Indian Fern J. 36 : 133-153 (2019) ISSN 0970-2741
PHENOLOGY AND LEAF LIFESPAN OF AN ENDANGERED FERN
ANGIOPTERIS SOMAE (MARATTIACEAE)
YAO-MOAN HUANG, PEI-HSUAN LEE AND WEN-LIANG CHIOU*
Taiwan Forestry Research Institute, Taipei City 10066, Taiwan
(Received December 10, 2018; Revised Accepted July 6, 2019)
A B S T R A C T
A n g i o p t e r i s s o m a e ( H a y a t a ) M a k i n o & N e m o t o i s a n e n d e m i c a n d e n d a n gere d fern i n Ta i wa n . We i nve s t i ga t e d m o n t h ly t h e p h e n o l og y o f p o p u l a t i o n o f t h i s fe r n t h a t wa s l o c a t e d i n m i d d l e Ta i wa n f ro m J a n u a r y 2 0 0 2 t o D e c e m b e r 2 0 0 8 .
R e s u l t s s h ow e d t h a t A . s o m a e i s a p e r e n n i a l f e rn , a n d a l l s a m p l e d p l a n t s s u r v ive d a c r o s s t h e s t u d y p e r i o d . F e r t i l e l e a v e s ( 9 8 % ) m o s t l y e m e r g e d d u r i n g s p r i n g a n d e a r l y s u m m e r ( M a r c h t o J u n e ) . T h e y r e l e a s e d s p o r e s m a i n l y ( 8 6 % ) i n w i n t e r
( D e c e m b e r t o F e b r u a r y ) i n c o n t r a s t t o t h e s u m m e r - a u t u m n r e l e a s e p a t t e r n o f m o s t t ropical fer ns. On the other hand, most sterile leaves (91%) emerged during A pril to
S e p t e m b e r. T h e n u m b e r o f e m e rg i n g f e r t i l e l e ave s , u s e d t o r e p r e s e n t t h e e m e rg e n t s e a s o n a l i t y, d i d n o t c o r r e l a t e w i t h m o n t h l y p r e c i p i t a t i o n ( M P ) , t e m p e r a t u r e ( M T ) , a n d d a y l e n g t h ( M D ) , w h i l e s t e r i l e l e a v e s h a d s i g n i f i c a n t c o r r e l a t i o n w i t h t h e s e t h r e e e n v i r o n m e n t a l f a c t o r s . T h e c o r r e l a t i o n o f t h e m o n t h l y n u m b e r o f s p o r e releasing leaves was significantly negative with respect to MT and MD, but not with r e s p e c t t o M P. T h e m e a n a n n u a l n u m b e r o f e m e rg e n t l e av e s p e r p l a n t w a s 1 . 9 7 , w h i c h i s l o w c o m p a r e d t o o t h e r f e r n s t u d i e s . L e a f s e n e s c e n c e m a i n l y o c c u r r e d f r o m
A p r i l t o S e p t e m b e r i n a s i g n i f i c a n t l y s e a s o n a l p a t t e r n w i t h 8 5 . 7 % f e r t i l e a n d 7 2 . 7 % s t e r i l e l e a v e s s e n e s c i n g i n t h i s p e r i o d . T h e n u m b e r s o f s e n e s c e n t f e r t i l e l e a v e s s i g n i fi c a n t l y c o r r e l a t e d w i t h M P, M T, a n d M D , w h e r e a s s t e r i l e l e av e s o n l y s i g n i fi c a n t l y c o r re l a t e d w i t h M P a n d M T, n o t M D. T h e m e a n c o u n t o f l iv i n g l e ave s p e r p l a n t r a n g e d f r o m a l o w o f 4 . 6 4 ( F e b r u a r y ) t o a h i g h o f 5 . 5 6 ( M a y ) , a s e a s o n a l pattern that had significant correlation with MP, MT, and MD. Leaves of Angiopteris somae had long leaf lifespans. The mean lifespans of sterile and fertile leaves were
4 0 . 7 a n d 2 5 . 6 m o n t h s r e s p e c t i v e l y b a s e d o n d i r e c t o b s e r v a t i o n ; 5 3 . 3 m o n t h s a n d
2 3 . 8 m o n t h s r e s p e c t iv e l y e s t i m a t e d b y t u r n ov e r r a t e . A l t h o u g h t h i s s p e c i e s i s c a t e g o r i z e d a s m o n o m o r p h i c d u e t o t h e s i m i l a r m o r p h o l o g y o f i t s f e r t i l e a n d s t e r i l e l e a v e s , t h e t i m i n g o f p h e n o p h a s e s a n d l i f e s p a n s o f t h e s e t w o t y p e s o f l e a v e s a r e s i g n i f i c a n t l y d i f f e r e n t . E l e v e n t y p h o o n s a t t a c k e d t h i s s t u d i e d a r e a i n f i v e o f s e v e n m o n i t o r i n g y e a r s . T h e e f f e c t o f t y p h o o n s o n p h e n o l o g i c a l t r a i t s o f t h i s s p e c i e s i s s t at e d a n d d i s c u s s e d . T h i s s t u d y, d e m o n s t r a t e s t h a t a l l m o n i t o re d p h e n o p h a s e s h ave s i g n i f i c a n t s e a s o n a l i t y a n d w i n t e r i s t h e b e s t t i m e o f y e a r t o h a r v e s t m a t u r e s p o r e s o f t h i s e n d a n g e r e d s p e c i e s f o r c u l t u r i n g a n d ex-situ conservation.
Ke y Wo r d s : C i r c u l a r s t a t i s t i c s , L e a f e m e r g e n c e , L e a f s e n e s c e n c e , S p o r e release, Seasonality, Taiwan
INTRODUCTION
Studies of plant phenology identify the timing and duration of specific plant growth and fertility responses to seasonal changes in such climate factors as temperature, rainfall,
Corresponding author E-mail : * chiouwl@gmail.com

134 Indian Fern Journal Volume XXXVI (2019) and daylength. Such observations can also be used for elucidating the ecological and reproductive biology of a plant species (Newstrom & Frankie 1994, Mehltreter 2008). This kind of study also provides helpful knowledge for plant conservation but is often neglected and less practically applied, especially for ferns.
The phenology of ferns is most strongly affected by abiotic factors because of their independence from pollinations and dispersers (Wagner & Gómez 1983). Most ferns display seasonal phenological patterns. The occurrences of their phenophases are usually correlated with climatic conditions that ensure the population survival and regeneration (Mehltreter
2008). Fern phenology has been increasing explored in recent decades (reviewed in Lee et al. 2018). However, most fern phenological studies were conducted over a relatively short time span (e.g., one to three years), and thus long-term phenological information is less available. A long-term phenological study provides an opportunity to explore unexpected implications and make intriguing discovery (Halleck et al. 2004) for that can lead to further studies and/or hypothesis proposals, especially for those ferns with long-lived leaves. In fact, a long-term phenological study could offer much valuable information on survival, annual variation of phenophases, the impact of external climatic factors
(Morellato et al. 2000), including natural disturbance such as hurricane (Sharpe 2010,
Sharpe & Shiels 2014), and suitable collecting spore season for fern species (Odland 1995;
Ying & Huang 1995). All of these data are basic knowledge that is necessary for the conservation of threatened ferns.
For ferns, leaves are their main photosynthetic as well as spore producing organs.
Thus, ferns’ leaf lifespans (LLS) have relevant impacts on their sporeling recruitment and population fluctuation. Mehltreter and Sharpe (2013) compare documented LLS of 71 fern species, but most of those data do not distinguish fertile LLS from sterile ones, and that might lead to a deviated conclusion (Lee et al. 2018). Differences between fertile and sterile leaves not only appear in LLS but also in the phenophases (Nagano & Suzuki 2007), especially of dimorphic ferns (Sharpe & Jernstedt 1990, de Paiva Farias et al. 2018).
However, the distinction of this “behavior”, as mentioned by Wagner & Wagner (1977), is seldom recognized in monomorphic ferns (see examples in Lee et al. 2018).
Angiopteris somae (Hayata) Makino & Nemoto (= Archangiopteris somai Hayata) is a long-lived monomorphic fern that grows on shady moist soils in low-elevation forests
(Plates 1 & 2). It is endemic to Taiwan, sparsely distributed with less than 1000 mature plants, and is categorized as endangered based on the criteria of IUCN (2003) (Wang et al.
2012). Its phenological traits have never been studied before.
Because circular statistics could calculate phenological variables, such as the mean occurrence date and concentration degree of a phenophase (divergence from a random or uniform distribution) (Morellato et al. 2010), this method can get a fair interpretation for a species growth and is applied to analyze the phenological data in this study. We conducted a long-term (7 years) phenological survey on A. somae 1) to monitor variations in

Yao-Moan Huang et al. : Phenology & Leaf Lifespan of an Endangered Fern Angiopteris somae (Marattiaceae) 137 phenophase seasonality and leaf lifespan and differences between those of fertile and sterile leaves, 2) to explore influences of typhoon on phenophases, 3) to analyze the correlation of phenophases with environmental factors, and 4) to identify a time of year most suitable for spore harvesting to facilitate propagation and ex situ conservation of this threatened species.
Study site and investigation
MATERIALS AND METHODS
The study site was located in a shady valley under a subtropical broadleaf forest, which is managed by the Lienhuachih Research Center (LRC) of Taiwan Forestry Research
Institute in central Taiwan (23°55’43'’ N, 120°54’00'’E, alt. ca. 680 m). The forest is dominated by trees in the Fagaceae and Lauraceae families.
Ten plants of A. somae were sampled. All leaves were labeled with a small plastic tag when they had emerged and expanded to ca. 1 cm tall. Five phenophases i.e., emergence and senescence of both fertile and sterile leaves and spore release, were observed early in every month (1 st –10 th day of each month) from January 2002 to December 2008. In addition, the size and the number of pinnae of fully expanded leaves were recorded. Leaf lifespans
(LLS) were determined by direct observation from their emergence to senescence (when a leaf totally turned brown) and by indirect estimate from leaf turnover rate (LLS = (the mean annual number of living leaves / the mean number of emergent leaves per year) ×12 month; Seiler 1981, Tanner 1983).
Emergence of the fern leaf was signaled by the appearance of a coiled leaf (crozier) that then took one to two months to fully expand. Leaf senescence was the end process of leaf growth, when leaf turned brown. Degree of sporangium openness was used to represent spore release, i.e., ca. 5% of sori having open sporangia indicates the start of spore release.
Although a leaf may release spores for a span of up to three months, the spore release dates in this study reflect the start of that release period and indicate the time of spore complete maturation.
Environmental data
Environmental data were obtained from the LRC weather station (23°55’07'’ N,
120°53’07'’E, alt. 681m), ca 1.8 km away from the study site. Annual precipitation varied every year during the study period and ranged from 1,410 to 4,302 mm with a mean of
2,672 mm. Eleven typhoons attacked this area during this study period (Table 1). The annual precipitation showed a significantly positive correlation with the number of typhoons
( r = 0.88**). All typhoons attacked during July to September in different years. The mean annual temperature was 19.9–20.5°C with a mean of 20.1°C, with min/max monthly mean temperatures of 14.5/24.4°C (January/July). Mean annual day length was 12.2 hrs, with a maximum monthly value in June (13.6 hrs) and a minimum in January (10.8 hrs). The season classification follows Walter et al. (1975). Perhumid season, with monthly precipitation more than 100 mm, appeared in April to September. Other months belong to

138 Indian Fern Journal Volume XXXVI (2019)
TABLE 1 : The mean annual temperature, accumulative precipitation and typhoon in Lienhuachih area during the study period
Year
2002
2003
2004
2005
2006
2007
2008
Average
Temperature ( 0 C) Precipitation (mm) Ty p h o o n
20.4
1410.0
20.3
20.0
19.9
20.4
1622.3
2656.5
2721.4
3067.4
Mindulle
Haitang, Matsa, Talim
Ewiniar; Bilis
20.1
19.9
20.1
2924.5
4302.5
2672.1
Sepat
Kalmaegi, Fung-Wong, Sinlaku, Jangmi relative humid season, of which the monthly precipitation is less than 100 mm but more than the predicted evaporation, i.e., mean monthly temperature*2. Dry season, with monthly precipitation less than 100 mm and less than the predicted evaporation, did not occur during typhoon years but was present in non-typhoon years (February and November,
2002–2003) (Fig. 1).
Data analysis
For circular statistics each monitoring date was first assigned to a Julian day: e.g.,
1 st Jan = 1 day; 31st Dec = 365 or 366 days, depending on whether it was a common year or leap year. Then the formula of Zar (2010) was used for calculating the corresponding angular direction.
a = ((360°)(X)) / k where a = angular direction, X = Julian days, k =365 (or 366 in leap year)
Then circular statistics were used to calculate the mean angle a (= mean of angular direction) and vector r . Length of vector r , a measure of concentration approaching the mean angle, has no unit and varies from 0 (when occurrence times of phenophases are distributed uniformly throughout the year) to 1 (when occurrence times are concentrated at one single date). Rayleigh test was used to detect the significance of vector r (Morellato et al. 2000, 2010). The Watson-Williams test (F) was performed (Kanji 2006) to compare the mean angles a of occurrence times of phenophases between sterile and fertile leaves
(methods see Morellato et al. 2000, 2010).
Because phenophases were observed at different times rather than angles, the mean angle was converted to a corresponding date (Zar 2010). Pearson product-moment correlation coefficient was used to test correlations ( r) between the timings of phenophases
(indicated by leaf numbers of occurrence) and environmental data.

Yao-Moan Huang et al. : Phenology & Leaf Lifespan of an Endangered Fern Angiopteris somae (Marattiaceae) 139
RESULTS
Emergence of leaves
A total of 138 new leaves, including 64 fertile and 74 sterile ones, emerged during the 7 years for the 10 monitored plants at a mean rate of 1.97 leaves plant -1 year -1 . Mean annual production of leaves varied from year to year and ranged from 1.40 (2003) to 2.70
per plant (2008) (Table 2).
Different numbers of new leaves emerged in all months except January and
February when none appeared. Almost all fertile leaves (98%) emerged during March to
June, whereas most sterile leaves (91%) emerged during April to September (Fig. 2a).
Emergence dates of both fertile and sterile leaves were seasonal, with mean dates on 17
April (vector r = 0.90
** ) and 30 June (vector r = 0.55
** ), respectively, and were significantly different (Table 3).
TABLE 2 : Annual leaf numbers of different phenophases per plant in A n g i o p t e r i s s o m a e . F= f er tile leaf; S= sterile leaf.
Year
Emergence S e n e s c e n c e L i v i n g
F S Sum F S Sum F S Sum
2002 0.60
1.30
1.90
2.20
1.00
3.20
1.78
2.38
4.16
2003 0.90
0.50
1.40
0.90
1.10
2.00
1.28
2.53
3.81
2004 0.30
2.10
2.40
0.70
0.30
1.00
0.68
2.96
3.64
2005 0.60
1.50
2.10
0.20
1.30
1.50
0.98
3.97
4.95
2006 0.90
0.90
1.80
0.20
0.40
0.60
1.56
4.31
5.87
2007 1.10
0.40
1.50
0.20
1.20
1.40
2.38
4.16
6.54
2008 2.00
0.70
2.70
1.20
1.30
2.50
3.43
3.48
6.91
Mean 0.91
1.06
1.97
0.80
0.94
1.74
1.73
3.40
5.13
R e l e a s i n g s p o r e s
1.10
0.40
0.10
0.50
0.30
0.50
1.40
0.61
TA B L E 3 : D a t a o f c i r c u l a r a n a l y s i s o f s e a s o n a l i t y i n A n g i o p t e r i s s o m a e . n f
= n u m b e r o f f e r t i l e l e a v e s , n s
= n u m b e r o f s t e r i l e l e a v e s , a = m e a n a n g l e , r = v e c t o r r , c o n c e n t r a t i o n approaching a .
Emergence
Senescence n f
Mean date ( a ) r
6 4 17, Apr (107) 0.90
**
5 6 2, Jul (181) 0.42
*
Spore release 4 3 11, Jan (11) 0.77
**
* p<0.05, ** p<0.01
Fertile leaves Sterile leaves n s
Mean date ( a ) r
7 4 30, Jun (179) 0.55
**
6 6 15, Aug (224) 0.45
**
Watson-
Williams tests
F
13.82
4.09
*
**

140 Indian Fern Journal Volume XXXVI (2019)
In fertile leaves, the number of monthly emerging leaves did not correlate with monthly precipitation (MP), temperature (MT), or day length (MD), while sterile leaves had significant correlations with these three environmental factors (Table 4).
Senescence of leaves
A total of 122 senescent leaves, including 56 fertile and 66 sterile ones, were recorded in this study. Mean number of senescent leaves were 1.74 per plant annually, slightly lower than that of emergence (1.97). Annual senescent leaves ranged from 0.6 (in
2006) to 3.2 per plant (in 2002) (Table 2).
Although leaves withered almost throughout year, senescence mainly occurred in perhumid season (from April to September) (Fig. 2b) and expressed a significantly seasonal pattern, i.e., 85.7% and 72.7% fertile and sterile leaves senesced in this period, respectively. Mean dates of senescence of fertile and sterile leaves were significantly different occurring on 2, July (vector r = 0.42
* ) and 15, August (vector r = 0.45
** ) respectively (Table 3).
Numbers of monthly senescent fertile leaves were significantly positively correlated with MP, MT, and MD, but counts of monthly senescent sterile leaves had significant correlations only with MP and MT, not with MD (Table 4).
TABLE 4 : The Pear son correlation coefficients ( r ) between monthly climatic factor s with the mean monthly leaf number of each phenophase.
Precipitation Temperature Day length
Emergence
fertile
sterile
all
Senescence
fertile
sterile
all
Living
fertile
sterile
all
Spore release
-0.05
0.81
0.28
0.67
0.56
0.72
0.66
0.78
**
0.78
**
-0.51
ns
** ns
*
*
**
* ns
0.11
0.86
0.43
0.58
0.65
0.72
0.75
-0.83
ns
** ns
*
*
**
**
0.84
**
0.86
**
**
0.29
0.87
0.58
0.61
0.40
0.59
0.83
ns
**
*
** ns
*
**
0.62
*
0.84
**
-0.64
* ns p>0.05, * p<0.05, ** p<0.01

144 Indian Fern Journal Volume XXXVI (2019)
Fertile vs. sterile leaf morphology
Fertile leaves usually had longer stipes than sterile leaves. Other morphological traits (blade length, blade width, and the number of pinna) of fertile and sterile leaves did not show significant differences although all of them of fertile leaves were larger than the latter (Table 5).
Leaf lifespans (LLS)
The estimated mean LLS was 32.5 months based on the turnover rate method. It was slightly lower than that of direct observation (34.6 months), but the difference was not significant ( p=0.32). According to the direct observation of senescence date minus emergence date, the minimum and maximum LLSs were coincidently the same, with 9 and
61 months, respectively; whereas those were 18.2 and 52.3 months, respectively, estimated by turnover rate method. Furthermore, sterile leaves had longer average LLS than fertile ones’ either counted by direct observation (40.7±13.0 vs. 25.6±15.6 months) or estimated by turnover rate (53.3±36.5 vs. 23.8±6.3 months) (Table 6). The differences of sterile or fertile LLS between values of direct observation and turnover rate estimation were not significant ( p=0.20, 0.33, respectively). Other data of LLS are shown in Table 6. Given that the fertile LLS equals to 25.6 months, and based on estimates of mean dates of phenophases shown in Table 3, on average a fertile leaf lives ca. 16.8 months after its spores released, or about two third of its whole life.
Spore release
A total of 43 leaves with spore release were recorded. Mean number of leaves with spore release was 0.61 per plant annually and ranged from 0.10 (in 2004) to 1.40 per plant
(in 2008) (Table 2). Spore release, indicated by leaf numbers, exhibited significant seasonality (vector r = 0.77), mainly (86%) concentrated in December–February (Fig. 2d), with the mean date of 11, January (Table 3). The monthly number of leaves with spore release was significantly negative correlated with MT and MD, but not correlated with MP
(Table 4).
TA B L E 5 : C o m p a r i s o n b e t w e e n t h e s i z e s ( m e a n ± S E ( m i n –m a x ) ) o f f e r t i l e a n d s t e r i l e l e a v e s o f
A n g i o p t e r i s s o m a e .
Stipe length (cm)
Blade length (cm)
Blade wide (cm)
No of pinna
Fertile leaves (n = 32)
45.2±10.0
a (26–70)
31.7±3.9
a (23–40)
33.3±6.1
a (20–48)
4.8±0.7
a (4 – 6)
Sterile leaves (n = 61)
29.0±5.5
b (16–39)
26.6±3.7
a (19–36)
29.4±4.6
a (15–42)
4.5±0.6
a (4 – 6)
* Different letter indicates significant difference on the same line ( t-test, p<0.05)

Yao-Moan Huang et al. : Phenology & Leaf Lifespan of an Endangered Fern Angiopteris somae (Marattiaceae) 145
Comparison of parameters monitored between typhoon and nontyphoon year
During this monitoring period, no typhoon came to the studying site in the first two years, and then one to four typhoons attacked in each of the following five years (Table
1). None of the ten monitored plants died during this period. Amount of mean annual precipitation in typhoon years was significantly larger than in nontyphoon years, while the mean annual temperature was not (Table 7). Numbers of emergent, senescent, living, and spore-releasing leaves were larger or smaller between nontyphoon and typhoon years, but all of them were not significant different. The occurrence mean dates of each phenophase were also not significantly different between nontyphoon and typhoon years except the mean dates of spore release.
DISCUSSION
Seasonality of leaves
There is a significant difference between the timing of the leaf-emergence seasons of fertile and sterile leaves of A. somae, in this whole-year humid site, i.e., either perhumid or relative humid. This difference is similar to that seen in forests of northern and northeastern Taiwan that are also in whole-year humid areas (Lee et al. 2009a, b). In contrast, the emergence timing of sterile and fertile leaves of about half of the monomorphic species of ferns observed was not different in a monsoon forest of southern
Taiwan that featured with dry-humid alternation seasonality (Lee et al. 2016, 2018).
TA B L E 6 : L e a f l i f e s p a n s o f A n g i o p t e r i s s o m a e e s t i m a t e d b y d i r e c t o b s e rv a t i o n a n d t u rn o v e r rate (unit : months).
Direct measurement
# of leaves
Mean±SE*
Max
Min
Medium
Turnover rate**
Mean±SE*
Max (year)
Min (year)
Medium
Fertile
2 5
25.6±15.6
a
6 1
9
2 1
23.8±6.3
a
35.6 (2002)
17.1 (2003)
20.8
Sterile
3 7
40.7±13.0
c
6 1
9
4 3
53.3±36.5
c
124.8 (2007)
16.9 (2004)
57.5
* Different letter on the same row indicates significant difference ( t-test, p<0.05)
** The average of 10 plants across seven monitored years.
All
6 2
34.6±15.8
b
6 1
9
3 8
32.5±10.8
b
52.3 (2007)
18.2 (2004)
39.1

146 Indian Fern Journal Volume XXXVI (2019)
In addition to the difference in leaf-emergence seasons, the emergent period of fertile leaves was much more intensive than sterile ones (vector r = 0.90
** vs. 0.55
** ) in A.
somae. Emergence of fertile leaves in higher concentrations has been found in many studied dimorphic ferns and monomorphic ferns (Lee et al. unpublished).
Similar to the emergence of leaves, the senescent seasons of fertile and sterile leaves also exhibited significantly differences. However, both of their occurrence times overlapped considerably and mainly occurred in the perhumid season with high temperature and heavy precipitation. The significant difference of seasonality resulted from the senescence numbers in each month and this is also indicated by their discrete mean dates.
Spore release
Spore release of most ferns appeared in late spring to early autumn (e.g., Lee et al.
2009b, 2016). In contrast, A. somae released spores mainly in the cooler and drier winter, an unfavorable season for spore germination immediately after their release. Spores of a monomorphic fern, Asplenium scolopendrium L. var. americanum (Fern.) Kartesz and
Gandhi, exhibited a higher germination rate following the vernalization (a requirement for plants to produce new buds with cool condition) treatment (–15 0 C freezer for 90 d) relative to the control (~20 0 C during the freezing period) (Testo & Watkins 2013). In our spore culture experience, the germination rate of spores of A. somae also increased after vernalization treatment (fresh leaves with mature spores stored at 4 0 C for 2 month)
(unpublished data). This shows that spore maturation (indicated by spore release here) of
A. somae in winter and subsequent vernalization may favor spore germination and gametophyte growth in the following warm and wet season.
Contrary to other monomorphic species documented by Lee et al. (2009 a, b), the seasons of leaf emergence and spore release are not closely “synchronized” in A. somae. In most monomorphic ferns, spore release pattern usually corresponds to the seasonality in leaf emergence patterns, following fertile leaf emergence by a few (ca. 1–4) months. In A.
somae, however, spore release is delayed (ca. 9 months) into a later season, and thus the seasonality of fertile leaf emergence does not correspond to the seasonal pattern of spore release.
Leaf lifespan (LLS)
Mehltreter & Sharpe (2013) stated that both direct measurement (emergence to senescence) and indirect estimation (based on leaf count and production rates) of LLS require close observation at least one year. It is reasonably assumed that direct measurement usually obtains more precise lifespan data than the estimation by the turnover rate (indirect estimation). In this study, although the mean LLS of A. somae was slightly higher based on direct measurement than the indirect estimate (34.6 vs. 31.2 mo), the difference is not statistically significant. Counting lifespans of fertile and sterile leaves separately, LLS measured by direct observation was higher or lower than by turnover rate estimation. It

Yao-Moan Huang et al. : Phenology & Leaf Lifespan of an Endangered Fern Angiopteris somae (Marattiaceae) 147
TABLE 7 : Compar ison of climate data, g rowth parameter s, and phenophases of A n g i o p t e r i s s o m a e b e t w e e n n o n t y p h o o n a n d t y p h o o n y e a r s . A l l p a r a m e t e r s b e t w e e n n o n t y p h o o n y e a r a n d typhoon year are not significantly different unless specifically noted.
Mean annual precipitation (mm) 1
Mean annual temperature ( 0 C)
# of emergence leaves plant -1 year -1
Fertile leaves
Sterile leaves
All leaves
# of senescence leaves plant -1 year -1
Fertile leaves
Sterile leaves
All leaves
# of living leaves
Fertile leaves
Sterile leaves
All leaves
# of spore-released leaves plant -1 year -1
Mean date ( a); vector r of phenophase 2
Emergence of fertile leaves
Emergence of sterile leaves
Senescence of fertile leaves
Senescence of sterile leaves
Spore releasing 3
Nontyphoon years Typhoon year s
( 2 0 0 2 – 2 0 0 3 ) ( 2 0 0 4 – 2 0 0 8 )
1516 b 3134±637 a
20.4
20.0±0.2
0.75
0.90
1.65
1.55
1.05
2.60
1.53
2.46
3.99
0.75
0.98±0.65
1.12±0.68
2.10±0.47
0.50±0.44
0.90±0.50
1.40±0.71
1.81±1.12
3.78±0.55
5.58±1.32
0.56±0.50
All years
( 2 0 0 2 – 2 0 0 8 )
2672±964 a
20.1±0.2
0.91±0.55
1.06±0.68
1.97±0.61
0.80±0.78
0.94±0.42
1.74±0.89
1.73±0.93
3.40±0.79
5.13±1.33
0.61±0.46
11, Apr (100); 19, Apr (108); 17, Apr (107);
0.89** 0.90** 0.90
**
6, Jul (185); 28, Jun (177); 30, Jun (179);
0.68** 0.51** 0.55
*
28, Jun (177); 21, Jul (200); 2, Jul (181);
0.62** 0.18
ns 0.42
**
21, Aug (230); 12, Aug (221); 15, Aug (224);
0.52** 0.43** 0.45
**
14, Feb (45); 24, Dec (354); 11, Jan (11);
0.83** 0.87** 0.77**
1
2
3
: Different letters on the same row indicate significant difference ( t-test, p<0.05)
: Significance of vector r is detected by Rayleigh test (Morellato et al. 2000, 2010)
: S i g n i f i c a n t l y d i f f e r e n t b e t w e e n n o n t y p h o o n y e a r a n d t y p h o o n y e a r d e t e c t e d b y
Watson-Williams test

148 Indian Fern Journal Volume XXXVI (2019) suggests that obtaining LLS by these two methods leads to a similar (no significant difference) result giving a long enough monitoring period.
Direct measurement requires a longer time to collect leaf stages with studies lasting at least twice the mean lifespan, which is often unknown when planning the study. In contrast, indirect estimation of leaf lifespan is a relatively economical and timesaving method and thus has been widely applied (Seiler 1981, Tanner 1983, Bittner & Breckle
1995, Sharpe 1997, Mehltreter & Sharpe 2013, Silva et al. 2018). However, estimating leaf lifespans does result in the loss of information about individual variation and biased range of lifespans. For example, the maximum sterile LLS, 124.8 months, estimated in 2007 is noticeably deviated from the mean and medium values. That results from the very low emergent leaf number but high living leaf number in that monitoring year. Apparently estimating the LLS of a fern by turnover rate in a short period risks a misjudged conclusion.
Compared to the data set of LLS of 71 fern species (Mehltreter and Sharpe 2013), the mean LLS of A. somae are fairly longer, only shorter than a Mexican epiphytic monomorphic fern Terpsichore asplenifolia (L.) A. R. Sm., with the mean LLS for fertile leaves of 4.9 years (ca. 59 months) (Monge Gonzalez 2007). Vincent (2006) suggested that plant species with longer LLS are likely to have a sequence of slower ageing of leaves as a result of a slower photosynthetic metabolism. This would coincide with the physiological characteristic of A. somae with a low photosynthesis capacity (Wong et al. 2012, Weng &
Wong. 2015).
Dimorphic vs. monomorphic
The leaf morphology of sterile and fertile leaves was similar except that the stipes of fertile leaves were significantly longer than sterile ones. The ratio of fertile leaves LLS/ sterile leaves LLS of A. somae, 0.63 (25.6/40.7), is lower than other monomorphic species
(0.68–1.76), but far larger than dimorphic species (0.10–0.39) (Lee et al. 2018). The sterile
LLS of A. somae is significantly longer than the fertile LLS. In dimorphic ferns, fertile leaves die soon after investing energy in producing spores (Watkins et al. 2016), while the fertile leaves of A. somae continuously live in green and presumably photosynthesize after releasing spores, serving as a potential source of nourishment as well as reproduction. These fertile leaves do not completely exhaust energy during producing spores as seen in dimorphic ferns. Therefore, in this respect A. somae is more properly categorized into a monomorphic fern.
Although morphologically similar the fertile and sterile leaves of A. somae have very different phenophases of emergence and senescence between sterile and fertile leaves, as in dimorphic ferns, e.g., Danaea geniculata (de Paiva Farias et al. 2018), Plagiogyria adnata & P. dunii (Lee et al. 2009b). The possibility of this “behavior” differences is noted by Wagner & Wagner (1977), but the difference extent is only documented with exemplary

Yao-Moan Huang et al. : Phenology & Leaf Lifespan of an Endangered Fern Angiopteris somae (Marattiaceae) 149 detailed studies like this one. Therefore, we recommend that the phenology of both leaf types should be separately analyzed for both dimorphic and monomorphic ferns.
Effects of typhoons
Typhoon is a very important disturbance event in many forest ecosystems (Everham
& Brokaw 1996, Wang et al. 2016). During last 5 years of our 7-year phenological survey period, 11 typhoons passed over the study site. Except for the amount of precipitation which greatly increased and the much earlier occurrence of spore maturation (indicated by releasing here) during the typhoon years, all monitored parameters were not significantly different, but some trends are interesting and noted below.
The annual mean numbers of living leaves and emergent leaves of A. somae correspondingly increased during the typhoon years. It is suggested that A. somae received more sunlight that could have triggered the initiation of leaf emergence and increased the rate of fertile leaf production. Typhoons in Taiwan are a type of wind-initiated disturbance accompanied by large amounts of precipitation that result in the formation of large gaps in the canopy and deposition of larger amounts of leaf litter (personal observation). Those canopy gaps let more light shine on the floor.
Simultaneously, nitrogen availability might increase when higher temperatures in canopy gaps accelerate decomposition of organic matter (Takafumi et al. 2010), and thereafter more nutrients could be available for leaf emergence/growth. A similar response to light is also reported in Matteuccia struthiopteris
(L.) Todaro, commonly found in shady habitats and increased the number of leaves when irradiance levels are increased (Prange 1980). Sharpe & Shiels (2014) discovered that two understory ferns, Thelypteris deltoidea (Sw.) Proctor and Cyathea borinquena (Maxon)
Domin, can considerably increase the production of spore-bearing leaves when light levels increase. They also found that adding debris may have a positive effect but only in a combination with added light. The larger number of senescent leaves in nontyphoon years than in typhoon years is probably due to the relative drought condition resulting from less precipitation in the former. An increase in leaf mortality in less rainfall years is also found in some tree fern species (Silva et al. 2018).
An increase in light caused by typhoon also leads to a more even leaf production throughout the year, i.e
., less seasonality (Angulo-Sandoval et al. 2004). The phenophase difference of leaf emergence between typhoon and nontyphoon years in this study does not reflect a same response. It indicates that light (and other factors) brought by typhoon does not affect the seasonality of the leaf production for A. somae.
Spore release is affected by temperature and humidity. Low temperature may delay spore release (Arosa et al. 2009). Spores of A. somae released ca. seven weeks earlier in typhoon years than in nontyphoon years. It perhaps contributed to the higher temperature of microhabitat caused by more light resulting from typhoons. Minimum precipitation happened in February and December to January for nontyphoon year and typhoon year, respectively. Most spores released (indicated by the mean dates and vector r )

150 Indian Fern Journal Volume XXXVI (2019) correspondently occurred in the driest (least precipitation) seasons of these two climate patterns.
The above inferences regarding those phenomena might be too simple. After all, evaluations of plant character responses to disturbance must include the combined interacting responses of the comprehensive elements of that ecosystem (Zimmerman et al.
1996, Watson & Estes 2011). Besides, two nontyphoon years obviously are insufficient to collect long-term phenological data to get a solid reference. Here we have only pointed out some intriguing issues for more consideration in future studies.
Conservation
Ex-situ conservation is important to the preservation of an endangered species, especially for those not located in a protected area, such as A. somae. Although leaf-base stipules of A. somae provide useful materials for its ex-situ propagation (Chiou et al. 2006), the resulting vegetative offspring lack genetic variation from their parents. The number of available stipules is also low because of limited population sizes and relatively low annual leaf production rates. On the other hand, spore culture provides an efficient method to increase the number and genetic heterogeneity of descendants and should be regarded as the best choice for ex situ conservation of A. somae (Chou et al. 2007). In this study, we found that winter is the most suitable season for collecting mature spores of A. somae for further culture and to be used in its ex situ conservation.
CONCLUSION AND FUTURE ASPECT
The relevance of phenological research has been recognized for decades. However, most phenological studies, especially on ferns, have been short-term, ending after only one or two years and may not present a complete phenological picture for a species, possibly resulting in our misunderstanding possible long-term changes and disturbance effects.
Seven-year monitoring of Angiopteris somae in our study is the longest fern phenological study currently reported in the world. Our results show the annual averages and variations of different phenophases, including leaf emergence and senescence and spore release, and lifespans of both fertile and sterile leaves of this species. The correlations of those phenophases with environmental factors are presented as well. Those long-term data are comprehensive and potentially useful. More exploration and further analyses of those data will raise additional intriguing features, which will be useful for elucidating more related biological phenomena and application in the future.
In addition to the need for more long-term studies, the formation of a broad geographical network is also encouraged to further facilitate the development and understanding of fern phenology (Lee et al. 2018). Many phenological studies with diverse representation of various climate conditions have been done in Taiwan (e.g., Lee et al. 2008,
2009a, b, 2016). South to Southeastern Asia, with rich tropical to subtropical fern diversity, is another ideal region for conducting this kind of broad-scale phenological research. This

Yao-Moan Huang et al. : Phenology & Leaf Lifespan of an Endangered Fern Angiopteris somae (Marattiaceae) 151 region is also inhabited many Angiopteris species, a genus in the Marattiales that is an ancient fern lineage, and could therefore be a candidate group for such study. Phenological data for A. somae collected in this study set a valuable base for such future approach.
ACKNOWLEDGEMENTS
We thank Sheng-Yuan Hsu, Chun-Ming Chen, Chia-Wen Ko, Yu-Wen Huang and Yi-
Shan Chao for helping field investigation, Pi-Fong Lu for providing some plate photos, and
Dr. Joanne Sharpe for providing valuable comments.
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