Fire-stimulated Flowering Research Articles

Masting, fire-stimulated flowering, and the evolutionary ecology of synchronized reproduction.

Synchronized episodic reproduction among long-lived plants shapes ecological interactions, ecosystem dynamics, and evolutionary processes worldwide. Two active scientific fields investigate the causes and consequences of such synchronized reproduction: the fields of masting and fire-stimulated flowering. While parallels between masting and fire-stimulated flowering have been previously noted, there has been little dialogue between these historically independent fields. We predict that the synthesis of these fields will facilitate new insight into the causes and consequences of synchronized reproduction. Here we briefly review parallels between masting and fire-stimulated flowering, using two case studies and a database of 1870 plant species to facilitate methodological, conceptual, geographical, taxonomic, and phylogenetic comparisons. We identify avenues for future research and describe three key opportunities associated with synthesis. First, the taxonomic and geographic complementarity of empirical studies from these historically independent fields highlights the potential to derive more general inferences about global patterns and consequences of synchronized reproduction in perennial plants. Second, masting's well developed conceptual framework for evaluating adaptive hypotheses can help guide empirical studies of fire-stimulated species and enable stronger inferences about the evolutionary ecology of fire-stimulated flowering. Third, experimental manipulation of reproductive variation in fire-stimulated species presents unique opportunities to empirically investigate foundational questions about ecological and evolutionary processes underlying synchronized reproduction. Synthesis of these fields and their complementary insights offers a unique opportunity to advance our understanding of the evolutionary ecology of synchronized reproduction in perennial plants.

Habitat fragmentation decouples fire-stimulated flowering from plant reproductive fitness

Many plant species in historically fire-dependent ecosystems exhibit fire-stimulated flowering. While greater reproductive effort after fire is expected to result in increased reproductive outcomes, seed production often depends on pollination, the spatial distribution of prospective mates, and the timing of their reproductive activity. Fire-stimulated flowering may thus have limited fitness benefits in small, isolated populations where mating opportunities are restricted and pollination rates are low. We conducted a 6-y study of 6,357 Echinacea angustifolia (Asteraceae) individuals across 35 remnant prairies in Minnesota (USA) to experimentally evaluate how fire effects on multiple components of reproduction vary with population size in a common species. Fire increased annual reproductive effort across populations, doubling the proportion of plants in flower and increasing the number of flower heads 65% per plant. In contrast, fire's influence on reproductive outcomes differed between large and small populations, reflecting the density-dependent effects of fire on spatiotemporal mating potential and pollination. In populations with fewer than 20 individuals, fire did not consistently increase pollination or annual seed production. Above this threshold, fire increased mating potential, leading to a 24% increase in seed set and a 71% increase in annual seed production. Our findings suggest that density-dependent effects of fire on pollination largely determine plant reproductive outcomes and could influence population dynamics across fire-dependent systems. Failure to account for the density-dependent effects of fire on seed production may lead us to overestimate the beneficial effects of fire on plant demography and the capacity of fire to maintain plant diversity, especially in fragmented habitats.

Quick qualitative and quantitative changes in reproductive efforts in an open cerrado community: An explorative study of fire-stimulated species

Cerrado is a tropical savanna hotspot that is impacted by frequent wildfires, but where many effects of fire still are poorly understood. This is especially true for the herbaceous strata at the community level, in which reproductive efforts are deeply affected by fire. The objectives of this study were the following: evaluate if fire qualitatively and/or quantitatively affects the production of sexual reproductive structures in an open cerrado community; describe fire-stimulated or fire-inhibited flowering and fruiting species; and evaluate the influence of water availability on flowering and fruiting. The number of species with flowers and fruits/m2 and the number of reproductive units/m2 were sampled in eight 20×20 m2 plots in Chapada Diamantina, Brazil. After the first sampling in the beginning of the rainy season (November 2009), the vegetation in four plots was burned and then the eight plots were resampled over five months. Indexes of fire-stimulated and fire-inhibited flowering and fruiting species were calculated. Non-metric multidimensional scaling and cross-correlation analyses were calculated and differences between the burnt and unburnt plots were compared with an analysis of variance. Sexual reproduction was deeply affected by fire, which changed the composition of reproducing species. Profuse reproduction of graminoids (Poaceae) and geophytic herbs classified as fire-stimulated flowering and/or fire-stimulated fruiting species concomitantly occurred with a high increase of water in the burnt soil compared to the unburnt soil in the first two months after the fires. The sexual reproduction of shrubby species was inhibited by fire. In an objective way, 21 species stimulated or inhibited by fire were recorded. Fire also changed the influence of rainfall on reproductive efforts. This study shows quick qualitative and quantitative effects of fire on open cerrado functioning and highlights the necessity of fire management for biodiversity conservation in savannas.

Fire as a novel technique to stimulate adventitious shoots in the laboratory

Fire-stimulated flowering and fire-stimulated resprouting are associated traits common in plants that evolved in fire-prone habitats, e.g., Vellozia pyrantha, an iconic plant that has economic potential and is endemic to a fully protected area. By combining a natural phenomenon that drives demography and in situ evolution, we tested if fire can be used as a novel technique for plant multiplication through vegetative bud activation in V. pyrantha. The basal parts of microplants cultivated for 60 days (5 to 6 cm tall) were exposed to a flame using a Bunsen burner for five periods controlled by a timer (2, 4, 6, 8, and 10 s) and compared to unburned plants (control). After 30 days, the number of new shoots was counted, and the length of the longest shoot produced per individual was measured. Adventitious shoot development started 7 days after the fire incidence. The number of shoots per individual and length of the longest shoot produced were significantly higher in the 6- to 10-s treatments. Fire was an efficient and cheap way to induce adventitious shoot formation. This new method could also be applied to other resprouter species from fire-prone environments in the world. By combining a natural phenomenon that drives evolution with the bud stimulus expected, we found fire as an efficient and cheap way to induce buds.

Evolutionary history of fire-stimulated resprouting, flowering, seed release and germination.

Fire has shaped the evolution of many plant traits in fire-prone environments: fire-resistant tissues with heat-insulated meristems, post-fire resprouting or fire-killed but regenerating from stored seeds, fire-stimulated flowering, release of on-plant-stored seeds, and germination of soil-stored seeds. Flowering, seed release and germination fit into three categories of response to intensifying fire: fire not required, weakly fire-adapted or strongly fire-adapted. Resprouting also has three categories but survival is always reduced by increasing fire intensity. We collated 286 records for 20 angiosperm and two gymnosperm families and 50 trait assignments to dated phylogenies. We placed these into three fire-adapted trait types: those associated with the origin of their clade and the onset of fire-proneness [primary diversification, contributing 20% of speciation events over the last 120millionyears (My)], those originating much later coincident with a change in the fire regime (secondary diversification, 30%), and those conserved in the daughter lineage as already adapted to the fire regime (stabilisation, 50%). All four fire-response types could be traced to >100My ago (Mya) with pyrogenic flowering slightly younger because of its dependence on resprouting. There was no evidence that resprouting was always an older trait than either seed storage or non-sprouting throughout this period, with either/both ancestral or derived in different clades and times. Fire-adapted traits evolved slowly in the Cretaceous, 120-65Mya, and rapidly but fitfully in the Cenozoic, 65-0Mya, peaking over the last 20My. The four trait-types climaxed at different times, with the peak in resprouter speciation over the last 5My attributable to fluctuating growing conditions and increasing savanna grasslands unsuitable for non-sprouters. All experienced a trough in the 40-30-Mya period following a reduction in world temperatures and oxygen levels and expected reduced fire activity. Thick bark and serotiny arose in the Mid-Cretaceous among extant Pinaceae. Heat-stimulated germination of hard seeds is ancestral in the 103-My-old Fabales. Smoke-(karrikin)-stimulated germination of non-hard seeds is even older, and includes the 101-My-old Restionaceae-Anarthriaceae. A smoke/karrikin response is detectable in some fire-free lineages that prove to have a fire-prone ancestry. Among clades that are predominantly fire-prone, absence of fire-related traits is the advanced condition, associated either with increased fire frequency (loss of serotiny and soil storage), or migration to fire-free habitats (loss of thick bark, pyrogenic flowering, serotiny or soil storage). Protea (Africa) and Hakea (Australia) illustrate the importance of stabilisation processes between resprouting/non-sprouting in accounting for speciation events over the last 20My and highlight the frequent interchange possible between these two traits. Apart from Pinus, most ancestral trait reconstruction relative to fire has been conducted on predominantly Southern Hemisphere clades and this needs to be redressed. Despite these limitations, it is clear that fire has had a profound effect on fire-related trait evolution worldwide, and set the platform for subsequent evolution of many non-fire-related traits. Genetics of the triggering mechanisms remain poorly understood, except the karrikin system for smoke-stimulated germination. We exhort biologists to include fire-proneness and fire-related traits in their thinking on possible factors controlling the evolution of plants.

Fire-Stimulated Flowering: A Review and Look to the Future

ABSTRACTThe literature on fire-stimulated flowering is reviewed in terms of post-fire flowering patterns, proximal ultimate factors that affect flowering of plants post-fire, as well as application of evolutionary theory and development of evolutionary models in relation to fire-stimulated flowering. Consideration is given to the concepts involved, available empirical information, and areas that warrant further research. Understanding the factors responsible for fire-stimulated flowering is limited. Studies suggest factors involved, but confounding of variables prevents their separation. Experiments evaluate different factors, but there have been few such studies and little consideration regarding soil attributes, synergistic effects of multiple factors, and large-scale factors such as herbivory, florivory, seed dispersal, and pollination. Understanding the adaptive nature, and hence evolution, of fire-stimulated flowering is poor. Prevalence of particular fire-related responses has been related to geographical and other patterns, with deduction of adaptive nature of plant responses to fire and factors driving evolution of these responses. However, confounding of factors hinders this approach and can lead to disagreement between researchers. A better approach would be to hypothesize that evolution has resulted in plant responses to fire that are Evolutionarily Stable Strategies and to develop consequent mathematical models for such evolution, leading to predictions and tests. However, this approach requires quantitative assessment of responses to fire-related factors and influences of such responses on plant fitness, and so far few such assessments exist. This poor state of knowledge regarding plants with fire-stimulated flowering means that we cannot easily replace or enhance fire for managing species with fire-stimulated flowering, as sometimes necessary, and it also restricts their commercial cultivation. Experimental evaluation of plant responses to fire and development of evolutionary models is required. Our knowledge of the factors that trigger post-fire flowering by re-sprouting plant species remains poor, and so we cannot incorporate relationships between them and plant fitness into mathematical models of plant evolution.

Homage to L. M. Coutinho: fire adaptations in cerrado plants

Professor Coutinho (1934–2016; Sao Paulo, Brazil) studied fire adaptations in Brazilian savannas during the 1970s, when very few researchers recognised fire as an evolutionary force. His main contributions were on fire-stimulated flowering, serotiny and nutrient cycling. However, he is little known, partly because he was not Anglo-Saxon but also because he was ahead of his time, when fire and evolution were still distant concepts.

Fire-Proneness as a Prerequisite for the Evolution of Fire-Adapted Traits.

Fire as a major evolutionary force has been disputed because it is considered to lack supporting evidence. If a trait has evolved in response to selection by fire then the environment of the plant must have been fire-prone before the appearance of that trait. Using outcomes of trait assignments applied to molecular phylogenies for fire-stimulated flowering, seed-release, and germination, in this Opinion article we show that fire-proneness precedes, or rarely coincides with, the evolution of these fire-adapted traits. In addition, fire remains central to understanding germination promoted by smoke among species occurring in non-fire-prone environments because of the historical association of their clade with fire. Fire-mimicking selection and associated exaptations have no place in understanding the evolution of fire-adapted traits because we find no support for any reversal in the fire-trait sequence through time.

A Cretaceous origin for fire adaptations in the Cape flora.

Fire has had a profound effect on the evolution of worldwide biotas. The Cape Floristic Region is one of the world’s most species-rich regions, yet it is highly prone to recurrent fires and fire-adapted species contribute strongly to the overall flora. It is hypothesized that the current fire regimes in the Cape could be as old as 6–8 million years (My), while indirect evidence indicates that the onset of fire could have reached 18 million years ago (Ma). Here, we trace the origin of fire-dependent traits in two monocot families that are significant elements in the fire-prone Cape flora. Our analysis shows that fire-stimulated flowering originated in the Cape Haemodoraceae 81 Ma, while fire-stimulated germination arose in the African Restionaceae at least 70 Ma, implying that wildfires have been a significant force in the evolution of the Cape flora at least 60 My earlier than previous estimates. Our results provide strong evidence for the presence of fire adaptations in the Cape from the Cretaceous, leading to the extraordinary persistence of a fire-adapted flora in this biodiversity hotspot, and giving support to the hypothesis that Cretaceous fire was a global phenomenon that shaped the evolution of terrestrial floras.

Reforestation or conservation? The attributes of old growth grasslands in South Africa.

Deforestation as a result of burning and land conversion in the tropics and subtropics has been widely studied and active restoration of forests has been widely promoted. Besides other benefits, reforestation can sequester carbon thereby reducing CO2 emissions to the atmosphere. However, before grasslands are targeted for 'reforestation', it is necessary to distinguish whether they are ancient natural grasslands or secondary vegetation colonizing deforested areas. Here we report the results of a study comparing primary grasslands in South Africa with 4-40 year old secondary grasslands recovering from afforestation with Pinus species. Primary grasslands had significantly higher plant species richness overall, especially of forb species. Ground cover of primary grasslands was more evenly distributed among species than secondary grasslands which tended to mono-dominance. Forbs with underground storage organs (USOs) were common in primary grasslands but conspicuously absent in the recovering systems. Comparison of secondary grasslands of different ages (up to 40 years) showed negligible recovery of the original species composition. Three key features distinguish old growth primary from secondary grasslands: total and forb species numbers, evenness of species contributions to cover and the presence of USOs. Old growth grasslands also differed in their fire response, showing significant post-burn resprouting and fire-stimulated flowering in contrast to secondary grasslands. Though similar contrasting attributes of ancient and secondary grasslands have been reported in South America, more studies are needed to explore their generality in other geographical regions.This article is part of the themed issue 'Tropical grassy biomes: linking ecology, human use and conservation'.

Fire-Related Traits in Mediterranean Basin Plants

Fire is a frequent and severe disturbance that affects plants on large scales, especially in Mediterranean-type ecosystems (MTE). Plants have evolved traits that confer resilience to fire and other disturbances, ensuring their persistence in fire-prone systems, but MTE floras differ in fire-related traits and their frequencies. Using available literature, we compare fire-related plant traits and syndromes of the flora of the Mediterranean Basin with those of other MTEs, discuss the differences and their possible causes, and point to knowledge gaps. Plants with lignotubers are relatively rare in the Mediterranean, as is serotiny. Many Mediterranean species have physically dormant seeds that are cued to germinate after fire by heat shock, while the effect of smoke on seed germination in the Mediterranean flora is less common than in other MTEs. The geophytes in the MB that flower massively afterfire flowering are opportunistic and not obligate fire-stimulated flowering species. Based on this literature surv...

Fire-stimulated flowering among resprouters and geophytes in Australia and South Africa

Data on 386 species with fire-stimulated flowering (fsf) in Australasia and South Africa/Madagascar were collated to show that they occur under a wide range of fire regimes, with 71% confined to the mediterranean-climate regions. About 40% only flower up to 2 years after fire (obligate), while the rest continue at a low rate until the next fire (facultative). Peak flowering occurs 5–18 months after fire in the mediterranean regions but at 1–7 months in savannas. Fsf is recorded in 34 families, headed by terrestrial orchids (45% of species), spread throughout the seed-plant phylogeny from cycads to daisies. Tuberous geophytes (essentially orchids) dominate (51%), but other resprouting growth forms include lignotuberous shrubs and forbs, rhizomatous and bunch grasses, leaf succulents, grasstrees, epicormic trees, and hemiparasites. Most have wind-dispersed diaspores (72%), store their diaspores in the soil (93%), and seeds that do not germinate until the next fire (72%). Fsf in association with resprouting takes advantage of optimal resources and minimal competition for growth and reproduction, conditions that favor wind dispersal and maximize the interval for seed accumulation before the next fire and build-up of fire-tolerant organs. Reduced herbivory has little role in accounting for its benefits. The proximal causes of fsf center around cueing factors (direct effects such as ethylene), resource factors (direct and indirect effects, e.g., extra nutrients), and predisposing factors (circumstantial effects, e.g., fire interval). The evolutionary history of fsf has been explored recently in orchids, proteas, blood roots, droseras, and mistletoes and shown to stretch back over a period of at least 50 million years, indicating that flowering in many groups has a long association with fire as an agent of natural selection.

Reduced flower visitation by nectar-feeding birds in response to fire in Cape fynbos vegetation, South Africa

Nectar-feeding birds are important pollinators in fire-prone regions of the world, but the impact of fires on these bird communities has seldom been studied. Nectar-feeding bird communities were censused during peak flowering, before and after fire in the Cape fynbos of South Africa. The abundance and species richness of nectar-feeding birds decreased at all sites. In a controlled experiment, two common bird-pollinated plants, which flower profusely after a fire, were presented in floral arrays in burnt and unburnt vegetation. Birds visited flowers only in the unburnt areas. The results are surprising given the large number of bird-pollinated plants that have fire-stimulated flowering.

A six-year study of fire-related flowering cues and coexistence of two perennial grasses in a wet longleaf pine (Pinus palustris) savanna

Integrating population and community ecology can improve our understanding of the impacts of natural disturbances. Fire-stimulated flowering occurs in many long-lived herbaceous species of fire-maintained grasslands and savannas. Coexistence of these long-lived species may be affected in part by interspecific differences in the effect of fire-stimulated flowering on resource conservation, clonal growth, and longevity. This study comprised two parts. The first part investigated the effectiveness of different fire-related cues on fire-stimulated flowering in two cooccurring dominant grass species in a wet longleaf pine (Pinus palustris) savanna in southeastern Mississippi, USA. The second part investigated the immediate effects of the most important of these cues (damage and removal of aboveground vegetation and surface litter in May) along with nutrient addition on several measures of fitness and abundance over 6 years. Despite being a very effective inductive cue, when repeated frequently over 6 years, clipping plus surface litter removal significantly reduced flowering in both species. This negative effect was reduced to some extent by nutrient addition in Muhlenbergia expansa (which exhibited higher reproductive investment following clipping and fire than did Ctenium aromaticum). Frequent clipping resulted in an increasing numerical advantage of C. aromaticum over M. expansa with time. There was evidence of a modest release of C. aromaticum from competition with M. expansa in response to annual clipping. Responses suggest that suppressing flowering until after fire reduces the cost of flowering and maintains shoot densities, at least in M. expansa. Differences in the responses of these two species to repeated clipping and nutrient addition suggest that, despite their both exhibiting fire-stimulated flowering, each species is favored by slightly different fire frequencies. Moderate variation in fire frequency could maintain their coexistence in the long term.

Convergent seed germination in South African fynbos and Californian chaparral

California chaparral and South African fynbos are fire-prone communities dominated by species exhibiting remarkable similarities in germination response. In both regions there are a substantial number of species with germination stimulated chemically by charred wood and smoke. This type of germination behaviour has arisen independently in distantly related families and is interpreted as convergent evolution. Heat-shock is also an important germination trigger that is widespread, although in both regions it is most common in the same families. Phylogeney may play an important role in the presence of this postfire germination cue in both regions, but a much more rigorous analysis is required to show that this trait represents a single unique event in each lineage. In both regions, germination response is not randomly distributed across growth forms and there are marked regional similiarities in the type of germination behaviour associated with certain growth forms. Geophytes largely lack refractory seeds, which require fire-type cues for germination, but the presence of fire-stimulated flowering of bulbs and corms may time recruitment to subsequent postfire years. Annuals that cue germination to postfire conditions are predominantly triggered by chemicals from smoke and/or charred wood.

The Relationship between Soil Fertility and Fire-Stimulated Floral Induction in Two Populations of Grass-Leaved Golden Aster, Pityopsis graminifolia

Classic life-history theories of reproductive strategies ignore the relationship between the cost of reproduction and reproductive plasticity. In this study, I examined the extent to which two populations of a perennial plant (Pityopsis graminifolia) differed in their floral induction responses to manipulation of fire, clipping, and fertilization regimes. I also measured site differences in soil concentrations of several mineral nutrients. The two populations differed dramatically in their observed patterns of reproduction ; the north Florida population substantially increased rates of bolting in response to fire, clipping and litter removal, and nutrient addition, whereas the central Florida population did not. Soils at the central Florida site contained over three times the concentration of phosphorus compared to soils at the north Florida site. Soil phosphorus levels were significantly (albeit slightly) increased by fire at the north Florida site but not at the central Florida site. Results of a field experiment using clonal transplants indicated that the population differences in reproductive sensitivity to fire-related environmental changes were associated with genetic differences. A May fire was more effective at stimulating floral induction in clonal fragments from the north Florida site than from the central Florida site. The results of this study were consistent with the prediction that selection pressure for fire-stimulated flowering is most intense in habitats in which flowering is highly resource (e.g., phosphorus) limited. I hypothesize that fire-stimulated flowering may be a means of reducing the direct resource costs of reproduction.