Biogeochemical and Hydrologic Controls on Food Web Structure in the Everglades
Carol Kendall , Bryan E. Bemis, and Scott D. Wankel
U. S. Geological Survey, Menlo Park, CA
Ted Lange
Florida Fish and Wildlife Conservation Commission, Eustis, FL
David P. Krabbenhoft
U. S. Geological Survey, Middleton, WI
A clear understanding of the aquatic food web -- the relative trophic positions of different fish, birds, and other aquatic life -- is essential for determining the entry points and subsequent biomagnification pathways of contaminants such as methyl-mercury (MeHg) in the Everglades. Anthropogenic changes in nutrients and sulfur can significantly affect the entry points of MeHg by changing food web structure from one dominated by algal productivity to one dominated by macrophytes and associated microbial activity. These changes in the base of the food web also influence the distribution of animals within the ecosystem, and subsequently the bioaccumulation of MeHg up the food chain. We are attempting to use the δ
15 N, δ 13 C, and δ 34
S of biota in marshes and canals in the
Everglades as (1) indicators of local environmental conditions that may impact water quality and biota, and (2) indicators of food web structure.
The isotopic compositions of several thousand sediment, plant, invertebrate, and fish samples collected in collaboration with several agencies from several hundred sites in the
Everglades show strong spatial patterns on a landscape scale. The spatial variability of
δ 15 N, δ 13 C, and δ 34
S values reflects spatial variability of reducing conditions in the marshes that promote methane production, sulfate reduction and denitrification. The isotopic compositions of aquatic plants integrate the variability in water column isotopic compositions, and the resulting spatial patterns are incorporated throughout the food web.
Therefore, organisms that live in sites where geochemical conditions are dominated by particular redox reactions have distinctive isotopic compositions. The temporal and spatial variability in the isotopic compositions of aquatic plants at the base of the food webs complicates the use of isotopic techniques for determining food web structure in the
Everglades. In particular, the isotopic effect of these biogeochemical reactions must be removed from the isotopic compositions of biota before it is possible to evaluate temporal and spatial changes in food webs.
The temporal and spatial variability of biota isotopic compositions provide very useful insight into seasonal and spatial changes in biogeochemical and hydrological processes across the Everglades. For example, aquatic vegetation and detritus samples collected in
September 1998 and March 1999 from various sites along two parallel transects in WCA
2A show that
 15
N values of vegetation tend to decrease (from around +5‰ to around
0‰) with distance from the canal, while  13
C values show an increase with distance from the canal (from –30‰ to –26‰). Shrimp and other invertebrate samples collected at the same times also show a ~2‰ decrease in  15
N and ~5‰ increase in
 13
C along the same

gradient. Also, we find that plants and macro-invertebrates collected from microhabitats
(such as open-water sloughs, cattail marsh, sawgrass marsh and spikerush stands) within
100 m of site U3 in WCA2A have 0.5 to 1‰ variation in
 13 C and a 1 to 2‰ variation in
 15
N between marsh types. The differences in isotopic composition of biota within microhabitats at each site suggest that local influences, such as differences in the relative rates of photosynthesis and respiration, and differences in nitrification and denitrification, strongly affect the
 13
C and
 15
N (respectively) of local biota. Temporal changes in these same processes, as well as changes in species composition, cause algae samples collected weekly from 3 slightly different microhabitats near U3, to have
 13
C values that range from –32‰ to –27‰, and
 15
N values that range from +2‰ to +6‰ during the fall of
1997.
The

values of organisms collected at the same site usually show an inverse relation between
 13
C and
 15
N over time. Seasonal shifts in water level can cause shifts in biogeochemical reactions and nutrient levels, with corresponding variations in the
 values of biota. For example, small changes in water level may change the balance of photosynthesis, respiration, and atmospheric exchange reactions that control the
 13 C of dissolved inorganic C (DIC). Such changes will probably also affect the
 15 N of dissolved inorganic N (DIN) because of corresponding changes in N uptake and redox conditions. During the dry season, the marshes probably become more anoxic because of shallower water levels, less photosynthesis, and increased quantities of decaying vegetation. At some sites, the
 13
C and
 15
N of algae show strong positive correlations with water level fluctuations. These oscillations are substantially damped up the food chain, probably because of the longer C and N integration times of animals vs. plants.
Our large dataset of
 13
C and
 15
N analyses of samples collected at 15 sites studied by the
USGS ACME (Aquatic Cycling of Mercury in the Environment) team during multiple trips in 1995-1999 was used to calculate the differences in
 15
N and
 13
C between all possible consumer-diet pairs. The difference in
 15
N between consumer and diet (
 15
N) is a proxy for the length of the food chain between the species at a particular site and date, and the difference in
 13 C (
 13 C) reflects differences in the base of the food webs of the species. An evaluation was then made of how often the
 15 N and
 13 C values differed between types of sites. There were no statistically significant differences in
 15
N values between high and low nutrient sites, suggesting that there was no evidence for shorter food chains at high nutrient sites. However, there are statistically significant differences in
 13
C values between low and high nutrient sites.
We find that
 13
C values provide a powerful tool for distinguishing between sites where algae is the dominant base of the food web vs. sites where macrophyte debris (and the bacteria living on it) is also a significant food source. The
 13 C values of organisms from relatively pristine marsh sites sampled by the USGS are consistent with algae being the dominant food web base most of the time (perhaps depending on water levels). At the more nutrient-impacted sites, the
 13
C and
 15
N values of scavengers such as shrimp and crayfish are consistent with macrophyte debris being an important food source most of the time. The
 13
C values of samples collected by the EPA REMAP program in

September 1996 also show spatial differences in the importance of algae as a base of the food web. Macrophyte debris appears to also be important to the mosquitofish food web at about half of these sites.
The
 15
N calculated for periphyton and mosquitofish pairs at the REMAP sites showed no correlation with region or latitude, and no significant correlation with mosquitofish Hg levels, suggesting a lack of evidence for spatial differences in food chain length.
However, the
 13
C values showed strong spatial patterns, including statistically significant differences between data from different regions (p = 0.04) and latitudes (p <
0.01). One likely explanation for the patterns is that they reflect spatial differences in the relative importance of algae vs. macrophyte debris to the mosquitofish food web. In general, the spatial patterns of
 13
C values are very similar to spatial patterns interpreted by Stober et al. (2001) as differences in food web structure. Hence, two very different sets of samples and data from the same regional assessment agree that there are similar spatial differences in some aspect of the food web structure, but disagree about whether this difference is mostly due to trophic variations or food base differences.
Several chemical parameters measured at the sites by the REMAP program show significant differences between sites where the food webs are predominantly algal versus ones with appreciable contributions from macrophyte debris. These data are consistent with macrophyte-impacted sites generally having more anoxic conditions than sites where algae is the dominant base of the food web. The general agreement of the REMAP data with the conceptual model developed to explain temporal and spatial variability in food webs at USGS sites provides moderate evidence that spatial differences in the dominant food web base across the Everglades are related to environmental conditions such as nutrient availability, redox conditions, and hydroperiod.
Applications of our isotopic investigations to the Everglades Restoration include: (1)
Biota isotopes provide a map of the current spatial distributions of the extent of several biogeochemical reactions (especially sulfate reduction) affecting nutrient and Hg uptake.
(2) By comparing the spatial patterns in the biota with those in the shallow sediments, recent anthropogenic changes in biogeochemical processes at the landscape scale can be demonstrated and dated. (3) Isotopes provide detailed information about temporal and spatial changes in trophic relations that complements traditional gut-contents analyses used by the FFWCC (and others) for understanding food webs and the bioaccumulation of contaminants. (4) The preliminary synthesis of the biota isotopes at USGS and 1996
REMAP sites provides a mechanism for extrapolating the detailed food webs developed at the intensive USGS sites to the entire marsh system sampled by REMAP. (5) Biota isotopes provide a simple means for monitoring how future ecosystem changes affect the role of periphyton (vs. macrophyte-dominated detritus) in the mosquitofish food chain, and for predictive models for MeHg bioaccumulation under different proposed landmanagement changes.
Carol, Kendall, U.S. Geological Survey, 345 Middlefield Road, MS 434, Menlo Park,
CA, 94025, Phone: 650-329-4576, Fax: 650-329-5590, ckendall@usgs.gov,