Direct and Indirect Effects of Salt Spray and Fire on Coastal Heathland Plant Physiology and Community Composition

RHODORA, Vol. 108, No. 933, pp. 32–42, 2006

DIRECT AND INDIRECT EFFECTS OF SALT SPRAY AND FIRE ON COASTAL HEATHLAND PLANT PHYSIOLOGY AND COMMUNITY COMPOSITION

1 2 MEGAN E. GRIFFITHS, ROBIN P. KEITH, AND COLIN M. ORIANS Department of Biology, Tufts University, Medford, MA 02155 1Current Address: Forest Biodiversity Research Unit, School of Biological and Conservation Sciences, University of KwaZulu-Natal, Private Bag X01, Scottsville 3209, South Africa e-mail: grifﬁ[email protected] 2Current Address: Department of Geography, University of Colorado, Boulder, CO 80309

ABSTRACT. Coastal sandplain heathlands are managed largely by prescribed burning. While it is known that salt spray is an important natural disturbance contributing to the maintenance of coastal heathlands, it is unclear whether fire in coastal areas intensifies the detrimental effects of salt spray on plants growing close to the ocean. We carried out a field experiment to test the interactive effects of fire and salt spray on Martha’s Vineyard, Massachusetts. Following a prescribed fire, one-meter-square plots were established in burned and unburned areas and randomly assigned a control or salt spray treatment. After ten weeks of spray treatments we found that burning stimulated new growth and salt spray consistently increased plant water stress, increased leaf necrosis, and inhibited shoot elongation. Burning did not increase the negative effects of salt spray in individual plants; salt spray and control treated plants growing in burned areas showed less water stress and leaf necrosis than those in unburned areas. This may be due to increased water availability in the burned area resulting from lower biomass and therefore lower competition for water and lower evapotranspiration rates. Burning reduced plant canopy height, decreased vascular plant species richness, and stimulated new growth in plants. Our results suggest that fire indirectly reduces the damaging effects of salt spray by increasing soil water availability and decreasing plant water stress.

Key Words: disturbance regime, physiological responses, prescribed burning, vascular plant community structure, water balance

A fundamental principle of modern ecology is that disturbance maintains the structural and species diversity of communities (Pickett and White 1986). Coastal sandplain heathlands in the northeastern United States are characterized by their dependence on salt spray, burning, grazing, mowing, and plowing to remain in an early successional state. Recent studies have demonstrated that heathland communities developed in response to intensive agricultural and forest clearance by European settlers (Foster et al. 2002; Foster and Motzkin 32 2006] Grifﬁths et al.—Salt Spray and Fire in Heathlands 33

2003; Motzkin et al. 2002). In the present day, however, these land use practices are infrequent and the lack of large-scale disturbance has al- lowed succession by native woody species such as Pinus rigida P. Mill. and Quercus ilicifolia Wangenh. to proceed in many formerly shrub- dominated heathlands (Dunwiddie 1989). Current management in coastal heathlands emphasizes the use of prescribed burning to maintain both the characteristic low stature and the composition of these vascular plant communities (Dunwiddie and Caljouw 1990). While fire has been the primary focus of restoration efforts in these heathlands, salt spray has also been shown to play a role in maintaining the low stature of plants and the distinctive plant community composition of heathlands that grow in close proximity to the ocean and receive naturally high levels of salt spray (Griffiths 2003). Research from heathlands in coastal regions of Tasmania suggests that fire might act synergistically with salt spray, resulting in high levels of damage to burned plant communities in areas with intense salt spray (Thomas and Kirkpatrick 1996). Synergistic fire and salt spray effects have also been conjectured for coastal sandplain heathlands in the United States (Dunwiddie et al. 1997). Such interactions could occur on a very short-term basis because heathland species show rapid resprouting in the growing season immediately following a burn. The new tissue is expected to be more susceptible to damage by salt spray because young leaves have less well-developed cuticles and are therefore more easily penetrated by salt spray (Franke 1967). Consequently, we hypothesized that recently burned plants would exhibit higher levels of necrotic damage and water stress in response to salt spray, as compared with plants that had not been burned. The combined effects of fire and salt spray are important to consider when creating fire management plans because salt spray damage to plants may be increased in recently burned sites. This damage could limit aboveground growth in heathlands and selectively inhibit salt-intolerant species, thereby changing the stature and composition in these communities. The purposes of this research were therefore to: (1) establish whether burning exacerbates the morphological and physiological effects of salt spray applied at natural levels, (2) determine the mechanism of the response of individual plants to burning and salt spray, and (3) ascertain if burning and salt spray effects are expressed in changes in heathland community structure and composition.

MATERIALS AND METHODS

Field measurements. The plant species composition of a stand before burning is a major determinant of the plant community response 34 Rhodora [Vol. 108 to fire (Hobbs and Gimingham 1987). For that reason we used a single site for experimental work to control for differences in pre-fire plant community composition. The combined effects of burning and salt spray on vascular heathland plants were investigated at King Point in Edgartown, Martha’s Vineyard, Massachusetts (418219200N, 708329300W), a conservation area managed by the Sheriff’s Meadow Foundation. The site is situated approximately 2 km from the ocean and there was no natural salt spray accumulation on plants in the study area during the experimental period (data not shown), allowing us to manipulate the amount of salt spray a plant received. King Point was used as sheep pasture in the late 19th century but both grazing and fire had not occurred in the area since 1950 (R. Johnson, Sheriff’s Meadow Foundation, pers. comm.). The Nature Conservancy’s Fire Management Program burned approximately 6 ha of heathland at King Point on 14 April, 2000. The fire was of moderate intensity and resulted in 75–95% top kill of shrubs (J. Carlson, The Nature Conservancy Fire Management Program, pers. comm.). We randomly placed 48 one-meter-square (1 m2) plots throughout the 6 ha burned area and an equivalently sized unburned area of King Point following the prescribed fire. The experiment was designed to have 12 plots each in four different treatments: unburned þ control spray (UC), unburned þ salt spray (US), burned þ control spray (BC), and burned þ salt spray (BS). Control plots were sprayed every second day with deionized water using a handheld plant mister to account for any physical effect the spraying had on plants. For the salt spray treatment, filtered seawater (31 ppt) was collected off the southern shore of Martha’s Vineyard, and applied every second day at a concentration of 8 mg NaCl/dm2, which is equivalent to the accumulation rate found on plants growing close to the ocean (Griffiths 2003). Spray treatments began 12 June, 2000 and lasted for 10 weeks. Within each plot, we tagged individuals of three perennial heathland plant species: Solidago rugosa P. Mill., Gaylussacia baccata (Wan- genh.) K. Koch, and Vaccinium angustifolium Aiton. Plants were standardized by height for each species. Prior to the treatment period, shoot height and number of leaves were measured for each focal plant used in the experiment. Shoot height and leaf number were sampled again following the spray treatment period so that shoot elongation and leaf production could be calculated. Additional morphological measurements included mean area of the first three fully expanded leaves and the total number of fruits produced by the entire plant for G. baccata and V. angustifolium. 2006] Griffiths et al.—Salt Spray and Fire in Heathlands 35

Two aspects of water status were tested at the end of the treatment period: predawn xylem pressure potential and leaf water content. Predawn xylem pressure potential of stems was measured in the ﬁeld at 04:00 using a pressure chamber (PMS Instrument Company, Corvalis, OR). Leaf water content was measured for the ﬁrst three fully expanded leaves at the top of each plant. Leaves were dried at approximately 608C for 48 h to determine dry mass. Leaf water content was calculated using the following equation:

leaf wet mass 2 leaf dry mass water content ¼ leaf dry mass

Leaf necrosis was assessed on the same leaves used for water content measurements. It was measured using a grid and expressed as a pro- portion of the total leaf area with necrotic damage. Leaf necrosis serves as an effective index for salt spray damage because it occurs directly as an accumulation of chloride ions to levels toxic for plants (Parsons and Gill 1968). The overall plant community stature for each 1 m2 plot was determined as a mean of 15 randomly placed canopy height measures that included any vascular plant species. Vascular plant community composition of each plot was also surveyed to determine plant species richness. These surveys included measurements for all species of grasses, forbs, climbers, shrubs, and trees.

Statistical analysis. Statistical analyses were carried out using general linear model procedures in SPSS 11.5.0 (SPSS, Chicago, IL). Preliminary analyses showed that the three focal species responded sig- niﬁcantly differently to burning and spray treatments (F14, 254 ¼ 24.35, p , 0.001) therefore each species was analyzed with a separate MANOVA to determine the effects of burning, salt spray, and the interaction between treatments. We interpreted overall effects based on Wilks’ k statistics but also considered the ANOVA results for each individual plant trait that was measured. Responses of plant community canopy height and vascular plant species richness to burning and spray treatments were investigated using two-way ANOVAs.

RESULTS

Individual plant responses. In all three plant species tested there were significant effects of burning and salt spray, and a significant 36 Rhodora [Vol. 108 interaction between the two factors was found in Gaylussacia baccata and Vaccinium angustifolium. For Solidago rugosa, there were significant morphological and physiological effects of burning (MANOVA; Wilks’ k ¼0.55; F6,39 ¼5.36, p , 0.001) and salt spray (MANOVA; Wilks’ k¼ 0.53; F6,39 ¼ 5.86, p , 0.001) but no interactive effects between burning and salt spray overall (MANOVA; Wilks’ k ¼ 0.80; F6,39 ¼ 1.67, p ¼ 0.153). However, there was one significant burning and salt spray interaction found when testing for between-subject effects on individual plant traits in the MANOVA: plants in burned plots exhibited higher levels of shoot elongation, but this growth was inhibited when the plants were subjected to salt spray (Table 1). In contrast, there was no effect of burning or salt spray on the number of leaves produced but new leaves in the burned treatments had larger areas than leaves produced on plants in the unburned treatments. There were no effects of burning and salt spray on the predawn xylem pressure potential of S. rugosa, nor were there effects on the leaf water content, indicating that water balance was not disrupted in this species. Despite this finding, we did observe significantly higher levels of necrosis on plants that had been treated with salt spray, which demonstrates that chloride toxicity did occur. For Gaylussacia baccata, we found significant morphological and physiological effects of burning (MANOVA; Wilks’ k ¼ 0.15; F7,38 ¼ 31.21, p , 0.001) and salt spray (MANOVA; Wilks’ k ¼ 0.59; F7,38 ¼ 3.80, p ¼ 0.003), and interactive effects between burning and salt spray (MANOVA; Wilks’ k ¼ 0.65; F7,38 ¼ 2.93, p ¼ 0.015). There was significantly enhanced shoot elongation in burned treatments, but no salt effects and no interactive effects between burning and salt (Table 1). There were also growth responses in terms of leaf production; more new leaves were produced in the burned treatments. Conversely, there was no fruit produced by plants in the burned treatments. Gaylussacia baccata plants had more negative predawn xylem pressure potential and higher leaf water content in plants subjected to salt spray, indicating a disruption in water balance. We also observed effects of burning, salt spray, and a burning 3 salt spray interaction on necrosis. Plants in the salt spray treatments had significantly more necrotic damage and the necrosis levels were higher for salt spray-treated plants in the unburned area. Vaccinium angustifolium also showed significant morphological and physiological responses to burning (MANOVA; Wilks’ k ¼ 0.24; F7,38 ¼ 17.33, p , 0.001), salt spray (MANOVA; Wilks’ k ¼ 0.45; F7,38 ¼ 6.71, p , 0.001), and a burning 3 salt spray interaction (MANOVA; Wilks’ k ¼ 0.61; F7,38 ¼ 3.45, p ¼ 0.006). Consistent with the other two species tested, we found significantly higher rates of shoot Table 1. Morphological and physiological responses of three focal heathland plant species to burning and salt spray treatments (mean 6 1 SD). XPP ¼ predawn xylem pressure potential, UC ¼ unburned þ control spray, US ¼ unburned þ salt spray, BC ¼ burned þ control spray, BS ¼ 2006] burned þ salt spray. The significance of the effects of burning (B), salt spray (S), and the interactive effects of burning and salt spray (B 3 S) are indicated as follows: NS ¼ not significant, * ¼ significant at p , 0.05, ** ¼ significant at p , 0.01, *** ¼ significant at p , 0.001. Hypothesis df ¼ 1 and error df ¼ 44 for all comparisons.

Treatment 37 Heathlands in Fire and Spray al.—Salt et Grifﬁths UC US BC BS BSB3 S Solidago rugosa Shoot elongation (cm) 14.2 6 11.9 17.7 6 12.4 36.3 6 12.2 25.5 6 10.3 *** NS * Leaf production (#) 21.1 6 15.5 21.8 6 14.1 26.8 6 6.9 22.8 6 7.9 NS NS NS Mean leaf area (cm2) 6.5 6 2.6 6.5 6 2.5 9.2 6 2.5 10.3 6 3.0 *** NS NS XPP (MPa) 0.5 6 0.2 0.7 6 0.4 0.6 6 0.1 0.7 6 0.2 NS NS NS Leaf water content (%) 1.6 6 0.1 1.7 6 0.2 1.7 6 0.4 1.7 6 0.2 NS NS NS Necrotic leaf area (cm2) 0.1 6 0.3 9.0 6 8.9 0.5 6 1.2 5.9 6 3.7 NS *** NS Gaylussacia baccata Shoot elongation (cm) 1.4 6 1.3 1.3 6 1.9 8.7 6 3.1 8.1 6 1.6 *** NS NS Leaf production (#) 1.9 6 2.8 2.3 6 3.8 12.7 6 3.8 13.2 6 3.0 *** NS NS Mean leaf area (cm2) 4.9 6 0.8 5.2 6 1.0 5.7 6 0.7 4.9 6 0.5 NS NS * Fruit production (#) 2.5 6 4.4 4.1 6 8.8 0.0 6 0.0 0.0 6 0.0 * NS NS XPP (MPa) 0.5 6 0.2 0.7 6 0.5 0.4 6 0.1 0.5 6 0.2 NS * NS Leaf water content (%) 1.1 6 0.1 1.3 6 0.1 1.1 6 0.1 1.2 6 0.2 NS ** NS Necrotic leaf area (cm2) 0.0 6 0.0 10.8 6 11.8 0.0 6 0.0 0.4 6 1.0 *** *** ** Vaccinium angustifolium Shoot elongation (cm) 1.4 6 1.3 1.3 6 1.9 8.7 6 3.1 8.1 6 1.6 *** NS NS Leaf production (#) 1.9 6 2.8 2.3 6 1.1 12.7 6 3.8 13.2 6 3.0 *** NS NS Mean leaf area (cm2) 4.9 6 0.8 5.2 6 1.0 5.7 6 0.7 4.9 6 0.5 *** NS NS Fruit production (#) 2.5 6 4.4 4.1 6 8.8 0.0 6 0.0 0.0 6 0.0 ** NS NS XPP (MPa) 0.5 6 0.2 0.7 6 0.5 0.4 6 0.1 0.5 6 0.2 NS * NS Leaf water content (%) 1.1 6 0.1 1.3 6 0.1 1.1 6 0.1 1.2 6 0.2 NS NS NS Necrotic leaf area (cm2) 0.0 6 0.0 10.8 6 11.8 0.0 6 0.0 0.4 6 1.0 ** *** ** 38 Rhodora [Vol. 108 elongation, more leaves produced, larger leaf areas, and no fruit production in the burned treatments (Table 1). Individuals of V. angustifolium exhibited lower predawn xylem pressure potential when treated with salt spray but no differences in leaf water content. There were also higher levels of necrosis with salt spray treatment and higher necrosis in the unburned treatments.

Vascular plant community responses. Burning had an overall positive effect on the change in plant community canopy height (ANOVA; F1,44 ¼ 43.66, p , 0.001) but there were no salt spray effects (ANOVA; F1,44 ¼ 0.92, p ¼ 0.343) and no interactive effects (ANOVA; F1,44 ¼ 0.07, p ¼ 0.788). There was signiﬁcantly more growth of vascular plants in burned treatments when compared with unburned controls (Figure 1A). There were effects of burning on vascular plant species richness (ANOVA; F1,44 ¼ 10.08, p ¼ 0.003) but no salt effects and no interactive effects. Plant species richness was lower in plots that had been burned, but the species richness of these plots increased over the treatment period (Figure 1B).

DISCUSSION

Burning and salt spray had significant effects on the morphology and physiology of heathland plants and on the structure of the vascular plant community. All of the focal plant species exhibited more shoot elongation in the burned treatments compared to the unburned treatments. Gaylussacia baccata and Vaccinium angustifolium also produced more leaves in response to burning, while Solidago rugosa and V. angustifolium produced leaves with larger areas. These results demonstrate that the focal heathland plant species respond to fire with rapid regrowth. Many studies have shown that heathland plant species resprout from underground structures following burning (Clarke et al. 2005; Valbuena and Trabaud 2001), and this is true for perennial plant species found in New England coastal heathlands. We also found that fruit production was entirely inhibited in recently burned G. baccata and V. angustifolium, suggesting that there is a trade-off between vegetative growth and reproduction and that these species allocate resources to growth rather than reproduction following a fire. Salt spray did not have any effects on growth in the three heathland plant species tested, which differs from findings in earlier field (Griffiths and Orians 2003a) and greenhouse (Griffiths and Orians 2003b) studies. The observed result is most likely a consequence of the relatively high 2006] Griffiths et al.—Salt Spray and Fire in Heathlands 39

Figure 1. Heathland plant community canopy height (A) and vascular plant species richness (B) in 1 m2 plots before (u) and after (n) ten weeks of control and salt spray treatments. UC ¼ unburned þ control spray, US ¼ unburned þ salt spray, BC ¼ burned þ control spray, BS ¼ burned þ salt spray. Bars represent mean 6 1 SD. 40 Rhodora [Vol. 108 rainfall that occurred during the growing season. Higher water availability overall would ameliorate the effects of salt spray on the plants (Griffiths and Orians 2003a). In this field study, the effects of salt spray were limited to changes in water balance and necrosis. Both Gaylussacia baccata and Vaccinium angustifolium exhibited more negative predawn xylem pressure potentials in plants subjected to salt spray and G. baccata had higher leaf water content, indicating a disruption in water balance and an osmoregulatory response of the plants to maintain water uptake. While the water balance of Solidago rugosa was not affected by salt spray, the species did have more necrosis in the salt spray treatment. Gaylussacia baccata and V. angustifolium plants in salt spray treatments also had significantly more necrotic damage, indicating that natural levels of salt spray have a toxic effect on all three heathland plant species. There were few interactions between burning and salt spray. The new growth observed in the three focal plant species was not inhibited by salt spray, with the exception of Solidago rugosa, which had marginally less growth in plants that were both burned and subjected to salt spray. Burning and salt spray interactions were found for Gaylussacia baccata and Vaccinium angustifolium; plants in the salt spray treatments had significantly more necrotic damage for salt spray-treated plants in the unburned area. Plants that have limited water availability are more likely to exhibit necrosis when exposed to salt spray (Griffiths and Orians 2003a). Since plants from both species were marginally more water stressed in the unburned salt spray treatment, this suggests that water was more limiting in the unburned area than in the burned area. We propose that this trend is related to a reduction in plant biomass in the burned area, which leads to lower competition for water among plants. Increased water availability in the burned areas may have further contributed to an amelioration of the negative effects of salt spray on the heathland species tested (Griffiths and Orians 2003a). Numerous studies in heathlands have demonstrated that burning controls woody vegetation and that it is important for biodiversity conservation (Bartolome et al. 2005; Russell-Smith et al. 2002; Tozer and Bradstock 2002; Watson and Wardell-Johnson 2004). We found that plant community canopy height was greatly reduced by burning but vascular plant species richness changed marginally. This suggests that the physical structure of the heathland community is more strongly affected by fire than is the species composition of the vascular plant community. It is well established that fire (Dunwiddie and Caljouw 1990; Dunwiddie et al. 1997) and salt spray (Griffiths and Orians 2004) 2006] Griffiths et al.—Salt Spray and Fire in Heathlands 41 independently contribute to the maintenance of coastal sandplain heathland plant communities in North America and we hypothesized that the two might interact on a physiological level, with consequences for the vascular plant community structure and composition. We found no evidence that burning intensifies the toxic effects of salt spray, however, and our results suggest that fire might actually minimize salt spray damage to vascular plants in the short term by altering water availability. This effect would disappear once the vegetation returned to its pre-burn condition. Previous research has demonstrated that natural salt spray affects vascular plant community stature and composition in heathlands along the coast (Griffiths and Orians 2003a). Based on the findings in this experiment, we conclude that the negative effects of salt spray will be lower in areas that are burned. At the same time, burning results in a lower stature in heathland plant communities and this might allow for salt spray to disperse further (Dunwiddie 1990; Griffiths 2003). As a result, it is important to consider both the salt spray conditions and the water availability of a particular site when planning prescribed burns in these habitats.

ACKNOWLEDGMENTS. The authors thank R. Johnson and the Sheriff’s Meadow Foundation for facilitating research at King Point. We also thank J. Carlson and The Nature Conservancy Fire Management Pro- gram for carrying out the controlled burn. The Islands Program of the Massachusetts Chapter of The Nature Conservancy provided housing during the ﬁeld season. This research was made possible through funding from the Biology Department at Tufts University, the Andrew W. Mellon Foundation, the Massachusetts Environmental Trust, and the Draupner Ring Foundation.

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