Food web structure in a Salix subfragilis dominated wetland in Hangang estuary using stable isotopes and fatty acid biomarkers
Food web structure in a Salix subfragilis dominated wetland in Hangang estuary using stable...
Han, Donguk; Yang, Dongwoo; Lee, Eun
Joo; Park, Sangkyu
2012-04-01 00:00:00
Animal Cells and Systems Vol. 16, No. 2, April 2012, 162171 Food web structure in a Salix subfragilis dominated wetland in Hangang estuary using stable isotopes and fatty acid biomarkers a b a b Donguk Han , Dongwoo Yang , Eun Joo Lee and Sangkyu Park * a b School of Biological Sciences, Seoul National University, Seoul 151-742, Republic of Korea; Department of Biological Science, Ajou University, Suwon 443-749, Republic of Korea (Received 5 April 2011; accepted 26 August 2011) We investigated food webs of a Salix subfragilis-dominated wetland in the Janghang wetland in the Hangang estuary, which is very close to the Demilitarized Zone, along the west coast of Korea. Our study focused on understanding sesarmine crab (Sesarma dehaani)-related food webs in a S. subfragilis forest. For our study, we used carbon and nitrogen stable isotopes and fatty acid biomarkers. We collected samples of plants, animals, and detrital sediment from four quadrats (55m ) set in the S. subfragilis community. Samples were collected from September 2006 to June 2009, except during the winter hibernation period of S. dehaani. In the wet season, the sediment showed 13 15 relatively high d C and low d N signatures compared with relatively low d13C and high d15N signatures in the dry season. Mature S. dehaani appeared to feed on fresh leaves and other carbon sources, such as immature individuals or fish, in addition to detrital sediment, which appeared to be the main carbon source for immature crabs. Principal component analysis of fatty acid biomarkers of S. dehaani showed a clear difference between immature individuals (1030 mm) and mature ones (larger than 30 mm), indicating that the main food source for immature crabs was detrital sediment, whereas mature crabs foraged plants in addition to consuming detrital sediment. On the basis of our results from stable isotope and fatty acid analyses, mature S. dehaani appeared to feed on detrital sediment and fresh leaves of S. subfragilis in summer in addition to engaging in cannibalism of immature individuals. Keywords: fatty acid biomarkers; food webs; Salix subfragilis: Sesarma dehaani; stable isotopes Introduction The traditional approach to food web studies has been gut content analysis (Cre ´ach et al. 1997). Estuaries generally have a relatively low species diver- However, despite considerable time and effort, it has sity and high productivity, and are characterized by low been difficult to quantify trophic relations through gut salinity, shallow water depths, high turbidity, and content analysis. In addition, the traditional trophic excessive nutrients (Elliot & McLusky 2002). Food level concept has limitations with regard to locating webs in estuaries are complex, incorporating both omnivorous species such as S. dehaani in food webs terrestrial and aquatic environments, with organisms (Vander Zanden and Rasmussen 1996). Recently, stable engaging in diverse foraging strategies (Haines and isotopes and fatty acid biomarkers have become Montague 1979). In estuarine ecosystems, the major popular tools for studying food web structure (Jeong carbon source for individual food webs is detrital and Park 2010). Stable isotope monitoring can provide organic matter input from rivers (Mann 1972; Odum an objective and quantitative food web structure when et al. 1973). ratios of stable isotopes such as carbon and nitrogen The Janghang wetland is a tidal willow forest are measured from tissues of biological components in wetland dominated by Salix subfragilis. It is located food webs (Vander Zanden et al. 1999). The nitrogen in the upper brackish region of the Hangang River. The isotope signature, in particular, can be used as an index primary productivity of S. subfragilis is estimated to be for quantitative trophic position from the observation 2 1 as high as 4777 g dry weight (DW) m yr , which 15 that the nitrogen isotope N tends to be enriched appears to be one of highest primary productivities between prey and predator by 3.490.3 (Vander measured in South Korea (Han et al. 2010). The Zanden and Rasmussen 1996; Vander Zanden et al. sesarmine crab Sesarma dehaani is an important food 1997; Guest and Connolly 2004; Thimdee et al. 2004). web component in S. subfragilis-dominated estuarine In addition, fatty acid biomarkers can provide wetlands (Han et al. 2010). It has been suggested that additional information about trophic relations. Recent the tunnels made by S. dehaani benefit S. subfragilis by studies have used specific fatty acid biomarkers to aeration of the rhizosphere (Han et al. 2010). To fully understand sources of organic matter or food web elucidate the interactions between S. subfragilis and structure (Meziane et al. 1997; Meziane et al. 2002; S. dehaani, it is necessary to understand the trophic Ruess et al. 2005). A recent report showed that the fatty relations of the two species. acid composition of a sesarmine crab, S. bidens,is *Corresponding author. Email: daphnia@ajou.ac.kr ISSN 1976-8354 print/ISSN 2151-2485 online # 2012 Korean Society for Integrative Biology http://dx.doi.org/10.1080/19768354.2011.620623 http://www.tandfonline.com ECOLOGY & POPULATION BIOLOGY Animal Cells and Systems 163 similar to that of mangrove plants (Shin et al. 2004). Sampling There are new trends that use both stable isotope We set four quadrats (55m )in a S. subfragilis monitoring and fatty acid biomarkers to study trophic community in the Janghang wetland of Hangang where relations or energy flows in food webs (Kiyashko et al. habitats of S. dehaani were in good conditions. Quadrats 2004; Ruess et al. 2005; Pond et al. 2006). Since the two were approximately 10 m apart. Further details on approaches provide limited clues about trophic rela- sampling sites can be found elsewhere (Han et al. tions, using both approaches would provide us with 2010). Samples of plants, animals (except for fish and more information to elucidate complex food webs. benthos), and detrital sediment were collected monthly In this study, we investigated trophic relations from these quadrats between September 2006 and centered on S. dehaani in the S. subfragilis community November 2007, except for during the winter hiberna- in the Janghang wetland in order to elucidate the tion period. Crabs collected from each quadrat were classified into four size groups: 1020 mm (Age1), interactions between S. subfragilis and S. dehaani and 2030 mm (Age2), 3040 mm (Age3), and larger than their roles in an estuarine willow forest-dominated 40 mm (Age4). From each size class, five crabs were wetland. We used carbon and nitrogen stable isotopes randomly selected for stable isotope and fatty acid and fatty acid biomarkers for this purpose. analyses. Fish and benthic samples were collected using gill-nets between January 2008 and June 2009 from the water and water channel in front of the willow forest in Materials and methods Hangang. Study area The Hangang estuary is a natural estuary facing the Yellow Sea. Although there are diverse brackish wet- Stable isotope monitoring lands, they are not well studied due to limited access to Carbon and nitrogen isotope signatures were measured them in the Demilitarized Zone (DMZ) area. Among for all organisms collected in the study sites, including these wetlands, 60.668 km between Goyang City, S. subfragilis, S. dehaani, and detrital sediment. For Geonggi-do and Ganghwa County, Incheon Metropo- periphytic algae, we collected samples by scraping them litan City is designated as a wetland protected area of from detrital sediment, followed by filtering using glass national importance. The Janghang wetland is a fiber paper (GF/C, 25 mm; Whatman, Maidstone, UK) riparian wetland with an upper part of brackish water pre-combusted at 4008C. Samples from S. dehaani were (N 378 38? 17ƒ, E 1268 45? 47ƒ) (Figure 1). This wetland collected from tissue parts inside the carapace, followed is a forested wetland dominated by S. subfragilis and by freezing and drying. After drying the filter papers tidal mudflats. Its total area is 7.494 km , and a willow and samples from collected plants and animals at 608C forest covers 0.71 km , which is 19.6% of the vegetated for more than 1 day, we ground them using pestles and area. mortars. Ground samples were wrapped in tin discs Figure 1. Map of the Janghang wetland in Hangang estuary, South Korea. 164 D. Han et al. (Perkin Elmer, Waltham, USA) into compact spherical Detector. Fatty acids were quantified by comparing the shapes with a maximum diameter of 6 mm and stored area ratios of samples to the internal standard. Re- in well plates until analyzed. Analysis was conducted sponse factors for the single fatty acid standards were by the Center for Stable Isotope Biogeochemistry at obtained by comparing quantitative fatty acid standards UC Berkeley, using a Delta Plus XL isotope ratio mass with the internal standard. The differences between spectrometer, Thermo Fisher Scientific Inc., Waltham, estimated fatty acid concentrations from the internal 13 15 13 USA). The d C and d N values were expressed as C standard and quantitative standards were within 5%. to C ratio (R) differences in parts per thousand () between samples and standards [Pee Dee Belemnite Principal component analysis and other statistical marine limestone for C and atmospheric nitrogen for analysis N] as follows: Percentage values of each fatty acid to the total fatty "# acid amount were compiled to produce a data matrix R R sample standard 13 15 3 d Cor d N%ðÞ o¼ 1a0 (18 observations 35 fatty acid peaks). All fatty acids standard less than 1% of the total fatty acid amount were 12 14 13 15 R ¼ C= Cor N= N removed from the dataset before analysis without re- calculating the remaining fatty acid percentage value The total carbon and nitrogen contents were analyzed (Hessen and Leu 2006). Centered fatty acid peak at the same time. intensity (area) data were standardized to relative abundance to the peaks with the highest intensities prior to PCA. We used log transformation [log (x1)] Fatty acid analysis to ensure the homogeneity of variance (Poerschmann Since most animals, including crabs, cannot synthesize et al. 2004). We assigned 0 if there was no matching polyunsaturated fatty acids, they acquire these fatty peak. PCA was conducted using covariance data acids from their diet, resulting in similar fatty acid matrices to reduce their dimensionality. All statistical profiles for these animals (Suprayudi et al. 2004; analyses, including PCA, were performed with S-Plus 6 Chamberlain et al. 2005). Therefore, we can use multi- for Windows (Insightful Corp., Seattle, USA). variate analysis such as principal component analysis (PCA) to infer trophic relationships based on simila- rities in their fatty acid profiles (Dalsgaard et al. 2003). Results Samples were frozen using dry ice while transporta- Stable isotope signature of detrital sediment, tion to the laboratory and stored in a deep freezer at S. subfragilis, and S. dehaani 808C until extraction. Frozen samples were dried Carbon and nitrogen isotope signatures showed varia- using a freeze dryer (Model FD2.5; Heto, Waltham, bility with season and crab age (Figure 2). The d C USA) before extraction. These freeze-dried samples values of S. dehaani belonging to Age1 and Age2 were were weighed using an electric balance (Model A120S; similar to those of detrital sediment, while the d C Sartorius, Goettingen, Germany) to calculate fatty acid values of crabs in the Age3 and Age4 group were much content per dry weight (g FA g ). Dried and weighed higher than those of the Age1 and Age2 groups, samples were wrapped in glass fiber filter paper pre- indicating carbon sources other than detrital sediment combusted at 4008C for extraction. Fatty acids from (Figure 2A). The d N values of Age3 and Age4 were filter papers were measured to determine the basal significantly higher than those of Age1 and Age2 after amount of fatty acids. We used a mix of 37 fatty acid July, which, in turn, were higher than those of detrital methyl esters (Supelco Cat. No. 47885-u) and marine sediment (Figure 2B). Detrital sediment showed a source fatty acid methyl esters (Sigma-Aldrich, 13 15 relatively low d C and relatively high d N value in St. Louis, USA, Cat. No. 47033) to identify fatty acids April 2007, which was the dry season (average tem- on the basis of retention time. Further, we used perature: 12.18C), than in the wet and high temperature heneicosanoic acid (21:0, 1 mg mL ) as an internal season (average temperature: 25.48C) in August 2007. standard; it was added to the freeze-dried samples immediately prior to the extraction process. Extraction and methylation were performed according to the Stable isotope signatures of S. dehaani Kattner and Fricke (1986) method. Extracted fatty in the wet and dry periods acid samples were analyzed using a gas chromatograph (Agilent, Santa Clara, USA, 6890N) with a Program- S. dehaani showed very distinctive stable isotope signa- mable-Temperature-Vaporizer and a Flame-Ionization- tures between the dry period (April) and wet period Animal Cells and Systems 165 Figure 2. (A) Mean (barSD) d C of detrital sediment, Salix subfragilis, and Sesarma dehaani in the Janghang wetland in 2007. (B) Mean (barSD) d N of detrital sediment, S. subfragilis, and S. dehaani in the Janghang wetland in 2007. a, b, c, and d indicate the results of Tukey multiple comparison. (August) (Figure 3). In April, the d C value of Age4 was Food web structure in the Janghang wetland based on a stable isotope signature much higher than that of other age classes, which were close to the d C value of detrital sediment. In the wet To understand the whole food web structure in an period (August), the d C values of Age3 and Age4 were S. subfragilis-dominated wetland, we included carbon clearly higher than those of Age1 and Age2, which were and nitrogen isotope signatures of other organisms close to the d C values of detrital sediment, indicating such as fish and lugworm collected from near the study that Age3 and Age4 had other carbon sources. The d N site. The d C value of fish such as Gobiidae and values of Age3 and Age4 were higher than those of Age1 flathead mullet (Mugil cephalus) were much higher and Age2. In the wet period (August), in particular, the than those of Age3 and Age4, suggesting that these fish d N values of Age3 and Age4 were approximately 1.8% were possible carbon sources for Age3 and Age4. higher than those of Age1 and Age2, supporting the Further, the d C value of skin carp (Hemibarbus observation that Age3/Age4 cannibalized Age1/Age2. labeo) was close to that of S. dehaani (Figure 4). 166 D. Han et al. 13 15 Figure 3. A d C and d N diagram of the Janghang wetland in the (A) dry period (April 2007) and (B) wet and humid period (August 2007). 14, Crab; 1, Age1; 2, Age2; 3, Age3; 4, Age4; 5, Spider; 68, Plant; 6, Monocotyledon; 7, Dicotyledon; 8, Salix;9, detrital sediment. Fatty acid biomarkers for detrital sediment and Comparison of fatty acid profiles among age classes of S. subfragilis leaves S. dehaani To select useful biomarkers for carbon sources, we PCA of the fatty acid profiles of each age class of analyzed the fatty acid profiles of detrital sediment and S. dehaani showed distinctive grouping between Age1/ S. subfragilis (Figure 5). The levels of fatty acids 18:2v6 Age2 and Age3/Age4 along the first principal compo- and 18:3v3 appeared to be higher in the fresh leaves of nent (PC1) and second component (PC2) (Figure 6A). S. subfragilis than in detrital sediment. In contrast, PC1 explained 55.2% of the total variance, while PC2 16:1v7 and 22:2v6 levels appeared to be higher in explained 16.9%, covering 72.1% of the total variance detrital sediment than in S. subfragilis leaves. There- together. With regard to PC1, the scores of both Age1/ fore, we selected 18:2v6 and 18:3v3 as markers for Age2 and Age3/Age4 were located between the scores living plant material and 16:1v7 and 22:2v6 as markers for detrital sediment and S. subfragilis leaves. The PC1 for detrital sediment. Individuals of S. dehaani in Age1 scores of Age1/Age2 were relatively close to that of and Age2 showed relatively high 16:1v7 content while detrital sediment, while the PC1 scores of Age3/Age4 18:3v3 content was relatively high in Age2, Age3, and were relatively close to that of S. subfragilis leaves. As Age4 S. dehaani grows from Age1/Age2 to Age3/Age4, Animal Cells and Systems 167 13 15 Figure 4. A d C and d N diagram of the Janghang wetland, using annual average values and candidate food sources for S. dehaani.14, Crab; 1, Age1; 2, Age2; 3, Age3; 4, Age4; 510, Plant; 5, Monocotyledon; 6, Dicotyledon; 7, Sium suave; 8, Reed; 9, Salix; 10, Salix (litter); 1113, Arthropod; 11, Insect; 12, Spider; 13, Lugworm; 14, Fungus, Mushroom; 1517, Fish; 15, Skin carp; 16, Goby; 17, Flathead mullet; 18, detrital sediment. 16:1v7, the sediment biomarker, appears to decrease, addition, the ranges of PCA scores on the fatty acid while 18:2v6 and 18:3v3, the S. subfragilis leaf profiles were wider for Age3/Age4 than Age1/Age2, biomarker, increases (Figure 6B). indicating that mature individuals feed on more diverse carbon sources than immature ones. Our results were well supported by field observa- Discussion tions of the feeding behavior of S. dehaani. Mature individuals of S. dehaani have been observed to feed on Studies on interactions between trees and crabs in diverse fresh and fallen leaves of S. subfragilis, litter of forested estuarine wetlands have focused on mangrove S. subfragilis in detrital sediment, leaves of Phragmites forests in tropical and subtropical regions. These communis, molted carapaces of S. dehaani, and dead studies have found that crabs feed on the leaves or fish and bivalves. The cannibalistic behavior of mature litter of mangroves, detritus, or sediment (Lee 1997; S. dehaani was observed by the authors on several Skov and Harnoll 2002). In these regions, mangrove occasions. crabs return organic matter through their excreta, Our results indicate that S. dehaani experience accounting for as much as 24% of mangrove leaf ontogenic diet changes from sediment feeding to production (Lee 1997), and they feed on 81.3% of omnivorous feeding. Although ontogenic diet shifts mangrove annual production (Inga et al. 2006). How- are well known for many aquatic species such as fish, ever, there are few studies on forested estuarine wet- there are few studies on ontogenic diet shift in crabs lands in temperate regions. Our previous study found (Werner and Gilliam 1984). A blue crab, Callinectes that the secondary productivity of S. dehaani was as sapidus, and a portunid crab, Liocarcinus depurator, high as 100.2 g fresh weight (FW) C m , indicating have been reported to show different feeding behaviors that the crabs feed on up to 60% of the organic matter depending on size (Laughlin 1982; Freire et al. 1996). produced by S. subfragilis (Han et al. 2010). Results However, there are no reports available on ontogenic from both stable isotope and fatty acid analyses in the diet shifts of crabs in woody wetlands such as present study indicate that mature S. dehaani indivi- mangrove ecosystems (Cannicci et al. 2008; Kristensen duals (Age3 and Age4) feed on both detrital sediment and S. subfragilis leaves in the summer in addition to et al. 2010). Cannibalism among crustaceans is well documen- engaging in the cannibalism of younger individuals and ted (Jormalainen and Shuster 1997). Jormalainen and decaying fish. In contrast, immature crabs (Age1 and Age2) appear to feed on detrital sediment only. In Shuster (1997) summarized four conditions conducive 168 D. Han et al. Figure 5. (A) Comparison of important fatty acid contents in detrital sediment and S. subfragilis (n3). (B) Fatty acid content in each age class of S. dehaani in the Janghang wetland (n17). Bars indicate average fatty acid content with error bars (9standard deviation). We showed results of t-test with a star (A) and Tukey multiple comparison with a, b, c, and d. to cannibalism: small habitat, high local population individuals, except for Age4, exhibited increases in density, food shortage, and structural simplicity of C:N ratios after August 2007, indicating that the habitats. In addition to these, food quality in terms animals had high C:N diets (Figure 7B). Mature S. of carbon to nitrogen (C:N) ratio has been suggested dehaani individuals, particularly those belonging to as an important factor for cannibalism (Wolcott and Age4, appeared to have managed to keep their C:N Wolcott 1984). Our results indicate that S. dehaani ratio low, except in September, possibly by cannibal- individuals might have experienced nitrogen defi- ism of younger individuals (Linton and Greenaway ciency during summer and fall since the C:N ratio of 2007). S. subfragilis leaves dramatically increased to more Intensive studies on mangrove ecosystems suggest that sesarmid crabs are ecosystem engineers, than 20 after June 2007 (Figure 7A). S. dehaani Animal Cells and Systems 169 Figure 6. (A) PCA scores based on fatty acid profiles of sediment, S. subfragilis and S. dehaani of each age class in the Janghang wetland in September 2006, and (B) the most important loading values on the first and second principal components. responsible for burrowing construction and mainte- In conclusion, our results show the differences in nance, redistribution of organic matter and burial of the feeding patterns of immature and mature S. dehaani litter, and exchange between sediment and water/air individuals through carbon and nitrogen stable isotope (Kristensen 2008). Further, herbivorous crabs in man- signatures and fatty acid biomarkers. Immature indivi- grove forests have been reported to affect vegetation duals appear to feed mainly on detrital sediment, while structure and ecosystem function in various ways: mature individuals feed on more diverse carbon grazing, maintaining high leaf litter turnover rates, sources such as fresh and fallen leaves of S. subfragilis, recycling mangrove organic production, and propagule fish, and younger individuals of their own species in predation (Cannicci et al. 2008). We expect that addition to detrital sediment. Our results provide S. dehaani plays similar roles in S. subfragilis wetlands. useful information regarding energy flows and nutrient Future studies are required to understand the ecological cycling in S. subfragilis forest wetlands and estuarine roles of S. dehaani in S. subfragilis wetland ecosystems. ecosystems. 170 D. Han et al. Figure 7. (A) Seasonal changes in C:N ratio in S. dehaani, detrital sediment, and S. subfragilis. 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Food web structure in a Salix subfragilis dominated wetland in Hangang estuary using stable isotopes and fatty acid biomarkers
Food web structure in a Salix subfragilis dominated wetland in Hangang estuary using stable isotopes and fatty acid biomarkers
Abstract
Abstract We investigated food webs of a Salix subfragilis-dominated wetland in the Janghang wetland in the Hangang estuary, which is very close to the Demilitarized Zone, along the west coast of Korea. Our study focused on understanding sesarmine crab (Sesarma dehaani)-related food webs in a S. subfragilis forest. For our study, we used carbon and nitrogen stable isotopes and fatty acid biomarkers. We collected samples of plants, animals, and detrital sediment from four quadrats (5×5...
Animal Cells and Systems Vol. 16, No. 2, April 2012, 162171 Food web structure in a Salix subfragilis dominated wetland in Hangang estuary using stable isotopes and fatty acid biomarkers a b a b Donguk Han , Dongwoo Yang , Eun Joo Lee and Sangkyu Park * a b School of Biological Sciences, Seoul National University, Seoul 151-742, Republic of Korea; Department of Biological Science, Ajou University, Suwon 443-749, Republic of Korea (Received 5 April 2011; accepted 26 August 2011) We investigated food webs of a Salix subfragilis-dominated wetland in the Janghang wetland in the Hangang estuary, which is very close to the Demilitarized Zone, along the west coast of Korea. Our study focused on understanding sesarmine crab (Sesarma dehaani)-related food webs in a S. subfragilis forest. For our study, we used carbon and nitrogen stable isotopes and fatty acid biomarkers. We collected samples of plants, animals, and detrital sediment from four quadrats (55m ) set in the S. subfragilis community. Samples were collected from September 2006 to June 2009, except during the winter hibernation period of S. dehaani. In the wet season, the sediment showed 13 15 relatively high d C and low d N signatures compared with relatively low d13C and high d15N signatures in the dry season. Mature S. dehaani appeared to feed on fresh leaves and other carbon sources, such as immature individuals or fish, in addition to detrital sediment, which appeared to be the main carbon source for immature crabs. Principal component analysis of fatty acid biomarkers of S. dehaani showed a clear difference between immature individuals (1030 mm) and mature ones (larger than 30 mm), indicating that the main food source for immature crabs was detrital sediment, whereas mature crabs foraged plants in addition to consuming detrital sediment. On the basis of our results from stable isotope and fatty acid analyses, mature S. dehaani appeared to feed on detrital sediment and fresh leaves of S. subfragilis in summer in addition to engaging in cannibalism of immature individuals. Keywords: fatty acid biomarkers; food webs; Salix subfragilis: Sesarma dehaani; stable isotopes Introduction The traditional approach to food web studies has been gut content analysis (Cre ´ach et al. 1997). Estuaries generally have a relatively low species diver- However, despite considerable time and effort, it has sity and high productivity, and are characterized by low been difficult to quantify trophic relations through gut salinity, shallow water depths, high turbidity, and content analysis. In addition, the traditional trophic excessive nutrients (Elliot & McLusky 2002). Food level concept has limitations with regard to locating webs in estuaries are complex, incorporating both omnivorous species such as S. dehaani in food webs terrestrial and aquatic environments, with organisms (Vander Zanden and Rasmussen 1996). Recently, stable engaging in diverse foraging strategies (Haines and isotopes and fatty acid biomarkers have become Montague 1979). In estuarine ecosystems, the major popular tools for studying food web structure (Jeong carbon source for individual food webs is detrital and Park 2010). Stable isotope monitoring can provide organic matter input from rivers (Mann 1972; Odum an objective and quantitative food web structure when et al. 1973). ratios of stable isotopes such as carbon and nitrogen The Janghang wetland is a tidal willow forest are measured from tissues of biological components in wetland dominated by Salix subfragilis. It is located food webs (Vander Zanden et al. 1999). The nitrogen in the upper brackish region of the Hangang River. The isotope signature, in particular, can be used as an index primary productivity of S. subfragilis is estimated to be for quantitative trophic position from the observation 2 1 as high as 4777 g dry weight (DW) m yr , which 15 that the nitrogen isotope N tends to be enriched appears to be one of highest primary productivities between prey and predator by 3.490.3 (Vander measured in South Korea (Han et al. 2010). The Zanden and Rasmussen 1996; Vander Zanden et al. sesarmine crab Sesarma dehaani is an important food 1997; Guest and Connolly 2004; Thimdee et al. 2004). web component in S. subfragilis-dominated estuarine In addition, fatty acid biomarkers can provide wetlands (Han et al. 2010). It has been suggested that additional information about trophic relations. Recent the tunnels made by S. dehaani benefit S. subfragilis by studies have used specific fatty acid biomarkers to aeration of the rhizosphere (Han et al. 2010). To fully understand sources of organic matter or food web elucidate the interactions between S. subfragilis and structure (Meziane et al. 1997; Meziane et al. 2002; S. dehaani, it is necessary to understand the trophic Ruess et al. 2005). A recent report showed that the fatty relations of the two species. acid composition of a sesarmine crab, S. bidens,is *Corresponding author. Email: daphnia@ajou.ac.kr ISSN 1976-8354 print/ISSN 2151-2485 online # 2012 Korean Society for Integrative Biology http://dx.doi.org/10.1080/19768354.2011.620623 http://www.tandfonline.com ECOLOGY & POPULATION BIOLOGY Animal Cells and Systems 163 similar to that of mangrove plants (Shin et al. 2004). Sampling There are new trends that use both stable isotope We set four quadrats (55m )in a S. subfragilis monitoring and fatty acid biomarkers to study trophic community in the Janghang wetland of Hangang where relations or energy flows in food webs (Kiyashko et al. habitats of S. dehaani were in good conditions. Quadrats 2004; Ruess et al. 2005; Pond et al. 2006). Since the two were approximately 10 m apart. Further details on approaches provide limited clues about trophic rela- sampling sites can be found elsewhere (Han et al. tions, using both approaches would provide us with 2010). Samples of plants, animals (except for fish and more information to elucidate complex food webs. benthos), and detrital sediment were collected monthly In this study, we investigated trophic relations from these quadrats between September 2006 and centered on S. dehaani in the S. subfragilis community November 2007, except for during the winter hiberna- in the Janghang wetland in order to elucidate the tion period. Crabs collected from each quadrat were classified into four size groups: 1020 mm (Age1), interactions between S. subfragilis and S. dehaani and 2030 mm (Age2), 3040 mm (Age3), and larger than their roles in an estuarine willow forest-dominated 40 mm (Age4). From each size class, five crabs were wetland. We used carbon and nitrogen stable isotopes randomly selected for stable isotope and fatty acid and fatty acid biomarkers for this purpose. analyses. Fish and benthic samples were collected using gill-nets between January 2008 and June 2009 from the water and water channel in front of the willow forest in Materials and methods Hangang. Study area The Hangang estuary is a natural estuary facing the Yellow Sea. Although there are diverse brackish wet- Stable isotope monitoring lands, they are not well studied due to limited access to Carbon and nitrogen isotope signatures were measured them in the Demilitarized Zone (DMZ) area. Among for all organisms collected in the study sites, including these wetlands, 60.668 km between Goyang City, S. subfragilis, S. dehaani, and detrital sediment. For Geonggi-do and Ganghwa County, Incheon Metropo- periphytic algae, we collected samples by scraping them litan City is designated as a wetland protected area of from detrital sediment, followed by filtering using glass national importance. The Janghang wetland is a fiber paper (GF/C, 25 mm; Whatman, Maidstone, UK) riparian wetland with an upper part of brackish water pre-combusted at 4008C. Samples from S. dehaani were (N 378 38? 17ƒ, E 1268 45? 47ƒ) (Figure 1). This wetland collected from tissue parts inside the carapace, followed is a forested wetland dominated by S. subfragilis and by freezing and drying. After drying the filter papers tidal mudflats. Its total area is 7.494 km , and a willow and samples from collected plants and animals at 608C forest covers 0.71 km , which is 19.6% of the vegetated for more than 1 day, we ground them using pestles and area. mortars. Ground samples were wrapped in tin discs Figure 1. Map of the Janghang wetland in Hangang estuary, South Korea. 164 D. Han et al. (Perkin Elmer, Waltham, USA) into compact spherical Detector. Fatty acids were quantified by comparing the shapes with a maximum diameter of 6 mm and stored area ratios of samples to the internal standard. Re- in well plates until analyzed. Analysis was conducted sponse factors for the single fatty acid standards were by the Center for Stable Isotope Biogeochemistry at obtained by comparing quantitative fatty acid standards UC Berkeley, using a Delta Plus XL isotope ratio mass with the internal standard. The differences between spectrometer, Thermo Fisher Scientific Inc., Waltham, estimated fatty acid concentrations from the internal 13 15 13 USA). The d C and d N values were expressed as C standard and quantitative standards were within 5%. to C ratio (R) differences in parts per thousand () between samples and standards [Pee Dee Belemnite Principal component analysis and other statistical marine limestone for C and atmospheric nitrogen for analysis N] as follows: Percentage values of each fatty acid to the total fatty "# acid amount were compiled to produce a data matrix R R sample standard 13 15 3 d Cor d N%ðÞ o¼ 1a0 (18 observations 35 fatty acid peaks). All fatty acids standard less than 1% of the total fatty acid amount were 12 14 13 15 R ¼ C= Cor N= N removed from the dataset before analysis without re- calculating the remaining fatty acid percentage value The total carbon and nitrogen contents were analyzed (Hessen and Leu 2006). Centered fatty acid peak at the same time. intensity (area) data were standardized to relative abundance to the peaks with the highest intensities prior to PCA. We used log transformation [log (x1)] Fatty acid analysis to ensure the homogeneity of variance (Poerschmann Since most animals, including crabs, cannot synthesize et al. 2004). We assigned 0 if there was no matching polyunsaturated fatty acids, they acquire these fatty peak. PCA was conducted using covariance data acids from their diet, resulting in similar fatty acid matrices to reduce their dimensionality. All statistical profiles for these animals (Suprayudi et al. 2004; analyses, including PCA, were performed with S-Plus 6 Chamberlain et al. 2005). Therefore, we can use multi- for Windows (Insightful Corp., Seattle, USA). variate analysis such as principal component analysis (PCA) to infer trophic relationships based on simila- rities in their fatty acid profiles (Dalsgaard et al. 2003). Results Samples were frozen using dry ice while transporta- Stable isotope signature of detrital sediment, tion to the laboratory and stored in a deep freezer at S. subfragilis, and S. dehaani 808C until extraction. Frozen samples were dried Carbon and nitrogen isotope signatures showed varia- using a freeze dryer (Model FD2.5; Heto, Waltham, bility with season and crab age (Figure 2). The d C USA) before extraction. These freeze-dried samples values of S. dehaani belonging to Age1 and Age2 were were weighed using an electric balance (Model A120S; similar to those of detrital sediment, while the d C Sartorius, Goettingen, Germany) to calculate fatty acid values of crabs in the Age3 and Age4 group were much content per dry weight (g FA g ). Dried and weighed higher than those of the Age1 and Age2 groups, samples were wrapped in glass fiber filter paper pre- indicating carbon sources other than detrital sediment combusted at 4008C for extraction. Fatty acids from (Figure 2A). The d N values of Age3 and Age4 were filter papers were measured to determine the basal significantly higher than those of Age1 and Age2 after amount of fatty acids. We used a mix of 37 fatty acid July, which, in turn, were higher than those of detrital methyl esters (Supelco Cat. No. 47885-u) and marine sediment (Figure 2B). Detrital sediment showed a source fatty acid methyl esters (Sigma-Aldrich, 13 15 relatively low d C and relatively high d N value in St. Louis, USA, Cat. No. 47033) to identify fatty acids April 2007, which was the dry season (average tem- on the basis of retention time. Further, we used perature: 12.18C), than in the wet and high temperature heneicosanoic acid (21:0, 1 mg mL ) as an internal season (average temperature: 25.48C) in August 2007. standard; it was added to the freeze-dried samples immediately prior to the extraction process. Extraction and methylation were performed according to the Stable isotope signatures of S. dehaani Kattner and Fricke (1986) method. Extracted fatty in the wet and dry periods acid samples were analyzed using a gas chromatograph (Agilent, Santa Clara, USA, 6890N) with a Program- S. dehaani showed very distinctive stable isotope signa- mable-Temperature-Vaporizer and a Flame-Ionization- tures between the dry period (April) and wet period Animal Cells and Systems 165 Figure 2. (A) Mean (barSD) d C of detrital sediment, Salix subfragilis, and Sesarma dehaani in the Janghang wetland in 2007. (B) Mean (barSD) d N of detrital sediment, S. subfragilis, and S. dehaani in the Janghang wetland in 2007. a, b, c, and d indicate the results of Tukey multiple comparison. (August) (Figure 3). In April, the d C value of Age4 was Food web structure in the Janghang wetland based on a stable isotope signature much higher than that of other age classes, which were close to the d C value of detrital sediment. In the wet To understand the whole food web structure in an period (August), the d C values of Age3 and Age4 were S. subfragilis-dominated wetland, we included carbon clearly higher than those of Age1 and Age2, which were and nitrogen isotope signatures of other organisms close to the d C values of detrital sediment, indicating such as fish and lugworm collected from near the study that Age3 and Age4 had other carbon sources. The d N site. The d C value of fish such as Gobiidae and values of Age3 and Age4 were higher than those of Age1 flathead mullet (Mugil cephalus) were much higher and Age2. In the wet period (August), in particular, the than those of Age3 and Age4, suggesting that these fish d N values of Age3 and Age4 were approximately 1.8% were possible carbon sources for Age3 and Age4. higher than those of Age1 and Age2, supporting the Further, the d C value of skin carp (Hemibarbus observation that Age3/Age4 cannibalized Age1/Age2. labeo) was close to that of S. dehaani (Figure 4). 166 D. Han et al. 13 15 Figure 3. A d C and d N diagram of the Janghang wetland in the (A) dry period (April 2007) and (B) wet and humid period (August 2007). 14, Crab; 1, Age1; 2, Age2; 3, Age3; 4, Age4; 5, Spider; 68, Plant; 6, Monocotyledon; 7, Dicotyledon; 8, Salix;9, detrital sediment. Fatty acid biomarkers for detrital sediment and Comparison of fatty acid profiles among age classes of S. subfragilis leaves S. dehaani To select useful biomarkers for carbon sources, we PCA of the fatty acid profiles of each age class of analyzed the fatty acid profiles of detrital sediment and S. dehaani showed distinctive grouping between Age1/ S. subfragilis (Figure 5). The levels of fatty acids 18:2v6 Age2 and Age3/Age4 along the first principal compo- and 18:3v3 appeared to be higher in the fresh leaves of nent (PC1) and second component (PC2) (Figure 6A). S. subfragilis than in detrital sediment. In contrast, PC1 explained 55.2% of the total variance, while PC2 16:1v7 and 22:2v6 levels appeared to be higher in explained 16.9%, covering 72.1% of the total variance detrital sediment than in S. subfragilis leaves. There- together. With regard to PC1, the scores of both Age1/ fore, we selected 18:2v6 and 18:3v3 as markers for Age2 and Age3/Age4 were located between the scores living plant material and 16:1v7 and 22:2v6 as markers for detrital sediment and S. subfragilis leaves. The PC1 for detrital sediment. Individuals of S. dehaani in Age1 scores of Age1/Age2 were relatively close to that of and Age2 showed relatively high 16:1v7 content while detrital sediment, while the PC1 scores of Age3/Age4 18:3v3 content was relatively high in Age2, Age3, and were relatively close to that of S. subfragilis leaves. As Age4 S. dehaani grows from Age1/Age2 to Age3/Age4, Animal Cells and Systems 167 13 15 Figure 4. A d C and d N diagram of the Janghang wetland, using annual average values and candidate food sources for S. dehaani.14, Crab; 1, Age1; 2, Age2; 3, Age3; 4, Age4; 510, Plant; 5, Monocotyledon; 6, Dicotyledon; 7, Sium suave; 8, Reed; 9, Salix; 10, Salix (litter); 1113, Arthropod; 11, Insect; 12, Spider; 13, Lugworm; 14, Fungus, Mushroom; 1517, Fish; 15, Skin carp; 16, Goby; 17, Flathead mullet; 18, detrital sediment. 16:1v7, the sediment biomarker, appears to decrease, addition, the ranges of PCA scores on the fatty acid while 18:2v6 and 18:3v3, the S. subfragilis leaf profiles were wider for Age3/Age4 than Age1/Age2, biomarker, increases (Figure 6B). indicating that mature individuals feed on more diverse carbon sources than immature ones. Our results were well supported by field observa- Discussion tions of the feeding behavior of S. dehaani. Mature individuals of S. dehaani have been observed to feed on Studies on interactions between trees and crabs in diverse fresh and fallen leaves of S. subfragilis, litter of forested estuarine wetlands have focused on mangrove S. subfragilis in detrital sediment, leaves of Phragmites forests in tropical and subtropical regions. These communis, molted carapaces of S. dehaani, and dead studies have found that crabs feed on the leaves or fish and bivalves. The cannibalistic behavior of mature litter of mangroves, detritus, or sediment (Lee 1997; S. dehaani was observed by the authors on several Skov and Harnoll 2002). In these regions, mangrove occasions. crabs return organic matter through their excreta, Our results indicate that S. dehaani experience accounting for as much as 24% of mangrove leaf ontogenic diet changes from sediment feeding to production (Lee 1997), and they feed on 81.3% of omnivorous feeding. Although ontogenic diet shifts mangrove annual production (Inga et al. 2006). How- are well known for many aquatic species such as fish, ever, there are few studies on forested estuarine wet- there are few studies on ontogenic diet shift in crabs lands in temperate regions. Our previous study found (Werner and Gilliam 1984). A blue crab, Callinectes that the secondary productivity of S. dehaani was as sapidus, and a portunid crab, Liocarcinus depurator, high as 100.2 g fresh weight (FW) C m , indicating have been reported to show different feeding behaviors that the crabs feed on up to 60% of the organic matter depending on size (Laughlin 1982; Freire et al. 1996). produced by S. subfragilis (Han et al. 2010). Results However, there are no reports available on ontogenic from both stable isotope and fatty acid analyses in the diet shifts of crabs in woody wetlands such as present study indicate that mature S. dehaani indivi- mangrove ecosystems (Cannicci et al. 2008; Kristensen duals (Age3 and Age4) feed on both detrital sediment and S. subfragilis leaves in the summer in addition to et al. 2010). Cannibalism among crustaceans is well documen- engaging in the cannibalism of younger individuals and ted (Jormalainen and Shuster 1997). Jormalainen and decaying fish. In contrast, immature crabs (Age1 and Age2) appear to feed on detrital sediment only. In Shuster (1997) summarized four conditions conducive 168 D. Han et al. Figure 5. (A) Comparison of important fatty acid contents in detrital sediment and S. subfragilis (n3). (B) Fatty acid content in each age class of S. dehaani in the Janghang wetland (n17). Bars indicate average fatty acid content with error bars (9standard deviation). We showed results of t-test with a star (A) and Tukey multiple comparison with a, b, c, and d. to cannibalism: small habitat, high local population individuals, except for Age4, exhibited increases in density, food shortage, and structural simplicity of C:N ratios after August 2007, indicating that the habitats. In addition to these, food quality in terms animals had high C:N diets (Figure 7B). Mature S. of carbon to nitrogen (C:N) ratio has been suggested dehaani individuals, particularly those belonging to as an important factor for cannibalism (Wolcott and Age4, appeared to have managed to keep their C:N Wolcott 1984). Our results indicate that S. dehaani ratio low, except in September, possibly by cannibal- individuals might have experienced nitrogen defi- ism of younger individuals (Linton and Greenaway ciency during summer and fall since the C:N ratio of 2007). S. subfragilis leaves dramatically increased to more Intensive studies on mangrove ecosystems suggest that sesarmid crabs are ecosystem engineers, than 20 after June 2007 (Figure 7A). S. dehaani Animal Cells and Systems 169 Figure 6. (A) PCA scores based on fatty acid profiles of sediment, S. subfragilis and S. dehaani of each age class in the Janghang wetland in September 2006, and (B) the most important loading values on the first and second principal components. responsible for burrowing construction and mainte- In conclusion, our results show the differences in nance, redistribution of organic matter and burial of the feeding patterns of immature and mature S. dehaani litter, and exchange between sediment and water/air individuals through carbon and nitrogen stable isotope (Kristensen 2008). Further, herbivorous crabs in man- signatures and fatty acid biomarkers. Immature indivi- grove forests have been reported to affect vegetation duals appear to feed mainly on detrital sediment, while structure and ecosystem function in various ways: mature individuals feed on more diverse carbon grazing, maintaining high leaf litter turnover rates, sources such as fresh and fallen leaves of S. subfragilis, recycling mangrove organic production, and propagule fish, and younger individuals of their own species in predation (Cannicci et al. 2008). We expect that addition to detrital sediment. Our results provide S. dehaani plays similar roles in S. subfragilis wetlands. useful information regarding energy flows and nutrient Future studies are required to understand the ecological cycling in S. subfragilis forest wetlands and estuarine roles of S. dehaani in S. subfragilis wetland ecosystems. ecosystems. 170 D. Han et al. Figure 7. (A) Seasonal changes in C:N ratio in S. dehaani, detrital sediment, and S. subfragilis. 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