Variability in the fractionation of stable isotopes during degradation of two intertidal red algae
Introduction
At temperate and high latitudes, extensive beds of kelps have productivities comparable to the most productive terrestrial ecosystems (Barnes and Hughes, 1982). Despite this, there are very few grazing species that utilize this material directly and consequently the primary production of kelps vastly exceeds herbivorous consumption (Newell and Lucas, 1981) and most enters the detrital food chain (e.g. Newell and Lucas, 1981, Mann, 1988, Duggins et al., 1989, Kaehler et al., 2000, Kaehler et al., 2006, Fredriksen, 2003). On the west coast of South Africa for example, the kelps Ecklonia maxima and Laminaria pallida account for upwards of 65% of the detritus found in intertidal suspended particulate matter or SPM (Bustamante and Branch, 1996). In the same fashion, primary production by salt marsh plants (e.g. Spartina alterniflora) can be very high, with only a small percent of the above-ground vegetation being consumed by grazers (e.g. Hackney and De La Cruz, 1980, Valiela et al., 1985, Benner et al., 1987, Buth, 1987, Currin et al., 1995). The rest degrades and enters the detrital food web and many studies have underlined the importance of detrital material to salt marsh and estuarine ecosystems (e.g. Haines, 1977, Haines and Montague, 1979, Hughes and Sherr, 1983, Paterson and Whitfield, 1997).
Studies of algal–grazer interactions in the intertidal zone indicate that the biomass and distribution of some macroalgae can be limited by grazers (Williams, 1993). However, many benthic grazers in both marine and freshwater systems also feed on the periphyton of macrophytes, or on epilithic microalgae, including algal sporelings which show much higher turnover rates and contain less refractory material than macrophytes (McQuaid, 1996, Hillebrand et al., 2002). Consequently, as with salt marshes and kelp beds, the bulk of other macroalgal production is likely to enter a detrital food chain (McQuaid and Branch, 1985), so that understanding the process of macroalgal decomposition is central to elucidating food webs in these communities.
In recent years, food web resolution in a number of estuarine and coastal communities has been achieved through stable isotope analysis (e.g. Bustamante and Branch, 1996, Froneman, 2001, Fredriksen, 2003, Carmichael et al., 2004, Hill et al., 2006). However, few of these studies have considered isotopic changes in organic carbon sources (i.e. phytoplankton, macroalgae) due to decomposition. If isotope fractionation occurs during degradation, the isotopic signatures of many detritivores may bear little resemblance to the signatures of living algae. This will complicate the interpretation of trophic relationships where the bulk of primary production is consumed as detritus. The majority of macrophyte detritus is fibrous and nitrogen poor, but microbial colonization during decomposition results in reduced fiber content and increased available nitrogen (Stuart et al., 1981), making the previously refractory detritus digestible for detritivores and filter feeders (Mann, 1988, Levinton et al., 2002). Because of microbial colonization, the δ13C and δ15N values of macroalgal detritus will not necessarily reflect those of the living alga, but rather a combination of signatures from the decomposing alga, plus the various microbial communities colonizing it (Newell and Lucas, 1981, Newell et al., 1982). In addition the alga's signature may be altered by leaching during decomposition (Benner et al., 1991, Asada et al., 2005)
Although a number of studies have addressed the isotopic effects of degradation in aquatic vegetation, the focus has been on angiosperms and the results have often been conflicting. There appears to be little or no change in δ13C or δ15N during decay in the seagrasses Zostera noltii (Machás et al., 2006), Thalassia testudinum and Zostera marina (Zieman et al., 1984, Stephenson et al., 1986, Fenton and Ritz, 1988) or the mangrove Rhizophora mangle (Wooller, 2003). In contrast, Spartina alterniflora showed distinct δ13C depletion during diagenesis in salt marsh sediments (Benner et al., 1987, Benner et al., 1991, Alberts et al., 1988, Fogel et al., 1989) and δ15N depletion has been described in degrading mangroves (Zieman et al., 1984) and in seven species of tropical angiosperms (2–6‰), with no significant accompanying changes in δ13C (Currin et al., 1995, Fellerhoff et al., 2003).
In comparison to angiosperms, little work has been done on shifts in the isotopic ratios of decomposing macroalgae. Fenton and Ritz (1988) reported both small enrichments and depletions in carbon during decomposition and Stephenson et al. (1986) described a lack of change in carbon isotope composition associated with the degradation of kelp and the formation of detritus. As a consequence, the isotopic differences between living macroalgae and their detritus are poorly understood. The south coast of South Africa is too warm to support extensive kelp beds, but maintains a high biomass of intertidal and subtidal algae that appear to contribute large amounts of organic carbon to intertidal food webs (Hill et al., 2006). Although there are beds of Zostera capensis that occur in nearby estuaries, these estuaries are few and small, so that the contribution of angiosperm production to the intertidal zone is thought to be minimal (Taylor and Allanson, 1995). A substantial percentage of intertidal SPM is thus likely to be macroalgal detritus. The aims of this study were, firstly, to conduct a preliminary investigation of isotopic variation of different tissue types within a single plant and secondly to elucidate changes in C:N ratios, δ13C and δ15N signatures during decomposition of two abundant intertidal rhodophytes: Gelidium pristoides and Hypnea spicifera. We hypothesized that (1) in agreement with the work done by Stephenson et al. (1986), δ13C signatures macroalgae would demonstrate very little change during both degradation and the formation of detritus; (2) δ15N signatures would become enriched due to colonizing bacteria preferentially retaining organic nitrogen during biochemical processing (e.g. see Macko and Estep, 1984); and (3) C:N ratios of degrading plants would decrease relative to healthy plants as a result of microbial mineralization during decomposition (Kirstensen, 1994).
Section snippets
Study site
The macroalgae Gelidium pristoides and Hypnea spicifera were chosen for decomposition studies as they are important contributors to macroalgal biomass and primary production on the South African coast and are likely to contribute large amounts of SPM to the intertidal zone. Both G. pristoides and H. spicifera have a polysiphonia-type life history (Carter, 1985, Reis and Yoneshigue-Valentin, 2000), and possess erect fronds borne on creeping rhizomes (De Clerck et al., 2005). Algal samples were
Basic structural differences
No significant differences were found between wet/dry ratios of Gelidium pristoides and Hypnea spicifera (T0.5(18) = −0.20, p = 0.84).
Differences between thallus parts
Patterns of isotopic signatures between different parts of the alga differed between species, but clearly indicated significant differences in δ13C, δ15N and C:N ratios among thallus parts within a single plant. The holdfast of Gelidium pristoides was significantly more depleted in δ13C than both the healthy and senescent fronds (F2, 14 = 16.17, p < 0.0001). The δ
Discussion
Only the C:N ratios in the laboratory experiments conformed to our hypotheses, while δ15N signatures of both macroalgae (field and lab) and SPM (lab only), with one exception, depleted during degradation and all carbon signatures showed isotope changes presumably related to decomposition (Table 1).
Acknowledgements
Many thanks to F. Porri and M. Villet at Rhodes University, for providing statistical help and direction and to J. Lanham, stable light isotope unit, University of Cape Town for completing all isotope analysis. This work is based upon research supported by the South African Research Chairs Initiative of the Department of Science and Technology and National Research Foundation. This help is gratefully acknowledged.
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