Trophic Ecology of the American Eel, Anguilla rostrata, in Tidally Restricted and Unrestricted New England Salt Marshes
Historically the American eel, Anguilla rostrata, was abundant in the Gulf of Maine (Goode 2006) and served as an important source of income and sustenance throughout northern New England and Canada (Bolster 2002, SRSF 2002). However, A. rostrata is currently in decline over the entirety of its range (Haro et al. 2000). Potential causes include the introduction of a non-native nematode parasite (Barse and Secor 1999), dioxin-like contaminants (Palstra et al. 2006), overfishing and habitat loss (Haro et al. 2000).
Larval A. rostrata are distributed by ocean currents from its breeding grounds in the Sargasso Sea throughout the western Atlantic, Gulf of Maine and Caribbean Sea (Tesch 2003). Upon reaching coastal waters, A. rostrata can remain in inshore habitats for up to 40 years in the juvenile “yellow” life stage (Jessop 1987; Tesch 2003) before making the seaward spawning migration. The conventional understanding of eelinshore habitat use has been obligate catadromy (e.g., residency in freshwater before migrating to spawn in saltwater); in fact, A. rostrata’s reliance on freshwater habitats is so well accepted that its common name is the “freshwater eel.” However, recent research examining the life history of eels has supported alternative hypotheses where brackish and marine habitats are emerging as more important in eel life history than originally thought. Through microchemical analysis of otoliths, Tsukamoto et al. (1998) found a high degree of residency in eel habitat use of both fresh and marine/brackish environments. Subsequent research has observed use of exclusively brackish and marine habitats, providing further evidence of facultative, rather than obligate catadromy in eels (Tsukamoto and Arai 2001; Jessop et al. 2002; Tsukamoto et al. 2002; Jessop et al. 2004). Based on the abundance of food as well as evidence for faster growth in estuarine habitats (Oliveira 1999), Tsukamoto et al. (1998) and Tsukamoto and Arai (2001) concluded that eels from estuarine habitats might provide the greatest contribution to coastal productivity and eel recruitment. Accordingly, due to the emerging evidence for greater reliance on estuaries, there is a need for greater understanding of eel estuarine habitat use.
Within estuaries, eels are frequently captured in salt marsh habitats (Ford and Mercer 1979; Lafaille et al. 2000; Eberhardt 2004; Selgado et al. 2004; Kimball and Able 2007) and in some systems comprise the majority of fish biomass (Dionne et al. 1999). Despite the presence of eels in salt marshes, little is known about eel use of these habitats. Particularly in light of the potential for the yellow life stage to remain resident in estuarine habitats such as salt marshes for many years (Jessop 1987; Tsukamoto and Arai 2001), a need exists for greater understanding of eel use of salt marshes in terms of movements and trophic support.
Coastal habitats such as salt marshes are particularly vulnerable to habitat impacts due to high rates of coastal development and use of salt marshes as transportation corridors. Structures such as culverts are frequently installed to allow the tide to continue underneath roads and highways where they intersect salt marsh creeks. Historically, engineers designed these structures to allow water to drain under the road and little consideration was given to factors such as fish passage or support of the upstream ecosystem. As a result, many culverts do not accommodate the full tidal regime, resulting in a tidally restricted system upstream. In hydrologically restricted salt marshes, replacement of halophytic vegetation by invasive species (Roman et al. 1984; Burdick et al. 1997) as well as changes to the infaunal communities (Fell et al. 1991) can shift the food base of restricted salt marshes resulting in an altered food web. Furthermore, decreased flooding in hydrologically restricted marshes can limit fish access to food resources (Weisberg and Lotrich 1982). Decreased eel movement and use of hydrologically restricted salt marshes may result in some marsh areas or habitats contributing disproportionately to fish populations (Gillanders 2005). Our previous research investigating fish use of salt marshes further suggests that tidally restricted salt marshes do not provide the equivalent trophic support for fish as unrestricted marshes; however, this was not explicitly tested. The requested funding will support efforts to directly examine the question of functional equivalency in salt marsh trophic support of A. rostrata.
The proposed project addresses multiple strategic goals of N.H. Sea Grant. Results will inform resource managers on the value of salt marsh habitats for the American eel, a declining fish resource. Understanding eel use of salt marshes as a foraging resource will aid in the development of effective strategies for eel conservation and management (N.H. Sea Grant theme area: Conservation and sustainable utilization of fisheries resource - goal 1). Comparison of salt marsh trophic structure between tidally restricted and unrestricted systems will provide valuable information to characterize the current health of salt marsh ecosystems, identify restoration needs and help guide regional decision-making of how best to manage them to maintain ecological functions (theme area: Coastal ecosystem and public health - goals 3 and 4). In addition, the proposed project will also support the N.H. Sea Grant goal of providing training in marine sciences to undergraduate students by supporting an hourly worker to assist in fieldwork and laboratory analyses (theme area: Marine and aquatic literacy - goal B1).
The data collected from the proposed research will serve to improve a full proposal to be submitted to the National Oceanic and Atmospheric Administration (NOAA) for expanded research on A. rostrata habitat use within salt marshes. Future research will examine eel residency in salt marshes over both short and long temporal scales, as well as eel movements within salt marsh habitats.
1. To understand A. rostrata use of salt marsh habitats as a food source and the role of A. rostrata in salt marsh food webs.
2. To evaluate the functional equivalency of hydrologically restricted and unrestricted salt marshes in the trophic support of higher trophic levels, such as A. rostrata.
To evaluate the foraging ecology of Anguilla rostrata, estuaries containing extensive marsh complexes were selected: the Hampton-Seabrook Estuary, New Hampshire; the Parker River Estuary, Massachusetts; and the Webhannet Estuary, Maine. Within each marsh, one hydrologically restricted and one reference creek will be sampled for a total of six creeks (n=3 for each hydrology treatment). Creeks will be selected with similar characteristics such as size, salinity and availability of intertidal and subtidal habitats.
Stable isotope analysis
Analysis of stable isotope values can provide valuable information about the role of organisms in the trophic spectrum. Specifically, stable isotope analysis can be used to identify the relative contribution of organic matter sources to an organism’s diet (Haines and Montague 1979; Peterson et al. 1985; DeNiro and Epstein 1978), and the trophic level at which an organism feeds (Minagawa and Wada 1984; Griffin and Valiela 2001; Post 2002). For collection of samples for stable isotope analysis, each creek will be divided into three regions – upper, middle and lower – to examine foraging patterns over the longitudinal axis of the marsh. Tissue from 5 eels will be sampled and processed for carbon and nitrogen stable isotope analysis (15 fish total per creek). Nekton species constituting potential prey, including Fundulus heteroclitus, Paelaemonetes pugio, and others will also be collected from each creek and processed. Captured nekton will be anesthetized, sacrificed and frozen according to a protocol approved by the Institutional Animal Care and Use Committee (protocol #070702). Benthic cores will be collected at each site to determine A. rostrata use of invertebrate food sources. To determine the relative contribution of primary production to A. rostrata diet, leaves from 5 plants of each vascular species and 5 thalla of each algal species will be collected from each site in spring and fall due to the potential for seasonal changes in isotopic composition (Peterson et al. 1986). Benthic microalgae will be collected on a 210 μm mesh screen set on the vegetated marsh at ebb tide. After several hours, the screen will be removed and brought to the laboratory where samples will be filtered onto precombusted glass fiber filters (GF/F) using a vacuum pump filtration system. Particulate organic matter will be collected by pre-filtering creek water through a 100 µm mesh to remove macrodetritus and zooplankton, and then filtering a known quantity of the sample through a 47 mm GF/F until the filter clogs. All samples will be dried to a constant weight and weighed to the nearest microgram into a tin capsule. Tin capsules will be loaded into a stable isotope ratio mass spectrometer connected to an elemental analyzer for analysis of carbon and nitrogen isotope values.
Gut content analysis
A. rostrata gut contents will be analyzed to determine instantaneous use of salt marshes for foraging. Gut contents from all collected eels will be examined with a dissecting microscope and identified to major taxon. To identify the contribution of each food type to the diet, the relative volume of each food type will be estimated for each gut and assigned to one of the following categories: abundant (>50% of the total gut content), common (10-50% of the total gut content) and present (<10% of the total gut content; Hyslop 1980, Allen et al. 1994).
Mixing models will be developed from stable isotope data with Isosource software (Phillips and Gregg 2003) to understand the relative contributions of food items to A. rostrata diets. Differences in A. rostrata diet between hydrologic treatments (restricted, unrestricted) and creek regions (upper, middle, lower) will be compared using a two-way analysis of variance (hydrologic status, region, and the interaction) with site as a blocking factor to evaluate variability between estuaries. Effects of the hydrologic treatment on gut contents of fish will be evaluated using an analysis of similarity with PRIMER statistical software (PRIMER-E 2002). Analysis of trophic structure will include measures of trophic structure size, diversity, and redundancy according to the methods of Layman et al. (2007).
A. rostrata will rely primarily on salt marsh derived primary production; however, stable isotope values and gut contents will reveal spatial variation in A. rostrata diets within creeks. The greatest reliance on salt marsh derived primary and secondary production will occur in the mid regions of creeks; phytoplankton and salt marsh production will comprise diets from lower regions. Eels collected from upstream regions of unrestricted creeks will utilize a mix of salt marsh and terrestrial/freshwater production, while eels collected upstream of tidal restrictions will rely on exclusively freshwater and terrestrial derived production due to colonization by terrestrial and invasive wetland species.
A. rostrata is an opportunistic predator; therefore, it is expected that eels will occupy upper tropic levels throughout all regions with the exception of upstream regions in tidally restricted sites. Due to the reduced tidal regime and species composition upstream of tidal restrictions (Roman et al. 1984; Fell et al. 1991; Burdick et al. 1999), it is anticipated that the trophic level at which A. rostrata feeds will be lower and the overall trophic structure will be compromised.
Results will be synthesized into an expanded proposal to further examine eel use of salt marsh habitats in terms of large (otolith microchemistry) and small-scale (telemetry) movements. The proposal will be submitted in response to the NOAA Broad Agency Announcement.
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