Tracing New and Old Resources in Estuarine Ecosystems

Post provided by Thomas Larsen, Kim Vane & Ricardo Fernandes

This week, more than 150 events along the US shores will celebrate estuaries and educate the public and policy makers of the many benefits we get from healthy and thriving ecosystems. But why do we need to pay more attention to estuaries?

A woman collecting snails in the Yellow River estuary, China. Estuaries are important habitats for marine gastropods and nurturing grounds for marine fishes. ©Thomas Larsen

Estuaries are important habitats for marine gastropods and nurturing grounds for marine fishes. ©Thomas Larsen

Estuaries are biological hotspots and by far the most productive ecosystems on our planet. The shallow waters where streams and rivers meet the sea often harbour a rich terrestrial and aquatic flora and are home to many animals. They’re important feeding and reproduction areas for a diverse array of wildlife such as birds and fish, which can include both freshwater and marine species. A large portion of the world’s marine fisheries today depend on the ecosystem services of estuaries; it has been estimated that well over half of all marine fishes develop in the protective environment of an estuary. Historically, humans have been attracted to these large expanses of shallow water that could sustain their basic needs. Nowadays, these estuaries also have economic value as recreational and touristic destinations as for example fishing, boating and swimming spots.

However, our understanding of how estuaries function and sustain this amount of biodiversity is limited. As is the case for most ecosystems on our planet, estuaries are under increasing pressure from human activities. Estuaries are subjected to intensive land reclamation and developments like harbours and aquacultural farms. They also receive excessive amounts of of nutrients, soil and organic matter from intensive farms and urban landscapes via small streams and large rivers. These stressors are accentuated by environmental changes such as sea level rise, increasing water temperatures and extreme weather conditions causing droughts and flooding.

Scientists play an important role in promoting sustainable management and development of estuaries by providing insights into their function and vulnerabilities. One of the key questions we ask is how estuarine food webs are affected by human activities. In contrast to the open ocean — where food webs are primarily fuelled by living phytoplankton — estuarine ecosystems also receive organic matter from the land. They are also supported by decomposing material produced within estuarine systems, mostly from falling vegetation such as seagrasses and mangroves. The flux of terrestrial organic carbon is increasing because of industrialized agriculture, urbanization and extreme weather events, and the direct contribution of these carbon sources to estuarine food webs remains a major research question.

Radiocarbon as a Source Tracer

Radiocarbon distribution in the environment. 14C ranges are approximate and illustrate the large dynamic radiocarbon range among different carbon reservoirs. The arrows denote carbon pathways.

Radiocarbon distribution in the environment. 14C ranges are approximate and illustrate the large dynamic radiocarbon range among different carbon reservoirs. The arrows denote carbon pathways.

Our group relies on a variety of tools to track the origins and fate of organic carbon in aquatic systems to understand how food webs function. To track carbon, we primarily rely on isotope ratios to trace source contributions. In the case of carbon, the lighter isotope 12C represents ca. 99% and the heavier 13C ca. 1%. Since the ratio of these two stable isotopes varies slightly among earth’s carbon reservoirs it is possible to use it as a tracer to distinguish between different organic carbon sources in many ecological settings.

In complex estuarine food webs though, a narrow dynamic range and unpredictable shifts in 12C/13C ratios during trophic transfer can make different carbon sources indistinguishable. So ecologists are increasingly relying on the third and least abundant carbon isotope, the radioactive radiocarbon (14C). This isotope has a much greater dynamic range than its stable isotope counterparts (see figure above) and retains a distinctive source signal during trophic transfer. The radioactivity of 14C does not pose a danger to biological life at natural levels because only one part per trillion of the carbon in the biosphere is in the 14C form. Radiocarbon is continually produced in the upper atmosphere via the interaction between energetic neutrons created by cosmic radiation and atmospheric nitrogen. In the atmosphere, 14C combines with oxygen to form 14CO2, which is then fixed by plants and algae. Upon the death or senescence of photosynthetic tissues, carbon exchange with the atmosphere ceases and the 14C concentration of dead organic matter is reduced by half every ca. 5730 years.

Extraction of natural resources, in this case salt mining in Rio Grande do Norte, Brazil, is one of many threats to mangrove ecosystems. © Kim Vane

Extraction of natural resources, in this case salt mining in Rio Grande do Norte, Brazil, is one of many threats to mangrove ecosystems. © Kim Vane

Radiocarbon abundances often differ between riverine and oceanic sources. For example, water brought in from the deep ocean often has a much lower amount of 14C than that of surface waters or the atmosphere. On the other hand, rivers can contribute 14C-depleted carbon sources towards estuaries. This will be the case if the waters include carbonates originating from a drainage basin with sedimentary or volcanic rocks, which are essentially 14C-free. Contributions from particulate organic carbon, which has run off from older or deeper soil layers, will also lower the14C abundance of riverine waters. This is often the case when soils undergo drastic changes caused by heavy erosion or during thawing of permafrost or melting of glaciers. Provided that these different carbon sources are well characterized, 14C can provide a unique insight into carbon pathways in the biosphere. Ecologists can also use 14C to uncover how animals migrate between different habitats, how terrestrial resources may provide important nutritional supplements during low productivity periods, and whether old or new organic matter fuels filter and suspension feeders such as bivalves.

A mangrove creek in an Amazon estuary of Pará, Brazil. The Amazon delta has one of the largest mangrove estuaries in the world and houses a large biodiversity. ©Kim Vane

The Amazon delta has one of the largest mangrove estuaries in the world and houses a large biodiversity. ©Kim Vane

Compared to observational studies and prevailing methods such as bulk stable isotope ratios, 14C can provide much more specific information on, for example, fish migration during different life stages. This was recently demonstrated in a Japanese study analysing otolith growth rings in fish (in Japanese). By analyzing juvenile and adult growth rings, the researchers were able to track lifetime fish migration from deep to surface waters because deep waters typically have lower 14C abundances than surface waters. This approach of reconstructing migration histories can also be applied to various tissues with incremental growth layers such as baleen plates from humpback whales.

For bivalves, ecologists can take advantage of the fact that shell 14C abundances mostly reflect inorganic carbon sources and soft tissues reflect organic metabolic carbon sources. So, significant 14C differences between tissue and shells can either indicate that the bivalves’ food sources were imported from different habitats or originated from old detrital sources. The ability to track carbon fluxes with 14C and identify herbivore- and detritivore-based food chains shows its potential for investigating human impact on estuarine ecosystems.

Integrating Multiple Sources of Information with Bayesian Modelling

As demonstrated in the above examples, there’s a great benefit to including 14C in your toolbox. In our 14C review paper, we demonstrate how Bayesian software designed for advanced dietary modelling can reduce uncertainty in assigning food sources to consumers by integrating information from observational studies, stable isotopes and 14C.

Estimates of dietary contributions from different food sources (littoral invertebrates (LI), chironomidae, calanoid zooplankton (CZ), and Daphnia) to a population of pollans (generated using FRUITS based on data from Keaveney, Reimer and Foy (https://doi:10.2458/azu_rc.57.18354).

Estimates of dietary contributions from different food sources (littoral invertebrates (LI), chironomidae, calanoid zooplankton (CZ), and Daphnia) to a population of pollans (generated using FRUITS based on data from Keaveney, Reimer and Foy).

Since studies on estuarine food webs based on both stable isotope and 14C data are still sparse, we show a proof-of-concept example from a recent lake study using the Bayesian mixing model “Food Reconstruction Using Isotopic Transferred Signals” (FRUITS). In our example, we use isotopic values of pollans (Coregonus pollan), its food sources, and diet-to-consumer isotopic offsets according to Keaveney, Reimer and Foy. As relevant food sources, we included calanoid zooplankton, chironomidae, Daphnia, and littoral invertebrates. Our estimates were highly ambiguous when the mixing model was based on δ13C and δ15N values only (top graph). But by taking into account that littoral invertebrates represent the smallest dietary contribution, the model estimates improved. The ranking among the three remaining food sources, chironomidae, calanoid zooplankton, and Daphnia, remain inconclusive though (central graph).

When we included 14C, the model showed that Daphnia are less important dietary sources than chironomidae or calanoid zooplankton (bottom graph). This example illustrates how inclusion of 14C into stable isotope based mixing models can make the models more precise. We suggest that the performance of such models can be improved even further when combined with compound-specific stable isotope analyses — the information that can be drawn from both approaches is highly complementary.

Outlook

A fisherman netting with the tides for fish in a mangrove estuary of Maranhão, Brazil. In Brazil such artisanal fishing is still the main source of sustenance for a large part of the population living at the coast. © Kim Vane

A fisherman netting with the tides for fish in a mangrove estuary of Maranhão, Brazil. © Kim Vane

Radiocarbon is far from being a standard tool in ecological research despite the fact that studies for more than 40 years have demonstrated its potential as a source tracer. As highlighted in our review paper, several studies have already demonstrated how 14C analysis can help us track what animals eat across a variety of ecosystems. With the advent of semi-automated sample preparation techniques and compact accelerator mass spectrometers, 14C analysis is gradually becoming more affordable. The option of using 14C to characterize estuarine food webs gets even better when combined with other sources of information into Bayesian mixing models. By taking advantage of these analytical possibilities we can improve our understanding of estuarine food web processes. In light of the increasing human pressure on estuaries, we hope such research efforts will help to increase public awareness of how vital estuaries are for aquatic life and ultimately the sustenance for millions of people.

To find out more about using 14C as a source tracer read our Open Access Methods in Ecology and Evolution article ‘Radiocarbon in ecology: Insights and perspectives from aquatic and terrestrial studies’.

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