temporal delta13c records from bottlenose dolphins (tursiops truncatus) reflect variation in...

MARINE MAMMAL SCIENCE, 29(4): 705–718 (October 2013)© 2012 by the Society for Marine MammalogyDOI: 10.1111/j.1748-7692.2012.00618.x

Retrospective analysis of bottlenose dolphin foraging:A legacy of anthropogenic ecosystem disturbance

SAM ROSSMAN,1 Department of Zoology, Michigan State University, East Lansing, Michigan48824, U.S.A.; NELIO B. BARROS,2 Chicago Zoological Society, ! Mote Marine Laboratory,1600 Ken Thompson Parkway, Sarasota, Florida 34236, U.S.A.; PEGGY H. OSTROM, Depart-ment of Zoology, Michigan State University, East Lansing, Michigan 48824, U.S.A.; CRAIG

A. STRICKER, U.S. Geological Survey, Fort Collins Science Center, Denver Federal Center,Denver, Colorado 80225, U.S.A.; ALETA A. HOHN, National Marine Fisheries Service,Southeast Fisheries Science Center, 101 Pivers Island Rd., Beaufort, North Carolina 28516,U.S.A.;HASAND GANDHI, Department of Zoology, Michigan State University, East Lansing,Michigan 48824, U.S.A.; RANDALL S. WELLS, Chicago Zoological Society, ! Mote MarineLaboratory, 1600 Ken Thompson Parkway, Sarasota, Florida 34236, U.S.A.

Abstract

We used stable isotope analysis to investigate the foraging ecology of coastal bot-tlenose dolphins (Tursiops truncatus) in relation to a series of anthropogenic distur-bances. We first demonstrated that stable isotopes are a faithful indicator of habitatuse by comparing muscle isotope values to behavioral foraging data from the sameindividuals. d13C values increased, while d34S and d15N values decreased with thepercentage of feeding observations in seagrass habitat. We then utilized stable iso-tope values of muscle to assess temporal variation in foraging habitat from 1991 to2010 and collagen from tooth crown tips to assess the time period 1944 to 2007.From 1991 to 2010, d13C values of muscle decreased while d34S values increasedindicating reduced utilization of seagrass habitat. From 1944 to 1989 d13C values ofthe crown tip declined significantly, likely due to a reduction in the coverage of sea-grass habitat and d15N values significantly increased, a trend we attribute to nutrientloading from a rapidly increasing human population. Our results demonstrate theutility of using marine mammal foraging habits to retrospectively assess the extentto which anthropogenic disturbance impacts coastal food webs.

Key words: Tursiops truncatus, bottlenose dolphin, stable isotopes, foraging ecology,seagrass, nutrient loading.

Coastal marine ecosystems can be impacted by a multitude of anthropogenic distur-bances including pollution, habitat alteration, overfishing, and climate disruption.Ecosystem change is often difficult to document because disturbances occur acrossmultiple temporal scales and the vast majority of ecological studies span only a fewyears (Knowlton and Jackson 2008). Because of their high trophic position within the

1Corresponding author (e-mail: [email protected]).2Submitted posthumously.

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food web and their typically long lifespan, large marine predators integrate distur-bance across multiple trophic levels and are of particular interest as sentinels of ecosys-tem change (Sergio et al. 2008). However, collection of consistent, continuous dataover large spatial scales is expensive, requires extensive effort, and is generally onlyavailable from data associated with commercial fishing. While catch data have docu-mented profound global declines in predatory fish populations (Myers and Worm2003), causal mechanisms are difficult to assess. Declining fish stocks are often attrib-uted to intense fishing pressure, but other factors contribute to the diversity and abun-dance of marine organisms. For example, changes in foraging ecology (trophic level,foraging location) have been implicated as important regulators of population size anddistribution of marine organisms (Emslie and Patterson 2007, Osterblom et al. 2008).Because top predators rely on energy transfers from each trophic step, they are sensitiveto perturbations at any point in the food web. Thus, changes in population size, distri-bution, or foraging ecology of top predators are indicators of ecosystem change.The study of marine predator foraging ecology traditionally involves stomach con-

tent analysis or direct observation of feeding behavior (Barros and Wells 1998).Stomach content analysis usually requires deceased animals and stomachs are oftenempty and may be influenced by differential digestion and/or cause of death. Directobservation of prey consumption is informative for predators who capture or consumeprey at or near the water’s surface, but can be time consuming, expensive, and may bebiased toward prey living high in the water column. Stable isotope analysis ofselected tissues from predators is a relatively inexpensive alternative to traditionaldiet analysis and has a long-standing history in food web studies (Peterson and Fry1987). Carbon isotope values (d13C) are valuable because they differ among forms ofprimary production and are passed up the food web to consumers. Thus, they distin-guish organisms from habitats with isotopically unique primary producers (Petersonand Fry 1987). Similar to carbon, sulfur isotope values (d34S) distinguish consumerswho derive nutrition from rooted marine plants vs. phytoplankton (Connolly et al.2004). Nitrogen isotopes (d15N) have been used extensively in food web studiesbecause of the strong positive correlation with trophic level (Peterson and Fry 1987,Harrigan et al. 1989, Gould et al. 1997).Isotope analysis of different tissues aids in the assessment of foraging over different

time scales or through life historymilestones because animal tissues turn over at varyingrates. Blood plasma records foraging over a period of days (Hobson 1999) and muscleintegrates overmanymonths for largemammals (Sponheimer et al. 2006). Protein fromtooth dentin remains metabolically inert once formed and, thus, records foraging at thetime of synthesis (Knoff et al. 2008). The teeth of marine mammals, such as bottlenosedolphins (Tursiops truncatus) have annual growth layers (Hohn et al. 1989) in which col-lagen can be examined to assess isotopic variation of an individual over its lifetime(Mendes et al. 2006, Newsome et al. 2009). The isotope value of collagen in well-pre-served tooth and bone can provide a historical record of foraging (Hobson and Sease1998).Using bone collagen samples from North Sea harbor porpoises (Phocoena phocoena),

Christensen and Richardson (2008) attributed a decrease in d15N to the decliningavailability of high trophic level prey from 1848 to present. In a study of dentin frommid-Atlantic bottlenose dolphin teeth, Walker et al. (1999) found no significantincrease in d15N from the 1880s to the 1980s suggesting little to no change in dol-phin diet over this time period. Unfortunately, information on parameters such as lifehistory, geographic range, migration, sex, and age are often limited for historicalsamples or those from stranded animals of unknown origin; however, any one of these

706 MARINE MAMMAL SCIENCE, VOL. 29, NO. 4, 2013

factors may confound the ability to attribute changes in foraging to disturbance. Dataon any subset of these parameters may offer the possibility to partition variance inisotope values and control for factors unrelated to ecological disturbance.Bottlenose dolphins from Sarasota Bay (SB), Florida, have a well-established, long-

term, residency within SB (Wells et al. 1987, Wells 2003) and thus provide an idealstudy population for probing long-term effects of anthropogenic disturbance on forag-ing ecology. In addition, the Sarasota Dolphin Research Program has collected data onvital rates and a number of other parameters for a multigenerational resident popula-tion of approximately 160 dolphins since 1970 (Wells 2009, Bowen et al. 2010).These dolphins have experienced numerous anthropogenic disturbances likely to influ-ence various aspects of their ecology. For example, since about 1950 SB has undergonelarge-scale changes that altered seagrass coverage and nutrient inputs. Furthermore,the human population surrounding the bay has tripled since 1970 with associatedchanges in commercial and recreational fishing pressure (Sarasota BayNational EstuaryProgram 2010, U.S. Census Bureau 2010). As predators that consume a wide varietyof prey items across numerous estuarine and coastal marine habitats (Barros andWells1998), bottlenose dolphins are likely influenced by ecosystem disturbance.The purpose of this study was to examine the role of anthropogenic disturbance on

the foraging ecology of bottlenose dolphins resident to SB. We first explore the rela-tionship between isotope values and observational foraging data (percentage of feed-ings in seagrass habitat). We then examined muscle tissue from dolphins strandedbetween 1991 and 2010 to assess changes in foraging ecology (habitat and trophiclevel) during a period including the implementation of a 1995 state-wide commercialnet fishing ban. To extend our retrospective analysis of foraging ecology to six dec-ades (1944–2007), we examined the isotope values of dentin from the crown tip(external 2–3 mm of the crown) of teeth collected from known SB stranded or livedolphins sampled during health assessments (Hohn et al. 1989).

Methods

Sample Site and Acquisition

SB is a complex of shallow bays (<4 m deep, 40 km long) on Florida’s central westcoast, communicating with the Gulf of Mexico through narrow deep passes separat-ing a series of narrow barrier islands. The study area encompasses a diverse array ofhabitats including seagrass meadows, mangroves, shorelines, and open bay (Fig. 1).All samples were obtained from a long-term resident population of approximately160 bottlenose dolphins. As part of the Sarasota Dolphin Research Program, mostdolphins from SB are identifiable and of known age and sex (Wells 2003, 2009).Some of the dolphins included in this study were also reported on in Barros andWells (1998). Thus, we were able to compare isotope values from this study to thepercentage of observed feedings in seagrass habitat, documented in Barros and Wells(1998), for the same individuals. Observational data on seagrass foraging and isotopevalues of muscle tissue are reported for six individuals, identified by freeze brandnumber (FB): FB19, FB21, FB31, FB41, FB57, FB98. Four of the individuals usedfor observation-isotope comparison died in 1991, the other two stranded in 1994 and1996. Thus, all but one individual died prior to the net ban.Samples of muscle tissue from SB individuals were obtained from stranded,

deceased dolphins (n = 41) recovered and sampled by Mote Marine Laboratory’s

ROSSMAN ET AL.: BOTTLENOSE DOLPHIN FORAGING 707

Stranding Investigations Program during 1991–2010. Tooth samples were obtainedfrom live animals under local anesthesia during brief capture-release health assess-ments (n = 27) (Hohn et al. 1989) or from stranded, deceased dolphins (1984–2009)(n = 40, total for crown tip data set n = 67).

Sample Preparation

Muscle tissue was freeze-dried, lipid extracted, and homogenized to a fine powderin a ball and capsule amalgamator (Crescent Industries, New Freedom, PA). Aliquots(1 mg) were transferred to tin capsules for stable carbon and nitrogen isotope analy-sis. Stable sulfur isotopes were analyzed separately by weighing 6 mg of sample into

Figure 1. Distribution of habitats used by bottlenose dolphins resident to Sarasota Bay,Florida.


tin capsules amended with 2 mg of vanadium pentoxide. The external 2–3 mm ofthe crown of the tooth (crown tip) was used for isotope analysis. This material isformed prior to one year of age during gestation and early development and is there-fore an indicator of maternal diet. Ages used in this study were obtained from dol-phins of known age via observation or quantification of growth layer groups (GLG)in teeth (Hohn et al. 1989).The crown was separated using a Dremel tool and demineralized in HCl (1N) for

72 h leaving behind a collagenous replica of the tooth. The replica was then driedand lipid extracted. We were able to extract the oldest material, the crown tip, bysectioning 2–3 mm of collagen from the apex of the crown. Collagen samples (1 mg)were transferred to tin cups for d13C and d15N analysis. Insufficient mass precludedsulfur isotope analysis.Aliquots of muscle and tooth collagen were analyzed for stable carbon and nitrogen

isotopic composition using an elemental analyzer (Eurovector, Milan, Italy) interfacedto an Isoprime mass spectrometer (Elementar Americas, Inc., Mt. Laurel, NJ). Sampleswere analyzed for sulfur isotopic composition using an elemental analyzer (CostechAnalytical Technologies, Inc., Valencia, CA) interfaced to a DeltaPlus XP mass spec-trometer (Thermo-Fisher Scientific, Waltham, PA). Isotope values are expressed as:

dX ! "#Rsample=Rstandard$ % 1& ' 1; 000

where X represents 13C, 34S, or 15N and R represents the abundance ratios: 13C/12C,34S/32S, or 15N/14N, respectively. In-house standards used for d13C and d15N were cal-ibrated with respect to international standards VPDB and air, respectively. NBS127(21.1&) and IAEA-SO-6 (!34.05&) were used to normalize d34S data to V-CDT.In-house standard precision is ± 0.2& for d13C, d34S, and d15N values.

Statistical Analysis

All data were approximately normal and homoscedastic. To test the relationshipbetween isotope values of muscle (d13C, d34S, or d15N) and the percentage of observedfeedings in seagrass, we used a linear regression model and a random bivariate resam-pling for 1,000 permutations. For muscle tissue samples collected from 1991 to 2010we used a general linear model (GLM) with d13C, d34S, and d15N as dependent vari-ables and age, sex, weaning status, season, and year as independent variables. Whilemost calves are weaned at 18–20 mo (Perrin and Reilly 1984), calves with ages up to2.5 yr were grouped as preweaned to minimize the contribution of a maternal isotopesignal. Thus the variable weaning/sex consists of dolphins divided into classes of male(n = 9), female (n = 25) or preweaned calf (n = 8). For the variable season dolphinisotope data was grouped by seasons based on the calendar date of stranding: spring(21 April–6 June, n = 8), summer (21 June–20 September, n = 24), fall (21 Septem-ber–20 December, n = 3) and winter (21 December–21 April, n = 6). Categoricalvariables (sex/weaning or season) with a significant effect on isotope value were furtherexamined for differences between groups with Tukey’s post hoc pair-wise comparisons.For teeth collected from live animals, the date of birth was back-calculated from

the age at date of collection. Isotope values from the crown tip reflect the diet ofbottlenose dolphins prior to age one. We used an analysis of covariance (ANCOVA)in which d13C and d15N values were modeled with a continuous variable, year, and acategorical variable, nutrient loading, separating two time periods that markedlydiffered with regard to nutrient loading (prior to and after 1989) (Tomasko et al.


2005). Carbon isotope values from the crown tip were corrected 0.2& per decade toaccount for changes in the d13C of atmospheric CO2 due to the burning of fossil fuels(Suess effect) (Quay et al. 2003). There should be no influence of sex or age on crowntip isotope values as the crown tip is formed prior to 1 yr of age and exclusively influ-enced by maternal foraging ecology. Statistical tests were conducted in R 2.14(R Development Core Team 2011).

Results

Carbon isotope values of muscle indicated a significant positive regression withpercentage of observed foraging in seagrass habitat (Fig. 2A; n = 6, regression withbivariate resampling, r2 = 0.807, P < 0.001); d15N and d34S values were inverselyrelated to observed foraging in seagrass habitat (Fig. 2B, 2C, n = 6, regression withbivariate resampling, d34S: r2 = 0.836, d15N: r2 = 0.952, d34S and d15N:P < 0.001).For muscle samples collected from strandings (1991–2010), the results of the

GLM model explained a significant portion of the variance for carbon and nitrogenisotope values but not sulfur (d13C: n = 41, F5, 35 = 4.17, P = 0.004; d34S: n = 39,F5, 33 = 1.81, P = 0.1383; d15N: n = 41 F5, 35 = 6.24, P < 0.001,). Age was nota significant factor for any of the three isotope values (d13C: t35 = 1.14, P = 0.29;d34S: t33 = 1.12, P = 0.23; d15N: t35 = 1.08, P = 0.29). Weaning/sex was a signifi-cant determinant of d13C (F2, 38 = 6.85, P = 0.002) and d15N (F2, 38 = 15.05,P < 0.001) but not d34S (F2, 36 = 0.62, P = 0.544). Preweaned calves had higherd13C values compared to males but did not significantly differ from females (pre-weaned vs. males, t35 = 2.33, P = 0.026, preweaned vs. females t35 = 1.71,P = 0.095). Preweaned calves had significantly higher nitrogen isotope values com-pared to both males and females (preweaned vs. males, t35 = 2.61, P = 0.013, pre-weaned vs. females, t35 = 4.04, P < 0.001). Males and females were not significantlydifferent for carbon or nitrogen isotope values (d13C: t35 = 0.78, P = 0.710; d15N:t35 = 1.48, P = 0.310). Season was not significant for any of the three isotopes (d13C:F3, 37 = 0.73, P = 0.543; d34S: F3, 35 = 1.12, P = 0.353; d15N: F3, 37 = 0.03,P = 0.993). Carbon isotope values significantly decreased as a function of year, whilesulfur isotope values significantly increased with year (d13C: Fig. 3A, t35 = 2.32,P = 0.026; d34S: Fig. 3B, t33 = 2.63, P = 0.013). Nitrogen isotope values showedno significant trend with year (Fig. 3C, t35 = 0.50, P = 0.62).For data from the tooth crown tip spanning the time period 1944–2007 an AN-

COVA for both d13C and d15N explained a significant portion of the variance (d13C:Fig. 4, n = 67, F2, 64 = 4.97, P = 0.001; d15N: Fig. 5, n = 67, F2, 64 = 10.68,P < 0.001). For carbon and nitrogen isotope values both year and nutrient loadinghad a significant effect in the ANCOVA model (d13C: Fig. 4, year: t64 = 3.05,P = 0.003; nutrient loading: t64 = 2.72, P = 0.008; d15N: Fig. 5, year: t64 = 4.38,P < 0.001; nutrient loading: t64 = 2.04, P = 0.045).

Discussion

Our multidecadal study of bottlenose dolphin foraging ecology documents largetemporal variation in the d13C, d15N, and d34S values of individuals resident to SB.Because our study population does not frequent the offshore waters including the


open waters of the Gulf of Mexico (Wells et al. 1987, Wells 2003), isotopic differ-ences derive from variation in foraging habits within SB. Isotopic variation is usefulbecause it can provide insight into the ecology of organisms and historical changes inenvironmental conditions (Newsome et al. 2010) particularly in nearshore environ-ments. Carbon isotope values have long been used to distinguish seagrass from non-seagrass based food webs (Peterson and Fry 1987, Harrigan et al. 1989). Similarly,d34S values of consumers frequenting nearshore seagrass habitats are unique compared

Figure 2. d13C, d34S, and d15N values of bottlenose dolphins and percentage of observedfeedings in seagrass habitat. Percentage of observed feedings in seagrass habitat are from Barrosand Wells (1998). Lines indicate the best-fit trend between percent of feedings observed in sea-grass and isotope values.


to those utilizing nonseagrass habitat (Barros et al. 2010). This is because sulfur iso-topes distinguish rooted and nonrooted photo-trophs and these differences are passedup the food web. The uniquely low d34S values of rooted plants, such as seagrass,derive from the incorporation of 34S-depleted sulfides, common in reducing sedi-ments (Connolly et al. 2004, Oakes and Connolly 2004, Brunner and Bernasconi

Figure 3. d13C, d34S and d15N values of muscle from 1991-2010. Open symbols indicatecalves <2.5 yr of age while closed symbols are individuals >2.5 yr old. Lines indicate thebest-fit trend between year and isotope values.


2005) . However, we cannot rule out the possibility that low d34S values are influ-enced by the transfer of sulfur from the terrestrial environment (d34S value approxi-mately 0&) into estuaries where it is taken up by benthic plants and incorporatedinto the food web (Trust and Fry 1992). Regardless, individuals with low sulfur iso-tope and high d13C values likely derive proportionally more nutrition from seagrassbased food webs than open water areas within SB (Bottcher et al. 2006).While d13C and d34S values are established indicators of habitat use, few studies of

wild populations have compared the isotope value of highly mobile organisms totheir habitat of origin. This requires an isotope study that is coordinated with tag-ging or observational efforts, both of which can be quite expensive and labor inten-sive. Thus, we took the unique opportunity to compare our isotope values topreviously reported observational data for six individuals. d13C values are positivelycorrelated with percent observations in seagrass and d34S are negatively correlatedwith the observational data suggesting a close association between observational dataon habitat use and stable isotopes. Thus, it appears that dolphins frequenting seagrasshabitat also derived their carbon and sulfur from seagrass based food webs.Like d13C and d34S, d15N values also vary as a function of percent observations for-

aging in seagrass habitat. d15N values significantly decrease as the percentage ofobserved feeding in seagrass increases (Fig. 2). This may result from variation in theisotope composition of nutrients supplied to the base of the food web (Dillon andChanton 2008, Graham et al. 2010). Alternatively, prey trophic level and availabilityvary by habitat and may also be important controls on d15N values. For example, pin-fish (Lagodon rhomboides) are a dominant dietary item of SB dolphins, are frequentlyassociated with seagrass, and often derive a large portion of their diet from seagrass(Luczkovich and Stellwag 1993, Barros and Wells 1998). Thus, bottlenose dolphinsutilizing seagrass habitats would likely forage at a low trophic level. In contrast, lowtrophic level fish that are abundant in open water habitats (e.g., clupeids) are not com-mon dietary items of bottlenose dolphins (Barros and Wells 1998, Gannon et al.2009, Berens McCabe et al. 2010). Thus, there may be a tendency for dolphins from

Figure 4. d13C values of collagen isolated from the crown tip dating from 1944 to 2007.Closed circles represent the time period of increasing nutrient loading (1944–1989) and theopen circles represent the time period of nutrient loading mitigation (1990–2007).


nonseagrass habitats to feed at higher trophic levels than those that forage in seagrass,consistent with the observed trend in d15N.Muscle isotope data provide foraging information from 1991 to 2010. Among the

variables we tested only weaning status and year had a significant influence on d13Cand d34S values. Calves <2.5 yr old had significantly higher d13C values than olderindividuals. High d13C values are likely the result of both trophic enrichment andthe use of seagrass habitats as a nursery ground for Sarasota Bay dolphins (Wells1991, 1993). In addition to weaning and year, several other factors (e.g., predator dis-tribution or boat traffic) could influence foraging ecology and contribute to the largevariation we observed in our data. Our observational data suggest that SB dolphinsdemonstrate some degree of individual foraging specialization that may also contrib-ute to the wide range of isotope values observed for muscle data from 1991 to 2010.Despite this, the significant influence of year on d13C and d34S values suggests thatthe use of nonseagrass habitats by bottlenose dolphins in Sarasota Bay increased from1991 to 2010, consistent with observations of increased use of open bay habitat bySB dolphins in recent years (Wells 2003). A state-wide net fishing ban may have beena salient factor contributing to this trend. Prior to 1995 dolphins were likely in com-petition with the fishery for some prey species. As a consequence, prior to 1995 dol-phins may have been forced to consume species of no commercial value that derivetheir carbon primarily from inshore seagrass habitats (i.e., pinfish) (Berens McCabe etal. 2010). However, decreased abundance of predator sharks and increased boat trafficin shallow water may also contribute to the trend in d13C (Wells 2003). d15N valuesshowed no significant change between 1991 and 2010. This suggests that factorsother than habitat use are impacting d15N values, a possibility that can be exploredfurther with our long-term tooth crown tip data set.Analyses from crown tips enable us to examine temporal records of bottlenose dol-

phin foraging ecology from 1944 to 2007, as teeth have been collected from knownresident dolphins born as early as 1944. Even after the Suess correction, d13C valuessignificantly declined from 1944 to 1989; a trend that would be falsely inflated if thedata had not been corrected. The temporal decrease in d13C values likely results froma 25% decrease in SB seagrass cover from 1950 to 1989 (Tomasko et al. 2005).In contrast to d13C values, d15N values of crown tips increase from 1944 to 1989.

This trend likely reflects an increase in wastewater loading to Sarasota Bay (Tomaskoet al. 2005). The 15N-enriched nutrients typical of wastewater are taken up by photo-trophs, are passed to consumers, and result in elevated d15N values throughout thefood web (Macko and Ostrom 1994, Cole et al. 2005, Schlacher et al. 2005). Theincrease in d15N values from 1944 to 1989 is proportional to the increase in thehuman population size of Sarasota and Manatee Counties combined, the two countiesencompassing Sarasota Bay (Fig. 5) (U.S. Census Bureau 2010). After 1989, totalnitrogen loading was dramatically reduced due to advances in the treatment of waste-water. In 1988 the total nitrogen entering SB was estimated at 905,386 kg comparedto 488,981 kg in 1990 and a baseline of 191,419 kg in 1890 (Tomasko et al. 2005).The absence of a temporal trend in d15N values after 1989 likely reflects a response ofthe ecosystem to reduced influence of 15N-enriched wastewater.Like the post-1989 tooth data, d15N values of muscle tissue show no relationship

with time from 1991 to 2010. The observation that only carbon and sulfur isotopedata suggest an increased usage of nonseagrass foraging habitats during this period isenigmatic in that all three isotopes correlate with the percentage of observed foragingin seagrass habitat (fig. 2). The influence of habitat use on d15N values may beconfounded by other variables. For example, the expected increases in d15N values of


dolphins resulting from a higher propensity to forage in open water habitat may beobscured by a decrease in nutrient loading and associated with a decline in the contri-bution of 15N enriched nutrients to the food web.In addition to the effects of nutrient loading on nitrogen isotope data, d13C values

of primary producers may be impacted. For example, phytoplankton blooms stimu-lated by nutrient loadings can reduce dissolved CO2 concentrations and increase d

13Cof phototrophs (Popp et al. 1998). However, d13C values declined from 1944 to1989. Thus, we propose an alternative explanation that addresses the temporal trendsin all three isotopes in the context of historical changes to SB.For much of the last half century, SB experienced a slow, steady decline in health

that is strongly related to nitrogen pollution. Nitrogen loadings in 1989 were 4.7times higher than they were in 1890, a phenomenon linked to increased inputs fromwastewater, storm water, and groundwater (e.g., from septic systems) as human popu-lation and development increased (Tomsko et al. 2005). The excess nitrogen stimu-lated algal growth which, in turn, reduced light penetration and caused widespreaddeclines in seagrass across the bay through ca. 1989 (loss of 28% of total seagrass cov-erage 1950–1988) (Tomasko et al. 2005). The recovery of seagrass after 1989 is, inpart, a response to the Grizzle-Figg legislation of August 1988 passed by the Floridastate legislature (Section 403.086, Florida Statutes). This legislation placed limits onthe amount of nitrogen in wastewater discharge and promoted wastewater recoveryefforts. From 1988 to 1990 nitrogen loads entering SB decreased 46% (Tomasko et al.2005). Since then improvements in water treatment technology resulted in furtherreduction of nitrogen loading bay-wide. Today SB receives a nitrogen load equivalentto only 5% of the 1988 value (Sarasota Bay National Estuary Program 2010). Since1988, an improvement in water clarity has been accompanied by a 24% increase inseagrass acreage compared to 1950 values (Sarasota Bay National Estuary Program2010).The undulation in nitrogen loadings and associated seagrass coverage are recorded

in the carbon, sulfur, and nitrogen isotope data preserved within various dolphin

Figure 5. d15N values of collagen isolated from the crown tip dating from 1944 to 2007.Closed circles represent the time period of increasing nutrient loading (1944–1989), the opencircles represent the time period of nutrient loading mitigation (1990–2007) and trianglesshow the human population size of Sarasota and Manatee Counties summed.


tissues. We demonstrate that changes in foraging patterns that correlate withperturbations to the SB ecosystem have been propagated throughout the food webfrom the earliest time we investigated, the 1940s. Thus, marine mammals are notonly sentinels of marine ecosystem health (Wells et al. 2004, Bossart 2010) but canprovide historical context for past ecological change, providing compelling datarelated to human disturbance.

Acknowledgments

Thanks to C. Gulbransen (USGS) for conducting the sulfur isotope analyses and Yun-Jia Lo(Michigan State University) for statistical consulting. We are indebted to the efforts of NelioBarros who provided samples and the inspiration for this work. Nathaniel Ostrom (MichiganState University), Jay Leverone and Mark Alderson (Sarasota Bay Estuary Program) as well asDavid Tomasko provided discussions that improved this manuscript. Samples from live dol-phins were collected under a series of National Marine Fisheries Service Scientific Research Per-mits since 1984 and Mote Marine Laboratory IACUC approvals. Sample collection fromSarasota Bay resident dolphins was supported by Dolphin Quest, Earthwatch Institute, DisneyWorldwide Conservation Fund, National Marine Fisheries Service, The U.S. EnvironmentalProtection Agency, and the International Whaling Commission. This material is based uponwork supported by the National Science Foundation Graduate Research Fellowship underGrant No. (0802267) as well as Marine Mammal Commission Contract #E4047334. Any useof trade, firm, or product names is for descriptive purposes only and does not imply endorse-ment by the U.S. Government, Mote Marine Lab, Chicago Zoological Society or MichiganState University.

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Received: 17 November 2011Accepted: 22 August 2012


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