Using tree census data from four large, permanent FDPs with different disturbance regimes that are primarily attributed to cyclonic storm frequency (Table 1
), we have shown differences in forest demographic (Figure 2
, Figure 3
and Figure 4
, Table 2
) and functional responses at the small patch scale (20 × 20 m quadrats) (Figure 5
, Table 5
) to large cyclonic storms. BCI did experience some moderate winds, but not the sustained and damaging cyclonic storms of the other three FDPs; therefore, at BCI forest dynamics can be attributed to gap-phase dynamics related to tree senescence and fall. Luquillo, Puerto Rico, was the most demographically dynamic forest and demonstrated the most functional variation in community composition. BCI, Panama, was the most dynamic in terms of stem growth increment and biomass dynamics, probably because of the more fertile soil conditions and other ecosystem factors that differ between montane island forests and lowland continental forests (e.g., nutrient cycling, hydrology). Of the directly cyclone-impacted plots, Palanan, Philippines, was less dynamic in population abundances, but about as functionally dynamic as Luquillo. Fushan, Taiwan, was neither very dynamic in population fluctuations of species nor in functional responses to cyclonic storms, despite being affected by them most-frequently.
Within an ecological disturbance framework [66
] and employing the definition of forest resistance to the cyclonic storm as the degree to which forest demographic and functional composition remain unchanged by disturbance, we show the Fushan FDP to be highly resistant to cyclonic storms. BCI also exhibits a relatively high degree of forest stability in the absence of cyclonic storms (Figure 5
, Table 5
). Fushan and BCI are comparable in their relatively low degree of demographic and functional variability across census intervals but differ considerably in the type of tropical forest they contain, which is evident in the degree of biomass flux at the hectare (Table 2
) and quadrat (Figure 5
) scales. Luquillo and Palanan are both more dynamic in forest demographics and their functional responses, with the functional divergence in relation to cyclonic storms persisting for longer at Luquillo after a storm. The forest at BCI is a typical neotropical lowland forest with an average canopy height of 30 m [68
], but the canopy height at Fushan is 15–20 m in the valleys and flat areas and 5–10 m on the ridges [41
]. Luquillo and Palanan possess an intermediate canopy height of about 20 m [13
]. Such differences in canopy height are driven by the constant pruning of canopy of the forests by cyclonic wind disturbance [70
]. Furthermore, Luquillo, Fushan, and Palanan all lack canopy emergent trees, which is undoubtedly a forest-wide result of recurrent cyclonic storms [13
This clear relationship of decreasing canopy height and storm frequency invokes the idea of disturbance legacy effects and the idea of ecological memory sensu
Johnstone et al. [71
]. Indeed, there is an underappreciated level of evolution at the species level and adaption at the individual level to environments that experience intense wind. Griffith et al. [72
] showed that palms from cyclonic storm-prone provenance have an order of magnitude of lower percent mortality than those from non-cyclonic storm-prone provenances in the living collections of Montgomery Botanical Garden, Florida following Hurricane Wilma in 2005. A cyclonic storm-resistant palm, Presotea acuminata
(Graham) A.J. Hend. and Galeano is the most abundant species at Luquillo, accounting for a third of the stems in the plot. Furthermore, the dominant canopy tree at Luquillo, Dacryodes excelsa
Vahl forms complex root unions, which help collectively stabilize individuals during high winds and help maintain a regeneration foothold in the community [73
]. Trees at Fushan maintain a smaller stature, because those that are exposed above the canopy or grow in gap habitats are frequently damaged by cyclonic storms and incur higher rates of mortality [74
]. This disturbance effect operates more strongly and consistently at Fushan and Palanan than at Luquillo and has no effect on the forest structure of BCI, hence the occurrence of canopy emergents, oftentimes extending above the forest canopy layer by 10 m or more [69
]. Such adaptations to wind disturbance at the individual and species level, and the ability of trees to adapt to and persist under changing disturbance regimes, have implications for ecosystem processes (e.g., carbon and nutrient cycling) and the fate of future tropical forests.
4.2. Do Forests That Have Storm Recurrence Intervals That Coincide with the Time to Reproductive Maturity of Tropical Trees Show Greater Changes in Functional Community Composition (i.e., More Variation in Species Life-History Strategy per Unit Area over Time) Than Forests with More Frequent or No Cyclonic Storms?
The functional trait-demographic rate correlations (Table 3
and Table 4
) are both congruent with previous studies [46
] and confirm a previous finding by Wright et al. [48
] that relationships strengthen when including all stems (those ≥1 cm dbh, as opposed to limiting the analysis to large trees ≥10 cm dbh). In cyclonic-storm affected forests, tree height was a poor correlate for population growth rates (Table 3
), because of the interchanging dynamics of tall canopy trees and understory shrubs. Depending on the structure of the forest and its patch dynamism, the population growth of trees or shrubs may be greater. However, tree H
was negatively correlated with mortality rates (Table 4
), except for large trees at Palanan and Fushan. For functional trait-population growth rate relationships, there exists a tradeoff between WD and SLA. In census intervals where cyclonic storm damage occurred, WD was positively correlated with the community-wide intrinsic rate of population growth, yet in census intervals where the forest was recovering from storm damage, SLA was the strongest correlate. This relates species life-history strategies to the relative strength of cyclonic storm damage verses light-dependent processes governing population dynamics [6
]. Specifically, during storm intervals the populations of dense wooded species grow faster than pioneer species with less-dense wood, whereas following storms the opposite is true. In a world with increasing cyclonic storm occurrence, dense wooded, slow-growing, shade-tolerant species may have increasingly dynamic population fluctuations.
The cyclonic storm return interval is important because it determines the successional composition of adult trees that are impacted by the disturbance. Namely, at shorter intervals, species with fast population growth rates that typically have high SLA or other acquisitive, pioneer-type functional traits tend to be more negatively affected by storms (i.e., incur greater degrees of stem damage and mortality), decreasing the intrinsic rates of population growth of those species to a greater degree than late-successional species. Conversely, at longer intervals, few pioneer species comprise the community of adult trees, and late-successional species are more damaged, subsequently decreasing the population growth rates of those species to a greater degree. Pioneer species can, then, readily colonize the canopy in the high-light environment of a cyclone-disturbed forest and populations can grow rapidly.
The correlations of functional traits and population growth rates of species (Table 3
) tended to weaken or become non-significant over census intervals in between cyclonic storms occurrence (e.g., Luquillo census interval 2 and Palanan census interval 1), illustrating not only the widespread damaging effects of the storms, but also the interplay in forest successional status and individual life-history strategies as they relate to storm intensity, recurrence interval, and the composition of species in each plot. These results support a growing need in the discipline of functional plant ecology to delve deeper into our understanding of individual performance and the underlying factors influencing functional trait variability, or lack thereof [77
]. We show mixed evidence for the applicability of functional traits in explaining population and community dynamics in response to disturbance, using trait data collected at the species level (Table 3
and Table 4
). Notably, relationships were weaker for population growth than mortality rates (Table 4
), likely owing to the distinct biological processes, and a greater degree of demographic variability, in stem recruitment versus stem mortality. Indeed, the short-term damage of cyclonic storms appears indiscriminate (Figure 1
), yet the effects of the disturbance on the population dynamics of species and the community (e.g., ecological selection processes, delayed mortality, recruitment) take time to register in forest dynamics data [16
]. As hypothesized, all three functional traits correlated to some degree with the variation in stem mortality (Table 4
). Luquillo had some of the strongest Pearson correlation coefficients for SLA, and Palanan had the strongest correlations for tree H. In a world with increasing cyclonic storm occurrence, this implies possible selection against species with large or cheaply-constructed leaves (high SLA), as illustrated by forest dynamics at Luquillo, and trees with tall stature, as illustrated by the dynamics at Palanan.
Among BCI, Luquillo, Palanan, and Fushan, Fushan had the most-stable functional communities. For example, the community-weighted mean value for WD at the quadrat (20 × 20 m) scale remained unchanged over a decade (Table 5
). SLA and tree H mirrored this dynamic. Similarly, Fushan had the least functionally divergent assemblages among quadrats (Figure 5
). It was difficult to account for differences in forest biomass distribution among FDPs. Biomass fluctuations for quadrats at BCI were six to seven times greater than those at Fushan, likely because of the difference in tree size and effect of a large treefalls at BCI. However, when comparing quadrats within ±10 kg quadrat−1
biomass change, the change in standardized effect size for functional divergence rarely exceed ±1 for Fushan, ±2 for BCI, and occasionally exceeded ±2 for Palanan and Luquillo, notably when the FDPs were recently affected by cyclonic storms (Figure 5
). Thus, in a world with increasing cyclonic storm occurrence, community assemblages could become increasingly mixed with a wider range of tree life-histories, or functionally divergent. However, this is largely context dependent, and depends on the individual population dynamics of tree species in the community, and species immigration and extinction—demographic responses which are either directly or indirectly affected by disturbance. Our results also show increasing similarity in certain assemblages.
At Luquillo, Hurricane Georges (1998) increased the variability in the functional divergence of quadrat assemblages, which can be most clearly seen in census intervals 2 and 3. Similarly, at Palanan during census interval 1, the functional divergence variation among quadrats increased because of Typhoon Zeb (Figure 5
). This means that quadrats became either more similar or more different in their functional composition when struck by the category 2 storm. At Luquillo, this is likely due to the differential susceptibilities of species [18
] and how they are preferentially sorted in space across the plot by past land use [25
]. Hurricane Georges interacted with the land-use legacies, forcing communities to become more different, via functional divergence, which was primarily driven by a proliferation of understory shrubs [25
]. At Palanan, typhoons interact with the plot topography, mainly windward vs. leeward slopes, where mortality and recruitment are higher during and after cyclonic storm disturbance [40
]. At BCI and Fushan, such events are limited to gap areas and are more spatially and temporally variable because of the lesser degree of landscape-scale canopy alteration via disturbance. This limits the functional divergence of those FDPs to be less variable, thus making the communities relatively more stable.
Our result about cyclonic storms increasing community functional divergence aligns with previous research on the functional diversity of Luquillo, which has shown a variety of functional traits to be phylogenetically overdispersed [49
] when compared to BCI and other forests [80
]. Together these confirm that the functional trait diversity expressed in the community arises from a more-distantly related assemblage of angiosperms than in other forests such as BCI, which we contend is related to disturbance-effects on the community, chiefly a greater persistence of pioneer species. Truly, over a given timespan, forests that have storm recurrence intervals at timescales closer to the average tree lifespan show greater changes in functional community composition than forests with more frequent or no cyclonic storms. The interval of storm recurrence is a significant factor, in that at shorter intervals the persistence of pioneer species is decreased, as shown in the example of the Fushan plot, thereby decreasing the degree of functional trait diversity in the community. At longer intervals, late-successional species can dominate, shifting functional composition toward lower SLA and higher WD, with pioneer species persisting primarily in forest gaps. Therefore, a world with increasing cyclonic storm occurrence should permit for the co-existence of a wide range of ecological strategies within tropical forests, and possibly increase the functional diversity of forests experiencing new, or more frequent cyclonic storms, potentially increasing forest dynamism.