Abstract
Previous work has suggested that excess nitrogen (N) alters the degree to which forest canopy versus soil variables influence forest herb communities. This study tested the hypothesis that excess N would shift this influence on individual herb species from soil N availability to stand structural variables that determine light availability to the forest floor. Two watersheds at the Fernow Experimental Forest, West Virginia, USA were used: WS4 and WS3 as untreated reference and treatment watersheds, respectively. WS3 receives 35 kg N/ha/year via aerial application. Herb cover and composition was measured in seven permanent plots/WS from 1991, currently on-going. In 2011, soil moisture and N availability were measured in each plot, along with several variables of canopy structure. Backwards stepwise regression was used to determine relationships between herb cover/individual species and soil/canopy measurements. Herb cover varied spatially with soil resources on WS4, whereas cover varied spatially with canopy structure on WS3. Although results for total herb layer cover supported this hypothesis, results for individual herb species rejected it. This contrast was especially evident for Rubus allegheniensis (blackberry), a nitrophilic species which increased with increasing soil N on both watersheds, but was not correlated with canopy structure on reference WS4, while being correlated with canopy structure on N-treated WS3. Excess N from atmospheric deposition has been shown to decrease plant biodiversity of impacted forests, especially in its effects on herbaceous layer communities. This work demonstrates that one of the mechanisms of such response is in N-mediated changes in the response of herb communities to soil resources and light availability.
Similar content being viewed by others
References
Adams MB, DeWalle DR, Hom J (eds) (2006) The Fernow watershed acidification study. Springer, New York
Aiba S, Akutsu K, Onoda Y (2013) Canopy structure of tropical and sub-tropical rain forests in relation to conifer dominance analysed with a portable LIDAR system. Ann Bot 112:1899–1909
Anderson RC, Loucks OL, Swain AM (1969) Herbaceous response to canopy cover, light intensity, and throughfall precipitation in coniferous forests. Ecology 50:255–263
Atkins JW, Fahey RT, Hardiman BS, Gough CM (2018) Forest canopy structural complexity and light absorption relationships at the subcontinental scale. J Geophys Res Biogeosci 123:1387–1405
Bartels SF, Chen HYN (2010) Is understory plant species diversity driven by resource quantity or resource heterogeneity? Ecology 91:1931–1938
Bellemare J, Moeller DA (2014) Climate change and forest herbs of temperate deciduous forests. In: Gilliam FS (ed) The herbaceous layer in forests of Eastern North America, 2nd edn. Oxford University Press, New York, pp 460–493
Clark CM, Morefield P, Gilliam FS, Pardo LH (2013) Estimated losses of plant biodiversity across the U.S. from historical N deposition from 1985–2010. Ecology 94:1441–1448
Clark CM, Simkin SM, Allen EB, Bowman WD, Belnap J, Brooks ML, Collins SL, Geiser LH, Gilliam FS, Jovani SE, Pardo LH, Schulz BK, Stevens CJ, Suding KN, Throop HL, Waller DM (2019) Vulnerability of 348 herbaceous species to atmospheric deposition of nitrogen and sulfur in the U.S. Nature Plants 5:697–705
Clements FE (1936) Nature and structure of the climax. J Ecol 24:252–284
De Frenne P, Rodríguez-Sánchez F, Coomes DA, Baeten L, Verstraeten G, Vellend M, Bernhardt-Römermann M, Brown CD, Brunet J, Cornelis J et al (2013) Microclimate moderates plant responses to macroclimate warming. Proc Natl Acad Sci USA 110:18561–18565
Dirnböck T, Grandin U, Bernhardt-Römermann M, Beudert B, Canullo R, Forsius M, Grabner M-T, Holmberg M, Kleemola S, Lundin L et al (2014) Forest floor vegetation response to nitrogen deposition in Europe. Glob Chang Biol 20:429–440
Gilliam FS (2006) Response of the herbaceous layer of forest ecosystems to excess nitrogen deposition. J Ecol 94:1176–1191
Gilliam FS (2007) The ecological significance of the herbaceous layer in forest ecosystems. Bioscience 57:845–858
Gilliam FS (2014) Introduction: the herbaceous layer—the forest between the trees. In: Gilliam FS (ed) The herbaceous layer in forests of Eastern North America, 2nd edn. Oxford University Press, New York, pp 1–9
Gilliam FS (2016) A novel mechanism to explain success of invasive herbaceous species at the expense of natives in eastern hardwood forests. New Phytol 209:451–453
Gilliam FS (2019) Excess nitrogen in temperate forest ecosystems decreases herbaceous layer diversity and shifts control from soil to canopy structure. Forests 10:1–13
Gilliam FS, Billmyer JH, Walter CA, Peterjohn WT (2016a) Effects of excess nitrogen on biogeochemistry of a temperate hardwood forest: evidence of nutrient redistribution by a forest understory species. Atmos Environ 146:261–270
Gilliam FS, Welch NT, Phillips AH, Billmyer JH, Peterjohn WT, Fowler ZK, Walter C, Burnham M, May JD, Adams MB (2016b) Twenty-five year response of the herbaceous layer of a temperate hardwood forest to elevated nitrogen deposition. Ecosphere 7(4):e01250. https://doi.org/10.1002/ecs2.1250
Gilliam FS, May JD, Adams MB (2018a) Response of foliar nutrients of Rubus allegheniensis to nutrient amendments in a central Appalachian hardwood forest. Forest Ecol Manag 411:101–107
Gilliam FS, Walter CA, Adams MB, Peterjohn WT (2018b) Nitrogen (N) dynamics in the mineral soil of a central Appalachian hardwood forest during a quarter century of whole-watershed N additions. Ecosystems 21:1489–1504
Gilliam FS, Burns DA, Driscoll CT, Frey SD, Lovett GM, Watmough SA (2019) Decreased atmospheric nitrogen deposition in eastern North America: Predicted responses of forest ecosystems. Environ Pollut 244:560–574
Gleason HA (1926) The individualistic concept of the plant association. Bull Torrey Bot Club 53:7–26
Grime JP (2006) Plant strategies, vegetation processes, and ecosystem properties, 2nd edn. Wiley, Chichester
Hardiman BS, Bohrer G, Gough CM, Vogel CS, Curtis PS (2011) The role of canopy structural complexity in wood net primary production of a maturing northern deciduous forest. Ecology 92:1818–1827
Hardiman BS, Gough CM, Halperin A, Hofmeister KL, Nave LE, Bohrer G, Curtis PS (2013) The role of canopy structural complexity in wood net primary production of a maturing northern deciduous forest. For Ecol Manag 298:111–119
Hutchings MJ, John EA, Wijesinghe DK (2003) Toward understanding the consequences of soil heterogeneity for plant populations and communities. Ecology 84:2322–2334
Jasinski MF, Crago RD (1999) Estimation of vegetation aerodynamic roughness of natural areas using frontal area density determined from satellite imagery. Agric For Meteorol 94:65–77
Jobidon R (1993) Nitrate fertilization stimulates emergence of red raspberry (Rubus idaeus L.) under forest canopy. Fert Res 36:91–94
Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386
Kochenderfer JN (2006) Fernow and the Appalachian hardwood region. In: Adams MB, DeWalle DR, Hom JL (eds) The Fernow watershed acidification study. Springer, Dordrecht, pp 17–40
Kula E, Hrdlicka P, Hedbavny J, Svec P (2012) Various content of manganese in selected forest tree species and plants in the undergrowth. Beskydy 5:19–26
Kumar P, Chen HYN, Searle EB, Shahi C (2018a) Dynamics of understorey biomass, production and turnover associated with long-term overstorey succession in boreal forest of Canada. For Ecol Manag 427:152–161
Kumar P, Chen HYN, Thomas SC, Shahi C (2018b) Linking resource availability and heterogeneity to understorey species diversity through succession in boreal forest of Canada. J Ecol 106:1266–1276
Laliberté E, Grace JB, Huston MA, Lambers H, Teste FP, Turner BL, Wardle DA (2013) How does pedogenesis drive plant diversity? Trends Ecol Evol 28:331–340
LaRue EA, Atkins JW, Dahlin K, Fahey R, Fei S, Gough C, Hardiman BS (2018) Linking Landsat to terrestrial LiDAR: Vegetation metrics of forest greenness are correlated with canopy structural complexity. Int J Appl Earth Obs Geoinf 73:420–427
Lefsky MA, Cohen WB, Parker GG, Harding DJ (2002) Lidar remote sensing for ecosystem studies. Bioscience 52:19–30
Lu X, Mo J, Gilliam FS, Zhou G, Fang Y (2010) Effects of experimental nitrogen deposition on plant diversity in an old-growth tropical forest. Glob Chang Biol 16:2688–2700
MacArthur RH, Horn HS (1969) Foliage profiles by vertical measurements. Ecology 50:802–804
McMahon SM, Bebber DP, Butt N, Crockatt M, Kirby K, Parker GG, Riutta T, Slade EM (2015) Ground based LiDAR demonstrates the legacy of management history to canopy structure and composition across a fragmented temperate woodland. For Ecol Manag 335:255–260
Nagajyoti PC, Lee KD, Sreekanth TVM (1992e) Heavy metals, occurrence and toxicity for plants. Environ Chem Lett 8:1992e16
Neufeld HS, Young DR (2014) Ecophysiology of the herbaceous layer in temperate deciduous forests. In: Gilliam FS (ed) The herbaceous layer in forests of Eastern North America, 2nd edn. Oxford University Press, New York, pp 35–95
Parker GG, Harding DJ, Berger M (2004a) A portable LIDAR system for rapid determination of forest canopy structure. J Appl Ecol 41:755–767
Parker GG, Harmon ME, Lefsky MA, Chen J, Van Pelt R, Weiss SB, Thomas SC, Winner WE, Shaw DC, Franklin JF (2004b) Three-dimensional structure of an old-growth Pseudotsuga-tsuga canopy and its implications for radiation balance, microclimate, and gas exchange. Ecosystems 7:440–453
Peterjohn WT, Adams MB, Gilliam FS (1996) Symptoms of nitrogen saturation in two central Appalachian hardwood forest ecosystems. Biogeochemistry 35:507–522
Reich PB, Frelich LE, Voldseth RA, Bakke P, Adair EC (2012) Understorey diversity in southern boreal forests is regulated by productivity and its indirect impacts on resource availability and heterogeneity. J Ecol 100:539–545
Reiners WA (1992) Twenty years of ecosystem reorganization following experimental deforestation and regrowth suppression. Ecol Monogr 62:503–523
Roberts MR (2004) Response of the herbaceous layer to natural disturbance in North American forests. Can J Bot 82:1273–1283
Rogers RS (1980) Hemlock stands from Wisconsin to Nova Scotia: transitions in understory composition along a floristic gradient. Ecology 61:178–193
Rogers RS (1981) Mature mesophytic hardwood forest: community transitions, by layer, from east-central Minnesota to southeastern Michigan. Ecology 62:1634–1647
Rogers RS (1982) Early spring herb communities in mesophytic forests of the Great Lakes Region. Ecology 63:1050–1063
Rogers RS (1983) Annual variability in community organization of forest herbs: effect of an extremely warm and dry early spring. Ecology 64:1086–1091
Rogers RS (1985) Local coexistence of deciduous-forest groundlayer species growing in different seasons. Ecology 66:701–707
Simkin SM, Allen EB, Bowman WD, Clark CM, Belnap J, Brooks ML, Cade BS, Collins SL, Geiser LH, Gilliam FS et al (2016) A continental analysis of ecosystem vulnerability to atmospheric nitrogen deposition. Proc Natl Acad Sci USA 113:4086–4091
Strik BC (2008) A review of nitrogen nutrition of Rubus. Acta Hortic 777:403–410
Struik GJ, Curtis JT (1962) Herb distribution in an Acer saccharum forest. Am Midl Nat 68:285–296
Thrippleton T, Bugmann H, Kramer-Priewasser K, Snell RS (2016) Herbaceous understorey: an overlooked player in forest landscape dynamics? Ecosystems 19:1240–1254
van der Ent A, Baker AJM, Reeves RD, Pollard J, Schat H (2013) Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant Soil 362:319–334
Walter CA, Burnham MB, Gilliam FS, Peterjohn WT (2015) A reference-based approach for measuring the cover of forest herbs. Environ Monit Assess 187:657
Walter CA, Raiff DT, Burnham MB, Gilliam FS, Adams MB, Peterjohn WT (2016) Nitrogen fertilization interacts with light to increase Rubus spp. cover in a temperate forest. Plant Ecol 217:421–430
Walter CA, Adams MB, Gilliam FS, Peterjohn WT (2017) Non-random species loss in a forest herbaceous layer following nitrogen addition. Ecology 98:2322–2332
Whittaker RH (1962) Classification of natural communities. Bot Rev 28:1–239
Zar JH (2009) Biostatistical analysis, 5th edn. Prentice-Hall, Upper Saddle River
Zavitkovski J (1976) Ground vegetation biomass, production, and efficiency of energy utilization in some northern Wisconsin forest ecosystems. Ecology 57:694–706
Acknowledgements
I am indebted to the excellent field assistance of several undergraduate and graduate students at Marshall University and West Virginia University. I am also pleased to thank Bill Peterjohn (West Virginia University) and Mary Beth Adams (USDA Forest Service) for field and logistical support, and am particularly indebted to Jess Parker (Smithsonian Environmental Research Center) for the LiDAR canopy measurements. The long-term support of the USDA Forest Service in establishing and maintaining the research watersheds is acknowledged. This research was funded in part through United States Department of Agriculture (USDA) Forest Service, Fernow Experimental Forest, Timber and Watershed Laboratory, Parsons, W.V., under USDA Forest Service Cooperative Grants 23-165, 23-590, and 23-842 to Marshall University. Additional funding for this research was provided by USDA National Research Initiative Competitive Grants (Grant NRICGP #2006-35101-17097) to Marshall University and by the Long Term Research in Environmental Biology (LTREB) program at the National Science Foundation (Grant Nos. DEB-0417678 and DEB-1019522) to West Virginia University.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Claus Holzapfel.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Gilliam, F.S. Response of herbaceous layer species to canopy and soil variables in a central Appalachian hardwood forest ecosystem. Plant Ecol 220, 1131–1138 (2019). https://doi.org/10.1007/s11258-019-00984-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11258-019-00984-3