Microalgae and Mangroves as Carbon Sources for Estuarine Invertebrates: Evidence from Stable Isotope Enrichment Experiments

Abstract

The importance of different sources of carbon (energy) supporting secondary productivity in estuaries and coastal waters is still rather uncertain, despite decades of research on this topic. One of the major uncertainties is the relative importance of carbon from macrophyte detritus and microalgae, particularly diatoms and cyanobacteria within sediments (microphytobenthos, MPB). Existing methods have been unable to determine their relative contributions to consumer nutrition. This thesis addresses some of the limitations of existing methods, and then uses an innovative combination of techniques to determine the relative contributions of detritus and MPB to the nutrition of consumers within a mangrove forest in southeast Queensland, Australia. To ensure wide applicability, techniques were developed for both mud and sand, encompassing the range of sediments encountered in estuaries and protected coastal waters. Stable isotope analysis is commonly used to resolve food web issues. Difficulty extracting MPB from sediment to obtain a pure carbon isotopic signature (δ13C), however, has hampered efforts to determine the importance of MPB as a carbon source for consumers. I showed that compound-specific isotope analysis of phytol, part of the chlorophyll molecule, can be used to estimate MPB δ13C with enough precision for most food web studies: within 1-1.8‰ of actual values (95% CI) at normal levels of replication (n = 5 or 10). Although the majority of phytol in sediments is produced in situ by MPB, part of the phytol pool is derived from detritus (e.g. 33% for mud, 17% for sand in the current study). In some situations, this could lead to errors in estimating MPBδ13C, realistically by about 1‰ (in sand) or 2‰ (in mud), but an adjustment can be made where necessary. Compound-specific isotope analysis of phytol (the phytol method) can therefore be confidently used to estimate MPB δ13C values in estuarine environments. Where δ13C values of detritus and MPB are similar, natural abundance stable isotopes are unable to resolve their contribution to consumer nutrition. Enrichment of producers with the heavy 13C isotope generates distinct δ13C values that can be traced into consumers. Studies aiming to enrich MPB using 13C-enriched sodium bicarbonate have, however, observed simultaneous enrichment of bacteria. This may simply be due to use of MPB-derived carbon by bacteria, but if bacteria acquire the label directly, enrichment of consumers would indicate use of bacteria, rather than MPB, as a primary carbon source. Application of 13C-enriched bicarbonate resulted in enrichment of MPB in both mud and sand and subsequent secondary enrichment of bacteria. Direct bacterial uptake was trivial in comparison to MPB uptake. Any labelling of animals in subsequent enrichment experiments could therefore be attributed to use of MPB as a primary carbon source. I used a combination of the phytol method, stable isotope enrichment, and compartment modelling within a mangrove forest to examine use of detritus and MPB as carbon sources for common consumers; crabs (Australoplax tridentata and Parasesarma erythrodactyla) and foraminifera (Ammonia beccarii and Trochammina inflata). Compartment modelling quantified the extent of use through comparison of producer and consumer enrichment over time. The main carbon source for T. inflata was unable to be established, but all other species acquired virtually all of their carbon locally (within a 1 m radius), from MPB and/or mangrove detritus. The majority of carbon for A. tridentata was derived from MPB (99%), whereas P. erythrodactyla and A. beccarii predominantly utilised mangrove detritus (88 and 84%, respectively). For the latter two species, the remainder of carbon was derived from MPB. The different strategies in carbon utilisation by the crab species indicate feeding selectivity that may be a strategy to avoid interspecific competition for food resources. The high abundance of benthic invertebrates and their rapid assimilation of local carbon sources highlight their potential importance in influencing carbon cycling and productivity in estuaries. Consumption of benthic invertebrates by more mobile, higher consumers may also allow for transport of locally-produced carbon to adjacent waters via trophic relay. The methods demonstrated in this thesis have potential application in resolving food web issues in a variety of habitats. Further application of these techniques at a variety of temporal and spatial scales would help to develop a broader understanding of the importance of macrophyte detritus and MPB, and establish general patterns in utilisation of carbon sources in estuarine systems.