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Department of Integrative Biology, 3060 VLSB, University of California, Berkeley, California 94720-3140 USA
Received for publication February 15, 2000. Accepted for publication June 20, 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: cloud forest • Cyathea • Cyatheaceae • generalist • habitat • specialist • succession • tree fern
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Quantitative studies of species distribution in a mid-elevation cloud forest on the Pacific slope of the Colombian Andes showed that some species, such as Lophosoria quadripinnata (J. Gmel.) C. Chr., are restricted to sunny, open habitats (Arens and Sánchez Baracaldo, 1998
). Other species, such as Cyathea planadae N.C. Arens & A.R. Sm., are found only in the understory of closed-canopy forests (Arens and Sánchez Baracaldo, 1998
; Arens and Smith, 1998
). Like many tree ferns, Cyathea caracasana (Klotzsch) Domin was distributed across all of the successional habitats studied and also occurs in undisturbed primary forest (Arens and Sánchez Baracaldo, 1998
). Furthermore, the species showed both anatomical (Arens, 1997
) and morphological (Seiler, 1984
; Arens and Sánchez Baracaldo, 2000
) variation among habitats. This variation was well correlated with both habitat type (Arens and Sánchez Baracaldo, 2000)
, and with specific environmental parameters (e.g., available light; Arens, 1997
). Consequently, we have proposed that some anatomical and morphological traits are phenotypically flexible responses that allow C. caracasana to live across the range of successional habitats found in the Andean cloud forest. In this paper I ask how plant performance, as reflected in stem growth rate, rate of leaf production, leaf longevity, and rate of spore production, varies with successional habitat. These data more completely describe the life history of Cyathea caracasana and provide the basis for hypotheses on the evolution of this life history.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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25 m composed of relatively few tree species. The most common canopy trees include Alchornea (Euphorbiaceae), Clusia (Guttiferae), Inga (Fabaceae), Miconia (Melastomataceae), Myrica and Psidium (Myrtaceae), and Otoba (Myristicaceae). The majority of the reserve's 3200 ha is covered with primary forest, which has been little disturbed by human activity. These forests occur on both level ground in the floor of the volcanic caldera, for which the reserve is named, and on the steep slopes of the volcano's flanks. Within the primary forest, canopy gaps are an important component of the habitat dynamic. In a typical year, 3% of mature forest is under gaps, yielding an average forest turnover rate of 74 yr (Samper K., 1992
). This figure may be higher on slopes, where heavy rain produces frequent landslides. The majority of gaps result from tree or branch falls and are <40 m2 in size (Samper K., 1992
). The reserve also contains recently abandoned pasture land and secondary forest that has been under natural regeneration for <50 yr. Land use history information available at the reserve allows accurate estimation of regeneration age for these parcels. In this study, I used this habitat mosaic in space as a proxy for the temporal dynamic of gap formation and closure that characterizes this forest.
Data gathering
In November 1993, I initiated a long-term monitoring study of growth and performance of 20 individuals of Cyathea caracasana in each of three habitat types. (1) Open habitat consisted of recently abandoned pasture in which woody angiosperms were absent or present only as seedlings. In this open habitat, tree ferns formed the canopy and received full sun. (2) Secondary forest 15 yr into regeneration was characterized by a dense, nearly monotypic stand of Miconia, with a canopy between 3 and 4 m in height. I refer to this as low-canopy forest. (3) Secondary forest 30 yr into regeneration from pasture was characterized by a more open understory beneath a canopy of 10–15 m; dominant trees included Inga, Myrica, and Otoba. This is referred to as high-canopy forest. Twenty individuals within each habitat type were located within a 1-ha area so that they might reasonably be assumed to be experiencing similar environmental conditions (e.g., soil type, moisture, slope, aspect). No information on the age of individual ferns was available, however all were 2 m in height or less at the beginning of the study. Plants were monitored monthly for 33 mo. Cyathea caracasana also occurs in mature, undisturbed cloud forest at La Planada. I did not include mature forest ferns in this study because individuals are widely separated in the forest, making sampling difficult and control for soil, slope and aspect impossible.
At each monthly visit, new, fully expanded leaves were marked with a dated tag; senesced leaves (>50% brown) were noted, and their tags removed and dated. This allowed calculation of rates of leaf production, leaf senescence, and leaf life span. At each monthly visit, fertile leaves were also noted, permitting the calculation of spore production rates and the documentation of annual patterns. At 6-mo intervals trunk height was measured from the apical meristem to ground level, and the total number of leaves was noted. These data allowed me to calculate stem growth rate and double-check the accounting of new and senesced leaves. No mortality was observed among study individuals during the 33 mo of observation.
Manipulations and statistical analyses, detailed in results, were performed in Microsoft Excel 5.0a and SYSTAT 5.2 (Wilkinson, 1989
) for Macintosh.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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30 cm/yr in C. caracasana was somewhat lower than that observed for Cyathea hornei (Baker) Copel. in Fiji (Ash, 1987
). A student's t test, assuming unequal variances, showed that growth rates were statistically indistinguishable between open habitat and low-canopy forest (P = 0.90; unless otherwise noted, all P values reported in this paper are two-tailed probabilities for tcritical 
t for a two-sample t test assuming unequal variances), while both differed significantly from the high-canopy forest (P < 0.001). However, the variance observed in the low-canopy forest was significantly greater (F test for equality of variance, P < 0.001) than that seen in either the high-canopy forest or open habitat, which had statistically indistinguishable variance (F test for equality of variance, P = 0.4).
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. A similar pattern was found for Nephelea tryoniana Gastony growing in the understory of the mid-elevation forests of El Salvador (Seiler, 1984
). Arens and Sánchez Baracaldo (2000)
hypothesized that ferns with long stipes could continue to function as open-habitat plants even after their meristem had been overtopped by the surrounding woody angiosperms. To explore this hypothesis, I segregated the low-canopy plants in this study into two groups: one in which long stipes or tall trunks allowed the photosynthetic surfaces to persist in the canopy (12 individuals), and one in which ferns in the low-canopy forest were fully understory plants (eight individuals). In both groups, the meristems of low-canopy forest individuals were at least 1 m below the Miconia canopy. Figure 4 shows that ferns in the low-canopy forest that place their blades in the canopy have growth rates similar to those of open habitat (P = 0.04). Conversely, individuals growing fully in the understory of the low- canopy forest have growth rates indistinguishable (P = 0.47) from those in the understory of the high-canopy forest. Average growth rates between the two subgroups of low-canopy ferns also differ statistically (P < 0.001).
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. Therefore, in forests where an individual tree fern may experience a variety of light environments during its lifetime, trunk height may be a poor estimation of an individual's age. Some authors have proposed trunk height as a useful proxy for age in demographic studies of tree ferns, (Seiler, 1981
; Bittner and Breckle, 1995
). This proxy seems useful only in a relative sense (taller co-occurring plants are older), when plants grow close together and are therefore likely to have experienced the same variation in light environment through time.
Leaf production
The average fern in open habitat produced a total of 21.3 new leaves during the course of the study (Fig. 5). Ferns in the understory of the high-canopy forest produced an average of 7.7 new leaves during the study, while the average fern in the low-canopy forest produced 14 new leaves. As with growth rate, there was a significant difference in rate of leaf production between open habitat and both closed-canopy forests (P < 0.001). High- and low-canopy forests also differed in leaf production rate (P = 0.001). However, as with growth rate, the low-canopy forest displayed greater variances due to the two strategies present there. Ferns in the low-canopy forest that placed their fronds in the canopy also showed leaf production rates indistinguishable from those of open-habitat individuals (P = 0.18), while fully understory individuals in the low-canopy forest resembled those in the understory of the high-canopy forest (P = 0.93).
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). This result highlights the notable interspecific variation in growth observed among Cyathea species.
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Spore production
This study did not evaluate either gametophyte establishment or sporophyte recruitment. Instead, I estimated reproductive potential by the rates of spore production (proportion of fertile plants per month in each habitat) across habitats. Figure 8 shows the percentage of ferns with at least one fertile leaf during each month of the study. The most striking result here is that only one individual (in February 1995) in the high-canopy forest produced spores during the 33 mo of observation. In contrast, an average 23% of plants in open habitat produced spores in an average month, with rates of 60% or greater in some months. In the low- canopy forest, significantly fewer (average 9%, P = 0.002) plants produced spores. As with growth and leaf production rate, there is a significant difference in spore production rate between plants in the low-canopy forest that place their blades in the canopy (an average of 12% fertile per month) and those living entirely in the understory (2% fertility; P < 0.001).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), to acclimatization of individuals to temporally changing conditions, or to intrapopulational adaptation to specific microsites (e.g., Dudley and Schmitt, 1995
). These competing hypotheses can only be distinguished with transplant experiments that move individuals from one microsite to another or by experiments that manipulate the physical environment experienced by individual plants. La Planada policy prohibits invasive experiments in the forest, and so neither transplants nor in situ environmental manipulations were possible. However, given the relatively short periods of time since pasture abandonment in both forested study sites, it seems unlikely that there has been sufficient time for the multi-generational selection that would be required to produce microsite adaptation. Therefore, any differences in performances observed are best attributed to either plasticity (sensu Bradshaw, 1965
) or acclimatization of individuals to a fluctuating environment.
My data show that Cyathea caracasana grows most rapidly, produces more leaves of shorter life span, and generates spores almost exclusively under conditions of full sun. In the Andes, this preferred sunny habitat may be found in human-altered environments such as abandoned pastures and roadsides. In natural mid-elevation forests, sunny habitats are characteristic of forest gaps. Individual plants may also track their preferred sunny habitat by producing long stipes, which place their fronds in a low canopy (Arens and Sánchez Baracaldo, 2000)
. When that strategy is no longer effective, growth and leaf production slow, and spore production ceases. Cyathea caracasana also does not recruit young sporophytes under a closed canopy at La Planada (Arens and Sánchez Baracaldo, 1998
). These results parallel those of Ortega (1984)
who reported that Sphaeropteris senilis (Klotzsch) R.M. Tryon [= Cyathea senilis (Klotzsch) Domin] had lower growth rates and no recruitment under closed canopy conditions in a Venezuelan cloud forest.
Together, these observations suggest a life history in which Cyathea caracasana adults produce spores and establish young sporophytes exclusively in sunny environments. When individuals begin to experience understory shade that they cannot escape through stipe elongation, they enter a "persistence mode" characterized by low growth rates, low leaf production rates, and longer lived leaves. Reproduction by spores is also curtailed. Ferns appear to be able to remain in persistence mode for relatively long periods. The high-canopy ferns in this study, for example, have probably persisted in the understory for >20 yr with no apparent mortality. (Because tree fern trunks resist decay, dead individuals are easy to locate in the forest.) Persistence mode may be triggered by a carbon shortage in the deep shade of the understory. In the absence of human disturbance, ferns remain in this persistence mode until a gap opens above them and they may begin another cycle of rapid growth, spore production, and recruitment. If a gap fails to open, however, plants may eventually die in the understory. Since C. caracasana is uncommon in the mature forest at La Planada, it seems likely that many individuals do die in the understory.
During the 33 mo of this study, I did not observe the opening of a canopy gap over understory individuals and so cannot directly document the increase in growth rate predicted to follow the change in light environment. In a location where long- term experimental manipulations would be possible, this portion of the life history hypothesis would be easy to test. However, anecdotal evidence from the mature forest at La Planada supports the role of gaps in the demographic dynamic of Cyathea caracasana. Cyathea caracasana is uncommon in mature forest; where it occurs, plants grow in clusters of four to ten individuals in two to four height classes (Arens and Sánchez Baracaldo, 1998
). Differing height classes within such clusters may represent cycles of recruitment during successive episodes of gap formation at that site. Without a way to age individual tree ferns independent of trunk height and leaf production, this interpretation remains provisional. However, if this interpretation of height cohorts in the mature forest is correct, it suggests that C. caracasana experiences cycles of growth and reproduction in the mature forest. Because the species grows well, produces spores, and recruits young sporophytes only under sunny conditions, it seems reasonable to infer that such cycles of growth and reproduction in mature forest individuals would be associated with gap formation.
This life history strategy appears to parallel the cycles of understory suppression and gap release described for some slow-growing temperate trees (Oliver and Stephens, 1977
). For these woody angiosperms, several cycles of suppression and release eventually allow individuals to reach the full sun of the canopy, the environment in which they reproduce. In contrast, tree ferns in the mid-elevation forest seldom reach the canopy under natural conditions and so are not using the gap cycle to reach their preferred sunny habitat. Instead, they may rely on the temporal distribution of gaps in space to maintain small natural populations. Such a life history relies on gaps opening above a given individual before it succumbs to light starvation in the understory. Therefore, this strategy would be effective only in those forests, like La Planada, with high canopy turnover rates. It is important to note, however, that we currently have no data on the length of time Cyathea caracasana individuals can persist in the understory, although individuals in the high-canopy secondary forest in this study have lived in subcanopy shade for at least 20 yr.
Cyathea caracasana is a member of the Neotropical Cyathea divergens clade (Fig. 9; Conant et al., 1995, 1996
). Basal members of this clade, Cyathea furfuracea Baker and Trichipteris pauciflora (Kuhn) R.M. Tryon [= Cyathea pauciflora (Kuhn) Lellinger], are restricted to "elfin" forests in Puerto Rico (Proctor, 1989
), and Venezuela and Colombia (Barrington, 1978
) respectively. In these high-elevation forests, tree ferns are reported to be a component of the canopy because woody angiosperms tend to be stunted. Cyathea caracasana, C. divergens Kunze, C. fulva (M. Martens & Galeotti) Fée, and C. delgadii Sternb. are montane forest species (Tryon, 1976
). Although few details of their life history and distribution are known, all of these except C. delgadii are reported to thrive in open areas and are less common in deep shade. In Bolivia, C. delgadii is more common in undisturbed forest but may persist along roadsides or in degraded forest (M. Kessler, A.-V. Haller-Institut fuer Pflanzenwissenschaften, Gottingen, Germany, personal communication, 2000). This suggests that sunny, open, or canopy habitats are the ancestral preference of members of this clade. The phylogenetic pattern suggests that C. caracasana's understory tolerance is derived from a narrower preference for sunny, canopy habitats. This conclusion is speculative because few detailed studies describing the habitat breadth of tree ferns have been performed. However, if correct, this conclusion is counter to the often-invoked principle that species with narrow habitat preferences are thought to evolve from generalists, which have a broader range of environmental tolerance from which natural selection can hone more specific habitat preferences (Mayr, 1942
; Simpson, 1984
; Kelley and Farrell, 1998
).
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). In contrast, the evolutionary specialist does well only in a narrow environmental range. By this definition, C. caracasana is better interpreted as an evolutionary specialist that has added something new—the "persistence phase"—to its life history. Therefore, C. caracasana's ability to survive in the understory of a closed canopy appears to be a derived trait that allows the sun-loving lineage to occupy montane forests where gaps are common and canopy turnover rates are high. This derived trait allows C. caracasana to exploit the temporal distribution of gaps in the montane forests and thus allows the lineage to occupy this forest type. Similar investigation of the life history and performance of other members of the Cyathea divergens clade across their habitat ranges is needed to further elucidate this pattern.
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FOOTNOTES |
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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———, and P. Sánchez Baracaldo. 1998 Distribution of tree ferns (Cyatheaceae) across the successional mosaic in an Andean cloud forest, Nariño, Colombia. American Fern Journal 88: 60–71[CrossRef]
———, and ———. 2000 Variation in tree fern stipe length with canopy height: tracking preferred habitat through morphological change. American Fern Journal 90: 1–15[CrossRef]
———, and A. R. Smith. 1998 Cyathea planadae, a remarkable new creeping tree fern from Colombia, South America. American Fern Journal 88: 49–59[CrossRef]
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Conant, D. S., L. A. Raubeson, D. K. Attwood, S. Perera, E. A. Zimmer, J. A. Sweere, and D. B. Stein. 1996 Phylogenetic and evolutionary implications of combined analysis of DNA and morphology in the Cyatheaceae. In J. M. Camus, M. Gibby, and R. J. Johns [eds.], Pteridology in Perspective, 231–248. Royal Botanic Gardens, Kew, UK
———, ———, ———, and D. B. Stein. 1995 The relationships of the Papuasian Cyatheaceae to New World tree ferns. American Fern Journal 85: 328–340[CrossRef]
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Ortega, M. F. J. 1984 Notas sobre la autecología de Sphaeropteris senilis (Kl.) Tryon (Cyatheaceae) en el Parque Nacional el Avila. Pittieria 12: 31–53
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———. 1987 Habitat selection as a source of biological diversity. Evolutionary Ecology 1: 315–330
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Seiler, R. L. 1981 Leaf turnover rates and natural history of the Central American tree fern Alsophila salvinii. American Fern Journal 71: 75– 81
———. 1984 Trunk length and frond size in a population of Nephelea tryoniana from El Salvador. American Fern Journal 74: 105–107
Simpson, G. G. 1984 Tempo and mode in evolution. Columbia University Press, New York, New York, USA
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