89 ISSN: 2406-7334 │ E-ISSN: 2406-7342 IJSTAS Vol: 2 No. 1 (2015) 89 - 96 │

PHENOLOGICAL TRAITS OF obovata GROWN IN MANKO WETLAND, OKINAWA ISLAND, JAPAN

Kangkuso Analuddin1&3, Andi Septiana1, Sahadev Sharma2&3 and Akio Hagihara3

1 Department of Biology, Faculty of mathematics and natural Sciences, Halu Oleo University, Kendari, Indonesia 2Department of Natural Resources and Environmental Management, University of Hawaii at Manoa, Honolulu, HI 96822, USA 3Graduate School of Engineering and Science, University of the Ryukyus Abstract Phenological traits of (S., L.) Yong was investigated on the basis of seasonal leaf recruit, leaf death and leaf growth. The seasonal leaf growth was estimated using the logistic growth curve. Leaf recruitment, leaf death and reproductive cycle were obtained by survey data. This study results showed that new leaf recruitment occurred during the year indicating high productivity of mangrove Kandelia obovata forest. The highest leaf recruit was in July, while it was the lowest in January. However, the highest leaf death was in August, whereas it was the lowest in January. Growth pattern of leaves varied among seasons as of winter leaves are taken longger time to get their maximum size, while other season leaves are taken short time to get their maximum size. Period from flowering to mature propagules of K. obovata trees is considered to be around 12 months, while most the propagules become mature in the next spring season (April and May), which indicated shorter reproduction cycle.

------Keywords : Phenological traits, Leaf recruitment and death; Leaf growth; Reproductive cycle; Kandelia obovata

*)Correspondence: E-mail: ([email protected])

INTRODUCTION the most vital keys for studying Mangrove ecosystem plays functions of mangrove forest ecosystem, important part in the global carbon and therefore, phenological study on cycle, and therefore occupies a position is very important to know of increasing importance in the climatic the mangrove productivity, material and debates and in the mitigation program. nutrient cycling, as well as predicting The mangroves play very important role mangrove adaptation to the climate in the coastal area as nursery grounds change. and breeding sites for various animals, a Mangrove phenology is an renewable resource of wood; sites for important subject for investigating the accumulation of sediment and nutrients effect of climatic factors on mangrove and offer protection against coastal growth and productivity. Phenological erosion, cyclones and tsunami (Twilley traits of mangroves are essential for 1995). Mangrove forest is known to understanding of mangrove′s ability to maintain the ecological equilibrium in adapt growth and breeding strategies to coastal waters and preserve rich ambient conditions. Phenological traits biological resources and species on mangroves are known influenced by diversity (Saenger 2002). Productivity climatic factors like day length (Duke assesment of mangrove forest is one of 1990), air temperature (Duke 1990; 90 ISSN: 2406-7334 │ E-ISSN: 2406-7342 IJSTAS Vol: 2 No. 1 (2015) 89 - 96 │

Fernandes 1999;) and rainfall cm) was selected for the direct (Fernandes 1999). Vegetative and observation of leaf recruit and reproductive phenologies of mangrove survivorship. New leaves of the sample communities are known to linking with tree were labeled and recorded twice a seasonal variations in temperature and month, while fallen leaves were monthly rainfall (Fernandes 1999; Gwada et al. counted. Twenty newly flushed leaves 2000; Carolina and Ertemeijer 2002). from the sample tree respectively in Many phenological studies on April, August and October 2005, and mangrove forest are mentioned their January 2006 were chosen to pursue the seasonal trends of leaf recruit, leaf fall growth of leaves, whose length and and reproduction cycle (Fernandes 1999; width were measured twice a week. The Gwada et al. 2000; Ochieng and data of climatic factors were taken from Ertemeijer 2002; Coupland et al., 2003; Meterogical office, Naha City, Okinawa, Mehling 2006). However, the Japan information of mangroves phenological traits in term of seasonal leaf area RESULT AND DISCUSSION growth, leaf recruit and death together Climatic factors with repduction cycle is scare. These data are fundamental for assessing the Figure 1 depicts monthly trends effect of climatic factors on mangrove in climatic parameters at the study site growth and productivity. Therefore, the including day length, global solar objectives of this study was to elucidate radiation, temperature, sunshine time, the phenological traits of a K. obovata in precipitation and relative humidity (Data term of seasonal patterns in leaf recruit, from Okinawa Meteorogical leaf death and leaf growth, as well as Observatory). Monthly mean reproduction cycle. temperature, global solar radiation and sunshine time were found to be the MATERIAL AND METHOD higher in July, while monthly mean day length, precipitation and relative Study Site humidity were found to be the higher in This study was carried out from April June. The lowest monthly mean 2005 to March 2006 at Manko Wetland, temperature, global solar radiation, which is located in the southern part of mean day length and mean relative humidity were in December. Monthly Okinawa Island, Japan (26º 11′ N and precipitation and sunshine time were the 127º 40 E). The Manko Wetland ′ lowest in July and March, respectively. mangrove is dominated by Kandelia obovata (S., L.) Yong. The wetland has Leaf recruit and death been recognized as an important area in the transit point or wintering area for Table 1 represents the seasonal migratory birds, and has been registered leaf recruit and death in mangrove with the Ramsar Covention since 1999. Kandelia obovata tree. Seasonal changes This mangrove is monospecific in leaf recruit and death varied dominant with crowded stands. throughout the year. The leaf recruit and death were the highest in summer (July Leaf recruit, leaf death and leaf or August), while were the lowest in growth January. The highest leaf recruit and death in summer may be due to the One sample tree (tree height H, 3.1 m, highest global solar radiation and stem diameter at 10 % of H D 4.1 0.1H, monthly mean temperature (Fig. 2), 91 ISSN: 2406-7334 │ E-ISSN: 2406-7342 IJSTAS Vol: 2 No. 1 (2015) 89 - 96 │ which indicated that leaf recruit and expansion period (t*) of leaf area is death in mangrove Kandelia obovata defined as: synchronize with the seasonal changes ln k in climatic factors. t*  (2) Table 1. Monthly leaf recruit and leaf  death of mangrove Kandelia obovata tree (Data April 2005- 15 24 )

a 2 22

March 2006) )

-1 14 20 Number of Number of 18 Month leaf recruit leaf death 13 April 125 25 16 12 May 88 45 14 12 June 102 53 11 July 157 96 Mean day length (h d 10 10 8 Globalsolar radiation (MJ m August 57 151 M J S N J M September 79 63 2005 2006 October 111 57 30 250

C) b November 54 56 o 28 ) December 33 31 200 -1 January 22 9 26 150 February 30 19 24

March 65 18 22 100

20 50 18

Figure 3 depicts growth patterns of leaf Sunshinetime (hmonth Mean monthly temperature ( 16 0 area in different seasons. The growth M J S N J M process was well described with the 2005 2006 logistic growth curve as follows: 1000 85 c U 80 u  (1) 800 1 ke t 75 600 where U,  and k are the maximum 70 leaf area, intrinsic rate of increase and 400 constant, respectively. The growth 65 200 patterns of leaf area showed unequal 60 Mean relativehumidity (%) trends among seasons. The values of Monthly precipitation (mm) 0 55 U,  and k for spring leaves were M J S N J M estimated as 10.97 (cm2), 0.081 (cm2 d- 2005 2006 1 ) and 2.53, respectively. In addition, the Figure 1. values of U,  and k for summer leaves 2 were estimated as 10.56 (cm ), 0.10 (a) Seasonal patterns in total solar radiation ○ and day length ●, of U,  and k for winter leaves were (b) Seasonal patterns in sunshine time ○ and 2 temperature ● respective estimated as 14.46 (cm ), (c) Seasonal patterns in precipitation ○ and relative 0.054 (cm2 d-1) and 4.42. The half- humidity ●. 92 ISSN: 2406-7334 │ E-ISSN: 2406-7342 IJSTAS Vol: 2 No. 1 (2015) 89 - 96 │

160 160 a 140 b ) 140 -1 ) -1 120 120 (month 100 100

80 80

60 60

40

40 death leaf of Number Number of leaf recruit (month recruit leaf of Number 20 20 0 16 18 20 22 24 26 28 30 8 10 12 14 16 18 20 22 Monthly mean temperature ( oC) Monthly global solar radiation (MJ m -2)

Figure 2. Relationships of leaf recruit and death to climatic factors: (a) Relationship of leaf recruit to global solar radiation, where r = 0.799, p = 0.002. (b) Relationship of leaf death to temperature, where r = 0.816, p = 0.001.

16 spring, summer and autumn are grown faster, and taken short time to reach their 14 maximum size. On other hand, the

12 leaves flushed in winter seemed to be ) 2 grow slower and taken longer time to get

(cm 10

u their maximum size. However, the autumn leaves showed the shortest half 8 expasnion period. Therefore, it seems Leaf area Leaf 6 that growth patterns of leaf area of a K. obovata synchronize to the seasonal 4 changes in climatic factors.

2 0 20 40 60 80 100 Time (d)

Figure 3. Seasonal patterns of leaf area growth: ○ Spring, ● Summer, △ Autumn and ▲ Winter seasons. (cm2 d-1) and 2.89. The values of U,  and k for autumn leaves were estimated as 9.42 (cm2), 0.083 (cm2 d-1) and 1.61. On the other hand, the values The values of half expansion periods of leaves growth were estimated as 11.5 days for spring leaves, 10.6 days for Figure 4. Reproduction cycle of a mangrove summer leaves, 5.8 days for autumn Kandelia obovata tree leaves and 27.5 days for winter leaves, respectively. The leaves recruited in 93 ISSN: 2406-7334 │ E-ISSN: 2406-7342 IJSTAS Vol: 2 No. 1 (2015) 89 - 96 │

Figure 4 shows the candel at Sashiki village, Okinawa reproduction cycle of a mangrove K Island, Japan, by Lopez partillo and obovata in Manko Wetland The Ercura (1985) in Avicenna germinants in flowering period occurs in spring, i.e. Mexico and by Ochieng and Erftemeijer from April to June, while fruiting occurs (2002) in Avicennia marina at Grazi in summer. However, propagules Bay, Kenya. However, different patterns development is from summer (July) to in leaf recruit and death were observed spring (May) seasons. Most of by Coupland et al. (2005) in Avicenna propagules become mature in spring marina, Sonneratia alba and Rhizophora (April or May) of the next year, which stylosa and by Cristensen and Wium- indicates that reproduction cycle of a K andersen (1977) in Rhizophora obovata is approximately one year. apiculata. New leaves recruitment in mangrove Kandelia obovata occur 4. Discussion through the year, which indicates high productivity of mangrove in this region. The present study clearly showed the It is different as compared with Ceriops phenological traits of a mangrove australis at north-eastern Australia, Kandelia obovata (S., L.) Yong, which which the canopy of Ceriops australis is has been correlated with seasonal effectively dormant for six months of changes in climatic factors. Many the year during dry season (Duke et al., studies reported that phenological events 1984). Leaf production in mangrove was in mangroves and other tropical trees very much tied to changes in can be influenced by environmental temperature (Saenger and Moverley factors like day length (Duke 1990; 1985). However, leaf flush in Kandelia Rivera and Borchert, 2001), air candel at the Okinawan mangrove, temperature (Saenger and Moverley, Japan was most closely linked to 1985; Duke 1990; Fernandes 1999; temperature and humidity, the two Coupland et al., 2005) and rainfall factors being closely interdependent (Fernandes 1999; Gwada et al. 2000; (Gwada et al. 2000). Similarly, Duke Ochieng and Ertemeijer 2002; Coupland (1990) also reported that changes in et al., 2005) or water status (Naidoo, temperature, rainfall and moisture level 1989). Our results suggest that are likely to control mangrove leaf phenological events of a mangrove K. production. Although the leaf recruit and obovata synchronize to the seasonal death of a mangrove Kandelia obovata changes in climatic factors of Okinawa were strongly linked to the seasonal region, such as global solar radiation, changes in global solar radiation and temperature, sunshine time, precipitation temperature, the other factors, such as and humidity. sunshine time, precipitation and The leaf recruit and death of a humidity are probably among the mangrove K. obovata are strongly important factors influencing the correlated to the seasonal changes in phenological events on mangrove trees global solar radiation (r = 0.799, p = in this region. 0.002; Fig. 2a) and temperature (r = Trend in leaf area growth for a 0.816, p = 0.001; Fig. 2b). Leaf recruit mangrove Kandelia obovata also and death were the highest in summer, synchronize to the seasonal changes in whereas the lowest in autumn. Similar climatic factors. It appears that winter trends in leaf production were observed leaves are the longer leaf area growth by Gwada et al. (2000) in Kandelia and taken time to get their maximum 94 ISSN: 2406-7334 │ E-ISSN: 2406-7342 IJSTAS Vol: 2 No. 1 (2015) 89 - 96 │ size as compared the other seasons. reproductive organs in a mangrove Mehltreter and Palacios-Rios (2003) Kandelia obavata are probably inter- reported that monthly leaf growth of the correlated in coordination each other. mangrove Acrostichum danaeifolium Duke et al. (1984) suggested that grown in the Gulf of Mexico was coordination between production of significantly correlated with mean flower/fruit and leaves may be an temperature and precipitation. In the indication of resource partitioning present study, growth patterns of leaf within . The potential resource area are probably linked to seasonal partitioning within mangroves was changes in temperature, precipitation observed by Coupland et al (2005) in and relative humidity. It shows that the Sonneratia alba, i.e. leaf recruit in S. averages temperature, precipitation and alba was clear dejection during the time humidity in winter were about 18oC, 135 of peak flowering and fruiting. mm and 71 %, respectively, and were 5. Conclusion probably effective for leaf area growth as compared with the other seasons. New leaves recruitment in mangrove The timing of the reproductive cycle Kandelia obovata forest occur through of a Kandelia obovata is also seasonally. the year indicating its high productivity. Flower occurs in spring (April-June), Leaf recruitment was highest in July while propagules occurs in summer (summer season), while it was lowest in (July-August). Most the propagules January (winter season). The growth of become mature in the next spring season leaves varied among seasons as of (April and May). It suggests that the winter leaves are taken longger time to period from flowering to mature get their maximum size as compared propagules of K. obovata is considered other season leaves. However, larger to be around 12 months which is lower leaf area was found for winter leaves, as compared to 3 years for Rhizophora which is probably effective for K. apiculata and 1-1.5 year for obovata to capture as much as possible gymnorhiza, Cerip tagal and R. stylosa quite low radiation in winter compared (Hutchings and Saenger 1987), while it with the other seasons. Period from was slightly longer than 9 months for flowering to mature propagules of K. propagule development in Avicennia obovata trees is considered to be around marina (Clarke and Myerscough 1991). 12 months, while most the propagules Reproductive phenological of a become mature in the next spring season Kandelia obovata forest was different as (April and May), which indicated compared with the other mangroves, i.e. shorter reproduction cycle. the flowering and fruiting patterns of Acknowledgments Amazonian mangrove (Avicennia, Rhizophora and Laguncularia) occur We thank Drs. M.N.I. Khan, S.M. Feroz throughout the year, which is the peak and R. Suwa, and Mr. W. Paina for their flowering and fruiting in dry period, and invaluable help with the fieldwork. This between the end dry period and the onset study was partially supported by Grants- of the wet season (Fernandes 1999). in-Aid for Scientific Research (no. There might be existed some 20510011) from the Ministry of synchronizations between productions of Education, Culture, Sports, Science and flowers, fruits or propagules and leaves Technology, Japan, and by the 21st in mangrove Kandelia obovata forest. Century COE program of the University This study results suggest that of the Ryukyus,. We owe our deep thank production of vegetative and to Professor (Emeritus) Akio Hagihara 95 ISSN: 2406-7334 │ E-ISSN: 2406-7342 IJSTAS Vol: 2 No. 1 (2015) 89 - 96 │ for his crodial help during field research Gaertn. F. in Amazonian and study in Ryukyus University, mangrove swamp. Biotropica, Okinawa, Japan. 23, 555-567

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