Geoffrey E. Burrows

Resprouting as a key functional trait: how buds, protection and resources drive persistence after fire

Resprouting as a response to disturbance is now widely recognized as a key functional trait among woody plants and as the basis for the persistence niche. However, the underlying mechanisms that define resprouting responses to disturbance are poorly conceptualized. Resprouting ability is constrained by the interaction of the disturbance regime that depletes the buds and resources needed to fund resprouting, and the environment that drives growth and resource allocation. We develop a buds-protection-resources (BPR) framework for understanding resprouting in fire-prone ecosystems, based on bud bank location, bud protection, and how buds are resourced. Using this framework we go beyond earlier emphases on basal resprouting and highlight the importance of apical, epicormic and below-ground resprouting to the persistence niche. The BPR framework provides insights into: resprouting typologies that include both fire resisters (i.e. survive fire but do not resprout) and fire resprouters; the methods by which buds escape fire effects, such as thick bark; and the predictability of community assembly of resprouting types in relation to site productivity, disturbance regime and competition. Furthermore, predicting the consequences of global change is enhanced by the BPR framework because it potentially forecasts the retention or loss of above-ground biomass.

Flammable biomes dominated by eucalypts originated at the Cretaceous–Palaeogene boundary

Fire is a major modifier of communities, but the evolutionary origins of its prevalent role in shaping current biomes are uncertain. Australia is among the most fire-prone continents, with most of the landmass occupied by the fire-dependent sclerophyll and savanna biomes. In contrast to biomes with similar climates in other continents, Australia has a tree flora dominated by a single genus, Eucalyptus, and related Myrtaceae. A unique mechanism in Myrtaceae for enduring and recovering from fire damage likely resulted in this dominance. Here, we find a conserved phylogenetic relationship between post-fire resprouting (epicormic) anatomy and biome evolution, dating from 60 to 62 Ma, in the earliest Palaeogene. Thus, fire-dependent communities likely existed 50 million years earlier than previously thought. We predict that epicormic resprouting could make eucalypt forests and woodlands an excellent long-term carbon bank for reducing atmospheric CO(2) compared with biomes with similar fire regimes in other continents.

Buds, bushfires and resprouting in the eucalypts

Eucalypts encounter a wide range of severe disturbances such as extensive defoliation by insects, major structural damage from cyclonic winds, as well as foliage and bark loss during drought and fire. Most healthy, mature eucalypts are not killed by these events, but regenerate vegetatively. With increasing intensity of disturbance, resprouting first occurs from the accessory buds in the small-diameter branchlets of the crown, followed by the epicormic buds in the medium- and large-diameter branches and stems, and then from the buds of the lignotuber. All these modes of regeneration are ultimately dependent on preventitious buds and, thus, the present review concentrates on axillary buds, their subsequent development into epicormic or lignotuber buds and their degree of protection from fire. The eucalypts have remarkably abundant, well protected and anatomically distinctive bud-forming structures in their leaf axils, branches, stems and lignotubers. These structures are quite consistent across this large genus, but are generally different from resprouting structures in many other plants. From an anatomical perspective, these structures seem best adapted to regeneration after fire, rather than damage from insects, storms or drought and this also correlates with ecological observations. On a worldwide basis, the eucalypts are some of the most successful post-fire resprouters, especially epicormic resprouting after medium- and high-intensity fires. Given the apparent ecological advantages of epicormic resprouting (the rapid reestablishment of extensive leaf area while simultaneously shading basal resprouters and seedlings) this could be an important factor in the success of eucalypts in Australia. Recent phylogenetic analysis has indicated a long relationship between eucalypts, fire and bud structures that facilitate resprouting.

A wide diversity of epicormic structures is present in Myrtaceae species in the northern Australian savanna biome – implications for adaptation to fire

Recent research has shown that the eucalypts of southern Australia have an unusual and apparently fire-adapted epicormic structure. By studying a range of myrtaceous species from northern Australia we hoped to determine if this structure was also present in northern eucalypts. We anatomically examined the epicormic structures from 21 myrtaceous species in 11 genera from the north of the Northern Territory, Australia. An extremely wide diversity of epicormic structures was found, ranging from buds absent, buds at or near the bark surface, to bud-forming meristems in the innermost bark. These Myrtaceae species displayed a far greater variation in epicormic structure than recorded in any other family. This is possibly a reflection of the importance of the resprouter strategy, a long fire history in Australia and the ecological diversification of the Myrtaceae. Nonetheless, all the investigated eucalypts (northern and southern) possessed the same specialised, apparently fire-adapted, epicormic structure. This is remarkably consistent given the taxonomic, geographical and morphological diversity of the eucalypts.

Seed production in woodland and isolated trees of Eucalyptus melliodora (yellow box, Myrtaceae) in the South Western Slopes of New South Wales

Seed production in woodland and isolated Eucalyptus melliodora Cunn. ex Schauer trees was investigated. Measurement of physical parameters such as mean capsule weight, mean seed weight and mean ratio of the weight of the capsule contents to the weight of the empty capsule showed no significant differences between woodland and isolated trees. In contrast, reproductive output as measured by mean number of seeds per capsule, mean number of seeds per 10 g of capsule contents and mean seed weight as a percentage of the weight of the capsule contents, was significantly lower (45–48% less) in isolated trees than in woodland trees. Mean percentage seed germination was also significantly lower (14% less) in the isolated trees and the mean number of viable seeds per 10 g of capsule contents was only 38% of the woodland trees. These results indicate that E. melliodora, like many eucalypts, has a mixed mating breeding system with preferential outcrossing but is also capable of self pollination leading to a reduction in seed yield and viability. The woodland and isolated trees produced a mean of 4.6 and 2.1 seeds per capsule, respectively. It would be relatively easy to collect large numbers of seeds from isolated trees of E. melliodora and subsequently propagate potentially genetically inferior plants.

Eucalyptus regnans (Myrtaceae): A fire-sensitive eucalypt with a resprouter epicormic structure

Determining the location of buds and bud-forming meristems and hence the level of protection from heat is essential to understanding plant response to fire. Most eucalypts resprout readily from the stem (epicormic resprouting) and the base after felling or high intensity fire. In contrast, Eucalyptus regnans is one of the few eastern Australian fire-sensitive, obligate seeder eucalypts. Some authors have suggested that the relatively weak epicormic resprouting is due to a lack of bud-forming structures. Epicormic strands from the bark and outer xylem of three very large trees and two saplings were examined anatomically. Epicormic bud-forming structures were found in all samples examined. The bud-forming capacity consisted of narrow, radially elongated strips of cells of meristematic appearance. These strips were continuous from the outermost secondary xylem through to the outer bark. Bark was relatively thick at the base of the large trees, but remarkably thin above this basal skirt. Eucalyptus regnans was found to possess the apparently fire-adapted epicormic strands previously described in other eucalypts, thus showing its fire-adapted lineage. However, this fire-sensitive species apparently directs much of its resources to rapid height-growth rates in younger trees, rather than to vegetative fire survival.

Leaf axil anatomy and bud reserves in 21 Myrtaceae species from Northern Australia

Dormant axillary buds allow plants to repair minor damage to their canopies. In woody plants, these buds subsequently develop into epicormic structures that may allow vegetative recovery after major disturbances. They are an essential but little‐studied part of the persistence niche. We wondered what bud reserves were present in the leaf axils of northern Australian myrtaceous species, what levels of protection they have, and how this relates to the ecology of these species. Axillary buds of 21 species from 10 genera of northern Australian Myrtaceae were examined anatomically. All species possessed axillary buds in all axils examined, and accessory buds were recorded in 86% of species. The species exhibited an extremely wide range of variation—from axillary buds that consisted of only an apical dome with no leaf primordia (Calytrix exstipulata) to axils with a complex array of accessory buds and meristems located beneath the axil surface (Corymbia and Eucalyptus). The axils of the Eucalyptus and Corymbia species had a greater number of and better protected axillary buds and meristems than the other species studied, including some of their closest relatives, Arillastrum, Allosyncarpia, and Stockwellia. All investigated species had an excellent meristem reserve for recovery of photosynthetic capacity after minor canopy damage and for developing epicormic structures for sprouting after more severe damage. The complex and well‐protected axillary bud or meristem structures of Corymbia and Eucalyptus may be an important component of the success of these genera in Australia.

Syncarpia and Tristaniopsis (Myrtaceae) possess specialised fire-resistant epicormic structures

On a worldwide basis epicormic resprouting after intense or crown fire is extremely rare, but is quite common in the eucalypts. Recent research has shown that the eucalypts have a highly modified epicormic structure that provides the bud-forming tissues with excellent protection from heat. A small number of non-eucalypts from the Myrtaceae have also been recorded as post-fire epicormic resprouters and it was considered of interest to determine whether this response was achieved through a similar or different structural adaptation. Leaf axils and epicormic structures of two species of Syncarpia and three species of Tristaniopsis were examined anatomically. Although the leaf axil anatomy of Syncarpia and Tristaniopsis was quite different (and different from that of the eucalypts), the epicormic structure was similar to that of the eucalypts, as the outer region of each epicormic strand possessed several strips of cells of meristematic appearance that were best developed in the innermost bark or even the outermost secondary xylem. As Syncarpia, Tristaniopsis and the eucalypts are only distantly related to each other within the Myrtaceae, it appears that this specialised fire-adapted epicormic structure may have developed multiple times within the family or originated from a common ancestor of the family.

Effect of boiling water, seed coat structure and provenance on the germination of Acacia melanoxylon seeds

Acacia melanoxylon (Mimosoideae or Mimosaceae) is a high quality timber tree with an extensive natural distribution in Australia and a wide genetic and phenotypic diversity. Seeds from three widely differing provenances in Tasmania were tested to determine whether they had different responses to various dormancy-breaking treatments. All provenances had limited germination (<11%) if seeds were untreated and between 85% and 91% germination after 40 days if the seeds were nicked. For all provenances short (≤60 s) exposure to boiling water gave high germination percentages. These values were generally lower, although usually not significantly so, than the germination percentages following nicking. Germination percentages decreased with increasing time of exposure to boiling water, although one provenance had a significantly greater tolerance to one of the longer (20 min) treatments. Nicked seeds germinated quickly and uniformly, whereas those subjected to the boiling-water treatments germinated after a longer period and more gradually. In untreated seeds, the lens was a low, elliptically shaped dome (~110–135 µm wide, 140–190 µm long). In more than 99% of the seeds examined, the structure of the lens was markedly altered after a 10-s exposure to boiling water. A wide diversity of altered lens structure was found, from a circular hole between the macrosclereids, to a short fissure where the macrosclereids did not separate to their bases. Nicked seeds had a 200–375 times greater area for water uptake than a fully disrupted lens and this was probably the principal reason why the nicked seeds germinated sooner and more rapidly.

Wollemi Pine (Wollemia nobilis, Araucariaceae) Possesses the Same Unusual Leaf Axil Anatomy as the other Investigated Members of the Family

Most leaf axils of most conifers are devoid of any bud-forming potential. Bycontrast, the numerous, apparently blank, leaf axils of the previouslyinvestigated species of the Araucariaceae possess unusual, if not unique,little-differentiated axillary meristems which have neither a bud-likeorganisation nor vascular or provascular connections with the central vascularcylinder. These meristems are exogenous in origin but are buried beneath thestem surface by the formation of localised periderms. Leaf axils fromplagiotropic branch shoots of juvenile and adult morphology and fromorthotropic leaders of adult morphology of the recently described Wollemi pine(Wollemia nobilis W.G.Jones, K.D.Hill & J.M.Allen)have been found to possess a anatomy similar to that previously described forthe Araucariaceae. Thus, W. nobilis is, on the basis ofits leaf axil anatomy, a typical member of the Araucariaceae.