Resprouting as a key functional trait in woody plants – challenges to developing new organizing principles
Sprouting behaviour workshops, Working Group 67, ARC-NZ Research Network for Vegetation Function, Armidale, Australia, 2009–2010
Most global biomes are shaped by disturbances, such as fire or herbivory, that damage or kill the aboveground biomass of plants. In many of these biomes, however, the damaged plants do not die; rather, they persist through sprouting. In disturbance-prone environments, resprouting from meristems stabilizes plant populations where disturbance may cause demographic bottlenecks. The advantage of resprouting is that it confers persistence under disturbance; however, sprouting has disadvantages such as potentially reducing sexual reproduction and limiting gene flow (Bond & Midgley, 2001; Lamont & Wiens, 2003). Understanding resprouting is critically important for understanding long-term vegetation dynamics, extinction risks, carbon balance and woody plant management. A Vegetation Function Working Group (Working Group 67; http://www.vegfunction.net/wg/67/67_Sprouting.htm) was established in 2009 to identify challenges encountered in developing coherent models of the functional role of resprouting in fire-prone environments, with an emphasis on savanna and Mediterranean biomes. Fire is the most pervasive disturbance and is integral to the evolutionary ecology of these biomes. This broad disciplinary group met at the International Ecological Conference (INTECOL) in Brisbane in September 2009 and reconvened in July 2010 at The University of New England, Armidale, Australia, to review progress. In this report we highlight major challenges encountered in developing unifying models of the functional role of resprouting.
‘...to advance our understanding of sprouting dynamics in disturbance-driven systems, we need novel ways to incorporate ontogeny and spatio-temporal variation into resprouting typologies’
Resprouting typologies: beyond dichotomies
Disturbance has a binary effect on plant individuals – they either resprout or die. However, current classifications of species as resprouters or nonsprouters are based on a continuum of population responses to disturbance, and lack the understanding of individual mechanisms required to inform demographic analysis of response to disturbance. Thus, classifications that address both individual and population-level responses are desirable, and a primary aim of the working group. Simple dichotomous classification masks the variation in how plants are able to resprout, as well as the ontogenetic and environmental variation that occurs in resprouting. Some plants have a thick bark, others have deeply embedded meristems and others store massive amounts of resources in underground organs. Similarly, some biomes are dominated by intense, infrequent crown fires, whereas others have frequent, less-intense fires. Hence, to advance our understanding of sprouting dynamics in disturbance-driven systems, we need novel ways to incorporate ontogeny and spatio-temporal variation into resprouting typologies. Progress in understanding the ontogeny of resprouting has been made (Burrows, 2002) and classifications have been developed in terms of bud bank location (del Tredici, 2001; Klimešomá & Klimeš, 2007). In addition, classification schemes have been proposed to deal with plant response to disturbance severity (Bellingham & Sparrow, 2000). Future typologies should not only incorporate the disturbance regime, but also bud bank location, bud protection and the stages of plant development at which sprouting occurs. By considering bud anatomy and location, how these buds are protected (growth, bark thickness, bark growth rates) and how these buds are resourced, these three axes capture most of the variation in sprouting response to fire. An important outcome of the working group is to develop a classification scheme based on the Buds–Protection–Resources approach of characterizing sprouting responses.
Resource economies: functional drivers of resprouting ability
For global trait analyses of resprouting response we need to know what bud locations drive resprouting and to what extent storage is necessary to subsidise resprouting (Vesk & Westoby, 2004a). These bud and reserve economies will vary along a continuum of growth forms from perennial herbaceous to woody plants and reflect the risks of physical injury. A wealth of data exists for reserve economies in herbaceous and, to a lesser extent, shrub species, but syntheses are lacking in the context of resprouting ability. For example, we know that shrub resprouters in fire-prone heathlands generally allocate more resources to root than shoot biomass and store larger carbohydrate reserves for resprouting after fire than do nonsprouters (Bell & Ojeda, 1999; Verdaguer & Ojeda, 2002; Knox & Clarke, 2005). Whether this is the case for woody species in fire-prone mesic and semi-arid savannas is largely unknown. In forests, resprouter tree species not subjected to frequent fire lack the adaptive allocation and carbohydrate reserve-formation strategies exhibited by fire-prone resprouters, while in forests subjected to severe wind damage, individuals tend to be basal sprouters and multistemmed as a consequence. By contrast, in some forest systems with low, but pervasive, levels of disturbance, trees appear to be able to mobilize resources from both their belowground and aboveground reserves (Nzunda et al., 2008).
The storage of nonstructural carbohydrates can occur by accumulation and/or reserve formation but its role in resprouting has only recently been assessed (Knox & Clarke, 2005; Nzunda et al., 2008). While the seasonal allocation of resources in plants has frequently been explored, the comparative reserve economies of woody plants with contrasting resprouting abilities in seasonal environments are largely unresolved (cf. Schwilk & Ackerly, 2005). For example, generalizations about the effects of seasonal water stress and resprouting in Mediterranean-type environments are well known (Ackerly, 2004) but such generalizations for savannas are yet to emerge (Schutz et al., 2009; Wigley et al., 2009).
Life history trade-offs and competitive abilities: linking precision and generality
Comparative studies of taxa with contrasting resprouting ability have highlighted life history trade-offs that manifest in contrasting allocation, reproduction and, ultimately, demographic rates (Enright & Lamont, 1992; Schwilk & Ackerly, 2005). Remarkably, growth rates of congener nonsprouters and resprouter shrub seedlings have been shown to be similar (Knox & Clarke, 2005), suggesting leaf-level adjustment where carbon assimilation may be enhanced to meet the demands of resprouting (Paula & Pausas, 2006). In fire-prone systems, resprouters allocate more resources to storage, they tend to have lower seed output and low seedling recruitment rates, and their saplings take longer to reach maturity than nonsprouters (Bell et al., 1996; Bell & Ojeda, 1999), giving rise to the notion of a persistence vs reproduction trade-off relating to resprouting ability (Bond & Midgley, 2001). It remains to be seen how these attributes act to cause variation in seeder : sprouter ratios in various biomes. The utility of the persistence niche concept in understanding community pattern and co-existence has been demonstrated in a range of communities (Clarke & Dorji, 2008), but its usefulness in explaining community patterns in some disturbance-driven ecosystems needs testing. For example, most eucalypts are strong resprouters, yet produce abundant seed, so there appears to be no clear reproductive trade-off in the eucalypts. In addition to reproductive trade-offs, resprouters are often multistemmed and shorter than related nonsprouters and may be outcompeted by them when disturbances are rare. Recently, the utility of this concept was tested by a combination of field and glasshouse studies, where it was shown that seedlings of resprouters have better competitive abilities in grassy communities than congener nonsprouters (Clarke & Knox, 2009). These advances highlight the link between species-level resprouting traits and community-level processes that have important consequences in a changing world.
Emerging models of landscape resprouting patterns
Bold attempts at synthesizing global data on resprouting ability have begun to advance predictive models of resprouting (Pausas et al., 2004; Vesk & Westoby, 2004b). Conceptual models argue that the evolution of resprouting is driven by gradients in disturbance and/or site productivity (Bellingham & Sparrow, 2000) and these are being supported by more recent regional-scale comparisons in fire-prone landscapes that are being synthesized by the working group. These models are also being tested in relation to other forms of landscape disturbance (e.g. cyclones, earthquakes and drought), where advances are being made by comparing disturbance types (Franklin et al., 2010).
Vegetation dynamics and climate change
Climate change will affect disturbance regimes and it may affect the patterns of carbon accumulation in both aboveground and belowground organs in woody plants. Both of these, in turn, will alter resprouting responses and community dynamics (Bradley & Pregitzer, 2007). Increased atmospheric [CO2] is predicted to favour the establishment of woody plants over grasses and of resprouters over nonsprouters because starch stores may be increased (Bond et al., 2003). For example, Eamus et al. (1995) explored the effect of elevated [CO2] on root suckering in Eucalyptus tetrodonta in the mid-1990s and found a strongly positive response. However, the interactive effects of disturbance and increased [CO2] on the resprouting ability of woody plants in field experiments has yet to resolve whether increased atmospheric CO2 will favour resprouting because of allocation to storage, and if increased disturbance frequencies negate any net carbon gain to resprouter species. If increased [CO2] confers an advantage to resprouters and root suckers, this knowledge is important for land management and in understanding resprouting responses and will determine what land-use practices are appropriate under elevated [CO2].
Unravelling the complexities of plant resprouting in a changing world is a major challenge for plant biologists during the next decade. A conceptual framework for understanding the functional role of resprouting has emerged over the past decade, especially in fire-prone ecosystems, but the molecular basis for this syndrome remains unresolved. Equally, the resource economies of resprouting across plant growth forms are surprisingly poorly understood, as are hard-trait data on bud/meristem economies. Reviving the traditions of plant anatomy and allocation physiology will help in these endeavours, in collaboration with the work of molecular biologists. At landscape scales there is a growing recognition of ‘resprouting ability’ as a global functional trait that has predictive utility in understanding global vegetation boundary changes and woody : grass ratios. Bringing together diverse plant disciplines in meetings has developed a new resprouting typology and synthesized regional, national and global taxon-level description of resprouting ability; we encourage plant biologists to take up these and other challenges to develop better organizing principles for understanding plant resprouting.
William Bond, Ross Bradstock, Geoff Burrows, Mike Cramer, Neal Enright, Rod Fensham, Phil Groom, Lindsay Hutley, Kirsten Knox, Hans Lambers, Byron Lamont, Fernando Ojeda and Samantha Setterfield all participated and contributed to resprouting discussions as a part of Working Group 67, ARC-NZ Research Network for Vegetation Function.