Ecophysiological Characteristics of Three Cyathea Species in Northeastern Taiwan

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Ecophysiological Characteristics of Three Cyathea Species in Northeastern Taiwan

Tzu-Yun Chiu,¹⁾ Hsiang-Hua Wang,²⁾ Yau-Lun Kuo,³⁾ Kume Tomonori,⁴⁾ Wen-Liang Chiou,⁵⁾ Yao-Moan Huang^1,6)

【Summary】

Tree ferns are conspicuous in subtropical and tropical rainforests. Some closely related species of tree ferns often coexist in the forest; however, the mechanisms are poorly understood. The ecophysiological characteristics of 3 tree ferns, Cyathea lepifera, C. spinulosa, and C. podophylla, growing in forests of northeastern Taiwan were investigated. Results showed that C. lepifera preferred an open habitat (mean canopy openness (MCO) of 29.2%), while C. spinulosa and C.

podophylla preferred a shaded habitat (MCOs of 7.0 and 5.0%, respectively). The light-saturated photosynthetic rate of C. lepifera was significantly higher than that of C. podophylla, and C. spinu- losa had a medium one (11.46, 8.27, and 6.34 μmol CO2 m^-2 s^-1 for C. lepifera, C. spinulosa, and C.

podophylla, respectively). The light saturation point of C. podophylla was significantly lower than those of the other 2 species (1220, 1100, and 808 μmol photon m^-2 s^-1 for C. lepifera, C. spinulosa, and C. podophylla, respectively). The light compensation point (LCP) and dark respiration rate (Rd) of C. lepifera were significantly higher than those of C. spinulosa and C. podophylla. Cyathea lepifera had the shortest frond life spans (6.6 mo for fertile fronds and 7.2 mo for sterile fronds) among the 3 species, which was followed by those of C. spinulosa (7.2 mo for fertile fronds and 7.3 mo for sterile fronds), and the longest frond life spans were in C. podophylla (13.0 mo for fer- tile fronds and 12.0 months for sterile fronds). Cyathea lepifera, C. spinulosa, and C. podophylla respectively belonged to shade-intolerant species, mid-shade-tolerant species, and shade-tolerant species as inferred from their habitat preference and ecophysiological characteristics. Roads, trails, frequent typhoons, and occasional tree falls create habitats with different canopy openness levels which increase the opportunity of these 3 Cyathea species to coexist in this forest.

1)Division of Silviculture, Taiwan Forestry Research Institute, 53 Nanhai Rd., Taipei 10066, Taiwan.

林業試驗所育林組，10066台北市南海路53號。

2)Fushan Research Center, Taiwan Forestry Research Institute, 1 Fushan, Shuangpi Rd., Huxi Vil., Yuanshan Township, Yilan 26445, Taiwan. 林業試驗所福山研究中心，26445宜蘭縣員山鄉湖西村雙埤路福山1號。

3)Department of Forestry, National Pintung Univ. of Science and Technology, 1 Xuehfu Rd., Neipu Township, Pintung 91201, Taiwan. 國立屏東科技大學森林系，91201屏東縣內埔鄉學府路1號。

4)School of Forestry and Resource Conservation, National Taiwan Univ., 1 Roosevelt Rd., Sec. 4, Taipei 10617, Taiwan. 國立台灣大學森林環境暨資源學系，10617台北市羅斯福路四段1號。

5)Division of Boranical Garden, Taiwan Forestry Research Institute, 53 Nanhai Rd., Taipei 10066, Taiwan. 林業試驗所植物園組，10066台北市南海路53號。

6)Corresponding author, e-mail:huangym@tfri.gov.tw 通訊作者。

Received May 2015, Accepted June 2015. 2015年5月送審 2015年6月通過。

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Key words: canopy openness, Cyathea lepifera, Cyathea podophylla, Cyathea spinulosa, frond life span.

Chiu TY, Wang HH, Kuo YL, Tomonori K, Chiou WL, Huang YM. 2015. Ecophysiological char- acteristics of three Cyathea species in northeastern Taiwan. Taiwan J For Sci 30(3):147-55.

研究報告

台灣東北部三種桫欏屬植物之生態生理特性

邱子芸¹⁾ 王相華²⁾ 郭耀綸³⁾ 久米朋宣⁴⁾ 邱文良⁵⁾ 黃曜謀^1,6)

摘要

樹蕨為亞熱帶及熱帶雨林中顯著物種，一些近緣樹蕨常在森林中共存，然而，其共存機制鮮為瞭解。本研究調查生長在台灣東北部森林筆筒樹、台灣桫欏與鬼桫欏三種樹蕨生態生理特性。結果顯示筆筒樹偏好生長於開闊生育地(平均樹冠開闊度29.2%)，而台灣桫欏與鬼桫欏則偏好生長於鬱閉生育地 (平均樹冠開闊度分別為7.0及5.0%)。筆筒樹光飽和光合作用速率顯著高於鬼桫欏，台灣桫欏居中(筆筒樹、台灣桫欏及鬼桫欏分別為11.46, 8.27及6.34 μmol CO2 m^-2 s^-1)；鬼桫欏光飽和點顯著低於其它兩物種(筆筒樹、台灣桫欏及鬼桫欏分別為1220, 1100及808 μmol photon m^-2 s^-1)；筆筒樹的光補償點與暗呼吸率顯著高於台灣桫欏及鬼桫欏。另外，此三種物種以筆筒樹具最短之葉片壽命(孕性葉6.6月，營養葉7.2月)，台灣桫欏其次(孕性葉7.2月，營養葉7.3月)，鬼桫欏之葉片壽命則為最長(孕性葉13.0月，營養葉12.0月)。根據它們的棲地偏好及生態生理特性，筆筒樹、台灣桫欏及鬼桫欏分別屬於非耐陰性物種、中度耐陰性物種及耐陰性物種。道路及步道、頻繁颱風干擾和偶發性樹倒創造出不同樹冠開闊度棲地，提昇這三種桫欏屬植物共存在此一森林中的機會。

關鍵詞：樹冠開闊度、筆筒樹、鬼桫欏、台灣桫欏、葉片壽命。

邱子芸、王相華、郭耀綸、久米朋宣、邱文良、黃曜謀。2015。台灣東北部三種桫欏屬植物之生態生理特性。台灣林業科學30(3):147-55。

INTRODUCTION

Tree ferns are conspicuous components of subtropical and tropical mountain rainforests, sometimes making a large contribu- tion to the total basal area and stem density (Bystriakova et al. 2011). They have been recognized as a ‘‘keystone species’’ because their dense crowns act as filters on tree regen- eration processes (Coomes et al. 2005, Bystri- akova et al. 2011). Although closely related species of tree ferns often coexist in the forest (Jones et al. 2006), the mechanisms that enable local coexistence are poorly understood.

In a heterogeneous environment, the availability of resources for plants to success- fully survive and develop may change with time or microsites (Durand and Goldstein 2001a). Those environmental factors, includ- ing light, water, and nutrients, vary at different canopy openness levels even in a small forest area.

Heterogeneity of light environments can influence the photosynthesis of plants by means of a direct effect on the photosynthetic apparatus. However, plants can be damaged

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by photooxidative destruction under stress conditions (Valladares and Pearcy 1997, Saldaña et al. 2010). Plants growing at low light levels tend to have a lower photosynthetic capacity, light compensation point (LCP) and dark respiration rate (Rd) than those growing in sunny conditions (Björkman et al. 1972). Shade tolerance is a product of a combination of traits that enable plants to maintain a positive carbon balance in deep shade. Plants’ growth is influenced by the rate of photosynthesis and by the costs of leaf Rd

and leaf construction (Givnish 1988). Having a lower Rd is advantageous for plants growing in the shade, because it may help them maintain a positive carbon balance under low light conditions (Boardman 1977).

Different species of tree ferns under various light environments may have distinct ecophysiological characteristics, e.g., photosynthetic rate and Rd (Pattison et al. 1998, Durand and Goldstein 2001a, Bystriakova et al. 2011). Jones et al. (2007) discovered that habitat preferences of 4 common tree fern species (Cyatheaceae) in a lowland neotropi- cal rainforest were strongly associated with different sheltered topographic positions such as terraces or valleys. Therefore, exploring the explicit ecophysiological characteristics of tree ferns under different light environments is essential to understanding physiological adaptations to their habitats.

Many studies have shown that the life span of leaves is negatively correlated with the photosynthetic rate in gymnosperms, angiosperms, and some ferns. Species with higher photosynthetic rates usually have shorter leaf life spans than those with lower photosynthetic rates (Durand and Goldstein 2001b, Matsuki and Koike 2006, Karst and Lechowicz 2007). However, correlations among the above ecophysiological characteristics of leaves have been widely reported in

angiosperms but less so in ferns (Karst and Lechowicz 2007).

The Cyatheaceae is the main family among tree ferns. There are 7 species of this family native to Taiwan. Among these spe- cies, Cyathea lepifera (J. Sm. ex Hook.) Copel., C. spinulosa Wall. ex Hook., and C.

podophylla (Hook.) Copel. are common and often sympatrically distributed in subtropical broadleaf forests of northeastern Taiwan.

In this study, we first elucidated differences in their habitat preferences, and then docu- mented relationships among habitat preferences, ecophysiological characteristics, and life spans of fronds in these tree ferns.

MATERIALS AND METHODS Study area

Plants of C. lepifera, C. spinulosa, and C.

podophylla which grew in a subtropical broa- dleaf forest at an elevation of about 600 m in the Fushan Botanical Garden in northeastern Taiwan (24°46’N, 121°34’E) were monitored monthly from March 2011 to March 2013.

Canopy openness

The canopy openness of sampled tree ferns was measured in July and August, 2012.

A digital, hemispherical photograph was taken at about 0.5 m above each individual plant using a Cannon EOS 400 digital camera with a fisheye lens attachment. Images were then analyzed using Gap Light Analyzer software (Frazer et al. 1999, Watkins Jr. et al. 2007) to estimate the percentage of total light transmit- tance. There were 13, 21, and 21 samples of C. lepifera, C. spinulosa, and C. podophylla, respectively. (Table 1).

Measurement of photosynthetic light re- sponses

In situ photosynthetic light responses of

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the 3 tree ferns were measured in February 2012. Three sampled fronds each from different individuals of the 3 species were chosen for measurements. The sampled fronds of C.

lepifera and C. spinulosa were 4 m above the ground, and those of C. podophylla were 1 m above the ground. Portable construction platforms were used to access the sampled fronds for the photosynthetic measurements.

Net photosynthetic rates were measured with a portable photosynthesis system (LI-6400, LI-COR, Lincoln, NE, USA) with an artificial red/blue LED light source. Measurements were made at light levels (photosynthetic photon flux density; PPFD) of 0, 5, 10, 25, 50, 100, 200, 400, 600, 800, 1000, 1200, 1400, 1600, 1800, and 2000 μmol photon m^-2 s^-1. The leaf chamber environment was maintained as follows: CO2 of 400 μl L^-1, a temperature of 22℃, and a relative humidity of 65~70%.

Measurements were taken from 08:00~11:00 under clear to partly cloudy skies. The value of 95% of the highest net photosynthetic rate (Amax) of each light response was regarded as the light-saturated photosynthetic rate (Asat).

For each light response, the corresponding light intensity of the Asat was regarded as the light saturation point (LSP). The LCP and Rd were calculated from a linear regres- sion equation of the light intensity below 50 μmol photon m^-2 s^-1. The corresponding light

intensity at a zero net photosynthetic rate of each light response was the LCP. The net photosynthetic rate in the dark was the Rd. Frond life span

Thirty plants of C. lepifera, and 40 plants each of C. spinulosa and C. podophylla were selected in this study. All fronds of selected plants were labeled with plastic tags. Their fertility and development stages from emergence and expansion to death were investigated monthly from March 2011 to March 2013.

Therefore, the frond life span was calculated based on the timing of fronds from emergence to senescence (Lee et al. 2009b).

Statistical analysis

A two-way analysis of variance (two-way ANOVA) followed by Scheffe’s method and Duncan’s multiple-range test were carried on to determine differences among species and fronds for each variable measured. All statistical analyses were run using Microsoft Office Excel 2007 (Microsoft, Inc. 2007) and SPSS Statistics program 16.0 (SPSS, Inc. 2007).

RESULTS

Habitat and canopy openness

Cyathea lepifera, C. spinulosa, and C.

podophylla are abundant and often sympatri- cally distributed in this study area. However, the mean canopy openness above C. lepifera was significantly greater than those of C.

spinulosa and C. podophylla (29.9, 7.0, and 5.0%, respectively) (Table 1). According to our field observations, C. lepifera mainly ap- peared in open habitats. In contrast, C. spinu- losa and C. podophylla were dominant in shaded habitats.

Photosynthesis

The net photosynthetic rate increased Table 1. Forest canopy openness ( ) above

plants of Cyathea lepifera, C. spinulosa, and C. podophylla

Species Number Canopy of plants openness (s) Cyathea lepifera 13 29.9±14.1^a Cyathea spinulosa 21 7.0±3.7^b Cyathea podophylla 21 5.0±2.2^b Different superscript letters indicate a signifi- cant difference (by Scheffe’s test, p < 0.05) among species.

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with increasing PPFD from dark to the light saturation point. The LCP of C. lepifera (6.77±1.25 μmol photon m^-2 s^-1) was sig- nificantly higher than those of C. spinulosa (2.21±0.44 μmol photon m^-2 s^-1) and C. podo- phylla (1.88±0.37 μmol photon m^-2 s^-1). The LSP was estimated to be about 1220, 1100, and 808 μmol photon m^-2 s^-1 for C. lepifera, C. spinulosa, and C. podophylla, respectively.

The LSPs of the former 2 species were sig- nificantly higher than that of C. podophylla.

Asat values of C. lepifera, C. spinulosa, and C. podophylla were 11.46±1.34, 8.27±0.69, and 6.34±0.54 μmol CO2 m^-2 s^-1, respectively. Rd values of C. lepifera, C. spinu- losa, and C. podophylla were 0.56±0.06, 0.17±0.02, and 0.30±0.08 μmol CO2 m^-2 s^-1, respectively. The Rd of C. lepifera was significant higher than those of the other 2 species, but there were no significant differ- ence between C. spinulosa and C. podophylla (Table 2).

Frond life span

Totally 433 C. lepifera, 371 C. spinulosa, and 79 C. podophylla fronds were examined from emergence to senescence. The mean life spans of both fertile and sterile fronds of C.

podophylla (13.0 and 12.5 mo, respectively) were significantly longer than those of C.

lepifera (6.6 and 7.2 mo, respectively) and C.

spinulosa (7.2 and 7.3 mo, respectively). In C.

lepifera, the life span of fertile fronds was sig- nificantly shorter than that of sterile fronds although with only a half-month difference. Life spans of fertile and sterile fronds did not differ in C. spinulosa or C. podophylla (Table 3).

DISCUSSION

Habitat and photosynthetic characteristics Cyathea lepifera has long been regarded as a shade-intolerant tree fern and often re- generates in disturbed sites (e.g., Tsai et al.

2001). In contrast, C. podophylla is attributed Table 2. Light-saturated photosynthetic rate (Asat), light saturation point (LSP), light compensation point (LCP), and dark respiration rate (R_d) of Cyathea lepifera, C. spinulosa, and C. podophylla

C. lepifera C. spinulosa C. podophylla Asat (μmol CO2 m^-2 s^-1) 11.46±1.34â 8.27±0.69âb 6.34±0.54^b LSP (μmol photon m^-2 s^-1) 1220±68â 1100±33â 808±80^b LCP (μmol photon m^-2 s^-1) 6.77±1.25â 2.21±0.44^b 1.88±0.37^b Rd (μmol CO2 m^-2 s^-1) 0.56±0.06â 0.17±0.02^b 0.30±0.08^b Different superscript letters on the same line indicate a significant difference (by Duncan’s multiple- range test, p < 0.05) among the 3 Cyathea species.

Table 3. Life spans (mo) of fertile and sterile fronds of Cyathea lepifera, C. spinulosa, and C.

podophylla

Species Life span (no. of fronds)

Fertile fronds Sterile fronds Cyathea lepifera 6.6±1.3^a (277) 7.2±1.4^b (156) Cyathea spinulosa 7.2±1.5^b (128) 7.3±1.9^b (243) Cyathea podophylla 13.0±5.1^c (34) 12.5±5.0^c (45)

Different superscript letters indicate a significant difference (by Scheffe’s test, p < 0.05) among spe- cies and frond fertility.

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to a shade-tolerant species (e.g., Wang et al.

2003). Cyathea lepifera and C. podophylla are often respectively found in open and shaded habitats in this study area. On the other hand, although C. spinulosa usually occurred at intermediate sites, its canopy openness significantly differed from that of C.

lepifera and was slightly higher than that of C.

podophylla.

The Asat, LSP, LCP, and Rd of shade- intolerant and early-successional species are higher than those of shade-tolerant and late- successional species (Bazzaz 1979, Sumbele et al. 2012). This generality is widely accepted in flowering plants. This study documents that C. lepifera had a higher Asat, LSP, LCP, and Rd than those of C. podophylla, whereas C. spinulosa possessed intermediate values of these photosynthetic characteristics except for Rd. Many studies concerning frond ecophysiology of ferns mostly coincided with this generality. For example, in Hawaii, the LSP and Amax of the invasive tree fern Sphaeropt- eris cooperi (W. J. Hooker ex F. von Mueller) Tryon, which grows at relatively high light levels, are significantly higher than those of the 3 native Cibotium tree ferns (C. chamissoi Kaulf., C. menzeissi Hook., and C. glaucum (Sm.) Hook. & Arn.), which live in shaded habitats. However, the light compensation points did not statistically differ between the 2 groups of ferns (Durand and Goldstein 2001a).

In general, tropical shade-intolerant and shade-tolerant trees have Asat values within 10~20 and 4~7 μmol CO2 m^-2 s^-1, respectively (Larcher 1995, Strauss-Debenedetti and Baz- zaz 1996, Zotz and Winter 1996). According to this criterion, C. lepifera, and C. podo- phylla belong to shade-intolerant species and shade-tolerant species, respectively; and C.

spinulosa should be regarded as a mid-shade- tolerant species because of having an interme-

diate Asat value between shade-intolerant and shade-tolerant species.

A plant with a greater photosynthetic capacity as presented by the Amax, indicates that it is more efficient at utilizing light energy and/or has more carboxylating enzymes, under a high light intensity (Durand and Gold- stein 2001a). In Hawaii, the tree fern Spha- eropteris cooperi, which grows at relatively high light levels, has a significantly higher annual stem growth rate (15 cm) than 3 tree ferns in the genus Cibotium (2~3 cm) which live in shaded habitats (Durand and Goldstein 2001b). The mean annual stem height growth of C. lepifera is ca. 22 cm in a northeastern forest of Taiwan (Ying and Huang 1995), whereas that of C. podophylla is < 5 cm in a forest of central Taiwan (unpublished data).

For those species in this study, C. lepifera is proposed to grow faster than the other 2 species due to its higher Asat value.

It was suggested that the shade-tolerant species in low light environments still maintain growth because they have lower respiration rates and can use light resources more efficiently, whereas shade-intolerant species might not grow and have high mortality rates under low light levels (Givenish 1988, Wal- ters and Reich 1996). A similar scenario may also occur for tree ferns of this study and ex- plain their different habitat selections.

Forest roads and trails, frequent typhoons, and occasional tree falls create different gaps in the Fushan forest and provide various habitats for corresponding species to establish populations (Lin et al. 2006). These habitats with various canopy openness levels have a mosaic distribution and promote the coexistence of these 3 ferns with different ecophysiological characteristics in this forest.

Frond life span

In ferns, fertile fronds are expected to

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have a shorter life than sterile fronds because their reduced laminar surface makes them less photosynthetically efficient than sterile fronds (Mehltreter 2008). This was proven for dimorphic species in which fertile and sterile fronds distinctly differ in outline and size, but this generality does not always fit monomorphic fern species (Lee et al. 2009a, b).

In this study, fronds of all 3 Cyathea species belonged to the monomorphic type. The life span of sterile fronds was significantly lon- ger than fertile ones in C. lepifera (although only a half-month difference). However, life spans of both kinds of fronds were nearly the same in C. spinulosa and C. podophylla. The average life spans of fertile and sterile fronds were up to 26.1 and 25.8 mo in C. podophylla (Lee et al. 2009b), which were much longer than the life spans of C. podophylla fronds in this study. This may be attributed to the shorter observation period (2 yr), to only 28.5%

(79/277) of total fronds being observed from emergence to senescence, and to serious dam- age by squirrels and fungal infections in this study.

Variations in leaf life span were found to be an important predictor of numerous plant responses (Mehltreter 2008). In general, leaves of angiosperms and ferns with a higher photosynthetic ratehave a shorter leaf life span than those with a lower one (Reich et al. 1991, 1999, Durand and Goldstein 2001a, Craine et al. 2002, Matsuki and Koike 2006, Karst and Lechowicz 2007). The same ten- dency was observed among C. lepifera, C.

spinulosa, and C. podophylla. Several stud- ies demonstrated that species with long-lived leaves have higher costs (maintenance and defense) and fewer benefits (photosynthesis) than those with short-lived leaves (Chapin et al. 1980, Coley 1988, Reich et al. 1995). That is, in addition to the photosynthetic rate, the leaf life span is also associated with other leaf

functional traits such as the leaf nitrogen con- tent, leaf construction cost, and leaf mass per area (Matsuki and Koike 2006).

CONCLUSIONS

Cyathea lepifera, C. spinulosa, and C.

podophylla are 3 common and often sym- patric tree ferns in forests of northeastern Taiwan. They are classified as shade-intolerant, mid-shade-tolerant, and shade-tolerant species, respectively, as inferred from their habitat preferences and photosynthetic characteristics. Forest roads and trails, frequent typhoons, and occasional tree falls create habitats with different canopy openness lev- els. Hence, the 3 Cyathea species can coexist under various effective light resources of their habitats.

ACKNOWLEDGEMENTS

This work was supported by the Taiwan Forestry Research Institute (102AS-13.1.6- F1-G6 and 102AS-13.3.7-F1-G2).

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