Influence from Hydrological Modification on Energyand Nutrient Transference in a Deltaic Food Web

Margene E. Goecker & John F. Valentine &

Susan A. Sklenar & Glenn I. Chaplin

Received: 28 March 2008 /Revised: 23 September 2008 /Accepted: 30 September 2008 /Published online: 23 October 2008# Coastal and Estuarine Research Federation 2008

Abstract Alterations of hydrology are known to triggerchanges in coastal ecosystems, such as the composition andabundances of local flora and fauna. It is less well knownhow these alterations lead to changes in nutrient and energytransfers in these systems. We used comparisons of stableisotope signatures (δ13C, δ15N, and δ34S) in the tissues ofconspecific plants and animals collected on each side of theMobile Bay Causeway to determine the extent to which thecauseway may have altered energy and nutrient exchangebetween the Mobile–Tensaw Delta and upper Mobile Bay.While the δ13C signatures of most plants and animals variedirrespective of their location relative with causewaylocation, their δ15N and δ34S signatures were almost alwaysmore enriched south of the causeway, indicating significantalterations of trophic linkages within this estuarine foodweb. Dual isotope plots and mixing model analysesindicated that while terrestrial and floating plants weretrophically important to consumers north of the causeway,submerged aquatic vegetation was more important to

consumers south of the causeway. Although limited inspatial and temporal scale, our results preliminarily showthat there are noteworthy differences in stable isotopesignatures most likely due to the Mobile Bay Causewayaltering energy and nutrient transference.

Keywords Carbon . Estuary . Nitrogen . Sulfur .Mixingmodels .Mobile–Tensaw delta . Stable isotopes

Introduction

The transfer of production and nutrients across theboundaries of different ecosystems is thought to definefood web interactions in natural coastal settings. In manycases, these transfers support much greater levels ofproduction of higher-order consumers in receiving habitatsthan would otherwise be possible if such exchanges did notoccur (Kline et al. 1989; MacAvoy et al. 2001).

Deltas are unique areas found at the interface of threedramatically different ecosystems—freshwater, marine, andterrestrial ecosystems. Seasonal inputs of terrestrial andfreshwater production are thought to be responsible for theextraordinary production of lower trophic levels in deltaicfood webs (Borom 1979; Beshears 1982; Gosselink 1984;Day et al. 1989; Lehrter et al. 1999). These food webs arealso characterized by diverse assemblages of seasonallyabundant, estuarine-dependent consumers and appear to besites of exchanges of production and nutrients acrossecosystems.

Most deltas occur in close proximity to large urbancenters where hydrological modifications are commonlyused to either reduce the incidence of flooding in low-lyingareas or to provide transportation corridors among coastalcommunities. While the composition of estuarine commu-nities has been shown to be impacted by the placement ofsuch structures (Fahy et al. 1975; McAlice and Jaeger 1983;

Estuaries and Coasts (2009) 32:173–187DOI 10.1007/s12237-008-9105-0

M. E. Goecker (*)Government of South Australia, Eyre Peninsula NaturalResources Management Board,GPO Box 2916, Port Lincoln, SA 5606, Australiae-mail: meg.goecker@epnrm.com.au

J. F. Valentine : S. A. SklenarDauphin Island Sea Lab,101 Bienville Boulevard,Dauphin Island, AL 36528, USA

J. F. ValentineDepartment of Marine Science, University of South Alabama,Mobile, AL 36688, USA

G. I. ChaplinAuburn University,Auburn Marine Extension and Research Center,4170 Commander’s Drive,Mobile, AL 36615, USA

Wood et al. 1997), the impacts of hydrological modifica-tions on nutrient and energy transfer within deltaic foodwebs remain poorly understood. Nevertheless, it is reason-able to assume that hydrological modifications are likely toalter the strength of trophic transfer among coastalecosystems.

The Mobile–Tensaw Delta (hereafter referred to as theMTD) is the second largest river delta in the USA (Wallace1994) and sits at the base of the nation’s sixth largestwatershed in terms of areal coverage. Approximately 15%of the nation’s freshwater flows through the MTD’sestimated 100,000 ha of wetlands (Baya et al. 1998;USACOE 2001) of which over 60,000 hectares are forested

wetlands (Alabama Dept. Con. & Nat. Res., unpublisheddata). An earthen causeway constructed in 1926–1927,links the eastern and western shores of Mobile Bay and isperceived to have reduced the frequency and intensity ofestuarine water intrusion into a number of now semi-enclosed embayments in the MTD (USACoE 2001; Fig. 1).In addition, the causeway may have also enhanced thedepositional rates of embayments to the north, thussequestering greater quantities of production and nutrientsfrom the surrounding terrestrial environment for consumersto feed on than would otherwise have been the case if thecauseway had not have been constructed (Valentine et al.2004; Valentine and Sklenar 2006). Presently, the only

Fig. 1 Map of Mobile–TensawDelta. Number 1 and 2 identifysampling sites north and southof the causeway, respectively

174 Estuaries and Coasts (2009) 32:173–187

significant water exchange between the lower MTD (e.g.,Chocolatta Bay) and Mobile Bay occurs at four 400-mwide, artificial “spillways.”

To determine the extent to which this causeway mayhave altered production and nutrient exchange between theMobile–Tensaw Delta and the upper Mobile Bay, samplesof the local flora and fauna were collected from sites justabove (north) and below (south) the causeway for compar-ative stable isotope analyses (δ15N, δ13C, and δ34S). Thisapproach has previously been used to evaluate the strengthof cross habitat energy and nutrient exchanges in similarestuaries (e.g., Peterson et al. 1985; Peterson and Howarth1987; Sullivan and Moncreiff 1990; Deegan and Garritt1997; Kwak and Zedler 1997; Coffin and Cifuentes 1999;Chanton and Lewis 2002; Cloern et al 2002). We predictedthat there would be significant differences in the isotopicsignatures of plants and animals collected on each side ofthe causeway if construction of the causeway alteredtrophic linkages in the MTD.

Materials and Methods

Field Locations

Samples were collected in areas (0.25 km2) north of thecauseway in Chocolatta Bay and south of the causeway atthe upper reaches Mobile Bay, approximately 0.5 kmsouthwest of the Chocolatta Bay site (Fig. 1). There arefour 400 m wide, artificial “spillways” that allow somewater flow between these two locations. The depth of theareas sampled ranged from about 0.5 m for benthicsampling to 3 m during plankton and otter trawls.

There can be strong changes in stable isotope signaturesacross salinity gradients and with difference in waterquality (Fry 2002) therefore, YSI 6600 devices weredeployed for 1-year (November 2003–November 2004), tocontinuously record salinity, temperature, and dissolvedoxygen concentrations in Chocolatta Bay and at MeaherPark, just east of the southern causeway sampling area, at15- or 30-min intervals, respectively. Nitrogen and phos-phorus concentrations in the water were also measured ingrab samples collected in February, May, June, August, andOctober 2004 at the sites used in this study. Water grabsamples were analyzed for ammonia (method EPA 350.1),nitrate/nitrite (method EPA 353.2), total Kjeldahl nitrogen(method EPA 351.2), and total phosphorus (method EPA365.4; Valentine et al. 2004).

Sediment samples were also collected at the sites inFebruary 2004 and analyzed for percent clay, silt, sand,and gravel. Water content (%) and total carbon ofsediments were also measure (for details see Valentineet al. 2004).

Field Collections

Common conspecific plants and animals (Table 2) werecollected from the sampling areas north and south of thecauseway in July 2004 (Fig. 1).

Mid-water and surface plankton (including zooplanktonand suspended detritus) were collected in three separatesampling locations approximately 250 m from each othernorth and south of the causeway using 153 μm planktonnets. Ponar grabs were used to collect plant detritus,consisting of a mixture of the dead leaves of submergedaquatic vegetation and terrestrial plants, at the threelocations north and south of the causeway. Ponar grabswere washed through a 500-μm sieve. Sediment samples (top2 cm) were also collected using a petite ponar grab at threereplicate locations on either side of the causeway. Leaves ofsubmerged and aquatic floating plants were collected by handat three locations within the sampling area. Terrestrial leaves(i.e., Black willow, Salix nigra; phragmites, Phragmitesaustralia; and morning glory, Ipomoea sp.) were collectedfrom separate stands of plants within the sampling areasnorth and south of the causeway. Macroinvertebrates (i.e.,gastropods, Neritina reclivata; grass shrimp, Palaeomonetesspp.; and amphipods, Gammarus mucronatus) were collectedfrom the leaves of samples taken from the submergedmacrophytes. Bivalves (Rangia cuneata) were raked up fromwithin the sediments at three locations north and south of thecauseway within the sampling area. Fish, blue crabs, andwhite shrimp were collected north and south of the causewayin three replicate otter trawls within each sampling area. Allsamples were held on ice while being transported to thelaboratory where they were frozen until processing for stableisotopic analyses.

Laboratory Processing

Plankton samples were filtered through a glass-fiber filter(Whatman GF/C 42) and dried at 60°C for 24 h. Plant,detritus, and sediment samples were washed down withdistilled water and dried in a similar fashion. Wholespecimens of small invertebrates (e.g., amphipods Gamma-rus mucronatus and grass shrimp Palaeomonetes spp.) werepooled to provide enough tissue for analysis. Muscle tissuesof larger invertebrates (e.g., bivalves Rangia cuneata,gastropods Neritina reclivata, white shrimp Penaeusaztecus, and blue crabs Callinectes sapidus) were extractedby hand and pooled by replicate location for analysis. Theentire body of smaller fish (e.g., bay anchovy Anchoamitchilli and rainwater killifish Lucania parva) wasprocessed for analysis, while tissues from larger fish werefilleted. Once extracted, muscle tissues were washed withdistilled water, dried at 60°C for 24 h and ground into apowder with a Wiley Grinding Mill™.

Estuaries and Coasts (2009) 32:173–187 175175

Stable Isotope Measurements

The University of California-Davis Stable Isotope Facilityconducted the carbon and nitrogen isotope analyses using acontinuous flow isotope ratio mass spectrometer (IRMS;Europa Hydra 20/20). Three replicate samples of eachspecies were used for carbon and nitrogen isotope analyses.The Colorado Plateau Stable Isotope Laboratory, associatedwith the University of Northern Arizona, conducted sulfurstable isotope analyses using Thermo Electron gas isotoperatio mass spectrometers. Only one sample of each specieswas used for sulfur analysis.

In all cases, isotopic composition was quantified relativeto a standard. The standards for carbon, nitrogen, and sulfurwere Pee Dee Belemnite, air, and Canyon Diablo troilite,respectively.

Stable isotope abundances were expressed as the ratio ofthe two most abundant isotopes in the sample and werecompared to the same ratio using the following formula:

dX %ð Þ¼ Rsample

�Rstandard

� ��1� �� 1; 000

Where X is 13C, 15N, or 34S and R is the ratio 13C/12C,15N/14N, or 34S/32S. Higher δX values denote a greaterproportion of the heavy isotope. All results are expressed asparts per thousand (‰).

Data Analyses

Unpaired t tests (α=0.1) were used to compare carbon andnitrogen signatures of conspecific plants and animalscollected above (north) and below (south) the causeway.Since single samples were analyzed for sulfur signatures,no statistical tests were performed on these data (Table 3).

Comparisons of Food Web Structure

Dual Isotope Plots

To examine differences in food web structure between areasnorth and south of the causeway, δ13C vs. δ15N plots wereused. These plots were comprised of individual data pointsrather than averages. Due to fractionation with trophiclevel, the consumer nitrogen signatures are enriched andappear in the plots above probable food sources.

δ13C and δ34S plots were used to evaluate the relativeimportance of basal sources of production to consumers.δ13C and δ34S values are considered to be the most reliableindicators of which basic sources are used by consumerssince they are not thought to fractionate as they aretransmitted upward within coastal food webs (Petersonand Howarth 1987; Fry 1988 however see McCutchan et al.2003). Therefore, consumers will cluster around what foodsources they utilize. Plots of δ13C vs. δ34S contain the

single points for δ34S analysis and the average of δ13Cvalues without error bars (see Table 2 for SE values). Theδ15N vs. δ34S plot is not shown, as the other plots weresufficient to reveal causeway impacts on trophic linkageswithin the MTD.

Mixing Models

Two mixing models were run using IsoSource version 1.3.1software (provided by the U.S. Environmental ProtectionAgency) to assess if consumer diets (primary and secondaryconsumers) differed with causeway location. In the model,the isotopic signatures (δ values) for the selected foodsources and the consumer groups were supplied. Because oftrophic level fractionation of the stable nitrogen isotope,3‰ was subtracted from these signatures in consumersprior to the model analysis (see Peterson and Howarth1987; Post 2002; Vanderklift and Ponsard 2003). Carbonisotope fractionation has previously been assumed to benear zero (Peterson and Fry 1987), however, Post (2002)found δ13C fractionation to be, on average +0.4 ‰ (1 SD=1.3‰). Furthermore, results from McCutchan et al. 2003suggest that trophic shift for carbon can differ with wholeanimal and muscle tissue samples from +0.3‰ to +1.3‰,respectively. Since this study was focused on comparingsites and not elucidating trophic position specifically andsince both whole and muscle tissues samples were used forspecies, the models were run with no adjustments to δ13Cfor trophic shift to remain consistent in the model setup.Similarly, sulfur isotope fractionation was assumed to bezero (Peterson and Fry 1987; McCutchan et al. 2003). Withthe model, bounds for the contribution of each food sourcewere set by providing a specified increment (1%) in whichall possible combinations of each source contribution(0–100%) were examined. A mass balance tolerance wasalso specified to set bounds on feasible solutions of thecombinations that sum to the observed mixture isotopicsignatures. From this, a frequency and range of potentialsource contributions was provided (Ben-David and Schell2001; Phillips 2001; Phillips and Gregg 2001; Phillips andGregg 2003), and data were presented as a possibleproportional contribution of selected food sources to dietsof the consumers.

In the first mixing model, stable isotope signatures wereused to predict probable contributions of basal food sources(terrestrial leaves, floating and submerged vegetation, andbenthic detritus) to primary consumers (mollusks andcrustaceans) collected on each side of the causeway (threeisotopes × four sources model). In the second analysis, theIsoSource mixing model was used to identify probablecontributions of known food sources (primary productionand primary consumers) to secondary consumers (fish) oneach side of the causeway. Known fish prey including

176 Estuaries and Coasts (2009) 32:173–187

amphipods, grass shrimp, white shrimp, nerite olive snail,plankton, and detritus, were used in this second analysis(three isotopes × six sources model). In all cases, averagesof grouped samples were used in these model analyses.

Results

Physio-Chemical Site Comparisons

YSI data from either side of the causeway indicated thatthese salinity, temperature, and dissolved oxygen concen-trations in Chocolatta Bay and at Meaher Park were verysimilar at each of the sites (Fig. 2) with differences insalinity never exceeding one practical salinity unit (psu),except during the exceptional circumstance created by aHurricane (Valentine et al. 2004). Also, nitrogen andphosphorus concentrations in the water grab samplesshowed very little difference in any of these parameters atour sampling locations with the exception of sampling inJune 2004 when TKN was five times greater and TP wasten times greater south of the causeway. These resultsshould be considered cautiously as there were no replicatesamples on each sampling date (Table 1) (Valentine et al.

2004). Sediment samples, however, generally showed thatsites located south of the causeway had higher percentagesof sand (south: mean±STD, 39.64%±22.75; north: 26.34%±13.29), whereas sites north of the causeway had higherpercentages of clay (north: mean±STD, 19.20%±7.67;south: 12.84%±8.16) and silt (north: mean±STD, 54.44%±10.53; south: 47.52%±15.21). Water content (%) and totalcarbon of sediments north of the causeway were signifi-cantly higher than sites south of the causeway (for detailssee Valentine et al. 2004).

Comparisons of Primary Producer Isotopic Signatures

The δ13C stable isotope signatures of eight of the 11 basalsources of nutrition, varied significantly between loca-tions (Tables 2 and 3). The δ13C signatures of thesesources in aggregate, however, did not vary in similarways with causeway location (Fig. 3a). While the δ13Csignatures of water fern (Salvinia minima) did not differsignificantly with location, the δ13C signatures of waterhyacinth (Eichhornia crassipes) and the terrestrial morn-ing glory (Ipomoea sp.), black willow (Salix nigra) andthe common reed (Phragmites australis) did (Table 3 andFig. 3a).

Tem

pera

ture

(C

elci

us)

5

10

15

20

25

30

35

DO

(m

g/L)

2

4

6

8

10

12

14

Month

Nov

200

3

Dec

200

3

Jan

2004

Feb

200

4

Mar

200

4

Apr

il 20

04

May

200

4

June

200

4

July

200

4

Aug

200

4

Sep

t 200

4

Oct

200

4

Nov

200

4

Sal

inity

(ps

u)

01234567

Hurricane IvanFig. 2 Weekly averages of con-tinuous temperature (°C), dis-solved oxygen (mg/L) andsalinity measurements forChocolatta Bay and MeaherPark from November 2003 toNovember 2004. Closed sym-bols are data from ChocolattaBay, and open symbols are datafrom Meaher Park, south of theCauseway

Estuaries and Coasts (2009) 32:173–187 177177

The δ13C signatures of submerged aquatic vegetation(SAV), in most cases, were also variable with location. Theδ13C signatures of green algae (Cladophora spp.) and tapegrass (Vallisneria americana) collected south of thecauseway were significantly more enriched than conspe-cifics collected to the north. In contrast, the δ13C signatures

of Eurasian milfoil (Myriophyllum spicatum) and waterstargrass (Heteranthera dubia) were significantly moredepleted south of the causeway. Southern naiad (Najasguadalupensis) was the only species of SAV whose δ13Csignature did not differ significantly with location (Table 3and Fig. 3a). While the δ13C signature of sediments was

Table 1 Summary table for 2004 nutrient analyses (NH4, NO3–NO2, TKN, TP) by month and site

Nutrients (mg/L) Feb 2004 May 2004 June 2004 August 2004 Oct 2004

N S N S N S N S N S

NH4 0.04 0.05 <0.01 0.01 <0.01 0.02 0.01 0.05 0.06 0.16NO3–NO2 0.18 0.18 0.15 0.13 0.005 0.14 0.03 0.07 0.14 0.15TKN 0.59 0.29 0.35 0.22 0.10 0.49 0.64 0.72 0.70 0.93TP 0.090 0.10 0.05 0.04 0.005 0.05 0.04 0.07 0.08 0.10

N North of Causeway, S South of Causeway

Table 2 Samples collected for stable isotope analysis [δ13C (‰), δ15N(‰), δ34S(‰)]

Sampletype

Common name (Scientific name) δ13C(‰) δ15N(‰) δ34S(‰)

North South North South North South

Detritus −26.79±0.53 −26.55±1.20 (2) 5.21±0.37 4.95±0.37 −4.90 −0.39Sediment −25.43±0.05 −26.64±0.01 4.12±0.16 5.57±0.19 −1.26 −6.01

Primary producersTerrestrial Black Willow (Salix nigra) −30.27±0.14 −29.18±0.10 5.09±0.24 7.75±0.05 7.89 12.1

Morning Glory (Ipomoea sp.) −29.13±0.09 −28.32±0.10 1.81±0.16 7.30±0.14 6.05 11.15Phragmites (Phragmites australis) −25.79±0.08 −28.94±0.09 4.85±0.25 7.32±0.38 10.83 11.33

Submerged Tape grass (Vallisneria americana) −19.83±0.06 −19.55±0.01 (2) 5.73±0.20 7.35±0.05 8.31 9.65Najas (Najas guadalupensis) −21.41±0.95 −22.39±0.11 3.15±1.72 7.90±0.23 3.02 8.33Water stargrass (Heteranthera dubia) −19.31±0.22 −21.21±0.08 3.44±1.59 6.41±0.08 2.37 6.07Eurasian watermilfoil (Myriophyllumspicatum)

−19.38±0.01 −19.83±0.08 4.69±0.14 5.93±0.11 6.82 8.5

Cladophora (Cladophora sp.) −18.30±0.15 −16.40±0.03 5.88±0.27 5.57±0.26 8.05 14.99Floating Water fern (Salvinia minima) −27.03±1.36 −28.19±0.02 6.23±0.39 5.59±0.72 11.28 6.61

Water hyacinth (Eichhornia crassipes) −29.25±0.04 −28.71±0.07 5.59±0.72 4.55±0.90 9.61Plankton −25.82±0.11 (2) −25.87±0.12 (2) 8.38±0.51 6.29±0.45 1.84 2.19

Primary consumersCrustaceans Amphipods (Gammarus mucronatus) −20.16±0.07 −20.14±0.04 (2) 4.59±0.03 7.46±0.25 8.14 11.98

Grass shrimp (Palaeomonetes sp.) −22.89±0.25 −19.84±0.12 8.32±0.18 10.90±0.15 6.2 13.06White shrimp (Penaeus aztecus) −27.64±0.04 −25.62±0.11 9.12±0.01 10.48±0.22 5.55 7.84Blue Crab (Callinectes sapidus) −23.28±1.61 −22.28±0.91 9.02±0.49 10.06±0.14 6.79 11.54

Mollusks Olive Nerite (Neritina usnea) −21.23±0.13 −17.13±0.26 8.97±0.13 9.75±0.18 7.47 13.96Common rangia (Rangia cuneata) −28.89±0.46 −28.47±1.25 8.35±0.28 10.29±0.44 7.06 5.52

Secondary ConsumersFish Rainwater killifish (Lucania parva) −22.89±0.16 −19.53±0.09 9.04±0.23 11.62±0.20 5.58 12.57

Pipefish (Sygnathus scovelli) −23.48±0.15 −24.94±0.27 9.38±0.22 11.92±0.04 5.92 8.41Redear sunfish (Lepomis microlophus) −21.48±0.02 −21.13±0.05 10.72±0.03 13.14±0.11 6.37 10.02Croaker (Micropogonias undulatus) −26.90±0.23 −24.88±0.60 10.89±0.57 12.06±0.01 5.59 10.15Silverside (Menidia beryllina) −25.94±0.10 −22.96±0.07 11.36±0.08 11.89±0.13 4.64 9.29Anchovy (Anchoa mitchilli) −28.22±1.01 −27.01±1.45 11.69±0.63 12.31±0.82 6.55 9.32Spot (Leiostomus xanthurus) −24.31±0.38 −22.17±0.61 11.90±0.24 13.29±0.22 4.36 7.79

Unless identified in parentheses, three samples were averaged (±SE). Only one sample was analyzed for δ34 S.

178 Estuaries and Coasts (2009) 32:173–187

significantly more enriched north of the causeway, the δ13Csignature of the detritus in these samples did not varysignificantly with location.

The δ15N signatures of eight of the 11 probable basalsources of nutrition also varied significantly with location.Of these, the δ15N signatures of floating plants (waterhyacinth and plankton) were significantly enriched northof the causeway. In contrast, the δ15N signatures of allterrestrial plants were significantly enriched south of thecauseway, as were milfoil, southern naiad, and tapegrass(SAV species). The signatures of green algae and waterstargrass did not differ significantly with location. Sedi-ment samples were also enriched south of the causeway,but detritus samples did not differ (Tables 2 and 3 andFig. 3B).

The δ34S signatures of all species submerged plants,terrestrial plants, plankton, and detritus in the Ponar grabsamples were significantly enriched south of the causeway.Only the water fern and sediments were more enrichednorth of the causeway, and no comparison was able to bemade for water hyacinth (Fig. 3c).

Comparisons of Consumer Isotopic Composition

The δ13C signatures of nine of the 13 consumers collectedvaried significantly with location (Table 3). Among thefishes whose δ13C signatures varied significantly withlocation, all but the pipefish (Sygnathus scovelli) wereenriched south of the causeway. δ13C signatures of olivenerite snails (Neritina usnea), white shrimp (Litopenaeussetiferus), and grass shrimp (Palaeomonetes spp.) also weresignificantly enriched south of the causeway (Table 3 andFig. 4A). Only the δ13C signatures of bay anchovies (A.mitchilli), common rangia (R. cuneata), blue crabs (C.sapidus), and amphipods (G. mucronatus) were not foundto differ significantly with causeway location (Table 3 andFig. 4a).

With the exception of croaker, bay anchovy, and bluecrabs, the δ15N signatures of all of the consumers weresignificantly enriched south of the causeway (Table 3 andFig. 4b), and with the exception of the common rangia, theδ34S signatures of all of the consumers were enriched southof the causeway (Table 3 and Fig. 4c).

Table 3 Statistical results of t tests comparing δ13C and δ15N signatures in plants and animals collected north and south of causeway

Sample type Common name (Scientific name) δ13C (‰) δ15N (‰)

Detritus P=0.84, df=3, t=−0.21 P=0.66, df=3, t=0.47Sediment *P<0.01, df=4, t=21.92 *P<0.01, df=4, t=−5.75

Primary producersTerrestrial Black Willow (Salix nigra) *P<0.01, df=4, t=−6.33 *P<0.01, df=4, t=−11.01

Morning Glory (Ipomoea sp.) *P<0.01, df=4, t=−6.25 *P<0.01, df=4, t=−25.53Common reed (Phragmites australis) *P<0.01, df=4, t=26.51 *P<0.01, df=4, t=−5.48

Submerged Tape grass (Vallisneria americana) *P=0.03, df=3, t=−3.83 *P<0.01, df=3, t=−6.28Southern naiad (Najas guadalupensis) P=0.36, df=4, t=1.01 *P=0.05, df=4, t=−2.73Water stargrass (Heteranthera dubia) *P<0.01, df=4, t=8.09 P=0.14, df=4, t=−1.86Eurasian watermilfoil (Myriophyllum spicatum) *P<0.01, df=4, t=5.40 *P<0.01, df=4, t=−7.13Cladophora (Cladophora spp.) *P<0.01, df=4, t=−12.79 P=0.46, df=4, t=0.817

Floating Water fern (Salvinia minima) P=0.44, df=4, t=0.85 P=0.47, df=4, t=−6.28Water hyacinth (Eichhornia crassipes) *P<0.01, df=4, t=−7.16 *P=0.08, df=4, t=2.34Plankton P=0.83, df=2, t=0.25 *P=0.09, df=2, t=3.07

Primary consumersCrustaceans Amphipods (Gammarus mucronatus.) P=0.87, df=3, t=−0.18 *P<0.01, df=3, t=−14.96

Grass shrimp (Palaeomonetes sp.) *P<0.01, df=4, t=−11.02 *P<0.01, df=4, t=−11.12White shrimp (Litopenaeus aztecus) *P<0.01, df=4, t=−17.13 *P<0.01, df=4, t=−6.17Blue Crab (Callinectes sapidus) P=0.62, df=4, t=0.54 P=0.11, df=4, t=−2.04

Mollusks Olive nerite (Neritina usnea) *P<0.01, df=4, t=−14.28 *P=0.02, df=4, t=−3.56Common rangia (Rangia cuneata) P=0.77, df=4, t=−0.31 *P=0.04, df=4, t=−3.01

Secondary consumersFish Rainwater killifish (Lucania parva) *P<0.01, df=4, t=−18.04 *P<0.01, df=4, t=−8.39

Pipefish (Sygnathus scovelli) *P=0.01, df=4, t=4.74 *P<0.01, df=4, t=−11.28Redear sunfish (Lepomis microlophus) *P<0.01, df=4, t=−6.06 *P<0.01, df=4, t=−22.13Croaker (Micropogonias undulatus) *P=0.04, df=4, t=−3.15 P=0.11, df=4, t=−2.03Silverside (Menidia beryllina) *P<0.01, df=4, t=−23.58 *P=0.02, df=4, t=−3.58Bay anchovy (Anchoa mitchilli) P=0.53, df=4, t=−0.69 P=0.58, df=4, t=−0.60Spot (Leiostomus xanthurus) *P=0.04, df=4, t=−2.96 *P=0.01, df=4, t=−4.27

Estuaries and Coasts (2009) 32:173–187 179179

15N (‰)

0 2 4 6 8 10

Ter

rest

rial

Sediment*

Detritus

Black willow*

Morning Glory*

Phragmites*

Vallisneria*

Najas*

Heterantrea

Milfoil*

Cladophora

Plankton*

Water fern

Water hyacinth*

NorthSouth

Ben

thic

Flo

atin

gS

AV

Primary producers and benthos

Ter

rest

rial

Ben

thic

Flo

atin

gS

AV

13C (‰)

-32 -30 -28 -26 -24 -22 -20 -18 -16 -14

Sediment*

Detritus

Black willow*

Morning Glory*

Phragmites*

Vallisneria*

Najas

Heteranthera*

Milfoil*

Cladophora*

Plankton

Water fern

Water hyacinth*

34S (‰)

-10 -5 0 5 10 15 20

Sediment

Detritus

Black willow

Morning Glory

Phragmites

Vallisneria

Najas

Heteranthera

Milfoil

Cladophora

Plankton

Water fern

Water hyacinth

Ter

rest

rial

Ben

thic

Flo

atin

gS

AV

(a)

(b)

(c)

δ

δ

δ

Fig. 3 a, b, c δ13C, δ15N, andδ34S of primary producers, de-tritus, and sediment samplesnorth and south of the causeway.Asterisk represent significantdifferences

180 Estuaries and Coasts (2009) 32:173–187

Consumers

15N (‰)

4 6 8 10 12 14

Amphipods*

Grass shrimp*

White shrimp*

Blue Crab

Neritina*

Rangia*

Rainwater Killifish*

Pipefish*

Redear Sunfish*

Croaker

Silverside*

Anchovy

Spot*

NorthSouth

Mol

lusk

sC

rust

acea

nsF

ish

Mol

lusk

sC

rust

acea

nsF

ish

34S (‰)

2 4 6 8 10 12 14 16

Amphipods

Grass shrimp

White shrimp

Blue Crab

Neritina

Rangia

Rainwater Killifish

Pipefish

Redear Sunfish

Croaker

Silverside

Anchovy

Spot

Mol

lusk

sC

rust

acea

nsF

ish

(c)

13 C(‰)-32 -30 -28 -26 -24 -22 -20 -18 -16

Amphipods

Grass shrimp*

White Shrimp*

Blue Crab

Neritina*

Rangia

Rainwater Killifish*

Pipefish*

Redear Sunfish*

Croaker*

Silverside*

Anchovy

Spot*(a)

(b)

δ

δ

δ

Fig. 4 a, b, c δ13C, δ15N, andδ34S of consumers north andsouth of the causeway. Asteriskrepresent significant differences

Estuaries and Coasts (2009) 32:173–187 181181

Comparisons of Food Web Structure

Dual Isotope Plots

Plots of δ13C vs. δ34S signatures north of the causewayshow consumers clustering both closely with terrestrial andfloating vegetation and in between all sources, with only afew consumers appearing to be feeding on submergedplants (Fig. 5a). In contrast, plots of these same consumerscollected south of the causeway clustered more closely withsubmerged plants, suggesting an important shift in thetransmittance of production among the MTD food web(Fig. 5b). Similarly, plots of δ13C vs. δ15N of consumers

and plants also indicated the importance of floating andterrestrial plants to consumers north of the causeway(Fig. 5c). In contrast, plots of δ13C vs. δ15N signatures ofconsumers and plants south of the causeway suggest thatconsumers rely more heavily on submerged plants to meettheir nutritional needs (Fig. 5D).

Mixing Models

The results of three isotopes × four sources mixing modelanalyses also showed that the relative importance ofprimary producers to primary consumers varied withlocation. As with the dual isotope plots, floating plants

North

δ13C (‰) δ13C (‰)

δ13C (‰)δ

δδ

13C(‰)

15N

(‰)

δ 15N

(‰)

0

2

4

6

8

10

12

14

South

0

2

4

6

8

10

12

14(c) (d)

34S

(‰)

-5

0

5

10

15

-32 -30 -28 -26 -24 -22 -20 -18 -16

-32 -30 -28 -26 -24 -22 -20 -18 -16

-32 -30 -28 -26 -24 -22 -20 -18 -16

-32 -30 -28 -26 -24 -22 -20 -18 -16

34S

(‰)

-5

0

5

10

15

Detritus Terrestrial

Floating Submerged CrustaceansMolluscs

Fish

(a) (b)δ

Fig. 5 a–d Dual isotope plots of δ13C vs. δ34S (a and b) and δ13C vs. δ15N (c and d) north and south of the causeway. δ13C vs. δ34S plots containan average value for δ13C. δ13C vs. δ15N plots contains all data points from every sample. They are represented as groups by symbols

182 Estuaries and Coasts (2009) 32:173–187

probably play a more prominent role in crustacean andmollusk diets north of the causeway than south of thecauseway. To the south, submerged plants again figuredmore prominently in crustacean and mollusk diets (Table 4).

Results from the three isotope × six source mixing modelanalyses using fish and their probable food sources(secondary consumers) found little evidence of differencesin localized feeding by fish on either side of the causeway(Table 5).

Discussion

Paired samples of isotopic signatures from each side of thecauseway suggest that hydrological modification of thedelta resulting from the causeway has fundamentally alteredenergy exchange between northern and southern areas ofthe delta. This study was constrained in both space andtime, and was based on the assumption that the samplingareas located within 500 m of each other would havesimilar hydrology and hence indistinguishable isotopicsignatures in the absence of the causeway. While temporalchanges in isotope signatures most likely occur in theselocations with changes in salinity and water quality(Chanton and Lewis, 2002; Cloern et al., 2002; Fry 2002;Hoffman and Bronk, 2006), there was no salinity gradientfor 8 months prior to sampling (Fig. 1), and water qualitywas similar at both locations (Table 1). Similarly, whileranges of isotope signatures reported here are within theranges reported for aquatic species (e.g., Fry and Sherr1984; Sullivan and Moncreiff 1990; Boon and Bunn 1994;Deegan and Garritt 1997; Cloern et al. 2002) and differ-ences between locations may therefore reflect naturalvariation, isotope signatures differed in similar ways for amajority of species, and trends are similar to what would beexpected if estuarine water were not regularly penetratingChocolatta Bay. Thus, it is reasonable to conclude thatdifferences in isotope signatures reported here reflectchanges in energy exchange between northern and southernareas of the delta resulting from the causeway.

Comparison of Isotopic Signatures

δ15N signatures of submerged and terrestrial plants collect-ed south of the causeway, with only one exception, weremore enriched than were conspecifics collected north of thecauseway. Depleted signatures of δ15N are thought toindicate terrestrial/freshwater systems while more enrichedsignatures reflect estuarine/marine-influenced systems (Fryand Sherr 1984; Schoeninger and DeNiro 1984; Michenerand Schell 1994). These assumptions are based oninformation that lowland forest vegetation tends to havenitrogen isotope values close to 0‰ (atmospheric nitrogen),whereas nearshore nitrogen isotope values range from 6‰to 10‰ (Peterson and Howarth 1987). Our results suggestthat estuarine nutrients are more important than terrestrialnutrients to production south of the causeway than north ofthe causeway.

In contrast to submerged and terrestrial plants, the threesamples of floating plants showed trends toward δ15Nenrichment north of the causeway. A potential explanationis that these plants rely solely on nutrients in the watercolumn, whereas rooted terrestrial and SAV plant speciesalso receive nutrients from sediments. For example,submerged aquatic species such as Vallisneria are knownto take up nutrients in both sediments and water columnsdepending on relative nutrient availability (Xie et al 2005),whereas floating species can only get nutrients from thewater column. Furthermore, sediment δ15N signatures weresimilar to the trends found for SAV (enriched south of thecauseway) indicating that these plants were getting theirnitrogen from sediment sources.

The disparity between δ15N signatures north and southof the causeway for SAV and terrestrial plants signaturescould be attributed to anthropogenic sources. Enriched δ15Nsignatures in aquatic macrophytes have been show to becorrelated with exposure to human septic and sewage wastein both estuarine and freshwater ecosystems (McClelland etal. 1997; Udy and Dennison 1997; McClelland and Valiela1998; Tucker et al 1999; Costanzo et al 2001; Wayland andHobson 2001; Cole et al. 2004; Steffy and Kilham 2004;Kaushal et al. 2006; Benson et al 2008). For example,Benson et al. (2008) found that elevated nitrogen signatures

Table 4 Range of probable contributions of food sources for primaryconsumers collected north and south of the causeway

Possible foodsources

Crustaceans Mollusks

North (%) South (%) North (%) South (%)

Detritus 0–11 0–1 0–7 0–14Terrestrial 0–55 30–36 0–49 7–43SAV 39–67 64–70 19–47 53–78Floating 0–61 0–1 18–81 0–23

Table 5 Percentage range of probable contributions of food sourcesfor secondary consumers (fish) north and south of the causeway

Possible food sources North (%) South (%)

Amphipods 0–50 0–62Grass shrimp 0–81 0–63White shrimp 0–74 0–82Detritus 0–21 0–30Plankton 0–53 0–40Nerite olive 0–59 0–42

Estuaries and Coasts (2009) 32:173–187 183183

in Vallesneria americana can suggest increased uptake ofnitrogen derived from human and/or animal waste. TheMTD is located west of the city of Mobile and down riverfrom the State’s agricultural lands both of which arepossible sources of enriched 15N. It is also possible thathuman sources of nitrogen are being vectored differentlyinto the locations north and south of the causeway due tothe hydrological modifications (Mobile Causeway). Nitro-gen sources from the major rivers may get flushed down tosouth of the causeway and not into the closed ChocolattaBay north of the causeway. Water quality grab samples didshow elevated nutrient levels in June 2004 south of thecauseway, a few weeks before sampling (Table 1) as didsediment isotopic signatures. Further study on the nutrientsources and their frequency would be needed to confirmthese speculations.

Interestingly, δ15N signatures of consumers showedsimilar isotopic trends to primary producers in theirrespective locations, with more enriched nitrogen isotopevalues south of the causeway and less enriched signaturesnorth of the causeway. This indicates that there is littlemovement or exchange between these consumers (Fig. 4B)and also a dependence of primary consumers on rootedmacrophytes as a food resource. The extent of thisdependence is further elucidated in the dual isotope plotsand mixing models (see “Discussion” section below).Moeri et al. (2003) have shown that ambient ammoniacan have direct effects on nitrogen isotope ratios of fishtissue. Although sampling of nutrients for respective siteswas minimal and perhaps not biologically different(Table 1), there were higher levels of ammonia south ofthe causeway. Raised levels of ammonia south of thecauseway may therefore be labeling fish as enriched. Ineither scenario, the difference is due to cessation of flownorth and south of the causeway.

The δ34S signatures could not be compared statisticallybecause there was only one sample for each, and the resultsneed to be interpreted cautiously. While recognizing thislimitation, the δ34S signatures of the submerged plants,terrestrial plants, and detritus were all enriched south of thecauseway. Seawater sulfate usually has a value around+21‰, whereas terrestrial plants use sulfate available fromprecipitation and have values ranging from +2‰ to +8‰(Peterson and Howarth 1987). With our samples, sulfurconcentrations of submerged plants ranged from 6‰ to 15‰south of the causeway compared to 2‰ to 8‰ north of thecauseway, indicating that there are more estuarine influencessouth of the causeway. The notable exception to this trendwas sediments which were highly enriched north of thecauseway. This may be directly linked to microbial processeswithin sediment types (see the “Discussion” section below).

δ13C signatures were usually enriched south of thecauseway for consumers (Fig. 4); however, this was not

the case with basal primary producers which did not showconsistent differences on either side of the causeway.Floating plants and terrestrial plants had similar δ13Csignatures regardless of location, whereas the SAVon eitherside of the causeway was more enriched than the terrestrialand floating samples (Fig. 3). However, this trend was notapparent with the nitrogen or sulfur isotopic compositions,making it a uniquely carbon-related difference. A potentialexplanation for these results is that the sources of carbontaken up by submerged plants differ among species (SAVvs. terrestrial/floating plants) but not impacted in anysignificant way by the presence of the causeway (Fig. 3).Perhaps the usable sources of carbon to basal primaryproducers is the same north and south of the causeway.

Detritus samples had surprising results worth discussingspecifically as their physical characteristics were obviouslyvery different north and south of the causeway. Detritussamples south of the causeway were more intact, whereasnorth of the causeway, the detritus was very fine. Weexpected the detritus samples to reflect the obvious north/south causeway trends found for δ15N, but they were notsignificantly different. Similarly, the detritus carbon isotopesignatures also did not differ significantly. In many studies,δ13C and δ15N samples of detritus have been shown to behighly variable (e.g., Fry and Sherr 1984; Cloern et al2002) due to numerous sources of organic matter. There area variety of potential carbon and nitrogen sources to thesesystems that may skew these results including terrestrialrunoff from forest and agriculture lands, urban runoff, andindustrial effluent (Coffin and Cifuentes 1999). Withdetritus, the discrepancy between living and dead biomasscan be very different (∼5–10‰) for carbon and nitrogenisotope signatures (Cloern et al 2002) which could be whyour isotope results do not reflect the reported trends in basalprimary production.

Another reason for the trends seen in the isotopicsignatures at a basal level could be the difference insediment types north and south of the causeway reported byValentine et al. (2004). As a supposed effect of thehydrological modification, sediments north of the causewayare more clay-based, whereas south of the causeway, sandysediments are prevalent. Evidence is lacking as to whetherdifferent sediment types effect isotopic signatures ofprimary producers, however, given the overwhelmingevidence that sediment type can have dramatic effects onplant growth. For example, Vallisneria natans, shoot/leafgrowth is higher in clay than in sandy loam (Xie et al.2005, Xie et al. 2005), but root biomass is higher in sandyloam in order to increase nutrient uptake. Morphologicalchanges in plants due to sediment nutrient concentrationswould also have effects on sediment isotopic composition.Nitrogen isotope signatures of the sediment reflect the trendseen in the SAV and terrestrial plants north and south of the

184 Estuaries and Coasts (2009) 32:173–187

causeway, while the sulfur isotope signature does not. Thismay reflect the differences of microbial activity andbiomass in different sediment types (e.g., Dale 1974;Yamamoto and Lopez 1985; Nealson 1997), but needs tobe interpreted with caution as Cloern et al (2002) haveshown that there can be large dissimilarity between thecarbon and nitrogen isotope signatures of primary pro-ducers and the organic-matter pools in sediments.

An effect of the causeway has been a decrease in waterflow north of the causeway. This would be worthinvestigating further as a source of discrepancy betweenwater velocity has been shown to have effects on isotopicsignatures (MacLeod and Barton 1998; Finlay et al 1999;Crossley et al 2002; Trudeau and Rasmussen 2003).

Comparison of Food Web Structure

With confirmation that little exchange is occurring betweenthe causeway sites as indicated by the isotope signaturedata, the dual isotope plots and mixing models allowed forfurther elucidation if any differences also existed in foodweb structure. Dual isotope plots can be used to showassociations among isotopic distributions of primary pro-ducers and consumers and also indicate differences in foodweb structure. Dual plot of δ13C vs. δ34S signatures areuseful in elucidating differences in food web structure asneither one fractionates a great amount with trophic level.Inspection of the shape of the plots indicates differences inthe food web structure (Fig. 5a and b) from north to southof the causeway. Data points for consumers seem to clustermore closely between terrestrial, floating, and submergedplant sources north of the causeway, whereas south of thecauseway, consumers seem to be clustered more so aroundsubmerged plants and somewhat on floating (less soterrestrial plants).

δ13C vs. δ15N dual plots help to reveal differences infood sources for consumers due to fractionation of nitrogenwith trophic position. These plots confirm the results fromthe δ13C vs. δ34S plots showing that the food web structurediffers from north to south of the causeway. There is someobvious displacement of mollusks and crustaceans towardsubmerged plants as a food sources south of the causeway,and some fish also seem to follow this trend consuming theenriched crustaceans and mollusks (Fig. 5c and d). Relevantabundances of primary production can be suggested as oneexplanation for the differences in food dependence byprimary consumers. Although measure of relative abun-dance of plant species were not made, it would be safe toassume from observations that floating plant species suchas water fern and hyacinth and terrestrial plants are moreabundant in the closed bays north of the causeway due tohydrology changes from the causeway, thus explainingprimary consumer dependence in these locations. SAV is

highly abundant in both locations if not more so north ofthe causeway where it was not shown to be as much a partof the diet. Perhaps the plethora of food choices north of thecauseway is reflected in the primary consumer foodpreferences as shown in the dual isotope plots.

The conclusions drawn from the results of the mixingmodels are very similar to those drawn from the dualisotope plots, showing a shift in food dependence tosubmerged plants south of the causeway. The mollusksand crustaceans were all somewhat more dependent onsubmerged plants south of the causeway, showing a widerrange of probability of submerged plants as a food sourcecompared to north of the causeway (Table 4). The probablefood sources chosen for this model typically reflect diets ofthe primary consumers. Nerite snails, amphipods, grassshrimp, and white shrimp are cited as consuming detritusand algae (Odum and Heald 1972; Zimmerman et al. 1979),and all these species were found within SAV. Species suchas blue crabs are known to consume algae and SAValthough they prefer mollusks (e.g., Eggleston 1990),whereas Rangia cuneata is a nonselective filter-feeder thatconsumes plant detritus and plankton (Darnell 1958).

The second model showed that localized food sources(mostly grass shrimp and white shrimp) played similarlyimportant roles in fish diets both north and south of thecauseway (Table 5). Overall, this analysis indicated that, atsecondary levels, consumers are eating very similar sourceswithin their localized food web. In other words, there areseparate food webs (north vs. south) with similar structureat a secondary level. This is further evident in the similarshape of the dual isotope plots with subtle differences in thebasal level and secondary level based on their significantlydifferent δ15N and δ34S signatures.

The probable food sources chosen for this model, for themost part, mirror the reported diets of the fishes collected inthe MTD. Bay anchovy feed heavily on zooplankton(mysids), microinvertebrates, and detritus; redear sunfishhave been reported to utilize snails as a major food item(Darnell 1961; Sheridan 1978); croaker ingest detritus asjuveniles and then shift to feeding extensively on benthicorganisms as they grow (Darnell 1958, 1961; Etzold andChristmas 1979); both pipefish and rainwater killifish areknown to feed on amphipods, shrimp, and algae; silversidesare thought to feed on detritus and amphipods; and juvenileand adult spot are benthic feeders that prey on infaunal andepibenthic invertebrates (Harrington and Harrington 1961).

Conclusion

Analysis of multiple stable isotopes has provided evidenceof altered energy exchange between the MTD and the upperreaches of the Mobile Bay estuary due to hydrological

Estuaries and Coasts (2009) 32:173–187 185185

modification within the spatial–temporal constraints of thestudy. Comparison of isotopic signatures of conspecificscollected north and south of the causeway indicated thatnonmotile lower trophic levels had highly enriched δ15Nand δ34S isotope signatures south of the causeway. Thisdifference was reflected in the less motile (e.g., theherbivores) primary consumer signatures and in motilesecondary consumers (fish). Based on these results, furtheranalysis using dual isotope plots and mixing modelsshowed that primary consumers were utilizing the primaryproduction differently north and south of the causeway, yetsecondary mobile consumers had similar diets in theirrespective locations. Considering these sites were less than0.5 km from each other and had similar salinity and waterquality parameters, we can assume that cessation of flowdue to hydrological modifications has closed this once opensystem from energy exchange, with little estuarine influ-ence from Mobile Bay making it north of the causeway.Expanding this study to include sampling from up river tomid-Mobile Bay over different seasons may give a clearerpicture of the extent of change the Causeway has had on theonce open bays.

Acknowledgments Special thanks to A. Gunter for all his help inthe field. This project was funded by Mobile Bay National EstuaryProgram Mini-Grant Program and the Alabama Center for EstuarineStudies (ACES). Thank you to anonymous reviewers for their helpfulcomments.

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