taxa had occurred along basal
stems of clades that our analysis currently assigns as in fireprone habitats, this would not alter the assignment as this (correctly) infers that the surviving lineage was fire-tolerant at that point in time. The only requirement then is to show that the lineage actually existed at that time via fossil evidence. In this regard it is noteworthy that 15 of the 26 pollen/leaf types assessed by Sauquet et al.
] were allocated to the base of extant rainforest clades or sediments arising > 88 Ma, i.e. prior to the oldest time that our analysis identifies fireprone habitats for the Proteaceae. In addition, five are associated with younger rainforest clades, ten with fireprone habitats, and all 26 can be traced to extant genera (though few could be confidently assigned to any one), i.e. none necessarily implies an extinct lineage.
A related problem with the purported origin of the three extant fire-tolerant Proteaceae lineages in the Upper Cretaceous (Figure
a) is the possible exterminatory effect of the subsequent early Eocene (40–56 Ma), one of the wettest periods known. Indeed, fire-derived inertinite in coal dropped markedly in Northern Hemisphere mires after 60 Ma
]. While the climate was especially wet and aseasonal throughout eastern Gondwana during the Eocene, it remained warm (except in the Tasmanian region) and much of the Central-West zones of the Australian portion of Gondwana had moderate and strongly seasonal rainfall
]. Atmospheric oxygen levels were up to 15% higher than currently and burn probability was the highest for the last 60 My (Figure
). Further, deeply weathered sands or siliceous/lateritic rocks, often in open, well-drained parts of the landscape, were widespread and would have provided ideal refugia for the sclerophylls, especially Proteaceae, in their own communities
]. Indeed, the Proteaceae (Banksia
-like wood, pollen akin to Petrophile
) at Lake Lefroy, SWA in the mid-Eocene accounted for 34% of all pollen (when Nothogfagus
was omitted), with species richness values comparable with those in SWA scrub-heath today
]. Interestingly, where fire did occur around the eastern Otway Basin, it not only led to a severe reduction in Nothofagus
but also in Proteaceae and Myrtaceae
], implying that the species there were more vulnerable to fire than their western counterparts
We therefore suggest that much of the fire-dependent, sclerophyll element contracted west during the Eocene. Some of these returned/expanded in a second wave of migration during the Oligocene-Miocene (e.g. Banksia
) but usually remained poorly represented (e.g. Adenanthos
), others did not return (e.g. Franklandia
), while others only arose then but never reached eastern Australia (e.g. Dryandra
). In support, Figure
shows no increase in proliferation rates of non-fireprone-habitat lineages at the expense of fireprone lineages in the 40–60 My period; if anything the reverse is true. In addition, we point to the exacerbated bias against increasingly isolated pockets of sclerophyll vegetation in the fossil record from lake sediments during particularly wet periods, and note that strongly fire-adapted Pinus
in the NH (fossils) and Nuytsia
in SWA (molecular dating) have also been recorded from the mid-Eocene
Finally, the two seed storage mechanisms that facilitate postfire germination and seedling recruitment were already appearing 88−81 Ma according to our analysis, though neither type prevailed in any clade, indicating that much diversification and extinction along the major stems must have been occurring. By 81 Ma, seed storage was firmly established in one basal clade. By 71 Ma, clades in fire-prone habitats were characterized by either soil or on-plant fruit storage (except for continuing variation in the Beauprea
clade). Note that the two rainforest genera in Proteoideae, Eidotheia
, did not speciate to any extent (or suffered almost complete extinction), while two remained monotypic (Agastachys
) or had limited speciation (Beauprea
) in genera with populations or species respectively largely remaining in rainforest today. In particular, only Beauprea
among the seven genera occupying mixed habitats has the capacity for seed storage, though it would be of interest to know why this once-widespread genus became extinct in Australia. The only genera lacking strong speciation once in fireprone habitats are Beaupreopsis
, with a small soil-stored pyrene, that occurs in scrub-heath of New Caledonia and is monotypic (44), and Symphionema
with two species in scrub-heath of NSW and possesses a thin-walled achene “expected to show some form of dormancy”
]. Comparing speciation rates overall between fireprone-habitat and non-fireprone sister clades (Figure
k), the pivotal role of seed storage for successful occupation of fireprone habitats is supported (Figure
a) and the two are highly correlated through time (P
< 0.001) confirming their classification as true fire adaptations.
The mechanism of seed storage on the plant is different between the Grevilleoideae and Proteoideae: in the former, woody fruits protect and support the seeds and dehisce in response to heat and desiccation while, in the latter, bracts (assisted by branchlets in the case of Aulax
) protect and support the fruits and spread to release the single-seeded fruits in response to heat and desiccation. This has arisen four times independently in the Grevilleoideae, and four times in the Proteoideae (Figure
a). While they were treated as the one trait for purposes of the analysis this did not create origin artefacts as the two subfamilies remained independent with respect to the evolution of serotiny in the family.
All soil-stored seeds are actually one-seeded fruits in the Proteaceae (except Grevillea
), comprising a thin pericarp (swollen at the base to form an elaiosome in the Adenanthos–Mimetes clade, Figure
a), exotesta (of varying thickness and texture) and crystalliferous endotesta
]. The succulent-fruited Persoonieae (Persoonioideae) had an independent origin from the dry-fruited Proteoideae/Symphionematoideae that appeared independently five times (Figure
has a possible sixth independent origin where our informal analysis of a cladogram for 62 of its 96 taxa
] indicates that the ancestral state is serotiny with winged fruits followed by dormant nutlets and soil-stored achenes, followed much later by a few species with elaiosome-bearing achenes – this requires more detailed research, especially the need for smoke-stimulated germination throughout the genus. This is the only genus that had to be assigned mixed traits – in all others the assigned trait was part of the circumscription of the genus or shown to be the ancestral condition (Banksia
, Lamont and He unpublished). The separate origins of soil-storage in the Stirlingia–Synaphea
(71 Ma) and Franklandia–Mimetes
(74 Ma) clades do not merge in the analysis (Figure
, with its exotesta modified into a brittle wing or aril attractive to ants, is unique among the dehiscent Proteaceae and had no effect on the outcomes for ancestral assignments of soil-storage.