Stable isotopes reveal habitat-related diet shifts in facultative deposit-feeders

Highlights

• We investigated macrofauna diet across an eelgrass bed and bare-sediment habitats.

• In the eelgrass bed trophic position increased.

• More detrital macrophytes composed animals' diet in the vegetated habitat.

• Diet shift may increase spatial dynamics of the food web.

• Adequate management measures should be undertaken to protect this variability.

Abstract

Seagrass patches interspersed in a sediment matrix may vary environmental conditions and affect feeding habits of consumers and food-web structure. This paper investigates diet shifts between bare sediments and a Zostera noltei (Hornemann, 1832) meadow for three facultative deposit-feeding macrofaunal consumers, notably the bivalve Scrobicularia plana (da Costa, 1778), the polychaete Hediste diversicolor (O.T. Müller, 1776), and the gastropod Hydrobia ulvae (Pennant, 1778). In July 2008, one eelgrass meadow and two bare sediment locations were chosen in the Mondego estuary (40° 08″ N, 8° 50′ W, Portugal) and sampled for stable isotope signatures (δ¹³C and δ¹⁵N) of macrofauna consumers and some of their potential basal food sources, such as sedimentary organic matter (SOM), microphytobenthos (MPB), seagrass shoots, leaves and seaweeds laying on the surface sediment. The δ¹⁵N of H. diversicolor was 3‰ higher in the eelgrass meadow than in bare sediment, indicating a change of trophic position, whereas the Bayesian stable-isotope mixing model showed that S. plana assimilated more macroalgal detritus than microphytobenthos in the eelgrass bed. Such habitat-related diet shifts have the potential to change structure and spatial dynamics of benthic food webs.

Introduction

Seagrass meadows occupy large portions of coastal areas, where they play fundamental ecological roles as habitat-forming ecosystem engineers and provide shelter and food to many species of consumers (Duarte, 2002, Larkum et al., 2006). In a marine landscape, seagrass meadows often appear as vegetated patches interspersed in a matrix of bare sediment (Boström et al., 2006). As compared to bare sediments, seagrasses change nutritional conditions for intermediate consumers and predators (Peterson et al., 2004). They, for instance, provide a large variety of food for benthic consumers. Seagrass species can supply food to herbivores, not only because they represent a food source themselves (Heck and Valentine, 2006) but also because they support communities of other primary producers such as epiphytes and epibenthic or other microalgae in the sediment (Moncreiff and Sullivan, 2001). Moreover, the portion of seagrass biomass not consumed by herbivores can subsidize the detrital food web within seagrass meadows or within adjacent habitats, where seagrass detritus can be imported by waves and tides (Cebrian, 1999, Connolly et al., 2005, Heck et al., 2008). Within the seagrass meadow, the detrital food web is also subsidised with external sources of detritus because the projection of physical structures in the form of seagrass leaves into the water column reduces water flow near the seafloor, thereby enhancing deposition of fine particles of organic matter and entrapping drifting macroalgae (Bell et al., 1995, Peterson et al., 2004).

Several macrofauna invertebrates are relatively sedentary benthic consumers whose feeding behaviour includes facultative deposit- and suspension -feeding or grazing (Fauchald and Jumars, 1979, Levinton, 1991, Lopez and Levinton, 1987). These consumers can variably obtain their food from different primary producers and detritus and vary their feeding behaviour following food quantity and nutritional quality, unless they have physiological constraints such as those related to their size or their individual development (Bock and Miller, 1997, Galván et al., 2011, Hentschel, 1998, Riera, 2010, Rossi et al., 2004, Taghon and Greene, 1992). Consequently, their diet could change among seagrass patches and bare sediment habitats, following the differential availability of food derived from local sources or subsidised by other habitats.

Knowledge on how these consumers get their food following the spatial heterogeneity of the marine landscape is important to understand food web dynamics and how the energy and nutrients are transported through the coastal food webs because macrofauna consumers represent the link between basal sources and top predators and contribute significantly to the energy transfer through the coastal food webs (Herman et al., 1999). This knowledge may allow managers to better define habitat protection measures in order to safeguard not only mapped habitat units but also the overall trophic structure of the area (Törnroos et al., 2013).

Stable isotope analysis (δ¹³C and the δ¹⁵N) are commonly used for identifying the diet of macrofauna, determining food web structures (e.g. Baeta et al., 2009, Carlier et al., 2009, Fry, 2008, Lebreton et al., 2011, Page and Lastra, 2003, Post, 2002, Riera, 2010, Riera and Richard, 1996, Vafeiadou et al., 2013b) and, sometimes, the extent of carbon movement by resident fauna across marine and estuarine habitats (Connolly et al., 2005, Törnroos et al., 2013). The relatively few studies that have confronted isotopic values of consumers among habitats have, sometimes, found differences across habitats, suggesting limited movement of organic material by resident macrofauna (Guest et al., 2004). Other studies have, however, measured variability over small spatial scales, within, rather than among habitats, as well as no differences across habitats, probably because basal sources such as particulate organic matter are moved across habitats by hydrodynamics (Connolly et al., 2005, Guest et al., 2004).

This study aims at understanding how the diet of macrofauna facultative deposit-feeding consumers changes between bare sediment and seagrass habitats. By comparing the isotope signatures of the three most abundant consumers in a Zostera noltei (Hornemann, 1832) bed and in nearby bare sediments, we tested the hypothesis that there would be differences in the δ¹³C and the δ¹⁵N of consumers inhabiting the Z. noltei meadow and those in bare sediments. Changes in the stable isotope signatures of a consumer may be not only due to a shift in diet but also to a shift in the signal of the same food source. We, therefore, tested whether there were differences among locations in the basal food sources and estimated the contribution of these sources to consumers' diet, based on stable isotope signatures. Eventually, since we expected that a shift in diet would depend to the availability of food sources, we evaluated differences in the quality and quantity of basal food sources, by measuring the concentrations of organic carbon and nitrogen, detrital primary producers and microalgae in the sediment.