Andrew J. Denham

Projected soil temperature increase and seed dormancy response along an altitudinal gradient: implications for seed bank persistence under climate change

Background and aimsUnderstanding the mechanistic effects of climate change on species key life-history stages is essential for predicting ecological responses. In fire-prone regions, long-term seed banks allow post-fire recovery and persistence of plant populations. For physically dormant species, seed bank longevity depends on the maintenance of dormancy which is controlled primarily by temperature. Successful inter-fire recruitment is rare and dormancy loss between fires produces a net loss to the seed bank. We assessed whether temperature increases related to climate change can affect seed dormancy and, potentially, seed bank longevity.MethodsWe quantified the relationship between air temperatures and soil temperatures. Seeds of two shrub species, from four populations along an altitudinal gradient, were then exposed to a range of soil temperatures calculated to occur at the end of the 21st century, using projected mean and heat wave scenarios. Alterations to dormancy were assessed via germination.ResultsFor every 1°C increase in air temperature, associated soil temperature increased by 1.5°C. Mean temperature increase had no affect on seed dormancy. However, future heat wave conditions produced soil temperatures that significantly increased dormancy loss. This impact was greatest in seeds from cooler, high elevation populations.ConclusionsProjected heat wave events produce conditions that provide a mechanism for seed bank compromise. Dormancy-breaking temperatures for each population were positively related to parental environment temperatures, indicating local adaptation. Whilst heat from fire may govern post-fire recruitment response, we suggest that parental climate is the key selective force determining dormancy-breaking threshold temperatures, ensuring inter-fire seed bank persistence.

Temperature thresholds of physically dormant seeds and plant functional response to fire: variation among species and relative impact of climate change

Variation in dormancy thresholds among species is rarely studied but may provide a basis to better understand the mechanisms controlling population persistence. Incorporating dormancy-breaking temperature thresholds into existing trait frameworks could improve predictions regarding seed bank persistence, and subsequently species resilience in response to fire, climate change and anthropogenic management. A key ecological strategy for many species from fire-prone ecosystems is the possession of a long-lived seed bank, ensuring recovery after fire. Physical dormancy is dominant in these ecosystems and maintaining this dormancy is directly linked to seed bank persistence. We identified a suite of seed-related factors relevant to maintaining populations in fire-prone regions for 14 co-occurring physically dormant species. We measured variation in initial levels of dormancy and then applied experimental heating treatments, based on current seasonal temperatures and those occurring during fires, to seeds of all study species. Additionally, higher seasonal temperature treatments were applied to assess response of seeds to temperatures projected under future climate scenarios. Levels of germination response and mortality were determined to assess how tightly germination response was bound to either fire or seasonal cues. Six species were found to have dormancy cues bound to temperatures that only occur during fires (80°C and above) and were grouped as having obligate pyrogenic dormancy release. The remaining species, classified as having facultative pyrogenic dormancy, had lower temperature dormancy thresholds and committed at least 30% of seeds to germinate after summer-temperature treatments. Evidence from this study supports including dormancy-breaking temperature thresholds as an attribute for identifying functional types. High temperature thresholds for breaking dormancy, found in our obligate pyrogenic group, appear to be a fire-adapted trait, while we predict that species in the facultative group are most at risk to increased seed bank decay resulting from elevated soil temperatures under projected climate change.

Effects of soil temperature regimes after fire on seed dormancy and germination in six Australian Fabaceae species

In addition to direct fire cues such as heat, smoke and charred wood, the passage of fire leads indirectly to changes in environmental conditions which may be able to break physical dormancy in hard-coated seeds. After a fire, the open canopy and the burnt material lying on the surface alter the thermal properties of the soil, resulting in elevated soil temperatures for long periods of time. We simulated daily temperature regimes experienced at different depths of soil profile after a summer fire. Our aim was to determine whether these temperature regimes and the duration of exposure (5, 15 and 30 days) play an important role breaking physical seed dormancy in six legumes from south-eastern Australia. Our results showed that simulated temperature regimes break seed dormancy. This effect is specially pronounced at temperatures that are expected to occur near the soil surface (0–2 cm depth). The duration of exposure interacts with temperature to break dormancy, with the highest germination rates reached after the longest duration and highest temperatures. However, the germination response varied among species. Therefore, this indirect post-fire cue could play a role in the regeneration of plant communities, and could stimulate seedling emergence independent of direct fire cues as well as in interaction with direct cues.

Flowering, seed dispersal, seed predation and seedling recruitment in two pyrogenic flowering resprouters

A few resprouting plants in fire-prone environments have no local seed bank (soil or canopy) when a fire occurs. These species rely on post-fire flowering and the production of non-dormant seeds to exploit favourable post-fire establishment and growth conditions. For two such pyrogenic flowering species (Doryanthes excelsa Correa and Telopea speciosissima (Smith) R.Br.), we examined the timing of seed release, patterns of fruit production, seed dispersal, seed predation and seedling establishment following a fire in the Sydney region of south-eastern Australia. Both species took some 19 months after the fire to flower and the first seeds were released 2 years after the fire. D. excelsa flowered and fruited only once after the fire. For T. speciosissima, plants also flowered at least once more in the subsequent 5 years, but produced seed in only the first three post-fire flowering years. Fruit production differed between species, with fruiting individuals of D. excelsa producing fewer infructescences, similar numbers of follicles, but many more seeds per follicle than fruiting individuals of T. speciosissima. Ultimately, D. excelsa produced approximately six times as many seeds per m2 and four times as many seeds per adult in one flowering season than T. speciosissima did after four flowering (three successful fruiting) seasons. Seeds were passively dispersed from fruits borne 3–4 m (D. excelsa) or 1–2 m (T. speciosissima) above the ground. Most seeds were found within 5 m (D. excelsa) or 3 m (T. speciosissima) of parent plants. The primary seed shadow of both species was a poor predictor of the distribution of seedlings, with more seedlings occurring further from the adults than expected from the distribution of seeds. Seed loss to predators was high in both species in exclusion experiments where mammals had access to clumps of seeds (77–88%). It was variable and generally lower (8–65%) in experiments where seeds were not locally clumped. However, for T. speciosissima, at one site, some 65% of seeds were lost to mammals and invertebrates in these latter experiments. At this site, these losses appeared to influence subsequent recruitment levels, as very low seedling densities were observed. For both species, germination of seedlings first occurred some 2.5–3 years after the passage of the fire. The percentage of seeds produced to seedlings successfully established was low in D. excelsa (2–3%) and more variable across sites and years in T. speciosissima (0–18%). Resultant post-fire seedling densities of D. excelsa (two sites) and T. speciosissima at one site were similar, but they were much lower at the T. speciosissima site that had high levels of seed predation. Both D. excelsa and T. speciosissima are amongst the slowest woody resprouting species to recruit seedlings after fire in south-eastern Australia and lag years behind species with soil or canopy seed banks.

Dispersal and recruitment dynamics in the fleshy-fruited Persoonia lanceolata (Proteaceae)

Abstract Question: What is the role of dispersal, persistent soil seed banks and seedling recruitment in population persistence of fleshy-fruited obligate seeding plant species in fire-prone habitats? Location: Southeastern Australia. Methods: We used a long-term study of a shrubby, fleshy-fruited Persoonia species (Proteaceae) to examine (1) seed removal from beneath the canopy of adult plants; (2) seedling recruitment after fire; (3) the magnitude and location of the residual soil seed bank; and (4) the implications for fire management of obligate seeding species. We used demographic sampling techniques combined with Generalised Linear Modelling and regression to quantify population changes over time. Results: Most of the mature fruits (90%) on the ground below the canopy of plants were removed by Wallabia bicolor (Swamp wallaby) with 88% of seeds extracted from W. bicolor scats viable and dormant. Wallabies play an important role in moving seeds away from parent plants. Their role in occasional long distance dispersal events remains unknown. We detected almost no seed predation in situ under canopies (< 1%). Seedling recruitment was cued to fire, with post-fire seedling densities 6–7 times pre-fire adult densities. After fire, a residual soil seed bank was present, as many seeds (77–100%) remained dormant and viable at a soil depth where successful future seedling emergence is possible (0–5 cm). Seedling survival was high (> 80%) with most mortality within 2 years of emergence. Plant growth averaged 17 cm per year. The primary juvenile period of plants was 7–8 years, within the period of likely return fire intervals in the study area. We predicted that the study population increased some five-fold after the wildfire at the site. Conclusions: Residual soil seed banks are important, especially in species with long primary juvenile periods, to buffer the populations against the impact of a second fire occurring before the seed bank is replenished. Nomenclature: Harden, G.J. (1990–1992).

Characterizing the Litter in Postfire Environments: Implications for Seedling Recruitment

Litter accumulation after fire influences the magnitude of seed predation and seed germination. How litter accumulation and patchiness influence postfire seedling recruitment is poorly known. Species with persistent seed banks have seeds available for germination in the immediate postfire period. In contrast, plants with transient seed banks must flower after fire to place seeds in the postfire habitat. In southeastern Australian sclerophyll forests, most seedling recruitment occurs within 3 yr after fire. We found that less litter had accumulated in sites <6 mo postfire than in those 2–3 yr postfire. Seedlings of species with persistent seed banks therefore encounter postfire environments with large areas covered by little or no litter. Among these species there is great variation in seed mass, including some species with very light seeds. In contrast, the seed mass of transient seed bank species is less variable, with the lightest species more than 70 times heavier than the lightest persistent seed bank species. These seeds arrive 1–3 yr postfire and encounter habitats with more litter and fewer bare patches. This pattern suggests that litter accumulation after fire has influenced the evolution of seed mass either directly, by affecting germination and seedling survival, or indirectly, by affecting seed predators.

Predispersal seed predation in shrubs of Grevillea (Proteaceae) from south-eastern Australia

The agents responsible for predispersal seed losses and the magnitude of these losses in five shrubby Grevillea species from the Sydney region of south-eastern Australia were examined by scoring seed fates in ripe fruits. Predispersal seed predation was evident in all study species, with losses varying from 5 to 46%. Seed losses of from <1 to 27% were attributed to the weevils Cydmaea dorsalis (Coleoptera: Curculionidae) (occurring in all study species), and Cydmaeasp. (occurring in Grevillea buxifolia only), with greatest losses in the two largest-seeded species (G. buxifolia and the endangered G. caleyi). Seed losses to the wasp Eurytoma sp. (Hymenoptera: Eurytomidae) were also found in all species except G. buxifolia. In G. caleyi such losses were confined to only one of three sampled sites and one of two sampled years. Highest seed losses to Eurytoma sp. occurred in the threatened plant G. shiressii (46% of developing seeds). Levels of predispersal seed predation varied across different sampling years and species occupying the same site.

A technique to estimate the pre-fire depth of burial of Grevillea seeds by using seedlings after fire

In a glasshouse experiment, we used the shrub Grevillea speciosa to examine the reliability of estimating the depth of seed burial based on the distance from the soil surface to the junction of the swollen hypocotyl with the radicle. We then examined the applicability of the technique in the field by using post-fire seedling emergence. We found that the mean length of the swollen hypocotyl in seedlings was a good predictor of the depth of seed burial (R2 = 0.97). Most variation occurred for seeds buried near the surface at 2-cm depth, where the swollen hypocotyl overestimated the depth of seed burial by about 1 cm. There was a decline in the ability of seeds to successfully emerge from soil depths below 2 cm, with seedlings of G. speciosa able to emerge from soil depths up to 8 cm in the glasshouse. This corresponds with the estimated maximum emergence depth based on seed mass. In the field, seedlings were estimated to have emerged from depths of 1–7 cm after an intense wildfire. There was an approximately normal distribution of seedling emergence depths; however, the mode of this distribution varied among locations. The technique gave comparable results to a similar technique developed for Acacia spp., allowing consideration of a greater range of species and post-fire locations. Use of the technique has the potential to provide insights into the impacts of fires below ground, including the nature of post-fire germination, residual soil seed banks, the depth-related action of fire-induced germination cues and small-scale spatial variation.

Acacia shrubs respond positively to high severity wildfire: Implications for conservation and fuel hazard management

High severity wildfires pose threats to human assets, but are also perceived to impact vegetation communities because a small number of species may become dominant immediately after fire. However there are considerable gaps in our knowledge about species-specific responses of plants to different fire severities, and how this influences fuel hazard in the short and long-term. Here we conduct a floristic survey at sites before and two years after a wildfire of unprecedented size and severity in the Warrumbungle National Park (Australia) to explore relationships between post-fire growth of a fire responsive shrub genera (Acacia), total mid-story vegetation cover, fire severity and fuel hazard. We then survey 129 plots surrounding the park to assess relationships between mid-story vegetation cover and time-since-fire. Acacia species richness and cover were 2.3 and 4.3 times greater at plots after than before the fire. However the same common dominant species were present throughout the study. Mid-story vegetation cover was 1.5 times greater after than before the wildfire, and Acacia species contribution to mid-story cover increased from 10 to 40%. Acacia species richness was not affected by fire severity, however strong positive associations were observed between Acacia and total mid-story vegetation cover and severity. Our analysis of mid-story vegetation recovery showed that cover was similarly high between 2 and 30years post-fire, then decreased until 52years. Collectively, our results suggest that Acacia species are extremely resilient to high severity wildfire and drive short to mid-term increases in fuel hazard. Our results are discussed in relation to fire regime management from the twin perspectives of conserving biodiversity and mitigating human losses due to wildfire.

Microsatellite markers for vulnerable Australian aridzone Acacias

Several Australian arid zone Acacia species are under threat because of decades of fruiting and recruitment failure that may reflect the loss of genetic diversity within small and isolated populations. We developed primers for eight microsatellite loci for Acacia carneorum and Acacia loderi. We detected high levels of clonality in each of two stands of A. carneorum (1 and 2 genets). In contrast, one stand of A. loderi was wholly clonal (1 genet), while in a second there were 30 unique genotypes. These loci allow assessment of the genetic diversity and connectedness of populations, the relative contribution of asexual reproduction to genotypic diversity and population structure, and use of paternity analysis to identify sires of seed within populations known to have set seed in past decades. This type of information may provide a basis for a recovery plan based on ‘genetic rescue’.