Utilization of organic matter by invertebrates along an estuarine gradient in an intermittently open estuary
Graphical abstract
Introduction
Estuaries are often characterised by soft-sediment habitats that receive spatial subsidies, which fuel extensive ecosystem food chains (Canuel et al., 1995, Constable and Fairweather, 1999). These organic matter subsidies can be derived from autochthonous estuarine primary production or subsidised by allochthonous marine or freshwater sources (Deegan and Garritt, 1997, Cook et al., 2004, McLusky and Elliott, 2004, Doi et al., 2005, Doi et al., 2009, Elliott and Whitfield, 2011). Determining the relative importance of different organic matter sources for estuarine consumers can be complicated by several factors. These include the spatial complexity of estuaries, variability of available sources (e.g. seasonal primary producers) and shifts in source dominance caused by exchange of organic matter with adjacent habitats and spatial and temporal variations in water exchange (e.g. tides and flow, Deegan and Garritt, 1997, Kwak and Zedler, 1997). Accordingly, when collecting samples or making observations, previous studies have focussed on longitudinal estuarine gradients such as salinity or distance from estuary mouth, and recorded various degrees of mixing of in situ estuarine production and allochthonous subsidies (Owens, 1985, Canuel et al., 1995, Deegan and Garritt, 1997, Bucci et al., 2007).
Stable isotope analysis (SIA) can be used to quantify the input of primary production (sources) into ecosystems and to gain information about consumer diets and trophic position. Generally, previous studies in permanently open estuaries have found gradual longitudinal enrichment in δ13C signatures from the upper to the lower estuary in particulate organic matter, seston and invertebrate consumers (Thornton and McManus, 1994, Canuel et al., 1995, Deegan and Garritt, 1997, Doi et al., 2005, Bucci et al., 2007, Kanaya et al., 2008). This is caused by increased diet contribution of marine organic matter sources; particularly those derived from macroalgae with enriched δ13C (Smith and Epstein, 1971, Moore and Suthers, 2005). Terrestrial sources, particularly C3 plants with depleted δ13C signatures, contribute more to particulate organic matter and consumer diet towards the estuary head (Park and Epstein, 1960;; O'Leary, 1981). Consequently, gradual downstream enrichment of δ13C signatures suggests changes in the relative importance of allochthonous terrestrial and marine organic matter subsidies along the estuary.
Similar longitudinal trends have been shown for δ15N signatures. Freshwater invertebrates often exhibit depleted δ15N signatures compared to their marine counterparts, reflecting the assimilation of predominantly terrestrial-derived material that has atmospheric nitrogen (δ15N = 0) as a major nitrogen source (Schoeninger and DeNiro, 1984, Owens, 1985). This has also been detected in estuarine suspended organic matter (Mariotti et al., 1984, Owens, 1985). As a result, France (1994) assumed the presence of a linear trend in δ15N along an estuarine gradient and recommended using δ15N signatures as a marker of ecotonal coupling in coastal environments to measure the dietary proportion of food from different environmental sources.
While many studies using stable isotopes have been conducted in permanently open estuaries (Haines, 1977, Haines and Montague, 1979, Rainer, 1982, Peterson et al., 1985, Guest et al., 2004, Doi et al., 2005, Connolly et al., 2005a, Winemiller et al., 2007), information on intermittently open or seasonally-closed systems is scarce (Hirst, 2004, Hastie and Smith, 2006). These systems are typically located in semi-arid areas with high-energy, microtidal coastlines (Perissinotto et al., 2000, Elliott and McLusky, 2002, Moreno et al., 2010). Low river discharge in summer leads to the formation of a temporary sand barrier disconnecting the estuary from the ocean (Fairbridge, 1980, Kench, 1999, Haines et al., 2006). During mouth closure, input from the marine environment is blocked, while due to variable flow, contributions from freshwater are limited as well (Nozais et al., 2001). These circumstances can result in spatial subsidies being added or interrupted rapidly and greatly during the hydrodynamic cycle and it remains to be investigated whether the assimilation of organic matter by estuarine invertebrates is affected.
Furthermore, southeastern Australia experienced a marked reduction in rainfall between 2000 and 2010, which resulted in severe drought and reduced flows in riverine systems (Matthews, 2006, Murphy and Timbal, 2008, Timbal, 2009). Despite heavy rainfall associated with a strong La Niña event during 2010 and 2011, projections of climate change strongly predict a reduction in rainfall across southern Australia in the future (Hughes, 2003). In intermittently open estuaries, reduced freshwater flow might cause greatly altered hydrodynamic patterns (Sherwood, 1988, Teske and Wooldridge, 2001), thereby potentially affecting spatial subsidies and consumer diets.
The primary aim of the present study was to determine dominant organic matter sources for benthic invertebrates along an estuarine gradient in an intermittently open estuary. Also, there is only limited information about trophic interactions for most species (Ponder, 1965, Lucas, 1980, Wells and Threlfall, 1982, Matthews and Fairweather, 2008). The extent to which spatial subsidies influence the diet of different invertebrate feeding types is unknown. A further aim of this study was to investigate which feeding groups were affected most by potential changes in spatial subsidies. Specific objectives were to: (1) interpret carbon and nitrogen SI signatures and diet contributions for invertebrates with a range of feeding modes, and (2) characterise temporal and spatial patterns in δ13C and δ15N of common primary producers and consumers along an estuarine gradient in an intermittently open estuary.
Section snippets
Study area
The Hopkins River estuary is an intermittently open estuary of approx. 10 km length near Warrnambool, on the south-western coast of Victoria, Australia (Fig. 1). The Hopkins River originates at 240 km north at Mount Langi Ghiran, and its catchment comprises 8651 km2. Within 1 km of major tributes, 99% of the area has been cleared for pasture and cultivation (Sherwood, 1988, Matthews, 2000, Nicholson et al., 2008). The estuary occupies a limestone canyon (Sherwood, 1988) with a well-defined
δ13C and δ15N of primary producers and consumers
Two groups of primary producers could be distinguished according to their δ13C signatures (Fig. 3). The first group consisted of emergent primary producers (Emergent PP), including the estuarine fringing grasses, Phragmites australis and Juncus kraussii, and the freshwater floating fern Azolla filiculoides. The second group consisted of submerged primary producers (Submerged PP) including the estuarine seagrass Zostera muelleri, and the two marine phaeophytes, Phyllospora comosa and Macrocystis
Stable isotope signatures and diets of invertebrates
Most invertebrates in the present study, including the crab Amarinus laevis, the gastropods Nassarius sp. and Salinator tecta, and the polychaetes Simplisetia aequisetis and Scoloplos sp., derived their diet from a mix of Submerged and Emergent PP. The scavenging whelk Nassarius sp. displayed very enriched δ15N values, which was expected due to trophic fractionation. Among the deposit feeders, Scoloplos sp. has a comparably enriched δ15N in contrast to the nereid polychaete S. aequisetis and
Conclusion
The present study indicates that carbon and nitrogen stable isotope analysis can be used to gain information about various aspects of trophic ecology in intermittently open estuaries, in particular invertebrate diet composition and organic matter subsidies. In the Hopkins River estuary, analysis of δ15N showed possible anthropogenic input in the upper estuary, which could have been enhanced due to poor flushing during years of reduced flow. More importantly though, invertebrate consumer diet
Acknowledgements
This work was supported by the Holsworth Wildlife Research Fund (RM22042), and an International Postgraduate Research Scholarship (IPRS) and Publication Scholarship, both by Deakin University, Australia. Special thanks go to Lynda Avery for her generous assistance with invertebrate identification, to Dr Alex Rattray for producing maps and to Dr Rebecca Lester for comments on the manuscript. We greatly appreciate the help of Dr Jessica McKenzie, Mini Hogan and Calista Bingham in the field and
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