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Ecological Associations of Littoraria irrorata with Spartina cynosuroides and Spartina alterniflora

Abstract

It is well-documented that marsh periwinkles (Littoraria irrorata) consume and inhabit smooth cordgrass (Spartina alterniflora), but their interactions with big cordgrass (Spartina cynosuroides) remain unknown. Plant communities in mesohaline marshes will change as sea-level rise shifts species from salt-intolerant (e.g., S. cynosuroides) plants to salt-tolerant (e.g., S. alterniflora) ones. Therefore, understanding how L. irrorata interacts with different habitats provides insight into this species’ generalist nature and allows us to predict the potential impacts of changing plant communities on L. irrorata. We show, for the first time, that L. irrorata inhabits, climbs, and grazes S. cynosuroides. We compared both habitats and found snails were larger, plant tissue was tougher, and sediment surface temperatures were higher in S. alterniflora than S. cynosuroides. Snails had greater survivorship from predators in S. cynosuroides than in S. alterniflora. Further, snails grazed S. cynosuroides more than S. alterniflora, evidenced by a greater number of radulation scars. Despite these differences, snail densities were equal between habitats suggesting functional redundancy between S. cynosuroides and S. alterniflora for L. irrorata. Our results indicate L. irrorata is a habitat generalist that uses both S. alterniflora and S. cynosuroides, which may allow it to gain an ecological foothold as sea-level rises.

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References

  1. Alexander SK (1979) Diet of the periwinkle Littorina irrorata in a Louisiana salt marsh. Gulf Research Reports 6:293–295

  2. Anderson RR, Brown RG, Rappleye RD (1968) Water quality and plant distribution along the upper Patuxent River, Maryland. Chesapeake Science 9:145–156

    Google Scholar 

  3. Beck MW, Heck KL Jr, Able KW, Childers DL, Eggleston DB, Gillanders BM, Halpern B, Hays CG, Hoshino K, Minello TJ, Orth RJ, Sheridan PF, Weinstein MP (2001) The identification, conservation, and management of estuarine and marine nurseries for fish and invertebrates. BioScience 51:633–641

    Google Scholar 

  4. Bingham FO (1972) The influence of environmental stimuli on the direction of movement of the supralittoral gastropod Littorina irrorata. Bulletin of Marine Science 22:309–335

    Google Scholar 

  5. Boesch DF, Field JC, Scavia D (eds) (2000) The potential consequences of climate variability and change on coastal areas and marine resources: report of the coastal areas and marine resources sector team, U.S. national assessment of the potential consequences of climate variability and change, U.S. global change research program, NOAA Coastal Ocean program decision analysis series no, vol 21. NOAA Coastal Ocean Program, Silver Spring, MD, 163 pp

  6. Carroll JM, Church MB, Finelli CM (2018) Periwinkle climbing response to water- and airborne predator chemical cues may depend on home-marsh geography. PeerJ 6:e5744

    PubMed  PubMed Central  Google Scholar 

  7. Constantin AJ, Broussard WP III, Cherry JA (2019) Environmental gradients and overlapping ranges of dominant coastal wetland plants in Weeks Bay, AL. Southeastern Naturalist 18:224–239

    Google Scholar 

  8. Core Team R (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria https://www.R-project.org

    Google Scholar 

  9. Crist RW, Banta WC (1983) Distribution of marsh periwinkle Littorina irrorata (say) in a Virginia salt marsh. Gulf Research Reports 7:225–235

    Google Scholar 

  10. Deis D, Fleeger JW, Bourgoin SM, Mendelssohn IA, Lin Q, Hou A (2017) Shoreline oiling effects and recovery of salt marsh macroinvertebrates from the Deepwater Horizon oil spill. PeerJ 5:e3680

    PubMed  PubMed Central  Google Scholar 

  11. Greenberg R, Maldonado JE, Droege S, McDonald MV (2006) Tidal marshes: a global perspective on the evolution and conservation of their terrestrial vertebrates. BioScience 56:675–685

    Google Scholar 

  12. Hamilton PV (1976) Predation on Littorina irrorata (Mollusca:Gastropoda) by Callinectes sapidus (Crustacea:Portunidae). Bulletin of Marine Science 26:403–409

    Google Scholar 

  13. Hamilton PV (1978) Intertidal distribution and long-term movements of Littorina irrorata (Mollusca: Gastropoda). Marine Biology 46:49–58

    Google Scholar 

  14. Hendricks LG, Mossop HE, Kicklighter CE (2011) Palatability and chemical defense of Phragmites australis to the marsh periwinkle snail Littoraria irrorata. Journal of Chemical Ecology 37:838–845

    CAS  PubMed  Google Scholar 

  15. Henry RP, McBride CJ, Williams AH (1993) Responses of the marsh periwinkle, Littoraria (Littorina) irrorata to temperature, salinity, and desiccation, and the potential physiological relationship to climbing behavior. Marine Behavioral Physiology 24:45–54

    Google Scholar 

  16. Hughes R (2012) A neighboring plant species creates associational refuge for consumer and host. Ecology 93:1411–1420

    PubMed  Google Scholar 

  17. Jarrell ER, Kolker AS, Campbell C, Blum MJ (2016) Brackish marsh plant community responses to regional precipitation and relative sea-level rise. Wetlands 36:607–619

    Google Scholar 

  18. Jeffrey SW, Welschmeyer NA (1997) Spectrophotometric and fluorometric equations in common use in oceanography. In: Jeffrey SW, Mantoura RFC, Wright SW (eds) Phytoplankton pigments in oceanography: guidelines to modern methods. UNESCO, Paris, France, pp 597–615

    Google Scholar 

  19. Johnson DS, Williams BL (2017) Sea level rise may increase extinction risk of a saltmarsh ontogenetic habitat specialist. Ecology and Evolution 7:7786–7795

    PubMed  PubMed Central  Google Scholar 

  20. Kicklighter CE, Duca S, Jozwick AKS, Locke H, Hundley C, Hite B, Hannifin G (2018) Grazer deterrence and fungal inhibition by the invasive marsh grass Phragmites australis and the native sedge Bolboschoenus robustus in a mesohaline marsh. Chemoecology 28:163–172

    CAS  Google Scholar 

  21. Lee SC, Silliman BR (2006) Competitive displacement of a detritivorous salt marsh snail. Journal of Experimental Marine Biology and Ecology 339:75–85

    Google Scholar 

  22. Lewis DB, Eby LA (2002) Spatially heterogeneous refugia and predation risk in intertidal salt marshes. OIKOS 96:119–129

    Google Scholar 

  23. Li F, Pennings SC (2018) Responses of tidal freshwater and brackish marsh macrophytes to pulses of saline water simulating sea level rise and reduced discharge. Wetlands 38:885–891

    Google Scholar 

  24. Lin J (1989) Influence of location in a salt marsh on survivorship of ribbed mussels. Marine Ecology Progress Series 56:105–110

    Google Scholar 

  25. Lorenzen C (1967) Determination of chlorophyll and phaeopigments: spectrophotometric equations. Limnology and Oceanography 12:343–346

    CAS  Google Scholar 

  26. McCann MJ, Able KW, Christian RR, Fodrie FJ, Jensen OP, Johnson JJ, López-Duarte PC, Martin CW, Olin JA, Polito MJ, Roberts BJ, Ziegler SL (2017) Key taxa in food web responses to stressors: the Deepwater Horizon oil spill. Frontiers in Ecology and the Environment 15:142–149

    Google Scholar 

  27. McHugh JM, Dighton J (2004) Influence of mycorrhizal inoculation, inundation period, salinity, and phosphorus availability on the growth of two salt marsh grasses, Spartina alterniflora Lois. And Spartina cynosuroides (L.) Roth., in nursery systems. Restoration Ecology 12:533–545

    Google Scholar 

  28. Odum WE (1988) Comparative ecology of tidal freshwater and salt marshes. Annual Review of Ecology and Systematics 19:147–176

    Google Scholar 

  29. Odum WE, Smith TJ III, Hoover JK, McIvor CC (1984) The ecology of tidal freshwater marshes of the United States east coast: a community profile. U.S. Fish and Wildlife Service, FWS/OBS-83/17. pp 177

  30. Otte ML, Wilson G, Morris JT, Moran BM (2004) Dimethylsulphoniopropionate (DMSP) and related compounds in higher plants. Journal of Experimental Botany 55:1919–1925

    CAS  PubMed  Google Scholar 

  31. Penfound WT, Hathaway ES (1938) Plant communities in the marshlands of southeastern Louisiana. Ecological Monographs 8:1–56

    CAS  Google Scholar 

  32. Pennings SC, Carefoot TH, Siska EL, Chase ME, Page TA (1998) Feeding preferences of a generalist salt-marsh crab: relative importance of multiple plant traits. Ecology 79:1968–1979

    Google Scholar 

  33. Perry JE, Atkinson RB (1997) Plant diversity along a salinity gradient of four marshes on the York and Pamunkey Rivers in Virginia. Castanea 62:112–118

    Google Scholar 

  34. Rietl AJ, Sorrentino MG, Roberts BJ (2018) Spatial distribution and morphological responses to predation in the salt marsh periwinkle. Ecosphere 9:e02316

    Google Scholar 

  35. Schindler DE, Johnson BM, MacKay NA, Bouwes N, Kitchell JF (1994) Snail size-structured interactions and salt marsh predation gradients. Oecologia 97:49–61

    PubMed  Google Scholar 

  36. Shepard CC, Crain CM, Beck MW (2011) The protective role of coastal marshes: a systematic review and meta-analysis. PLoS One 6:e27374

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Sieg RD, Wolfe K, Willey D, Ortiz-Santiago V, Kubanek J (2013) Chemical defenses against herbivores and fungi limit establishment of fungal farms on salt marsh angiosperms. Journal of Experimental Marine Biology and Ecology 446:122–130

    CAS  Google Scholar 

  38. Silberhorn G (1992) Big cordgrass, Giant cordgrass Spartina cynosuroides (L.) Roth. Wetland Flora technical reports, wetlands program, Virginia Institute of Marine Science. Virginia Institute of Marine Science, College of William and Mary.

  39. Silliman BR, Newell SY (2003) Fungal farming in a snail. Proceedings of the National Academy of Sciences of the United States of America 100:15643–15648

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Silliman BR, Zieman JC (2001) Top-down control of Spartina alterniflora production by periwinkle grazing in a Virginia salt marsh. Ecology 82:2830–2845

    Google Scholar 

  41. Siska EL, Pennings SC, Buck TL, Hanisak MD (2002) Latitudinal variation in palatability of salt-marsh plants: which traits are responsible? Ecology 83:3369–3381

    Google Scholar 

  42. Stevenson JC, Rooth JE, Kearney MS, Sundberg KL (2000) The health and long term stability of natural and restored marshes in the Chesapeake Bay. In: Weinstein MP, Kraeger DA (eds) concepts and controversies in tidal marsh ecology, Kluwer academic publishing, Dordrecht, the Netherlands, pp 709-735

  43. Stribling JM (1997) The relative importance of sulfate availability in the growth of Spartina alterniflora and Spartina cynosuroides. Aquatic Botany 56:131–143

    CAS  Google Scholar 

  44. Vaughn CC, Fisher FM (1992) Dispersion of the salt-marsh periwinkle Littoraria irrorata: effects of water level, size, and season. Estuaries 15:246–250

    Google Scholar 

  45. VECOS Database. Virginia Estuarine and Coastal Observing System. Station TSK000.23 (Taskinas Creek). http://vecos.vims.edu/. Accessed July 16, 2019

  46. Warren JH (1985) Climbing as an avoidance behaviour in the salt marsh periwinkle, Littorina irrorata (say). Journal of Experimental Marine Biology and Ecology 89:11–28

    Google Scholar 

  47. Wass ML, Wright TD (1969) Coastal wetlands of Virginia. In: applied marine science and ocean engineering, number 10, Virginia Institute of Marine Science, College of William and Mary, Gloucester point, pp 154

  48. White SN, Alber M (2009) Drought-associated shifts in Spartina alterniflora and S. cynosuroides in the Altamaha River estuary. Wetlands 29:215–224

    Google Scholar 

  49. Zengel S, Weaver J, Pennings SC, Silliman B, Deis DR, Montague CL, Rutherford N, Nixon Z, Zimmerman AR (2017) Five years of Deepwater Horizon oil spill effects on marsh periwinkles Littoraria irrorata. Marine Ecology Progress Series 576:135–144

    Google Scholar 

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Acknowledgements

We thank the following people for help in the field and laboratory: Manisha Pant, Catherine Wilhelm, Kayla Martínez-Soto, Emily Goetz, Anna Ledwin, Leah Scott, Mark Brush, and Sarah Blachman. Many thanks go to the Chesapeake Bay National Estuarine Research Reserve of Virginia (CBNERR-VA) and York River State Park for access to our study site, Taskinas Creek. We are thankful to the Virginia Institute of Marine Science for funding this project. This work was funded, in part, by the National Science Foundation (grant number 1832221) and the Virginia Institute of Marine Science. This paper is Contribution No. 3899 of the Virginia Institute of Marine Science, William & Mary. Lastly, we thank the snails for their persistent efforts to escape.

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Correspondence to Caroline Mackenzie Failon.

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Failon, C.M., Wittyngham, S.S. & Johnson, D.S. Ecological Associations of Littoraria irrorata with Spartina cynosuroides and Spartina alterniflora. Wetlands 40, 1317–1325 (2020). https://doi.org/10.1007/s13157-020-01306-4

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Keywords

  • Brackish marsh
  • Mesohaline marsh
  • Salt marsh
  • Ecological equivalence
  • Sea level rise