CONFERENCE PROCEEDINGS Australian Bushfire Conference, Albury, July 1999

copyright 1999

Abstract

Introduction

In fire-prone habitats recruitment in plant species is frequently linked to the passage of a fire (Tyler 1995). This results from at least two main mechanisms. Firstly in species with soil seed banks, characteristics of fires break seed dormancy (e.g. heat, smoke, charred wood Keeley 1991; Brown 1993). Examples include many legumes, (Jeffery et al. 1988; Auld and O’Connell 1991) and non leguminous species (Brown 1993; Dixon et al. 1995). Secondly, in species with canopy seed banks, fires result in the mass opening of fruits and release of seeds (Lamont et al. 1991).

There are however, a number of species that have no available seed storage in either the soil or canopy at the time of the passage of a fire (Keith 1996). A few may rely on dispersal from unburnt areas, but most have mechanisms that allow established plants to generally survive fire (buried lignotubers, rhizomes or buds; protected apical meristems). For these species to take advantage of favourable conditions for seedling establishment and growth in the post-fire habitat (light, nutrients, space) they need to be capable of flowering soon after fire to release seeds. Alternatively, they would need to have mechanisms that allow significant recruitment independent of fire and few species show this trait (Keeley 1991). For species dependant upon post-fire flowering for recruitment, the timing and magnitude of this flowering will influence at what stage after fire seedling establishment is possible. The longer the interval between the passage of a fire and seedling recruitment, the more of the available resources are likely to have been captured by those species with soil or canopy seedbanks that can recruit in the immediate post-fire period.

In Australia, there is little known concerning the timing of seed release and subsequent seedling establishment for resprouting species that rely on post-fire flowering for recruitment (e.g. Angophora hispida, Auld 1986; Blandfordia nobilis, Johnson et al. 1994; Telopea speciosissima, Bradstock 1995), although all are thought to release seeds in a non dormant state and hence form transient soil seedbanks (sensu Parker and Kelly 1989). Similarly, there is only limited information on the seasonal patterns of post-fire flowering in these species. For some species there appears to usually be only one flowering/fruiting event after any fire (e.g. Angophora hispida, Auld 1986; Lomatia silaifolia, Denham and Whelan 1999). In this case, this one event represents the only opportunity to recruit between fires. For other species, flowering may extend over several years following a fire (Telopea speciosissima, Pyke 1983), although recruitment in these species has been little studied (Bradstock 1995).

In this study, we assessed the timing of seedling recruitment after fire in a range of functional plant groups from the available literature. This included both fire-sensitive and resprouting species with either canopy or soil seed banks and resprouting species reliant on post-fire flowering for seed production and subsequent seedling establishment. Then, using two species from the Sydney area of south-eastern Australia (Doryanthes excelsa and Telopea speciosissima) that rely on post-fire flowering for recruitment, we examined:

a) the timing of flowering and degree of seed production over 4 years after a large wildfire;

b) the impact of post-dispersal seed predation on seedling recruitment; and

c) the proportion of seeds released that successfully established as seedlings.

Methods

Study species

Doryanthes excelsa Correa (Gymea lily - Doryanthaceae) is a large perennial rosette plant with a bulbous rhizome and long broad linear leaves up to 3 m long. It is capable of asexual reproduction by division of the rhizome (Nash 1996). It grows in dry sclerophyll forests and woodlands on soils derived from sandstone containing some clay and is restricted the Sydney Basin with three outlying populations in northern New South Wales (Harden 1993). The species survives fire by having its apical buds protected in leaf bases (often underground). It flowers in a large red inflorescence held up to 5 m above the foliage of the plant.

Telopea speciosissima (Smith) R. Br. (Waratah - Proteaceae) is a tall shrub which is renowned for its striking blooms which appear emerging above resprouting vegetation in the post-fire environment. The species survives fire by dormant buds protected in an underground lignotuber (Bradstock 1995). Aerial stems are completely regrown after each fire.

Sites

Both T. speciosissima and D. excelsa co-occur in some areas. Two sample sites were chosen for each species within 10 km in Royal National Park to the south of Sydney. Site 1 contained both species and was a relatively rich shale ridge on Hawkesbury sandstone. It supported a forest of Eucalyptus sieberi with Corymbia gummifera, Banksia serrata, Xylomelum pyriforme and Ceratopetalum gummiferum. The understorey included Grevillea diffusa, Banksia spinulosa, Prostanthera sp., Isopogon anethifolius, Acacia myrtifolia, Lomandra spp., Dianella sp. Site 2 (D. excelsa only) had soils ranging from shallow skeletal to relatively deep alluvial. The vegetation was similarly variable, but mostly forest of Angophora costata, Banksia serrata, Ceratopetalum gummiferum, Eucalyptus piperita and Eucalyptus sieberi with an understorey including Boronia pinnata, Grevillea mucronulata, Acacia terminalis, Lomandra longifolia and Caustis flexuosa. Site 3 (T. speciosissima only) was an exposed hill of shallow sandstone derived soil. The trees are reduced in size compared to the former sites. Tree species include Corymbia gummifera, Eucalyptus obstans, E. sclerophylla and Banksia serrata. The understorey included Lambertia formosa, Lissanthe strigosa and a range of sedges.

All sites were burnt in January 1994. Prior to 1994 there was variation in fire history across sites. Site 1 (the eastern part only - sampled for D. excelsa) and Site 3 were burnt in 1988. Site 1 (western side, sampled for both study species) and Site 2 were burnt in the early 1980s (NPWS fire records; Keith pers comm.).

Timing of seed release

The 3 study sites and were monitored to observe the season of first flowering after the 1994 fire for both species. General observations were also made throughout Royal National Park to determine if the pattern of the study sites was representative of the study species response to fire in this area. The timing of fruit development and seed release were recorded for the first three flowering seasons after the 1994 fire.

Estimates of seed production

Six 30 by 30 m plots were established as follows: D. excelsa 2 plots at each of Sites 1 and 2; T. speciosissima one plot at each of Sites 1 and 3. For both study species, within each plot at each site, the numbers of infructescences and follicles on all plants was scored each year. To estimate of numbers of seeds per follicle, intact follicles were collected prior to dehiscence for each species from each site. For T. speciosissima, samples of 23 and 25 follicles were collected from Sites 1 and 3 respectively, and for D. excelsa, samples of 15 and 29 follicles were collected from Sites 1 and 2 respectively. The individuals used to estimate numbers of seeds per follicle were sampled from outside the plots to avoid impacts on seedling recruitment. A measure of seed density (seeds m^-2) per plot was derived from these data.

Seed Predation

In 1996, two trials were established at the time of seed release in the study species. Firstly, an exclusion experiment was used to investigate the degree of post-dispersal predation at each site. It was assumed that no secondary dispersal of seeds by invertebrates such as ants was likely since neither species have lipid bodies attached to their seeds. Pers. obs. supported this assumption. Two treatments were established:

a) cages (1 cm² mesh size) to exclude vertebrate predators while still allowing access to most small invertebrates. To prevent seeds from washing away in heavy rain, a PVC ring sawn from 10 cm pipe and approx. 1 cm thick was placed on the ground. This ring was inserted into the soil with only the top 0.5 cm above ground. Ten seeds were put inside the ring and a small cage, 5 cm tall was placed over the ring and fastened down with wire stakes.; and

b) uncaged, where only the PVC ring was used. This allowed access to invertebrates and mammals.

At each site, 10 blocks constituting a replicate of each treatment were used, the blocks haphazardly placed approximately 5 m apart. The number of seeds remaining in each dish was recorded every day for the first week, and approximately every second day for the following 10 weeks. Additionally, any information concerning the condition of seeds (such as whether chewed or germinated) or the presence of testa remains was recorded at each visit.

For both study species, a second trial was established to test the levels of predation on seeds which were placed singly at random locations throughout the plots at each study site, rather than clumped as above. Ten seeds were placed in randomly located positions according to a 30 by 30 m grid established at each site each week for 4 weeks. The seeds were marked by a steel stake 20 cm away and their fate followed for the next 10 weeks, with details recorded as above. These trials were established in two plots for D. excelsa at Site 1 and at one plot for Site 2 and both T. speciosissima sites.

Seedling establishment

Establishment of seedlings in each species was monitored during the winter and spring after the fruits opened. After the first flowering season after the 1994 fires, five randomly allocated 1 m by 30 m transects were searched for seedlings within the 30 by 30 m plot already established. This sampling was repeated in subsequent seasons when further flowering occurred.

Analysis

Seed production was compared: in D. excelsa across sites using a t-test with plots as replicates; in T. speciosissima across sites and years using a two factor ANOVA without replication (Zar 1996).

The proportion of seeds remaining in each of the 10 plots after 75 days in the exclusion experiment was compared using a two factor ANOVA (factors were treatment and site) for each species. An additional two factor ANOVA was used to compare species and caging treatment at Site 1, where both species were sampled. For the placement of single seeds trial, the proportion of seeds remaining in each weekly cohort of 10 seeds after 9 weeks was compared using a one factor ANOVA for each study species (plot as factor). Again, a comparison of the two study species was possible at Site 1 (one factor ANOVA).

For seedling establishment in D. excelsa, the number of seedlings per transect was compared across sites using a nested 2-Factor ANOVA with plots nested in sites. For T. speciosissima, seedling establishment was compared across sites and years using a 2-Factor ANOVA. Homogeneity of variances was tested using Cochran’s test. Where variances were significantly heterogeneous an arcsine transformation was applied to proportion data or a square root transformation was applied to count data. If variances were still heterogeneous the analysis was carried out on the raw data with a conservative approach to rejection of the null hypothesis.

Results

Timing of seed release

For both D. excelsa and T. speciosissima, the first flowering after the January 1994 fires occurred in the spring of 1995, some 19 months after the fire. Fruits matured in the following autumn with D. excelsa first releasing seeds in March 1996 and T. speciosissima in April 1996. Seeds were not released into the post-fire habitat until some 25-26 months post-fire. Seed fall was quite prolonged with some seeds still in fruits in June (both species). Telopea speciosissima individuals also flowered in the subsequent two years, with a similar timing of flowering and fruiting. Doryanthes excelsa did not flower in subsequent seasons.

Seed production

In the first post-fire flowering year for T. speciosissima the estimated density of seeds produced varied from 0.66 seeds m^-2 at Site 1 to 1.076 seeds m^-2 at Site 3 (Table 1). This density of seed production increased in the second fruiting year (1.11 .v. 1.64 seeds m^-2 at Sites 1 and 3, respectively), but declined dramatically in the third (0.2 .v. 0.2 seeds m^-2 at Sites 1 and 3, respectively). There was no significant difference between sites, but there were significantly fewer seeds produced in 1998 than in 1997. D. excelsa had a higher seed production than T. speciosissima in the one year it fruited (mean seed density of 11.4 ± 1.4 and 15.3 ± 5.0 seeds m^-2 at Site 1 and 2, respectively), with no significant difference between sites.

Seed Predation

In the exclusion experiment, predation on uncaged seeds was high, with over 70% of seeds taken after 60 days in both species (Fig. 1). In contrast, few seeds were removed from or eaten in the caged treatment. There was a significant treatment/site interaction for T. speciosissima (P = 0.027) resulting from higher seed losses from the caged treatment at Site 3 than Site 1. This suggests a greater impact of invertebrate predation at Site 3. For D. excelsa, no interaction or site effects were significant. Despite the presence of heterogeneous variances, we consider the treatment effect (P = 0.023) to be significant, given the robust nature of ANOVA and the large difference in means (Underwood 1981). Where both study species were compared at Site 1, there was only a significant treatment effect (P < 0.001) with the pattern for both species being similar, i.e. caging significantly reduced seed predation levels. Seed losses to predators was of two types, with consumption of whole seeds (occasionally all ten seeds in a replicate) suggesting mammalian predation, and partial seed damage suggesting losses to insects.

Fig. 1. Rates of seed predation in exclusion experiment: (a) Doryanthes excelsa and (b) Telopea speciosissima. Different symbols represent different sites, open symbols for caged treatment, filled for uncaged. Standard errors on day 75 (points juggled for clarity).

Losses to seed predation in the single seed trial were mostly not as great as in the uncaged treatment from the exclusion experiment where seeds were clumped in batches of 10. For D. excelsa, there was no significant site effect: the greatest losses were at Site 2 (mean of 18.1%), while at Site 1 mean losses per plot ranged from 7.5 to 17.5% (Fig 2). For T. speciosissima, there was a significantly (P = 0.037) greater loss of seeds from Site 3 (mean 72.5%) than from Site 1 (22.5%). At Site 1 there was no significant difference between the levels of predation between study species. A number of the seeds still present 9 weeks after placement had germinated.

Seedling establishment

The first seed germination event after the 1994 fire for both species was observed in June 1996, some 2.5 years after the fire. Seedlings were found at all sites. The number of seedlings m^-2 that established for D. excelsa varied from 0.28 ± 0.08 at Site 2 to 0.31 ± 0.15 at Site 1 (Table 1). There was no significant difference between sites or plots. The number of seedlings m^-2 for T. speciosissima ranged from 0 at Site 3 in 1998 to 0.147 ± 0.07 at Site 1 in 1997 (Table 1). There was a significant site effect, with more seedlings recruited at Site 1 than at Site 3 (P = 0.003).

The percentage of the seeds released that established as seedlings varied between species, sites and years (Table 1). For D. excelsa, both sites had only low establishment percentages (2-3%), as did Site 3 for T. speciosissima in all years (0-1.9%). In contrast, at Site 1, there was a higher percentage of seedling establishment, a pattern consistent across three fruiting years (12-18%, Table 1). At both study sites the percentage of seedlings establishing declined from the first post-fire fruiting year (1996) to the 3rd (1998). This decline may be partly due to variation in seed production, which showed a pattern of highest in the second year and lowest in the third year.

Fig. 2. Rates of predation of single seeds: (a) Doryanthes excelsa and (b) Telopea speciosissima. Different lines represent different plots. Standard errors based on week 9.

Note: Doryanthes excelsa only produced seeds in one year (1996).

Discussion

Both D. excelsa and T. speciosissima took some 18 months to flower after the January 1994 fire. For D. excelsa, this represented the only post-fire flowering event, a pattern similar to several other local taxa (Auld 1986, Denham and Whelan 1999), whilst in T. speciosissima, there was annual flowering for at least three years after the fire. In T. speciosissima, there was a trend for the highest seed production in the first two post-fire fruiting seasons followed by a marked decline in the third. Both species took some 2.5 years after the fire to establish seedlings (Fig. 3). Other species cohabiting with D. excelsa and T. speciosissima will establish seedling much quicker, including those with a soil seedbank (most establishment in first 6 months, Fig. 3) a canopy seedbank (most release seed in the first 6 months, Lamont et al. 1991, and establish in the first year) or even other species that rely on post-fire flowering for seedling establishment (species such as Xanthorrhoea spp. and Lomatia silaifolia appear to be 1-1.5 years quicker than D. excelsa and T. speciosissima, Denham and Whelan 1999, Keith pers comm.). Consequently, when seedlings of D. excelsa and T. speciosissima are trying to establish, much of the space, light and nutrients made available by the fire may have been captured by other species (both resprouting plants and seedlings). This will be particularly the case for seedlings from the second and third fruit crops post-fire in T. speciosissima. Seedlings of both D. excelsa and T. speciosissima will need to be able to persist in a highly competitive environment. The success of these species may be due to their large seed size that ensures the seedlings have good seed reserves when establishing.

The exclosure experiment revealed that seed losses to mammals and invertebrates occur in the field, as has been found for other large seeded species in similar habitats (i.e. Grevillea species, Auld and Denham 1999). Losses were high for clumped seeds, but generally lower for seeds placed singly, implying that local seed density may affect the ability of seed predators to find and subsequently eat seeds. However, at Site 3 for T. speciosissima, losses were high in both trials and seed predators are likely to be having an impact on the magnitude of seedling recruitment in this species. This is reflected in significantly lower seedling densities at this site even though seed production was not significantly different between sites. Seedling recruitment was observed at all sites, but only a small proportion of the seedbank established as new recruits, with Site 1 for T. speciosissima having the highest recruitment levels. The highest levels of seedling recruitment observed here are comparable for some estimates from local species with canopy seedbanks (Banksia serrata (6-12%), Isopogon anemonifolius (6-18%) Bradstock 1990; and from previous work on T. speciosissima (7-9%) Bradstock 1995), while levels for D. excelsa and T. speciosissima (Site 3) are lower. Variation in recruitment levels across the three sampled fruiting seasons in T. speciosissima may be explained by variation in seed predation, environmental conditions for establishment or a decline in available safe sites by the third season. While D. excelsa produced an order of magnitude more seed in 1996 than T. speciosissima, a lower establishment success meant that resultant seedling densities were only slightly higher.

Fig. 3. Comparison of timing of post-fire seedling establishment in different functional groups. Obligate pyrogenic flowerers: Doryanthes excelsa, Telopea speciosissima (this study); obligate seeders with a soil seedbank:  Grevillea spp.,  Acacia suaveolens (Auld and Tozer 1995);  Persoonia lanceolata (unpubl. data).

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