Analysis of primary food sources and trophic relationships of aquatic animals in a mangrove-fringed estuary,Khung Krabaen Bay (Thailand) using dual stable isotope techniques

Stable carbon (¹³C) and nitrogen (¹⁵N) isotopes were used to elucidate primary food sources and trophic relationships of organisms in Khung Krabaen Bay and adjacent offshore waters. The three separate sampling sites were mangroves, inner bay and offshore. The ¹³C values of mangrove leaves were –28.2 to –29.4, seagrass –10.5, macroalgae –14.9 to –18.2, plankton –20.0 to –21.8, benthic detritus –15.1 to –26.3, invertebrates –16.5 to –26.0, and fishes –13.4 to –26.3. The ¹⁵N values of mangrove leaves were 4.3 to 5.7, seagrass 4.3, macroalgae 2.2 to 4.4, plankton 5.7 to 6.4 , benthic detritus 5.1 to 5.3, invertebrates 7.2 to 12.2 , and fishes 6.3 to 15.9. The primary producers had distinct ¹³C values. The ¹³C values of animals collected from mangroves were more negative than those of animals collected far from shore. The primary carbon sources that support food webs clearly depended on location. The contribution of mangroves to food webs was confined only to mangroves, but a mixture of macroalgae and plankton was a major carbon source for organisms in the inner bay area. Offshore organisms clearly derived their carbon through the planktonic food web. The ¹⁵N values of consumers were enriched by 3–4 relative to their diets. The ¹⁵N data suggests that some of aquatic animals had capacity to change their feeding habits according to places and availability of foods and as a result, individuals of the same species could be assigned to different trophic levels at different places.     

Food web structure in exotic and native mangroves: a Hawaii–Puerto Rico comparison

Plant invasions can fundamentally alter detrital inputs and the structure of detritus-based food webs. We examined the detrital pathways in mangrove food webs in native (Puerto Rican) and introduced (Hawaiian) Rhizophora mangle forests using a dual isotope approach and a mixing model. Based on trophic-level fractionation of 0–1‰ for δ ¹³C and 2–3‰ for δ ¹⁵N, among the invertebrates, only nematodes, oligochaetes, and nereid polychaetes from native mangroves exhibited stable isotopes consistent with a mangrove-derived diet. Certain fauna, in particular tubificid oligochaetes, had δ ¹³C values consistent with the consumption of mangrove leaves, but they were depleted in ¹⁵N, suggesting their primary nitrogen source was low in ¹⁵N, and was possibly N₂-fixing bacteria. In introduced mangroves, all feeding groups appeared to rely heavily on non-mangrove sources, especially phytoplankton inputs. Mixing model results and discriminant analysis showed clear separation of introduced and native mangrove sites based on differential food source utilization within feeding groups, with stronger and more diverse use of benthic foods observed in native forests. Observed differences between native and invasive mangrove food webs may be due to Hawaiian detritivores being poorly adapted to utilizing the tannin-rich, nitrogen-poor mangrove detritus. In addition, differential utilization of mangrove detritus between native and introduced mangroves may be a consequence of forest age. We postulate that increasing mangrove forest age may promote diversification of bacterial food webs important in N and S cycling. Our results also suggest a potentially important role for sulfur bacteria in supporting the most abundant infaunal consumers, nematodes, in the most mature systems. Electronic supplementary material The online version of this article (doi:) contains supplementary material that is available to authorized users.     

Mechanism for the small-scale movement of carbon among estuarine habitats: organic matter transfer not crab movement

In theory, carbon is highly mobile in aquatic systems. Recent evidence from carbon stable isotopes of crabs (Parasesarma erythrodactyla and Australoplax tridentata), however, shows that in subtropical Australian waters, measurable carbon movement between adjacent mangrove and saltmarsh habitats is limited to no more than a few metres. We tested whether the pattern in crab δ¹³C values across mangrove and saltmarsh habitats was explained by crab movement, or the movement of particulate organic matter. We estimated crab movement in a mark–recapture program using an array of pitfall traps on 13 transects (a total of 65 traps) covering an area of 600 m² across the interface of these two habitats. Over a 19-day period, the majority of crabs (91% for P. erythrodactyla, 93% for A. tridentata) moved <2 m from the place of initial capture. Crab movement cannot, therefore, explain the patterns in δ¹³C values of crabs. δ¹³C values of detritus collected at 2-m intervals across the same habitat interface fitted a sigmoidal curve of a similar form to that fitting the δ¹³C values of crabs. δ¹³C values of detritus were 2–4‰ more depleted in saltmarsh (−18.5±0.6‰), and 4–7‰ more depleted in mangroves (−25.9±0.1‰) than δ¹³C values of crabs recorded previously in each habitat. Assimilation by crabs of very small detrital fragments or microphytobenthos, more enriched in ¹³C, may explain the disparity in δ¹³C values. Nevertheless, the pattern in δ¹³C values of detritus suggests that crabs obtain their carbon from up to several metres away, but without themselves foraging more then a metre or so from their burrow. Such detailed measurements of carbon movement in estuaries provide a spatially explicit understanding of the functioning of food webs in saltmarsh and mangrove habitats.     

Trophic polymorphism in bluegill sunfish (<Emphasis Type="Italic">Lepomis macrochirus</Emphasis>) introduced into Lake Biwa: evidence from stable isotope analysis

Trophic polymorphism was recently reported in introduced bluegill (Lepomis macrochirus) in Lake Biwa, Japan, where three morphs are specialized in benthic invertebrates (benthivorous type), submerged aquatic plants (herbivorous type), and zooplankton (planktivorous type). We evaluated the long-term effects of food resource utilization by these trophic morphs using stable isotope ratios, δ¹⁵N and δ¹³C. A significant difference in δ¹⁵N was found between the benthivorous and planktivorous types. The planktivorous type had the higher δ¹⁵N value, which corresponded with the value expected from its prey, zooplankton. The lower δ¹⁵N value of the benthivorous type would be derived from the lower δ¹⁵N values of benthic prey organisms compared to zooplankton. These results support previous findings that the benthivorous and planktivorous types have different food resource utilization. In contrast, the δ¹⁵N and δ¹³C values of the herbivorous type were distinctly different from the expected values, indicating that this type was unlikely to utilize aquatic plants substantially, contradicting the results of the dietary analysis.     

Spatial variability in Florida Bay particulate organic matter composition: combining flow cytometry with stable isotope analyses

Long-term management plans for restoration of natural flow conditions through the Everglades increase the importance of understanding potential nutrient impacts of increased freshwater delivery on Florida Bay biogeochemistry. Planktonic communities respond quickly to changes in water quality, thus spatial variability in community composition and relationships to nutrient parameters must be understood in order to evaluate future downstream impacts of modifications to Everglades hydrology. Here we present initial results combining flow cytometry analyses of phytoplankton and bacterial populations (0.1–50 μm size fraction) with measurements of δ¹³C and δ¹⁵N composition and dissolved inorganic nutrient concentrations to explore proxies for planktonic species assemblage compositions and nutrient cycling. Particulate organic material in the 0.1–50 μm size fraction was collected from five stations in Northeastern and Western Florida Bay to characterize spatial variability in species assemblage and stable isotopic composition. A dense bloom of the picocyanobacterium, Synechococcus elongatus, was observed at Western Florida Bay sites. Smaller Synechococcus sp. were present at Northeast sites in much lower abundance. Bacteria and detrital particles were also more abundant at Western Florida Bay stations than in the northeast region. The highest abundance of detritus occurred at Trout Creek, which receives freshwater discharge from the Everglades through Taylor Slough. In terms of nutrient availability and stable isotopic values, the S. elongatus population in the Western bay corresponded to low DIN (0.5 μM NH ₄ ⁺ ; 0.2 μM NO ₃ ⁻ ) concentrations and depleted δ¹⁵N signatures ranging from +0.3 to +0.8‰, suggesting that the bloom supported high productivity levels through N₂-fixation. δ¹⁵N values from the Northeast bay were more enriched (+2.0 to +3.0‰), characteristic of N-recycling. δ¹³C values were similar for all marine Florida Bay stations, ranging from −17.6 to −14.4‰, however were more depleted at the mangrove ecotone station (−25.5 to −22.3‰). The difference in the isotopic values reflects differences in carbon sources. These findings imply that variations in resource availability and nutrient sources exert significant control over planktonic community composition, which is reflected by stable isotopic signatures.     

Isotopic analysis of three food web theories in constricted and floodplain regions of a large river

Analyses of stable isotope (δ¹³C and δ¹⁵N) and C:N ratios of food webs within a floodplain and a constricted-channel region of the Ohio River during October 1993 and July 1994 indicate that the increasingly influential flood pulse concept (FPC) does not, for either location, adequately address food web structure for this very large river. Furthermore, results of this study suggest that the riverine productivity model (RPM) is more appropriate than the widely known river continuum concept (RCC) for the constricted region of this river. These␣conclusions are based on stable isotope analyses of potential sources of organic matter (riparian C₃ trees, riparian C₄ grasses and agricultural crops, submerged macrophytes, benthic filamentous algae, benthic particulate organic matter, and transported organic matter containing detritus and phytoplankton) and various functional feeding groups of invertebrate and fish consumers. The FPC, which stresses the key contribution of organic matter, particularly terrestrial organic matter, originating from the floodplain to riverine food webs, was judged inappropriate for the floodplain region of the Ohio River for hydrodynamic and biotic reasons. The rising limb and peak period of discharge typically occur in November through March when temperatures are low (generally much less than 10°C) and greater than bank-full conditions are relatively unpredictable and short-lived. The major food potentially available to riverine organisms migrating into the floodplain would be decaying vegetation because autotrophic production is temperature and light limited and terrestrial insect production is minimal at that time. It is clear from our data that terrestrial C₄ plants contribute little, if anything, to the consumer food web (based on δ¹³C values), and δ¹⁵N values for C₃ plants, coarse benthic organic matter, and fine benthic organic matter were too depleted (∼7–12‰ lower than most invertebrate consumer values) for this organic matter to be supporting the food web. The RPM, which emphasizes the primary role of autotrophic production in large rivers, is the most viable of the remaining two ecosystem models for the constricted-channel region of the Ohio based on stable isotope linkage between sources and consumers of organic matter in the food web. The most important form of food web organic matter is apparently transported (suspended) fine (FTOM) and ultra-fine particulate organic matter. We propose that phytoplankton and detritus of an autochthonous origin in the seston would represent a more usable energy source for benthic (bivalve molluscs, hydropsychid caddisflies) and planktonic (microcrustaceans) suspension feeders than the more refractory allochthonous materials derived from upstream processing of terrestrial organic matter. Benthic grazers depend heavily on nonfilamentous benthic algae (based on gut analysis from a separate study), but filamentous benthic algae have no apparent connection to invertebrate consumers (based on δ¹³C values). Amphipod and crayfish show a strong relationship to aquatic macrophytes (possibly through detrital organic matter rather than living plant tissue). These observations contrast with the prediction of the RCC that food webs in large rivers are based principally on refractory FTOM and dissolved organic matter from upstream inefficiencies in organic-matter processing and the bacteria growing upon these suspended or dissolved detrital compounds. The conclusions drawn here for the Ohio River cannot yet be extended to other floodplain and constricted-channel rivers in temperate and tropical latitudes until more comparable data are available on relatively pristine and moderately regulated rivers. Received: 3 January 1997 / Accepted: 28 August 1998     

Piscivorous birds as top predators and fishery competitors in the lagoon ecosystem

Trophic patterns of omnivorous freshwater shrimps, Exopalaemon modestus and Macrobrachium nipponensis, were investigated in two shallow eutrophic lakes by using stable isotope analysis. δ¹⁵N and δ¹³C of M. nipponensis and E. modestus increased with increasing body weight, which might be attributed to larger individuals ingesting organisms that feed higher up the food chain and/or increased assimilation of benthic food items with enriched isotopic signatures. Of the freshwater shrimps occurring in the studied lakes, those from Lake Taihu had significantly elevated δ¹⁵N and δ¹³C values (4.3‰ and 1.8‰, respectively) compared with those from the less eutrophic Lake Chaohu, indicating that the isotopic signature might partially reflect the trophic states of their habitats. Mixing model results suggested that the benthic food web provides the primary carbon source for both shrimp species, and that E. modestus assimilated relatively more pelagic food sources than M. nipponensis in these lakes. Handling editor: S. Wellekens     

Benthic-pelagic trophic interactions within the fish assemblage in the western Bering Sea shelf area according to stomach content analysis and ratios of C and N stable isotopes

The composition, abundance, diet and trophic status of zooplankton, bottom invertebrates, fish and nekton were analyzed based on the data collected by the staff of the TINRO-Center during complex bottom trawl catches on the Bering Sea shelf in the fall of 2004. The stomach contents of mass fish species were analyzed and the nitrogen and carbon isotopic composition of 36 mass species of plankton, benthos, nekton and nektobenthos, which together make up the basis of pelagic and bottom communities, was determined. It was found that zooplankton noticeably differ from benthic invertebrates in carbon isotopic composition: δ¹³C values in zooplankton varied from −20.3‰ to −17.9‰; in benthos—from −17.5‰to −13.0‰; and in fish—from −19.2‰ (juvenile walleye pollock) to −15.3‰ (saffron cod). The levels of ¹³C isotope in the tissues of fish depended mostly on the share of pelagic or benthic animals in their diet. δ¹⁵N values in the studied species ranged from 8.6‰ (in sea urchins) to 17.2‰ (in large Pacific cods), which corresponds to a trophic level of 2.8. Obviously the δ¹⁵N values reflect the degree of predation and generally show the ratio of primary, secondary and tertiary consumers in a fish’s diet. Trophic interactions manifest a high degree of interdependence between benthic and pelagic communities (even without taking into account such lower components of the food web as phytoplankton, bacteria, and protozoa) occurring in most nektonic species that depend on both bottom and pelagic food.     

Trophic relationships of juvenile blue crabs (Callinectes sapidus) in estuarine habitats

Salt marshes and shallow-water macroalgal beds are known to provide nursery habitat for many species of fish and invertebrates. The role of these habitats as refuge from predation is well established, but the degree to which indigenous primary production within the nursery provides food for growth and development of estuarine species remains unresolved. In this study, we tested the hypothesis that juvenile blue crabs depend on indigenous primary production, directly or indirectly, during their entire stay within the nursery. To test this hypothesis, we conducted isotopic studies and stomach content analyses of juveniles from habitats near the mouth of Delaware Bay and from an adjacent lagoonal estuary (ca. 39.5° N, 75.1° W). Primary producers, marsh detritus, various life-history stages of blue crabs and potential prey species were sampled in the main estuary and in an adjacent marsh during the summer and early fall of two consecutive years. Newly settled juveniles (<15 mm carapace width) from the marsh were about 1.8‰ lighter in carbon (−17.2‰) relative to larger juveniles from the marsh (15–30 mm carapace width) and appeared to have retained a carbon isotopic signature indicative of the phytoplankton-based food web associated with larval stages. However, the signature of juveniles changed as a function of size. Large juveniles and crabs >60 mm were enriched in δ¹³C (−14.7 ± 0.1‰) compared to small crabs, suggesting a gradual shift in diet from a planktonic to a detritus-based food web with increasing size. As with crabs from Delaware Bay, the δ¹³C signature of juvenile crabs sampled from macroalgal beds in the lagoonal estuary (Rehoboth Bay) changed as a function of size. Also, δ¹³C ratios of crabs varied among the various species of macroalgae. The δ¹⁵N composition of primary producers in the marsh and main estuary also was reflected in the δ¹⁵N values of crabs and other benthic consumers in the respective habitats. Results of stomach-content analysis in this study were consistent with isotope data. Observed changes in prey preferences were related to changes in size of juvenile crabs and also differed among habitats. Gut content analyses of the three size classes of juveniles in macroalgal beds from Rehoboth Bay indicated that the crabs depend heavily on various amphipod species that occur on the seaweeds. These amphipods graze directly on the macroalgae and are among the most abundant invertebrates in the macroalgal beds. This implies a direct trophic relationship between the juvenile crabs and the macroalgae. In summary, our study provides strong evidence that the value of nursery areas such as salt marshes and macroalgal beds goes beyond that of providing refuge from predation, and that species using these nurseries (e.g. juvenile blue crabs) are ultimately dependent on primary production originating in benthic plants indigenous to the nursery.     

Food web structure of a shallow eutrophic lake (Lake Taihu,China) assessed by stable isotope analysis

Lake Taihu is a large, shallow, and eutrophic lake in China. It has provided local communities with valuable fisheries for centuries, but little is known of the trophodynamics, or of its faunal communities. Carbon and nitrogen isotopic composition was used to assess its trophic pathways and the food web structure [food sources and trophic levels (TL)]. Basal food sources were distinguishable based on their δ¹³C values, ranging from −27.2 to −15.2‰. Consumers were also well separated in δ¹³C (−26.9 to −17.9‰ for invertebrates and −25.7 to −18.1‰ for fishes), which allowed for an effective discrimination of carbon sources between these fauna. An average trophic enrichment factor of 3.4‰ was used to calculate the TLs based on δ¹⁵N of zooplankton, with results indicating a food web having four TLs. Although δ¹⁵N values overlap and cover a large range within trophic compartments, the isotopic signatures of the species assessed revealed a general trend of ¹⁵N enrichment with increasing TL. Stable isotope signatures were also used to establish a general food web scheme in which five main trophic pathways were analyzed.