BIOTROPICA 44(1): 10–18 2012 10.1111/j.1744-7429.2011.00771.x

Disturbance Type and Successional Communities in Bahamian Dry Forests

Claire C. Larkin1, Charles Kwit1,2,6, Joseph M. Wunderle Jr.3, Eileen H. Helmer3, M. Henry H. Stevens1, Montara T. K. Roberts4, and David N. Ewert5

1 Department of Botany, Miami University, Oxford, Ohio 45056, U.S.A. 2 Department of Biology, Wittenberg University, Springfield, Ohio 45501, U.S.A. 3 International Institute of Tropical Forestry, USDA Forest Service, Sabana Field Research Station, HC 02 Box 6205, Luquillo, Puerto Rico 00773, U.S.A. 4 Department of Fisheries, Wildlife and Conservation Biology, University of Minnesota, St. Paul, Minnesota 55108, U.S.A. 5 The Nature Conservancy, 101 East Grand River, Lansing, Michigan 48906, U.S.A.

ABSTRACT Different disturbances in similar habitats can produce unique successional assemblages of . We collected plant species composition and cover data to investigate the effects of three common types of disturbances—fire, anthropogenic clearing (‘cleared’), and clearing followed by goat grazing (‘cleared‐and‐grazed’)—on early‐successional coppice (dry forest) community structure and development on Eleuthera, Bahamas. For each disturbance type, both the ground layer ( < 0.5 m height) and shrub layer ( > 0.5 m height) were sam- pled in eight patches ( > 1 ha) of varying age (1–28 yr) since large‐scale mature coppice disturbance. Overall, plant communities dif- fered among disturbance types; several common species had significantly higher cover in the shrub layer of fire patches, and cleared‐ and‐grazed patches exhibited higher woody ground cover. Total percent cover in the shrub layer increased in a similar linear fashion along the investigated chronosequence of each disturbance type; however, cover of the common tree species, Bursera simaruba, increased at a notably slower rate in cleared‐and‐grazed patches. The pattern of increase and subsequent decrease in cover of spp. and Zanthoxylum fagara in the shrub layer was characterized by longer persistence and higher covers, respectively, in cleared‐and‐grazed patches, which also exhibited low peak cover and fast decline of nonwoody ground cover. Our results suggest that goats may accelerate some aspects of succession (e.g., quickly removing nonwoody ground cover) and retard other aspects (e.g., inhibiting growth of tree spe- cies and maintaining early‐successional shrubs in the shrub layer). These effects may lead to different successional trajectories, and have important conservation implications.

Key words: Bahamas; coppice; dry evergreen forest; fire; goat grazing; Kirtland's Warbler; succession.

DIFFERENT DISTURBANCES IN SIMILAR HABITATS can produce unique cern. Regeneration of tropical and subtropical plant communities successional assemblages of plants. This may be explained by the following fire will depend on fire tolerance and resprouting abili- different selective filters that various disturbances impart on the ties of plants directly affected by fire, plants escaping the poten- plants that are directly affected. For example, anthropogenic tially patchy nature of fire in such systems (see Kellman & clearing and fire, two large‐scale disturbances within tropical for- Tackaberry 1993), local seed inputs, and immigration via wind ests, would be expected to result in different plant communities and animal seed dispersal. A general increase in species diversity and successional trajectories through time. Clearing for agriculture over time has been documented in some instances following and pasture, which is often followed quickly by abandonment, is clearing (Chazdon et al. 2007), and fire (Uhl et al. 1981), though arguably the most common large‐scale disturbance in Neotropical the composition of early‐successional plant communities in such forests (Chazdon et al. 2007) and involves the near complete settings should differ. removal of vegetation. Regeneration of tropical and subtropical Managed grazing of anthropogenically cleared lands can also plant communities following abandonment depends on root res- affect successional trajectories and resultant plant communities in prouting abilities, release from soil seed banks, and immigration. tropical and subtropical forest systems. After an initial clearing Fire tends to be a disturbance of low intensity in tropical and event, grazers reduce recovery of species‐richness and diversity of subtropical systems (compared with its effects elsewhere; Giglio natural vegetation in tropical dry forest (Stern et al. 2002). Grazers et al. 2006); though prospects of its increasing frequency due to also affect structural attributes of early‐successional plant commu- deforestation, fragmentation, and climate change (Cochrane et al. nities by increasing numbers of small stems and preventing the 1999; Cochrane 2001, 2003) make it a disturbance of high con- growth and development of larger stems (Stern et al. 2002); both of these effects can be interpreted as retarding forest succession. Received 10 May 2010; revision accepted 16 January 2011. When grasses and nonwoody vegetation dominate cleared land- 6Corresponding author; e‐mail: [email protected] scapes, however, grazers at low stocking densities can accelerate 10 ª 2011 The Author(s) Journal compilation ª 2011 by The Association for Tropical Biology and Conservation Disturbance and Dry Forest Succession 11

the establishment and cover of woody/shrubby vegetation (Posada temporal differences in (A) subsets of species or species groups et al. 2000). Because land use history, including grazing, is a major and (B) total cover (%) of vegetation as a function of disturbance driver of developing plant communities in tropical forests (see type. Specifically, here, we were concerned with recovery of pri- Aide et al. 1996), inclusion of data on the effects that grazers may mary tree species such as Bursera simaruba (L.) Sarg. (Burseraceae) have on vegetation dynamics following an initial clearing, rather and Coccoloba diversifolia Jacq. (Polygonaceae) following different than solely after the removal of grazing, is necessary to strengthen disturbances. We also expected species with mechanical defenses our understanding of succession in these systems. or low palatability to goats (i.e., less preferred browse; see Relva In this study, we collected plant species composition data to & Veblen 1998), such as Zanthoxylum fagara (L.) Sarg. (Rutaceae) investigate the effects of three different types of disturbances— and Lantana spp. (), to perform better in cleared‐and‐ fire, clearing (i.e., bulldozing), and clearing followed by goat graz- grazed patches. We intend our findings to contribute to a better ing—on the vegetation composition and structure of resultant conceptual understanding of three common disturbances in terms early‐successional coppice (also known as ‘dry evergreen forest’; of their successional outcomes. see Smith & Vankat 1992) communities ( > 1 ha) on Eleuthera, the Bahamas. Coppice, a term used to describe dry broadleaf (as METHODS opposed to pine) forested communities with low to high canopy height (2–12 m) throughout the Bahamian archipelago (see Smith STUDY SITE.—Fieldwork for the study was conducted on the & Vankat 1992), is found at various stages of development on Ba- southern end of Eleuthera, the Bahamas (Fig. S1). Eleuthera (26 hamian islands, and makes up a substantial portion of the vegeta- 060 N, 76080 W) is a low elevation (63 m maximum elevation) tion on large islands and cays of the archipelago's central and island located in the middle of the Bahamian Archipelago and southern portions (Correll & Correll 1982). Fire and clearing via has a climate consisting of an annual wet and dry season, with bulldozing are common in the Bahamas (see Smith & Vankat most of its mean annual rainfall (1090 mm/yr) occurring from 1992), and goat farming is practiced on a number of the Com- May through October (Campbell 1978, Sealey 2006). Vegetation monwealth's islands. Although information on contemporary rates on the island is dominated by coppice scrub. Coppice plant of such disturbances in the Bahamas is lacking, it has been argued communities include primarily evergreen and semi‐deciduous that anthropogenic disturbance has led to the loss of coppice plant broadleaf trees and shrubs, which form thick brush or dense veg- species (Correll & Correll 1982), and that disturbance‐related pres- etation on poorly developed soils on limestone substrate (Correll sures on coppice communities will invariably increase in the future, 1979, Byrne 1980, Sealey 2006). The most common plant fami- with the potential for further loss of plant species, even at local lies include Leguminosae, Gramineae, Asteraceae, Euphorbiaceae, (within island) scales (Smith & Vankat 1992). Identifying different and Cyperaceae (Vincent & Kwit 2007). vegetation patterns in coppice habitats recently impacted by different Early‐successional habitat patches ( > 1 ha) matching disturbances may assist conservation efforts aimed at main- descriptions of having been (1) cleared for agriculture or intended taining the diversity of the plant community. In addition, early‐ development (hereafter, ‘cleared’ patches); (2) cleared and subse- successional coppice habitats have been identified as important to quently subjected to managed grazing by goats (hereafter, resident and Neotropical migratory birds (Currie et al. 2005), includ- ‘cleared‐and‐grazed’ patches); and (3) created exclusively by fire ing the Kirtland's Warbler, which winters in early‐successional (hereafter, ‘fire’ patches), were initially identified using remote habitats exclusively in the Bahamian archipelago and consumes sensing‐based maps of forest disturbance type and age since fruits of early‐successional coppice species (Wunderle et al. 2010). large‐scale disturbance in mature coppice (Helmer et al. 2010). Therefore, identifying which disturbance types best promote The maps came from simultaneously classifying forest distur- desired habitats may be beneficial to bird conservation. bance type and age with a time series of cloud‐cleared image We test several hypotheses regarding the general and tempo- mosaics extending from 1984 to 2005. The image mosaic for ral effects of fire, clearing, and clearing with subsequent managed each time step was composed of the clear parts of Landsat and goat grazing on several plant community metrics in a chronose- Advance Land Imager data and was created with regression tree quence context. Although the mechanisms underlying vegetation normalization. Vegetations resulting from the various disturbance dynamics cannot be identified in chronosequence studies (see types and the various years of disturbance have unique spectral Chazdon et al. 2007), these studies provide a means of identifying signatures over time, making their distinction possible when the general patterns of successional vegetation dynamics following image bands from all dates in a time series are used when devel- disturbance and can help generate hypotheses of underlying oping maps from the satellite imagery. Vegetation recovering mechanisms, which could later be tested using long‐term perma- from disturbance in 1 yr, for example, has a different spectral‐ nent plots (see Bakker et al. 1996). In addition, metrics related to temporal signature from vegetation disturbed during some other ‘cover’, which is of interest in our study, have shown consistent year, with spectral indices indicative of green vegetation and can- linear patterns in successional chronosequences and long‐term opy structure dropping sharply at time of disturbance and gradu- permanent‐plot studies (Chazdon et al. 2007). We predicted that ally increasing afterwards. Time since disturbance, therefore, is there would be general differences in coppice plant communities detectable and defined in this manner. In addition, the different as a function of disturbance type due to species‐specific disturbance types differ spectrally, both initially and in the pattern responses to different disturbances. We also predicted there to be of spectral changes over time. Return to pre‐disturbance spectral 12 Larkin et al.

signatures, for example, takes 8 yr for escaped fire but up to TABLE 1. General information on 24 study sites (i.e., patch) sampled for species 14 yr for land cleared by bulldozing at our study site. Validation composition data on Eleuthera, the Bahamas. Each patch has been of disturbance types with mature coppice disturbance occurring disturbed by clearing (i.e., bulldozing), clearing followed by subsequent goat from 1996 onward was accomplished by field verification; for grazing, or fire. disturbances before 1996, disturbance type was validated with visual interpretation of single image dates. Other chronosequence Elevation Size Patch age Line intercept studies in tropical forests have also used time series of aerial pho- Patch Disturbance (m) (ha) (yr) length (m) tos or satellite images in choosing sites (e.g., Aide et al. 1996, Ruiz et al. 2005), and in our case, the resultant maps have been useful 1 Cleared 2.4 1 2 50 in other studies on southern Eleuthera (Wunderle et al. 2010). 2 Cleared 4.5 2.61 6 100 Cleared patches were typically bulldozed and subsequently aban- 3 Cleared 1.72 1.35 7.5 50 doned or left alone. Patches of coppice on Eleuthera are cleared 4 Cleared 1.32 1 4 50 for two reasons: (1) proof of land utilization (e.g., clearing to exhi- 5 Cleared 5.38 2.79 10 100 bit, at a minimum, intention of agriculture, especially on commu- 6 Cleared 9.28 4.23 10 100 nity‐held land) and (2) development, the latter of which often 7 Cleared 4.02 6.6 7.5 150 does not materialize. Cleared‐and‐grazed patches were typically 8 Cleared 3.1 4 21 100 ‐ ‐ bulldozed and subsequently grazed intermittently by goats for up 9 Cleared and 0.06 7.29 10 150 to several years. Fire patches were the result of escaped fires of grazed ‐ ‐ natural or anthropogenic origin. Large‐scale ‘gaps’ during the 10 Cleared and 1.14 5 10 100 timeframe of interest were not created by tropical cyclones, grazed ‐ ‐ although Hurricane Floyd, which impacted Eleuthera in Septem- 11 Cleared and 3.98 16.83 2 150 ber 1999, may have contributed to increased fuels, and thus grazed ‐ ‐ improved fire spread, as well as the ability to detect burned areas 12 Cleared and 0.08 1 6 50 remotely (Helmer et al. 2010). A total of eight patches of each grazed ‐ ‐ type of disturbance were selected in a stratified random fashion. 13 Cleared and 0.1 5.5 4 100 Sampled patches ranged in size and age from 1 to 23 ha and 1 grazed ‐ ‐ to 28 yr since onset of disturbance (Table 1), and were not 14 Cleared and 1.86 1 1 50 subject to subsequent large‐scale disturbances. grazed 15 Cleared‐and‐ 4.42 1 28 50 grazed VEGETATION SAMPLING.—The line‐intercept method (Canfield ‐ ‐ 1941) was used to sample vegetation in each patch. Vegetation 16 Cleared and 0.96 5 15 90 was sampled in May and June of 2008 and 2009, periods that grazed encompassed the beginning of the rainy season in the Bahamian 17 Fire 3.6 3.4 5 50 archipelago. A total of 50–150 m was sampled in each patch 18 Fire 2.3 5 5 100 depending on the size of the patch; patches <2 ha had 50 m 19 Fire 5.9 2.97 6.5 100 sampled, patches between 2 and 6 ha had 100 m sampled, and 20 Fire 4.6 600 8.5 150 patches > 6 ha had 150 m sampled. Both the ground layer 21 Fire 4.2 4.5 10 100 ( < 0.5 m height) and the shrub/tree layer ( > 0.5 m height; 22 Fire 8.4 13.84 23 100 hereafter ‘shrub layer’) were sampled simultaneously along the 23 Fire 5.3 5 5 90 same line. When possible, one line, originating > 10 m from a 24 Fire 13.4 6 7 100 patch edge at a random location along the patch perimeter and proceeding in a random direction toward the patch center, was used for vegetation sampling. Because of certain barriers such as cases, the 95% confidence interval of the sample‐based rarefac- thick brush and karst sinkholes, one continuous line was not tion estimate at the end of the line intercept overlapped with the always used to sample each patch, and sometimes several lines 95% confidence interval of the Chao 2 species‐richness estimator were needed to sample a patch. All shrubs, trees, and herbs for the sampled patch. Vegetation < 0.5 m height (hereafter, the (excluding vines) intersecting the line at a height > 0.5 m (hereaf- ‘ground layer’) was categorized as woody or nonwoody (i.e., no ter, ‘shrub layer’) were identified to species or genus, and hori- species‐level data were collected for the ground layer) due to lack zontal linear measurements (cm) of plant intercepts along the of floral structures necessary to distinguish among species (espe- course of the transect were recorded. The sampling regime used cially nonwoody species) at the time of sampling, and linear mea- sufficiently captured the a richness of each patch; this was deter- surements of these two categories were taken in the same mined by producing sample‐based rarefaction curves for each manner as described for species in the shrub layer. Linear mea- patch (using EstimateS software; Colwell 2006) by splitting the sures were converted to percent cover and relative cover (i.e., per- ‘transect’ (line intercept) into 10 m segments and counting the cent of total plant cover) in each patch. Measures of cover number of ‘hits’ for each species along the 10‐m segment. In all reflected the canopy ‘influence’ and hence may have included Disturbance and Dry Forest Succession 13

minute breaks in cover (see Bonham 1989). Nomenclature of where s is species‐richness, and pi is the relative cover of the ith plant species followed Correll and Correll (1982), and voucher species (e.g., Whittaker 1960, Bazzaz 1975, Ikeda 2003). specimens were collected and deposited in the Bahamas National Herbarium in the Nassau Botanical Garden. ANALYSES: CHRONOSEQUENCE TRENDS.—Successional trends among the three disturbances were investigated for the following vari- ANALYSES: PLANT COMMUNITIES AND SPECIES AS A FUNCTION OF ables obtained in each patch's shrub layer: total plant cover, cover DISTURBANCE.—Nonmetric multidimensional scaling (NMDS) was of the two primary tree species, and cover of two species of used to construct ordinations depicting distances among sampled ephemeral and unpalatable shrub species (i.e., species which con- patches as a function of species percent covers (shrub layer), tain significant secondary compounds or mechanical defenses). which were transformed (Wisconsin standardization) to reduce Total plant cover was calculated as the sum of percent covers of undue emphasis on the most common species and to adjust for all species sampled in a patch. Primary tree species with sufficient differences in total vegetation cover among sites. More specifically, cover data to address separately included B. simaruba and C. diver- each species entry (i.e., each value in a column in a site x species sifolia. Ephemeral and unpalatable shrub species with sufficient matrix) was divided by its own maximum value. For each site (i.e., cover data included Lantana spp. (summed covers of Lantana each row in the site x species matrix), the resultant species entries bahamensis Britt. (Verbenaceae), Lantana involucrata L., and Lantana were divided by their resultant total for that site. The Bray–Curtis demutata Millsp., all of which are native to the study area), which distance measure was used because it is known to be consistently is known to contain secondary compounds harmful to ruminant interpretable across very long gradients (McCune & Grace 2002). grazers (Sharma et al. 2007), and Z. fagara, which is the most This approach allowed the visualization of general differences in abundant thorny shrub in our study system. plant community composition, in the shrub layer, among the three For total plant cover and primary tree species cover through disturbance types (see McCune & Grace 2002). The fewest num- time (years since large‐scale mature coppice disturbance; hereaf- ber of axes that would adequately represent the data in the NMDS ter, ‘age’), our goal was to test whether the linear rate of increase ordination was determined by using stress values (McCune & (i.e., slope) in percent cover differed among disturbance catego- Grace 2002). Stress values showed that two dimensions was the ries. A no‐intercept analysis of covariance (ANCOVA) approach lowest number of axes that would adequately represent our shrub was used for total plant cover and for B. simaruba cover. For layer data in the NMDS plots (one axis 30, two axes 15.56, C. diversifolia, we used a full ANCOVA (intercept included) three axes 10.22, four axes 7.19, five axes 5.55). Adding a approach due to the presence of significant intercept and inter- third dimension did not provide additional insight and did not cept adjustment terms, and the simultaneous alteration of the substantially alter NMDS plots. All NMDS analyses included inference regarding the slope adjustment term. In each case, an multiple random initializations to help reduce the possibility that F‐test for the inclusion of a slope adjustment term was used to the numerical optimization procedures were not trapped far from test for different linear chronosequence patterns among the three global optima. In addition, the Bray–Curtis distances were utilized disturbance types (MIXED procedure, SAS Institute Inc. 2008). in a permutational multivariate analysis of variance (MANOVA) For ephemeral and nonpalatable species in the shrub layer, (Excoffier et al. 1992, McArdle & Anderson 2001). In general, this as well as for woody and nonwoody cover in the ground layer, a method partitions multivariate variation among independent vari- nonlinear approach was used to test for different patterns of ables, and here tests for differences in plant communities (based cover increase and subsequent decline among the different distur- on species and their associated covers in each patch) as a function bance types. More specifically, full and reduced Ricker models of of disturbance type. All multivariate analyses were accomplished the general form using the vegan package (Oksanen et al. 2010) in the R language and environment (R Development Core Team 2010). y ¼ axe ba; To compare percent cover of individual species in the shrub layer among the three different patch types, single‐factor analysis where y is the percent cover, x is the age, and a and b are maxi- of variance (ANOVA) was conducted on all species found in mum‐likelihood‐estimated parameters, were used. Full models more than 50 percent of the patches (i.e., >12 patches). Tukey’s contained separate parameter estimates for a and b for each dis- pairwise comparisons were calculated for species with P‐values turbance, and an F‐test was used to test whether these parame- that were statistically significant (P<0.05). Shapiro–Wilks test of ters differed among the different disturbances. When this Normality and Levene's test of homogeneity were used to test occurred, we interpreted this as evidence for different succes- for normality and homogeneity of variance, respectively. sional trajectories. This nonlinear modeling approach is practical Tests for differences in a diversity among different distur- here, where ephemeral and nonpalatable species ‘enter’ the bance types were accomplished by ANOVA. We calculated Shan- patches after clearing, generally increase in cover, and then non–Weiner diversity indices (H0) for each patch using the decline to zero (or near zero) by the end of the chronosequence. following equation: In addition, the Ricker model can be used to estimate the peak XS of percent cover and the time (yr) at which this occurs. These 0 H ¼ pi ln pi ; analyses were performed using the NLIN procedure and the i¼1 SSReductionTest macro in SAS (SAS Institute Inc. 2008). 14 Larkin et al.

RESULTS 1.0 CG CG CG F GENERAL FINDINGS.—A total of 74 species in the shrub layer fi fi 0.5 ( > 0.5 m) were identi ed (Table S1). Both re and cleared patches F had a mean species‐richness of 23 species, while cleared‐and‐grazed F CG C ‐ C patches had a mean species richness of 19 species. Of the 74 spe- F 0.0 CG F F cies, most were woody, and 18 species were found in at least 50 C F F percent of the patches (i.e., 12 patches). These species included C C C Acacia choriophylla Benth. (Leguminosae), Bourreria ovata Miers NMDS2 C −0.5 (Boraginaceae), Bumelia salicifolia (L.) Sw. (Sapotaceae), B. simaruba, C Chiococca alba (L.) Hitchc. (Rubiaceae), C. diversifolia, Erithalis fruiticosa CG L. (Rubiaceae), Eugenia axillaris (Sw.) Willd. (Myrtaceae), Guapira dis- −1.0 CG color (Spreng.) Little (Nyctaginaceae), Guapira obtusata (Jacq.) Little CG (Nyctaginaceae), Lantana spp. Leucaena leucocephala (Lam.) de Wit

(Leguminosae), Metopium toxiferum (L.) Krug & Urb. (Anacardia- −1.5 −1.0 −0.5 0.0 0.5 1.0 ceae), Pithecellobium keyense Britt. (Leguminosae), Psychotria ligustrifolia NMDS1 (Northrop) Millsp. (Rubiaceae), Randia aculeata L. (Rubiaceae), Tabebuia bahamensis (Northrop) Britt. (Bignoniaceae), and Z. fagara. FIGURE 1. Ordination derived from nonmetric multidimensional scaling Six of the 18 species found in the shrub layer in more than 50 comparing percent cover of shrub layer (>0.5 m) species in early‐successional percent of the patches had significantly different mean percent cover coppice patches on Eleuthera, the Bahamas. Plots (patches) are labeled by among patches with differing disturbances. Three of these species, their disturbance, which include cleared (C), cleared‐and‐grazed (CG), and fire fi A. choriophylla (F2, 21 =6.99,P < 0.01), B. simaruba (F2, 21 =8.06, (F). Polygons represent range of data and ellipses represent 95% con dence P < 0.001), and C. diversifolia (F2, 21 =6.12,P < 0.01), contributed, intervals drawn around the data centroids. on average, a substantial portion of the total cover in patches (mean percent covers of 6.9, 7.8, and 11.1, respectively, across all patches). rate slope parameters for each disturbance was not significant for

For these species, higher cover (at least twice as much) was found C. diversifolia (F2, 18 = 1.32, P = 0.29), suggesting increase in per- in fire patches than in cleared and cleared‐and‐grazed patches (Fig. cent cover through the chronosequence for C. diversifolia occurs at S2). The other three species, B. salicifolia (F2, 21 =4.07,P < 0.05), the same rate among the three disturbance types (Fig. 2B). E. axillaris (F2, 21 =9.91, P < 0.001), and P. ligustrifolia Increase in percent cover through the chronosequence for fi (F2, 21 =5.28,P < 0.05), though exhibiting signi cant differences B. simaruba was affected by disturbance type (F2, 21 = 18.52, in cover among patches with different disturbance types, contrib- P < 0.0001; Fig. 2C). Percent cover increased quickest in fire uted on average < 5 percent cover within patches. plots, followed by cleared and cleared‐and‐grazed, respectively. Shrub layer vegetation (based on species composition and their Bursera simaruba had a negligible increase in cover in cleared‐and‐ percent cover) differed as a function of disturbance type. Our grazed plots across our chronosequence (Fig. 2C). NMDS ordination showed separation in shrub layer communities, Certain species and species groups exhibited an initial particularly between fire patches vs. cleared and cleared‐and‐grazed increase in shrub layer cover, followed by a decline through the patches (Fig. 1). Permutational MANOVA indicated that disturbance chronosequence. This general nonlinear pattern differed among type explained approximately 23 percent of the among‐patch varia- patches with different disturbance types for Lantana spp. tion in plant community composition (F2, 21 =3.12, P < 0.001), (F4, 18 = 6.38, P < 0.01) and Z. fagara (F4, 18 = 6.91, P < 0.01). and pairwise comparisons indicated unique plant communities for Lantana spp. cover increased rapidly in cleared patches early in the each disturbance (P < 0.05 for each pairwise comparison). chronosequence reaching peak estimated cover ( 30%) 3 yr after Shannon–Weiner a diversity indices differed significantly clearing, followed by a sharp decline through the chronosequence among the three disturbance types (F2, 21 = 5.10, P < 0.05; Fig. (Fig. 3A). Although Lantana spp. cover was not estimated to be as S3). Cleared‐and‐grazed patches had a lower mean Shannon–Wei- high in cleared‐and‐grazed patches compared with cleared patches 0 ner diversity index (H = 1.91) compared with cleared initially after disturbance, the Ricker model depicted Lantana spp. 0 0 (H = 2.33) and fire patches (H = 2.40). being maintained longer through the chronosequence in clear‐and‐ grazed patches compared with cleared patches (Fig. 3A). Zanthoxy- CHRONOSEQUENCE TRENDS.—Total percent cover in the shrub lum fagara exhibited highest estimated cover in cleared‐and‐grazed layer linearly increased across the investigated chronosequence patches reaching peak cover ( 25%) 7 yr following disturbance, (Fig. 2A). The rate of increase, which was positive and differed and then subsequently declined. Zanthoxylum fagara was estimated significantly from zero (F1, 21 = 78.54, P < 0.001), was similar to increase in fire and cleared patches reaching 10 percent cover across all disturbance types (F2, 21 = 2.48, P = 0.11). > 20 yr after disturbance (Fig. 3B). For C. diversifolia, fire patches had the highest initial C. diversifo- In the ground layer, the cover of woody and nonwoody spe- lia cover at time zero (Fig. 2B). The test for the inclusion of sepa- cies exhibited an initial increase, followed by a decline through Disturbance and Dry Forest Succession 15

A A

B B

C

FIGURE 3. Ricker model‐based estimates (predicted) and observed values of percent cover of (A) Lantana spp. and (B) Zanthoxylum fagara in cleared, cleared‐and‐grazed, and fire patches.

grazed and fire patches (Fig. 4A). For woody species collectively in the ground layer, this nonlinear pattern did not differ among

patches of different disturbance types (Fig. 4B; F4, 18 = 2.69, P = 0.06). DISCUSSION

Our results indicate significant differences in early‐successional FIGURE 2. Analysis of covariance‐based estimates (predicted) and observed coppice plant communities as a function of disturbance type. values of (A) total percent cover summed across all species; (B) Coccoloba diver- Our NMDS ordination, as well as results from permutational sifolia; and (C) Bursera simaruba in cleared, cleared‐and‐grazed, and fire patches. MANOVA, demonstrated that shrub layer plant communities in fi Plots depict where differences among disturbance types were detected. Note: patches disturbed by re were notably different compared with Linear regression line for B. simaruba in cleared‐and‐grazed patches hugs the patches affected by clearing and clearing followed by goat grazing. fi x‐axis. This is partly due to the signi cantly greater cover of three tree species in fire patches including B. simaruba, C. diversifolia, and A. choriophylla. Although the proportion of land affected in the chronosequence. For nonwoody species collectively in the patches differing in their disturbance is similar, intensity of fires ground layer, the nonlinear pattern differed among patches with in fire patches was not determined from the remote sensing different disturbances (F4, 18 = 5.44, P < 0.01). Nonwoody spe- maps. Fire severity differed within and among some patches of cies had higher estimated cover in the cleared patches early in the burned forest (Helmer et al. 2010), and in some places fires may chronosequence compared with those exhibited in cleared‐and‐ have been lower intensity ground cover fires, which would not 16 Larkin et al.

A first glance, seem to corroborate with other studies highlighting the ill effects of introduced grazers in island ecosystems (Coblentz 1978, Schofield 1989, Desender et al. 1999). We posit, though, that the difference among the a diversity indices may not be substantial, and moreover, that the compositional and struc- tural diversity exhibited by cleared‐and‐grazed patches across the landscape (i.e., b diversity) may have been greatest in those patches (Fig. 1). In addition, it is worth noting that the managed grazing in our study area on Eleuthera is far different from the feral goat grazing in many tropical and subtropical island systems, where spatial and population controls are lacking or insufficient. Our results shed new light on the effects of managed graz- ing on plant succession in dry tropical and subtropical forest set- tings. More specifically, our results suggest that grazing by goats B in coppice communities could accelerate or retard succession. Managed goat grazing may accelerate succession in the ground layer by quickly removing nonwoody ground cover and allowing the brief formation of a more notable woody community therein. In contrast, by slowing growth or establishment of common cop- pice trees such as B. simaruba in the shrub layer, goats may also be inhibiting or retarding canopy development. It has been dem- onstrated that like other ungulates, goats selectively feed on vege- tation and can subsequently alter vegetation composition (Lepš et al. 1995). Studies have documented alteration of woody species composition due to preferential feeding by goats (Riggs & Urness 1989). Lepš et al. (1995) cites four other effects of grazers on vegetation including trampling, creation of gaps, increase of nutri- ents via excretion of wastes, and increase of nutrient availability due to turnover of nutrients. The exact mechanisms by which FIGURE 4. Ricker model‐based estimates (predicted) and observed values goats may alter species composition in forested habitats in sub- of percent: (A) nonwoody and (B) woody ground cover in cleared, cleared‐ tropical regions are in need of further research. and‐grazed, and fire patches. Plots depict where differences among distur- In addition to slowing cover of common coppice trees, goats bance types were detected. may allow a subset of early‐successional shrub species to remain in early‐successional systems for longer periods of time. Early‐ affect larger trees such as B. simaruba, C. diversifolia, and A. chorio- successional species such as Lantana spp. were found in higher phylla. Evidence from the full ANCOVA model for C. diversifolia cover in older goat‐grazed patches compared with cleared patches would suggest this to be the case, because fire patches were pre- of similar age, which suggest that Lantana spp. are maintained dicted to have a significantly higher cover at time zero compared longer in goat‐grazed patches. The overall effects of grazing, with cleared and cleared‐and‐grazed patches (Fig. 2B). Given that particularly at early stages following initial clearing, may allow for fire is usually of low intensity in tropical systems (compared with a preponderance of shrub species (relative to that of tree those experienced by temperate systems; Giglio et al. 2006), species), perhaps physiognomically similar to those that typified patches affected by fire may have been subjected to a lower nearby Andros Island 3200–1500 year before present (Kjellmark intensity disturbance than those that were cleared. It is well‐ 1996). Other studies have shown that grazing maintains early‐ known that fire is needed to maintain open Caribbean pine (Pinus successional plant species. In patches intermittently grazed by cat- caribaea var. bahamensis [Griseb.] W.H. Barrett and Golfari [Pina- tle in Costa Rica, early‐successional species such as Tabebuia rosea, ceae]) forest in the Bahamas (see Campbell 1978); however, Cassia pallida, and Piscidia carthagenesis were found to be some of broadleaf coppice is not considered fire dependent (see Currie the most abundant species (Stern et al. 2002). Because of second- et al. 2005), and fire is typically assumed to be detrimental to cop- ary compounds contained in many Lantana spp., herbivory by pice (Campbell 1978). Our results indicate that coppice patches livestock such as goats may be deterred, favoring the growth of impacted by fire structurally recover at rates similar to those Lantana spp. (Sharma et al. 2007). This may benefit species such patches affected by clearing and clearing and goat grazing; though as the Kirtland's Warbler (Dendroica kirtlandii) which feeds on species composition and cover, irrespective of time since distur- L. involucrata fruits during the winter (Wunderle et al. 2010). bance, appears to differ in the fire patches. Other studies in the Caribbean have highlighted the resis- The results regarding goat grazing on plant species diversity tance and resiliency of coppice‐like systems to large‐scale distur- in early‐successional coppice communities on Eleuthera may, at bances. Low plant species turnover following hurricanes has been Disturbance and Dry Forest Succession 17

noted on the Bahamian islands of Andros, Exuma Cays LITERATURE CITED (Morrison 2003), and Exuma (Morrison & Spiller 2008). Although turnover was not directly measured in our study, many AIDE, T. M., J. K. ZIMMERMAN,M.ROSARIO, AND H. MARCANO. 1996. Forest of the same plant species were found in patches regardless of the recovery in abandoned cattle pastures along an elevational gradient in – disturbance type or time since disturbance. In addition, basal area northeastern Puerto Rico. Biotropica 28: 537 548. ‐ BAKKER, J. P., H. OLFF,J.H.WILLEMS, AND M. ZOBEL. 1996. Why do we need recovery was quick and notable ( 1/3 pre disturbance levels permanent plots in the study of long‐term vegetation dynamics? attained in 1 yr) in cleared Jamaican dry forest (McLaren & J. Veg. Sci. 7: 147–155. McDonald 2003). Although we lacked pre‐disturbance data, total BAZZAZ, F. A. 1975. Plant species diversity in old‐field successional ecosys- cover in the shrub layer increased at similar rates in patches tems in Southern Illinois. Ecology 56: 485–488. regardless of the disturbance type. Our study provided baseline BONHAM, C. D. 1989. Measurements for terrestrial vegetation. John Wiley and Sons, New York, New York. data relating to three common disturbances in coppice communi- BYRNE, R. 1980. Man and the variable vulnerability of island life: A study of ties; however, the effects of only one type of disturbance per recent vegetation change in the Bahamas. Atoll Res. Bull. 240: 1–200. patch on succession in coppice communities were tested. Future CAMPBELL, D. G. 1978. The ephemeral islands: A natural history of the Baha- research should include work on smaller disturbances, as well as mas. McMillian Education Limited, London, U.K. ‐ the interactions of these and other disturbances on successional CANFIELD, R. H. 1941. Application of the line intercept method in sampling range vegetation. J. For. 39: 388–394. trajectories in subtropical and tropical dry forest systems. CHAZDON, R. L., S. G. LETCHER,M.VAN BREUGEL,M.MARTÍNEZ‐RAMOS, F. B ONGERS, AND B. FINEGAN. 2007. Rates of change in tree communi- ACKNOWLEDGMENTS ties of secondary Neotropical forests following major disturbances. Philos. Trans. R. Soc. B 362: 273–289. We thank K. Reichenbach and D. Carey for their help in the field. COBLENTZ, B. E. 1978. The effects of feral goats (Capra hircus) on island eco- systems. Biol. Conserv. 13: 279–286. We are grateful for assistance provided by E. Carey and the Baha- COCHRANE, M. A. 2001. Synergistic interactions between habitat fragmentation mas National Trust, E. Phillips and The Nature Conservancy— and fire in evergreen tropical forests. Conserv. Biol. 15: 1515–1521. the Bahamas, and M. Vincent and J. Hickey. We also thank COCHRANE, M. A. 2003. Fire science for rainforests. Nature 421: 913–919. G. Fleming, J. White, and J. O'Brien for their input throughout the COCHRANE, M. A., A. ALENCAR,M.D.SCHULZE,C.M.SOUZA,D.C.NEPSTAD, fi project, T. Crist and B. Schussler for helping with manuscript revi- P. L EFEBVRE, AND E. DAVIDSON. 1999. Positive feedback in the re dynamic of closed canopy tropical forests. Science 284: 1832–1835. sions, and S. Otterstrom and three anonymous reviewers for their COLWELL, R. K. 2006. EstimateS: Statistical estimation of species richness and informative comments and suggestions. This research was sup- shared species from samples. Version 8. Available at http://purl.oclc. ported by a cooperative agreement between the International Insti- org/estimates (accessed 21 August 2010). tute of Tropical Forestry, USDA Forest Service and Miami CORRELL, D. S. 1979. The Bahama archipelago and its plant communities. – University, and an Academic Challenge grant to the lead author 28: 35 40. CORRELL,D.S.,AND H. B. CORRELL. 1982. Flora of the Bahama Archipelago. from the Department of Botany, Miami University. This work was J. Cramer, Vaduz, Liechtenstein. conducted in cooperation with the Kirtland's Warbler Research CURRIE, D., J. M. WUNDERLE,Jr.,D.N.EWERT,M.ANDERSON,A.DAVIS, AND and Training project funded by International Programs of the Z. MCKENZIE. 2005. Winter avian distribution in six terrestrial habitats USDA Forest Service and The Nature Conservancy. on southern Eleuthera, the Bahamas. Caribb. J. Sci. 41: 88–100. DESENDER, K., L. BAERT,J.P.MAELFAIT, AND P. V ERDYCK. 1999. Conservation SUPPORTING INFORMATION on Volcán Alcedo (Galápagos): Terrestrial invertebrates and the impact of introduced feral goats. Biol. Conserv. 87: 303–310. EXCOFFIER, L., P. E. SMOUSE, AND J. M. QUATTRO. 1992. Analysis of molecular Additional Supporting Information may be found in the online variance inferred from metric distances among DNA haplotypes: version of this article: Application to human mitochondrial DNA restriction data. Genetics 131: 479–491. TABLE S1. Species identified in the shrub layer in coppice patches on GIGLIO, L., I. CSISZAR, AND C. O. JUSTICE. 2006. Global distribution and sea- Eleuthera, the Bahamas, affected by different disturbances including clearing, sonality of active fires as observed with the terra and aqua moderate clearing and subsequent goat grazing (i.e., cleared‐and‐grazed), and fire. resolution imaging spectroradiometer (MODIS) sensors. J. Geophys. Res. 111: 1–12. FIGURE S1. Location of Eleuthera within the Commonwealth HELMER, E. H., T. S. RUZYCKI,J.M.WUNDERLE,Jr.,S.VOGESSER,B.RUEFEN- of the Bahamas. ACHT,C.KWIT,T.J.BRANDEIS, AND D. N. E WERT. 2010. Mapping tropi- FIGURE S2. Mean percent cover of A. choriophylla, B. simaruba, cal dry forest height, foliage height profiles and disturbance type and ‐ and C. diversifolia in early‐successional coppice patches on Eleu- age with a time series of cloud cleared Landsat and ALI image mosaics – thera, the Bahamas. to characterize avian habitat. Remote Sens. Environ. 114: 2457 2473. – IKEDA, H. 2003. Testing the intermediate disturbance hypothesis on species FIGURE S3. Mean Shannon Weiner diversity indices of diversity in herbaceous plant communities along a human trampling cleared, cleared‐and‐grazed, and fire patches on Eleuthera, the gradient using a 4‐year experiment in an old‐field. Ecol. Res. 18: 185– Bahamas. 197. KELLMAN, M., AND R. TACKABERRY. 1993. Disturbance and tree species coexis- Please note: Wiley‐Blackwell is not responsible for the content tence in tropical riparian forest fragments. Global Ecol. Biogeogr. 3: or functionality of any supporting materials supplied by the authors. 1–9. Any queries (other than missing material) should be directed to the KJELLMARK, E. 1996. Late Holocene climate change and human disturbance – corresponding author for the article. on Andros Island, Bahamas. J. Paleolimnol. 15: 133 145. 18 Larkin et al.

LEPŠ, J., J. MICHÁLENICK,P.KULISEK, AND P. U HLÍK. 1995. Use of paired plots RUIZ, J., M. C. FANDINO, AND R. L. CHAZDON. 2005. Vegetation structure, and multivariate analysis for the determination of goat grazing prefer- composition, and species richness across a 56‐year chronosequence of ence. J. Veg. Sci. 6: 37–62. dry tropical forest on Providencia Island, Colombia. Biotropica 37: 520 MCARDLE,B.H.,AND M. J. ANDERSON. 2001. Fitting multivariate models to –530. community data: A comment on distance-based redundancy analysis. SAS INSTITUTE INC. 2008. SAS 9.2. Enhanced Logging Facilities. SAS Insti- Ecology 82: 290–297. tute Inc., Cary, North Carolina. MCCUNE,B.,AND J. B. GRACE. 2002. Analysis of ecological communities. MjM SCHOFIELD, E. K. 1989. Effects of introduced plants and animals on island Software Design, Gleneden Beach, Oregon. vegetation: Examples from the Galapagos Archipelago. Conserv. Biol. MCLAREN,K.P.,AND M. A. MCDONALD. 2003. Coppice regrowth in a dis- 3: 227–238. turbed tropical dry limestone forest in Jamaica. For. Ecol. Manage. SEALEY, N. E. 2006. Bahamian landscapes, an introduction to the geology and 180: 99–111. physical geography of the Bahamas. Macmillan Caribbean, Oxford, MORRISON, L. W. 2003. Plant species persistence and turnover on small Baha- U.K. mian Islands. Oecologia 136: 51–62. SHARMA,O.P.,S.SHARMA,V.PATTABHI,S.B.MAHATO, AND P. D. S HARMA. MORRISON,L.W.,AND D. A. SPILLER. 2008. Patterns and processes in insular 2007. A review of the hepatotoxic plant Lantana camara. Crit. Rev. flora affected by hurricanes. J. Biogeogr. 35: 1701–1710. Toxicol. 37: 313–352. OKSANEN, J., F. GUILLAUME BLANCHET,R.KINDT,P.LEGENDRE,R.B.O'HARA, SMITH, I. K., AND J. L. VANKAT. 1992. Dry evergreen forest (coppice) commu- G. L. SIMPSON,P.SOLYMOS,M.H.H.STEVENS, AND H. WAGNER. 2010. nities of North Andros Island, Bahamas. Bull. Torrey Bot. Club 119: Vegan: Community ecology package. R package version 1.17‐3. Avail- 181–191. able at http://CRAN.R‐project.org/package=vegan (accessed 21 STERN, M., M. QUESADA, AND K. E. STONER. 2002. Changes in composition August 2010). and structure of a tropical dry forest following intermittent cattle POSADA, J. M., T. M. AIDE, AND J. CAVELIER. 2000. Cattle and weedy shrubs grazing. Rev. Biol. Trop. 50: 1021–1034. as restoration tools of tropical montane rainforest. Restor. Ecol. 8: UHL, C., K. CLARK,H.CLARK, AND P. M URPHY. 1981. Early plant succession 370–379. after cutting and burning in the upper Rio Negro region of the RDEVELOPMENT CORE TEAM. 2010. R: A language and environment for Amazon Basin. J. Ecol. 69: 631–649. statistical computing. R Foundation for Statistical Computing, Vienna, VINCENT, M. A., AND C. KWIT. 2007. Additions to the flora on Austria. Available at http://www.R‐project.org (accessed 15 April Eleuthera. Bahamas Nat. J. Sci. 2: 52–54. 2010). WHITTAKER, R. H. 1960. Vegetation of the Siskiyou Mountains, Oregon and RELVA, M. A., AND T. T. VEBLEN. 1998. Impacts of introduced large herbi- California. Ecol. Monogr. 30: 279–338. vores on Austrocedrus chilensis forests in northern Patagonia, Argentina. WUNDERLE, J. M., D. CURRIE,E.H.HELMER,D.N.EWERT,J.D.WHITE,T.S. For. Ecol. Manage. 108: 27–40. RUZYCKI,B.PARRESOL, AND C. KWIT. 2010. Kirtland's warblers in RIGGS, R. A., AND P. J. U RNESS. 1989. Effects of goat browsing on gambel anthropogenically disturbed early‐successional habitats on Eleuthera, oak communities in northern Utah. J. Range Manage. 42: 354–360. the Bahamas. Condor 112: 123–137.