Redefining the trophic importance of seagrasses for fauna in tropical Indo-Pacific meadows

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Abstract

Fauna species living in seagrass meadows depend on different food sources, with seagrasses often being marginally important for higher trophic levels. To determine the food web of a mixed-species tropical seagrass meadow in Sulawesi, Indonesia, we analyzed the stable isotope (δ13C and δ15N) signatures of primary producers, particulate organic matter (POM) and fauna species. In addition invertebrates, both infauna and macrobenthic, and fish densities were examined to identify the important species in the meadow. The aims of this study were to identify the main food sources of fauna species by comparing isotopic signatures of different primary producers and fauna, and to estimate qualitatively the importance of seagrass material in the food web. Phytoplankton and water column POM were the most depleted primary food sources for δ13C (range −23.1 to −19.6‰), but no fauna species depended only on these sources for carbon. Epiphytes and Sargassum sp. had intermediate δ13C values (−14.2 to −11.9‰). Sea urchins, gastropods and certain fish species were the main species assimilating this material. Seagrasses and sedimentary POM had the least depleted values (−11.5 to −5.7‰). Between the five seagrass species significant differences in δ13C were measured. The small species Halophila ovalis and Halodule uninervis were most depleted, the largest species Enhalus acoroides was least depleted, while Thalassia hemprichii and Cymodocea rotundata had intermediate values. Fourteen fauna species, accounting for ∼10% of the total fauna density, were shown to assimilate predominantly (>50%) seagrass material, either directly or indirectly by feeding on seagrass consumers. These species ranged from amphipods up to the benthic top predator Taeniura lymma. Besides these species, about half of the 55 fauna species analyzed had δ13C values higher than the least depleted non-seagrass source, indicating they depended at least partly for their food on seagrass material. This study shows that seagrass material is consumed by a large number of fauna species and is important for a large portion of the food web in tropical seagrass meadows.

Introduction

Stable isotope analyses are widely used for the identification of food sources assimilated, since consumer species have an isotopic signature reflecting their diet (Hobson, 1999, Vander Zanden and Rasmussen, 1999, Smit, 2001). Stable isotopes reflect the assimilation of organic matter into tissue of the consumer and provide an average of the diet over periods of weeks to months (Gearing, 1991). This is in contrast to conventional techniques such as visual sensus and gut content analysis, which only indicate the food items consumed, but do not reflect the actual assimilation by consumers (Gearing, 1991, Polis and Strong, 1996). A prerequisite for using stable isotopes at natural abundance levels as tracers for food sources is that there should be significant differences in δ-values between potential food sources (Vander Zanden and Rasmussen, 1999). In seagrass meadows different groups of producers have distinct δ13C ratios (Smit et al., 2005, Benstead et al., 2006) with seagrasses often the least depleted 13C primary producer (Hemminga and Mateo, 1996, Smit, 2001). Potential food sources for primary consumers are seagrasses, detritus, epiphytes, phytoplankton and benthic micro- and macroalgae (Lepoint et al., 2000, Smit et al., 2005, Smit et al., 2006). In areas without upwelling or river discharge, and low nutrient concentrations in the water column, food webs seem to rely on benthic and epiphytic primary production as the ultimate source of dietary carbon (Moncreiff and Sullivan, 2001, Smit et al., 2006).

Dugong, green turtle and water fowl have historically been identified as seagrass grazers (Heck and Valentine, 2006), but their numbers have largely declined. During the last two decades, most food web analyses in seagrass meadows showed that assimilation of seagrass material was minimal (Fry, 1984, Kitting et al., 1984, Dauby, 1989, Yamamuro, 1999, Lepoint et al., 2000, Moncreiff and Sullivan, 2001, Vizzini et al., 2002, Smit et al., 2005, Smit et al., 2006; but see Kharlamenko et al., 2001). This is in contrast to observations of intake of seagrass by a large number of fauna species (150 reviewed in McRoy and Helfferich, 1980), and grazing experiments which show that grazers can consume large amounts of aboveground seagrass biomass (Heck and Valentine, 2006). Low assimilation and high excretion of seagrass material by fauna species is mostly used to explain this paradigm (Mateo et al., 2006). However, most seagrass food web analyses have been performed in higher latitudes, characterized by lower direct grazing compared to tropical areas (Heck and Valentine, 2006). All year round tropical seagrasses have a high leaf production and fast turnover (Vermaat et al., 1995, Stapel et al., 2001). This combined with a lower fibre concentration compared to temperate seagrasses (Klumpp et al., 1989), indicates tropical seagrasses have a higher palatability for grazers compared to the latter (Cebrián and Duarte, 1998). The palatability of tropical seagrasses is even in the range of macroalgae species (Hay, 1984). Therefore we hypothesize that the contribution of seagrass material to the food web of tropical offshore meadows may be substantial.

This study is one of a few assessing the food web of tropical seagrasses in the Indo-Pacific (cf. Yamamuro, 1999, Benstead et al., 2006), and the first in an offshore mixed-species meadow, using stable isotopes to analyse the importance of fast growing seagrass species in the food web. The aims of this study were (1) to compare isotopic signatures of the seagrass species, other primary producers and particulate organic matter (POM), (2) to identify the main food sources for different fauna species and (3) to estimate qualitatively the importance of seagrass material to the food web in a tropical offshore mixed-species seagrass meadow. We determined fauna densities (fish, epifauna and infauna) in a mixed-species meadow and created a multiple stable-isotope food web of the meadow using δ13C and δ15N signatures of the most important fauna species, primary producers and POM.

Section snippets

Site description

The experiments were carried out in the Spermonde Archipelago, Indonesia. The archipelago (200 km long, 40 km wide) consists of a large group of coral islands and submerged reefs on the continental shelf along the west coast of South Sulawesi (Fig. 1; see Stapel et al., 2001, for details). For the research locations we chose Bone Batang (5°01′00″ S; 119°19′30″ E). This uninhabited island is located ∼15 km off the coast and 30 km from the shelf edge, indicating a low influence of river discharge or

Macrophyte and fauna densities

The seagrass density was about 3000 shoots m−2 (Table 1). The largest part of the seagrass biomass was belowground (rhizomes and roots), while the aboveground (leaf) biomass accounted for 15% of the total. The large species Thalassia hemprichii accounted for about half of the biomass while the tiny Halodule uninervis made up more than half of the shoot density. Epiphytes were most abundant on older Enhalus acoroides leaves, and occurred in low densities on the dominant seagrass species. The

Discussion

The seagrass shoot density and biomass of the studied meadows was comparable with other tropical meadows (Nienhuis et al., 1989, Erftemeijer, 1994, Vermaat et al., 1995). The macro invertebrate densities differed from other meadows in Indonesia, analysed by Nienhuis et al. (1989). Especially the densities of Porifera and Holothuroidae were small in our studied meadow. The latter may be caused by selective fishing by local fishermen for sea cucumbers, which have increased considerably during the

Conclusion

In this food web study we showed that phytoplankton and water column POM were the most depleted primary food sources for δ13C, but no fauna species depended exclusively on these sources for carbon. Epiphytes and Sargassum sp. had intermediate δ13C values and sea urchins, gastropods, and certain fish species were the main species assimilating this material. Seagrasses and sedimentary POM had the least depleted values. Between the five seagrass species significant differences in δ13C were

Acknowledgement

We thank Jelle Eygensteyn for performing the stable isotope analyses, Piet Nienhuis and two anonymous referees for comments on the manuscript, Alfian Noor for administrative arrangements in Indonesia, and Marjolein Pijnappels and Saido for assistance with sampling. This research was funded by NWO-WOTRO grant W86-168, Schure-Beijerinck-Popping fund grant SBP/JK/2005-44 and the Department of Environmental Science, Radboud University Nijmegen.

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