Heredity (2011) 107, 558–564 & 2011 Macmillan Publishers Limited All rights reserved 0018-067X/11 www.nature.com/hdy ORIGINAL ARTICLE Evidence for the equal resilience of Triodia spp. (Poaceae), from different functional groups, to frequent fire dating back to the late Pleistocene G Armstrong School of Environmental Research, Charles Darwin University, Darwin, Northern Territory, Australia Species with different regenerative responses to fire are T. bitextura, an obligate resprouter, Triodia sp., an obligate hypothesised to coexist by utilising the different temporal and seeder, and T. epactia, a facultative resprouter, had mean spatial niche opportunities created by the stochasticity of the Tmrca values of 65k, 40k and 111k generations, respectively. fire regime. This is strongly supported by observations of Usingamutationrateof3.2Â 10À5 andagenerationtimeof5 instability of species’ presence and abundance at the local years gave Tmrca values of 436k, 203k and 556 k years, scale while these are stable at the community scale. However, respectively. These results provide evidence for the coex- observations of species coexistence in fire-prone communities istence of these species to the same fire regime dating back to are limited to several decades only. To improve the robustness the late Pleistocene. It also demonstrates the long-term of this hypothesis, coalescent analysis, using chloroplast resilience of an obligate seeder, Triodia sp., in a frequently microsatellites, was undertaken on three sympatric species burnt environment at the community scale. of Triodia from different functional groups in the fire-prone Heredity (2011) 107, 558–564; doi:10.1038/hdy.2011.42; Kimberley region of Western Australia. The results inferred that published online 15 June 2011 Keywords: fire; coexistence; Pleistocene; obligate seeder; obligate resprouter; facultative resprouter Introduction 2002; Prior et al., 2007). However, the temporal and spatial scale and the reasons for which this occurs differ Plant functional groups are defined by a common set of across plant structural groups meaning there is no single physiological or phenological responses to environmen- fire frequency that favours all species in a community tal conditions or disturbances (Hooper and Vitousek, (Pausas and Lloret, 2007). Tree species that require 1997). Applicable over a range of scales, the concept decades to reach maturity will be far more vulnerable distinguishes annual from perennial, tree from herb or than grasses to subdecadal fire intervals (Genries et al., resprouter from obligate seeder, among many others. As 2009). The impact of the fire regime can therefore be such, using functional groups to classify plants provides species specific and variable across functional and a tractable means to study large-scale ecosystem pro- structural groups. However, coexistence of both groups cesses (Ustin and Gamon, 2010). Plant functional groups is widespread, with disturbance, particularly fire, defined by their regeneration strategies are hypothesised hypothesised to mediate fluctuations in dominance of to differ in their resilience (sensu Holling, 1973) to the particular groups over time (Chesson, 2000; Clarke and same fire regime. This is due to to differential allocation Dorji, 2008). of resources to vegetative or sexual reproduction, which The stable coexistence of species from different determines the probability of persisting through the fire functional groups is possible owing to the covariance return interval (Verdu, 2000). If the time taken to return between environmental and competitive responses to reproductive maturity is not achieved before the next among species, which is known as the storage effect fire event, populations will decline and suffer localised (Sears and Chesson, 2007). Empirical evidence for this extinctions (Bradstock et al., 1996; Russell-Smith et al., has been shown across a range of fire-prone habitats on 2002). Slow-growing obligate seeding species, those that different continents for periods of up to several decades rely entirely on seed germination after fire for regenera- (Williams et al., 2003; Andersen et al., 2005; Thuiller tion, are considered to be the most vulnerable to this et al., 2007). Thuiller et al. (2007) showed that although scenario (Hoffmann, 1998) and localised reductions and presence and abundance of species was highly unstable extinctions have been observed (Russell-Smith et al., at the local scale, it was stable at the meta-community scale. These results help resolve contradictions that arise in regard to the vulnerability of particular functional Correspondence: G Armstrong, Fitzroy Basin Association, PO Box 139, groups to fire, that is, obligate seeders vs obligate Rockhampton, Queensland, Australia. E-mail: [email protected] resprouter, depending on the spatial and temporal scale Received 15 January 2011; revised 30 March 2011; accepted 27 April of the observation. Given global changes in fire regimes 2011; published online 15 June 2011 across the world due to climate change and changes in Resilience of Triodia spp. to frequent fire G Armstrong 559 land-use practices (Beerling and Osborne 2006; Shlisky et al., 2007), the ability to generalise and therefore predict Figure 1 Representation of sequential sampling method. The black long-term responses of functional groups to the fire dots represent individual plants and leaf samples were collected regime is important for conservation-management prac- from those with white dots. The sequence is counted as the number tices. If the resilience of different functional groups in a of individuals between samples: 0,1,1,1,1,4,4 etc. See text for further community could be resolved over historical time details. periods, this would provide a much more robust analysis than studies spanning years or even decades. Coalescence (Kingman, 1982) provides a technique for (17132.3250S, 12619.4520E). T. epactia is a facultative such an analysis, enabling the demography of a species resprouter with strong regrowth after fire plus some to be inferred over times beyond that available from seed germination, T. bitextura is an obligate resprouter direct observation (see Kuhner, 2009 for a recent review). that has strong regrowth after fire, produces ramets and The ideal system to test the comparative historical has virtually no seed production, and Triodia sp. is an resilience between plants from different functional obligate seeder in which all adults die during fire with groups would be in a region with high fire frequency total regeneration from the seed bank (unpublished using plants in which reproduction is initiated by fire. data). Seeds are observed to be dispersed by both wind The tropical savannas of northern Australia provide and surface water during rain events in the wet season. such a model system, as there are many plant species Plants were sampled along a transect of exponentially that rely on fire for regeneration and the average increasing inter-plant distances in an attempt to capture fire return interval is 5 years in lower-rainfall areas, potentially autocorrelated samples for which the scale increasing to biannual at lower latitudes, which have was unknown. Plants were sampled, in the first half of greater rainfall and therefore greater fuel accumula- the transect, not by fixed distances, but by the number of tion (Felderhof and Gillieson, 2006). Taxa within Triodia individuals between those sampled, following the provide ideal model species because they are reliant sequence; 0, 1, 1, 1, 1, 4, 4, 4, 8, 8, 16, 16, with the on fire for reproduction (Burbidge, 1943; Noble, 1989; numbers being the number of plants between those Rice and Westoby, 1999) and encompass several func- sampled (Figure 1). This was done because plants grow tional groups, including obligate seeders (Casson and in a labyrinthine pattern with bare ground separating Fox, 1987), facultative resprouters and obligate resprouters individual ‘hummocks’ at varying distances (Figure 4). (Wells, 1999). As with other species of obligate seeders, This means any potential spatial autocorrelation would the resilience of obligate seeding Triodia spp. to short fire not be based on regular distances, but by the number of return intervals, as occurs in northern Australia, has been individuals that separate those that are sampled. questioned (Rice and Westoby, 1999). However, as with Sampling in the latter half of the transect used all other predictions regarding the resilience of parti- predetermined fixed distances at 50, 50, 100 and 100 m cular functional groups to particular fire regimes, the because many individuals are included at this scale. Total evidence is based on short-term observations. Here, I use distances of each transect were therefore slightly differ- coalescent analysis to determine the minimum time that ent, being 372 m for T. bitextura, 366 m for T. epactia and three Triodia species, each from a different functional 383 m for Triodia sp. group, have persisted in the landscape where fire has Leaf tissue samples, approximately 3 cm long, were been present for millennia. stored in Eppendorf tubes in a refrigerator until analysis, whereupon samples were ground in liquid nitrogen and total DNA extracted using DNneasy Plant Mini Kit Materials and methods (Qiagen, Valencia, CA, USA) following the manufac- turer’s protocol. Chloroplast microsatellites were chosen Site details and sampling to determine demographic histories as they are non- The study was carried out at Mornington Wildlife recombining, haploid and effectively