BlOTROPlCA 33(4): 573-582
2001
Effects of Multiple Disturbances (Fire and Hurricane) on Epiphyte Community Dynamics in a Subtropical Forest, Florida, U.S.A.’ Kevin M. Robertson‘ Department of Plant Biology, University of Illinois, Urbana, Illinois 61801, U S A . and
William J. Platt Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana 70803, U.S.A.
ABSTRACT We addressed the interacting effects of a natural large-scale fire and a subsequent major hurricane on relative positions of epiphytes in a subtropical forest. In Everglades National Park, subtropical hammocks (hardwood tree “islands”; burned and unburned) during the Ingraham Fire (1989) were surveyed for trees and epiphytic bromeliads (Tillandtia spp.) one year before, as well as one and five years after, Hurricane Andrew (1992). We measured trees (species, diameter, and status [aliveldead]) and epiphytes (species, height, host tree characteristics, substrate life status, and density). The fire decreased the height of epiphytes during the hurricane because branches and bark of trees killed by the fire were unstable epiphyte substrates in the high winds. Proportions of epiphytes on Querm virginiana were equally increased after the hurricane in both unburned and burned hammocks; the large size and bark characteristics resulted in greater proportional survival of epiphytes on this species. During the five years following the hurricane, changes in the distributions of epiphytes generally were toward pre-hurricane distributions, but recovery was faster in unburned than burned hammocks. We conclude that disturbances that kill trees are likely to amplify the vertical reduction of epiphytes during a subsequent hurricane and that effects of a single disturbance on plant populations can be influenced by the disturbance history of the system, including different types of disturbances.
Kq word: disturbance ecologv; epiphyte recovery; Hurricane Andrew: Ingraham Fire; Long Pine Kq: plant rnortaliry; Quercus virginiana; south Florida habitats: subtropical hardwood hammocks; Tillandsia; tree and epiphyte hmage. EFFECTS O F O N E DISTURBANCE O N PLANT POPULATIONS and communities may influence the subsequent effects of a different type of disturbance (Everham & Brokaw 1996, Willig & Walker 1999). Vascular epiphytes in subtropical and tropical forests are affected by disturbances that vary in origin, frequency, and magnitude (Benzing 1980). For example, the epiphyte-rich subtropical hardwood forests of south Florida are affected by fires (Robertson & Platt 1992, Gunderson & Snyder 1994), hurricanes (Horvitz et al. 1995, Slater et al. 1995), frosts (Olmsted et al. 1993), and periods of drought (Alexander 1967) at relatively frequent intervals. These disturbances kill epiphytes directly (Craighead & Gilbert 1962, Benzing 1980, Robertson & Platt 1992). They also damage and kill host trees, thereby altering the environment of surviving epiphytes (Benzing 1978, Bennett 1987) and potentially influencing their vulnerability to subsequent disturbances. Our objective was to determine if a fire increased a subsequent hurricane’s effect on the distribution of epiphytes. We hypothesized that the Received 11 May 2000; revision accepted 4 April 2001. Corresponding author. E-mail:
[email protected]
death of trees from fire would decrease the stability of epiphyte substrates and magnify changes in their distributions during the hurricane by increasing their selective removal by wind. We predicted that in burned hammocks there would be a greater reduction in the height of epiphytes and larger changes in epiphyte distributions with regard to host tree species, diameter, and life status. We further hypothesized that the fire would influence post-hurricane recovery, such that the return of epiphyte and host tree distributions to pre-hurricane unburned conditions (Craighead & Gilbert 1962, WiUig &Walker 1999) would be slower in burned than in unburned hammocks. We evaluated these hypotheses by using pre-hurricane data collected on epiphytes and host trees from subtropical hardwood hammocks (forest “islands”) in areas recently burned and not recently burned by a natural fire to compare with data collected for the same hammocks one and four years following the hurricane.
METHODS SUBTROPICAL HmMocKS.-The study was conducted in subtropical hammocks within the Long Pine Key region of Everglades National Park (25”22’N,
573
574
Robertson and Plan
80'45'W). Long Pine Key, ca 8000 ha of oolitic limestone ( 1 - 4 m elev.), forms the eastern border of the south Florida Everglades region (Hoffmeister et al. 1967). Most of Long Pine Key contains species-rich pine savannas (sensu Platt 1999) as well as short hydroperiod prairies and sawgrass savannas (Olmsted et al. 1983). Numerous hammocks ranging in size from several trees to several hectares are embedded in these habitat types. The largest, most prominent trees in most Long Pine Key hammocks are live oaks (Quercus virginiana),locally the most important epiphyte host (Craighead & Gilbert 1962). Therefore, our study focused on changes in the proportion of epiphytes on this species relative to the ca 100 other tree species grouped (Craighead 1971). Prior to the Ingraham Fire and Hurricane Andrew, Long Pine Key hammocks had a closed canopy at ca 5 m with scattered taller, emergent trees (Olrnsted et al. 1983). Hammocks have been mapped and assigned numbers (Olmsted et al. 1983), which we used in this study. EPIPHrrES.-we focused on the four most common epiphyte species, Tilkzndsia balbisiana Schult., 7: facicuhta Sw., 7: setacea Sw., and 7: valenzuehna A. Rich. (Bromeliaceae). Tilkzndsia balbisiana is an atmospheric (non-tank) species with a bulbous rosette and rapidly tapering, twisted leaves growing to ca 70 crn in length. It is found in relatively highlight locations (Benzing 1980). Tifhndsia fascicukzta is a tank species with a large, typically upright rosette and straight, stiff, tapering leaves growing to ca 70 cm in length. Relatively large individuals commonly are located on large branches in the canopy (Oberbauer et al. 1996). Tilkzndsia setacea, like 7: balbisiana, is an atmospheric species, with needle like leaves growing to ca 40 cm in length and occurring both high in the canopy and in the subcanopy. Tilkzndsia valenzuekzna is a tank species with an upright rosette and soft, tapering leaves growing to ca 40 cm in length. Most individuals occur on tree boles in the subcanopy of the Long Pine Key region (Robertson & Platt 1992). Each of these species reproduce clonally by producing basal ramets; however, genets, identified as a group of ramets connected at a common point, were considered to be epiphyte individuals for the purposes of this study.
INCRAHAM FiRE.-In late May and early June 1989, a 50,000 ha lightning-strike fire (Ingraham Fire) burned the western end of Long Pine Key. Records of this fire are archived at Everglades National Park. The interior of several hammocks along the west-
ern end of Long Pine Key burned (Robertson & Platt 1992). Although flame lengths rarely exceeded 20 cm, most trees in burned hammocks were partially or completely killed by girdling of trunks or roots. Canopy cover was reduced to less than 25 percent of that before the fire, and the subcanopy became exposed to high light levels (Robertson & Platt 1992) that persisted for several years (K. Robertson, pers. obs.). Epiphytes above ca 1 m were not directly affected by the fire but were exposed to increased light levels not present in unburned hammocks (Robertson & Platt 1992). At the time of Hurricane Andrew, many stems of dead and surviving trees, as well as many epiphytes, extended above the reforming canopy, which was 1-2 m above ground level in the burned hammocks.
HURRICANE hIxEw.-Hurricane Andrew crossed the Florida peninsula on 24 August 1992. After making landfall along Biscayne Bay, it traveled in a westerly direction (275") at 32 km/h and crossed the peninsula in four hours (Stone et al. 1993, Mayfield et al. 1994). Wind speeds of Hurricane Andrew were among the most intense ever recorded for hurricanes in south Florida (Powell & Houston 1996), producing a 50 km band of defoliated vegetation across the peninsula (Pimm et al. 1994). The southern inner eyewall of Hurricane Andrew passed directly over Long Pine Key (Armentano et al. 1995), where maximum one-minute surface wind speeds in the Long Pine Key region have been estimated at ca 50 m/sec (180 km/h; Powell & Houston 1996). Subtropical hammocks beneath the eyewalls were extensively damaged (Armentano et al. 1995, Horvitz et al. 1995, Slater et al. 1995). Over half of the trees in Long Pine Key hammocks were snapped or uprooted, and almost all trees were damaged to some extent (Slater et al. 1995); however, only ca 12 percent of tree stems greater than or equal to 2 cm DBH (diameter at breast height) were killed in hammocks that had not burned during the Ingraham Fire. Most trees killed were in smaller size classes (Slater et al. 1995). Most surviving trees resprouted within a few weeks of the hurricane. By 1997, a low (< 5 m), dense forest canopy had redeveloped in unburned hammocks, but the subcanopy layer of burned hammocks was still exposed to sunlight (K. Robertson, pers. obs.). FiE1.D sAMi'i.iNc.-Epiphytes and trees were surveyed in three different years during the early wet season (May-July). We sampled in 199 1, two years after the Ingraham Fire, then in 1993, one year
Fire, Hurricane, and Epiphytes
afrer Hurricane Andrew, and finally in 1997. We used hammocks readily accessible from either side of fire roads along the western edge of Long Pine Key (Olmsted et al. 1983, Robertson & Platt 1992). The humus substrate of four hammocks (nos. 9, 10, 11, and 119) had burned, but that of four other hammocks (nos. 4, 90, 101, and 113) had not burned during the Ingraham Fire. All eight hammocks were generally round and 80-100 m in diameter and had last burned prior to the Ingraham Fire in 1940 (Olmsted et al. 1983). Epiphytes and all trees (whether or not they were supporting epiphytes) were surveyed within quadrats established along a transect through the center of the hammock. Thus, any effects on epiphyte distributions related to distance from hammock edge were replicated equally among hammocks. Quadrats measuring 5 X 5 m were established at 20 m intervals along each transect. Three unburned and three burned hammocks contained five quadrats, and one hammock in each category contained four quadrats. The total area sampled was 950 m2, with half of the area in each burn category. For each epiphyte with leaves longer than 2 cm, we recorded species, height above ground (including 0 if substrate was detached and fallen), host tree species, DBH (ca 1.5 m) of host tree, and substrate status (live tree, dead standing tree, dead fallen tree, or detached branch or bark). The census in 1991 totaled 2437 epiphyte genets (108 7: balbisiana, 807 7:faciculata, 1154 7: setarea, and 368 7: valenzuelana) and 434 standing trees (alive and dead) 2 cm DBH or greater. The eight most common tree species, Q. virginiana Mill., Sideroxylon salicifalium (L.) Lam., Nectandra coriacea (Sw.) Griseb., Metopium toxiferum Kr. Urb., Bursera simarouba (L.) Sarg., Lysiloma latisiliquum (L.) Benth., Ficus aurea Nutt., and Eema micrantba (L.) Blume, comprised ca 70 percent of all trees censused. We calculated the importance value [ZV= (relative relative basal area)/2] of Q. virginiana density for each hammock. Hammock no. 11 (burned) was not surveyed for trees in 1993 and hammock no. 4 (unburned) was not surveyed for trees or epiphytes in 1997, because flooding prevented access.
+
hALYsis.-The analyses were designed to compare distributions of epiphytes and trees between unburned and burned hammocks and among years. Significant interactions between the burn status and year factors would suggest an influence of fire effects on hurricane effects. Unburned hammocks were considered to be a “control” for fire effects,
575
with the assumption that epiphyte and tree distributions in unburned hammocks would have remained nearly unchanged between the first ( 1 99 1 ) and second (1993) census if there had not been a hurricane between them. This assumption is consistent with our observation that mortality due to the fire was immediate, while dead trees remained largely intact during the subsequent three years and continued to support populations of epiphytes. Distributions recorded in the census one year following the hurricane were similarly assumed to represent those immediately following the hurricane, supported by our observation that both damage and mortality to trees occurred in close association with the hurricane, with little residual mortality or degradation of remaining live and dead trees. Individual analyses tested for changes in each of the following response variables: (1) proportion of epiphytes located at more than 2 m height above the ground; (2) proportion of epiphytes on trees (live or dead) greater than 10 cm DBH; (3) proportion of all trees (live or dead) greater than 10 cm DBH; (4) proportion of epiphytes on Q. uirginiana; (5) importance value of Q. virginiana; (6) proportion of epiphytes on live versus dead standing trees; (7) proportion live versus dead standing trees; and (8) proportion of epiphytes on standing trees (live or dead) versus detached or fallen substrates (branchfalls, detached bark, or dead treefalls). “Live standing trees” included leaning trees and tree stumps still producing leaves or epicormic sprouts. In each test, hammocks were used as replicates, nested within burn status as a random variable, and burn status and survey year were factors in a two-way repeated measures ANOVA (Sokal & Rohlf 1995). The four epiphyte species were combined for tests on the proportion of epiphytes on Q. virginiana because of the patchy distribution of epiphytes among trees. Results for the model, main, and interaction effects for each ANOVA are reported in Table 1 . Least significant difference contrasts were calculated for each test having significant main or interaction effects to determine sources of overall significance. Contrasts included burn status x year interactions for the 1991-1993 and 1993-1997 intervals (hereafter referred to as the “hurricane interval” and “recovery interval,” respectively), differences between subsequent censuses within burn status and with unburned and burned hammocks combined, and differences between unburned and burned hammocks within each census year. Results for contrasts that were significant at the a = 0.05 level are referred to in the text. Homogeneity of variance was tested for
8, 5 8, 6 9, 8 8, 5 9, 8 10, 10
8. 6 8, 6 9, S 8, 6 10, 10
8, 6 8, 6 8, 6 8, 6 11, 12
8, 6 8, 6 8, 6 8, 6
2.27 16.16 10.15 9.46 2.05 1.96
16.07 3.66 3.92 1.97 4.80
7.53 3.79 6.04 2.66 5.44
2.46 4.03 5.80 0.63
F
Model df
0.145 0.053 0.023 0.773
0.012 0.061 0.021 0.125 0.003
0.001 0.066 0.034 0.213 0.010
0.167 0.002 0.002 0.007 0.162 0.153
P
5.66 6.71 5.72 0.04
2.71 5.03 9.68 3.43 16.84
3.72 3.52 4.73 1.77 7.81
6.29 17.34 11.52 17.39 5.68 0.59
F
10
8
6 6 8 6
2, 2, 2, 2,
2, 2, 2, 2, 2, 6 6 6 6
6 6 6 6 12
2, 6 2, 6 2, 8 2, 6 2, 10
2, 2, 2, 2, 2, 2,
Year df
0.042 0.030 0.041 0.957
0.145 0.052 0.013 0.102 I 0 crn DBH T. balbisiana T.fmciculata 7:setacea T. uaknzuelana Trees > 10 cm DBH Epiphytes on live trees T. balbisiana T.fascicuhta 7: setacea T. valenzuelana Trees living Epiphytes on standing trees T. balbisiana T fmciculata T. setacea T valenzuelana
TABLE 1.
B
n
9 2Q
Fire, Hurricane, and Epiphytes
W1991 a1993171997
1991 FA1993 0 1997 100
Unburned
100
a.
Unburned 1
i
r 100
'*I
I
80
60 40 20
3 60
8
eD
40
E 2o -
A
0c
0
O 100
b.
.a 80 3 60
'
n
0
B
Burned
a,
I/)
40
80 .% 60
60
3
40
40
20
20
I:
0
20
0
Epiphytes
n "
b
577
f s V Epiphyte Species
FIGURE 1 . Percent of total epiphytes in each species located at more than 2 m height above the ground in (a) unburned hammocks and (b) burned hammocks in 1991 (pre-hurricane), 1993 (post-hurricane), and 1997. Epiphyte species are fillandria balbisiana (b). 7: fasciculata (f), 7: setacea (s), and 7: valenzuelana (v). Error bars are standard error of the mean for replicate hammocks in each burn status category and year.
the burn status and year factors for each dependent variable using the Levene test (SPSS Inc., Chicago, Illinois). Variables, all of which were proportions, not having homogenous variances were arcsine square root transformed to meet the homoscedasticity assumption of the tests (Sokal & Rohlf 1995). ANOVAs were run using SAS PROC MIXED (SAS Institute, Cary, North Carolina).
RESULTS As predicted, there was a greater reduction in height of epiphytes in burned than in unburned hammocks (Figla, b; Table 1). During the recovery interval, proportions of epiphytes more than 2 m above ground generally increased in both unburned and burned hammocks (Fig. la, b). These changes toward pre-hurricane conditions did not show the predicted larger recovery in unburned than burned hammocks, but heights of epiphytes in the final census were significantly higher in unburned hammocks for 7:fmcicuhta, 7: setacea, and 7: valenzuelana (Fig. 1 a, b).
Q. virg.
FIGURE 2. Percent of total epiphytes, species combined, located on trees of Quercus virginiana (left axis) of Q. virginiana (right axis) and the importance value in (a) unburned and (b) burned hammocks in 1991 (prehurricane), 1993 (post-hurricane), and 1997. Error bars are as in Figure 1 .
(m
The proportion of epiphytes (species combined) on Q. virginiana increased significantly during the hurricane interval in unburned and burned hammocks; however, the predicted larger change in burned hammocks was not evident (Fig. 2a, b; Table 1). The importance value of Q. virginiana increased during the hurricane interval only in unburned hammocks (Fig. 2a, b; Table 1). During the recovery interval, the proportion of epiphytes on trees in Q. virginiana decreased slightly toward pre-hurricane conditions without the predicted difference between unburned and burned hammocks (Fig. 2a, b), while the importance value of Q. virginiana did not change significantly (Fig. 2a, b; Table 1). The proportion of epiphytes on trees greater than 10 cm DBH increased significantly during the hurricane interval for 7: balbisiana in burned hammocks and for Tfasciculata and 7: setacea in general, but the expected larger changes in burned hammocks occurred only for 7: balbisiana (Fig. 3a, b; Table 1 ) . The proportion of trees greater than 10 cm DBH increased significantly in unburned but not in burned hammocks, also in contrast to predictions (Fig. 3a, b). During the recovery interval, changes in the proportion of epiphytes on trees greater than 10 cm DBH varied among species (Fig. 3a, b). The proportion of trees greater than
Robertson and Platt
578
11991 R1993 01997
.I991 Ed1993 01997 Unburned
Unburned
8 60
T
I
100
I
80
60
v)
100
80 60
40 40 A v)
0
2
20 0
20
0
g
x c
Burned
0
z
b
XI00
80
M
.E >
4
60
.-Q 40
u" 20 3
f
0
s v Epiphyte Species
b
f
FIGURE 3. Percent of total epiphytes on trees greater than 10 cm DBH (left axis) and trees less than 10 cm DBH (right axis) in (a) unburned and (b) burned hammocks in 1991 (pre-hurricane). 1993 (post-hurricane), and 1997. Epiphyte species and error bars are as in Figure 1. Trees include live and dead standing trees combined.
10 cm DBH decreased significantly in unburned hammocks toward pre-hurricane levels and did not change significantly in burned hammocks (Fig. 3a, b; Table 1). During the hurricane interval, the proportion of epiphytes on live versus dead trees increased to a greater extent in burned than in unburned hammocks as predicted (Fig. 4a, b), although the overall interaction effect was significant only for 7: setacea (Table 1). In contrast, the proportion of live standing trees did not change significantly during the hurricane interval in either unburned or burned hammocks (Fig. 4a, b). During the recovery interval, the proportion of epiphytes on live trees in unburned hammocks decreased, and in burned hammocks increased, such that both approached pre-hurricane unburned conditions at the final survey (Fig. 4a, b). The proportion of epiphytes on standing trees (live or dead) decreased for all species in burned hammocks in contrast to unburned hammocks (Fig. 5a, b), although the predicted significant interaction effect occurred only for 7: setacea (Table 1). During the recovery interval, changes in proportions of epiphytes on standing trees were generally toward pre-hurricane unburned conditions, but the magnitude of change was not measurably
b
s
v
trees
Epiphyte Species
trees
FIGURE 4. Percent of total epiphytes on live trees (vs. dead trees; left axis) and percent of total trees living (right axis) in (a) unburned and (b) burned hammocks in 1991 (pre-hurricane), 1993 (post-hurricane), and 1997. Epiphyte species and error bars are as in Figure 1.
m1991 B1993 01997
Unburned m
100
g
80 60 40 20
Z
n"
!.a
c
Burned
0
-g 100 4 vl
..a
80
$
40 20 0
8
b.
60
b
f s V Epiphyte Species
FIGURE 5. Percent of total epiphytes on standing trees (vs. detached substrates) in (a) unburned and (b) burned hammocks in 1991 (pre-hurricane). 1993 (post-hurricane), and 1997. Epiphyte species and error bars are as in Figure 1.
Fire, Hurricane, and Epiphytes
TABLE 2.
579
Mean number of epiphyte genets (>2 em leaf length) per 5 x 5 m quadrat survPyed in unburned and burned hammocks for four epiphyte species. NA = data not available.
Unburned Tillandiia balbisiana 7:fmcicukzta 7: setacea 7: valenzuelana
Burned
1991
1993
1997
1991
1993
1997
5.3 4.9 44.2 17.6
1.6 4.6 20.9 9.7
1 .o
1.8
5.4 14.2
9.9 24.1 8.1
2.1 5.3 16.1 5.4
2.4 9.8 5.9 10.7
NA
nated by Q. virginiana suggests that this tree is a particularly important support of epiphytes during hurricanes. Its large size, rough, deeply &crowed EPIPHYTEDENSITY.-DenSitieS of epiphytes de- bark, and lateral branches may initially promote creased during the hurricane interval for epiphytes frequent attachment and germination of seeds and in each species except T. balbisiana in burned ham- subsequently offer greater resistance to wind than mocks (Table 2). Reductions were greater in un- the bark of tropical tree species (Benzing 1978, burned than burned hammocks for epiphytes of T. Robertson & Platt 1992, Caldiz et al. 1993). Large balbisiana, 7: setacea, and T. valenzuelana. During trees in general may provide the most stable epithe recovery interval, densities of epiphytes in- phyte substrate during high winds, possibly concreased except for those of 7: balbisiana in un- tributing to the disproportionate occurrence of epiburned hammocks and 7: setacea in both unburned phytes on large trees documented in other studies and burned hammocks (Table 2). (Yeaton & Gladestone 1982, Bennett 1987, HeitzSeifert et al. 1995, Pascarella 1997). Some of the effects of the fire and hurricane DISCUSSION on the distributions of epiphytes differed among Results were consistent with our hypothesis that epiphyte species. During the hurricane interval, T fire decreased the stability of epiphyte substrates fasciculata in unburned hammocks remained mostand magnified the effect of the hurricane on epi- ly on large, live trees, persisted in upper height catphyte distributions with regard to height and pro- egories, and had relatively high survival. Ellandria portions on live and standing trees. In burned facciculata is a large tank species noted for strong hammocks, epiphytes had larger reductions in adherence to large branches and boles of living trees height, larger increases in proportion on live trees, (Craighead & Gilbert 1962, Benzing 1978, Oband larger reductions in proportion on standing erbauer et al. 1996) and has stiff leaves unlikely to trees, despite the negligible change in the propor- be damaged by hurricane winds. In burned hamtion of live versus dead standing trees. These pat- mocks, its large size, combined with its occurrence terns suggest that branches and bark of dead trees, on dead substrates, apparently caused it to be frewhich dominated burned hammocks, were fre- quently removed from trees and reduced in height, quently detached, relocating epiphytes to or near as were other species in burned hammocks. Elthe ground. Conversely, epiphytes were less fre- landria setacea and T. vahnzuelana similarly adquently removed from live trees, which dominated hered firmly to live trees in unburned hammocks, unburned hammocks, indicating that live trees pro- usually in clusters of ramets, and were frequently vided a more stable substrate. Thus, epiphytes re- removed from dead trees in burned hammocks. O n mained at greater heights above the ground in un- live trees in unburned hammocks, the relatively delicate leaves of T. setacea and T. valenzuelana burned hammocks. Although the hurricane significantly increased made them more likely to be damaged by wind the proportion of epiphytes on Q. virginiana and while adhered to a more stable substrate above the increased proportions on larger trees, these changes ground where wind exposure was high. These qualwere not influenced by the preceding fire as pre- ities appeared to result in greater reductions in dendicted by our hypothesis. The increase in the pro- sity for these two species in unburned than in portion of epiphytes on Q. virginiana, the increase burned hammocks during the hurricane interval. in the importance value of this species, and increase Unlike other species, T. balbisiana was frequently in proportion of epiphytes on larger trees domi- removed from trees in unburned as well as burned different between unburned and burned hammocks (Fig. 5a, b).
580
Robertson and Platt
hammocks. This species is an atmospheric type with thick leaves and a dense rosette, but with a narrow, flexible root base allowing it to occupy small, easily breakable branches and to be torn from tree trunks during high winds. In contrast to our prediction, the rate of change toward recovery was equally slow in unburned and burned hammocks during the measured period; however, larger proportions of epiphytes at greater than 2 m height and on standing trees in unburned than in burned hammocks at the end of the study suggests that recovery with regard to these variables will take less time in unburned than in burned hammocks. The frequent occurrence of hurricanes in south Florida (Platt et al. 2000) relative to the observed recovery rates suggests that vertical distributions of epiphytes may be changing almost continually in these subtropical forests. Alteration of the environment by the hurricane may have long-term effects on populations of some epiphyte species. During the recovery interval, the continuing decline of 7: balbisiana populations in unburned hammocks and 7: setacea in general may have resulted from the increase in exposure caused by the denudation of the forest by the hurricane. Increased light levels and temperatures may desiccate plants and prohibit germination, and the lower position of surviving epiphytes may reduce seed dispersal and recruitment (Benzing 1981). Results from our study may be generally applicable to forests that contain epiphytes, are susceptible to disturbances that kill trees, and are altered by periodic by hurricanes. Such environments include much of Central America, Mexico, the Caribbean islands, South Pacific islands, and Southeast Asia (Benzing 1980, Everham & Brokaw 1996). Tree-damaging disturbances (in addition to hurricanes) in tropical or subtropical environments include fire (Whigham et al. 1991, Elmqvist et al. 1994), frost (Olmsted etal. 1993), lightning strikes (Smith et al. 1994), and drought (Alexander 1967). Any of these may kill trees and therefore increase the effects of a subsequent hurricane on epiphyte populations in a manner similar to the Ingraham Fire. The generality of our results is further sup-
ported by characteristics of epiphyte populations and hurricane damage. The need for adequate light levels results in epiphytes of many species occurring primarily in the canopy (Pittendrigh 1948), which sustains the most damage during hurricanes (Dittus 1985, Brokaw & Grear 1991, Walker 1991). The few studies on the effects of hurricanes on epiphytes have reported significant reductions in epiphyte height (Rodriguez-Robles et al. 1990, Migenis & Ackerman 1993, Oberbauer et al. 1996). Given the adherence of epiphytes to live trees in the current study, the often-reported high survival of trees severely damaged by hurricanes (Yih et al. 1991, Bellingham et al. 1992, Zimmerman e t al. 1994, Slater et al. 1995) suggests that they will continue to provide a stable substrate for surviving epiphytes. The sequence of proximate disturbances can influence their effects on epiphyte populations. The Ingraham Fire appeared to directly kill only epiphytes on the ground or at heights less than 1 m (Robertson & Platt 1992) while Hurricane Andrew caused significant mortality for most species; however, fires following hurricanes in subtropical forests (Furley & Newey 1979, Whigham et al. 1991, Elmqvist et al. 1994) could have a much larger effect on population densities than direct effects of the preceding hurricane because of the lowered heights of surviving epiphytes and larger numbers on the ground following the storm. In general, our study underscores the importance of considering disturbance history when attempting to determine how the distribution of plants is affected by any single disturbance.
ACKNOWLEDGMENTS We thank David Baker, Hester Johnson, Ann Goodson, and Kathy Knight for assistance with field work, Harold Slater for resources and logistical support, and Bob Doren for encouragement and logistical support of this project. Everglades National Park provided access and transportation to field sites. We also thank Peter Bellingham, Nick Brokaw, James Ackerman, and an anonymous reviewer for helpful comments on prior drafts of the manuscript. Funding was provided by NSF grant DEB 9314265, W. J. Platt, PI., USDI National Park Service Cooperative Agreement CA5280-3-9009, W. J. Platt, PI., and by Everglades National Park.
LITERATURE CITED h . w u t x , T. R. 1967. A tropical hammock on the Miami (Florida) limestone-a
twenty-five-year study. Ecology 48: 863-867. h M L w r A N o , T., R. F. DOREN, w. J. PUTT, AND T. MULLINS. 1995. Effects of Hurricane Andrew on coastal and interior forests of southern Florida: overview and synthesis. J. Coastal Res. SI 21: 111-1 14.
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