Experimental seed sowing reveals seedling recruitment vulnerability to unseasonal fire.

Unseasonal fire occurrence is increasing globally, driven by climate change and other human activity. Changed timing of fire can inhibit postfire seedling recruitment through interactions with plant phenology (the timing of key processes, e.g., flower initiation, seed production, dispersal, germination), and therefore threaten the persistence of many plant species. Although empirical evidence from winter-rainfall ecosystems shows that optimal seedling recruitment is expected following summer and autumn (dry season) fires, we sought experimental evidence isolating the mechanisms of poor recruitment following unseasonal (wet season) fire. We implemented a seed-sowing experiment using nine species native to fire-prone, Mediterranean-climate woodlands in southwestern Australia to emulate the timing of postfire recruitment and test key mechanisms of fire seasonality effects. For seeds sown during months when fire is unseasonal (i.e., August-September: end of the wet winter season), seedling recruitment was reduced by up to 99% relative to seeds sown during seasonal fire months (i.e., May-June: end of the dry summer season) because of varying seed persistence, seedling emergence, and seedling survival. We found that up to 70 times more seedlings emerged when seeds were sown during seasonal fire months compared to when seeds were sown during unseasonal fire months. The few seedlings that emerged from unseasonal sowings all died with the onset of the dry season. Of the seeds that failed to germinate from unseasonal sowings, only 2% survived exposure on the soil surface over the ensuing hot and dry summer. Our experimental results demonstrate the potential for unseasonal fire to inhibit seedling recruitment via impacts on pregermination seed persistence and seedling establishment. As ongoing climate change lengthens fire seasons (i.e., unseasonal wildfires become more common) and managed fires are implemented further outside historically typical fire seasons, postfire seedling recruitment may become more vulnerable to failure, causing shifts in plant community composition towards those with fewer species solely dependent on seeds for regeneration.

A research agenda for seed-trait functional ecology.

Trait-based approaches have improved our understanding of plant evolution, community assembly and ecosystem functioning. A major challenge for the upcoming decades is to understand the functions and evolution of early life-history traits, across levels of organization and ecological strategies. Although a variety of seed traits are critical for dispersal, persistence, germination timing and seedling establishment, only seed mass has been considered systematically. Here we suggest broadening the range of morphological, physiological and biochemical seed traits to add new understanding on plant niches, population dynamics and community assembly. The diversity of seed traits and functions provides an important challenge that will require international collaboration in three areas of research. First, we present a conceptual framework for a seed ecological spectrum that builds upon current understanding of plant niches. We then lay the foundation for a seed-trait functional network, the establishment of which will underpin and facilitate trait-based inferences. Finally, we anticipate novel insights and challenges associated with incorporating diverse seed traits into predictive evolutionary ecology, community ecology and applied ecology. If the community invests in standardized seed-trait collection and the implementation of rigorous databases, major strides can be made at this exciting frontier of functional ecology.

Spatio-temporal water dynamics in mature Banksia menziesii trees during drought.

Southwest Australian Banksia woodlands are highly diverse plant communities that are threatened by drought- or temperature-induced mortality due to the region's changing climate. We examined water relations in dominant Banksia menziesii R. Br. trees using magnetic leaf patch clamp pressure (ZIM-) probes that allow continuous, real-time monitoring of leaf water status. Multiple ZIM-probes across the crown were complemented by traditional ecophysiological measurements. During summer, early stomatal downregulation of transpiration prevented midday balancing pressures from exceeding 2.5 MPa. Diurnal patterns of ZIM-probe and pressure chamber readings agreed reasonably well, however, ZIM-probes recorded short-term dynamics, which are impossible to capture using a pressure chamber. Simultaneous recordings of three ZIM-probes evenly spaced along leaf laminas revealed intrafoliar turgor gradients, which, however, did not develop in a strictly basi- or acropetal fashion and varied with cardinal direction. Drought stress manifested as increasing daily signal amplitude (low leaf water status) and occasionally as rising baseline at night (delayed rehydration). These symptoms occurred more often locally than across the entire crown. Microclimate effects on leaf water status were strongest in crown regions experiencing peak morning radiation (East and North). Extreme spring temperatures preceded the sudden death of B. menziesii trees, suggesting a temperature- or humidity-related tipping point causing rapid hydraulic failure as evidenced by collapsing ZIM-probe readings from an affected tree. In a warmer and drier future, increased frequency of B. menziesii mortality will result in significantly altered community structure and ecosystem function.

Environmental Factors Driving Seed Hydration Status of Soil Seed Banks and the Implications for Post-fire Recruitment.

Changes in fire regimes due to climate change and fire management practices are affecting the timing, length, and distribution of vegetation fires throughout the year. Plant species responses and tolerances to fire differ from season to season and are influenced by species-specific phenological processes. The ability of seeds to tolerate extreme temperatures associated with fire is one of these processes, with survival linked to seed moisture content at the time of exposure. As fire is more often occurring outside historic dry fire seasons, the probability of fire occurring when seeds are hydrated may also be increasing. In this study, we set out to understand the seasonal dynamics of seed hydration for seeds of Banksia woodland species, and how certain seed traits interact with environmental conditions to influence survival of high temperatures associated with fire. We measured the moisture content of seeds buried to 2 cm in the soil seed bank for four common native species and one invasive species on a weekly basis throughout 2017, along with soil moisture content and environmental correlates. We determined water sorption isotherms at 20°C for seeds of each species and used these functions to model weekly variation in seed water activity and predict when seeds are most sensitive to soil heating. Using Generalised additive models (GAMs), we were able to describe approximately 67% of the weekly variance in seed water activity and explored differences in seed hydration dynamics between species. Seed water activity was sufficiently high (i.e., ≥ 0.85 a w) so as to have created an increased risk of mortality if a fire had occurred during an almost continuous period between May and November in the study period (i.e., 2017). There were brief windows when seeds may have been in a dry state during early winter and late spring, and also when they may have been in a wet state during summer and late autumn. These data, and the associated analyses, provide an opportunity to develop approaches to minimize seed mortality during fire and maximize the seed bank response.

High-resolution distribution modeling of a threatened short-range endemic plant informed by edaphic factors.

Short-range endemic plants often have edaphic specializations that, with their restricted distributions, expose them to increased risk of anthropogenic extinction.Here, we present a modeling approach to understand habitat suitability for Ricinocarpos brevis R.J.F.Hend. & Mollemans (Euphorbiaceae), a threatened shrub confined to three isolated populations in the semi-arid south-west of Western Australia. The model is a maximum entropy species distribution projection constructed on the basis of physical soil characteristics and geomorphology data at approximately 25 m2 (1 arc-second) resolution.The model predicts the species to occur on shallow, low bulk density soils that are located high in the landscape. The model shows high affinity (72.1% average likelihood of occurrence) for the known populations of R. brevis, as well as identifying likely locations that are not currently known to support the species. There was a strong relationship between the likelihood of R. brevis occurrence and soil moisture content that the model estimated at a depth of 20 cm.We advocate that our approach should be standardized using publicly available data to generate testable hypotheses for the distribution and conservation management of short-range endemic plant species for all of continental Australia.

Ants cannot account for interpopulation dispersal of the arillate pea Daviesia triflora.

Estimating distances and rates of seed dispersal, especially long-distance dispersal (LDD), is critical for understanding the dynamics of patchily distributed populations and species' range shifts in response to environmental change. Daviesia triflora (Papilionaceae) is an ant-dispersed shrub. The ant Rhytidoponera violacea was recorded dispersing its seeds to a maximum distance of 4.7 m, and in more intensive trials seeds of a related species from the study area, to a maximum of 8.1 m. Microsatellite DNA markers and population assignment tests identified interpopulation immigrants among 764 plants on 23 adjacent dunes bearing D. triflora, and 13 interpopulation seed dispersal (LDD) events (1.7%) were inferred. The distance between source and sink populations ranged from 410 m to 2350 m (mean 1260 m). These distances exceed ant dispersal distances by two to three orders of magnitude but are comparable with previous measurements of LDD for two co-occurring wing-seeded (wind-dispersed) species from the same system. The observed distances of seed dispersal in this arillate species demonstrate the significance of nonstandard dispersal mechanisms in LDD and the independence of these from primary dispersal syndromes. The likely role of emus in dispersal of the many 'ant-dispersed' species in Australia is discussed.

Protecting Offspring Against Fire: Lessons From Banksia Seed Pods.

Wildfires are a natural component in many terrestrial ecosystems and often play a crucial role in maintaining biodiversity, particularly in the fire-prone regions of Australia. A prime example of plants that are able to persist in these regions is the genus Banksia. Most Banksia species that occur in fire-prone regions produce woody seed pods (follicles), which open during or soon after fire to release seeds into the post-fire environment. For population persistence, many Banksia species depend on recruitment from these canopy-stored seeds. Therefore, it is critical that their seeds are protected from heat and rapid oxidation during fire. Here, we show how different species of Banksia protect their seeds inside follicles while simultaneously opening up when experiencing fire. The ability of the follicles to protect seeds from heat is demonstrated by intense 180 s experimental burns, in which the maximum temperatures near the seeds ranged from ∼75°C for B. serrata to ∼90°C for B. prionotes and ∼95°C for B. candolleana, contrasting with the mean surface temperature of ∼450°C. Many seeds of native Australian plants, including those of Banksia, are able to survive these temperatures. Structural analysis of individual follicles from these three Banksia species demonstrates that all of them rely on a multicomponent system, consisting of two valves, a porous separator and a thin layer of air surrounding the seeds. The particular geometric arrangement of these components determines the rate of heat transfer more than the tissue properties alone, revealing that a strong embedment into the central rachis can compensate for thin follicle valves. Furthermore, we highlight the role of the separator as an important thermal insulator. Our study suggests that the genus Banksia employs a variety of combinations in terms of follicle size, valve thickness, composition and geometric arrangement to effectively protect canopy-stored seeds during fire.

Mechanisms of Fire Seasonality Effects on Plant Populations.

Altered fire regimes resulting from climate change and human activity threaten many terrestrial ecosystems. However, we lack a holistic and detailed understanding of the effects of altering one key fire regime component - season of fire. Altered fire seasonality can strongly affect post-fire recovery of plant populations through interactions with plant phenology. We identify seven key mechanisms of fire seasonality effects under a conceptual demographic framework and review evidence for these. We reveal negative impacts of altered fire seasonality and identify research gaps for mechanisms and climate types for future analyses of fire seasonality effects within the identified demographic framework. This framework and these mechanisms can inform critical decisions for conservation, land management, and fire management policy development globally.

Temperature-induced self-sealing capability of Banksia follicles.

Many plants in fire-prone regions retain their seeds in woody fruits in the plant canopy until the passage of a fire causes the fruit to open and release the seeds. To enable this function, suitable tissues are required that effectively store and protect seeds until they are released. Here, we show that three different species of the Australian genus Banksia incorporate waxes at the interface of the two valves of the follicle enclosing the seeds, which melt between 45°C and 55°C. Since the melting temperature of the waxes is lower than the opening temperatures of the follicles in all investigated species (B. candolleana, B. serrata, B. attenuata), we propose that melting of these waxes allows the sealing of micro-fissures at the interface of the two valves while they are still closed. Such a self-sealing mechanism likely contributes to the structural integrity of the seed pods, and benefits seed viability and persistence during storage on the plants. Furthermore, we show in a simplified, bioinspired model system that temperature treatments seal artificially applied surface cuts and restore the barrier properties.

Climate-Dependent Heat-Triggered Opening Mechanism of Banksia Seed Pods.

Heat-triggered fruit opening and delayed release of mature seeds are widespread among plants in fire-prone ecosystems. Here, the material characteristics of the seed-containing follicles of Banksia attenuata (Proteaceae), which open in response to heat frequently caused by fire, are investigated. Material analysis reveals that long-term dimensional stability and opening temperatures of follicles collected across an environmental gradient increase as habitats become drier, hotter, and more fire prone. A gradual increase in the biaxial curvature of the hygroscopic valves provides the follicles in the driest region with the highest flexural rigidity. The irreversible deformation of the valves for opening is enabled via a temperature-dependent reduction of the elastic modulus of the innermost tissue layer, which then allows releasing the stresses previously generated by shrinkage of the fiber bundles in the adjacent layer during follicle drying. These findings illustrate the level of sophistication by which this species optimizes its fruit opening mechanism over a large distribution range with varying environmental conditions, and may not only have great relevance for developing biomimetic actuators, but also for elucidating the species' capacity to cope with climatic changes.

Subcontinental heat wave triggers terrestrial and marine, multi-taxa responses.

Heat waves have profoundly impacted biota globally over the past decade, especially where their ecological impacts are rapid, diverse, and broad-scale. Although usually considered in isolation for either terrestrial or marine ecosystems, heat waves can straddle ecosystems of both types at subcontinental scales, potentially impacting larger areas and taxonomic breadth than previously envisioned. Using climatic and multi-species demographic data collected in Western Australia, we show that a massive heat wave event straddling terrestrial and maritime ecosystems triggered abrupt, synchronous, and multi-trophic ecological disruptions, including mortality, demographic shifts and altered species distributions. Tree die-off and coral bleaching occurred concurrently in response to the heat wave, and were accompanied by terrestrial plant mortality, seagrass and kelp loss, population crash of an endangered terrestrial bird species, plummeting breeding success in marine penguins, and outbreaks of terrestrial wood-boring insects. These multiple taxa and trophic-level impacts spanned >300,000 km2-comparable to the size of California-encompassing one terrestrial Global Biodiversity Hotspot and two marine World Heritage Areas. The subcontinental multi-taxa context documented here reveals that terrestrial and marine biotic responses to heat waves do not occur in isolation, implying that the extent of ecological vulnerability to projected increases in heat waves is underestimated.

Late Quaternary climate change and spatial genetic structure in the shrub Banksia hookeriana.

Spatial genetic variation within species is influenced by both contemporary and historical factors. We attempted to assess the impact of increased aridity and lower temperatures associated with the last glacial maximum on possible refugia and the structuring of genetic variation in Banksia hookeriana, a shrub species restricted to deep sands on the Eneabba sandplain and adjacent Gingin Scarp/Dandaragan Plateau, centred 300 km north of Perth, Western Australia. We used optically stimulated luminescence (OSL) dating to estimate the last time these sands were mobile, as well as amplified fragment length polymorphisms (AFLP) to infer spatial patterns and the phylogeographical history of genetic variation among 15 populations of B. hookeriana. While genetic variation at the species level was high, with 96.6% of 238 AFLP markers polymorphic, average within population gene diversity was low (H(pop) = 0.16). Of the total genetic variation, an analysis of molecular variance (amova) partitioned 70% within populations, 24% among populations within substrate and 6% between substrates. There was an isolation-by-distance effect among populations within the same substrate, but not across substrates, and ordination highlighted genetic differentiation between the sandplain and scarp/plateau populations. A neighbour-joining tree identified the sandplain populations as a distinct clade, with the exception of the most northern sandplain population, which clustered with two northern and eastern plateau populations. The most southern plateau populations formed a clade sister to the sandplain clade. OSL dating of sand at six extant populations suggested that dunes were last mobile 15,000-35,000 years ago, with no clear difference in the ages of sandplain and plateau dunes. These data are consistent with a historical scenario of (re)colonization from isolated refugia of smaller populations either within the patchily vegetated sandplain and/or refugia at the northern, eastern and southern sandplain/scarp margins following postglacial climate amelioration and dune stabilization. Historic interpretations were confounded by the possible effects of long-distance dispersal, natural selection by substrate, and weak and/or ancient introgression with the sister species, Banksia prionotes.

Long-distance seed dispersal in a metapopulation of Banksia hookeriana inferred from a population allocation analysis of amplified fragment length polymorphism data.

There is currently a poor understanding of the nature and extent of long-distance seed dispersal, largely due to the inherent difficulty of detection. New statistical approaches and molecular markers offer the potential to accurately address this issue. A log-likelihood population allocation test (AFLPOP) was applied to a plant metapopulation to characterize interpopulation seed dispersal. Banksia hookeriana is a fire-killed shrub, restricted to sandy dune crests in fire-prone shrublands of the Eneabba sandplain, southwest Australia. Population genetic variation was assessed for 221 individuals sampled from 21 adjacent dune-crest populations of B. hookeriana using amplified fragment length polymorphism. Genetic diversity was high, with 175 of 183 (96%) amplified fragment length polymorphism markers polymorphic. Of the total genetic diversity, 8% was partitioned among populations by amova and FST. There was no relationship between genetic diversity within populations and population demographic parameters such as population size and sample size. A population allocation test on these data unambiguously assigned 177 of 221 (80.1%) individuals to a single population. Of these, 171 (77.4% of total) were assigned to the population from which they were sampled and 6 (2.7% of total) were assigned to a known population other than the one from which they were sampled. A further 9 (4.1% of total) were assigned to outside the sampled metapopulation area, and 35 individuals (15.8%) could not be assigned unambiguously to any particular population. These results suggest that both the extent [15 of 221 (6.8%) individuals originating from a population other than the one in which they occur] and distance (1.6 to > 2.5 km), of seed dispersal between dune-crest populations is greater than expected from previous studies. The extent of long-distance interpopulation seed dispersal observed provides a basis for explaining the survival of populations of the fire-killed B. hookeriana in a landscape experiencing frequent fire, where local extinctions and recolonizations may be a regular occurrence.