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J. Agric. Sci., Tokyo Univ. Agric., 58 (3), 141-148 (2013) 東京農大農学集報，58（3），141-148（2013）

Litterfall Removal by Detritivorous in a Mangrove Forest of Miyakojima Island

By

† Tatsuma Matsutani*, Takashi Nagai** and Yasuhiro Nakanishi***

(Received May 23, 2013/Accepted September 10, 2013)

Summary：To clarify the dynamics of tannin translocation from mangrove leaves and the formation of complexes with metal ions such as Fe in the floor soil, we investigated the amount of litterfall and removal by detritivorous crabs using litter catchers in a mangrove forest in Okinawa, a subtropical part of . The results were : 1) the amount of litterfall was 1221 gm－2y－1, with the relative proportions of litter removed by crabs, the standing stock of litter, and litter export into the sea comprising 68.9, 9.6 and 21.4%, respectively. 2) The relative percentages of leaf litter derived from Bruguiera gymnorrhiza, Rhizophora stylosa and Derris trifoliata were 61.4, 31.1 and 7.5%, respectively. Crabs were responsible for the removal of 72.8, 69.3 and 35.7%, of each species, respectively. The percentages of leaf litter removed by crabs were high in the Tannin-rich mangrove species. 3) The amounts of tannins contained in the leaf litter and the removal by crabs were estimated to be 92.6 and 65.7 gm－2y－1, respectively. The crabs which selectively feed on mangrove leaves could provide opportunities for tannins in the leaves to react with the floor soil and cause the elution of dissolved Fe.

Key words：mangrove, litterfall, litter removal, detritivorous , tannins

tannins extracted from litter form complexes with metal 1. Introduction ions such as Fe and Mn in soil, making them water Research on the relationship between nutrients derived soluble6, 7）. from terrestrial areas and coastal ecosystems has made Previous studies from our laboratory on Miyakojima considerable progress in recent years. For example, it Island, Okinawa8）, indicate that tannins in mangrove leaf has been shown that complex fulvic acid and Fe (III) promote the elution of Fe from mangrove floor soil even compounds originating in the humus of forest soils are a in saline water. In this way, Fe complexes were formed very important factor in the growth of phytoplankton when mangrove soil was mixed with leaf tannins sug- which is a primary producer in marine ecosystems1）. gesting that Fe produced by tannins in mangrove leaves 2） Matsunaga et al. also reported that a fulvic acid-Fe growing in land/sea interfaces likely plays a direct role complex was effective in promoting phytoplankton in marine ecosystems. 9） growth in Kesennuma Bay, Japan. According to Spalding et al. , mangroves are found in On the other hand, it has been usually indicated in 123 countries and territories globally, and cover a total mangrove studies that mangrove species which grow in area of 152×103 k m 2, especially along wetter coast lines the intertidal zone in the tropics and subtropics contain and in deltaic and estuarine areas. Although the area relatively high amounts of tannins in their bark and covered by mangroves is not particularly large, man- 3 ） leaves. Basak et al. reported that the tannin contents in grove ecosystems are important as an interface between leaves of 9 mangrove species were 14.56-40.11% (dry land and sea, and a source of nutrients directly supplied wt.). As fulvic acids, tannins are mostly water soluble to coastal ecosystems. and highly reactive, and their ecological effects in soil However, since mangroves grow in the intertidal zone, science have been widely investigated4, 5）. For example, most of the litterfall could be carried away by tidal activ-

* Department of Environmental Symbiotic Studies, Graduate School of Agriculture, Tokyo University of Agriculture ** Okinawa Prefecture Environment Science Center *** Department of International Agricultural Development, Tokyo University of Agriculture † Corresponding author (E-mail : [email protected]) 142 Matsutani, Nagai and Nakanishi ities, resulting in reduced opportunities for tannins in the natural subtropical mangrove forest in Okinawa, Japan. litter to react with Fe in the soil. This paper consists of the part of a series of studies It is known that direct grazing of leaf litter by detri- revealing the role of tannins in mangrove ecosystems. tivorous crabs is an important trophic pathway in man- The results obtained in this study might be useful as a grove forests, preventing the tidal export of valuable data-set in a sub-tropical mangrove ecosystem. 10-13） detritus from the ecosystem . For example, Robertson 14） 2. Methods and Daniel reported that detritivorous crabs removed 71, 79, 20 and 32% of the total annual litterfall of Ceriops 2. 1. Study area tagel, Bruguiera exaristata and Avicennia marina, respec- The Shimajiri estuary on Miyako Island, Okinawa (Fig. 15） tively, in tropical northeastern . Slim et al. 1 ; 24°52’N, 125°17’E) was selected as our study area as it also reported that crabs removed 40.3% of the litterfall of is conserved by the municipal government and is located from the forest floor in East close to our research station (Miyako subtropical farm, 16） Africa, and Lee reported that they removed 57% of the Tokyo University of Agriculture), about 15 km away. daily leaf litter production from Kandelia candel during The climate of the island is subtropical, and the average their active season. Thus, supposing that detritivorous annual rainfall and air temperature are 2,034 mm and crabs remove a significant amount of mangrove leaf 23.6℃, respectively. On average, a typhoon approaches litter and carry it to their burrows, opportunities for within 300 km of the island 3.8 times per year (1981-2010, tannins in the leaves to react with the forest floor soil Okinawa Meteorological Station19）). The tidal range is could be greatly increased. 2.3 m. However, previous studies carried out to measure the The temperature and the precipitation in the study amount of leaf litter removal by crabs have not always period from April 2011 to March 2012 were at the same been conducted using a uniform method. In addition, level as an average year (Table 1). During the study only a few studies have been conducted using litter period, the highest monthly average air temperature catchers in subtropical areas for a full year or more. recorded was for July (28.8℃), and the lowest was for These reports have also indicated that the removal of January (18.3℃). The highest monthly rainfall (530 mm) litter by detritivorous crabs can vary, depending on was recorded with a typhoon in May (Table 1). The many factors including the tree species, benthos species, precipitation of this month was 3.6 times of the average air temperature, and tide height. year. Two more typhoons hit the site in June and Although results on the amount of litterfall17） and litter August. The lowest monthly rainfall recorded was 38 removal by crabs18） have been reported for mangrove mm in July. forests in Okinawa, each of them was a short-term experi- The mixed forest in the estuary contains five species, ment. Therefore, in our study, we validated the amount Rhizophora stylosa, Bruguiera gymnorrhiza, Derris of annual litterfall and the amount removed by crabs in trifoliata, Avicennia marina, and Kandelia candel (in the course of a year, using litter catchers set up in a decreasing order of stem density). The density of R.

Fig. 1 Location of the litter collection sites. Litterfall Removal by Detritivorous Crabs in a Mangrove Forest of Miyakojima Island 143

Table 1 Climate data for Miyako Island from 2001 to 2012.

Fig. 2 (1) Neosarmatium smithi and (2) the burrows. stylosa (higher than 2 m) was 11700±2465 trees ha－1. Table 2 Floral and faunal characteristics 2 According to Spalding et al. (2010), all species except for in the quadrat (100 m ). D. trifoliata are classified as mangrove species. The width from the edge of the riverbank to the edge of the forest varies from approximately 2 to 20 m, and the forest extends upstream from the river mouth for about 500 m. Detritivorous crab species inhabiting the estuary include Neosarmatium smithi, Helice leachi and Perisesarma bidens (in decreasing order of population density).

2. 2. Monitoring the amount of annual litterfall, standing stock of litter on the forest floor, Most of the field experiment methods used in this export of litter by tides, and litter removal by study are based on the techniques of Robertson and crabs Daniel (1989) and Chen et al., (2008), as follows. Field experiments to monitor the amount of litter were 2. 2. 1. Annual litterfall carried out using a quadrat (10 m×10 m) in an upstream As shown in Fig. 3, five square mid-air litter catchers area of the Shimajiri estuary. We selected this site be- (1 m×1 m tubular PVC frames to which a tapered 2 mm cause it is only flooded at high spring tides and because square mesh nylon cheesecloth bag was attached, sus- the stem densities of three tree species (R. stylosa, B. pended 1.2 m above the forest floor) were used to gymnorrhiza and D. trifoliata) growing at this site were monitor litterfall within the quadrat. Litter in the relatively uniform and their heights were all more than catchers was collected one day before every spring tide 4 m. Floral and faunal characteristics in the quadrat are and sorted into leaves, seeds, and stipules from each as shown in Table 2 and tree numbers per species within species. Samples were then dried at 60℃ for about 1 the quadrat were 54, 44 and 32, respectively. N. smithi week before measuring their weight. The sum of all (Fig. 2) was the dominant detritivorous crab species three litter components was defined as the total amount present and there were 456 crab burrows with a diameter of litterfall. In the case of the stipules, however, only the ≧25 mm and 786 burrows with a diameter ＜25 mm total weight was measured since it was not possible to within the quadrat. determine to which species they belonged. 144 Matsutani, Nagai and Nakanishi

2. 2. 2. Standing stock of litter on the forest floor days). Near each midair catcher in the quadrat, five ground 2. 2. 4. Litter removal by crabs catchers (1 m×1 m) were also set up, using color pegs We estimated the amount of litter removed by crabs (Figs 3 and 4). Litter in the ground catchers was using the following formula : collected on the same days as the midair catchers and C＝L－(S＋T) …………………………………… ⑴ handled in the same manner. We defined the amount of Where, C is the amount of litter removed by crabs, L litterfall collected from the ground catchers as the standing is the total amount of litterfall (collected from the midair stock of litter. catchers), S is the standing stock of litter (the amount 2. 2. 3. Export of litter by tides collected from the ground catchers), and T is the amount We estimated the amount of tidal export by multi- of tidal export. plying the number of days throughout the study period To determine whether crabs were actually responsible when the ground catchers were inundated (72 days) for removing the litter, we ran a trial experiment on the during spring tides by the mean annual amount of litter forest floor near the quadrat using tethered leaves to collected from the midair catchers, and then divided this follow the fate of litter once it reached the forest floor. Fig. 3 by the total length of the experimental period (355 In April 2011, we set up fixed pegs and tied ten fresh mangrove leaf petioles to each, using 1 m lengths of nylon twine. We prepared five of these devices for the leaves of each tree species (R. stylosaand B. gymnorrhiza) and monitored them with a digital video camera (FV M200 KIT, Canon) for one hour. All the leaves were carried off into crab burrows by N. smithi in less than 30 minutes (Fig. 4).

2. 3. Tannin content in leaves The data on tannin content in leaves for the tree spe- cies used in this study were analyzed using the following methods. The leaves were dried for 24 hours with a forced-air drier and ground into powder form with a grinder. Each 100 mg sample was mixed with 10 mL of an acetone-water solution (7 : 3 v/v)20） and shaken for 1 hour. The solution was then filtered through a glass Fig. 3 Location of litter catchers (1 m×1 m) within the fiber filter with a pore size of 1.7 μm (GF/A, Whatman). quadrat. Squares marked in solid lines and dotted lines This extraction operation was repeated three times for indicate the mid-air catchers and the ground each sample. The total phenol content of the filtrate was catchers, respectively. Numbers of Rhizophora measured using the Folin-Ciocalteu method21）. In a 10 mL stylosa, Bruguiera gymnorrhiza, and Derris measuring flask, 1 mL of Folin-Ciocalteu reagent (KANTO trifoliata within the quadrat were 54, 44 and CHEMICAL) was added to 1 mL of the filtrate and the 32, respectively. flask was vigorously shaken. After 3 minutes, 1 mL of 10%

Fig. 4 (1) the mid-air catchers and (2) the ground catchers. Litterfall Removal by Detritivorous Crabs in a Mangrove Forest of Miyakojima Island 145 sodium carbonate solution was added to the flask, and it produced by B. gymnorrhiza, R. stylosa and D. trifoliata was shaken thoroughly again. After 1 hour at room were 594 (61.4%), 301 (31.1%) and 72 (7.5%) gm－2y－1, and temperature, the absorptivity of the solution was read at the amounts of leaf litter removed by crabs were 501 700 nm using a spectrophotometer (U-5100, Hitachi). In (73.0%), 232 (69.0%) and 27 (36.0%) gm－2y－1, respectively. this analysis, tannic acid (Chinese gallotannin, which has The percentage of litter removal by crabs for the two a molecular weight of 1701.2 ; KANTO CHEMICAL) mangrove species (B. gymnorrhiza and R. stylosa) was solution was used as the standard reagent, and the value almost twice as large as that for D. trifoliata (Fig. 5). obtained through these procedures was defined as the The amount of tannins in all the leaf litter and the tannin content. amount removed by crabs were estimated to be 92.6 and 65.1 gm－2y－1, respectively (Table 4). 2. 4. Statistical analyses Differences in the amounts of litterfall, standing stock 3. 2. Seasonal changes of litter on the forest floor, tidal export of litter, and litter Monthly changes and the distribution of litterfall are removal by crabs were compared between species with shown in Figs. 5 and 6. As shown in Fig. 5, the amounts one-way analysis of variance (ANOVA) using Excel for of litter removed by crabs from B. gymnorrhiza and R. Windows (Excel Toukei 2010, SSRI). The Kruskal-Wallis stylosa accounted for over 70% of each monthly total, test was used to compare any two tree species. Means throughout the year. In particular, there was no standing and standard error values were calculated from the data stock of leaf litter in summer (from August to October). sets derived from the litter catchers. On the other hand, the amounts of litter removed by crabs from D. trifoliata accounted for less than 50% of the 3. Results total, except for the period from August to December. 3. 1. Amounts of litterfall, standing stock, tidal As shown in Fig. 6, when the strongest typhoon export, removal by crabs, and tannins in leaves experienced during the study period hit the island in The total amount of litterfall was 1220±63 gm－2y－1 May 2012, the largest amount of litterfall was collected (mean±SE ; n＝5). The amounts removed by crabs, tidal (35% of the annual total). As a result, the total litterfall export, and the standing stock of litter were estimated to for the months of May, June and August when typhoons be 845 (69.0%), 261 (21.3%) and 119 (9.7%) gm－2y－1, hit the study area three times was 654 gm－2y－1, a c - respectively (Table 3). The amounts of leaf litter counting for 54% of the annual litterfall.

Table 3 Amounts of litterfall, litter removal by crab, standing stock of litter, and tidal export in Shimajiri mangrove estuary, Miyako Island, Okinawa (Apr. 2011 to Mar. 2012). The different letters show significant differences (P＜0.01). 146 Matsutani, Nagai and Nakanishi

4. Discussion

The amount of litterfall in a subtropical mangrove forest consisting of Rhizophora stylosa, Bruguiera gymnorrhiza and Derris trifoliata was 1220 gm－2y－1 (Table 3). This amount is similar to the results obtained from study sites in tropical areas (1131 gm－2y－1 in Australia22） ; 930 gm－2y－1 in Australia23） ; 886 gm－2y－1 in Malaysia24）). (a) Bruguiera gymnorrhiza However, the annual amount of leaf litter obtained in this study, 967 gm－2y－1 (Table 3) is much greater than the amount observed in Jiulongjiang estuary, a subtropical area in the south of (648 gm－2y－1)13）. They also pointed out that removal rates of leaf litter by crabs in subtropical mangroves were less than those in tropical areas, especially in winter. However, in this study, although seasonal changes in the monthly removal rates for Rhizophora stylosa were observed in Shimajiri estuary, that for Bruguiera gymnorrhiza was not clear as shown in Fig. 5, and the annual removal rate, 69.0% as (b) Rhizophora stylosa shown in Table 3, was almost twice as high as the rate observed in the Jiulongjiang estuary (33%). These differences are thought to be caused by the influence of a warm sea current (the Kuroshio Current) flowing north along the islands in Okinawa. Although both study sites, Jiulongjiang and Shimajiri, are located at almost the same latitude, the current helps keep the latter site warmer even in winter. It has been reported previously that when the tannin content is high in plant leaves, the consumption rates of 25） (c) Derris trifoliata detritivorous crabs decrease . However, as shown in Table 3, the results obtained in this study suggested that Fig. 5 Monthly changes in the distribution of litterfall Neosarmatium smithi selectively collected leaves of man- (Shimajiri, Miyako Island : April 2011 to March 2012). grove species (B. gymnorrhiza and R. stylosa) which con- ■ Removal by crab ■ Tidal export □ Standing stock tain higher tannins rather than a non-mangrove species (D. trifoliata) which contains less tannins (Table 4). 14） Robertson and Daniel also reported that litter removal rates by crabs in tropical Australia were higher for mangrove species (79% for Bruguiera exaristata and 71% for Ceriops tagel) which contain more tannins than a species (33% for Avicennia marina) which contains less tannins (Table 4). Based on the results obtained in this study on the amounts of leaf litter and the removal by crabs, and tannin contents in the leaves, the amounts of tannins contained in the leaf litter and the removal by crabs were estimated to be 92.6 and 65.7 gm－2y－1, respectively. When tannins react with soil, this causes various Fig. 6 Monthly changes in the amount of litterfall. 7） (Shimajiri, Miyako Island : April 2011 to March 2012) chemical reactions. For example, Levanidov and 6） Arrows indicate the times when typhoons hit Miyako Arakawa et al. reported that tannins form complexes Island. Maximum instantaneous wind velocities were with metal ions such as Fe and Mn in the soil that makes 45.9 (May), 32.2 (June) and 29.9 (August) ms－1. them water soluble. Normally, dissolved Fe is one of the Litterfall Removal by Detritivorous Crabs in a Mangrove Forest of Miyakojima Island 147

Table 4 Estimated amount of tannins in Elution of dissolved Fe from mangrove soil by tannin solu- leaf litter removed by detritivorous tion. Wetlands Ecology and Management, 21 (2), 107-115. crabs to their burrows. 9） Spalding M, Kainuma M and Collins L (2010) World Atlas of mangroves. Earthscan, London. 10） Micheli F (1993) Feeding ecology of mangrove crabs in North Eastern Australia : mangrove litter consumption by Sesarma messa and Sesarma smithii. 11） Ashton C. Elizabeth (2002) Mangrove sesarmid crab feeding experiments in Peninsular . Journal of Experimental Marine Biology and Ecology, 273, 97-119. 12） Kristensen E (2008) Mangrove crabs as ecosystem engi- neers ; with emphasis on sediment processes. Journal of Sea Research, 59, 30-43. 13） Chen G C, and Ye Y (2008) Leaf consumption by Sesarma plicata in a mangrove forest at Jiulong Estuary, China. Marine Biology, 154 : 997-1007. critical elements that control the growth of phytoplankton 14） Robertson A I and Daniel P A (1989) The influence of crabs in aquatic ecosystems as Fe is easily oxidized into on litter processing in high intertidal mangrove forests in tropical Australia. Oecologia, 78, 191-198. insoluble forms. 15） Slim F J, Hemminga M A, Ochieng C, Jannink N T, E Cocheret Therefore, if detritivorous crabs selectively collect de la Morinière and G van der Velde (1997) Leaf litter mangrove leaves containing high levels of tannins and removal by the snail Terebralia palustris (Linnaeus) and carry them into their burrows, this behavior could play a sesarmid crabs in an East African mangrove forest (Gazi very important role in increasing opportunities for the Bay, Kenya). Journal of Experimental Marine Biology and Ecology, Vol. 215, (1) 35-48. tannins in leaves to react with Fe in the forest floor soil, 16） Lee SY (1989) The importance of sesarminae crabs Chiro- thereby making dissolved Fe available to phytoplankton manthes spp. and inundation frequency on mangrove in mangrove and coastal ecosystems. The dynamics of (Kandelia candel (L.) Druce) leaf litter turnover in a Hong tannins in the body and feces of the crab are still Kong tidal shrimp pond. Journal of Experimental Marine Biology and Ecology, Vol. 131, (1) 17, 23-43. outstanding topics. 17） Mokolensang J F and Tokuyama A (1998) Litter produc- Acknowledgements tion of mangrove forest at the Gesashi river. Bulletin of the College of Science, 65, 73-79. This study was partly funded by the Silviculture 18） Mfilinge PL and Tsuchiya M (2008) Effect of temperature on leaf litter consumption by grapsid crabs in a subtrop- Meeting of the Fukuzawa Fund of Keio University． ical mangrove (Okinawa, Japan). Journal of Sea Research, 59, 94-102. References 19） Japan Meteorological Agency (2011) Weather statistics, 1） Kuma K, Nishioka J and Matsunaga K (1996) Controls on (http : //www.jma.go.Jp/jma /menu/report.html). iron (III) hydroxide solubility in seawater : The influence 20） Yi M L, Jin W L, Ping X, Peng L, Zhen H D, Sternberg L S L of pH and natural organic chelators, Limnology and (2007) Tannin and nitrogen dynamics in mangrove leaves Oceanography 41 (3), 396-407. at different age decay stages (Jiulong River Estuary, 2） Matsunaga K, Nishioka J, Kuma K, Toya K and Suzuki Y China), Hydrobiologia 583, 285-295. (1998) River input of bioavailable iron supporting 21） Julkunen-Tiitto R (1985) Phenolic constituents in the leaves phytoplankton growth in Kesennuma bay. Water of northern willows: methods for the analysis of certain Research, 32, 11, 3436-3442. phenolics. 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宮古島の島尻マングローブ林帯における植食性カニ によるリター持ち去り量の定量 松谷達馬*・長井 隆**・中西康博*** †

（平成 25 年 5 月 23 日受付/平成 25 年 9 月 10 日受理）

要約：マングローブ葉中タンニンが林床土壌と接触するまでの動態を明らかにするため，日本の亜熱帯域に 位置する沖縄地域の宮古島の島尻地区マングローブ林において，リターキャッチャーを用いて植食性カニに よる落葉の巣穴への持去り量を通年調査した。得られた結果は以下の通りである。1）リター総量は 1221 gm－2y－1 であり，そのうちカニによる持去り率，林床への現存率，及び海域への持去り率はそれぞれ68.9，9.6 及び 21.4% であった。2）総リター量における各樹種（Bruguiera gymnorrhiza, Rhizophora stylosa 及び Derris trifoliata）の重量割合はそれぞれ 61.4，31.1 及び 7.5% であり，各樹種葉のカニによる持去り率はそ れぞれ 72.8，69.3 及び 35.7% であった。カニによる落葉の巣穴持去り率はタンニン含有率の高いマングロー ブ樹種において高かった。3）落葉及びカニに持去られた落葉中のタンニン含量は，それぞれ 92.6 及び 65.7 gm－2y－1 であった。これらの結果から，植食性カニがマングローブ葉を選択的に摂食するという行為は，葉 中タンニンと林床土壌との接触機会を増加させ，溶存 Fe 溶出を促進させる可能性が示唆された。

キーワード：マングローブ，リターフォール，植食性カニ，林床土壌，タンニン

* 東京農業大学大学院農学研究科環境共生学専攻 **（財）沖縄県環境科学センター *** 東京農業大学国際食料情報学部国際農業開発学科 † Corresponding author（E-mail : [email protected]）