A Role of a Herbivorous Crab, Neosarmatium Smithi, in Dissolved Iron Elution from Mangrove Ecosystems

ISSN : 0917-415X DOI:10.3759/tropics.MS19-06 TROPICS Vol. 28 (4) 91-97 Issued March 1, 2020 ORIGINAL ARTICLE A role of a herbivorous crab, Neosarmatium smithi, in dissolved iron elution from mangrove ecosystems Yasuhiro Nakanishi1*, Tatsuma Matsutani1, Ko Hinokidani1, Takashi Nagai2 and Mami Irie1 1 Graduate School of Agriculture, Tokyo University of Agriculture, 1-1-1 Sakuragaoka, Setagaya-ku, Tokyo 156-8502, Japan 2 Environment Science Department, Incorporated Foundation Okinawa Prefecture Environment Science Center, 720 Kyozuka, Urasoe, Okinawa 901-2111, Japan * Corresponding author: [email protected] Received: July 13, 2019 Accepted: November 21, 2019 ABSTRACT Iron solubilization in mangrove soils associated with polyphenols leached out from leaf-litter can improve iron bioavailability. In this context, the leaf-removing process by mangrove crabs would increase reacting frequency of the polyphenols in mangrove leaves with iron in the soils. In this study, we investigated ecological roles of a leaf-removing crab, Neosarmatium smithi, on the iron solubilization process. After the fallen leaves carried by the crabs to their burrows and eaten by them, polyphenols may be remained in their feces. If so, contact of polyphenols in the feces with mangrove soils could promote elution of dissolved iron from the soils. In order to demonstrate this hypothesis, we firstly surveyed the appearance ratio of the black part in crab burrows and measured total phenolic content in feces of N. smithi as well as in the black part soil. Then, we examined influences of the crab feces on dissolved iron elution from mangrove soils. As the results, the appearance ratio of the black part in the burrow was 67 % and the phenolic content in the feces, the black part, and the yellow part in crab burrows were 9.93, 0.49, and 0.12 mg g－1, respectively. Dissolved iron content in the solution (soil＋water extract from feces) was 0.65μg g－1 and this content was 4.5 times higher than the control (soil＋distilled water). We suggest that the polyphenols remained in the feces affect to solubilize insoluble forms of iron by iron reduction and chelating properties. Key words: mangrove, dissolved iron, herbivorous crab, polyphenols, tannins, feces INTRODUCTION were 14.56-40.11 % in dry-weight (Basak et al. 1999), and their ecological effects on nutrients cycle also have been In coastal marine ecosystems, riverine inputs are the investigated (Kraus et al. 2003). Those polyphenols such as dominant sources of nutrients, which contribute to the high tannins leached from leaf-litter can form organic complexes bio-productivity. Among the various nutrients, iron is a with insoluble forms of manganese and iron in soils, micronutrient essential for phytoplankton growth, and it is making them water-soluble forms (i.e. organic metal com- indicated that the iron supplying system from land con- plexes; Levanidov 1957; Arakawa et al. 1993; Matsutani et tributes significantly to primary production in marine al. 2013a). ecosystem, especially of coastal area (Martin and Fitzwater We have focused on this chemical property and simply 1988; Martin 1992; Matsunaga et al. 1998; Takeda 1998). demonstrated that the role of the polyphenolic components Attentions have been paid to a hypothesis that forest is a in mangrove leaf-litter on the iron solubilization processes major source of dissolved iron to seawaters. For example, it in mangrove forest soils by a laboratory experiment, and was reported that organic complex iron (e.g. fulvic acid- found the amounts of dissolved form of iron were signifi- iron compound) originated in humus layer in upland forest cantly increased by mixing the water-extracts, which was soils was a major source for the growth of marine phyto- extracted from mangrove leaves by distilled water, with plankton (Matsunaga et al. 1998; Kuma et al. 1996). soils compared with controls (soil＋distilled water). It is known that mangrove species which grow in the Furthermore, the significant positive correlation was shown intertidal zone of the tropics and subtropics contain high between amounts of iron eluted from soil mixed with the amounts of tannins which is classified as polyphenols, in water extract and polyphenolic contents in the water-extract their bark, leaves, and roots. For instance, it was reported which was added to the soil (Matsutani et al. 2013a). This that tannins content in leaves of nine mangrove species result indicated that water-soluble polyphenolic components 92 TROPICS Vol. 28 (4) Yasuhiro Nakanishi, Tatsuma Matsutani et al. Fig. 1. Undegraded mangrove litter observed in the inner wall of crab burrows. Fig. 2. Black parts observed in inner wall of crab burrows. contained in mangrove leaves functioned to solubilize the insoluble iron in mangrove soils. However, the chemical reaction above mentioned is not simple in the field, but it should be more complicated. In the intertidal zone and river mouth where mangroves grow, most of mangrove leaf-litter can be exported by tidal and river activities, which will reduce the reaction frequency of polyphenols in the fallen leaves with the forest soil. On the other hands, the presence of benthic animals that directly consume mangrove leaf-litter could increase the reaction between polyphenolic components leached from leaf-litter and mangrove floor soils by their feeding Fig. 3. Faecal materials of Neosarmatium smithi, rubbed against activities. For example, removal of fallen leaves by crabs the wall of the experimental box. into their burrows are generally known to be an important trophic pathway in mangrove forests, and this process can prevent the tidal export of detritus from mangrove ecosystems to adjacent ecosystems (Micheli 1993; Robertson and 2). To identify the black part, we have observed behavior of Daniel 1989; Ashton 2002; Kristensen 2008; Chen and Ye N. smithi in captivity in laboratory. Then, it was found that 2008). the crab evacuates feces as it was rubbed against the wall of According to our previous study conducted in a sub- the experimental box (Fig. 3), and this behavior explains tropical mangrove forest in Okinawa, southern Japan, it was that the black parts were stemmed from the feces. found that a leaf-removing crab, Neosarmatium smithi, After the fallen leaves carried by the crabs to their removed 71, 70 and 37 % of the total annual litter fall of burrows and eaten by them, polyphenolic components may Bruguiera gymnorrhiza, Rhizophora stylosa (mangrove be remained in their feces. If so, contact of polyphenols in species), and Derris trifoliata (non-mangrove species), the feces with the burrow soil could generate elution of respectively (Matsutani et al. 2013b). From the results, it dissolved iron from the soil. In order to demonstrate this has become clear that leaf-removing crabs carry most of the hypothesis, we firstly surveyed the appearance ratio of the leaf-litter into their burrows and the removing process black part in crab burrows, and measured total phenolic would mean an increased reacting frequency between content in feces of N. smithi as well as in the black part polyphenols in mangrove leaves and iron in the soil. In fact, collected from the crab burrows. Finally, we examined when we have dug up the burrows, many undegraded (or influences of the crab feces on dissolved iron elution from under fed) mangrove leaves were observed in the inner wall mangrove soils. of their burrows (Fig. 1) as well as black colored part (Fig. Role of a mangrove crab in dissolved iron elution 93 METHODS environment (e.g. soils) should be stemmed from plants. Regarding the black part observed on the inner wall of crab Study area burrows, if the black part contains much polyphenols, it would demonstrate that the black part is faecal material The study area selected was Shimajiri estuary (24°52′ deposited by the crabs. N, 125°17′E) on Miyako Island, Okinawa as the area is For this reason, we examined the total phenolic content conserved by the local municipality to maintain natural in the inner wall soils of their burrow and in feces of N. conditions and located close to our research station (Miyako smithi. Subtropical Farm, Tokyo University of Agriculture), being Faecal material: We collected 16 individuals of N. only about 15 km away. The climate of this area is sub- smithi crabs (male: n＝8; female: n＝8), with carapace tropical, and the average annual rainfall and air temperature width from 25 to 40 mm, from the study site on April and are 2,034 mm and 23.6 ℃, respectively. The difference November in 2012. Each crab was kept individually in a between the annual highest and lowest tide levels in the plastic box (Polypropylene; L400×W250×H200 mm; n＝ estuary is 2.3 m. 16) with 5 mm depth of brackish water (salinity: 1.5 %) and Vegetation in the estuary is a mixed forest containing starved for 2 days in captivity (room temp.; 25±5 ℃). five species; Rhizophora stylosa, Bruguiera gymnorrhiza, After the starvation, faecal samples (n＝16) which were Derris trifoliata, Avicennia marina, and Kandelia obovata adhered on the plastic wall were gathered from each box. in order of stem densities. Except for D. trifoliata, all of the Inner wall soil: In the upstream area of Shimajiri species are classified as mangroves (Spalding et al. 2010). estuary on November 11 in 2012, we collected two kinds of The width from the creek edge to the bank edge in the soil samples from the inside wall surface of the crab forest is about 2 to 20 m, and the length of forest from the burrows; soils black in colour (the black part: n＝16) and creek mouth to the upper end is about 500 m. Detritivorous soils yellow in colour (the yellow part: n＝16). Each part crabs inhabiting the estuary were Neosarmatium smithi, was collected carefully using a spatula.

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