For. Snow Landsc. Res. 75, 3: 339–356 (2000) 339

Ecology and post-fire recovery of perforata, an endangered -scrub

Rebecca Yahr1

Archbold Biological Station, PO Box 2057, Lake Placid, FL 33862, USA 1 Current address: Duke University, Department of Biology, Box 90338, Durham, NC 27708, USA [email protected]

Abstract Cladonia perforata is an endangered terrestrial lichen which co-occurs with many fire-adapted species in central Florida scrub. Prescribed fire is a common tool in the maintenance of natural landscapes and of high diversity within some plant communities, but its role in lichen communities is little studied. A prescribed fire at Archbold Biological Station on the southern end of the Lake Wales Ridge impacted three separate populations of C. perforata in July 1993, leaving only rem- nant unburned patches scattered among completely burned areas. This study was undertaken to investigate the rate and mode of post-fire recovery of C. perforata in comparison with co-occurring .Detailed GPS maps of individual patches of this lichen were made in January 1997 and com- pared with those made in August 1999. In addition, abundance of all lichen species was monitored yearly during the winters of 1997–1999. Although all of the other terrestrial species in the same habitat recovered from juvenile stages, no juvenile forms of C. perforata were recorded. The area occupied by C. perforata increased by more than 200% , on average, over the three sites. However, population growth (for all species) has so far been too slow to be documented and has not changed markedly over this period.Therefore, dispersal of unburned C. perforata into burned areas may be the primary method of short-term population recovery.

Keywords: fire, recovery, Cladonia, ecology, Florida scrub, endemic

1 Introduction

Fire is a widely studied natural disturbance that is critical in defining plant and animal com- munities (CHRISTENSEN 1985) since it reduces ground cover, spurs productivity and repro- duction, and maintains open space suitable for colonization (PICKETT and WHITE 1985, WHELAN 1995, MENGES and HAWKES 1998). Changes in plant community composition and species distribution patterns are known to vary with fire intensity, scale of disturbance,and time since disturbance (WHITE 1979, CHRISTENSEN 1985, MENGES and HAWKES 1998). In fire-maintained Florida scrub, post-fire vegetation recovery patterns vary with scrub type (MENGES and HAWKES 1998) and with species (MENGES and KOHFELDT 1995),although most vascular species recover pre-fire abundance after only a few years following fire. Cladonia perforata A. Evans () is an endangered terrestrial lichen which occurs in this fire-prone and fire-managed landscape. Florida scrub is populated by other more common Cladonia species and by many other endemic species with specific and varying niches in relation to fire.Historically in the south-eastern United States,fire has been an important part of the ecosystem process in scrub (MYERS 1990) and is increasingly used as a management tool for restoration and habitat maintenance. Yet, the post-fire rate and mode of recovery of these lichen species is unknown. 340 Rebecca Yahr

Many members of Florida scrub communities, ranging from Florida Scrub-Jays (FITZPATRICK et al. 1994) to invertebrates (DEYRUP 1989) to herbaceous plants, are dependent on periodic fire for habitat maintenance (reviewed in MENGES 1999). In the Florida scrub, many endemic herbaceous species rely on fire for the creation and maintenance of open sand gaps (JOHNSON and ABRAHAMSON 1990, HAWKES and MENGES 1996), though optimal fire- return intervals vary with species (MENGES 1999). In scrub dominated by Florida rosemary ( ericoides Michx.), at least three of these species, Hypericum cumulicola (Small) P. Adams, Eryngium cuneifolium Small, and Polygonella basiramia (Small) G.L. Nelson & V.M. Bates have peak population sizes within the first ten years following fire.These species recover from seedbanks or occasionally resprout (HAWKES andMENGES 1995,MENGES andKIMMICH 1996, QUINTANA-ASCENCIO et al. 1998). They decline more or less rapidly in the following years as favorable microhabitats change, with open gaps giving way to increasing shrub cover. In contrast,the dominant shrub,Ceratiola ericoides, does not reach reproductive maturity until at least seven years after fire (JOHNSON 1982), so that it is lost from sites with rapid fire-return intervals. The life-history of lichens in relation to fire has been little studied. Lichens have no perennating underground structures or other mechanisms which allow them to tolerate fire, which means fire either kills or severely damages them (JOHNSON and ABRAHAMSON 1990, SCHULTEN 1985), and recolonization is solely via dispersal from unburned sources. In addition, vegetative growth is quite slow (TOPHAM 1977), and the development of dense, dominant lichen mats probably takes several decades. The post-fire recovery of lichen populations has been investigated in boreal and north-temperate areas and can be generalized as follows: appearance of Cladonia species within the first five years, becoming dominant approx.20–25 years following fire and followed by replacement with per- sistent, stable Cladina mats (AHTI 1959, MAIKAWA and KERSHAW 1976, MORNEAU and PAYETTE 1989). In Florida scrub, MENGES and HAWKES (1998) have noted elements of a similar progression. Cladonia perforata occurs in a smaller percentage of available habitats than do other ter- restrial Cladonia species of Florida scrub. It is patchily distributed in open gaps in rosemary scrub, a xeric vegetation type characterized by abundant open space (“sand pine scrub, rose- mary phase” sensu ABRAHAMSON et al. 1984). Fires in the southern Florida peninsula, as well as hurricanes along the Gulf Coast,represent natural periodic disturbances that may be impor- tant in maintaining this open habitat structure for C. perforata and other species dependent upon gaps in the shrub canopy. Natural openings in rosemary scrub can persist for decades in some sites, though shrub and tree canopies and litter tend to slowly increase, eliminating the xeric bare sand gaps important for herbs and some lichens (HAWKES and MENGES 1996, MENGES and KOHFELDT 1995). Natural fire return intervals are estimated at between 10–100 years in this habitat (MAIN and MENGES 1997). During recent decades, natural fire has been replaced by either fire suppression or prescribed burning. The consequences of fire suppres- sion include the loss of open spaces,which presumably results in the loss of this lichen.In addi- tion, the effects of can compound changes due to fire suppression by altering fire frequency or intensity.Where prescribed fires replace natural fires,land managers must determine how to implement fire as a landscape-scale management tool to maintain diversity and encourage persistence of species and communities of interest. Three of the known populations of C. perforata were burned in recent years, and, in all cases, small remnant populations of the lichen have been found. For this study, populations are defined as discrete occurrences of C. perforata, limited by the extent of local habitat.The boundaries of each are easily discerned in the field. For. Snow Landsc. Res. 75, 3 (2000) 341

2 Objectives

This project was undertaken to characterize post-fire population recovery and growth, inter- specific interactions, and microsite preferences of the terrestrial Cladoniaceae in central Florida, especially C. perforata. Post-fire population recovery includes the mechanisms of establishment or the recolonization of burned sites and rate of population growth. A combi- nation of the data on population spread and on dispersal limitations can be used to refine habitat requirements and to estimate the relative threats and risks of local extirpations.These insights will offer confidence in the use of prescribed fire or other management tools to promote the species in a landscape. In addition, abundance estimates measured only a few years after a fire will provide a baseline for studies of population growth.

3 Methods

3.1 Species studied

Cladonia perforata, an endemic lichen of Florida sand pine scrub (BUCKLEY and HENDRICKSON 1986, EVANS 1952), is listed by the U.S. Fish and Wildlife Service (1989) as endangered.About 30 populations are distributed across three distinct regions,the north Gulf Coast, the Atlantic Coastal Ridge, and the Lake Wales Ridge. The latter probably supports about two thirds of all known sites. Only a few sites throughout its range are protected, while the rest are threatened by some combination of habitat loss due to development or agricultural conversion, human disturbance, improper management, and hurricane washover (USFWS, 1989, Ann F. Johnson and Dennis Teague, pers. comm.). Discrete populations are typically found as isolated patches on knoll tops of rosemary scrub patches, which form discrete habitat islands separated by intervening dense oak and palmet- to scrub.As vegetation develops after fire on these rosemary scrub patches,the shrubs become more dense, and bare sand gives way to increased litter and lichen cover. Nevertheless, roughly 30% of the bare sand persists for more than 25 years (HAWKES and MENGES 1996). In the surrounding lower-elevation vegetation, the open space drops to less than 10% in less than three years after fire (YOUNG and MENGES 1999). In addition to the rarity imposed by temporal variation in the availability of colonizable sites, dispersal limitations due to habitat factors and mode of reproduction may also be important in influencing this species’ patchy distribution. At present, no primary thallus, no spore-producing structures nor other specialized long-distance propagules, such as soredia, are known (EVANS 1952). Presumably, vegetative fragmentation of the thallus is the sole means of reproduction. Therefore, limitations to dispersal may be an important factor in explaining the rarity of C. perforata, even within seemingly appropriate habitat patches. The other Cladonia and Cladina species included in this study have wider North American distributions,ranging from all of eastern North America for Cladina subtenuis,extending from Texas to the middle-Atlantic Coastal Plain for Cladina evansii (Abbayes) Hale & W.L. Culb. and Cladonia leporina Fr., and including only the south-eastern Coastal Plain for Cladonia pachycladodes Vain., Cladonia prostrata A. Evans, and Cladonia subsetacea (Abbayes) Hale & W.L. Culb. Of these, only Cladonia leporina and, much less often, Cladina subtenuis are 342 Rebecca Yahr commonly found to be fertile. None of these species bear soredia, which are tiny specialized vegetative reproductive structures containing both fungal and algal partners. The term “juvenile” is used here in the sense of AHTI (2000), referring to the early lichenized stage con- sisting of squamules or granules, growing horizontally and attached to the lichen’s substrate. For several of the Florida scrub species, such as Cladonia pachycladodes, C. subsetacea and C. perforata, juveniles in this sense are not known; instead small vegetative fragments are assumed to disperse and propagate. The taxonomic treatment of vascular plants follows WUNDERLIN (1998).

3.2 Study site

This study was carried out at Archbold Biological Station (ABS), at the southern terminus of the Lake Wales Ridge, southern Highlands County, Florida (27°10’50”N, 81°21’00”W). This 1081 ha preserve is characterized by a mosaic of seasonally flooded wetlands, flatwoods, and scrubby flatwoods (fire-maintained oak scrub), with occasional scattered patches of rosemary scrub on the knoll tops. Rosemary scrub is found on the extremely well drained St. Lucie, Archbold, and Satellite soils, which can be characterized as acid, nutrient-poor sands. The regional climate is subtropical, with hot, wet summers and mild, dry winters (7.7 °C January mean, 34.6 °C July mean, 140 cm rain per annum; data from Archbold Biological Station). Of the over 100 available rosemary scrub patches at ABS, only eight currently support C. perforata.They are all within about 3.2 km of one another and none farther than 0.8 km from the next. The closest populations are within 50 m of one another.

3.3 Post-fire recolonization

A prescribed fire in July of 1993 partially burned five of the eight populations of C. perforata at ABS. In 1996, I selected three of the burned rosemary scrub balds as study sites. These are known as Balds 42, 49, and 50 (Fig. 1) according to a system already in use at ABS.Within each of these study sites, small, well-defined, unburned remnant patches of C. perforata remained following the fire. In addition to containing such unburned refugia, study sites were also characterized by large open areas of complete, high-intensity burns where no lichen mats survived. My studies of post-fire recolonization include: 1) comparing mapped boundaries of remnant patches at each site at the start and at the end of the study; 2) estimating changes in population growth by randomly sampling lichen abundance over the study period; and 3) investigating interspecific interactions and microsite preferences of the terrestrial Cladonia and Cladina species, with an emphasis on C. perforata.

3.3.1 Mapping

In January 1997, I used Global Positioning System (GPS) technology to map the individual remnant patches at each site accurately.Estimates of the areas covered by C.perforata in every remnant patch were made in January 1997 and in August 1999 to document population expan- sion from unburned refugia. The GPS work in 1997 was completed in cooperation with the Florida Plant Conservation Program of the Division of Forestry. The analyses of the patch areas were completed using ARC/VIEW and ARC/INFO. For. Snow Landsc. Res. 75, 3 (2000) 343

Archbold Biological Station Station property Study site sampling grids Cladonia perforata patch boundaries, 1997 Cladonia perforata sites

Bald 42

Bald 49

Bald 50 N Fig. 1.Archbold Biological Station locat- ed on central Florida’s Lake Wales Ridge.Shown inset are the three rosemary 0 500 1000 balds partially burned in 1993 and used Meters as study sites, Balds 42, 49, and 50.

3.3.2 Population changes

For the most part, fire intensity is negatively correlated with lichen abundance, so that fire intensity maps provide an estimate of post-burn extant lichen habitat and cover. However, even in areas with high-intensity burns, small patches of unburned or lightly burned patches often occur, which are too small to have been detected or mapped in large-scale fire intensity mapping techniques employed by ABS as part of their prescribed fire management regime. In addition, not all unburned patches contain C. perforata. In December 1996, I ground- truthed fire intensity maps for each site to estimate current boundaries of remnant C. perforata patches (ABS Geographic Information System Lab maps). Those approximate boundaries were used to install a grid of 20 x 20 m cells at each study site and were permanently marked at all corners with aluminum stakes and tags. In one study site, Bald 50, four 10 x 20 m grid cells were used since a pre-existing grid had already been established. In addition, along the western side of Bald 49, a row of 10 x 20 m grid cells was used to ensure that the roadside was included, since this area comprises most of the extant population at that site. Grids were set up in order to cover both burned and unburned areas, incorporating the border between these and extending up to 20 m into completely burned areas. The inclusion of grid cells that were completely burned on each site ensured that changes in lichen distribution across burn intensities would be obvious over time. The total size of each grid (on each site) varied with each site’s specific burn intensity and current lichen distribution. At one site, Bald 50, the entire rosemary bald is completely 344 Rebecca Yahr contained within the grid system, which covers a total of 6000 m2. At each of the other two sites, I aligned cell boundaries with the intersections between burned and unburned patches with the intention of capturing recolonization over the interval of the study without covering the entire bald. The grid system on Bald 42 covers 2800 m2 and on Bald 49 4400 m2. Recolonization will be marked by the appearance of lichen in a completely burned, previ- ously unoccupied area,probably via spread from an unburned or partially burned patch.Each grid cell is labeled with a unique number across all sites.A total of 27 20 x 20 m and 4 10 x 10 m grid cells were sampled in the winters of 1997, 1998, and 1999. Grids were mapped using the GPS. Maps showing remnant, unburned C. perforata patches overlaid on site and grid boundaries were prepared to allow spatial tracking of changes in population area and size. In each grid cell, randomly placed 0.1 m2 (20 x 50 cm) quadrats were used to determine the abundance (cover) of all terrestrial lichen species, the frequency of vascular plant cover, and the presence or absence of litter cover. In order to sample each grid cell evenly, I used 20 quadrats per 20 x 20 m cell and 10 per 10 x 20 m cell. Vascular plant frequency was recorded only for rooted species.Litter composition and presence was recorded only if it exceeded 30% of the quadrat area. Percent cover for all terrestrial lichen species follows a modified Braun- Blanquet cover class system with 10 classes ( 0% , <1% , 1–5% , 6–10% , 11–25% , 26–50% , 51–75% ,76–95% ,96–99% ,>99% ).In preliminary sampling,I compared 10,20 and 40 quadrats per 20 x 20 m grid cell and determined that using 20 quadrats per cell optimizes the balance between sampling time and areal coverage estimation for lichen species. Power analyses sug- gest that this sampling intensity can detect differences of 15% in the proportion of grid cells occupied and the abundance of C. perforata and other lichens (SamplePower v.8.0).For analy- sis, each cover class was translated into its respective mean cover (e.g. mean value of class with 0–1% cover = 0.5). These means were then averaged at the level of grid cell for each year. Each grid cell was classified individually as either burned or unburned according to sub- jective assessments in the field.The presence of fire-killed shrubs, completely consumed small twigs, no litter and absence of terrestrial lichens indicated “burned” grid cells. “Unburned” grid cells had unburned shrubs and accumulations of litter and dense mats of terrestrial lichens, but part of the grid cell might still have been burned. Differences in population changes for each species were examined at the level of grid cell in two classes: completely burned versus partially burned or unburned cells. The rationale for classifying grid cells that had been only partially-burned as “unburned” was that even small unburned patches often contain potential habitats for unburned terrestrial lichens. For all lichen species, I asked the questions: Is there evidence of population recovery over the period 1997–1999? Do species differ in their post-fire recovery strategies or rates in response to fire? For Cladonia perforata, I asked, more specifically: Is recovery measurable by a change in abundance and/or by changes in spatial extent, i.e. does a formerly unoccupied site recover at the expense of occupied sites? Tests of mean lichen cover and changes in mean lichen cover (mean percent cover in 1999 – mean percent lichen cover in 1997) were performed using SPSS v. 6.1.1.

3.3.3 Microsite

To resolve microsite preferences of the terrestrial lichens co-occurring with C. perforata, Spearman’s rho, a nonparametric correlation coefficient, was calculated. The microsite characteristics examined include its burn class (completely burned versus partially burned or unburned) and the frequency of vascular plants (found in at least 5% of the quadrats sampled), terrestrial lichens, and litter found on it. For. Snow Landsc. Res. 75, 3 (2000) 345

4 Results

4.1 Mapping

In 1997, there were a total of 13 patches of C. perforata across the three sites covering a total area of 2103 m2. In 1999, several of the smaller patches had grown together, comprising a total of 10 patches across the three sites with a total area of 4856 m2 (Table 1, Fig. 2). In Bald 50, one patch mapped in 1997 was missing in 1999, and one patch mapped in 1999 was missing in 1997. Most of the mapped changes can be attributed to local dispersal outward from the occupied patches. The most notable changes were in Bald 42, where dispersal occurred up to 20 m from the edge of the largest patch. Many small fragments of thalli were observed under the canopy and in the litter of oak shrubs. Small thallus fragments differ from ontogenetically early life stages in Cladoniaceae, where “juvenile” refers to the first developmental stage of horizontally growing crustose or foliose lichenized thalli. This stage was never observed for C. perforata.

Table 1. Changes in areal coverage of Cladonia perforata in three sites over 32 months, from January 1997 to August 1999 at Archbold Biological Station.All measurements were made using GPS data transferred to ARC/VIEW coverages.

Bald Total Area of Bald Patch Area 1997 (m2) Area 1999 (m2) Percent (available habitat, m2) Increase 42 1 1133 2807 2 19 968 3 331 (part of 2) 17010 All 1483 3775 254 49 1 208 251 2 93 263 3 35 (part of 2) 421 54 531 64 7100 All 388 632 163 50 1 137 265 2 7 missed 3277 4 30 (part of 3) 556 73 6 missed 34 3779 All 232 449 196 Total 27889 All Sites 2103 4856 X = 231 346 Rebecca Yahr a b

Sampling Grid 1997 (353 m2) 1999 (632 m2)

Sampling Grid 1997 (1483 m2) 1999 (3775 m2)

c

N

Sampling Grid 1997 (232 m2) 20 Meters 1999 (449 m2)

Fig. 2. Comparison of the size of occupied areas of C. perforata in January 1997 and August 1999. The sampling grid is shown for reference. a) Bald 42, b) Bald 49, c) Bald 50. For. Snow Landsc. Res. 75, 3 (2000) 347

4.2 Lichen abundance

All sites were sampled in the winters of (late December through early February) of 1997,1998, and 1999. Mean lichen cover varied over time in relation to both site and grid cell (depending on burn), with most grid cells experiencing either slight increases or no net change (increase in one year followed by a decrease the next,or vice versa).Table 2 summarizes the mean lichen cover of all species by burn category (burned or unburned as defined in the methods section) and year for each site.To detect differences in lichen populations at each sampling time,mean cover was investigated each year for each species. Burned grid cells had fewer species on average (Mann-Whitney U = 33.0, p <0.001) and lower mean cover while unburned plots typically had more lichen species and higher cover. No significant differences in mean cover were detected for any species according to year, although there was a very slight trend over- all for increased cover for all species combined (Table 2). Table 3 presents the results of the ANOVA of mean cover of each lichen species by site, year and bald, and their interactions. For all species, most of the variation in mean cover could be explained by whether or not the sampling area was burned or not during the prescribed fire (Table 3,Fig.3).In addition,except for the species C. perforata and C. subsetacea, there were significant interactions between the categories burn and site, since the response to burns varied from site to site (see below). Across the three sites,the proportion of completely burned grid cells varies (Table 2).Since interaction terms make interpretation difficult, ANOVAs of mean cover by burn and year were computed for each site separately for those species with interaction terms. Mean cover changed differently according to species and site, with some species increasing over time in one site and decreasing in another site, depending on whether the site had been burned (Fig. 4). Since the life history of each species differs, I also asked whether recovery of populations in response to fire differed among species by considering changes in mean cover between 1997 and 1999 in burned grid cells only. Despite much variation in the response of each species according to site (Fig. 4), there was no effect of species or site on changes in mean cover (F value for both site and species <1.3, p >0.2). In these analyses, the power of sampling was too low to distinguish error from small but significant changes in abundance.

Table 2. Summaries of total lichen cover by burn effect and year, where grid-cell-level data were aggre- gated to site (bald) level and averaged over all species.

Mean Percent Cover (Std. Dev.) Site No. Grid Burned Species/Grid cell 1997 1999 (Bald) Cells/Bald 42 5 No/Partial 6.2 0.58 (0.322) 0.61 (0.319) 2 Yes 2.5 0.00 (0.006) 0.04 (0.035) 49 4 No/Partial 4.5 0.36 (0.267) 0.29 (0.278) 7 Yes 3.4 0.06 (0.051) 0.06 (0.060) 50 4 No/Partial 5.3 0.18 (0.119) 0.29 (0.180) 9 Yes 3.8 0.06 (0.059) 0.09 (0.070) 348 Rebecca Yahr

0.20 Unburned or partially burned n = 13

0.15

0.10

Mean Change 0.05

0.00

-0.05 evansii pachycladodes prostrata subtenuis leporina perforata subsetacea

0.15 Burned n = 18

0.10

0.05 Mean Change

0.00

-0.05 evansii pachycladodes prostrata subtenuis leporina perforata subsetacea

Species

Fig. 3. Summaries of population changes by species between 1997 and 1999. Bars show mean changes in percent cover averaged over sampled grid cells and combined for all sites. Error bars are standard error. The difference between burned and unburned grid cells is significant; variation among species is not sig- nificantly different. For. Snow Landsc. Res. 75, 3 (2000) 349

Table 3. F values based on ANOVA with fixed effects of year, site (bald), and burned/unburned for mean cover of seven lichen species at Archbold Biological Station. * p <0.05, ** p <0.01, *** p <0.001

Source of Variation (Categories) Species Burn (2) Year (3) Site (3) Burn x Year Burn x Site Year x Site evansii 33.36*** 0.25 13.68*** 0.18 14.29*** 1.01 leporina 44.50*** 0.44 6.18** 0.11 8.63*** 0.62 pachycladodes 25.46*** 0.44 1.01 0.44 5.27** 1.79 perforata 19.75*** 0.23 0.72 0.24 1.04 0.41 prostrata 40.99*** 0.07 2.16 0.13 3.76* 0.85 subsetacea 24.20*** 0.24 1.95 0.19 0.40 0.65 subtenuis 13.76*** 0.74 4.69* 0.77 4.78* 1.03

Unburned or partially burned *** * * 0.6

0.4 Bald 42 n = 5 0.2 Bald 49 n = 4

Mean Change 0.0 Bald 50 n = 4

-0.2

evansii pachycladodes subtenuis leporina prostrata

0.6 Burned

0.4 *** * * Bald 42 n = 2

0.2 Bald 49 n = 7

Mean Change Bald 50 0.0 n = 9

-0.2

evansii pachycladodes subtenuis leporina prostrata Species

Fig. 4. Summaries of population changes between 1997 and 1999 according to site, shown only for those species which had significant interactions between burn effect and site. Bars show mean changes in per- cent cover averaged over sampled grid cells; error bars indicate standard error. For all species shown, the differences between burned and unburned/partially burned population changes were significant, but the magnitude of the change by species was not. 350 Rebecca Yahr

4.3 Microsite and interspecific interactions

The frequency of each lichen species was positively correlated with that of each of the other lichens and negatively with burned sites. Most species were negatively associated with oak litter (except C. evansii showed no correlation) and with the presence of oak shrubs (5 out of 7 species for Quercus inopina Ashe and 6 out of 7 for Q. geminata Small). Most showed a positive correlation with rosemary litter (except C. perforata, which had no correlation) (Appendix A). The presence of C. perforata is positively correlated with the presence of Cladonia leporina, Cladina evansii, Cladina subtenuis, Cladonia subsetacea, Cladonia prostrata, Cladonia pachycladodes, A ristida gyrans Ashe, and negatively with that of Serenoa repens (Bartr.) Small, Quercus inopina, Q. geminata, oak litter, and burned sites.

5 Discussion

5.1 Population recovery

It is clear that lichen population recovery is a slow process in Florida scrub, requiring several decades for cover to increase beyond a few percent (HAWKES and MENGES 1996). Although the occasional species found to be fertile or juvenile should recover much faster in the newly available, recently-burned habitats in this study, it was impossible to detect differences in recovery over the interval (change in mean cover between 1997 and 1999) according to species and such known life-history differences. In addition, although the size of the patches occupied by C. perforata increased substantially during this interval, its abundance overall, measured by mean cover, did not increase.Therefore, there may be no growth of this lichen overall, but only a locally wider distribution of the same individuals (Fig. 3). Recolonization by the dispersal of lichens from unburned areas is slow, but varies with species and site. For example, by 1999 on Bald 42, Cladonia leporina was rather common as juvenile thalli on the base of burned shrubs (Fig. 4), but was not as abundant in other sites. Site differences may be substantial, since each rosemary scrub bald is unique, characterized by different patterns of unburned and burned vegetation, pre-fire lichen cover, local envi- ronmental variation, and other factors. Most of the variation in observed lichen cover even eight years after a fire can still be accounted for only by whether or not that area was burned during the prescribed fire, indicating that unburned refugia are the sources of lichens in these habitats.Although burn category does explain a large amount of the variation in lichen cover in the sites, these two values (burned and unburned) do not adequately describe the amount of post-fire variation that exists as a result of uneven fire intensities across each site.As a result of the broad categorizations used here, even grid cells with very severe fire intensities were included in the “unburned or partially burned” category as long as one small area was left unburned.Although this allows a clear interpretation of changes in cover for those completely burned grid cells, the differences between, and even within, unburned grid cells was at the start of the study quite considerable. For example, in Bald 42, most grid cells were unburned, whereas in the other two sites, most of the grid cells were completely burned. In addition, the fire intensity within each category may vary. In Bald 42 many of the unburned or partially burned cells were part of a large area which experienced almost no effects of fire. In contrast, in Balds 49 and 50, the burn across the sites was more even, leaving several smaller patches burned with light-to-medium intensity as part of the unburned or partially burned category. For. Snow Landsc. Res. 75, 3 (2000) 351

In addition,site-to-site variation includes pre-fire differences in lichen cover and vegetation. For example, as an indication of variation among sites, the proportions of quadrats in each site dominated by oak cover were calculated, as they provide reasonable estimates of microsites unsuitable for lichens (these site-level values are negatively correlated with lichen cover averaged in unburned areas, r2 = 0.617, data not shown). Oak-dominated areas were most abundant in Bald 50 (ranging from about 48–52% of quadrats with at least 30% oak cover and litter), less abundant in Bald 49 (30–42% ) and least abundant in Bald 42 (23–35% ) in all three years.These differences are likely to be reflected in both pre-fire lichen abundance and the long-term development of lichen communities in these sites, since shrub canopies and litter create unfavorable microsites for terrestrial Cladoniaceae. It is likely that some of the variation detected in the analysis can be attributed, at least in part, to sampling error. Lichens are notoriously slow-growing and detectable changes will probably occur over a much longer time scale than that of this study. Studies of lichen recol- onization typically involve a time scale of decades (MAIKAWA and KERSHAW 1976, KLEIN 1982, MORNEAU and PAYETTE 1989). Nonetheless, repeated visits to the sites do allow some observations on lichen recovery: 1) Cladonia leporina was observed in the form of juvenile primary thalli on the bases of fire- burned shrubs by late 1997 and more abundantly the following year. None of these thalli were observed to be fertile at the end of the study. Cladina subtenuis was also observed recruiting as juvenile thalli on the base of fire-killed shrubs by the winter of 1997–1998 and Cladina evansii appeared by the following year. It is not uncommon to find juveniles of Cladonia leporina, Cladina subtenuis and, occasionally, Cladina evansii on lignified stumps or fence posts in the scrub. These three species are assumed to have begun as spores germinating on rotting wood. 2) Cladonia prostrata and Cladonia pachycladodes were observed to emerge directly from the bare sand in burned areas.These thalli were assumed to recruit in situ since they were round, symmetrical colonies, well imbedded in the soil rather than small fragments likely to have dispersed from unburned areas. 3) Cladonia perforata was only observed as vegetative fragments both in burned and unburned sites; the most likely explanation of these thalli in burned areas is dispersal from unburned refugia since primary thalli have never been observed. Elsewhere in Florida, both Cladina species considered in this study are found with apothecia. At Archbold Biological Station, however, all the species considered in this study except Cladonia leporina are found exclusively as sterile thalli, unattached to the soil. Estimates of the population size and growth of fragmenting species unattached to their substrates are complicated and seem best made via areal coverage measures combined with abundance measures. Counts of individual ramets or genets are unfeasible and typically not useful,since ramets easily fragment and genets cannot be determined in the field.For Cladonia perforata,post-fire populations increased substantially in areal coverage but not in abundance over the study period.The maximal distance of spread, measured from the edge of the occupied area in 1997 to that in 1999 is approx. 20 m. However, since all of these sites are moderately impacted by human trampling, this rate of spread may be inflated and can be inferred to represent a high estimate of dispersal. In addition, C. perforata was observed to recover from fire only by spreading outward from unburned refugia, whereas all the other species were observed to recruit from juvenile stages or inferred juvenile stages. In Florida scrub, vascular plant species recover from seedbanks and/or by resprouting, regaining pre-fire cover within only a few years (YOUNG and MENGES 1999). Similarly, in grasslands, the cover of vascular plants in burned areas becomes as extensive as that in unburned areas after only three years. On the other hand, lichens recover much more slowly (ANTOS et al. 1983, SCHULTEN 1985). JOHANSEN et al. (1984) found that after five years, 352 Rebecca Yahr recovery of lichens in terms of biomass or species composition was still not complete.In South American scrub (cerrado vegetation), bark-inhabiting species of lichens have been used as bioindicators of past fire (MISTRY 1998). Lichen cover can take decades to recovery after fire in boreal zones (MAIKAWA and KERSHAW 1976, KLEIN 1982, MORNEAU and PAYETTE 1989). Therefore it should not be surprising that over the short duration of this study, there were no significant changes in lichen cover. However, it is interesting to note that, despite contrasting recovery mechanisms, none of these species was significantly more abundant than the others.

5.2 Management implications

The interaction (“synergism” of PICKETT and WHITE 1985) of vegetation and disturbance can influence some components of the disturbance, like return interval and intensity, and can create variable microsites in the post-fire environment. The microsites of the terrestrial Cladoniaceae can be characterized by open sand without litter and lack of shrubs and are often correlated with the presence of other herbaceous species found in open sand gaps of rosemary scrub. Although lichens are killed by fire and recolonize solely via dispersal from unburned sources, C. perforata usually occurs in bare-sand gaps between shrubs and is there- fore somewhat protected from fire by occurring in these low- or no-fuel sites. In this study, C. perforata was often found as scattered thalli in the litter under trees or shrubs where dead leaves and litter can carry fire easily. With the high intensity fires typical of rosemary scrub habitats, it is extremely susceptible to destruction by fire even in gaps with relatively low fuels. In areas where lichen mats are dense, however, lichens themselves are excellent fuels (QUINTILIO et al. 1977). For under management, careful and deliberate monitoring of popula- tions is essential.The protocols here may offer methods for both mapping terrestrial vagrant lichens quickly and estimating their intensive abundance. Mapping the spatial extent of these lichens can be efficiently completed by GPS boundary mapping, which involves less than a day’s work for most populations; and in a subset of occupied areas, abundance can be esti- mated. Since changes in abundance occur over long time intervals and estimating abundance is time consuming, this should only be done perhaps every five years or even less frequently in stable sites. Population boundaries should be monitored before and after fires and other disturbances as well. Central Florida’s Lake Wales Ridge is a unique feature of the landscape in terms of both its geologic history and its rich endemic communities. By several estimates it is one of the richest regions of endemism in the United States (DOBSON et al. 1997). It is home to C. perforata and more than 20 narrowly endemic species of vascular plants (CHRISTMAN and JUDD 1990), two kinds of vertebrate, and dozens of invertebrates (DEYRUP andFRANZ 1994). In addition, it represents the bulk of the range of many other species only slightly more widely distributed. As such it is a target of coordinated and concerted regional conservation efforts aiming for sound ecological management. Management strategies that include periodic prescribed fire are an important part of maintaining suitable habitats for many species (FITZPATRICK et al. 1994, MENGES andHAWKES 1998).They must balance the habitat require- ments of all of the resident taxa, from herbs which peak immediately post-fire to slow-growing lichens. The magnitude and time scale of population dynamics varies, with some species resprout- ing immediately and increasing slowly to recover pre-fire abundance (MENGES and KOHFELDT 1995) and others sharply increasing immediately after fire and dropping back in numbers within ten years (HAWKES andMENGES 1996,QUINTANA-ASCENSIO andMORALES- For. Snow Landsc. Res. 75, 3 (2000) 353

HERNANDEZ 1997). Although lichens are killed by fire, the short-term costs of fire-caused mortality are far outweighed by the longer-term availability of habitat in a fire-maintained landscape. Land management must include an understanding of the consequences of specific management regimes for individual species of concern and, for these include a balance of the length of time since fire to accommodate differing life history strategies. The degree of temporal and spatial patchiness in each disturbance component should be of great interest to land managers charged with maintaining favorable habitats for species with varying microsite tolerances, life-histories and colonization abilities. Recovery and conservation on a per-species basis is costly and inefficient, so most recom- mendations deal with guilds of species that have similar ecological requirements. For example, the perennial herbs in canopy gaps of rosemary scrub have peak abundance within ten years post-fire (MENGES and HAWKES 1996). Although bare sand gaps are more persistent in rosemary scrub than in other scrub types (JOHNSON et al. 1986), they still diminish with time since fire as canopies close and litter accumulates.Lichens such as C. perforata,which are most common in bare sand gaps, are probably limited by canopy closure, but may be less resilient than herbs to fire, having no underground reservoir of seeds or storage organs from which to resprout. Mirroring this dependence on open gaps in scrub, Florida scrub jays may have similar habitat requirements to some scrub lichens.Recently burned habitats offer insufficient food and cover, and intermediate-aged habitats are preferred, whereas scrub that is decades old act as a population sink (WOOLFENDEN and FITZPATRICK 1984, FITZPATRICK et al. 1994). Land managers should therefore strive to promote relatively frequent patchy fires to allow the development and maintenance of a mosaic of times-since-fire (and therefore fuels), which includes both open low-fuel habitats where lichens can survive fires unburned and recently burned sites that are near unburned source populations. Implementing prescribed fire in this way probably mimics natural fire and promotes a mosaic of times-since-fire sites. Developing such mosaics is recommended to maintain the diversity of scrub species including, besides lichens, herbs, shrubs, and animals (MENGES 1999).

Acknowledgements This project was funded by cooperative agreement #1448-0004096-9199 from the U.S. Fish and Wildlife Service. I thank Eric Menges, Pedro Quintana-Ascencio, and Alan Herndon for valuable discussion and advice regarding project design. Rick Lavoy, Carl Weekley, and Karin Kettenring assisted with data collection. Carl Weekley and Roberta Pickert provided invaluable help with GIS software and analyses and Richard Miller provided much insight into statistical analyses. William Louis Culberson, Paula T. DePriest, Terry Henkel, Janneke HilRisLambers and an anonymous reviewer much improved earlier drafts of this manuscript. 354 Rebecca Yahr

6 References

Abrahamson, W.G.; Johnson, A.F.; Layne, J.N.; Peroni, P.A., 1984: Vegetation of the Archbold Biological Station, Florida:An example of the southern Lake Wales Ridge. Fla. Sci. 47:209–250. AHTI,T., 1959:Studies on the caribou lichens stands of Newfoundland.Annales Botanici Societatis Vanamo 30, 4: 1–44. AHTI, T., 2000: Cladoniaceae. Flora Neotropica Monograph 78. New York, Bronx, Botanical Garden. ANTOS,J.A.;MCCUNE,B.;BARA,C.,1983:The effect of fire on an ungrazed western Montana grass- land. Am. Midl. Nat. 110: 354–364. BUCKLEY,A.;HENDRICKSON, T.O., 1986: An update of the Macrolichens of Archbold Biological Station with emphasis on the status of Cladonia perforata Evans. Lake Placid, FL, Archbold Biological Station. CHRISTENSEN, N.L., 1985: Shrubland Fire Regimes and Their Evolutionary Consequences. In: PICKETT, S.T.A.; WHITE, P.S. (eds) Natural Disturbance and Patch Dynamics. Orlando, Academic Press. 86–100. CHRISTMAN, S.P.; Judd, W.S., 1990: Notes on plants endemic to Florida scrub. Fla. Sci. 53: 52–73. Deyrup, M., 1989:Arthropods endemic to the Florida scrub. Fla. Scientist 52: 254–270. DEYRUP,M.;FRANZ, R., 1994:Rare and endangered biota of Florida IV.Invertebrates. Gainesville, University Press of Florida. DOBSON, A.P.; RODRIGUEZ, J.P.; ROBERTS, W.M.; WILCOX, D.S., 1997: Geographic distribution of endangered species in the United States. Science 275: 550–553. EVANS, A., 1952:The Cladoniae of Florida. Transactions of the Connecticut Academy of Arts and Sciences 38: 249–336. FITZPATRICK, J.W.; WOOLFENDEN, G.E.; CURRY, R.L., 1994: Fire and conservation biology of Florida scrub jays. J. Ornithol. 135: 493. HAWKES, C.V.;MENGES, E.S., 1995:Density and seed production of a Florida endemic, Polygonella basiramia, in relation to time since fire and open sand. Am. Midl. Nat. 133: 138–148. HAWKES, C.V.; MENGES, E.S., 1996:The relationship between open space and fire for species in a xeric Florida shrubland. Bulletin of the Torrey Botanical Club 123, 2: 81–92. JOHANSEN, J.R.; St. CLAIR, L.L.; WEBB, B.L.; NEBEKER, G.T., 1984: Recovery patterns of cryp- togamic soil crusts in desert rangelands following fire disturbance. Bryologist 87: 238–243. JOHNSON,A.F.,1982:Some demographic characteristics of the Florida rosemary Ceratiola ericoides Michx. Am. Midl. Nat. 108, 1: 170–174. JOHNSON, A.F.; ABRAHAMSON, W.G., 1990: A note on the fire responses of species in rosemary scrubs on the southern Lake Wales Ridge. Fla. Sci. 53: 138–143. KLEIN, D.R., 1982: Fire, lichens, and caribou. J. Range Manage. 35: 390–395. MAIKAWA,E.;KERSHAW, K.A., 1976; Studies on lichen-dominated systems. XIX. The postfire recovery sequences of black spruce – lichen woodland in the Abitau Lake Region, N.W.T. Can. J. Bot. 54: 2679–2687. MAIN, K.N.; MENGES, E.S., 1997: Station Fire Management Plan. Lake Placid, FL, Archbold Biological Station. MENGES,E.S.,1999:Florida scrub.In:ANDERSON,R.C.;FRALISH,J.S.;BASKIN,J.M.(eds) Savannas, barrens, and rock outcrop plant communities of North America. Cambridge, University Press. MENGES, E.S.;HAWKES, C.V., 1998:Interactive effects of fire and microhabitat on plants of Florida scrub. Ecol. Appl. 8, 4: 935–946. MENGES, E.S.; KIMMICH, J., 1996: Microhabitat and time since fire: Effects on demography of Eryngium cuneifolium (Apiaceae), a Florida scrub endemic plant. Am. J. Bot. 83, 2: 185–191. MENGES, E.S.;KOHFELDT, N., 1995:Life history strategies of Florida scrub plants in relation to fire. Bulletin of the Torrey Botanical Club 122, 4: 282–297. MISTRY, J., 1998: Corticolous lichens as potential bionindicators of fire history: a study in the cerrado of the Distrito Federal, central Brazil. J. Biogeogr. 25: 409–441. MORNEAU,C.;PAYETTE, S., 1989: Postfire lichen-spruce woodland recovery at the limit of the boreal forest in northern Quebec. Can. J. Bot. 67: 2770–2782. For. Snow Landsc. Res. 75, 3 (2000) 355

MYERS, R.L., 1990: Scrub and high pine. In: MYERS, R.L.; EWEL, J.J. (eds) Ecosystems of Florida. Gainesville, University of Central Florida Press. 150–193. PICKETT, S.T.A.; WHITE, P.S., 1985: Natural Disturbance and Patch Dynamics:An introduction. In: PICKETT, S.T.A.; WHITE, P.S. (eds) Natural Disturbance and Patch Dynamics. Orlando, Academic Press. 3–12. QUINTANA-ASCENCIO,P.F.;DOLAN,R.W.;MENGES,E.S.,1998:Hypericum cumulicola demography in unoccupied and occupied Florida scrub patches with different times since fire. J. Ecol. 86, 4: 640–651. QUINTANA-ASCENSIO, P.F.; MORALES-HERNANDEZ, M., 1997: Fire-mediated effects of shrubs, lichens, and herbs on the demography of Hypericum cumulicola in patchy Florida scrub. Oecologia 112: 263–271. QUINTILIO,D.;FAHERNSTOCK, G.R.; DUBE, D.E., 1977: Fire behavior in upland jack pine: the Darwin lake project. Information report NOR-x-174. Edmonton, AB. Forestry Service, Fisheries and Environment Canada, Northern Forest Research Centre. 49 pp. SCHULTEN, J., 1985:The effects of burning on the soil lichen community of a sand prairie. Bryologist 88, 2: 110–114. U.S. Fish and Wildlife Service (USFWS), 1989: Endangered and threatened wildlife and plants; notice of finding on a petition to list: Cladonia perforata (Perforate Reindeer Lichen). Federal Register 54, 200: 42813. TOPHAM, P.B., 1977: Colonization, growth, succession and competition. In: SEAWARD, M. (ed) Lichen Ecology. New York, Academic Press. 293–320. WHELAN, R.J., 1995:The ecology of fire. Cambridge, University Press. WHITE, P.S., 1979: Pattern, process and natural disturbance in vegetation. Bot. Rev. 45: 229–299. WOOLFENDEN,G.E.;FITZPATRICK,J.W.,1984:The Florida Scrub-Jay:demography of a cooperative- breeding bird. Monographs in population biology No. 20, Princeton, New Jersey, University Press. WUNDERLIN, R.P., 1998: Guide to the vascular plants of Florida. Gainesville, Florida, University Press of Florida. 809 pp. YOUNG, C.C.; MENGES, E.S., 1999: Postfire gap-phase regeneration in scrubby flatwoods on the Lake Wales Ridge. Fla. Sci. 62: 1–12.

Appendix A.

Spearman’s rho correlation coefficients for terrestrial lichen species, vascular plants, litter and burn intensity (positive coefficients with burn intensity indicate that lichen frequency is correlated with quadrats within completely burned sampling grid cells).

Cladonia Cladonia Cladonia Cladonia Cladonia Cladonia Cladonia evansii leporina pachycla- perforata prostrata subsetacea subtenuis (cover) (cover) dodes (cover) (cover) (cover) (cover) (cover)

Cladonia leporina 0.3603 (cover) Sig .000

Cladonia 0.2707 0.4884 pachycladodes Sig .000 Sig .000 (cover)

Cladonia perforata 0.198 0.3336 0.2588 (cover) Sig .000 Sig .000 Sig .000

Cladonia prostrata 0.4158 0.4987 0.3536 0.335 (cover) Sig .000 Sig .000 Sig .000 Sig .000 356 Rebecca Yahr

Appendix A continued.

Cladonia Cladonia Cladonia Cladonia Cladonia Cladonia Cladonia evansii leporina pachycla- perforata prostrata subsetacea subtenuis (cover) (cover) dodes (cover) (cover) (cover) (cover) (cover)

Cladonia subsetacea 0.204 0.4285 0.3989 0.3031 0.3232 (cover) Sig .000 Sig .000 Sig .000 Sig .000 Sig .000

Cladonia subtenuis 0.2256 0.2063 0.1478 0.1341 0.2417 0.0852 (cover) Sig .000 Sig .000 Sig .000 Sig .000 Sig .000 Sig .001

A ristida gyrans –0.0061 0.0153 0.0365 0.051 0.0047 0.0541 –0.0368 (frequency) Sig .807 Sig .538 Sig .142 Sig .040 Sig .851 Sig .029 Sig .139

Ceratiola ericoides 0.0274 0.0446 0.0186 –0.027 0.0732 0.0448 0.0401 (frequency) Sig .270 Sig .073 Sig .454 Sig .278 Sig .003 Sig .071 Sig .106

L icania michauxii 0.0264 0.0299 –0.0221 0.0321 0.0498 –0.0002 –0.0559 (frequency) Sig .288 Sig .228 Sig .373 Sig .196 Sig .045 Sig .992 Sig .024

Paronychia –0.0272 0.0504 0.0537 0.0262 –0.0026 0.0098 –0.0197 chartacea Sig .273 Sig .042 Sig .031 Sig .292 Sig .917 Sig .694 Sig .429 (frequency)

Polygonella –0.0786 0.0305 0.143 0.013 –0.0417 0.0775 0.0001 basiramia Sig .002 Sig .220 Sig .000 Sig .602 Sig .093 Sig .002 Sig .998 (frequency)

Quercus chapmanii –0.0525 –0.0994 –0.0925 –0.0388 –0.0612 –0.081 –0.0375 (frequency) Sig .035 Sig .000 Sig .000 Sig .119 Sig .014 Sig .001 Sig .132

Quercus geminata –0.0529 –0.0513 –0.0673 –0.0504 –0.0839 –0.0655 –0.0201 (frequency) Sig .033 Sig .039 Sig .007 Sig .043 Sig .001 Sig .008 Sig .419

Quercus inopina –0.0108 –0.2132 –0.1791 –0.1289 –0.1546 –0.1658 –0.0669 (frequency) Sig .663 Sig .000 Sig .000 Sig .000 Sig .000 Sig .000 Sig .007

Selaginella arenicola 0.066 0.1469 0.1169 0.0215 0.0411 0.0696 0.0367 (frequency) Sig .008 Sig .000 Sig .000 Sig .387 Sig .098 Sig .005 Sig .140

Serenoa repens –0.0659 –0.0299 –0.0348 –0.0608 –0.0567 –0.0363 –0.0433 (frequency) Sig .008 Sig .229 Sig .162 Sig .014 Sig .022 Sig .144 Sig .081

Burn Class –0.2044 –0.12 –0.0815 –0.0738 –0.2056 –0.0952 –0.0534 Sig .000 Sig .000 Sig .001 Sig .003 Sig .000 Sig .000 Sig .031

Oak litter 0.0133 –0.1683 –0.1634 –0.1026 –0.1429 –0.1632 –0.0697 Sig .593 Sig .000 Sig .000 Sig .000 Sig .000 Sig .000 Sig .005

Rosemary litter 0.1758 0.148 0.1091 0.0215 0.2236 0.0803 0.1518 Sig .000 Sig .000 Sig .000 Sig .387 Sig .000 Sig .001 Sig .000