Resprouting after fire
Resprouting after shoot damage is a widespread trait in all fire-prone (and many nonfire-prone) environments, and clearly is an ancient trait among plants generally (Pausas & Keeley, 2009). Although it was not possible to reconstruct the ancestral state at the root and early nodes in the Banksia phylogeny, we report the highest rate of switching between resprouting and nonsprouting among all pairs of traits examined. This agrees with earlier findings that whole-plant fire response is a highly labile trait in some genera (despite the fact that it is actually a syndrome of correlated traits; Lamont & Wiens, 2003) and has evolved independently and repeatedly in many lineages (Bond & Midgley, 2001).
Although some argue that resprouting after fire is an exaptation to fire that evolved in response to many other types of selection pressures, such as herbivory (Hopper, 2009), our work suggests that fire has at least had a major influence on the evolution of resprouting types in Banksia. This also highlights that resprouting should not be treated as a single trait in trying to understand its evolution, as resprouting via rhizomes and root suckers, in particular, is clearly an advanced growth form in Banksia. Banksias evolved towards clonality from 16 Ma (possibly 20 Ma) during the Miocene. Clonal species have the lowest stature of all growth forms in Banksia, and so are most vulnerable to ignition, yet their meristematic tissues are insulated by soil, a poorer conductor of heat than is bark. Thus, they are rarely killed by fire (Lamont, 1989; Drechsler et al., 1999; Burrows, 2002). Seeds make a negligible contribution to postfire population size, avoiding the risk of recruitment failure completely and conserving nutrients for vegetative growth, and ramet formation promoted by fire may be as effective, if not more so, than postfire seedling recruitment in population recovery (Lamont & Barrett, 1988; Enright & Lamont, 1989, Witkowski & Lamont, 1997). Lamont & Wiens (2003) have even argued that there is no mutational penalty either. The extreme longevity of clonal banksias (e.g. 1000 yr for B. candolleana, T. He and B. Lamont, unpublished data; 500 yr for B. goodii, Drechsler et al., 1999) attests to their success in surviving recurrent fire and drought, and also buffering changes in fire regimes that may have been marked in the Miocene (Hopper, 1979).
Evolution of serotiny and flammability
Serotiny has long been regarded as a fire-adapted trait (Lamont et al., 1991). The key to fitness is general seed release by fire in a time in which conditions are most conducive to germination and seedling recruitment, i.e. in the wet season immediately following fire, rather than storage as such, which can be seen as a general protective mechanism in a seed-limited environment. Drought might be considered as an alternative follicle-opening cue, although seeds would fall onto a less-ideal seedbed. In this regard, we observed 15% of follicles open 2 yr after severe drought in 2006–07 in a population of Banksia hookeriana (serotinous, and retaining its dead leaves and florets) with 120 plants (97% dead), and the six seedlings had all died by 2009. By contrast, a nearby population that was burnt in 2007, and thus experienced the same drought, had 100% follicles open among 117 plants (100% dead) with 117 seedlings (3% dead). As here, and with other serotinous banksias, there is little follicle opening following plant death caused by drought (Lamont & Barker, 1988; Lamont et al., 1991; Lamont, 1996), leaving fire by far the more effective cue in seed release and seedling recruitment.
Further support for fire rather than simply branch death as the critical cue for fruit opening is provided by the results here. We show that the retention of dead florets has been intimately associated with serotiny since the origin of Banksia in the Palaeocene. Combustion of the mantle of dead florets ensures that the critical temperature for melting the resin sealing the valves is reached (Lamont & Cowling, 1984). Further, these species have a higher temperature requirement for follicle opening, corresponding to their greater degree of serotiny (Enright & Lamont, 1988). In fact, the florets obstruct seed release in unburnt cones, especially where the mantle is so dense it conceals the follicles – shown here to have evolved over the last 20 My and only proliferating during the last 5 My – suggesting the ‘fine-tuning’ of both traits to the increasing fire proneness of southwest Australia in particular.
Alternative interpretations of dead floret retention seem to be implausible: shading the follicles from direct sunlight to prevent premature opening only serves to highlight the importance of delaying this until the ideal recruitment conditions are created by fire. If complete concealment of the fruits from granivores, such as the cockatoo Calyptorhynchus latirostris (Lamont et al., 2007), was critical for fitness, this should not have been delayed by 40 My, as these birds arrived long before the evolution of Banksia (Barker et al., 2004). The florets make a negligible contribution to flammability in terms of combustible carbon content of the above-ground plant (Witkowski & Lamont, 1996), if the aim was to ‘kill thy neighbour’ (Bond & Midgley, 1995), that gives the species a fitness advantage. If serotiny/seed release can best be considered as a fire-dependent trait and dead floret retention a fire-enhancing trait, and they originated and evolved together, it seems reasonable to conclude that Banksia evolved in a fire-prone environment. The rainforest sister groups of Banksia, here taken as Macadamia and Musgravea, lack both of these traits. A drought-prone environment is neither adequate nor conducive to the same pairing of traits (later evolution showed that they are optional and independent traits). Patches of sclerophyll vegetation occurred (probably in southwest Australia; Hopper & Gioia, 2004) among the rainforest clothing Australia at 61 Ma that could ignite at intervals shorter than the lifespans of the ancestral banksias (Enright et al., 1998), and these traits enabled them to invade and flourish there.
Is there also adaptive significance in the recent loss of serotiny and floret shedding among some species? Not only does floret shedding precede the loss of serotiny by 15 My (necessary in the absence of fire as noted above), but the latter began only 10 Ma. This is in special habitats in which plants may escape fire and where interfire recruitment is likely (Lamont & Connell, 1996): B. dentata is confined to savanna/grasslands (that arose world-wide 8 Ma; Edwards et al., 2010) where the almost annually occurring ground fires would fail to reach the cones of this tree, thus being ineffective as a seed release mechanism; B. verticillata (rock outcrops) and B. littoralis (swamp margins) are not reliably fire prone; B. integrifolia and B. grandis may be tall trees whose cones again may escape the heat from noncrown fires.
Surprisingly, the retention of dead leaves first appeared 35 My later than serotiny and floret retention, and is restricted to southwest Australia. Further, the retention of dead leaves has not coevolved with serotiny, in contrast with previous observations on pines (Schwilk & Ackerly, 2001). Dead leaf and branch retention have been suggested as fire-enhancing traits (Mutch, 1970). It has been hypothesized that dead biomass is more likely to increase combustion and ensure a complete burn of plants (Schwilk & Ackerly, 2001). Dead leaf retention in Banksia is strongly correlated with dead floret retention and also with the fire-killed response. Cowan & Ackerly (2010) reported that fire-killed shrubs in Californian chaparral had higher fractions of dead branches. We suggest that the retention of dead leaves ensures ignition of the florets and maximum but brief heating of serotinous cones in fire-killed banksias, where seed release/seedling recruitment is critical for postfire fitness. In this regard, our results do not support the expected correlation between high flammability and resprouting ability recently proposed by Gagnon et al. (2010). The minimization of heating of the surface soil via dead leaf retention is irrelevant to fire-killed species that store their seeds in their crown, as we have here.
The retention of dead leaves could also have another advantage for fire-killed banksias. Seedlings of fire-killed species have high growth rates (Pate et al., 1990) that imply great nutrient demand. Mineral nutrients stored in the retained dead leaves in fire-killed species (Witkowski & Lamont, 1996) are released after fire and will benefit offspring that establish under their dead crown, especially nutrients such as calcium that are not readily translocated into the seeds (Lamont & Groom, 2002). It has been noted that most fire-killed banksias are restricted to nutrient-impoverished sands, whereas resprouting species occur on more fertile lateritic soils (Lamont & Connell, 1996).
Fire as a selective force in the origin and evolution of plant traits
Our results show that the fire-dependent trait, on-plant seed storage, and the fire-enhancing trait, dead floret retention, have coevolved in Banksia since the first appearance of the genus 60.8 Ma, implying that fire was already an effective agent of selection then. Together, these two traits ensure maximum seed release when the conditions for germination and seedling recruitment, as created by fire, are optimal. The results of our analyses provide support for two hypotheses: (1) there has been a long association of (particular) land plants with fire (Pausas & Keeley, 2009), certainly well before the onset of seasonal aridity 25 Ma in parts of Australia (Hopper & Gioia, 2004); and (2) some plant groups have evolved a set of traits consistent with adaptation to particular fire regimes (Simon et al., 2009), including towards (or sometimes away from) more effective fire-related traits, such as dead leaf retention, clonality and a denser mantle of dead florets. We have shown that the mapping of certain traits, here putative fire-related traits, onto a chronophylogeny can be used to test evolutionary theory, providing powerful insights into the identity and time of origin of ancestral traits and the selective forces that have driven their evolution. Our findings open the way for new hypotheses on the role of fire in the origin and evolution of plant traits.