Abstract
Tidal marsh habitats provide many important functions to coastal areas and are a valuable economic resource. Polyhaline marshes dominated by Spartina alterniflora can experience top-down control by the snail Littoraria irrorata who primarily impact Spartina through facilitating fungal growth on wounds they create. This grazing pressure may have selected for the production of chemical defenses in Spartina and other polyhaline marsh plants that deter snail feeding and fungal growth. Both Spartina and Littoraria can co-occur in mesohaline marshes that line the Chesapeake Bay, but little is known about interactions between this snail and plants in this habitat. Plant diversity, identity, and consumer abundance can differ between poly- and mesohaline marshes, and this may yield different patterns in the two marsh types. We investigated whether two abundant plants in a Chesapeake Bay mesohaline marsh of salinity ~ 13ppt deterred snail feeding and inhibited fungal growth. Through a bioassay-guided fractionation approach, we assessed palatability to snails and growth of the fungus Phaeosphaeria spartinae in response to chemical components in the invasive marsh grass Phragmites australis and the native sedge Bolboschoenus robustus. Both plants possessed chemicals that significantly deterred snail feeding compared to Spartina chemicals. In addition, both plants inhibited fungal growth, mediated by multiple metabolites. Snail density in this marsh was low (25 snails m−2), but may be enough to select for defenses in Bolboschoenus, or deterrent and inhibitory metabolites may be selected for by other consumers or factors. Chemical defenses in invasive Phragmites may contribute to its success in the Chesapeake Bay.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Angelini P, Rubini A, Gigante D, Reale L, Pagiotti R, Venanzoni R (2012) The endophytic fungal communities associated with the leaves and roots of the common reed (Phragmites australis) in Lake Trasimeno (Perugia, Italy) in declining and healthy stands. Fung Ecol 5:683–693. https://doi.org/10.1016/j.funeco.2012.03.001
Antti I, Ribaudo M, Hyytiäinen K (2015) Water protection in the Baltic Sea and the Chesapeake Bay: Institutions, policies and efficiency. Mar Pollut Bull 93:81–93. https://doi.org/10.1016/j.marpolbul.2015.02.011
Bärlocher F, Newell SY (1994) Phenolics and proteins affecting palatability of Spartina leaves to the gastropod Littoraria irrorata. Mar Ecol 15:65–75. https://doi.org/10.1111/j.1439-0485.1994.tb00042.x
Bertness MD, Ellison AM (1987) Determinants of pattern in a New England salt marsh plant community. Ecol Monogr 57:129–147. https://doi.org/10.2307/1942621
Crain CM, Silliman BR, Bertness SL, Bertness MD (2004) Physical and biotic drivers of plant distribution across estuarine salinity gradients. Ecology 85:2539–2549. https://doi.org/10.1890/03-0745
Cross DH, Fleming K (1989) Control of Phragmites or common reed. U.S. Fish and Wildlife Service, Office of Information Transfer, Ft. Collins, CO, USA FWS/OIT-13.4.12:1–5
Graça MA, Newell SY, Kneib RT (2000) Grazing rates of organic matter and living fungal biomass of decaying Spartina alterniflora by three species of salt-marsh invertebrates. Mar Biol 136:281–289. https://doi.org/10.1007/s002270050686
Hendricks LG, Mossop HE, Kicklighter CE (2011) Palatability and chemical defense of phragmites australis to the marsh periwinkle snail littoraria irrorata. J Chem Ecol 37(8):838–845. https://doi.org/10.1007/s10886-011-9990-8
Jarosz AM, Davelos AL (1995) Effects of disease in wild plant populations and the evolution of pathogen aggressiveness. New Phytol 129:371–387. https://doi.org/10.1111/j.1469-8137.1995.tb04308.x
Kohlmeyer J, Kohlmeyer E (1979) Marine mycology: the higher fungi. Academic Press, New York
Kubanek J, Hay ME, Brown PJ, Lindquist N, Fenical W (2001) Lignoid chemical defenses in the freshwater macrophyte Saururus cernuus. Chemoecology 11:1–8. https://doi.org/10.1007/pl00001826
Kupchan SM, Britton RW, Lacadie JA, Ziegler MF, Sigel CW (1975) The isolation and structural elucidation of bruceantin and bruceantinol. J Org Chem 40:648–654. https://doi.org/10.1002/chin.197524453
Lane AL, Nyadong L, Galhena AS, Shearer TL, Stout EP, Parry RM, Kwasnik M, Wang MD, Hay ME, Fernandez FM, Kubanek J (2009) Desorption electrospray ionization mass spectrometry reveals surface-mediated antifungal chemical defense of a tropical seaweed. Proc Natl Acad Sci USA 106:7314–7319. https://doi.org/10.1073/pnas.0812020106
Larena I, Salazar O, Gonzalez V, Julian M, Rubio V (1999) Design of a primer for ribosomal DNA internal transcribed spacer with enhanced specificity for ascomycetes. J Biotechnol 75:187–194. https://doi.org/10.1016/s0168-1656(99)00154-6
Li H, Zhang X, Zheng R, Li X, Elmer WH, Wolfe LM, Li B (2014) Indirect effects of non-native Spartina alterniflora and its fungal pathogen (Fusarium palustre) on native saltmarsh plants in China. J Ecol 102:1112–1119. https://doi.org/10.1111/1365-2745.12285
Lippson AJ, Lippson RL (1984) Life in the Chesapeake Bay. The Johns Hopkins University Press, Baltimore
Long JD, Mitchell JL, Sotka EE (2011) Local consumers induce resistance differentially between Spartina populations in the field. Ecology 92:180–188. https://doi.org/10.1890/10-0179.1
McCormick MK, Kettenring KM, Baron HM, Whigham DF (2010) Extent and reproductive mechanisms of Phragmites australis spread in brackish Wetlands in Chesapeake Bay, Maryland (USA). Wetlands 30:67–74. https://doi.org/10.1007/s13157-009-0007-0
Nechwatal J, Wielgoss A, Mendgen K (2005) Pythium phragmitis sp. Nov., a new species close to P. arrhenomanes as a pathogen of common reed (Phragmites australis). Mycol Res 109:1337–1346. https://doi.org/10.1017/s0953756205003990
Newell SY (2001) Spore-expulsion rates and extents of blade occupation by ascomycetes of smooth-cordgrass standing-decay system. Bot Mar 44:277–285. https://doi.org/10.1515/bot.2001.036. 285.
Newell SY, Bärlocher F (1993) Removal of fungal and total organic matter from decaying cordgrass leaves by shredder snails. J Exp Mar Biol Ecol 171:39–49. https://doi.org/10.1016/0022-0981(93)90138-e
Palmisano AW, Newson JD (1968) Ecological factors affecting occurrence of Scirpus olneyi and Scirpus robustus in the Louisiana coastal marshes. In: Proceedings of 21st annual conference southeastern association of game and fish commission 21, pp 161–172
Pennings SC, Silliman BR (2005) Linking biogeography and community ecology: latitudinal variation in plant-herbivore interaction strength. Ecology 86:2310–2319. https://doi.org/10.1890/04-1022
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. https://doi.org/10.2307/176702
Perry JE, Atkinson RB (2009) York River tidal marshes. J Coast Res 57:40–49. https://doi.org/10.2112/1551-5036-57.sp1.40
Rice D, Rooth J, Stevenson JC (2000) Colonization and expansion of Phragmites australis in upper Chesapeake Bay tidal marshes. Wetlands 20:280–299. https://doi.org/10.1672/0277-5212(2000)020%5B0280:caeopa%5D2.0.co;2
Rogers K, Boon PI, Branigan S, Duke NC, Field CD, Fitzsimons JA, Kirkman H, Mackenzie JR, Saintilan N (2016) The state of legislation and policy protecting Australia’s mangrove and salt marsh and their ecosystem services. Mar Pol 72:139–155. https://doi.org/10.1016/j.marpol.2016.06.025
Saltonstall K (2002) Cryptic invasion by a non-native genotype of the common reed, Phragmites australis, into North America. Proc Natl Acad Sci 99:2445–2449. https://doi.org/10.1073/pnas.032477999
Sieg RD, Wolfe K, Willey D, Ortiz-Santiago V, Kubanek J (2013a) Chemical defenses against herbivores and fungi limit establishment of fungal farms on salt marsh angiosperms. J Exp Mar Biol Ecol 446:122–130. https://doi.org/10.1016/j.jembe.2013.05.007
Sieg RD, Willey D, Wolfe K, Kubanek J (2013b) Multiple chemical defenses produced by Spartina alterniflora deter farming snails and their fungal crop. Mar Ecol Prog Ser 488:35–49. https://doi.org/10.3354/meps10415
Silliman BR, Bertness MD (2002) A trophic cascade regulates salt marsh primary productivity. Proc Natl Acad Sci 99:10500–10505. https://doi.org/10.1073/pnas.162366599
Silliman BR, Newell SY (2003) Fungal Farming in Snails. Proc Natl Acad Sci 100:15643–15648. https://doi.org/10.1073/pnas.2535227100
Silliman BR, Zieman JC (2001) Top-down control of Spartina alterniflora production by periwinkle grazing in a Virginia salt marsh. Ecology 82:2830–2845. https://doi.org/10.2307/2679964
Silliman BR, van de Koppel J, Bertness MD, Stanton LE, Mendelssohn IA (2005) Drought, snails, and large-scale die-off of southern U.S. salt marshes. Science 310:1803–1806. https://doi.org/10.1126/science.1118229
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. https://doi.org/10.2307/3072086
Acknowledgements
We would like to thank the Chesapeake Bay Environmental Center for access to field sites, Emma Greene, Ashley Privett, and Lydia Truitt for help with field collections and assays, and the Goucher College Summer Research Program in the Sciences.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Marko Rohlfs.
Rights and permissions
About this article
Cite this article
Kicklighter, C.E., Duca, S., Jozwick, A.K.S. et al. 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 (2018). https://doi.org/10.1007/s00049-018-0269-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00049-018-0269-1