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The use of stable isotopes of carbon (δ13C) and nitrogen (δ15N) from feces and breath offers potential as non-destructive tools to assess diets and nutrition. How stable isotope values derived from breath and feces compare with those from commonly used tissues, such as blood fractions and liver, remains uncertain, including understanding the metabolic routing of dietary nutrients. Here, we measured δ13C and δ15N from feces and δ13C of breath from captive Red-necked Stints (Calidris ruficollis) and 26 species of wild-caught migratory shorebirds (n = 259 individuals) and compared them against isotopic values from blood and feathers. For captive birds fed either cereal- or fish-based diets, differences in δ13C between feces and lipid-free diet were small, - 0.2 ± 0.5 and 0.1 ± 0.3, respectively, and differences in δ15N, - 0.7 ± 0.5 and - 0.5 ± 0.5, respectively. Hence, δ13C and δ15N values from feces can serve as proxies for ingested proteinaceous tissues and non-soluble carbohydrates because isotopic discrimination can be considered negligible. Stable isotope values in plasma and feces were strongly correlated in wild-caught shorebirds, indicating feces can be used to infer assimilated macronutrients. Breath δ13C was 1.6 ± 0.8 to 5.6 ± 1.2 lower than bulk food sources, and breath C derived from lipids was estimated at 47.5% (cereal) to 96.1% (fish), likely underlining the importance of dietary lipids for metabolism. The findings validate the use of stable isotope values of feces and breath in isotopic assays to better understand the dietary needs of shorebirds.
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Carbono , Dieta , Animais , Carboidratos , Isótopos de Carbono/metabolismo , Dieta/veterinária , Fezes , Peixes/metabolismo , Isótopos de Nitrogênio/metabolismoRESUMO
Because coastal habitats store large amounts of organic carbon (Corg ), the conservation and restoration of these habitats are considered to be important measures for mitigating global climate change. Although future sea-level rise is predicted to change the characteristics of these habitats, its impact on their rate of Corg sequestration is highly uncertain. Here we used historical depositional records to show that relative sea-level (RSL) changes regulated Corg accumulation rates in boreal contiguous seagrass-saltmarsh habitats. Age-depth modeling and geological and biogeochemical approaches indicated that Corg accumulation rates varied as a function of changes in depositional environments and habitat relocations. In particular, Corg accumulation rates were enhanced in subtidal seagrass meadows during times of RSL rise, which were caused by postseismic land subsidence and climate change. Our findings identify historical analogs for the future impact of RSL rise driven by global climate change on rates of Corg sequestration in coastal habitats.
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Sequestro de Carbono , Ecossistema , Monitoramento Ambiental , Estuários , Água do Mar/análise , Carbono/análise , Carbono/metabolismo , Mudança Climática , Conservação dos Recursos Naturais , Sedimentos Geológicos/análise , Plantas/metabolismoRESUMO
Carbon captured by marine organisms helps sequester atmospheric CO2 , especially in shallow coastal ecosystems, where rates of primary production and burial of organic carbon (OC) from multiple sources are high. However, linkages between the dynamics of OC derived from multiple sources and carbon sequestration are poorly understood. We investigated the origin (terrestrial, phytobenthos derived, and phytoplankton derived) of particulate OC (POC) and dissolved OC (DOC) in the water column and sedimentary OC using elemental, isotopic, and optical signatures in Furen Lagoon, Japan. Based on these data analysis, we explored how OC from multiple sources contributes to sequestration via storage in sediments, water column sequestration, and air-sea CO2 exchanges, and analyzed how the contributions vary with salinity in a shallow seagrass meadow as well. The relative contribution of terrestrial POC in the water column decreased with increasing salinity, whereas autochthonous POC increased in the salinity range 10-30. Phytoplankton-derived POC dominated the water column POC (65-95%) within this salinity range; however, it was minor in the sediments (3-29%). In contrast, terrestrial and phytobenthos-derived POC were relatively minor contributors in the water column but were major contributors in the sediments (49-78% and 19-36%, respectively), indicating that terrestrial and phytobenthos-derived POC were selectively stored in the sediments. Autochthonous DOC, part of which can contribute to long-term carbon sequestration in the water column, accounted for >25% of the total water column DOC pool in the salinity range 15-30. Autochthonous OC production decreased the concentration of dissolved inorganic carbon in the water column and thereby contributed to atmospheric CO2 uptake, except in the low-salinity zone. Our results indicate that shallow coastal ecosystems function not only as transition zones between land and ocean but also as carbon sequestration filters. They function at different timescales, depending on the salinity, and OC sources.
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'Blue Carbon', which is carbon captured by marine living organisms, has recently been highlighted as a new option for climate change mitigation initiatives. In particular, coastal ecosystems have been recognized as significant carbon stocks because of their high burial rates and long-term sequestration of carbon. However, the direct contribution of Blue Carbon to the uptake of atmospheric CO2 through air-sea gas exchange remains unclear. We performed in situ measurements of carbon flows, including air-sea CO2 fluxes, dissolved inorganic carbon changes, net ecosystem production, and carbon burial rates in the boreal (Furen), temperate (Kurihama), and subtropical (Fukido) seagrass meadows of Japan from 2010 to 2013. In particular, the air-sea CO2 flux was measured using three methods: the bulk formula method, the floating chamber method, and the eddy covariance method. Our empirical results show that submerged autotrophic vegetation in shallow coastal waters can be functionally a sink for atmospheric CO2. This finding is contrary to the conventional perception that most near-shore ecosystems are sources of atmospheric CO2. The key factor determining whether or not coastal ecosystems directly decrease the concentration of atmospheric CO2 may be net ecosystem production. This study thus identifies a new ecosystem function of coastal vegetated systems; they are direct sinks of atmospheric CO2.
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Alismatales/metabolismo , Ciclo do Carbono , Dióxido de Carbono/metabolismo , Ecossistema , Mudança Climática , Geografia , Japão , Estações do AnoRESUMO
Food webs are comprised of a network of trophic interactions and are essential to elucidating ecosystem processes and functions. However, the presence of unknown, but critical networks hampers understanding of complex and dynamic food webs in nature. Here, we empirically demonstrate a missing link, both critical and variable, by revealing that direct predator-prey relationships between shorebirds and biofilm are widespread and mediated by multiple ecological and evolutionary determinants. Food source mixing models and energy budget estimates indicate that the strength of the missing linkage is dependent on predator traits (body mass and foraging action rate) and the environment that determines food density. Morphological analyses, showing that smaller bodied species possess more developed feeding apparatus to consume biofilm, suggest that the linkage is also phylogenetically dependent and affords a compelling re-interpretation of niche differentiation. We contend that exploring missing links is a necessity for revealing true network structure and dynamics.
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Biofilmes , Charadriiformes/fisiologia , Comportamento Alimentar , Cadeia Alimentar , Animais , Bico/anatomia & histologia , Tamanho Corporal , Charadriiformes/classificação , Dieta , Metabolismo Energético , Isótopos/química , Modelos Biológicos , Filogenia , Comportamento Predatório , Língua/anatomia & histologia , Língua/ultraestruturaRESUMO
Shorebirds use key migratory stopover habitats in spring and fall where body proteins are replenished and lipids stored as fuel for the remaining journey. The Fraser River estuary, British Columbia, Canada, is a critical spring stopover site for hundreds of thousands of migrating western sandpiper, Calidris mauri, and dunlin, Calidris alpina. Intertidal biofilm in spring is an important nutritional source for western sandpiper, with previous isotopic research predicting 45-59% of total diet and 50% of total energy needs. However, these studies relied on isotopic mixing models that did not consider metabolic routing of key dietary macromolecules. Complexity arises due to the mixed macromolecular composition of biofilm that is difficult to characterize isotopically. We expanded on these earlier findings by considering a protein pathway from diet to the body protein pool represented by liver tissue, using a Bayesian mixing model based on δ 13C and δ 15N. We used δ 13C measurements of adipose tissue and breath CO2 to provide an estimate of the carbohydrate and protein δ 13C values of microphytobenthos and used these derived values to better inform the isotopic mixing models. Our results reinforce earlier estimates of the importance of biofilm to staging shorebirds in predicting that assimilated nutrients from biofilm contribute ~35% of the protein budgets for staging western sandpipers (n = 13) and dunlin (n = 11) and at least 41% of the energy budget of western sandpiper (n = 69). Dunlin's ingestion of biofilm appeared higher than anticipated given their expected reliance on invertebrate prey compared to western sandpiper, a biofilm specialist. Isotopic analyses of bulk tissues that consider metabolic routing and that make use of breath CO2 and adipose lipid assays can provide new insights into avian physiology. We advocate further isotopic research to better understand biofilm use by migratory shorebirds in general and as a critical requirement for more effective conservation.
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Shallow coastal ecosystems are reservoirs of carbon derived from allochthonous organic matter and autochthonous organic matter produced by microalgae and macrophytes. Carbon stored in vegetated coastal ecosystems has attracted broad attention as an important component of carbon sinks. Characterizing the source of carbon in sediments is essential for quantifying the carbon-sequestration function of shallow coastal ecosystems. In this study, we investigated the origins of organic matter using organic biomarkers (lignin phenols, fatty acids, cutin acids, diacids, and ω-hydroxy acids) in surface sediments in a seagrass-dominated lagoon (Furen Lagoon, Japan). Biomarkers derived from allochthonous vascular plants, such as long-chain fatty acids, showed higher concentrations near river mouths. Furthermore, biomarker signals indicated that sedimentary organic carbon originated in large part from degraded allochthonous vascular plants including roots. A Bayesian mixing model using the ratios of syringyl phenols to vanillyl phenols and cinnamyl phenols to vanillyl phenols indicated that up to about 65% of lignin in the sediments was derived from seagrass. This result indicates a substantial contribution of seagrass to the sedimentary lignin pool in an estuarine seagrass meadow. However, the percent contribution of seagrass to the lignin pool varied, with higher values near a tidal inlet and relatively low values near river mouths. Vertical profiles of organic biomarkers varied with the differences in degradability of organic compounds. Specifically, long-chain fatty acids decreased with increasing depth more than the other compounds, suggesting that they degraded more easily. Conversely, we observed a tendency for lignin phenols to be selectively preserved in the vertical sediment profiles. Our results show that sediment organic biomarkers can provide diverse information such as the composition and origins of organic carbon, the contribution of seagrass derived lignin, and the varying degrees of decomposition. This approach should bring new insights to the estimation of carbon in future blue carbon studies.
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Ecossistema , Lignina , Teorema de Bayes , Carbono , Sequestro de Carbono , Sedimentos GeológicosRESUMO
Dietary specialization is common in animals and has important implications for individual fitness, inter- and intraspecific competition, and the adaptive potential of a species. Diet composition can be influenced by age- and sex-related factors including an individual's morphology, social status, and acquired skills; however, specialization may only be necessary when competition is intensified by high population densities or increased energetic demands.To better understand the role of age- and sex-related dietary specialization in facilitating seasonal resource partitioning, we inferred the contribution of biofilm, microphytobenthos, and benthic invertebrates to the diets of western sandpipers (Calidris mauri) from different demographic groups during mid-winter (January/February) and at the onset of the breeding migration (April) using stable isotope mixing models. Western sandpipers are sexually dimorphic with females having significantly greater body mass and bill length than males.Diet composition differed between seasons and among demographic groups. In winter, prey consumption was similar among demographic groups, but, in spring, diet composition differed with bill length and body mass explaining 31% of the total variation in diet composition. Epifaunal invertebrates made up a greater proportion of the diet in males which had lesser mass and shorter bills than females. Consumption of Polychaeta increased with increasing bill length and was greatest in adult females. In contrast, consumption of microphytobenthos, thought to be an important food source for migrating sandpipers, increased with decreasing bill length and was greatest in juvenile males.Our results provide the first evidence that age- and sex-related dietary specialization in western sandpipers facilitate seasonal resource partitioning that could reduce competition during spring at the onset of the breeding migration.Our study underscores the importance of examining resource partitioning throughout the annual cycle to inform fitness and demographic models and facilitate conservation efforts.
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Mangrove, seagrass, and coral habitats often lie adjacent to each other in the tropics and subtropics. Lateral carbon fluxes and their consecutive effects on CO2 dynamics and air-water fluxes along the ecosystem continuum are often overlooked. We measured the partial pressure of CO2 in water and associated biogeochemical parameters with a high temporal resolution and estimated air-water CO2 fluxes along the ecosystem continuum. Their lateral fluxes were estimated by using a biogeochemical mass-balance model. The results showed that the waters surrounding mangrove, seagrass, and coral habitats acted as a strong, moderate, and weak source of atmospheric CO2, respectively. The mangrove zone acted as a net source for TAlk, DIC, and DOC, but as a net sink for POC. The contribution of riverine and mangrove-derived OM was substantially high in mangrove sediment, indicating that net transport of POC towards the coastal sea was suppressed by the sediment trapping function of mangroves. The seagrass zone acted as a net source of all carbon forms and TAlk, whereas the coral zone acted as a net sink of TAlk, DIC, and DOC. The lateral transport of carbon from mangroves and rivers offset atmospheric CO2 uptake in the seagrass zone. DOC degradation might increase DIC, and other biogeochemical processes facilitate the functioning of the coral zone as a DOC sink. However, as a result of DIC uptake by autotrophs, mainly in the coral zone, the whole ecosystem continuum was a net sink of DIC and atmospheric CO2 evasion was lowered. We conclude that lateral transport of riverine and mangrove-derived DIC, TAlk, and DOC affect CO2 dynamics and air-water fluxes in seagrass and coral ecosystems. Thus, studies of lateral carbon fluxes at local and regional scales can improve global carbon budget estimates.
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Antozoários , Ecossistema , Animais , Carbono , Dióxido de Carbono , Áreas AlagadasRESUMO
Wetlands, tidal flats, seaweed beds, and coral reefs are valuable not only as habitats for many species, but also as places where people interact with the sea. Unfortunately, these areas have declined in recent years, so environmental improvement projects to conserve and restore them are being carried out across the world. In this study, we propose a method for quantifying ecosystem services, that is, useful for the proper maintenance and management of artificial tidal flats, a type of environmental improvement project. With this method, a conceptual model of the relationship between each service and related environmental factors in natural and social systems was created, and the relationships between services and environmental factors were clarified. The state of the environmental factors affecting each service was quantified, and the state of those factors was reflected in the evaluation value of the service. As a result, the method can identify which environmental factors need to be improved and if the goal is to increase the value of the targeted tidal flat. The method demonstrates an effective approach in environmental conservation for the restoration and preservation of coastal areas.
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An amendment to this paper has been published and can be accessed via a link at the top of the paper.
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The term Blue Carbon (BC) was first coined a decade ago to describe the disproportionately large contribution of coastal vegetated ecosystems to global carbon sequestration. The role of BC in climate change mitigation and adaptation has now reached international prominence. To help prioritise future research, we assembled leading experts in the field to agree upon the top-ten pending questions in BC science. Understanding how climate change affects carbon accumulation in mature BC ecosystems and during their restoration was a high priority. Controversial questions included the role of carbonate and macroalgae in BC cycling, and the degree to which greenhouse gases are released following disturbance of BC ecosystems. Scientists seek improved precision of the extent of BC ecosystems; techniques to determine BC provenance; understanding of the factors that influence sequestration in BC ecosystems, with the corresponding value of BC; and the management actions that are effective in enhancing this value. Overall this overview provides a comprehensive road map for the coming decades on future research in BC science.
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We show that a higher vertebrate can graze surficial intertidal biofilm, previously only considered a food source for rasping invertebrates and a few specialized fish. Using evidence from video recordings, stomach contents, and stable isotopes, we describe for the first time the grazing behavior of Western Sandpipers (Calidris mauri) and estimate that biofilm accounts for 45-59% of their total diet or 50% of their daily energy budget. Our finding of shorebirds as herbivores extends the trophic range of shorebirds to primary consumers and potential competitors with grazing invertebrates. Also, given individual grazing rates estimated at seven times body mass per day and flock sizes into the tens of thousands, biofilm-feeding shorebirds could have major impacts on sediment dynamics. We stress the importance of the physical and biological processes maintaining biofilm to shorebird and intertidal conservation.
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Ração Animal , Biofilmes , Charadriiformes/fisiologia , Ecossistema , Fenômenos Fisiológicos da Nutrição Animal , Animais , Charadriiformes/crescimento & desenvolvimento , Conservação dos Recursos Naturais , Comportamento Alimentar , Cadeia Alimentar , Densidade Demográfica , Dinâmica Populacional , Gravação em VídeoRESUMO
Estuarine and shallow coastal systems (ESCS) are recognized as not only significant organic carbon reservoirs but also emitters of CO2 to the atmosphere through air-sea CO2 gas exchange, thus posing a dilemma on ESCS's role in climate change mitigation measures. However, some studies have shown that coastal waters take up atmospheric CO2 (Catm), although the magnitude and determinants remain unclear. We argue that the phenomenon of net uptake of Catm by ESCS is not unusual under a given set of terrestrial inputs and geophysical conditions. We assessed the key properties of systems that show the net Catm uptake and found that they are often characteristic of human-dominated systems: (1) input of high terrestrial nutrients, (2) input of treated wastewater in which labile carbon is highly removed, and (3) presence of hypoxia. We propose that human-dominated ESCS are worthy of investigation as a contributor to climate change mitigation.
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Carbono , Mudança Climática , Estuários , Água do Mar , Agricultura , Dióxido de Carbono , Atividades Humanas , Eliminação de Resíduos LíquidosRESUMO
Many shorebird species undertake long-distance migrations punctuated by brief stays at food-rich, estuarine stopover locations. Understanding use of these food resources helps guide conservation and responsible development decisions. We determined the extent and degree to which Western Sandpiper (Calidris mauri) utilized biofilm as a food resource across a large and variable stopover location during northward (spring) migration. We investigated the spatial heterogeneity in diet composition, to determine whether shorebirds were consistently feeding on biofilm or whether diet varied between naturally and anthropogenically delineated sites. We used stable isotope analysis to estimate that biofilm conservatively comprised 22% to 53% of Western Sandpiper droppings across all sampling sites and that prey composition differed significantly between areas within the stopover location. Widespread biofilm consumption demonstrates the importance of biofilm as a dietary component. Variable diet composition suggests that habitat heterogeneity may be an important component of high quality stopover locations in the context of "state-dependant trade-offs" of Western Sandpiper population sub-groups. Future management decisions must consider and address potential impacts on the biofilm community throughout a stopover location, as single site studies of diet composition may not be adequate to develop effective management strategies for entire stopover sites.
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Ração Animal , Biofilmes , Charadriiformes/fisiologia , Migração Animal , Animais , Isótopos de Carbono/química , Ecossistema , Comportamento Alimentar , Isótopos de Nitrogênio/química , Estações do AnoRESUMO
The response of bivalves to their abiotic environment has been widely studied in relation to hydroenvironmental conditions, sediment types and sediment grain sizes. However, the possible role of varying geoenvironmental conditions in their habitats remains poorly understood. Here, we show that the hardness of the surficial intertidal sediments varies by a factor of 20-50 due to suction development and suction-induced void state changes in the essentially saturated states of intertidal flats and beaches. We investigated the response of two species of bivalves, Ruditapes philippinarum and Donax semigranosus, in the laboratory by simulating such prevailing geoenvironmental conditions in the field. The experimental results demonstrate that the bivalve responses depended strongly on the varying geoenvironmental conditions. Notably, both bivalves consistently shifted their burrowing modes, reducing the burrowing angle and burial depth, in response to increasing hardness, to compensate for the excessive energy required for burrowing, as explained by a proposed conceptual model. This burrowing mode adjustment was accompanied by two burrowing criteria below or above which the bivalves accomplished vertical burrowing or failed to burrow, respectively. The suitable and fatal conditions differed markedly with species and shell lengths. The acute sensitivities of the observed bivalve responses to geoenvironmental changes revealed two distinctive mechanisms accounting for the adult-juvenile spatial distributions of Ruditapes philippinarum and the behavioral adaptation to a rapidly changing geoenvironment of Donax semigranosus. The present results may provide a rational basis by which to understand the ensuing, and to predict future, bivalve responses to geoenvironmental changes in intertidal zones.