Akinori Yamada, Ph.D. Last Updated: 27 11 08 Science Camp at Sakaerat Environmental Research Station, Thailand, on 29 Sep 2008.
CURRICULUM VITAE EDUCATION 2004 _ Doctor of Science, Center for Ecological Research, Graduate School of Science, Kyoto University 2001 _ Master of Science, Center for Ecological Research, Graduate School of Science, Kyoto University 1999 _ Bachelor of Science, Animal Ecology Laboratory, Faculty of Science, Kyoto University
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Abstract: <span style="font-style:normal">Deep-sea hydrothermal vents are unique light-independent ecosystems that are sustained by chemosynthetic bacteria. For many of the invertebrates inhabiting in such environments, bacteria play essential roles in both energy acquisition and detoxification of potentially toxic gases such as H<sub>2</sub>S. In this study, the bacterial flora present on the gills of <i>Alvinocaris longirostris</i> (Bresiliidae: Caridea), a shrimp inhabiting hydrothermal vents (1532 m depth) at the Hatoma Knoll of the Okinawa Trough, was investigated. Bacterial 16S rDNA fragments were successfully amplified from the gills and 70% of these fragments showed an identical pattern in the restriction fragment length polymorphism analysis. These fragments were assigned to the ribotype AL-1. Phylogenetic analyses suggest that AL-1 forms a monophyletic clade with <i>Sulfurovum</i> spp. (ε-Proteobacteria). Fluorescence in situ hybridization for AL-1 and electron microscopy showed the presence of short-rod bacteria lining up on the cuticular layer of the surface of the gill filaments. These results suggest that bacterial association with gills also occurs in bresiliid shrimps.</span>
Abstract: <span style="font-style:normal">The frequency of single strand breaks (SSBs) occurring on both strands of the pBR322 plasmid DNA region flanked by a pair of primers used for polymerase chain reaction (PCR) amplifications was determined after irradiation with <sup>137</sup>Cs g rays. We verified that real time PCR is suitable for the detection and quantitative analysis of SSBs caused by g ray irradiation. The utility of this approach was also supported by the comparison of the practical experimental data with the Monte Carlo simulation. The potential application of this PCR method for the detection of genomic DNA damage was also confirmed.</span>
Abstract: <span style="font-style:normal">Mounds of the termite <i>Amitermes laurensis</i> in northern Queensland, Australia, are frequently invaded and occupied by the meat ant <i>Iridomyrmex sanguineus</i>, but their interactions remain unclear. In 1999, 68 A. laurensis mounds that were mapped and examined for the presence of the meat ants in 1998 were studied by destructive sampling, and the occupancy percentages of the termites were compared during the 2 years of meat ant occupation. The results indicate that the occupancy percentages of the termites in the intact mounds (79%) are significantly different from those in the mounds that were occupied by the meat ants in 1998 (58%), 1999 (42%), or both (20%). Although the mean vales showed apparent differences, no significant difference was observed in the occupancy percentages among the latter three cases. Our results suggest that the meat ants are not lethal invaders of the termite mounds and that the recovery of the termite populations occurs after the meat ants abandon the mounds.</span>
Abstract: <span style="font-style:normal">A recent report by A. Yamada, T. Inoue, D. Wiwatwitaya, M. Ohkuma, T. Kudo, T. Abe & A. Sugimoto (2005) has suggested that the carbon (C) source competition between termites and litter-layer microbes may be employed for understanding the C mineralization processes in tropical forests, but the situation in dry tropical ecosystems (e.g., savannas) and the possible intergroup competition in termites remain unclear. Here, we observed termites in a dry tropical ecosystem (dry deciduous forest (DDF)) and a high-altitude tropical forest (hill evergreen forest (HEF)) in Thailand and estimated the C fractions in the annual aboveground litter fall (AAL) mineralized by the termites. In the DDF, 5.1% of the AAL was mineralized by termites, with dominant contribution from the fungus-growing group. In such dry tropical ecosystems, fire rather than litter-layer microbes is likely to be the most important limiting factor for the C source that can be used and mineralized by termites. On the other hand, termites contributed to the C mineralization of 4.2% of the AAL in the HEF, while the soil-feeding group played a substantial role. When comparing the importance of each termite group in Asian and African tropical forests, the smaller contribution of the fungus-growers and the larger contribution of the soil-feeders in the HEF suggests the presence of an asymmetric C source competition between the fungus-growers and soil-feeders through the C flow from the litter layer into the soil.</span>
Abstract: <span style="font-style:normal">Nitrogen fixation by gut microorganisms is one of the crucial aspects of symbiosis in wood-feeding termites since these termites thrive on a nitrogen-poor diet. In order to understand the evolution of this symbiosis, we analysed the nitrogenase structural gene nifH in the gut microbial communities. In conjunction with the published sequences, we compared approximately 320 putatively functional NifH protein sequences obtained from a total of 19 termite samples that represent all the major branches of their currently proposed phylogeny, and from one species of the cockroach <i>Cryptocercus</i> that shares a common ancestor with termites. Using multivariate techniques for clustering and ordination, a phylogeny of NifH protein sequences was created and plotted variously with host termite families, genera, and species. Close concordance was observed between NifH communities and the host termites at genus level, but family level relationships were not always congruent with accepted termite clade structure. Host groups examined included basal families (Mastotermitidae, Termopsidae, Kalotermitidae, as well as <i>Cryptocercus</i>), the most derived lower termite family Rhinotermitidae, and subfamilies representing the advanced and highly diverse apical family Termitidae (Macrotermitinae, Termitinae, and Nasutitermitinae). This selection encompassed the major nesting and feeding styles recognized in termites, and it was evident that NifH phylogenetic divergence, as well as the occurrence of alternative nitrogenase-type NifH, was to some extent dependent on host lifestyle as well as phylogenetic position.</span>
Abstract: <span style="font-style:normal">Termites are dominant invertebrates in tropical soils (Wood & Sands 1978) and are important mediators of decomposition in terrestrial ecosystems (Abe & Matsumoto 1979, Lawton <i>et al</i>. 1996, Lee & Wood 1971, Matsumoto & Abe 1979, Wood & Sands 1978, Yamada <i>et al</i>. 2005). Furthermore, these processes, such as carbon mineralization and nitrogen fixation, are dependent on the species assemblage structure of the termite community (Lawton <i>et al</i>. 1996, Yamada <i>et al</i>. 2005, 2006). Feeding habits of termites reflect their metabolic processes. The three major isopteran groups â wood-feeders, fungus-growers (fungus-growing wood/litter feeders), soil-feeders â appear to play very different roles in the decomposition process (Tayasu <i>et al</i>. 1997, Wood 1976, Wood & Sands 1978, Yamada <i>et al</i>. 2005). Consequently, the relative abundance of each feeding group provides useful information on the function of the termite assemblage in an ecosystem.</span>
Abstract: <span style="font-style:normal">Nitrogen (N) fixed by termites was evaluated as a N input to decomposition processes in two tropical forests, a dry deciduous forest (DDF) and the neighboring dry evergreen forest (DEF), Thailand. A diverse group of termite species were assayed by acetylene reduction method and only the wood/litter-feeding termites were found to fix N. More intensive samplings of two abundant species, <i>Microcerotermes crassus</i> and <i>Globitermes sulphureus</i>, were done across several seasons, suggesting N fixation rates of 0.21 and 0.28 kg ha<sup>â1</sup> y<sup>â1</sup> by termites in the DDF and DEF, respectively. Also, estimates of asymbiotic N fixation rates were 0.75 and 3.95 kg ha<sup>â1</sup> y<sup>â1</sup>. N fixed by termites and by asymbiotic fixers is directly supplied to decomposers breaking down dead plant material and could be a major source of their N. N fixed by termites was 7â22% of that fixed by termites and asymbiotic fixers. Although N fixed by termites is a small input compared to other inputs, this N is likely important for decomposition processes.</span>
Abstract: <span style="font-style:normal">Deep-sea hydrothermal vents and methane seeps are extreme environments that have a high concentration of hydrogen sulphide. However, abundant unique invertebrates including shrimps of the family Bresiliidae have been found in such environments. The bresiliid shrimps are believed to have radiated in the Miocene (less than 20 Myr); however, the period when and the mechanisms by which they dispersed across the hydrothermal vents and cold seeps in oceans worldwide have not been clarified. In the present study, we collected the deep-sea blind shrimp <i>Alvinocaris longirostris</i> from the hydrothermal vent site in the Okinawa Trough and carried out the first investigation of the 18S rRNA gene of a bresiliid shrimp. The phylogenetic analysis revealed that the bresiliid shrimp is situated at an intermediate lineage within the infraorder Caridea and shows monophyly with palaemonid shrimps, which live in shallow sea and freshwater. Furthermore, the mitochondrial cytochrome oxidase I (COI) gene sequences were analysed to determine the phylogenetic relationship with known bresiliid shrimps. <i>A. longirostris</i> of the Okinawa Trough had two haplotypes of the COI gene, one of which was identical to the <i>Alvinocaris</i> sp. of the cold seeps in Sagami Bay. These results indicate that a long-distance dispersal of <i>A. longirostris</i> occurred possibly within the last 100,000 years.</span>
Abstract: <span style="font-style:normal">The relictual <i>Mastotermes darwiniensis</i> is one of the world's most destructive termites. Like all phylogenetically basal termites, it possesses protozoa in its hindgut, which are believed to help it digest wood. L. Li, J. Frohlich, P. Pfeiffer, and H. Konig (Eukaryot. Cell 2:1091-1098, 2003) recently cloned the genes encoding cellulases from the protozoa of <i>M. darwiniensis</i>; however, they claimed that these genes are essentially inactive, not contributing significantly to cellulose digestion. Instead, they suggested that the protozoa sequester enzymes produced by the termite in its salivary glands and use these to degrade cellulose in the hindgut. We tested this idea by performing gel filtration of enzymes in extracts of the hindgut, as well as in a combination of the salivary glands, foregut, and midgut. Three major cellulases were found in the hindgut, each of which had a larger molecular size than termite-derived salivary gland enzymes. N-terminal amino acid sequencing of one of the hindgut-derived enzymes showed that it was identical to the putative amino acid sequence of one mRNA sequence isolated by Li <i>et al</i>. (Eukaryot. Cell 2:1091-1098, 2003). The overall activity of the hindgut cellulases was found to be of approximately equal magnitude to the termite-derived cellulases detected in the mixture of salivary gland, foregut, and midguts. Based on these results, we conclude that, contrary to Li <i>et al</i>. (Eukaryot. Cell 2:1091-1098, 2003), the hindgut protozoan fauna of <i>M. darwiniensis</i> actively produce cellulases, which play an important role in cellulose digestion of the host termite.</span>
Abstract: <span style="font-style:normal">A role of termites in decomposition processes was quantitatively evaluated in a dry evergreen forest (DEF) in Thailand, using respiration rates and biomasses of fungus combs as well as of termites themselves. The termite population and fungus combs mineralized 11.2% of carbon (C) in the annual aboveground litterfall (AAL) by their respiration. Fungus combs were responsible for a major part (7.2% of the AAL) of the C mineralization mediated by termites. For comparison, fractions of AAL mineralized by respiration from termite populations and fungus combs were estimated for tropical forests and savannas where termites
have been well studied, assuming that there is the same ratio as for the DEF between biomass of fungus combs and abundance of fungus growers. Termites in dry tropical forests (annual rainfall<2,000 mm) are shown to mineralize about 10% of C in the AAL by respiration from their populations and fungus combs, and their ecological impact in savannahs is comparable in this aspect. A significant negative correlation between fraction of AAL and annual rainfall demonstrates that the importance of termites in decomposition processes is greater in dry tropical forests than in moist tropical forests. Considering that fungus combs contributed
significantly to AAL mineralization in most of the tropical forests and savannas, fungus growers are a much more influential group than previously expected in tropical ecosystems.</span>
Abstract: <span style="font-style:normal">Four strains of hydrogenotrophic methanogens showing narrow ranges of utilizable substrates were isolated in pure cultures from the guts of various feeding groups of (phylogenetically) higher termites. An analysis of the 16S rRNA gene sequence revealed that three strains were closely related to <i>Methanobacterium bryantii</i> (>99% nucleotide identity), the other to the genus <i>Methanobrevibacter</i>. The latter was related to a clone identified previously from the gut of a higher termite without cultivation (clone MPn19) and <i>Methanobrevibacter arboriphilicus</i> (99.0 and 97.9% nucleotide identity, respectively) but distinct from the species identified in lower termites. The specific detection of related methanogens in the gut population by nested-PCR indicated that every termite harbored the species of <i>Methanobrevibacter</i>. However, the methanogen related to the <i>Methanobacterium</i> strain was not detected in two termite species from which the <i>Methanobacterium</i> strains were isolated, suggesting that they are less prevalent in the gut community.</span>
Abstract: <span style="font-style:normal">The families Termitidae and Rhinotermitidae are the most evolved and diverse groups of the social insects, termites (Order Isoptera), showing elaborated morphology and complex behavior. Molecular phylogeny of termites with the emphasis on these families was examined by Bayesian and maximum-likelihood analyses based on DNA sequence of mitochondrial cytochrome oxidase II (COII) gene of 31 genera sampled in Asia (mainly Thailand and Japan) along with those reported previously. Termitidae was monophyletic and originated from within polyphyletic Rhinotermitidae. Among the four subfamilies of Termitidae, Macrotermitinae was monophyletic suggesting a single common origin of fungus-growing habit characteristic for this subfamily, and was placed in the basal position in the family. A group consisting of other subfamilies Termitinae and Nasutitermitinae, though some important groups were still untouched, was the most apical but neither Termitinae nor Nasutitermitinae formed a monophyletic lineage. It was implied that, as defense systems of the soldier castes, the appearance of snapping mandibles has occurred at a single event, but the development of nasus for chemical secretion has probably not. Our tree provides some evidence concerning contradictions in the previously proposed phylogeny of termites.</span>
Abstract: <span style="font-style:normal">Phylogenetic relationships, diversity, and in situ identification of spirochetes in the gut of the termite <i>Neotermes koshunensis</i> were examined without cultivation, with an emphasis on ectosymbionts attached to flagellated protists. Spirochetes in the gut microbial community investigated so far are related to the genus <i>Treponema</i> and divided into two phylogenetic clusters. In situ hybridizations with a 16S rRNA-targeting consensus oligonucleotide probe for one cluster (known as termite <i>Treponema</i> cluster I) detected both the ectosymbiotic spirochetes on gut protists and the free-swimming spirochetes in the gut fluid of <i>N. koshunensis</i>. The probe for the other cluster (cluster II), which has been identified as ectosymbionts on gut protists of two other termite species, <i>Reticulitermes speratus</i> and <i>Hodotermopsis sjoestedti</i>, failed to detect any spirochete population. The absence of cluster II spirochetes in <i>N. koshunensis</i> was confirmed by intensive 16S ribosomal DNA (rDNA) clone analysis, in which remarkably diverse spirochetes of 45 phylotypes were identified, almost all belonging to cluster I. Ectosymbiotic spirochetes of the three gut protist species <i>Devescovina</i> sp., <i>Stephanonympha</i> sp., and <i>Oxymonas</i> sp. in <i>N. koshunensis</i> were identified by their 16S rDNA and by in situ hybridizations using specific probes. The probes specific for these ectosymbionts did not receive a signal from the free-swimming spirochetes. The ectosymbionts were dispersed in cluster I of the phylogeny, and they formed distinct phylogenetic lineages, suggesting multiple origins of the spirochete attachment. Each single protist cell harbored multiple spirochete species, and some of the spirochetes were common among protist species. The results indicate complex relationships of the ectosymbiotic spirochetes with the gut protists.</span>
Abstract: <span style="font-style:normal">The abundance and biomass of termites in dead wood were estimated in a dry evergreen forest in Thailand. Litter and dead wood were collected within ten 2 x 2 m quadrats on a 100 m transect, and then all termites in the litter and dead wood (= termites in dead wood) were dislodged. The biomass of litter and dead wood was 2.50 kg (dry weight) m<sup>-2</sup>, of which 76% was represented by dead wood with a diameter of ⥠1 cm. A total of 239 pieces of dead wood (diameter ⥠1 cm) were collected, and 38 of them contained termites. The frequency of termites in dead wood was significantly different between pieces with a diameter of 1-5 cm and pieces with a diameter of ⥠5 cm. The abundance and biomass of termites in dead wood were 1269 termites m<sup>-2</sup> and 3.53 g m<sup>-2</sup>, respectively. A total of 11 species, comprising Kalotermitidae, Rhinotermitidae and Termitidae, were collected; all of them belonged to the wood/litter-feeding group. Using our previous estimation for termites in the soil and data from other studies, the abundance and biomass of termites in the dry evergreen forest were estimated to be 7794 termites m<sup>-2</sup> and 16.7 g m<sup>-2</sup>, of which 16 and 21%, respectively, were represented by termites in dead wood. Our study confirmed the importance of termites in dead wood in tropical seasonal forests.</span>
Abstract: <span style="font-style:normal">The abundance and biomass of subterranean termites were assessed in the dry evergreen forest within the Sakaerat Environmental Research Station, northeast Thailand. The samplings were carried out by pit-digging in November 1998 (during rainy season) and February 1999 (during dry season). A total of 23 species of termites, comprising 17 genera were identified. Estimated abundance was 6450 tesmites/m<sup>2</sup> in November and 2526 termites/m<sup>2</sup> in February and biomass was 10.74g/m<sup>2</sup> (fresh mass) in November and 5.35g/m<sup>2</sup> in February, although no significant difference was detected in termite abundance and biomass between rainy and dry season. In 30cm depth pit-digging, we found more than 93% of individual termites and more than 94% of total biomass within the top 20cm of soil layer in both samplings. The termite abundance and biomass within the surficial soil layer (0-10cm layer) showed no significant difference between in November and February sampling.</span>
Abstract: <span style="font-style:normal">Subterranean-nesting termites do not colonize across the sea by rafting, and at the same time their winged-termites are also unlikely to fly such a long distance. The subterranean-nesting termite <i>Odontotermes formosanus</i> is common from Southeast Asia to the subtropics of East Asia, and is well-known as being discontinuously distributed in the Yaeyama Islands and the Shuri district of Okinawa Island; therefore, it may be hypothesized that <i>O. formosanus</i> was artificially introduced to Okinawa Island. Here we observed for the termites the vicinity of the Shuri district as well as islands of the Ryukyu Archipelago, and discussed the origin of the termites of Okinawa Island. Although we confirmed the presence in the Yaeyama Islands, we did not find the termites in the Miyako Islands, which situate between the Yaeyama Islands and Okinawa Island. In Okinawa Island, the termites exclusively occurred within a limited area that centers on the Shuri district (the old capital city area in the age of the Ryukyu Dynasty). In addition, by comparing their gene sequences deposited in the database, the populations in the Yaeyama Islands and Okinawa Island were estimated to have been separated relatively recently. We suggest that <i>O. formosanus</i> was brought into Shuri from the Yaeyama Islands in the age of the Ryukyu Dynasty in order to provide for the people the termite mushrooms that have been a valuable foodstuff for the local peoples.</span>
Abstract: <span style="font-style:normal">Expansion of <i>Eucalyptus</i> plantation is considered to be one of the major human disturbances to tropical forests, where termites are superabundant and an important decomposer. Here we studied the biomass of dead wood and the abundance and species composition of termites in dead wood in <i>Eucalyptus</i> plantation forest (EF) in Thailand and compared the data with those of the neighboring dry evergreen forest (DEF), which has been previously studied. The biomass of dead wood was much lower in the EF, especially for the dead wood with large diameters (⥠5 cm). Although the abundance of termites (termites m-2) was quite different, the abundance of termites per unit weight of dead wood (termites kg-1) was not different between the two forests, suggesting that the importance of termites in the decomposition is same in these forests. In the EF, however, we did not find the termite species that have been collected in the DEF from the dead wood with large diameters (⥠5 cm). <i>Eucalyptus</i> plantation may affect termite assemblages through the changes of dead wood biomass on the forest floor both quantitatively and qualitatively.</span>
Abstract: <span style="font-style:normal">Despite the obligate mutual relationships between termites and microbes in the guts, it still remains unclear where the symbiotic microbes come. We investigated this by using the termite, <i>Neotermes koshunensis</i>, and their symbiotic methanogenic microbes. Firstly, <i>N. koshunensis</i> colonies were examined for the presence or absence of symbiotic methanogens by microscopic observation and PCR amplification of the 16S rDNA. As a result, methanogens were not detected from some colonies. By keeping termites of these colonies with termites of other <i>N. koshunensis</i> colonies or <i>Coptotermes formosanus</i> colonies (from which methanogens were detected), methanogens were detected from the termites that initially lacked methanogens. These strongly suggest the horizontal transmission of methanogens among termites.</span>
Abstract: <span style="font-style:normal">A recent report (Yamada <i>et al</i>. 2005) has suggested that the carbon (C) source competition between termites and litter-layer microbes may be employed for understanding the C mineralization processes in tropical forests, but the situation in dry tropical ecosystems (e.g., savannas) and the possible intergroup competition in termites remain unclear. Here, we observed termites in a dry tropical ecosystem (dry deciduous forest (DDF)) and a high-altitude tropical forest (hill evergreen forest (HEF)) in Thailand and estimated the C fractions in the annual aboveground litterfall (AAL) mineralized by the termites. In the DDF, 5.1% of the AAL was mineralized by termites, with dominant contribution from the fungus-growing group. In such dry tropical ecosystems, fire rather than litter-layer microbes is likely to be the most important limiting factor for the C source that can be used and mineralized by termites. On the other hand, termites contributed to the C mineralization of 4.2% of the AAL in the HEF, while the soil-feeding group played a substantial role. Comparisons of the importance of each termite group in Asian and African tropical forests indicate that the coincidence of the smaller contribution of the fungus-growers and the larger contribution of the soil-feeders in the HEF, suggesting the presence of an asymmetric C source competition between the fungus-growers and soil-feeders through the C flow from the litter layer into the soil. Key words: fungus-growers, soil-feeders, termites, litter-layer microbes, fire, savannas, tropical forests, carbon source competitions.</span>
Abstract: <span style="font-style:normal">The importance of termites in decomposition processes is widely recognized, and is frequently emphasized especially in savannas. In tropical forests, there have been only a few studies that quantitatively demonstrated the roles of termites as a decomposer. We quantified the importance of termites in terms of carbon mineralization and nitrogen fixation on the basis of biomass data in a dry evergreen forest, northeast Thailand. By using observed respiration rates from termite individuals and fungus-combs with their biomasses, they were estimated to mineralize 11.2% of carbon (C) in the annual aboveground litterfall (AAL). Of these, fungus-combs were responsible for a major part (7.2% of the AAL) of the C mineralization mediated by termites. We measured nitrogen (N) fixation rates of termites and asymbiotic (free-living) bacteria in litter, dead wood and soil, and estimated the total N inputs from fixation to decomposing plant material on the forest floor. Annual mounts of N fixed by termites and asymbiotic bacteria were calculated to be 0.28 and 3.95 kg ha<sup>-1</sup>, respectively, showing that termites are responsible for 6.6% of the total.</span>
Abstract: <span style="font-style:normal">Termites have an important function in the decomposition process in tropical ecosystems. Although the ecological function of termites in savannas is well studied quantitatively in terms of litter removal, there has never been a convincing demonstration in tropical forests because the complex structure of tropical forests provides diverse nesting and feeding habitats for termites. The amounts of nutrients mediated by termites should be elucidated considering their diverse habitats in order to give an answer to the question: how important is the ecological function of termites in tropical forests?<br><br> The present thesis quantitatively shows the ecological function of termites in tropical forests, mainly in Thailand. First, I reveal the termite abundance and biomass with emphasis on termites distributed in dead wood. These are the most basic data for the quantitative evaluation of termites on an ecosystem scale. Then, amounts of carbon mineralization and of nitrogen fixation mediated by termites are elucidated on the basis of abundance and biomass, and compared not only with other mediators within an ecosystem, but also among ecosystems.<br><br> The abundance and biomass of termites in dead wood were observed in a dry evergreen forest (DEF) at Sakaerat Environmental Research Station in Thailand. Litter and dead wood were collected within ten 2 x 2 m quadrats on a 100 m transect, and all termites in the litter and dead wood (= termites in dead wood) were dislodged. The obtained abundance and biomass of termites in dead wood were 1269 termites m<sup>-2</sup> and 3.53 g m<sup>-2</sup>, respectively. A total of 11 species, comprising Kalotermitidae, Rhinotermitidae and Termitidae, were collected; all of them were assigned to wood/litter-feeding termites. The abundance and biomass of termites in the DEF, which consists of termites in dead wood, in the soil and in epigeal nests, were estimated to be 7794 termites m<sup>-2</sup> and 16.7 g m<sup>-2</sup>, using data from previous studies. Termites in dead wood were responsible for 16 and 21% of the abundance and biomass, respectively. This study confirms the importance of termites in dead wood for the estimation of the abundance and biomass of termites on an ecosystem scale.<br><br> In order to evaluate the contribution of termites to the mineralization of annual aboveground litterfall (AALF) in the DEF and a neighboring dry deciduous forest (DDF), the respiration rates of termites and of their symbiotic fungi on fungus-combs were measured. In advance, the biomass of fungus-combs in the DEF and the abundance and biomass of termites in the DDF were observed. Then, amounts of carbon mineralized by termites were determined using the respiration rates and the abundance and/or biomass of termites. As a whole, termites mineralized amounts of carbon equivalent to 11.6 and 7.0% of AALF (Wachrinrat & Takeda 2003 for DEF, Toda & Takeda 2003 for DDF) in DEF and DDF, respectively. Amounts of carbon mineralized by termites were recalculated for other tropical forests and African savannas, using the previously reported and newly obtained data. The values were fully comparable (7.6-13.0%) in two of five forests and in two of three savannas. The contributions of termites were about 1% of AALF in the other three forests. A possible explanation could be found in the obtained negative correlation between annual rainfall and termite abundance. The ecological function of termites is equally important in relatively dry tropical forests as in savannas in terms of carbon mineralization by respiration.<br><br> By dividing the amounts of carbon mineralized by termites into feeding groups, the AALF mineralization process in the DEF is described as follows. Wood/litter-feeding termites (2.7% of AALF for termite population; 7.8% of AALF for fungus-combs) and microorganisms in the litter layer (88.8% of AALF, Yoda & Nishioka 1982) were ascertained to complete AALF mineralization above the ground, indicating negligible carbon flow into the soil. A smaller contribution of soil-feeding termites (1.1% of AALF) is strongly suggested to be related to small amounts of available resources resulting from the negligible carbon flow. These clearly emphasize the importance of fungus-growing termites not only to the mineralization process, but also to the carbon flow into the soil, due to the large contributions of their fungus-combs. In contrast, in tropical forests in Cameroon where a relatively small amount of carbon (3.4% of AALF) was mineralized by wood/litter-feeders, the contribution of soil-feeders was much larger (5.2% of AALF) than in the DEF, probably because an expected increase of carbon flow into the soil provides larger amounts of available resources for soil-feeders. Therefore, fungus-growers are suggested to play the determinant role in the carbon flow into the soil, which may ultimately alter available resources for soil-feeders.<br><br> I observed the rates of nitrogen fixation by termites and by asymbiotic (free-living) bacteria which are distributed in the soil, litter, and dead wood, in the DEF and DDF. First, the acetylene reduction method was used to obtain natural nitrogen fixation rates of termites, and diverse species were assayed to determined the range of nitrogen fixation rates. Then, observations were carried out in rainy and dry seasons on two representative species, <i>Microcerotermes crassus</i> and <i>Globitermes sulphureus</i>, which have dominated the biomass of wood/litter-feeding termites in both the DEF and DDF. Using the obtained nitrogen fixation rates and the biomass of these species, nitrogen was calculated to be fixed at rates of 0.028 and 0.021 g m<sup>-2</sup> year<sup>-1</sup> (0.35 and 0.26 µmol C<sub>2</sub>H<sub>4</sub> m<sup>-2</sup> h<sup>-1</sup>) by termites in the DEF and DDF, respectively. The asymbiotic N fixation rates were also calculated to be 0.395 and 0.075 g m<sup>-2</sup> year<sup>-1</sup> (4.83 and 0.92 µmol C<sub>2</sub>H<sub>4</sub> m<sup>-2</sup> h<sup>-1</sup>) using the nitrogen fixation rates observed in the dry season and the biomass data . The amounts of nitrogen fixed by termites were responsible for obviously small parts of the total nitrogen inputs, which consist of biological nitrogen fixation in termite-symbiotic, plant-symbiotic and asymbiotic forms and of nitrogen in precipitation, into the forests. Meanwhile, the amounts of nitrogen fixed by termites and by asymbiotic forms contribute directly to the decomposition process. Termites in the DEF and DDF represented 7 and 22% of the nitrogen inputs into the decomposition processes, respectively. This indicates the importance of termites to the decomposition process in terms of nitrogen.</span>
Abstract: <span style="font-style:normal">The abundance and biomass of termites in wood were assessed in the dry evergreen forest (DEF) and hill evergreen forest (HEF) in Thailand. Estimated abundance and biomass were largely different between DEF and HEF, and 1269 individual/m<sup>2</sup> and 3530 mg(w.w.)/m<sup>2</sup> in DEF and 5 individual/m<sup>2</sup> and 12 mg(w.w.)/m<sup>2</sup> in HEF. At the same time, the biomass of litter and dead wood was assessedã(3037 g/m<sup>2</sup> for DEF and 1469 g/m<sup>2</sup> for HEF). The termite abundance for unit volume of dead wood was 0.35-0.36 individual/cm<sup>3</sup> (diameter of dead wood ï¼10cm) and 0.07 individual/cm<sup>3</sup> (diameter of dead wood ⥠10cm) in DEF. Those difference was, however, not significant statistically.<br><br> Respiration rates (CO<sub>2</sub> emission rates) of termites in DEF were measured and ranged from 680 CO<sub>2</sub>molÃ10<sup>-8</sup>/hour/g(w.w.) (worker of Procapritermes prosetiger) to 2895 (worker of Schedorhinotermes medioobscurus). Using the CO<sub>2</sub> emission rates of each species, CO<sub>2</sub> emission by total termites in wood was estimated to 1.2 g C/g(w.w.)/year. Using termite biomass observed in soil, mound density and termite in DEF was estimated to be 17.1 g(w.w.)/m<sup>2</sup>. Direct carbon mineralization of organic matters (respiration) by total termites was thus estimated to be 19.6 g C/m<sup>2</sup>/year, which accounted for 1.3% of litter and dead wood biomass and 3.4% of annual litter and dead wood production in DEF. The values are comparable to those observed in savanna when it has been believed termites contribute greatly on decomposition of organic matter. The results in this study suggest on reevaluation of the contribution of termites on the decomposition process in tropical forest may be needed.</span>
Abstract: <span style="font-style:normal">Here, we report the results of our studies on the termites in a dry evergreen forest in Thailand. In this report, we firstly describe the termite fauna in the study site, and estimate the direct carbon mineralization by termites. Secondly, we investigate the effect of termites from various feeding habits on decomposition processes. Thirdly, we present preliminary results on radioisotopes (<sup>14</sup>C) together with C and N stable isotope ratios, in order to study feeding habits, trophic position, and turnover time of carbon in termites.</span>
Abstract: Subterranean-nesting termites do not colonize across the sea by rafting, and at the same time their winged-termites are also unlikely to fly such a long distance. The subterranean-nesting termite Odontotermes formosanus is common from Southeast Asia to the subtropics of East Asia, and is well-known as being discontinuously distributed in the Yaeyama Islands and the Shuri district of Okinawa Island; therefore, it may be hypothesized that O. formosanus was artificially introduced to Okinawa Island. Here we observed for the termites the vicinity of the Shuri district as well as islands of the Ryukyu Archipelago, and discussed the origin of the termites of Okinawa Island. Although we confirmed the presence in the Yaeyama Islands, we did not find the termites in the Miyako Islands, which situate between the Yaeyama Islands and Okinawa Island. In Okinawa Island, the termites exclusively occurred within a limited area that centers on the Shuri district (the old capital city area in the age of the Ryukyu Dynasty). In addition, by comparing their gene sequences deposited in the database, the populations in the Yaeyama Islands and Okinawa Island were estimated to have been separated relatively recently. We suggest that O. formosanus was brought into Shuri from the Yaeyama Islands in the age of the Ryukyu Dynasty in order to provide for the people the termite mushrooms that have been a valuable foodstuff for the local peoples.
Abstract: <span style="font-style:normal">The relationships between termites and gut microbes are frequently depicted as a typical example of symbiosis. Despite the generally perceived vertical transmission of symbiotic microbes by termites, it still remains unclear whether all the microbes are transmitted from parents to offspring. Here we investigated the occurrence of horizontal transmission of methanogenic microbes by the termite <i>Neotermes koshunensis</i>. Firstly, we examined for methanogens <i>N. koshunensis</i> colonies, which are supposed to sometimes lack methanogens, by epifluorescence microscopic observation and 16S rRNA gene PCR amplification. Methanogens were detected from some colonies by both the methods while they were not detected at all from the other colonies. Hereafter, the former is referred to as MC (methanogen colony) and the latter as MFC (methanogen free colony). Termite individuals of a MFC were found to become harboring methanogens in their guts after being kept together with a single individual of a MC for two weeks. The results indicate that the gut environments of the MFC individuals are not necessarily unsuitable for methanogen growth and strongly suggest the complete absence of methanogens in the guts of the MFC. Furthermore, this disproves the claim of the vertical-transmission of all the symbiotic microbes by <i>N. koshunensis</i>. As another experiment, termite individuals of a MFC were kept with those of methanogen- harboring <i>Coptotermes formosanus</i> colony or with filter papers that contain gut contents of a MC. In both the cases, methanogens appeared in guts of the termite individuals of a MFC. These combined, it is probable that methanogen-harboring colonies of any termite species as well as the environments surrounding the termites are potential sources of methanogens for MFCs. Accordingly, it is predicted that a longer elapsed time of <i>N. koshunensis</i> colonies will increase the chance of contact with methanogen sources under natural conditions; our field observation showed that mean population size was apparently, though not significantly, different between MCs and MFCs. The present study suggests that the transmission of symbiotic microbes by <i>N. koshunensis</i> involves not only vertical mode, but also both horizontal mode (including that mediated by environments) and vertical mode.</span>
Abstract: <span style="font-style:normal">A recent report (Yamada <i>et al</i>. 2005) has suggested that the carbon (C) source competition between termites and litter-layer microbes may be employed for understanding the C mineralization processes in tropical forests, but the situation in dry tropical ecosystems (e.g., savannas) and the possible intergroup competition in termites remain unclear. Here, we observed termites in a dry tropical ecosystem (dry deciduous forest (DDF)) and a high-altitude tropical forest (hill evergreen forest (HEF)) in Thailand and estimated the C fractions in the annual aboveground litterfall (AAL) mineralized by the termites. In the DDF, 5.1% of the AAL was mineralized by termites, with dominant contribution from the fungus-growing group. In such dry tropical ecosystems, fire rather than litter-layer microbes is likely to be the most important limiting factor for the C source that can be used and mineralized by termites. On the other hand, termites contributed to the C mineralization of 4.2% of the AAL in the HEF, while the soil-feeding group played a substantial role. Comparisons of the importance of each termite group in Asian and African tropical forests indicate that the coincidence of the smaller contribution of the fungus-growers and the larger contribution of the soil-feeders in the HEF, suggesting the presence of an asymmetric C source competition between the fungus-growers and soil-feeders through the C flow from the litter layer into the soil. Key words: fungus-growers, soil-feeders, termites, litter-layer microbes, fire, savannas, tropical forests, carbon source competitions.</span>
Abstract: <span style="font-style:normal">A recent report (Yamada <i>et al</i>. 2005) has suggested that the carbon (C) source competition between termites and litter-layer microbes may be employed for understanding the C mineralization processes in tropical forests, but the situation in dry tropical ecosystems (e.g., savannas) and the possible intergroup competition in termites remain unclear. Here, we observed termites in a dry tropical ecosystem (dry deciduous forest (DDF)) and a high-altitude tropical forest (hill evergreen forest (HEF)) in Thailand and estimated the C fractions in the annual aboveground litterfall (AAL) mineralized by the termites, using their respiration rates and biomasses of fungus combs as well as termites themselves. In the DDF, 5.1% of the AAL was mineralized by termites, with dominant contribution from the fungus-growing group. In such dry tropical ecosystems, fire rather than litter-layer microbes is likely to be the most important limiting factor for the C source that can be used and mineralized by termites. On the other hand, termites contributed to the C mineralization of 4.2% of the AAL in the HEF, while the soil-feeding group played a substantial role. Comparisons of the importance of each termite group in Asian and African tropical forests indicate that the coincidence of the smaller contribution of the fungus-growers and the larger contribution of the soil-feeders in the HEF, suggesting the presence of an asymmetric C source competition between the fungus-growers and soil-feeders through the C flow from the litter layer into the soil (see Figure).<br><br>
References: Yamada <i>et al</i>. (2005) Ecological Research, 20:453-460; Yamada & Inoue <i>et al</i>. (2007) Sociobiology, 50:135-154.
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Abstract: <span style="font-style:normal">Symbioses between bacteria and eukaryotes impact the physiology, ecology and evolution of all organisms. Proteobacteria and invertebrates are ubiquitous in marine-reducing environments and are particularly well-characterized in the unique ecosystems structured around deep-sea hydrothermal vents and cold seeps. Unlike all other major ecosystems on the earth, which are driven by photosynthesis, hydrothermal vent and seep ecosystems rely on chemosynthesis. Although free-living chemosynthetic prokaryotes serve as the base of the food chain for some vent and seep organisms, reliance on symbiotic chemosynthetic bacteria is the primary nutritional strategy for many vent and seep invertebrates. In recent years, molecular phylogenetics has enabled exploration of the world of symbiotic bacteria in vent and seep invertebrates. We here report our molecular phylogenetic studies using vent and seep invertebrates collected within the Hatoma and Kuroshima Knolls, off the Ryukyu Islands.<br><br>
Polychaetes of the family Polynoidae (scale-worms) are well-represented at deep-sea vents and seeps. Nevertheless, little is known about lineages of symbiotic bacteria of scale-worms or even about the presence. We performed PCR-based detection and phylogenetic analysis of the bacteria associated with a free-living scale-worm. The scale-worm, related to the genus <i>Branchipolynoe</i>, harbored the significant bacterial population dominated by the novel phylotype that is tightly clustered with thioautotrophic endosymbionts of vesicomyid bivalves within gamma-proteobacteria. Our results strongly suggest that some scale-worms have established symbiotic relationships with thioautotrophic symbionts of gamma-Proteobacteria.<br><br>
Mussels of the genus <i>Bathymodiolus</i> are ubiquitous over the world vent and seep sites and hosting either thioautotrophic or methanotrophic symbionts or both. Although the ratio of methane to hydrogen sulfide has been supposed to impact the type of the hosted symbionts, it is still obscure. Furthermore, one of the most intriguing aspects of these three different symbioses concerns their evolutionary origins. On the basis of our molecular phylogenetic and ancestral-state analyses, it is strongly suggested that the most recent common ancestor of the <i>Bathymodiolus</i> possessed both of the two types of symbionts and have often lost and reacquired either one symbiont resulting in the present distribution of the types of the hosted symbionts.</span>
Abstract: <span style="font-style:normal">The importance of termites in decomposition processes is widely recognized, and is frequently emphasized especially in savannas. In tropical forests, there have been only a few studies that quantitatively demonstrated the roles of termites as a decomposer. We quantified the importance of termites in terms of carbon mineralization and nitrogen fixation on the basis of biomass data in a dry evergreen forest, northeast Thailand. By using observed respiration rates from termite individuals and fungus-combs with their biomasses, they were estimated to mineralize 11.2% of carbon (C) in the annual aboveground litterfall (AAL). Of these, fungus-combs were responsible for a major part (7.2% of the AAL) of the C mineralization mediated by termites. We measured nitrogen (N) fixation rates of termites and asymbiotic (free-living) bacteria in litter, dead wood and soil, and estimated the total N inputs from fixation to decomposing plant material on the forest floor. Annual mounts of N fixed by termites and asymbiotic bacteria were calculated to be 0.28 and 3.95 kg ha<sup>-1</sup>, respectively, showing that termites are responsible for 6.6% of the total.</span>
Abstract: <span style="font-style:normal">Nitrogen cycles involve its input by biological nitrogen fixation and by precipitation as well as its loss by denitrification and by leaching, and nitrogen, meanwhile, is the element most likely to limit primary production in terrestrial ecosystems. Wood/litter-feeding termites, which widely distribute over temperate, subtropical, and tropical regions, generally fix atmospheric nitrogen in order to maintain C/N balance between their foods and body tissues. The nitrogen fixed by termites may significantly contribute to the biogeochemical cycles of nitrogen.<br><Br>
The nitrogen fixation rates of termite assemblages were investigated in a dry deciduous forest (DDF) and the neighboring dry evergreen forest (DEF), Thailand, with the aim of evaluating the quantitative role of termites in the nitrogen cycles. Considering the known effects of disturbance on nitrogen fixation in termites, we used acetylene reduction method under field conditions. The observations were carried out in the early and the late rainy seasons in 2002 as well as in the late dry season 2003. Our previous study showed that the two species, <i>Microcerotermes crassus</i> and <i>Globitermes sulphureus</i>, dominant wood/litter-feeding termites in both DDF and DEF. Thus these two species can sufficiently represent the termite assemblages.<br><br>
The mean nitrogen fixation rates were 147.3 and 50.8 nmol C<sub>2</sub>H<sub>4</sub> m<sup>-2</sup> h<sup>-1</sup> for <i>M. crassus</i> in DDF and DEF, respectively, and 69.2 and 27.7 nmol C<sub>2</sub>H<sub>4</sub> m<sup>-2</sup> h<sup>-1</sup> for <i>G. sulphureus</i> in DDF and DEF, respectively. Using the biomass data of termites, these two species were calculated to fix nitrogen at total rates of 260 and 350 nmol C<sub>2</sub>H<sub>4</sub> m<sup>-2</sup> h<sup>-1</sup> (= 0.021 and 0.028 g N m<sup>-2</sup> y<sup>-1</sup>) in DDF and DEF, respectively. Although the amounts of nitrogen fixed by termites seemed to be less than those fixed by either symbiotic or non-symbiotic nitrogen fixers in tropical forests, we emphasized the important contributions of termites to nitrogen input to the detritus food-webs.
Abstract: <span style="font-style:normal">The gut symbiotic microbes of termites, especially wood/litter-feeders, fix atmospheric nitrogen to compensate for the low nitrogen concentrations in their foods. Nitrogen fixation has been found in the following termite families: Termopsidae (Tmp), Kalotermitidae (Klt), Rhinotermitidae (Rhn), and Termitidae (Tmt). <br><br>
We investigated the compositions of nifH genes by culture-independent methods in eight wood/litter-species: <i>Zootermopsis nevadensis</i> (Tmp), <i>Schedorhinotermes medioobscurus</i> (Rhn), <i>Coptotermes gestroi</i> (Rhn), <i>Microcerotermes</i> sp. (Tmt), <i>M. crassus</i> (Tmt), <i>Globitermes sulphureus</i> (Tmt), <i>Nasutitermes dimorphus</i> (Tmt), and <i>N. bicolor</i> (Tmt). For the higher termites <i>Microcerotermes</i> spp., we analyzed not only the PCR products from DNA, but also RT (reverse transcription)-PCR products from mRNA of the gut community in order to know real contributions to the activity.<br><br>
The functional nifH sequences obtained from the eight species were assigned to any of the known three nifH groups: Anaerobe, Proteo-Cyano, and Anf-Methano. Phylogenetic analysis of the nifH sequences from the present and previous studies revealed that the Anaerobe group was further categorized to the four clusters: Anaerobe Ia, Ib, II, and III. The major groups and/or clusters of the sequences derived from Tmp, Klt, Rhn, and Tmt were Anf-Methano, Anf-Methano and Anaerobe III, Anaerobe III, and Anaerobe Ib and II, respectively. Based on the analyses of the RT-PCR products in the present and previous studies, it is quite possible that nitrogenases encoded by the major nifH groups and/or clusters of each family are also mainly transcribed in their guts. Meanwhile, the common nifH groups and/or clusters, though usually minor, were shared between two closely related termite families. These suggest gradual shifts of nifH genes along the evolution of termites.</span>
Abstract: <span style="font-style:normal">Termites have various symbionts drawn from <I>Archaea</I>, <I>Bacteria</I> and <I>Eucarya</I>. Symbiotic methanogenic archaea (methanogens), which function as a terminal electron sink of the gut fermentation, are widely distributed among various termites, and most of them are distinct from known methanogens. So far there is no study on the infection process of methanogens: either a vertical mode or not.<br><br>
We conducted phylogenetic analysis of symbiotic methanogens in the gut of various higher termites in Thailand. In a dry evergreen forest (DEF) in Sakaerat and an orchard near Bangkok, we collected a total of 11 termite species, comprising 9 genera, namely <I>Speculitermes</I>, <I>Macrotermes</I>, <I>Nasutitermes</I>, <I>Amitermes</I>, <I>Dicuspiditermes</I>, <I>Globitermes</I>, <I>Microcerotermes</I>, <I>Pericapritermes</I>, and <I>Termes</I>. We collected <I>Microcerotermes</I> and <I>Termes</I> from both sites to evaluate the effects of the geographical separation on the methanogen community. DNA was extracted from the whole guts of the workers and 16S rRNA genes were amplified by PCR using <I>Archaea</I>-specific primers. Phylogenetic analysis of 16S rRNA genes revealed all the sequences were related to those reported previously from termite guts in the orders Methanobacteriales, Methanomicrobiales and Methanosarcinales. There were no sequence differences between two colonies of the same species collected in DEF. The phylogenic tree in the case of the order Methanosarcinales displayed concordance with that of their host for the most part. On the other hand, the phylogenic tree in the case of the order Methanobacteriales showed specificity of the symbionts with respect to their host and/or locality but not concordance with their host phylogeny.<br><br>
We also determined the methane emission rate of the termites and conducted T-RFLP analysis of 16S rRNA genes of the symbiotic methanogens to know relationships among the methane emission rate, feeding habitat of termites, and the methanogen composition. </span><br><br>
The Golden Jubilee XIV International Congress of IUSSI Proceedings p. 53
Abstract: <span style="font-style:normal">The rate of methane emission and the activity of nitrogen fixation of termites were measured. We collected four species of termites in a dry evergreen forest, namely two species of wood-feeding termites, <i>Microcerotermes crassus</i> and <i>Globitermes sulphureus</i>, one species of wood/soil interface feeding termite, <i>Termes comis</i>, and one species of soil-feeding termite, <i>Dicuspiditermes makhamensis</i>, to know inter-species and inter-feeding group variations. We also collected two species of termites, <i>M. crassus</i> and <i>T. comis</i>, in a plantation to compare environmental effects of two different ecosystems.<br><br> Activity of nitrogen fixation of the termites measured by acetylene reduction assay decreased markedly to almost undetectable level after twenty four hours from the collection in the field. The maximum activity was shown up to six hours after the collection. To minimize disturbances, the incubation was carried out in the field and that within two hours after the collection. The activity of nitrogen fixation was detected only for the wood-feeding termites and in DEF those of <i>M. crassus</i> and <i>G. sulphureus</i> were 59.3±14.2 and 21.6±7.3 C<sub>2</sub>H<sub>4</sub> nmol/h/g, respectively, and in the plantation that of <i>M. crassus</i> was 406.2±241.1 C<sub>2</sub>H<sub>4</sub> nmol/h/g.<br><br> Compared with the activity of nitrogen fixation, rate of methane emission of termites was so stable that the measurements were conducted in our laboratory within thirty six hours after the collection. The methane emission was detected for all species and in DEF the rates of <i>M. crassus</i> , <i>G. sulphureus</i> , <i>T. comis</i> and <i>D. makhamensis</i> were 579.6±75.6, 204.2±44.2, 126.6±18.8 and 267.4±24.1 nmol/h/g, respectively, and in the plantation those of <i>M. crassus</i> and <i>T. comis</i> were 188.3±6.7 and 515.1±26.3 nmol/h/g, respectively.</span>
Abstract: <span style="font-style:normal">If you go to the forest, it is very easy to find termites. You will find the âwhiteâ insects from everywhere within the forest; in many countries, people call termites âwhite antsâ, but taxonomically they are far from ants. Recent studies indicate that the most related insect of termites is cockroaches. Actually, some cockroach species live in dead wood with their offspring and eat the wood like as relatively primitive termite species. So, maybe you can call termites âwhite cockroachesâ.<br><br>
In the dry evergreen forest at Sakaerat, within only one square meter there are approximately 8,000 termites equivalent to 17 g in weight, while in the case of humans in Thailand the average biomass is only 8 g per square meter. It is well-known that termites are one of the most abundant animals on the earth. Species diversity of termites is also high in Sakaerat. There are probably more than 40 species, which eat a variety of dead plants such as fallen leaves, branches, trunks and very small plant particles in the soil; they play an essential role as decomposers in nutrient cycling. If termites were absent from the forest, nutrient could not be returned into the soil and to plants. Therefore, we should understand the ecology of termites in order to protect our precious forests.<br><br>
Here we will provide some photos and the short descriptions about popular termite species in Sakaerat.</span>
Abstract: <span style="font-style:normal">This biosphere reserve is situated on the edge of Thailandâs Khorat Plateau about 300 km north-east of Bangkok. It was created around the Sakaerat Environmental Research Station (SERS), which was established as a site for research on dry tropical forest.</span>