Abstract

To understand the mobility of trace elements from the environment and transfer across trophic levels in mangrove ecosystem, several associated studies have been conducted including study of food preference of the giant mudskipper (Periophthalmodon schlosseri), assessment of trace elements in sediments, mudskippers and its food items, and designing an ecological model of trace elements mobility in mangrove ecosystem. Several methods have been adopted including stomach content and stable isotopes analyses, and assessment of trace elements in sediments and biota tissues. Results showed trace elements level in sediments of Peninsular Malaysia were range from "unpolluted" to "very severely polluted", depending on activities occurring around the sampling area. Stomach content and stable isotopes analyses showed feeding preference of the mudskipper is depended on sexes and life stages. Bioaccumulations of trace elements in organs of the mudskipper were closely related with the functions and existing physiological activities. Trace elements were found low in lower trophic level and increase with increasing trophic level. Combination of stable isotopes analysis and trace elements concentrations in tissue samples showed biomagnification of certain trace elements occurred in the mangrove ecosystem.

Introduction

In present days, the field of ecotoxicology has become an important subject since various kinds of pollutants that are reported or potentially threats the environment and biota, including trace elements, dioxin, PCB, PAHs etc. Locally in Peninsular Malaysia, a deliberate but increasing understanding and paradigm shift on environmental issues among professionals and public communities has offered a new hope on resolving existing problems. Current practice on assessing and monitoring chemical contamination still apply conventional approaches in which studying effects of chemicals on separate organisms and hypothesize their effects on consumers at the upper level along the food chain. Present study used a novel approach to study the mobility of trace elements in the mangrove ecosystem. In order to justify the main objective, a few objectives were set: (1) assess the background level of trace elements in the surface sediments; (2) study the food preference of the sentinel species in mangrove area, the giant mudskipper (Periophthalmodon schlosseri); (3) determine bioaccumulation of trace elements in P. schlosseri and its' food items: (4) design a conceptual model for mobility of trace elements in the mangrove ecosystem

Materials and Method

Surface sediments were collected from intertidal areas around Peninsular Malaysia (Fig. 1). P. schlosseri and its' food items were collected from the mangrove area of Puloh River (Site # 7 on the map). All samples were stored at cooled temperature (-20oC) prior further analytical procedures. Assessments of trace elements were conducted according established methods including the aqua-regia method (ISO11466) for sediments, and microwave-assisted digestion method (Yang et al. 2004) for biota. Concentrations of trace elements were determined using an ICP-MS. The food preference of P. schlosseri was determined using the stomach content- (Hyslop 1980; Cortes 1997) and stable isotopes- (Nakamura et al. 2008) analyses. Pollution status in respective sampling station was determined by comparing with the Interim Sediment Quality Guidelines (ISQGs) of ANZECC/ARMCANZ and Hong Kong, and calculations of the enrichment factors (EF) and the geoaccumulation index (Igeo). Accuracy of analytical methods were determined using certified reference materials (trace elements: SRM 1646a, DORM-2 and SRM 1577b; stable isotopes: atmospheric nitrogen (N2) and Vienna- Pee Dee Belemnite (V-PDB)) with acceptable recovery values.

Results and Discussion

1) Trace elements in sediment of Peninsular Malaysia

In general, concentration of trace elements in surface sediments can be arranged as follows: Fe > Mn > Zn > V > As > Cr > Pb > Cu > Ni > Co > U > Mo > Ag > Cd. Concentrations of trace elements obtained in present study were within the range of other studies conducted around the world, except for V, As and U (Table 1). Data screening using a few simple calculation showed only certain locations around Peninsular Malaysia had mean concentration above ISQG-high and/or ISQG-low, thus raise a possibility that some biota species have been affected by these elements in the involved areas. After calculation using the EF and Igeo, trace elements in sediments were ranged between "no enrichment" and "extremely sever enrichment", and "unpolluted" and "very strongly polluted", respectively. Developed areas with high density of manufacturing industries, agricultural based industries (oil palm, rubber, etc.), husbandry and poultry farms, transportations, landfills, domestic wastes industrial, population and sea vessels were areas strongly related with high contamination of trace elements (e.g. Pasir Gudang, Lumut, Perai, Klang etc.). There for, we concluded that contamination of trace elements were localized in vicinity of nearby sources.

2) Food preference of P. schlosseri

As for the food preference of P. schlosseri, combination of stomach content analysis and stable isotope analysis was found to be perfect tools to investigate this matter (Fig. 2). Although the stomach content analysis revealed that there were four groups of food items for P. schlosseri (Uca sp., Oryzias sp., juveniles of other fish species, and unknown remainings), later the stable isotope analysis managed to exclude uncommon food items. The main food items were verified as Uca sp. and Oryzias sp. only. The unknown remainings were found to be either digested or partly digested of these main food items. Selection of food items was also influence by sexes and maturity stages, possibly due to different behavior and living strategy.

3) Trace elements in P. schlosseri and its' food items

The next stage was to assess trace elements concentration in P. schlosseri and its' food items. Bioaccumulation trend of selected trace elements in P. schlosseri can be arranged as follows: Fe > Zn > Mn > Cu > Cr > As > Ni > Pb > Cd. There was no significant difference in bioaccumulation of most trace elements among different sexes, except for Ni, Cu and As. However, bioaccumulation of trace elements was found significantly different among different maturity stages. Distribution of these elements was varied, depending on functions and metabolic activities occurring in each organ. In general, the most of highly bioaccumulated elements were found in detoxifying organs (spleen, liver and kidney) and those having calcified structures (bone and gills). In some occasions, other organs (i.e. brain, eye and gonad) were found bioaccumulated significantly high concentration certain elements due to adaptation and specific purposes. For the food items of P. schlosseri, Uca sp. was found bioaccumulated with higher concentration trace elements than Oryzias sp., except for Ni, Cu and As. In general, Cu and Zn was found occurring at higher concentration in invertebrates than their predator at the upper trophic level(s) since they are known to bound at metal-rich granules and sequestered as a detoxified forms, prior excretion out of their body.

4) Mobility of trace elements in mangrove area

Finally is about the mobility of trace elements in the mangrove ecosystem in relation with stable isotopes (δ13C and δ15N) ratios. Concentration of trace elements in each biota was correlated with the stable isotope ratios. Correlation analysis was used in present study to verify biomagnification process occur at the upper trophic level in the mangrove ecosystem of Puloh River. All non-essential trace elements (Ni, As, Cd and Pb) certain essential trace elements (Cr, Mn, Fe and Zn) were found biomagnified along the food chain. Cu was not biomagnified. A conceptual ecological model for the mobility of trace elements in the mangrove ecosystem was design to give clear illustration of transporting process of trace elements across trophic levels (Fig. 3). Biomagnification factors were calculated for respective trace elements and the results showed the factors increased with the increase of trophic level.

Conclusion

In conclusion, present study identified trace elements contaminations in sediments around Peninsular Malaysia were localized in vicinity of their sources. Bioaccumulation of trace elements in P. schlosseri was found highly bioaccumulated in detoxifying organs and calcified structures. Combination of stomach content and stable isotope analyses was found as ideal combination to identify the food preference of P. schlosseri from Puloh River, which comprised only Uca sp. and Oryzias sp. Biomagnifications of toxic elements (Ni, As, Cd, Pb) and some essential trace elements (Cr, Mn, Fe) along food chain were proven occurred in the mangrove ecosystem.

Recommendation

Further extensive and comprehensive studies involving assessment of stable isotope ratios and trace elements concentration of organisms at the lower trophic levels will be conducted to improve the conceptual models of trace elements mobility in mangrove ecosystem.

Fig. 1: Sampling location of sediments around Peninsular Malaysia

Table 1: Comparison of trace elements of present study with other studies around the world

Fig. 2: Percentage of prey items according life stages of female and male P. schlosseri (a), and δ13C and δ15N ratios of biota (b) from mangrove area of Puloh River

Fig. 3: A conceptual ecological model of the mobility of trace elements in mangrove ecosystem

本論文は6章からなり、第1章では、沿岸海洋環境保全の重要性とその背景を述べ、マレーシア半島沿岸域が現在直面している環境問題点を指摘し、本論文の研究目的を示した。第2章では、本研究で使用した試料に関する情報と分析方法を記述した。底質標本をマレーシア沿岸域の30地点から採集し、分析するまで-20℃で保存した。底質は表層から深度3-5cmの層から採集した。同時に、マレーシア半島東部のプロ川のマングローブ生態系からMudskipper (Periophthalmodon schlosseri)、メダカ(Oryzia sp.)、カニ(Uca sp.)などの主要な生物試料を採集した。これらの試料を日本に持ち帰り、海洋研究所のICP-MSを使用して、これらの試料中の14種類の金属類(V, Cr, Mn, Fe, Co, Ni, Cu, Zn, As, Mo, Ag, Cd, Pb, U)の濃度を測定した。底質中に存在しているこれらの金属類の平均濃度は国際的な基準以下であること、ならびに金属類の間ではFe>Mn>Zn>V>As>Cr.Pb>Cu>Ni>Co>U>Mo>Ag>Cdの順であることが明らかになった。都市、工業地域、農業地域などでは、これらの金属類による汚染状況が異なり、地域特異性を示していた。第3章では、プロ川の沿岸域のマングローブ生態系に生息しているMudskipperの胃内容物の解析を行い、本種の食性を明らかにするとともに、本種とその胃内容物の安定同位対比の値(δ15Nとδ13C)を比較した。メダカとカニがMudskipperの主な餌生物であるが、その組成はMudskipperの成長段階や成熟雌雄の間で異なっていた。第4章では、Mudskipperの11組織・器官(鰓、心臓、腎臓、肝臓、脾臓、生殖腺、脳、骨、筋肉、皮膚、眼球)に蓄積する金属類の濃度を調査し、それぞれの金属の組織・器官特異性を明らかにした。同時に、第三章で明らかになった食性調査をもとに、食物連鎖を通じて餌生物からMudskipperへの金属類の移行過程を調査した。第5章では、生態系の生物相互関係を明らかにするために、プロ川のマングローブ生態系に生存している生物試料を用いて、安定同位体比と金属類の濃度との関係について検討し、底質からメダカやカニを通じてMudskipperに移行する各金属類の移行を調査し、マングローブ生態系における上記の金属類の挙動を明らかにした。第6章では、各章で得られた成果をもとに、マングローブ生態系の頂点に位置するMudskipperを中心に、14種類の金属類の挙動を総括し、マングローブ生態系の保全と今後の対策について議論した。本研究は、マレーシア沿岸域における金属類の汚染の状況を明らかにするとともに、マングローブ生態系におけるこれらの化学物質の挙動を、Mudskipperとその餌生物を中心に明らかにしたことから、高く評価できる。

なお、本論文第二章の内容は、An assessment of selected trace elements in intertidal surface sediments collected from the Peninsula MalaysiaというタイトルでEnvironmental Monitoring and Assessmentに投稿済みである。本章は、Mohamat-Yusuff, 氏、A. Ismail氏、新井崇臣氏、宮崎信之氏との共同研究であるが、論文提出者が主体となってデータ収集および解析を行ったもので、論文提出者の寄与が充分であると判断する。したがって、博士(環境学)の学位を授与できると認める。

以上、本研究は、海洋環境の解明に極めて有意義な知見を得たことから、学術上、応用上貢献することが少なくない。よって審査委員一同は本論文が博士(環境学)の学位論文として価値があるものと認めた。