Seaside Sparrows Reveal Contrasting Food Web Responses to Large&#X26

Seaside Sparrows reveal contrasting food web responses to large-scale stressors in coastal Louisiana saltmarshes 1,5, 2,6 3 2 JILL A. OLIN, CHRISTINE M. BERGEON BURNS, STEFAN WOLTMANN, SABRINA S. TAYLOR, 2 1 4 1 PHILIP C. STOUFFER, WOKIL BAM, LINDA HOOPER-BUI, AND R. EUGENE TURNER

1Department of Oceanography and Coastal Sciences, Louisiana State University, Baton Rouge, Louisiana 70803 USA 2School of Renewable Natural Resources, Louisiana State University AgCenter, Baton Rouge, Louisiana 70803 USA 3Department of Biology and Center of Excellence for Field Biology, Austin Peay State University, Clarksville, Tennessee 37044 USA 4Department of Environmental Sciences, Louisiana State University, Baton Rouge, Louisiana 70803 USA

Citation: Olin, J. A., C. M. Bergeon Burns, S. Woltmann, S. S. Taylor, P. C. Stouffer, W. Bam, L. Hooper-Bui, and R. E. Turner. 2017. Seaside Sparrows reveal contrasting food web responses to large-scale stressors in coastal Louisiana saltmarshes. Ecosphere 8(7):e01878. 10.1002/ecs2.1878

Abstract. Large-scale ecosystem disturbances can alter the flow of energy through food webs, but such processes are not well defined for Gulf of Mexico saltmarsh ecosystems vulnerable to multiple interacting stressors. The 2010 Deepwater Horizon (DWH) oil spill significantly affected the composition of terrestrial saltmarsh communities in Louisiana, and thus had the potential to alter energy pathways through terrestrial and aquatic food webs, with direct consequences for higher trophic-level species restricted to these habitats. The Seaside Sparrow (Ammodramus maritimus) is endemic to saltmarshes and relies completely on the habitat and resources they provide; thus, the sparrows can serve as indicators of ecological change in response to disturbances. We analyzed food web pathways for birds residing in oiled and unoiled saltmarshes for the four years following the oil spill by quantifying the bulk carbon and nitrogen stable isotopes and fatty acid profiles of liver tissues, in addition to primary producers (e.g., marsh grasses) and invertebrate consumers representing the major energy resources in these systems. The stable isotope values of primary producers and most invertebrate consumers did not differ between oiled and unoiled sites, suggesting that the energy pathways within the food web were stable in spite of observed declines in these populations following the spill. The tracer profiles of the Seaside Sparrows confirmed that there was a nominal effect of oil on resource use or trophic position (TP). However, we detected significant inter- annual variation in resource use by these birds; the sparrows occupied a lower TP and exhibited greater assimilation of resources derived from benthic–aquatic relative to terrestrial pathways in 2013 compared to other years. This distinction is likely attributable to the effects of Hurricane Isaac in 2012, whose significant storm surge extensively inundated the saltmarsh landscape. Despite widespread concern for the saltmarsh ecosystem after the DWH event, the significant effects noted at the population level translated into only subtle differences to the flow of energy through this food web. These results demonstrate varying responses to different degrees of landscape-level disturbance, such as oil and hurricanes, and establish the need to better understand food web dynamics in these saltmarsh ecosystems.

Key words: Ammodramus maritimus; arthropods; Deepwater Horizon oil spill; fatty acids; hurricane; stable isotopes.

Received 20 January 2017; revised 28 April 2017; accepted 31 May 2017. Corresponding Editor: Brooke Maslo. Copyright: © 2017 Olin et al. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. 5 Present address: School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, New York 11794 USA. 6 Present address: Center for the Integrative Study of Animal Behavior, Indiana University, Bloomington, Indiana, USA. E-mail: [email protected]

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INTRODUCTION shorelines experiencing little or no oiling, while others were heavily oiled (Michel et al. 2013). Modifications in community composition and Oiled Spartina alterniflora saltmarshes experi- species abundance can alter interaction patterns enced strong effects, including heavy mortalities within food webs (Paine 1980, Polis and Strong that denuded and eroded coastlines (Lin and 1996, Thebault and Loreau 2003, Petchey et al. Mendelssohn 2012, Silliman et al. 2012, McCle- 2008). The food web patterns emerging from a nachan et al. 2013, Turner et al. 2016). These species’ feeding choices give rise to structural changes directly and indirectly affected the phys- complexity, ecosystem stability, and diverse func- ical structure of the saltmarsh, and contributed tioning (Rooney and McCann 2012). Changes in to subsequent declines in the abundance of inver- resource availability and environmental condi- tebrate taxa, including insects, spiders, snails, tions, as well as disturbance, can lead to changes and crabs (McCall and Pennings 2012, Huss- in trophic interactions (Rooney et al. 2006) in eneder et al. 2016). There was, however, consid- accordance with optimal foraging theory (Scho- erable variability in the sensitivity to oil by ener 1971), which predicts increased trophic gen- saltmarsh taxa. The densities of some terrestrial eralism with decreases in food availability or arthropods, for example, were reported to have food quality. The extent to which disturbances recovered one year following initial oiling mediate predator–prey interactions within food (McCall and Pennings 2012) at some locations, webs can lead to individual- and population-level but not at others (Bam 2015, Husseneder et al. effects through diminished growth, survival, 2016). Densities and size-structure of marsh peri- and/or reproductive successes that manifest in winkle (Littoraria irrorata) populations were still subsequent generations. Along the Pacific north- suppressed one year after the initial oiling, with west coast of North America, for example, a shift recovery projected to take several years (Zengel in the foraging ecology of the Glaucous-winged et al. 2016a); the recovery of fiddler crabs (Uca Gull (Larus glaucescens) from a marine- to terres- spp.) and several other benthic meiofaunal spe- trial-based diet was attributable to declining pop- cies was still ongoing four years following the ulations of its preferred fish prey resulting from initial oiling (Fleeger et al. 2015, 2017, Zengel harvesting activities (Blight et al. 2015). Crucially, et al. 2016b). Notably, these saltmarsh-associated these changes to gull diets were correlated with taxa play key ecological roles in supporting ter- the declining egg volume and reproductive restrial and aquatic food webs, linking produc- potential in their populations (Blight 2011). tion resources to higher trophic levels (Pennings Both natural and anthropogenic activities et al. 2014, McCann et al. 2017). Such noted threaten coastal ecosystems and the critical ser- responses of the foundational and lower trophic- vices they provide. The stresses to saltmarsh level invertebrate taxa to the DWH spill have a ecosystems, in particular, include physiological capacity to destabilize or re-organize saltmarsh (e.g., salinity, drought conditions), physical (e.g., food webs by altering the amount and pathways subsidence, storm surge), and biotic challenges of energy flow, with direct consequences for (e.g., competition, predation), all of which can higher trophic-level consumers exploiting the act singularly or synergistically to affect habitat affected habitats (McCann et al. 2017). and energy availability to consumers in these The Seaside Sparrow (Ammodramus maritimus) ecosystems (Doyle et al. 2010, Stouffer et al. is an abundant year-round resident in GOM 2013). Oil spills, in particular, pose a heightened coastal saltmarshes (Post and Greenlaw 1994, threat to ecosystem health because they can be 2006) that feeds on terrestrial and aquatic inver- unpredictable in space and time (Silliman et al. tebrates associated with S. alterniflora marshes 2012). The 2010 Deepwater Horizon (DWH) spill (Post 1974, Post and Greenlaw 2006). As conspic- oiled nearly 1800 km of the Gulf of Mexico uous upper trophic-level species, the Seaside (GOM) coastline (Michel et al. 2013): It was a Sparrow may serve as an indicator of ecological large spatial disturbance with the potential to changes in these ecosystems. In Louisiana, Sea- dramatically alter coastal saltmarsh community side Sparrows continued to occupy oiled marsh structure and functioning. The oiling across the habitat after the spill (Stouffer et al. 2013), con- GOM shoreline was heterogeneous, with some firming their dependence on the habitat and

❖ www.esajournals.org 2 July 2017 ❖ Volume 8(7) ❖ Article e01878 OLIN ET AL. resources provided by these ecosystems, despite oiled marshes consume different prey compared noted alterations to invertebrate populations to conspecifics in unoiled marshes. We expected after the oil spill. The results from studies evalu- both results to be attenuated with time following ating these populations suggest sensitivity to oil the DWH oil spill. from the DWH spill, and also a concern for individual-level growth and fitness that could result MATERIALS AND METHODS in population-level effects in these birds (Bergeon Burns et al. 2014, Bonisoli-Alquati et al. 2016). Study area Our understanding of the consequences of An estimated 45% of wetlands oiled by the large-scale ecosystem disturbances in saltmarsh DWH oil spill were located in coastal Louisiana food webs, including the DWH oil spill, benefits saltmarsh (60% of all habitats; Michel et al. from quantitative approaches that can track con- 2013). The heaviest oiling was most widespread temporary changes in a species’ diet through in the low tidal range, Spartina alterniflora-domi- time. To predict effects of a shifting prey base, nated saltmarsh, of northern Barataria Bay, empirical tools used to accurately characterize Plaquemines Parish, Louisiana. In the absence of dietary trends should allow quantification of pre-spill data with respect to Seaside Sparrow changes at several trophic levels and multiple resource use in Louisiana saltmarsh, we used a nutrient sources (marine, freshwater, and terres- multi-plot design, which allows examination of trial). Bulk stable isotopes (SI) and fatty acid (FA) the magnitude, reproducibility, and variance in profiles are commonly used to quantify food individual- and population-level responses to oil- webs and characterize trophic relationships ing (Skalski 2000). We established replicate study (Hebert et al. 2006) because these tracers can inte- plots on the basis of results from the Shoreline grate both temporal and spatial consumer habitat Cleanup Assessment Technique (SCAT) data to and dietary resource use. Specifically, bulk car- compare unaffected areas with areas that experi- bon isotope content is used to identify produc- enced moderate-to-heavy oiling. Specifically, in tion sources (and thus habitat use), and bulk 2011, we selected two plots, one oiled and one nitrogen isotope content indicates trophic posi- unoiled, in the Port Sulphur area of Barataria tioning and overall food web structuring (Peter- Bay. In 2012, we added four additional plots, two son and Fry 1987). Fatty acids are key nutritional oiled and two unoiled. Selection of all plots was components required for normal growth, devel- based on SCAT maps, with oil contamination opment, and reproduction, and their biosynthesis confirmed through sediment analyses (Michel largely occurs in primary producers (Parrish et al. 2013, Turner et al. 2014a, b). These six plots et al. 2000). The FA composition of producers dif- laid the basis for our experimental design in fers—aquatic producers contain higher total 2012–2014. Plots were 25 ha (500 m along the omega-3 (Σn-3) FA content, whereas terrestrial marsh edge 9 50 m inland). Plots were a mini- producers contain a higher total omega-6 (Σn-6) mum of 1 km apart (Fig. 1). FA content—and their ratio is useful to specify reliance on aquatic vs. terrestrial resources (Kous- Ethics statement soroplis et al. 2008, Hixson et al. 2015). Seaside Sparrows from 2011 were collected We used SI values of carbon (d13C) and nitrogen under U.S. Fish and Wildlife Service (USFWS) (d15N), and FA profiles of taxa from a saltmarsh collecting permit MB679782 and Louisiana food web studied over several years to determine Department of Wildlife and Fisheries (LDWF) (1) which production pathways support the scientific permit LNHP11-062. Birds from 2012 to saltmarsh community and (2) the response of 2014 were collected under USFWS collecting Seaside Sparrows to changes in habitat and prey permits MB095918-0 and MB095918-1; USFWS populations within the context of environmental Federal Bird Banding permit no. 22648; and change, that is, the DWH oil spill. Given the well- LDWF scientific collecting permits LNHP-12-023, described responses by invertebrate populations LNHP-13-059, and LNHP-14-051. This study was to oil, we hypothesized that (1) the terrestrial food carried out in strict accordance with the recom- web is simplified in oiled marshes relative to mendations in the Guide for the Care and Use of unoiled marshes and (2) Seaside Sparrows using Laboratory Animals of the National Institutes of

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Fig. 1. Plot locations in the Port Sulphur area of Barataria Bay, Louisiana. Filled circles represent oiled plots, and ﬁlled squares represent unoiled plots.

Health. Protocols were approved by the Institu- sufficient to represent plot-level differences. tional Animal Care and Use Committee of the Birds were flushed into a continuous line of four LSU AgCenter (IACUC A2012-05). to five, 12-m mist nets oriented perpendicular to the marsh edge (Gordon 2000). Netted individu- Sample collection als were briefly held in cloth bags until eutha- Seaside Sparrows (n = 66) were collected in nized via thoracic compression. All individuals August 2011 and in June of 2012–2014 from the were immediately weighed (g), sampled for liver locations outlined above (Fig. 1). Seaside Spar- and other tissues, and sexed (via examination of rows exhibit site fidelity (Post 1974; S. S. Taylor, gonads upon dissection in the field). The tissues fi S. Woltmann, and P. C. Stouffer, unpublished were stored in liquid N2 in the eld and then data); thus, these discrete locations were deemed transferred to a 80°C freezer in the laboratory.

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We collected sediment, primary producer, and operating at 350°C. Hydrogen was used as car- all invertebrate species in April, May, and June of rier gas flowing at 1.25 mL/min for 14 min and 2013 and 2014. Live S. alterniflora, Juncus roemari- ramped to 2.5 mL/min for 5 min. The split/split- anus, and Distichlis spicata plants were sampled less injector was heated to 260°C and run in split- by clipping them at ground level. Sediment less mode. The oven program was as follows: samples were collected as a composite sample of 60°C for 0.66 min; 22.82°C/min to 165°C with a the upper 1–2 cm to serve as a proxy for the 1.97-min hold; 4.56°C/min to 174°C and 7.61°C/ microphytobenthos/detrital pathway. Inverte- min to 200°C with a 6-min hold. The FA stan- brate species common to the saltmarsh were dards were obtained from Supelco (37 compo- opportunistically collected by hand and frozen in nent mix) and Nuchek (54 component mix). the field. These included fiddler crabs (Ocypodi- A known quantity of an internal standard dae), oval snails (Ellobiidae), periwinkles (Lit- (a-cholestane; Sigma 170 #C-8003) was added to torinidae), and ribbed mussels (Mytilidae). each sample prior to extraction to provide an Terrestrial arthropods were sampled using estimate of extraction efficiency. Seventy-three sweep nets along a linear transect from the edge FAME were identified using Agilent Technolo- of the marsh to 20 m inland (20 9 2 9 2 m for a gies ChemStation software via retention time total of 80 m2; Bam 2015). The collected terres- and known standard mixtures, and are reported trial arthropods were transferred into 3.7-L as the percentage of total FA (% TFA). Each FA is plastic zipper bags containing 95% ethanol. Ter- described using the shorthand nomenclature of restrial arthropods were classified to order and A:Bn-X, where A represents the number of car- family using taxonomic keys and the morphos- bon atoms, B represents the number of double pecies approach (see Bam 2015 and references bonds, and X represents the position of the dou- therein, including Triplehorn and Johnson 2005, ble bond closest to the terminal methyl group. In Wimp et al. 2010, Pennings et al. 2011). Domi- addition to individual FA, we also present results nant terrestrial arthropod taxa collected included as ΣSFA (saturated FA) to indicate the sum of all orders Heteroptera, Diptera, Orthoptera, Ara- FA with zero double bonds, ΣMUFA (monoun- neae, and Thysanoptera. We selected a subset of saturated FA) to indicate the sum of all FA with taxa representing a range of the feeding guilds one double bond, and ΣPUFA (polyunsaturated that were most abundant on our plots for further FA) to indicate the sum of all FA with ≥2 double isotopic analysis, including planthoppers (Del- bonds. We included Σn-3 PUFA, Σn-6 PUFA, and phacidae), mirid bugs (Miridae), striped flies the Σn-3/Σn-6 ratio to provide semi-quantitative (Ulidiidae), crickets (Orthoptera), coccinellid indices of aquatic vs. terrestrial FA sources beetles (Coccinellidae), spiders (Araneae), dam- (Hebert et al. 2008, Paterson et al. 2014, Hixson selflies and dragonflies (Odonata), and wasps et al. 2015). (Hymenoptera). All species were collected from Plant leaves were cleaned of foreign debris and both the oiled and unoiled plots. rinsed with distilled water before SI analysis. Ethanol was evaporated from terrestrial arthro- Tracer analyses pod samples in a hood for 48 h. Multiple individ- Seaside Sparrow FA profiles were quantified uals (2–10) from each arthropod taxon were using a three-step procedure: (1) triplicate pooled to obtain an adequate sample mass for the extractions of freeze-dried liver tissue in a 2:1 SI analysis. The snails, crabs, and mollusks were chloroform/methanol solution for gravimetric dissected and muscle tissue samples processed. determination of the total lipid (Folch et al. Liver tissue samples from Seaside Sparrows that 1957); (2) derivatization of FA methyl esters remained following FA extractions were used for (FAME) using sulfuric acid in methanol (1:100 SI analysis. Therefore, all bird tissues were lipid- mixture; Morrison and Smith 1964, Christie extracted before SI analysis. All tissue samples 1989); and (3) identification and quantification of were dried, ground to a fine powder, and FAME on an Agilent Technologies 7890N gas weighed into tin caps (0.5–1.0 mg), and the rela- chromatograph equipped with a 30-m J and W tive abundance of carbon (13C/12C) and nitrogen DB-23 column (0.25 mm I.D; 0.15 lm film thick- (15N/14N) was determined on a Thermo Finnigan ness), coupled to a flame ionization detector DeltaPlus mass spectrometer (Thermo Finnigan,

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San Jose, California, USA) coupled with an ele- because the TP is being estimated relative to pri- mental analyzer (Costech, Valencia, California, mary consumers rather than to primary produc- USA). Analytical accuracy was 0.06&,0.05&, ers (Vander Zanden et al. 2000). and 0.06& for d15N data based on National Insti- All statistical analyses were completed using the tute of Standards and Technology (NIST) stan- R statistical program (version 3.2.4, R Development dards 8573, 8548, and 8549, and 0.09& and 0.04& Core Team 2016). Before all analyses, we evalu- for d13C data based on NIST standards 8542 and ated data for normality (probability plots) and 8573, respectively. The analytical precision based homoscedasticity (boxplots). The relationships on the standard deviation of two standards (NIST between treatment (oiled and unoiled) and the bovine liver and fish muscle laboratory standard) year of the SI values for invertebrate taxa were for d15N was 0.15& and 0.11&, and for d13C analyzed with a factorial analysis of variance 0.09& and 0.07&, respectively. (ANOVA) followed by Tukey’s honest significant difference test with Bonferroni-adjusted P-values Data analysis (a = 0.01) for significant ANOVA results. We used trophic position (TP) to evaluate the We used a principal component analysis [PCA; trophic structure of the terrestrial saltmarsh food package vegan in R (Oksanen et al. 2016)] to web. When consumers potentially acquire investigate patterns in Seaside Sparrow FA pro- resources from more than one food web, each files. The data were obtained for 73 individual with a separate set of primary producers or detri- FAs, but the analyses were restricted to 13 FAs tal sources (e.g., species that feed on both terres- contributing to ≥1% of the total FA. Together, trial and aquatic food webs), the estimates of TP these 13 FAs accounted for 93% of the total liver must account for the potential spatial heterogene- FA of Seaside Sparrow. The sum proportions of ity at the base of the respective food webs. The saturated FA (ΣSFA), mono- (ΣMUFA), and primary consumers are temporally and spatially polyunsaturated FA (ΣPUFA), and aquatic less variable in their d13C than primary producers (Σn-3)/terrestrial (Σn-6) marker ratios were also (Vander Zanden et al. 1998), and are considered included in ordinations. We applied a logit trans- useful integrators of this potential variability in formation (Warton and Hui 2011) before analysis the TP estimate. We used the mean d15N and d13C to stabilize the normality and variance of the pro- values of primary consumers (i.e., assumed to portional data. All FA data were standardized to occupy TP = 2) of S. alterniflora (terrestrial: Del- a mean of zero and unit variance before inclusion phacidae, d15N = 4.8&; d13C = 12.4%) and of in the PCA. Fatty acid variable weights were microphytobenthos/detritus (aquatic: Ocypodi- extracted unscaled (i.e., scaling = 0) from the first dae, d15N = 4.7&; d13C = 18.1%) as the isotopic two principal components (PC), and the FA load- end-members for calculations of TP (Post 2002): ings on each component were calculated by mul- 0 1 tiplying the unscaled FA weight by the square 15 15 d NConsumer ½d NAquatic a B C root of the eigenvalue for that PC (McGarigal B þ d15 ð aÞ C ¼ þ NTerrestrial 1 and Cushman 2000). Fatty acids with loadings TP 2 B C ≥ fl @ Dd15N A 0.750 were considered in uential to that component (McGarigal and Cushman 2000). A linear mixed-effects model analysis was fit !using the restricted maximum likelihood (package d13 Dd13 d13 CConsumer C CAquatic a ¼ , lme4 in R; Pinheiro et al. 2017) to evaluate the ðd13 d13 Þ fi CTerrstral CAquatic relationships between SI values and FA pro les of the Seaside Sparrows, and the treatment (oiled where D15N and Δ13C represent d15N and d13C and unoiled) and year. The models included the trophic discrimination factors, respectively. The treatment and year as fixed effects, and the plot trophic discrimination factors for d15N were 3.0% and sex as random effects, because all plots were for all species, and 0.5& and 0.8& for d13Cof not sampled annually and both sexes were not Seaside Sparrows and invertebrates, respectively sampled at each plot. An examination of the prob- (Oelbermann and Scheu 2002, Kempster et al. ability plots of residuals from the models relating 2007, Bartrons et al. 2015). The +2 term is added tracer profiles to the treatment and year indicated

❖ www.esajournals.org 6 July 2017 ❖ Volume 8(7) ❖ Article e01878 OLIN ET AL. that the models fit adequately. Quantile–quantile RESULTS plots showed data to be generally described by normally distributed errors. P-values were Stable isotope values of the primary con- obtained by likelihood ratio tests followed by sumers (Delphacidae and Ocypodidae) did not pairwise comparisons (package “multcomp” in R; differ among years or between oiled and unoiled Hothorn et al. 2008) with adjusted P-values when plots (Table 1). Factorial ANOVAs indicated that asignificant result was observed. The confidence there were significant spatial differences for the intervals (95%; CI) were calculated to evaluate the d15N values of Littorinidae and for the d13C val- effects, with non-overlapping values considered ues of Littorinidae and Mytilidae (Table 1). to represent significant differences. Linear regres- Specifically, the d15N values of Littorinidae were sions were then used to examine the relationship lower in samples collected from oiled plots, between d15Nandd13C, and the ratio of Σn-3 to whereas the d13C values for Littorinidae and Σn-6, to document any shift between terrestrial Mytilidae were higher in samples from oiled and aquatic sources. plots. ANOVA results also indicated that there

Table 1. Stable isotope values and trophic position (TP) estimates (mean 1 SD) of the dominant primary producers, and the terrestrial arthropod and saltmarsh invertebrate taxa sampled from the Port Sulphur area of Barataria Bay, Louisiana, USA.

Oiled Unoiled Order/Family/Species Year n d13C(&) d15N(&) n d13C(&) d15N(&) TP

Spartina alterniflora Combined 3 12.8 0.1 3.7 0.2 3 12.9 0.2 4.1 0.2 Distichlis spicata Combined 3 13.7 0.1 3.9 0.1 3 13.7 0.1 3.8 0.1 Juncus roemerianus Combined 3 29.5 0.6 2.5 0.6 3 28.1 0.7 3.0 0.4 Sediment Combined 3 17.9 2.0 1.9 0.4 3 18.6 1.5 1.6 0.2 Delphacidae (Leaf hopper spp.) 2013 11 12.4 0.5 5.0 0.7 8 12.7 0.4 4.9 0.6 2.0 0.2 2014 8 12.3 0.8 4.4 0.4 6 12.1 0.4 4.7 0.4 Miridae (Leaf bug spp.) 2013 11 12.0 0.2 6.0 0.6 8 12.2 0.3 6.1 0.4 2.3 0.2 2014 11 11.8 0.3 5.2 0.6 8 11.9 0.4 6.0 0.5 Odonata (Dragon fly spp.) 2013 3 20.2 1.0 6.6 0.7 2 17.9, 18.5 6.5, 7.4 2.5 0.2 2014 5 18.6 0.4 5.8 0.5 4 19.0 0.7 6.0 0.5 Orthoptera (Cricket spp.) 2013 7 13.4 0.9 7.4 0.7a 1 15.1 6.9a 2.6 0.3 2014 13 14.7 1.5 6.1 0.6b 9 15.0 1.5 6.1 0.5b Ulidiidae (Striped fly spp.) 2013 9 13.8 0.6a 7.5 0.6 6 13.6 0.3a 7.8 0.3 3.0 0.2 2014 12 13.1 0.3b 7.9 0.7 8 13.1 0.3b 8.3 0.7 Araneae (Spider spp.) 2013 18 15.2 1.0 7.9 0.7 12 15.5 1.2 7.7 0.8 3.0 0.2 2014 11 14.6 1.2 7.8 0.6 9 15.8 1.5 7.6 0.5 Hymenoptera (Wasp spp.) 2013 –– ––3.1 0.3 2014 10 12.7 0.3 7.9 0.8 8 13.1 0.4 8.2 0.9 Odonata (Damsel fly spp.) 2013 ––1 17.2 7.0 3.2 0.4 2014 6 19.0 1.6 7.7 1.0 8 17.2 0.1 9.7 0.1 Coccinellidae (Beetle spp.) 2013 7 13.7 0.6 8.5 1.1 2 13.8, 14.2 9.3, 8.9 3.4 0.3 2014 11 13.7 1.0 9.2 0.8 3 14.2 1.0 8.9 0.5 Ellobiidae (Marsh snail spp.) 2013 4 14.8 1.6 4.2 0.9 3 16.0 1.9 4.3 0.5 1.9 0.2 2014 6 14.6 1.3 4.4 0.5 2 17.1, 17.7 4.8, 4.7 Ocypodidae (Fiddler crab spp.) 2013 6 17.6 0.7 4.2 0.9 7 18.1 0.8 5.3 1.2 2.0 0.3 2014 6 18.4 0.7 4.6 0.7 4 18.3 0.6 4.6 0.5 Littorinidae (Periwinkle spp.) 2013 22 13.8 1.2A 6.1 0.8 22 15.6 1.6B 6.5 0.6 2.5 0.2 2014 13 14.4 1.9 5.8 0.3A 8 15.6 1.7 7.0 0.4B Mytilidae (Ribbed mussel spp.) 2013 20 23.2 1.0a,A 7.4 0.3 18 24.3 0.5a,B 7.5 0.4 2.0 0.2 2014 8 24.6 0.5b 7.4 0.7 9 25.0 0.7b 7.4 0.7 Notes: n represents pooled individuals (2–10) to obtain adequate sample. Lowercase and capital letter superscripts indicate significant year and oil status differences for each species, respectively, at P = 0.01. TP estimates are combined across year and oil status.

❖ www.esajournals.org 7 July 2017 ❖ Volume 8(7) ❖ Article e01878 OLIN ET AL. were significant temporal differences between in 2013 had lower TP (~3.5 0.2) than in other the 2013 and 2014 samples for the d15N values of years (~3.8 0.2). Orthoptera, and between the d13C values of The major FAs detected in Seaside Sparrow Ulidiidae and Mytilidae, with opposite patterns liver tissues included 16:0, 18:0, 18:1n-9, 18:2n-6, being exhibited by the taxa for each isotope 20:4n-6, and 22:6n-3 (Table 2). Seaside Sparrows (Table 1). were characterized by high levels of 16:0 and Individual SI values for all Seaside Sparrow 18:0, with SFA representing approximately 40% liver tissues ranged between 11.4 and 16.7& of sum FAs. Polyunsaturated FAs were also pre- for d13C and between 8.4 and 11.6& for d15N sent in large proportions (>30%), followed by (Table 2). Birds had similar d13C(mean SD: MUFA (~20%; Table 2). Fatty acid compounds, 13.3 1.1& and 13.4 1.4&)andd15N such as 20:4n-6, 20:5n-3, and 22:6n-3, and marker (9.7 0.7&;9.8 0.7&) values at oiled and ratios, including Σn-3, Σn-3/Σn-6, and ΣPUFA, unoiled plots, and we found no statistical differ- were strongly positively correlated with the first ence in the SI values of these individuals (d13C: principal component (PC1; Fig. 3A). In contrast, v2 = 0.238, P = 0.627; d15N: v2 = 0.255, P = 0.613; the 18:1n-9 and ΣMUFA were strongly and nega- Fig. 2). Seaside Sparrow d13C values were also tively correlated with PC1 (Fig. 3A). Fatty acid not significantly affected by year (v2 = 5.686, compounds including 16:1n-7, 18:1n-7, 22:5n-3, P = 0.068; Fig. 2). In contrast, year was a signifi- and Σn-3/Σn-6 were strongly correlated with the cant factor for Seaside Sparrow d15N values second principal component (PC2) in the positive (v2 = 32.497, P < 0.01), with birds sampled in direction, whereas FA 18:0, Σn-6, and 18:2n-6 2013 having notably lower d15N values relative to were strongly correlated in the negative direction birds sampled in other years by ~0.9 0.2& on PC2 (Fig. 3A). The two axes accounted for a (Fig. 2). Moreover, based on TP calculations, birds combined 72.5% of the total variance.

Table 2. Stable isotope (&; mean 1 SD) and fatty acid proportions (% TFA) for liver tissues of Seaside Spar- rows sampled from the Port Sulphur area of Barataria Bay, Louisiana, USA.

2011 2012 2013 2014 Tracer Oiled Unoiled Oiled Unoiled Oiled Unoiled Oiled Unoiled n 55881012711 d13C 13.9 0.7 12.9 0.7 12.2 0.6 13.0 0.9 13.6 1.2 13.8 1.7 13.8 0.8 13.5 1.6 d15N 10.4 0.5 10.6 0.6 10.1 0.6 10.2 0.6 9.2 0.5 9.3 0.6 10.0 0.8 9.9 0.4 14:0 0.3 0.1 0.8 0.3 0.6 0.3 0.3 0.1 0.5 0.2 0.6 0.2 0.3 0.1 0.4 0.2 16:0 20.9 1.3 25.7 2.7 21.9 2.6 21.6 2.7 22.0 1.8 21.8 1.6 20.1 1.6 20.3 2.5 16:1n-7 2.3 0.6 2.2 0.9 4.2 1.5 2.6 1.1 6.0 3.1 4.8 1.7 3.3 2.2 2.0 0.7 17:0 0.6 0.2 0.6 0.2 0.6 0.1 0.8 0.1 0.7 0.3 0.8 0.3 0.6 0.2 0.7 0.3 18:0 17.9 3.3 18.2 1.8 17.2 2.0 18.6 1.8 15.8 2.1 15.6 2.1 17.9 1.7 19.3 2.5 18:1n-9 17.2 4.5 15.1 1.5 19.6 2.7 16.1 2.2 13.1 5.4 14.5 7.2 16.5 4.9 13.0 4.9 18:1n-7 1.8 0.2 1.3 0.3 1.7 0.3 2.1 0.3 2.6 0.7 2.5 0.7 1.8 0.5 1.8 0.4 18:2n-6 9.4 0.8 9.7 1.8 8.8 1.3 8.3 2.1 7.2 1.4 8.3 1.7 10.1 2.4 11.3 1.3 18:3n-3 0.5 0.4 0.4 0.3 0.7 0.2 0.6 0.5 0.4 0.3 0.5 0.6 0.7 0.5 0.8 0.4 20:4n-6 8.3 2.4 8.7 1.7 9.3 1.8 9.5 3.7 9.1 2.4 8.4 2.0 9.7 2.5 10.2 1.7 20:5n-3 0.5 0.2 0.8 0.3 0.9 0.3 0.6 0.3 1.6 0.5 1.9 0.7 0.9 0.3 0.8 0.2 22:5n-3 0.7 0.3 1.2 0.3 1.2 0.2 1.3 0.5 2.1 0.5 2.3 0.6 1.5 0.6 1.4 0.2 22:6n-3 7.6 3.6 6.8 1.2 6.9 2.1 8.2 3.2 14.9 3.9 12.5 3.7 9.8 2.7 10.6 1.6 Σn-3 12.1 2.8 11.1 0.9 11.3 1.8 13.9 1.7 19.3 3.7 17.6 4.2 13.9 2.8 14.6 1.4 Σn-6 19.2 2.8 19.8 3.1 19.2 2.2 19.2 4.2 17.2 3.4 17.7 2.8 20.9 3.0 22.8 3.0 Σn-3/n-6 0.6 0.1 0.6 0.1 0.6 0.1 0.8 0.2 1.1 0.2 1.0 0.3 0.7 0.1 0.6 0.1 ΣSFA 41.3 2.6 46.8 2.2 41.7 3.7 42.6 4.0 40.1 2.6 40.4 2.3 40.5 1.6 42.0 3.9 ΣMUFA 23.3 5.7 20.1 2.6 27.3 3.3 22.8 2.8 22.7 8.0 23.4 6.8 23.2 5.9 18.9 4.7 ΣPUFA 31.8 5.3 31.3 2.6 30.8 3.6 33.5 5.2 37.0 6.6 36.0 5.3 35.1 5.0 37.6 3.4 Notes: SFA, saturated fatty acid; MUFA, monounsaturated fatty acid; PUFA, polyunsaturated fatty acid. Only 13 (of 73) of the most abundant fatty acids are shown.

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Fig. 2. Biplot of d13C and d15N values for liver tissues of Seaside Sparrows (triangles) and saltmarsh taxa (pooled among plots and years; mean SD; see Table 1) from Port Sulphur, Barataria Bay, Louisiana. Bird stable isotopes values are diet tissue discrimination factor-corrected following Kempster et al. (2007).

The PCA of liver proportional FA data and mar- FA profiles of Seaside Sparrow on PC2. However, ker ratios provided clear separation of Seaside year (v2 = 6.543, P < 0.01) was a significant Sparrows collected among years (Fig. 3). Birds col- predictor, with pairwise comparisons indicating lected in 2013 scored in the positive direction of that the FA profiles of 2013 birds were differ- both PC1 and PC2, with birds collected in 2011 ent from all other years (Fig. 3B). Birds col- generally scoring in the negative direction along lected in 2013 had significantly lower values of these same axes (Fig. 3B). Birds sampled in 2011, terrestrial-derived FA, including 18:2n-6 and Σn-6, 2012, and 2014 exhibited a greater degree of over- and higher values of FA considered to represent lap of FA profiles relative to birds collected in an increasing importance of benthic-associated 2013, which were distinctly separated (Fig. 3B). habitats, including 16:1n-7 and 18:1n-7, relative to Year (v2 = 10.366, P < 0.01) was a significant pre- other years (Fig. 5). Liver tissue d15N values were dictor of Seaside Sparrow FA profiles on PC1, with inversely related to Σn-3/Σn-6 ratios (Fig. 6A). Rel- pairwise comparisons indicating that 2011 and ative to other years, birds collected in 2013 had 2012 were significantly different from 2013 and higher ratios at lower d15N values. Similarly, liver 2014. Birds sampled in 2013 and 2014 were gener- tissue d13C values were inversely related to Σn-3/ ally characterized by a higher proportion of Σn-6 ratios (Fig. 6B), with birds sampled in 2013 20:5n-3, 22:6n-3, Σn-3, and ΣPUFA (Fig. 4), sug- having higher ratios at lower d13Cvalues,though gesting higher contributions of aquatic resources this relationship was weak. relative to other years. Birds collected in 2013 and 2014 also showed lower amounts of 18:1n-9. Rela- DISCUSSION tive to year, neither the treatment (v2 = 3.363, P = 0.07) nor the interaction term of year 9 treat- Gulf of Mexico coastal saltmarsh is among the ment (v2 = 5.715, P = 0.06) was identified as a world’s most productive and valuable ecosys- significant predictor of the FA profiles of Seaside tems (Batker et al. 2010); as such, understanding Sparrows on PC1. Treatment (v2 = 0.088, the effects of large-scale disturbances is critical P = 0.766) was also not a significant predictor of for developing successful strategies aimed at

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invertebrate populations, few studies have focused on assessing the consequences to the food web. Our comparison of trophic relationships between terrestrial saltmarsh consumers that experienced different oil exposure indicated that the DWH oil spill resulted in subtle differences in the saltmarsh food web from the per- spective of energy transfer from producers to higher trophic levels. In contrast, significant temporal variation in resource use by Seaside Spar- rows did not appear to coincide with trophic changes in the broader food web. Characterizing the trophic response of organisms to changes in their environment is important for understanding food web dynamics in these habitats and for predicting future ecological responses to stressors. We found that saltmarsh consumers, in general, obtained the majority of their energy from C4 plant-based pathways, rather than from either C3 plant or phytoplankton-based pathways, thus confirming that Spartina alterniflora is an important energetic source for the GOM terrestrial saltmarsh food web. Carbon sourced from plants using the C4 photosynthetic process is enriched in 13C(d13C range: 6& to 15&) relative to car- d13 bon sourced from the C3 process ( C range: 24& to 30&; Moncreiff and Sullivan 2001, Winemiller et al. 2007). The mirid and delphacid bugs, represent consumers that were most reliant on C4 plant-derived energy, consistent with their Fig. 3. (A) Ordination of fatty acid (FA) proportions affinity for S. alterniflora (Denno et al. 2002, (% TFA) and marker ratios and (B) principal compo- Wimp et al. 2010). More mobile consumers, such > fi nent (PC) loadings ( 0.75) quanti ed in Seaside as the Odonata and ocypodid crabs, represented – Sparrows collected in 2011 2014 from Port Sulphur, the saltmarsh consumers that were most reliant Barataria Bay, Louisiana. Ellipses represent the 95% on aquatically derived energy—most likely via fi fi con dence regions for the FA pro les for each year, benthic algal and detrital pathways (d13C range: and total variance explained by each PC is included 18& to 20& Galvan et al. 2008, 2011)—with with axis labels. the potential to transport aquatic-derived energy into the terrestrial landscape. Across all taxa, maintaining these productive habitats. The the saltmarsh consumers obtained greater ener- DWH oil spill directly affected coastal habitats getic contributions from benthic algal and detri- causing, for example, immediate animal mortal- tal pathways than from either phytoplankton or ity and losses of ecosystem services (e.g., Carmi- C3 pathways. chael et al. 2012, Mendelssohn et al. 2012), as The patterns of variation in d15N values con- well as longer-lasting effects such as persistence formed to the expected trophic differentiation of oil-derived compounds (e.g., McClenachan among species groups in the terrestrial saltmarsh et al. 2013, Turner et al. 2014b). Despite wide- food web. Generally, families consisting largely spread concern for coastal saltmarsh in the after- of primary consumers, including herbivores math of the DWH oil spill, with the exception of (Delphacidae and Miridae) and detritivores the noted effects on marsh vegetation and (Ocypodidae and Ellobiidae), had low d15N

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Fig. 4. Fatty acid proportions (% TFA [mean 95% CI]) of (A) 18:1n-9, (B) monounsaturated fatty acid (ΣMUFA), (C) 22:6n-3, (D) Σn-3, (E) 20:5n-3, and (F) polyunsaturated fatty acid (ΣPUFA) of Seaside Sparrows collected in 2011–2014 from Port Sulphur, Barataria Bay, Louisiana. These fatty acid proportions reflect those that strongly correlated with the PC1 axis in Fig. 3A. Fatty acids are color-coded based on terrestrial vs. benthic– aquatic indicators as follows: terrestrial—green; benthic–aquatic—blue; ubiquitous—white. values compared to arthropod groups containing did not result in a trophic-level shift, nor were carnivores, specifically Odonata, Coccinellidae, these changes evident in higher trophic-level spe- and Araneae. These primary consumers had SI cies, supporting the limited trophic effects of these values that did not vary spatially or temporally, factors on the flow of energy through this food suggesting that the energy available at the base web. Further, the lack of significant variation in SI of the food web remained stable throughout values for primary consumers among years and our study. There were significant temporal and plots suggests that the differences observed in the spatial differences in the d15N values of intermedi- SI values of the secondary consumers were not a ate consumers. Orthopterans, for example, had result of changes in available energy, but likely higher d15N values in 2013 compared to in 2014, reflect availability of specific prey. Ascertaining and the littorinid snails showed higher d15N val- the exact response of saltmarsh consumers to the ues at unoiled sites relative to oiled sites. Notably, DWH is challenging due to the lack of baseline the littorinid snails have been designated as data prior to the spill, as well as the potential time highly sensitive to oil and of high food web lag between post-spill die-offs and ecosystem importance (i.e., serve as prey resource to many effects (Rabalais and Turner 2016). However, our species) to the broader saltmarsh food web comparison of saltmarsh consumers on oiled and (McCann et al. 2017). While changes in the d15N unoiled plots did show effects from the oil on con- values of these consumers were significant, they sumers, albeit to a limited extent, even two years

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Fig. 5. Fatty acid proportions (% TFA [mean 95% CI]) of (A) 16:1n-7, (B) 22:5n-3, (C) 18:1n-7, (D) 18:0, (E) 18:2n-6, and (F) Σn-6 of Seaside Sparrows collected in 2011–2014 from Port Sulphur, Barataria Bay, Louisiana. These fatty acid proportions reflect those that strongly correlated with the PC2 axis in Fig. 3A. Fatty acids are color-coded based on terrestrial vs. benthic–aquatic indicators as follows: terrestrial—green; benthic–aquatic— blue; ubiquitous—white. after the oil landed. Tracking energy pathways in nearly one year after oil landfall) when saltmarsh coastal systems will aid in the interpretation of invertebrate consumers showed some recovery in DWH impact studies and will—perhaps more oiled habitats (McCall and Pennings 2012). Even importantly—contribute to a new understanding so, a number of studies provide contrasting of baseline GOM ecosystem functioning, so that accounts of the recovery of invertebrate popula- future disturbances can be understood more thor- tions following the spill (including Bam 2015, oughly than at present. Fleeger et al. 2015, Husseneder et al. 2016, Zengel The absence of significant differences in tracer et al. 2016a, b). The lack of continuous population profiles of Seaside Sparrows from oiled and data for invertebrate saltmarsh taxa from pre-spill unoiled saltmarsh is unexpected given the evi- years and from the years immediately following dence for reduced biomass of invertebrate prey (2011–2012) makes definitive conclusions regard- across oiled saltmarshes in Barataria Bay. Con- ing this point limited. Alternatively, it could be trary to our initial hypothesis that birds inhabit- argued that the unoiled plots in our study had ing oiled saltmarsh would consume different measurable amounts of petroleum on them or prey resources compared to conspecifics inhabit- experienced subsequent re-distribution of oil ing unoiled marshes, our data suggest similar following storm events which could have equiva- resource use among treatments. This finding may lently affected prey populations at these loca- reflect when this study began (August 2011— tions. However, no identifiable Macondo oil was

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indicates that despite oiling, birds used resources consistently among sites. We think that these findings reflect the heterogeneous distribution of oil across the marsh, because some areas experienced little or no oiling, while others were heavily oiled (Michel et al. 2013). Oil from the DWH was deposited most heavily along the seaward edge of marsh and bulk oiling typically spread into the marsh no more than ~10–15 m perpendicular to the edge due in part to the small tidal range (~0.5 m), although oil did extend further into the marsh in some areas (~100 m; Lin and Mendelssohn 2012, Silliman et al. 2012, Michel et al. 2013, Zengel et al. 2015). Oil concentrations measured at 1, 10, and 100 m from the marsh edge did not differ (Turner et al. 2014a), yet invertebrate population estimates generally were quantified in the areas proximate to, and including, the marsh edge (McCall and Pennings 2012, Bam 2015, Fleeger et al. 2015, Husseneder et al. 2016, Zengel et al. 2016a, b). As such, the consideration that Seaside Sparrows foraged on adjacent areas while nest- ing is a plausible conclusion. Seaside Sparrows have been observed to move fairly large distances (3+ km; Post 1974; Woltmann et al., unpublished data), which is greater than the width of our plots. However, birds occupied and nested in the designated plots after the spill (Stouffer et al. 2013), and telemetry data from radio-tagged Fig. 6. Relationship between the ratio of Σn-3 to individuals in 2012 indicate average ( SE) home ~ Σn-6 and (A) d15N and (B) d13C values from the liver range sizes of 1 0.25 ha (Woltmann et al., un- tissues of Seaside Sparrows collected in 2011–2014 published data), suggesting that birds, in this case, fi from Port Sulphur, Barataria Bay, Louisiana. were relatively con ned spatially on the marsh and were not traveling long distances. Moreover, detected on unoiled plots (Turner et al. 2014b), the high metabolic rate of liver results in the and while the baseline conditions at these sites rapid turnover of dietary tracers in that tissue, were not pristine, the 2010 oiling event raised the providing short-term dietary information (~one average concentration of alkanes and polycyclic week; Hobson and Clark 1992, Kelly and Scheib- aromatic hydrocarbons (PAHs) in the oiled wet- ling 2012, Vander Zanden et al. 2015). Therefore, land sediments by 604 and 186 times, respectively the heterogeneous deposition of oil in the marsh (Turner et al. 2014b). Moreover, the lack of relative to the total marsh surface, to a certain reported reductions in invertebrate biomass on degree, may have limited the direct negative unoiled plots does not support this explanation. effects on these birds and other saltmarsh taxa. Despite occurring at lower densities on oiled Significant changes to tracer profiles of Seaside plots (S. Woltman, S. S. Taylor, P. C. Stouffer, Sparrows demonstrate a temporal effect on the unpublished data), birds appear to be using similar resource use by this species across all plots. resources, and our data do not support a shift in Specifically, the tracer profiles of birds sampled resource use as a consequence of oiling. More- in 2013 were markedly different from those in over, the limited differentiation in SI values of birds sampled in all other years. A likely expla- saltmarsh taxa buoys this contention and nation for this response is Hurricane Isaac, a

❖ www.esajournals.org 13 July 2017 ❖ Volume 8(7) ❖ Article e01878 OLIN ET AL. category-1 storm that made landfall in Plaquemi- such as benthic diatoms and dinoflagellates, can nes Parish, Louisiana, in late August of 2012. In make 20:5n-3 and 22:6n-3, but terrestrial plants contrast to the heterogeneous deposition of oil make 18-carbon PUFA (Richoux and Froneman from the DWH, the storm surge from this land- 2008, Kelly and Scheibling 2012), and species asso- scape-level event inundated Barataria Bay salt- ciated with aquatic food webs would be expected marsh with 1–4 m of water for ~2–3 d. Flooding to have higher proportions of these FAs than ter- together with the high winds and heavy rains restrial species (Hebert et al. 2008, Koussoroplis that accompanied this storm may have killed or et al. 2008). Indeed, terrestrial insects have low forced organisms to seek refuge elsewhere. For concentrations of 20:5n-3 and 22:6n-3 in their tis- example, it was estimated that ~400,000 Seaside sues (Uscian and Stanley-Samuelson 1994, Sparrows were displaced (Stouffer et al. 2013). Howard and Stanley-Samuelson 1996). Thus, the Dry land along the Mississippi River levee was marked increase in the proportions of n-3 FA in 5–15 km from our study plots and larger areas of SeasideSparrowtissues,andthenegativecorrela- dry marsh required movements of 50–100 km tion between d13CandΣn-3/Σn-6 ratios, is consis- (Stouffer et al. 2013), thus limiting the capacity tent with reduced incorporation of terrestrial- for many species to escape the inundation. The basedproductioninthedietofbirdsin2013.Con- arthropod communities quantified in 2013 and comitantly, birds sampled in 2013 relative to other 2014 differed, with significantly lower abun- years had higher proportions of 18:1n-7, a FA char- dance of species from groups including Odonata, acteristic of bacteria (Kelly and Scheibling 2012), Orthoptera, Pompilidae, Formicidae, and Culi- and of 16:1n-7, a FA characteristic of diatoms coidea reported on our plots in 2013 (Bam 2015). (Kelly and Scheibling 2012). Collectively, the shifts Such hurricane effects decimated arthropod in the relative proportions of terrestrial vs. aquatic populations on Bahamian islands, specifically biomarkers, and the increase in benthic-derived spiders and Hymenopteran parasitoids, and FA in the diet of these birds, support an increased population recovery was not observed for nearly reliance on prey resources derived from a different two years after the event (Spiller and Schoener food web in 2013. The shift between terrestrial and 2007). Notably, tracer profiles of birds sampled in aquatic resources by these birds suggests trophic 2011, 2012, and 2014 did not differ, supporting plasticity, a mechanism that may allow this species an effect of Hurricane Isaac on these populations to thrive in highly dynamic environments. that scaled to higher trophic levels. The similarity The significant temporal variation in resource in tracer profiles between these years could indi- use by Seaside Sparrows did not appear to coin- cate a recovery of prey populations one year after cide with the structural changes in the broader Hurricane Isaac, suggesting a limited timeline for food web, suggesting a systemic change in prey the impacts from this stressor. Yet, this large- availability. Based on a visual evaluation of the scale disturbance, in contrast to the DWH, may SI values of the saltmarsh food web (Fig. 2), the have greater implications for the Seaside Spar- birds appeared to feed more broadly and on row, as a landscape-level reduction in available lower trophic-level prey in 2013 compared with prey could increase bird competition for shared all other years. The change in diet in birds sam- resources, decreasing foraging time and nest suc- pled in 2013 is reflective of a trophic shift, cess (Woodrey et al. 2012, Kern and Shriver whereby increased reliance on aquatic resources 2014), warranting further evaluation. (e.g., higher Σn-3/Σn-6 ratios) was correlated with Seaside Sparrows relied predominately on lower d15N values. This trophic shift is supported — C4-based production, which is consistent with by the lower proportions of 18:1n-9 a FA con- their habitat preference for S. alterniflora saltmarsh sidered to be an indication of carnivory (Dals- (Rush et al. 2009). However, birds sampled in gaard et al. 2003, Kelly and Scheibling 2012)— 2013 exhibited a departure in d13C values toward quantified in birds sampled in 2013. The differ- benthic algae. In addition, significantly lower ences in tracer profiles of these birds, coupled proportions of terrestrial-derived FA including with the significant differences between the 18:2n-6 and Σn-6, and higher proportions of arthropod communities quantified in 2013 and aquatic-derived FA, including 20:5n-3 and 22:6n-3, 2014 (Bam 2015), support the contention that Sea- were quantified in their liver tissues. Marine algae, side Sparrows exhibit trophic generalism when

❖ www.esajournals.org 14 July 2017 ❖ Volume 8(7) ❖ Article e01878 OLIN ET AL. prey populations are compromised. However, but also strengthen their application as metrics of additional research is needed to quantify these saltmarsh integrity. relationships and to further investigate the relative influences of arthropod community compo- ACKNOWLEDGMENTS sition and disturbance on foraging behavior of mobile vertebrate consumers in saltmarsh We are grateful to F. Sheldon at the LSU Museum of ecosystems. Importantly, the differences in the Natural Science who collected Seaside Sparrow sam- fi quality of aquatic- vs. terrestrial-derived reso- ples in 2011. We thank T. Burkhard, R. Butter eld, urces will be a key avenue for future research to M. Duong, T. Halderson, M. Herse, A. Hussey, R. Leeson, provide further insight into the energetic link- E. Ospina, B. Rosenburg, M. Rumbach, L. Southcott, G. Tomy, J. Welklin, and S. Wheeler for field and labora- ages and how they affect growth, survival, and tory assistance. We are also grateful to two anonymous reproductive potential in this species. reviewers for their constructive comments. This research was made possible by a grant from the Gulf of CONCLUSIONS Mexico Research Initiative (GoMRI) to the Coastal Waters Consortium. Data are publicly available through Our findings contribute to the maturing under- the GoMRI Information & Data Cooperative (GRIIDC) standing of the energy pathways supporting food at https://data.gulfresearchinitiative.org (https://doi.org/ webs in the coastal saltmarsh landscape, and 10.7266/n7kk98p7, https://doi.org/10.7266/n7bv7dpq, illustrate the inherent complexity of understand- https://doi.org/10.7266/n7mc8x3b, https://doi.org/10.7266/ ing the effects of potential stressors in these sys- n7gm85df). The funding agency had no role in the tems. The impetus for this study was to quantify design, execution, or analyses associated with this project. The authors have no conflicts of interest. LHB, the effects of the DWH oil spill. However, assess- PCS, RET, SST, and SW designed the field survey; JAO ments of large-scale disturbances, such as those conceived the study; CMBB, JAO, SST, SW, and WB discussed here, are problematic because mea- collected the samples; JAO performed the statistical surements of post-disturbance conditions are analysis; JAO wrote the first draft of the manuscript; common, but measurements of pre-disturbance and CMBB, PCS, RET, SST, and SW substantially baselines are often rare. The data derived from contributed to revision. our comparative approach suggest that there was a subtle effect of oil on energy transfer LITERATURE CITED through the terrestrial saltmarsh food web, but highlight other factors, such as hurricanes, as Bam, W. 2015. Effects of oil spill and recovery of terres- potentially being more influential on these pro- trial arthropods in Louisiana saltmarsh ecosystem. cesses. These findings have greatly informed our Thesis. Louisiana State University, Baton Rouge, awareness of oil impacts, but have also high- Louisiana, USA. Bartrons, M., C. Gratton, B. J. Spiesman, and M. J. lighted the knowledge gaps in our understand- Vander Zanden. 2015. Taking the trophic bypass: ing of the effects of environmental stressors on Aquatic-terrestrial linkage reduces methylmercury these habitats and also on the baseline ecology of in a terrestrial food web. Ecological Applications these systems (e.g., population sizes, habitat use, 25:151–159. foraging strategies; Henkel et al. 2012). We Batker, D., I. de la Torre, R. Costanza, P. Swedeen, gained a greater understanding of the energy J. Day, R. Boumans, and K. Bagstad. 2010. Gaining flow and food web structure of GOM saltmarsh ground: wetlands, hurricanes, and the economy: communities through characterization of the the value of restoring the Mississippi River Delta. – trophic linkages across differentially stressed Environmental Law Reporter 40:11106 11110. habitats. As dynamic processes may be specific Bergeon Burns, C. M., J. A. Olin, S. Woltmann, P. C. to individual marshes, the extrapolation to, and Stouffer, and S. Taylor. 2014. Effects of oil on terrestrial vertebrates: predicting impacts of the Macondo comparisons of, the responses of saltmarsh con- blowout. BioScience 64:820–828. sumers to disturbance, even on a small geo- Blight, L. K. 2011. Egg production in a coastal seabird, graphic scale, should be approached with care the glaucous-winged gull (Larus glaucescens), decli- (Erwin et al. 2006). Yet, efforts such as these will nes during the last century. PLoS ONE 6:e22027. not only enhance predictions toward expected Blight, L. K., K. A. Hobson, T. K. Kyser, and P. Arcese. responses to future environmental conditions, 2015. Changing gull diet in a changing world: a

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