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Australian Journal of Botany, 2012, 60, 347–357 http://dx.doi.org/10.1071/BT11271

Burning creates contrasting demographic patterns in Polygala lewtonii (Polygalaceae): a cradle-to-grave analysis of multiple cohorts in a perennial herb Carl W. Weekley A,B and Eric S. Menges A A

Archbold Biological Station, 123 Main Drive, Venus, FL 33960, USA. Corresponding author. Email: [email protected]

B

Abstract. Fire drives the population dynamics of many plants. By following successive cohorts of Polygala lewtonii Small (Polygalaceae), a short-lived herb endemic to fire-maintained Florida sandhills, in both burned and unburned microsites, we investigated how fire affected vital rates throughout cohort lifetimes. We followed cohorts from before to 6 years after a prescribed fire in 220 25-cm-radius quadrats, recording survival and seedling recruitment quarterly, and growth and fecundity annually. Fire effects were most pronounced in the first 2 post-burn quarterly censuses, when cohorts in burned (v. unburned) quadrats had seven-fold higher seedling recruitment, significantly higher seedling survival, and a 16.7% gain (v. 1.2% loss) in quadrat occupancy. Plants in burned (v. unburned) quadrats also flowered earlier, were more likely to survive to reproduce and had longer lifespans. The negative effects of density on survival were relaxed in burned quadrats for the first 2 censuses. Burning creates contrasting demographic trajectories for burned v. unburned cohorts. In burned microsites, higher seedling recruitment and survival, earlier flowering and longer lifespans combine to produce a greater contribution to the seedbank and, thus, to population viability. The present study documents the pyro-demographic mechanisms linking the life history of a perennial herb with a frequent fire regime. Received 26 October 2011, accepted 11 April 2012, published online 25 June 2012

Introduction Plant species inhabiting pyrogenic communities typically display life-history traits that benefit from the natural fire regimes of the communities they occupy (Noble and Slatyer 1980; Christensen 1985; Whelan 1995; Bond and van Wilgen 1996; Menges 2007). Post-fire recovery strategies differ among fire-responsive species, but most resprout, recruit from persistent seedbanks, or both (Keeley and Zedler 1978; Abrahamson 1984a; Menges and Kohfeldt 1995). In addition, fire may increase seedling recruitment (Keeley 1987, 1992; Brewer and Platt 1994a), survival (Carrington 1999; Quintana-Ascencio and Menges 2000) and growth (Brewer and Platt 1994b; Anderson and Menges 1997). Fire may also stimulate flowering and seed production (Hartnett and Richardson 1989; Kirkman et al. 1998; McConnell and Menges 2002) and increase clonal spread (Hartnett 1987; Brewer and Platt 1994b; Menges and Root 2004). Because vital rates may increase under an appropriate fire regime, fire may promote population persistence in these fire-responsive species (Silva et al. 1991; Menges et al. 2006). At the community level, fire may increase herb abundances relative to woody species (Quintana-Ascencio et al. 2003; Weekley and Menges 2003; Menges and Quintana-Ascencio 2004), maintain the graminoid cover required to carry frequent low-intensity fires (Vila-Cabrera et al. 2008; Beckage et al. 2009), and affect the balance between resprouting plants and obligate seeders (Bradstock 1990). Journal compilation CSIRO 2012

However, the direct positive effects of fire for a species may be counterbalanced by indirect negative effects. For example, stimulation of seed germination or resprouting by co-occurring species may increase inter-specific competition for resources. Moreover, high post-burn seedling densities of a species may result in intra-specific competition through density-dependent negative effects on vital rates (Wellington and Noble 1985). The life-history strategies of fire-responsive species have been particularly well studied in chaparral (Keeley and Zedler 1978; Keeley 1991) and other Mediterranean shrublands (Purdie 1977; Whelan and Main 1979; Whelan 1985; Keeley 1986; Bell et al.1993; Pausas 1999; Keith 2002), Florida scrub (Whelan 1985; Menges et al. 2006) and the longleaf pine/wiregrass (Pinus palustris Mill./Aristida stricta Michx.) sandhill ecosystems of the US south-eastern coastal plain (Abrahamson 1984b; Platt et al. 1988; Kirkman et al. 1998; Hiers et al. 2000; Knight and Holt 2005). As most of these studies make clear, life-history strategies differ among species, life forms and functional groups, and are mediated by microhabitat, season of burn and variation in weather patterns. Many studies have included comparisons of vital rates of plant populations subjected to various burning treatments (Glitzenstein et al. 1995; Quintana-Ascencio et al. 2003; Villalobos et al. 2007) and population viability models of www.publish.csiro.au/journals/ajb

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pyrogenic species have often incorporated fire metrics such as time-since-fire and fire frequency (Hoffmann 1999; Kaye et al. 2001; Menges and Quintana-Ascencio 2004). Fewer studies have considered post-fire cohorts. Studies of post-fire cohorts have generally focussed for a short time on burned plants only. For example, Zammit and Zedler (1992) followed even-aged cohorts of Ceonothus greggii A.Gray for 5 years in chaparral stands of various post-burn ages (6–82 years) and Hansen et al. (1992) studied an obligate seeder (Gompholobium marginatum R.Br.) for 6 years. Post-fire cohort studies of pine seedlings (Daskalakou and Thanos 2004) and obligately seeding shrubs (Quintana et al. 2004) focussed on variation in recruitment and survival over time. These studies are useful in providing information such as the minimum age of reproduction and fecundity schedules as a function of postfire age, information potentially useful to fire management (Bradstock et al. 1996). However, none of these studies includes an analysis of density-dependence effects on vital rates. Our study is unique in that we combined frequent sampling of successive cohorts of a perennial plant in paired burned and unburned microsites, from seedling recruitment to plant death. A cohort study, particularly when it encompasses the life history of the cohort from recruitment to death, provides a cogent demonstration of the effects of fire. For example, we avoid attributing temporal or site effects to fire, which is a risk in chronosequence studies. Instead, we directly compare burned and unburned cohorts over the same time period and at the same site, making our inferences of burn effects on demography more conclusive. In addition, we investigated the impact of density-dependent mortality in burned and unburned microsites. The 186-km-long Lake Wales Ridge of south-central peninsular Florida, USA (Weekley et al. 2008), encompasses both Florida scrub and longleaf pine/wiregrass sandhills. Several previous studies have investigated the fire ecology of Lake Wales Ridge scrub and sandhill species (Abrahamson 1984b; Hartnett 1987; Hartnett and Richardson 1989; McConnell and Menges 2002; Satterthwaite et al. 2002; Reinhart and Menges 2004). Decades of fire suppression in these pyrogenic plant communities may have resulted in reduction or loss of plant populations (Satterthwaite et al. 2002; Menges and QuintanaAscencio 2004). Fire suppression may have had particularly dire consequences for Lake Wales Ridge sandhills, which historically experienced fire at 2–8-year intervals. In the absence of fire, hardwood cover increases and herb abundances decrease (Myers 1985; Menges et al. 1993). Our study organism, Polygala lewtonii, is a short-lived (2–10 years) perennial herb occurring in fire-maintained ecosystems in central Florida. Although Lindon and Menges (2008) investigated the effects of smoke on seed germination, there has been no previous study of the demography or fire responses of P. lewtonii. Our objectives were (1) to confirm that P. lewtonii is an obligate seeder by documenting the post-fire fate of preburn individuals, (2) to compare post-fire seedling recruitment in burned and unburned microsites, (3) to compare the vital rates (survival, growth and fecundity) of the resulting seedling cohorts and (4) to evaluate the effects of density on survival of plants in burned and unburned quadrats.

C. W. Weekley and E. S. Menges

Materials and methods Study species P. lewtonii, a state- (Coile and Garland 2003) and federally listed (USFWS 1999) endangered herb, is narrowly endemic to the Lake Wales Ridge and the nearby Mount Dora Ridge in central peninsular Florida. It is known exclusively from longleaf pine/ wiregrass (Aristida stricta Michx. var. beyrichiana (Trin. & Rupt.) D.B.Ward) sandhills and from oak/hickory (Quercus myrtifolia Willd./Carya floridana Sarg.) scrub (Menges 1999). P. lewtonii plants are usually killed by fire and seedlings recruit post-fire from a soil seedbank (B. Pace-Aldana, pers. comm.; C. W. Weekley, unpubl. data). Plants are generally found in open sandy microsites, but can persist in areas with litter, terrestrial lichens and/or shade (C. W. Weekley, unpubl. data). Plants produce multiple stems up to 20 cm in height from a well defined root crown. Populations recruit year round, but most recruitment is associated with periods of high rainfall and cooler temperatures (i.e. El Niño winters). High mortality, particularly of newly recruited seedlings, often occurs during spring droughts (April–May). Thus, populations often show dramatic fluctuations in size annually. P. lewtonii possesses an amphicarpic breeding system characterised by the presence of aboveground chasmogamous flowers and both above- and belowground cleistogamous flowers (James 1957; Weekley and Brothers 2006). Sexual maturation usually takes at least 1 year and chasmogamous flowering generally precedes cleistogamous flowering (C. W. Weekley, unpubl. data). Not all mature plants produce cleistogamous flowers and most cleistogamy occurs in larger and older adults. The fruit is a dehiscent two-seeded capsule (James 1957). Seeds bear fleshy elaiosome-like appendages (Zomlefer 1989) that attract ants (C. W. Weekley, unpubl. data). In a laboratory experiment, Lindon and Menges (2008) showed that short-term exposure to smoke promoted ex situ germination in P. lewtonii, but this result was not supported by a field experiment (C. W. Weekley, unpubl. data). A separate field experiment demonstrated that buried seeds may retain viability for at least 2 years (C. W. Weekley and E. S. Menges, unpubl. data), indicating that P. lewtonii is capable of accumulating a persistent (sensuThompson and Grime 1979) soil seedbank. The sudden appearance of large cohorts of seedling recruits suggests that the persistent seedbanks of P. lewtonii are ecologically relevant. Study site We conducted the present study on the Carter Creek tract of the Lake Wales Ridge National Wildlife Refuge near Sebring, Florida, USA (27290 N, 81260 W). Carter Creek comprises 254 ha of xeric uplands, mesic flatwoods, seasonal wetlands and bayhead swamp. About one-third of the site is longleaf pine/wiregrass sandhill. The Carter Creek sandhill is characterised by an open canopy of longleaf pines, a discontinuous subcanopy of oaks (Quercus geminata Small, Q. laevis Walter) and scrub hickory (Carya floridana), a shrub layer of oaks (Q. geminata, Q. laevis, Q. chapmanii Sarg, Q. myrtifolia) and palmettos (Sabal etonii Swingle ex Nash, Seronoa repens (W. Bartram) Small), and a ground layer with wiregrass, other graminoids and forbs. Most of the ~80 ha of

Post-fire cohort dynamics of a rare herb

sandhill on site had not burned for several decades before acquisition by the US Fish and Wildlife Service in 1998. In 2001, we initiated an experimental sandhill-restoration project by dividing a 40-ha section of sandhill into12 treatment blocks (Menges et al. 2008). USFWS fire managers applied prescribed fire to 8 of the treatment blocks on 16 August 2001 and left 4 others unburned as controls. Within this larger experiment, we studied the responses of P. lewtonii in treatment blocks where it occurred in reasonable sample sizes. Experimental design In April 2001, we established 220 25-cm-radius circular quadrats in 3 treatment blocks slated for burning, and in 3 control blocks, including areas supporting multiple patches of P. lewtonii. Because both natural and prescribed fires are often patchy, we set up almost twice as many quadrats in the burn blocks (142) as in the control blocks (78). Quadrats were paired such that 1 quadrat in each pair was occupied by P. lewtonii plants and 1 had no P. lewtonii plants (unoccupied). We included both occupied and unoccupied quadrats to track changes in microsite occupancy and to document colonisation of new microsites. Paired quadrats were within 2 m of one another and were physiographically similar (e.g. similar litter cover and shade). Within each occupied quadrat, we recorded polar coordinates (compass direction and distance from the centre of the quadrat) for each plant. We also recorded the height and maximum crown diameter of each plant, the total number of stems and the number of chasmogamous flowering stems. Preburn plots included 260 P. lewtonii plants; 79 plants were in the 39 occupied control quadrats and 181 plants in the 71 occupied burn treatment quadrats. Preburn plants in the control v. burn treatment blocks did not differ in height (t = 0.985, d.f. = 258, P = 0.326) or maximum crown diameter (t = 0.704, d.f. = 258, P = 0.482). Within 2 weeks following the August 2001 prescribed burn, we revisited all quadrats to record their post-burn status (unburned or burned). Within the burn-treatment blocks, 87 of 142 quadrats (61.3%) remained unburned, resulting in 165 unburned quadrats (including 78 in the control blocks) and 55 burned quadrats. Because post-burn censuses revealed no significant differences in seedling recruitment between control and unburned quadrats, in subsequent analyses we treated them as a single unburned treatment. In the first post-burn census (December 2001), we marked all P. lewtonii plants present with colour- and suit-coded plastic toothpicks. Thereafter, quadrats were censused quarterly for survival and recruitment. We also collected data on growth and fecundity (as measured by the number of chasmogamous flowering stems) in annual censuses conducted each March during peak chasmogamous flowering. The periodic samples allowed us to track how vital rates changed over time. We assigned all new seedlings encountered in each census to successive cohorts (e.g. seedlings recruiting in the quarter ending in March 2002 were labelled as the ‘March 2002 cohort’). Between December 2001 and September 2007, we recorded 24 post-burn cohorts, 1 for each quarterly census. As post-fire densities decreased, plants were marked with numbered vinyl flags on 15-inch wire stakes.


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Statistical analysis For comparison of post-burn survival of preburn plants in unburned and burned quadrats, we used Chi-square tests. We used life tables and the Wilcoxon (Gehan) statistic to compare medians of survival curves of seedling recruits in unburned and burned quadrats in the first 2 post-burn cohorts. To compare seedling recruitment in unburned and burned quardrats in the 24 postburn censuses, we used Chi-square tests with a Bonferroni adjusted a of 0.002 (0.05/24 tests). We calculated the annual relative growth rate (RGR) in height for the first 3 post-burn years, using the formula (ln(htt2) – ln(htt1))/(t2–t1), where ln is the natural log of plant height at Years 1 and 2. We used a similar formula to calculate RGR between Years 2 and 3. To compare RGR and frequency of flowering plants in unburned v. burned quadrats, we used Student’s t-tests and Chi-square tests, respectively. Because density and survival data were non-normal and resistant to transformation, we used the non-parametric Mann–Whitney U test to compare plant densities in burned and unburned quadrats, scatter plots to show the relationship between density and survival, and Spearman’s rank correlations to evaluate the effect of density on plant survival. All analyses were performed in SPSS v. 11.5 (SPSS 2002). Results Post-burn survival of preburn plants Post-burn survival was significantly higher for plants in unburned than in burned quadrats (64.9 v. 24.0%; c2 = 35.782, d.f. = 1, P < 0.001). The 18 survivors in the burned quadrats represented unburned or lightly scorched plants rather than post-burn resprouts. Mortality in both treatments included plants that died of non-treatment causes over the 8 months between the preburn and the first post-burn censuses. Post-burn seedling recruitment in occupied and unoccupied quadrats In the first 2 post-burn censuses, proportional seedling recruitment (number of seedlings/number of preburn plants) differed significantly between the burned and unburned quadrats due to recruitment into both previously occupied and previously unoccupied quadrats (Fig. 1). In the December 2001 census, proportional seedling recruitment was 8 times greater in burned than in unburned quadrats (881.3% v. 110.4%; c2 = 199.978, d.f. = 1, P < 0.001). In the March 2002 census, burned quadrats out-recruited unburned quadrats 3.7–1 (184.0% v. 49.2%; c2 = 48.880, d.f. = 1, P < 0.001). Over the 2 censuses, burned quadrats had proportional recruitment of 1065.3% v.159.5% for unburned quadrats. For these 2 cohorts, between 75.8% and 79.0% of seedlings recruited into burned quadrats with no surviving reproductive adults, indicating that most recruitment was from the preburn seedbank rather than from newly produced seeds. In each of the next 10 quarterly censuses (June 2002– September 2004), the combined proportional seedling recruitment in unburned and burned quadrats never exceeded 14% (and never exceeded 18% in either treatment). Nonetheless, over the 6 years encompassed by this study, burned quadrats out-recruited unburned quadrats four-fold (1632.0% v. 406.0% increase, based on number of plants present preburn).

350


Burned quads

Dec. 01 cohort Mar. 02 cohort

Unburned quads

55 quads with 75 preburn plants


Table 1. Summary of seedling recruitment of Polygala lewtonii in burned and unburned quadrats in Carter Creek sandhill for 24 postburn quarterly cohorts Shown are the census date, cohort number, number of new seedlings in quadrats unburned or burned in the August 2001 prescribed fire, and total number of seedlings observed. Within each census containing a minimum of 35 total seedlings, quadrats marked with an asterisk had significantly more new seedlings than quadrats in the contrasting treatment (P 0.001 for all comparisons) Census

Post-burn cohort

165 quads with 185 preburn plants

0

100 200 300 400 500 600 700 800 900 1000 1100 1200

Recruitment (%) Fig. 1. Post-burn seedling recruitment of Polygala lewtonii in burned and unburned quadrats in Carter Creek sandhill, following the August 2001 prescribed burn, as recorded in the first 2 post-burn quarterly censuses (December 2001 and March 2002).

Higher levels of seedling recruitment in 5 of the last 12 quarterly censuses (Table 1; December 2004–September 2007) may have primarily reflected seed production by postburn plants. Therefore, for these censuses, we also calculated alternative recruitment percentages based on the number of live plants within each quadrat, rather than on the number of preburn individuals. By this criterion, burned quadrats significantly outpaced unburned quadrats in 3 of the 5 censuses in which the total number of seedlings was >35 (for each of these 3 censuses c2 11.7, d.f. = 1, P 0.001; Table 1). Post-burn changes in quadrat occupancy Burned quadrats experienced a net increase in the number of occupied quadrats, whereas unburned quadrats experienced a net loss. In the first 2 post-burn cohorts, recruitment into unoccupied burned quadrats was 24.0% (6 of 25 quadrats) v. 8.2% (7 of 85 quadrats) for unburned quadrats (Fig. 2a). The difference was marginally significant with the correction for low expected frequencies in 1 cell of the 2 2 contingency table (c2 = 4.607, d.f. = 1, P = 0.032; Fisher’s exact test = 0.07). There was a 16.7% net gain in quadrat occupancy (the proportion of quadrats with P. lewtonii individuals) for burned quadrats v. a 1.2% net loss in quadrat occupancy for unburned quadrats (Fig. 2b). Altogether, in the first 2 post-burn censuses, 79 seedlings recruited into the 6 previously unoccupied burned quadrats (median = 6.5, range 3–47) v. 31 into 7 previously unoccupied unburned quadrats (median = 4, range 2–9). Vital rates of post-burn recruits (survival, growth and fecundity) Survival of post-burn recruits was significantly greater in burned than in unburned quadrats for the first 2 post-burn cohorts (Fig. 3). For the December 2001 cohort, median survival time was 3.3 times greater in burned quadrats than in unburned quadrats (25.5 v. 7.8 months; Wilcoxon (Gehan) statistic = 103.641, d.f. = 1, P < 0.001). For the March 2002 cohort, median survival time was 4.0 times greater in burned

Dec. 2001 Mar. 2002 June 2002 Sep. 2002 Dec. 2002 Mar. 2003 June 2003 Sep. 2003 Dec. 2003 Mar. 2004 June 2004 Sep. 2004 Dec. 2004 Mar. 2005 June 2005 Sep. 2005 Dec. 2005 Mar. 2006 June 2006 Sep. 2006 Dec. 2006 Mar. 2007 June 2007 Sep. 2007

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 Total

Number of new seedlings Unburned Burned Total quadrats quadrats 204 91 0 4 5 18 9 0 2 24 0 20 59 196* 22 3 13 14 6 41 3 16 1 0 751

661* 138* 2 11 0 13 12 4 0 10 4 3 88 86 6 3 13 36* 1 81* 8 39* 5 0 1224

865 229 2 15 5 31 21 4 2 34 4 23 147 282 28 6 26 50 7 122 11 55 6 0 1975

quadrats (20.2 v. 5.1 months; Wilcoxon (Gehan) statistic = 34.910, d.f. = 1, P < 0.001). The half-life of a cohort – i.e. the point at which 50% of its members are dead – was less than 1 year for unburned cohorts and more than 2 years for burned cohorts (Fig. 3). Survival curves in burned and unburned quadrats converged for the 2 cohorts after ~3 years (Fig. 3). For the first 2 post-burn cohorts in the first post-burn year (2002–03), RGR based on plant height was significantly greater in burned than in unburned quadrats (Fig. 4a, b). In the second post-burn year (2003–04), RGR did not differ significantly between unburned and burned quadrats for the first cohort, whereas second-cohort plants in unburned quadrats grew slightly but significantly faster than those in the burned quadrats (Fig. 4a, b). In the third post-burn year, first-cohort plants in the unburned quadrats had a higher RGR than those in the burned quadrats, but there was no statistical difference for the second cohort (Fig. 4a, b). For the first 2 post-burn cohorts, the frequency of chasmogamous flowering was significantly greater in burned than in unburned quadrats in the first post-burn year (Fig. 5). However, in Years 2 and 3, there was no significant difference in chasmogamous flowering for either cohort.


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Unburned quadrats

(a)

Burned quadrats

(a)

22

*

2

20

Colonisation of quadrats unoccupied preburn (%)

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18 16 14 1

12

Mean RGR (cm.cm–1.year–1) ± 95% CI

10 8 6 4 2 0 16

(b)

Net change in quadrat occupancy (%)

14 12 10 8 6

*

0

(b)

*

2

*

1

4 2 0

0 –2 Unburned

Burned

Fig. 2. Changes in quadrat occupancy for unburned and burned quadrats in Carter Creek sandhill, following the August 2001 prescribed burn: (a) percentage colonisation; (b) net percentage gain or loss in quadrat occupancy. 100 90 80

Survival (%)

70

Dec. 01 unburned Dec. 01 burned Mar. 02 unburned Mar. 02 burned

60 50 40

2002–03

2003–04

2004–05 –1

Fig. 4. Relative growth rate (RGR; height in cm cm year–1) of Polygala lewtonii plants in unburned and burned quadrats in Carter Creek sandhill for (a) first (December 2001) and (b) second (March 2002) post-burn quarterly cohorts for the first 3 post-burn years. For the December 2001 cohort, RGR was significantly greater in burned than in unburned quadrats in 2002–03 (t = 3.386, d.f. = 33, P = 0.002), but not in 2003–04 (t = 0.502, d.f. = 21, P = 0.621); in 2004–05, RGR was significantly greater in unburned quadrats (t = 2.429, d.f. = 61, P = 0.018). For the March 2002 cohort, RGR was significantly greater in burned than in unburned quadrats in 2002–03 (t = 2.422, d.f. = 20, P = 0.025), whereas it was significantly greater in unburned than in burned quadrats in 2003–04 (t = 2.409, d.f. = 9.9, P = 0.037), and there was no significant difference in 2004–05 (t = 0.888, d.f. = 22, P = 0.384).

30 20 10

Dec. 01 Mar. 02 Jun. 02 Sep. 02 Dec. 02 Mar. 03 Jun. 03 Sep. 03 Dec. 03 Mar. 04 Jun. 04 Sep. 04 Dec. 04 Mar. 05 Jun. 05 Sep. 05 Dec. 05 Mar. 06 Jun. 06 Sep. 06 Dec. 06 Mar. 07 Jun. 07 Sep. 07

0

Fig. 3. Survival curves for Polygala lewtonii seedlings in unburned and burned quadrats in the Carter Creek sandhill for the first 2 post-burn quarterly cohorts. The dotted horizontal line indicates the half life of the cohorts, the point at which the percentage of live plants in each cohort drops below 50%.

Post-burn plant density and density-dependent effects The post-burn seedling recruitment boom and the higher survival of recruits in burned quadrats resulted in significantly greater

plant density in burned than in unburned quadrats for the first 3 post-burn years (Fig. 6). Preburn plant density in unburned (median = 2.0 plants per quadrat, range = 1–6) and burned (median = 2.0 plants per quadrat, range = 1–19) quadrats did not differ significantly (Mann–Whitney U = 1350.5, P = 0.818; ratio of burned to unburned density = 1.08). However, for the first 13 post-burn surveys (December 2001–December 2004), density was at least 1.5 times greater in burned quadrats (range = 1.5–6.5; Fig. 6) and the median density for the period was significantly greater (Mann–Whitney U = 1.0, P < 0.001; median = 16.48 v. 2.68 plants per quadrat for burned and unburned quadrats, respectively). In contrast, in the next 11 surveys (March 2005–September 2007), the density ratio returned to preburn levels (range = 0.92–1.39) and the median density for the period did not differ significantly between the 2 burn treatments (Mann–Whitney U = 39.5, P = 0.171;

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1.0

90

Dec. 01 unburned Dec. 01 burned Mar. 02 unburned Mar. 02 burned

*

70

(a) 0.9

0.8

60 50

*

0.7

40 30

0.6

20 10 0

0

2003

2004

2005

Fig. 5. Percentage of Polygala lewtonii plants with chasmogamous flowers over 3 years, for 2 cohorts in burned and unburned quadrats in Carter Creek sandhill. Asterisks indicate significant differences between unburned and burned quadrats within a cohort: for Dec01 cohort, c2 = 11.014, d.f. = 1, P = 0.002; for Mar02 cohort, c2 = 5.867, d.f. = 1, P = 0.022 (P-value based on Fisher’s exact test; 1 cell had an expected frequency of 90% quarterly survival.

10

5

Discussion Apr. 01 Dec. 01 Mar. 02 Jun. 02 Sep. 02 Dec. 02 Mar. 03 Jun. 03 Sep. 03 Dec. 03 Mar. 04 Jun. 04 Sept. 04 Dec. 04 Mar. 05 Jun. 05 Sep. 05 Dec. 05 Mar. 06 Jun. 06 Sep. 06 Dec. 06 Mar. 07 Jun. 07 Sep. 07

0

Fig. 6. Change in quadrat density for Polygala lewtonii plants in unburned and burned quadrats in Carter Creek sandhill in pre- (April 2001) and 24 postburn censuses (December 2001–September 2007). Dashed lines mark annual censuses from 2002 to 2005, the period during which densities differed most greatly.

median = 3.02 v. 3.50 plants per quadrat for burned and unburned quadrats, respectively). Seedling survival decreased with conspecific density, but this negative effect in the first 6 post-burn quarterly censuses was weaker in burned than in unburned quadrats. In unburned quadrats, the highest survival was always associated with the lowest densities, but for early censuses in burned quadrats, survival was >90% even at high densities (Fig. 7). For burned quadrats, Spearman’s rank correlations between survival and density were particularly weak in the first 2 quarterly censuses (P > 0.05; Fig. 8). Density-dependent mortality in the burned quadrats increased in later censuses and the strength of the effect was generally greater than in unburned quadrats.

P. lewtonii plants are killed by fire, but fire promotes seedling recruitment, survival and small-scale colonisation, as well as growth and chasmogamous flowering in post-burn recruits. Our comprehensive study of cohorts shows that these effects are particularly important for cohorts that recruit within the first few months after fire. Although the benefits of fire are shortlived, they may be important for this short-lived herb in increasing survival and contributions to the seedbank. The positive effects of fire are sufficiently strong to temporarily relax the negative effects of increased plant density on survival in burned microsites. The combined effects of higher seedling recruitment, higher survival to reproduction and earlier flowering indicate that P. lewtonii plants recruiting into burned microsites make a greater contribution to the seedbank, and thus to the long-term viability of the population, than do recruits in unburned microsites. In the present study, we found that burned individuals of P. lewtonii do not resprout and that the only survivors in burned quadrats were the original aboveground parts of plants that were unburned or only slightly scorched. Therefore, we consider P. lewtonii an obligate seeder (Menges and Kohfeldt 1995; Whelan 1995). In this respect, P. lewtonii is similar to Eryngium cuneifolium Small (Menges and Quintana-Ascencio


0.0


353

Un 3 3 3 3 2 3 3 3 3 2 1 2 3 2 3 3 3 1 2 3 0 3 2 Bu 0 0 2 1 3 2 3 2 2 3 3 3 2 2 3 3 1 3 2 3 3 3 1

Strength of density dependence on survival based on Spearman's rho

Unburned quadrats –0.1

Burned quadrats Mean Spearman's rho

–0.2

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24

Census number Fig. 8. Spearman’s rank correlations (rho) of percentage survival with natural log of density for Polygala lewtonii plants in unburned and burned quadrats in Carter Creek sandhill based on 23 post-burn quarterly censuses. Note that 0 on the y-axis (= no correlation) is at the top of that axis and the lowest value (= strongest negative correlation) is at the bottom. Vertical lines intersecting the x-axis indicate annual censuses. Numbers above the graph indicate P-values of correlations for unburned (Un) and burned (Bu) quadrats: 0 = not significant; 1 = P 0.05; 2 = P 0.01; 3 = P 0.001.

2004), another Lake Wales Ridge endemic herb characterised as an obligate seeder, although a few resprouting individuals have been recorded. Recruits in the first 2 post-burn cohorts (December 2001 and March 2002) came from the seedbank, rather than from seeds shed by surviving adults, which did not produce chasmogamous flowers between the August 2001 burn and the December 2001 and March 2002 censuses. Although some post-burn recruitment may have come from chasmogamous seeds produced in spring 2001 or from cleistogamous seeds produced in fall 2001, it is likely that a portion originated from seeds produced in prior years. This interpretation is consistent with order-of-magnitude post-fire recruitment booms observed in other populations and with experimental evidence showing that P. lewtonii seeds sown in the field retain viability for at least 2 years (C. W. Weekley and E. S. Menges, unpubl. data). Whereas fire increased seedling recruitment in burned quadrats almost seven-fold relative to nearby unburned quadrats in the first 2 post-burn censuses, seedling recruitment was also impressive in unburned quadrats, particularly in the first census when the number of plants in unburned quadrats more than doubled. This may reflect smoke-stimulated germination, as smoke from adjacent burned areas wafted over quadrats in both the burned and control treatment blocks. Studies in other fire-maintained ecosystems have demonstrated that smoke alone may promote germination (Dixon et al. 1995; Keeley and Fotheringham 1997; Roche et al. 1997; Morris 2000; Brown et al. 2003; Williams et al. 2005). Seeds of a wide range of species germinate in response to cues from karrikins, including 3-methyl-2H-furo[2,3-c]pyran-2-one

(Flematti et al. 2004; Chiwocha et al. 2009), a component of smoke from burning vegetation. However, some species germinate in response to smoke but not to this specific chemical (Downes et al. 2010). Although smoke-enhanced germination has not yet been demonstrated in the field for any Florida scrub or sandhill species, Lindon and Menges (2008) have shown that short-term exposure to smoke significantly increased germination percentages of P. lewtonii seeds in the laboratory. Smoke has also been shown to increase the germination rate (but not the germination percentage) in the congeneric P. smallii (Fellows 2002), a rare herb endemic to Florida coastal scrub and pine rocklands (USFWS 1999). If smoke from adjacent fires can trigger increased germination from seeds in the seedbank, then the spatial scale of burn effects on demography may be far greater than previously thought. This would benefit species such as P. lewtonii even in unburned patches. Mosaic fires including unburned patches could thus be important to management, combining the benefits of stimulating recruitment in species with seedbanks, while also providing unburned refugia from which firesensitive species without seedbanks could colonise post-burn patches. Heterogenous fire regimes, by allowing for differential recruitment success in relation to different fire cues, are likely to favour floristic diversity (Clarke and French 2005). Above-average rainfall may also have contributed to the high germination percentages recorded following the August 2001 burn. Rainfall was 25% above the historical mean for the 5 fall and winter months between the burn and the first post-burn census. For the 2 months immediately preceding the census, rainfall was 43% above average. This result is consistent with previous

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records showing that P. lewtonii recruitment booms (in the absence of fire) often track rainfall patterns (C. W. Weekley, unpubl. data). However, despite high summer rainfall in the 3 years following the August 2001 burn, seedling recruitment was minimal in the 12 quarters following the initial post-fire booms of December 2001 and March 2002. By following recruits into both burned and unburned microsites, we were able to isolate the effects of fire on demographic performance against a background of rainfall variation. Colonisation of previously unoccupied quadrats by P. lewtonii was about 3 times greater in burned than in unburned quadrats. By removing litter and reducing competition, fire creates habitat for pyrogenic herbs such as P. lewtonii (McConnell and Menges 2002; Maret and Wilson 2005). Ant dispersal of P. lewtonii seeds (C. W. Weekley, unpubl. data) contributes to colonisation by transporting seeds to potentially favourable microsites. Because the seeds may remain dormant for at least 2 years (C. W. Weekley and E. S. Menges, unpubl. data), even seeds placed into initially unfavourable microsites may result in seedling recruitment following fire and the creation of more open microsites. P. lewtonii seeds readily imbibe water (C. Baskin, pers. comm.), ruling out physical dormancy (Baskin and Baskin 1998). However, in a ‘move-along’ experiment (Baskin and Baskin 2003) based on a range of photoperiod and temperatures regimes, no germinants emerged from 900 seeds, suggesting the possibility of physiological dormancy (C. Baskin, pers. comm.). The enhanced vital rates of P. lewtonii post-burn recruits are consistent with other studies in Florida scrub and sandhill ecosystems, showing that fire promotes survival (Menges and Gordon 1996; Carrington 1999; Menges and QuintanaAscencio 2004), growth (Menges and Kimmich 1996; Anderson and Menges 1997) and components of fecundity (Hartnett and Richardson 1989; Kirkman et al. 1998; McConnell and Menges 2002). Studies in pyrogenic ecosystems worldwide have shown similar results (e.g. Canales et al. 1994; Kaye et al. 2001). The mechanisms responsible for enhanced vital rates vary among ecosystems, and include removal of litter (McConnell and Menges 2002; Maret and Wilson 2005), ground lichens (Quintana-Ascencio and Menges 2000; Hawkes and Menges 2003) and competing vegetation (Reinhart and Menges 2004). Density-dependent mortality is common in the regulation of plant populations (Antonovics and Levin 1980). However, studies of the post-fire population dynamics of fire-responsive species have rarely considered the effects of density (an exception is Morris and Myerscough 1988). In our analysis of the effects of density on the survival of P. lewtonii seedlings recruiting into burned and unburned quadrats, we found a significant negative correlation between density and survival across all post-burn quarterly censuses. However, for burned quadrats in the first 2 post-burn censuses, the correlations were relatively weak, suggesting that for plants in burned quadrats, the positive effects of fire outweighed the negative effects of density. We also found that survival in the year after fire, as ascertained using quarterly censuses, was uniformly high, despite occasionally high densities. Clearly, something in the post-fire environment is relaxing the negative effects of density on survival. Post-fire benefits may be due to small-scale nutrient flushes (S. Hicks


and E. S. Menges, unpubl. data) and/or the removal of competing vegetation (Reinhart and Menges 2004). Although our study demonstrated multiple benefits of fire for P. lewtonii, this species also persists at some long-unburned sites. However, we have also documented small-scale local extirpations at sites that have gone without fire for only a few years (C. W. Weekley and E. S. Menges, unpubl. data). The maintenance of robust populations requires frequent fire and fire suppression risks the loss of populations. On the Lake Wales Ridge, over 85% of the yellow sand habitat required by P. lewtonii has been lost to development (Weekley et al. 2008) and remaining habitat fragments are often quite isolated. Therefore, populations in isolated patches of habitat may not be capable of being rescued by immigration if nearby populations have been extirpated because of fire suppression. With the inclusion of the present study, the benefits of fire on at least some part of the life cycle have now been documented in the peer-reviewed literature for 12 of the 20 federally listed vascular plants endemic to fire-maintained xeric uplands of the Lake Wales and adjacent ridges (USFWS 1999). The other 11 species are Bonamia grandiflora (A.Gray) Hallier f. (Hartnett and Richardson 1989), Conradina brevifolia Shinners (Slapcinsky et al. 2010), Crotalaria avonensis DeLaney & Wunderlin (Slapcinsky et al. 2010), Dicerandra frutescens Shinners (Menges et al. 2006; Slapcinsky et al. 2010), Eryngium cuneifolium (Menges and Quintana-Ascencio 2004), Eriogonum longifolium Nutt. var. gnaphalifolium Gand. (Satterthwaite et al. 2002), Hypericum cumulicola (Small) W.P. Adams (Quintana-Ascencio et al. 2003), Paronychia chartacea Fernald ssp. chartacea L.C.Anderson (Schafer et al. 2010), Polygonella basiramia (Small) G.L.Nesom & V.M. Bates (Quintana-Ascencio and Menges 2000), Prunus geniculata R.M. Harper (Weekley et al. 2010) and Warea carteri Small (Quintana-Ascencio et al. 2011). Compared with fire suppression, management regimes with occasional burns or individual fires generally have positive or neutral effects on vital rates or abundances of rare plants across the diversity of Florida ecosystems (Slapcinsky et al. 2010). For these species, and undoubtedly many others, fire suppression and habitat fragmentation constitute significant ongoing threats (Menges 1999; USFWS 1999). The threat is particularly acute for plants in longleaf pine/wiregrass sandhills and other ecosystems with short fire return intervals. Burning these habitats often enough to promote viable populations is a major challenge facing land managers. The challenge is compounded by habitat fragmentation, resulting in many relatively small protected parcels embedded in a rapidly expanding suburban matrix (Heuberger and Putz 2003), and creating limits on potential fire spread (Duncan and Schmalzer 2004). Addressing these challenges is key to the recovery and long-term survival of these rare and imperiled species. Acknowledgements The authors thank A. Craddock, M. Rickey, G. Clarke, S. Smith, S. Haller and several cohorts of plant laboratory interns for field assistance (complete list of interns available at http://www.archbold-station.org/abs/staff/menges/ esmcvasst.htm). We thank F. Adrian, D. Whitmore, B. Blihovde, D. Bender, and others at the US Fish and Wildlife Service for logistical support and for accomplishing the prescribed burn. The manuscript was improved by


trenchant comments from R. Dolan, T. Knight and R. Salguero-Gomez. Funding for this project was provided by the Florida Division of Plant Industry, the National Science Foundation (DEB0233899, DEB0812717) and Archbold Biological Station. We also thank Florida’s Endangered Plant Advisory Council for their support and advice. Finally, we thank reviewer David Keith and the associate editor for their helpful comments.

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