Marine Ecoregion and Deepwater Horizon Oil Spill Affect Recruitment and Population Structure of a Salt Marsh Snail 1, 2 3 4 5 6 STEVEN C

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Marine Ecoregion and Deepwater Horizon Oil Spill Affect Recruitment and Population Structure of a Salt Marsh Snail 1, 2 3 4 5 6 STEVEN C Marine ecoregion and Deepwater Horizon oil spill affect recruitment and population structure of a salt marsh snail 1, 2 3 4 5 6 STEVEN C. PENNINGS, SCOTT ZENGEL, JACOB OEHRIG, MERRYL ALBER, T. DALE BISHOP, DONALD R. DEIS, 7 8 9 10 DONNA DEVLIN, A. RANDALL HUGHES, JOHN J. HUTCHENS JR., WHITNEY M. KIEHN, 4 11 12 7 CAROLINE R. MCFARLIN, CLAY L. MONTAGUE, SEAN POWERS, C. EDWARD PROFFITT, 13 14 15 NICOLLE RUTHERFORD, CAMILLE L. STAGG, AND KEITH WALTERS 1Department of Biology and Biochemistry, University of Houston, Houston, Texas 77204 USA 2Research Planning, Inc. (RPI), Tallahassee, Florida 32303 USA 3NewFields, Atlanta, Georgia 30309 USA 4Department of Marine Sciences, University of Georgia, Athens, Georgia 30602 USA 5No Bones Coastal Biological Consultants, LLC, 1114 Hyatt Avenue, Murrells Inlet, South Carolina 29576 USA 6Atkins, Jacksonville, Florida 32256 USA 7Department of Biological Sciences, Harbor Branch Oceanographic Institution, Florida Atlantic University, 5600 U.S. 1 N, Fort Pierce, Florida 34946 USA 8Marine and Environmental Science, Northeastern University, Nahant, Massachusetts 01908 USA 9Department of Biology, Coastal Carolina University, PO Box 261954, Conway, South Carolina 29528 USA 10Tampa Bay Water, Clearwater, Florida 33761 USA 11Howard T. Odum Center For Wetlands, Department of Environmental Engineering Sciences, University of Florida, Gainesville, Florida 32611 USA 12Department of Marine Sciences, University of South Alabama, Mobile, Alabama 36688 USA 13Emergency Response Division, National Oceanic and Atmospheric Administration, Seattle, Washington 98115 USA 14U.S. Geological Survey, Wetland and Aquatic Research Center, Lafayette, Louisiana 70506 USA 15Department of Marine Science, Coastal Carolina University, PO Box 261954, Conway, South Carolina 29528 USA Citation: Pennings, S. C., S. Zengel, J. Oehrig, M. Alber, T. D. Bishop, D. R. Deis, D. Devlin, A. R. Hughes, J. J. Hutchens Jr., W. M. Kiehn, C. R. McFarlin, C. L. Montague, S. Powers, C. E. Proffitt, N. Rutherford, C. L. Stagg, and K. Walters. 2016. Marine ecoregion and Deepwater Horizon oil spill affect recruitment and population structure of a salt marsh snail. Ecosphere 7(12):e01588. 10.1002/ecs2.1588 Abstract. Marine species with planktonic larvae often have high spatial and temporal variation in recruitment that leads to subsequent variation in the ecology of benthic adults. Using a combination of published and unpublished data, we compared the population structure of the salt marsh snail, Littoraria irrorata, between the South Atlantic Bight and the Gulf Coast of the United States to infer geographic differ- ences in recruitment and to test the hypothesis that the Deepwater Horizon oil spill led to widespread recruitment failure of L. irrorata in Louisiana in 2010. Size-frequency distributions in both ecoregions were bimodal, with troughs in the distributions consistent with a transition from sub-adults to adults at ~13 mm in shell length as reported in the literature; however, adult snails reached larger sizes in the Gulf Coast. The ratio of sub-adults to adults was 1.5–2 times greater in the South Atlantic Bight than the Gulf Coast, consistent with higher recruitment rates in the South Atlantic Bight. Higher recruitment rates in the South Atlantic Bight could contribute to higher snail densities and reduced adult growth in this region. The ratio of sub-adults to adults in Louisiana was lower in 2011 than in previous years, and began to recover in 2012–2014, consistent with widespread recruitment failure in 2010, when large expanses of spilled oil were present in coastal waters. Our results reveal an important difference in the ecology of a key salt marsh invertebrate between the two ecoregions, and also suggest that the Deepwater Horizon oil spill may have caused widespread recruitment failure in this species and perhaps others with similar planktonic larval stages. Key words: biogeography; BP Deepwater Horizon; gastropod; Littoraria; marine invertebrate; oil spill; population structure; recruitment; salt marsh; Spartina. ❖ www.esajournals.org 1 December 2016 ❖ Volume 7(12) ❖ Article e01588 PENNINGS ET AL. Received 12 January 2016; revised 28 September 2016; accepted 4 October 2016. Corresponding Editor: Jonathan P. Benstead. Copyright: © 2016 Pennings 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. E-mail: [email protected] INTRODUCTION in recruitment from the size structure of older individuals that fall into distinct “cohorts” that Many marine algae, invertebrates, and fish resulted from past pulses of recruitment have a complex life cycle, with a small larval (Doherty and Fowler 1994). Here, we use this stage that disperses in the plankton, and a larger cohort-based approach to infer differences in adult stage that is totally or relatively sedentary, population dynamics of the salt marsh snail and much easier to observe (Reed et al. 1988). Littoraria irrorata between the South Atlantic The challenges in studying the larval stage limit Bight and Gulf Coast of the United States. our understanding of the population ecology of Littoraria irrorata is geographically widespread such species (Gaines and Bertness 1993, Jones and abundant in coastal salt marshes from the et al. 2015). Recruitment from the planktonic into Mid-Atlantic through the Gulf Coast of the Uni- the adult stage is affected by larval production, ted States (Dayan and Dillon 1995). It is extre- by currents that mediate larval transport, by bio- mely important ecologically throughout its tic and abiotic conditions in the water column range, mediating flow of primary production that affect larval survival, and by conditions in into detritivore and herbivore food chains, and the adult habitat that affect larval settlement and serving as food for higher trophic levels (Newell metamorphosis into juvenile or adult stages et al. 1989, Kemp et al. 1990, Silliman and Bert- (Pawlik 1992, Bertness et al. 1996, Witman et al. ness 2002). Nevertheless, because recent L. irro- 2010). These factors are likely to vary geographi- rata recruits are cryptic, studies have largely been cally and over time, contributing to the high spa- limited to adults that are months to over a year tial and temporal variation in recruitment that post-metamorphosis, and little is known about characterizes many marine species (Sale et al. the recruitment dynamics of this species. 1984, Raimondi 1990, Witman et al. 2010, Menge We compared the population structure of et al. 2015). L. irrorata populations between the South Recruitment variability is best understood for Atlantic Bight and the Gulf Coast of the United marine invertebrates on rocky shores, such as States. These two regions support relatively simi- barnacles and mussels, in which adults are com- lar salt marsh communities, with the flora domi- pletely sedentary and recruits can be counted nated by smooth cordgrass, Spartina alterniflora, soon after they settle and metamorphose from black needlerush, Juncus roemerianus, and a the plankton (Crisp and Barnes 1954, Connell handful of other plant species, and the fauna 1985). For these species, variation in recruitment dominated by the same or congeneric species of to the adult stage is often determined by near- crabs, snails, and insects (Kunza and Pennings shore currents, which tend to transport larvae 2008, McCall and Pennings 2012, McFarlin et al. toward or away from the shore, and vary in 2015). However, these similarities may belie direction and strength geographically and over underlying differences in abiotic forcing between time depending on coastal topography and the two regions. The South Atlantic Bight is oceanographic conditions (Roughgarden et al. mesotidal, with a tidal range of one to three 1988, Connolly et al. 2001). meters. In contrast, the Gulf Coast is microtidal, Measuring recruitment soon after metamor- with a tidal range of less than one meter. Because phosis from the plankton is more challenging meteorological forcing can add or subtract sev- for other taxa in which new recruits are cryptic eral decimeters to coastal sea level, meteorologi- or otherwise hard to sample (Reed et al. 1988). cal and lunar forcing of sea level are of a similar A well-established method for these taxa, magnitude in the Gulf Coast, with the result that including many marine fish, is to infer variation the tidal regime is often irregular and wind ❖ www.esajournals.org 2 December 2016 ❖ Volume 7(12) ❖ Article e01588 PENNINGS ET AL. driven, with extended periods of flooded or densities, L. irrorata is an important detritivore, drained conditions (Feng and Li 2010). In addi- shredding fungal-colonized dead S. alterniflora, tion, much of the Gulf Coast experiences more supporting organic matter and nutrient cycling, freshwater input from rivers, particularly in and supporting marsh–estuarine food chains Louisiana, such that coastal waters are often vari- (Newell et al. 1989, Kemp et al. 1990, Newell and able in salinity and well below full-strength sea- Barlocher€ 1993). If L. irrorata reaches densities of À water (Visser et al. 2006). This variation in 500 m 2 or more, its feeding activities suppress oceanographic and riverine forcing is likely to growth of S. alterniflora (Silliman and Zieman affect the structure and function of Gulf Coast vs. 2001, Silliman and Bertness 2002, Silliman et al. South Atlantic Bight salt marsh communities 2005). Littoraria irrorata also serves as an important (Kunza and Pennings 2008, McCall and Pennings food source for a wide variety of consumers, 2012, McFarlin et al. 2015). including fish, crabs, turtles, birds, and mammals We used size-frequency distributions of sub- (Silliman and Bertness 2002, Soomdat et al. 2014). adult and adult L. irrorata to infer differences in The duration of the planktonic larval stage of recruitment between the two geographic regions. L. irrorata has not been measured directly, but is We also examined variation in size-frequency estimated at 3–11 weeks based on studies of distributions in Louisiana over time to look for related species (Reid 1989).
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