Article
Patch‐Size Effects on Plant Phenolics in Successional Openings of the Southern Appalachians
Abstract
We examined the seasonal changes in plant chemical defenses of key tree species (Robinia pseudoacacia, Liriodendron tulipifera, Acer rubrum, and Cornus florida) regenerating during early succession in different patch sizes within Southern Appalachian forests. Trees of each species were sampled from five sizes of forest openings (0.016, 0.08, 0.4, 2.0, and 10 ha; two replicates each) and from the understory of surrounding forests. Leaves of rapidly growing, pioneer species (Robinia and Liriodendron) were slightly less tough and contained lower levels of hydrolyzable tannins and total phenolics, but higher condensed tannin concentrations than the slower growing, more shade—tolerant species (Acer and Cornus). These results generally support earlier findings indicating the evolutionary development of greater levels of constitutive phenolics in slow—growing than fast—growing species. The differential use of condensed and hydrolyzable tannins by slow— and fast—growing species may reflect adaptive trade—offs in the allocation of different types of phenolics. Regenerating trees often had tougher leaves and contained higher levels of phenolics in large than small openings by midsummer. The differences in phenolics were more pronounced for condensed tannins and when comparing the smallest canopy openings with larger patch sizes. Plant phenolics were also generally lower in understory trees than in conspecific sprouts in openings. These findings may reflect phenotypic carbon/nutrient adjustments as light availability changes across the patch—size gradient. The greater sunlight in large than small openings apparently promotes excess carbon production and a metabolic buildup of phenolic compounds. Independent measures of phenolic compounds peaked at different times during the growing season. Hydrolyzable tannins reached peak levels quite early whereas condensed tannins increased later in the growing season. Total phenolics peaked in midsummer. Herbivore damage was consistently high (5—9%) on Robinia sprouts in all openings. Insect herbivory on the remaining three species (1—5%) was significantly lower in large than small patch sizes. Tree species regenerating in the high sunlight of larger openings in Southern Appalachian forests thus tend to have tougher leaves, contain greater phenolics, and experience less herbivore damage than conspecifics in small openings.
Citing Literature
Number of times cited: 64
- Frida I. Piper, Scott H. Altmann and Christopher H. Lusk, Global patterns of insect herbivory in gap and understorey environments, and their implications for woody plant carbon storage, Oikos, 127, 4, (483-496), (2018).
- Don Cipollini, Dale Walters and Claudia Voelckel, Costs of Resistance in Plants: From Theory to Evidence, Annual Plant Reviews online, (263-307), (2017).
- Nathan P. Lemoine, Deron E. Burkepile and John D. Parker, Insect herbivores increase mortality and reduce tree seedling growth of some species in temperate forest canopy gaps, PeerJ, 5, (e3102), (2017).
- Benedicte Bachelot, María Uríarte, Jill Thompson, Jess K. Zimmerman and Martin Heil, The advantage of the extremes: tree seedlings at intermediate abundance in a tropical forest have the highest richness of above‐ground enemies and suffer the most damage, Journal of Ecology, 104, 1, (90-103), (2015).
- , Bibliography, Insect Ecology, 10.1016/B978-0-12-803033-2.00024-8, (609-702), (2016).
- Antonio López‐Carretero, Karina Boege, Cecilia Díaz‐Castelazo, Zaira Domínguez and Víctor Rico‐Gray, Influence of plant resistance traits in selectiveness and species strength in a tropical plant‐herbivore network, American Journal of Botany, 103, 8, (1436-1448), (2016).
- Ellen van Velzen and Rampal S. Etienne, The importance of ecological costs for the evolution of plant defense against herbivory, Journal of Theoretical Biology, 372, (89), (2015).
- Don Cipollini, Dale Walters and Claudia Voelckel, Costs of Resistance in Plants: From Theory to Evidence, Annual Plant Reviews, (263-307), (2014).
- Julian M. Norghauer and David M. Newbery, Herbivores equalize the seedling height growth of three dominant tree species in an African tropical rain forest, Forest Ecology and Management, 310, (555), (2013).
- , Insect Responses to Environmental Changes, Insects and Sustainability of Ecosystem Services, 10.1201/b14911-4, (53-96), (2013).
- Jonathan E. Hickman, Isabel W. Ashton, Katherine M. Howe and Manuel T. Lerdau, The native–invasive balance: implications for nutrient cycling in ecosystems, Oecologia, 173, 1, (319), (2013).
- Kaoru Kitajima, Anna‐Maria Llorens, Carla Stefanescu, Marta Vargas Timchenko, Peter W. Lucas and S. Joseph Wright, How cellulose‐based leaf toughness and lamina density contribute to long leaf lifespans of shade‐tolerant species, New Phytologist, 195, 3, (640-652), (2012).
- James W. Bressette, Harald Beck and Vanessa B. Beauchamp, Beyond the browse line: complex cascade effects mediated by white‐tailed deer, Oikos, 121, 11, (1749-1760), (2012).
- James F. Harbertson, Giuseppina P. Parpinello, Hildegarde Heymann and Mark O. Downey, Impact of exogenous tannin additions on wine chemistry and wine sensory character, Food Chemistry, 131, 3, (999), (2012).
- W.A. Johnson, J.R. Nechols, R.A. Cloyd, D. Rotenberg and M.M. Kennelly, Effect of Light Intensity on Brassica rapa Chemistry and Plutella xylostella (Lepidoptera: Plutellidae) Life History Traits., Journal of Entomological Science, 10.18474/0749-8004-47.4.327, 47, 4, (327-349), (2012).
- T.D. Schowalter, Insect Responses to Major Landscape-Level Disturbance, Annual Review of Entomology, 57, 1, (1), (2012).
- James W. Dalling, Adam S. Davis, Brian J. Schutte and A. Elizabeth Arnold, Seed survival in soil: interacting effects of predation, dormancy and the soil microbial community, Journal of Ecology, 99, 1, (89-95), (2010).
- Tran Van Do, Akira Osawa, Nguyen Toan Thang, Nguyen Ba Van, Bui Thanh Hang, Cam Quoc Khanh, Le Thi Thao and Diep Xuan Tuan, Population changes of early successional forest species after shifting cultivation in Northwestern Vietnam, New Forests, 41, 2, (247), (2011).
- , Bibliography, Insect Ecology, 10.1016/B978-0-12-381351-0.00018-4, (525-606), (2011).
- HINO TAKAFUMI, SATORU KAWASE, MASAHIRO NAKAMURA and TSUTOM HIURA, Herbivory in canopy gaps created by a typhoon varies by understory plant leaf phenology, Ecological Entomology, 35, 5, (576-585), (2010).
- Dale R. Walters, The Evolution of Plant Defense, Plant Defense, (153-200), (2010).
- Aya Imaji and Kenji Seiwa, Carbon allocation to defense, storage, and growth in seedlings of two temperate broad-leaved tree species, Oecologia, 162, 2, (273), (2010).
- Liza S. Comita, Maria Uriarte, Jill Thompson, Inge Jonckheere, Charles D. Canham and Jess K. Zimmerman, Abiotic and biotic drivers of seedling survival in a hurricane‐impacted tropical forest, Journal of Ecology, 97, 6, (1346-1359), (2009).
- Jonathan M. Adams, Brian Rehill, Yangjian Zhang and Jonathan Gower, A test of the latitudinal defense hypothesis: herbivory, tannins and total phenolics in four North American tree species, Ecological Research, 24, 3, (697), (2009).
- Norris Z. Muth, Emily C. Kluger, Jennifer H. Levy, Marten J. Edwards and Richard A. Niesenbaum, Increased per capita herbivory in the shade: Necessity, feedback, or luxury consumption?, Écoscience, 10.2980/15-2-3095, 15, 2, (182-188), (2015).
- Peter A. Van Zandt, PLANT DEFENSE, GROWTH, AND HABITAT: A COMPARATIVE ASSESSMENT OF CONSTITUTIVE AND INDUCED RESISTANCE, Ecology, 88, 8, (1984-1993), (2007).
- MASASHI MURAKAMI, TOSHIHIDE HIRAO and TOMOAKI ICHIE, Comparison of lepidopteran larval communities among tree species in a temperate deciduous forest, Japan, Ecological Entomology, 32, 6, (613-620), (2007).
- Donald J. Shure, Donald L. Phillips and P. Edward Bostick, Gap size and succession in cutover southern Appalachian forests: an 18 year study of vegetation dynamics, Plant Ecology, 185, 2, (299), (2006).
- Paulina Chacón and Juan J. Armesto, Do carbon-based defences reduce foliar damage? Habitat-related effects on tree seedling performance in a temperate rainforest of Chiloé Island, Chile, Oecologia, 146, 4, (555), (2006).
- James H. Graves, Robert K. Peet and Peter S. White, The influence of carbon—nutrient balance on herb and woody plant abundance in temperate forest understories, Journal of Vegetation Science, 17, 2, (217-226), (2009).
- Jennifer Read and Alexia Stokes, Plant biomechanics in an ecological context, American Journal of Botany, 93, 10, (1546-1565), (2006).
- , Bibliography, Insect Ecology, 10.1016/B978-012088772-9/50044-3, (483-536), (2006).
- James H. Graves, Robert K. Peet and Peter S. White, The influence of carbon - nutrient balance on herb and woody plant abundance in temperate forest understories, Journal of Vegetation Science, 17, 2, (217), (2006).
- D.L. O’Hanlon-Manners and P.M. Kotanen, Losses of seeds of temperate trees to soil fungi: effects of habitat and host ecology, Plant Ecology, 187, 1, (49), (2006).
- Timothy D. Schowalter, Yanli Zhang and Robert A. Progar, CANOPY ARTHROPOD RESPONSE TO DENSITY AND DISTRIBUTION OF GREEN TREES RETAINED AFTER PARTIAL HARVEST, Ecological Applications, 15, 5, (1594-1603), (2005).
- Michael D. Ulyshen, James L. Hanula, Scott Horn, John C. Kilgo and Christopher E. Moorman, Herbivorous Insect Response to Group Selection Cutting in a Southeastern Bottomland Hardwood Forest, Environmental Entomology, 34, 2, (395), (2005).
- Justin Amiot, Yann Salmon, Christian Collin and John D. Thompson, Differential resistance to freezing and spatial distribution in a chemically polymorphic plant Thymus vulgaris, Ecology Letters, 8, 4, (370-377), (2005).
- L. A. Dyer, D. K. Letourneau, C. D. Dodson, M. A. Tobler, J. O. Stireman and A. Hsu, ECOLOGICAL CAUSES AND CONSEQUENCES OF VARIATION IN DEFENSIVE CHEMISTRY OF A NEOTROPICAL SHRUB, Ecology, 85, 10, (2795-2803), (2004).
- D. L. O’Hanlon-Manners and P. M. Kotanen, Evidence that fungal pathogens inhibit recruitment of a shade-intolerant tree, white birch (Betula papyrifera), in understory habitats, Oecologia, 140, 4, (650), (2004).
- Elena Baraza, José M Gómez, José A Hódar and Regino Zamora, Herbivory has a greater impact in shade than in sun: response of Quercus pyrenaica seedlings to multifactorial environmental variation, Canadian Journal of Botany, 82, 3, (357), (2004).
- Rebecca E. Forkner and Robert J. Marquis, Uneven-aged and even-aged logging alter foliar phenolics of oak trees remaining in forested habitat matrix, Forest Ecology and Management, 199, 1, (21), (2004).
- C. Noemi Mazía, Thomas Kitzberger and Enrique J. Chaneton, Interannual changes in folivory and bird insectivory along a natural productivity gradient in northern Patagonian forests, Ecography, 27, 1, (29-40), (2004).
- Marc Rhainds and Greg English‐Loeb, Testing the resource concentration hypothesis with tarnished plant bug on strawberry: density of hosts and patch size influence the interaction between abundance of nymphs and incidence of damage, Ecological Entomology, 28, 3, (348-358), (2003).
- Timothy R. H. Pearson, David F. R. P. Burslem, Rachel E. Goeriz and James W. Dalling, Interactions of gap size and herbivory on establishment, growth and survival of three species of neotropical pioneer trees, Journal of Ecology, 91, 5, (785-796), (2003).
- Michel Fortin and Yves Mauffette, The suitability of leaves from different canopy layers for a generalist herbivore (Lepidoptera: Lasiocampidae) foraging on sugar maple, Canadian Journal of Forest Research, 32, 3, (379), (2002).
- Michel Fortin and Yves Mauffette, Forest edge effects on the biological performance of the forest tent caterpillar (Lepidoptera: Lasiocampidae) in sugar maple stands, Écoscience, 8, 2, (164), (2001).
- Steven W. Seagle and Suh-Yuen Liang, Application of a forest gap model for prediction of browsing effects on riparian forest succession, Ecological Modelling, 144, 2-3, (213), (2001).
- Alejandra Paez, G Michael Gebre, Maria E Gonzalez and Timothy J Tschaplinski, Growth, soluble carbohydrates, and aloin concentration of Aloe vera plants exposed to three irradiance levels, Environmental and Experimental Botany, 44, 2, (133), (2000).
- T. D. Schowalter and L. M. Ganio, Invertebrate communities in a tropical rain forest canopy in Puerto Rico following Hurricane Hugo, Ecological Entomology, 24, 2, (191-201), (2001).
- Mark D. Hunter and Rebecca E. Forkner, HURRICANE DAMAGE INFLUENCES FOLIAR POLYPHENOLICS AND SUBSEQUENT HERBIVORY ON SURVIVING TREES, Ecology, 80, 8, (2676-2682), (1999).
- Donald J. Shure, Peter D. Mooreside and Stephen M. Ogle, RAINFALL EFFECTS ON PLANT–HERBIVORE PROCESSES IN ANUPLAND OAK FOREST, Ecology, 79, 2, (604-617), (1998).
- Karolyn Darrow and M. Deane Bowers, Phenological and population variation in iridoid glycosides of Plantago lanceolata (Plantaginaceae), Biochemical Systematics and Ecology, 25, 1, (1), (1997).
- Jon D. Johnson, Roberto Tognetti, Marco Michelozzi, Simone Pinzauti, Gianfranco Minotta and Marco Borghetti, Ecophysiological responses of Fagus sylvatica seedlings to changing light conditions. II. The interaction of light environment and soil fertility on seedling physiology, Physiologia Plantarum, 101, 1, (124-134), (2006).
- V. Liakoura, M. Stefanou, Y. Manetas, C. Cholevas and G. Karabourniotis, Trichome density and its UV-B protective potential are affected by shading and leaf position on the canopy, Environmental and Experimental Botany, 38, 3, (223), (1997).
- K.Dave Coates and Philip J. Burton, A gap-based approach for development of silvicultural systems to address ecosystem management objectives, Forest Ecology and Management, 99, 3, (337), (1997).
- Alain Bazin, Solange Blaise and Delphine Cartier, Polymorphisme de deux mécanismes de défense chezLotus corniculatusL. (Fabaceae); mise en relation avec des facteurs abiotiques, Acta Botanica Gallica, 144, 4, (433), (1997).
- Christopher B. Mowry, Barbara S. Decker and Donald J. Shure, The role of phytochemistry in dietary choices of Tana River red colobus monkeys(Procolobus badius rufomitratus), International Journal of Primatology, 17, 1, (63), (1996).
- R. E. ESTELL, E. L. FREDRICKSON and K. M. HAVSTAD, Chemical composition of Flourensia cernua at four growth stages, Grass and Forage Science, 51, 4, (434-441), (2006).
- Leonardo A. Salas, Habitat use by lowland tapirs (Tapirus terrestris L.) in the Tabaro River valley, southern Venezuela, Canadian Journal of Zoology, 74, 8, (1452), (1996).
- Leonardo A. Salas and Todd K. Fuller, Diet of the lowland tapir (Tapirus terrestris L.) in the Tabaro River valley, southern Venezuela, Canadian Journal of Zoology, 74, 8, (1444), (1996).
- Patricia J. Folgarait and Diane W. Davidson, Myrmecophytic Cecropia: antiherbivore defenses under different nutrient treatments, Oecologia, 104, 2, (189), (1995).
- Michael Constantinides and James H. Fownes, Tissue‐to‐solvent ratio and other factors affecting determination of soluble polyphenols in tropical leaves, Communications in Soil Science and Plant Analysis, 25, 19-20, (3221), (1994).
- William M. Ford, A. Sydney Johnson and Philip E. Hale, Nutritional quality of deer browse in southern Appalachian clearcuts and mature forests, Forest Ecology and Management, 67, 1-3, (149), (1994).
- Phyllis D. Coley, Gap size and plant defenses, Trends in Ecology & Evolution, 8, 1, (1), (1993).
