Intraspecific leaf chemistry drives locally accelerated ecosystem function in aquatic and terrestrial communities

Ecology

Volumn 97, Issue 8, 2016, Pages 2125-2135

  Jackrel, Sara L ^a   Morton, Timothy C ^a   Wootton, J Timothy ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Defense chemistry; Diarylheptanoids; Ecosystem subsidies; Ellagitannins; Indirect effects; Intraspecific variation; Local adaptation; Trophic interactions

Indexed keywords

AQUATIC COMMUNITY; DECOMPOSITION; ECOSYSTEM FUNCTION; FOOD WEB; INTRASPECIFIC VARIATION; LEAF LITTER; LOCAL ADAPTATION; MOVEMENT; PATCHINESS; PHYTOCHEMISTRY; RESOURCE ALLOCATION; RIPARIAN VEGETATION; SECONDARY METABOLITE; SPATIAL VARIATION; TERRESTRIAL ECOSYSTEM; TROPHIC INTERACTION;

ALNUS RUBRA;

CHEMISTRY; ECOLOGY; ECOSYSTEM; FOOD CHAIN; PHYSIOLOGY; PLANT LEAF; RIVER; TREE;

ECOLOGY; ECOSYSTEM; FOOD CHAIN; PLANT LEAVES; RIVERS; TREES;

EID: 84982860192     PISSN: 00129658     EISSN: None     Source Type: Journal    
DOI: 10.1890/15-1763.1     Document Type: Article

References (53)

1. Agrawal, A. A. 1998. Induced responses to herbivory and increased plant performance. Science 279:1201-1202.
2. Agrawal, A. A., A. P. Hastings, M. T. J. Johnson, J. L. Maron, and J.-P. Salminen. 2012. Insect herbivores drive real-time ecological and evolutionary change in plant populations. Science 338:113-116.
3. Allmann, S., and I. T. Baldwin. 2010. Insects betray themselves in nature to predators by rapid isomerization of green leaf volatiles. Science 329:1075-1078.
4. Awmack, C. S., and S. R. Leather. 2002. Host plant quality and fecundity in herbivorous insects. Annual Review of Entomology 47:817-844.
5. Barbehenn, R., C. Jones, A. Hagerman, M. Karonen, and J.-P. Salminen. 2006. Ellagitannins have greater oxidative activities than condensed tannins and galloyl glucoses at high pH: potential impact on caterpillars. Journal of Chemical Ecology 32:2253-2267.
6. Barbehenn, R. V., A. Jaros, G. Lee, C. Mozola, Q. Weir, and J.-P. Salminen. 2009. Hydrolyzable tannins as "quantitative defenses": limited impact against Lymantria dispar caterpillars on hybrid poplar. Journal of Insect Physiology 55:297-304.
7. Benner, R., M. L. Fogel, E. K. Sprague, and R. E. Hodson. 1987. Depletion of 13C in lignin and its implications for stable carbon isotope studies. Nature 329:708-710.
8. Bruno, J. F., and M. I. O'Connor. 2005. Cascading effects of predator diversity and omnivory in a marine food web. Ecology Letters 8:1048-1056.
9. Bryant, J. P., T. P. Clausen, P. B. Reichardt, M. C. McCarthy, and R. A. Werner. 1987. Effect of nitrogen fertilization upon the secondary chemistry and nutritional value of quaking aspen (Populus tremuloides Michx.) leaves for the large aspen tortrix (Choristoneura conflictana (Walker)). Oecologia 73:513-517.
10. Cardinale, B. J., D. S. Srivastava, J. Emmett Duffy, J. P. Wright, A. L. Downing, M. Sankaran, and C. Jouseau. 2006. Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443:989-992.
11. Cebrian, J. 1999. Patterns in the fate of production in plant communities. American Naturalist 154:449-468.
12. Chen, J., R. F. Gonzalez-Laredo, and J. J. Karchesy. 2000. Minor diarylheptanoid glycosides of Alnus rubra bark. Phytochemistry 53:971-973.
13. Christensen, T. A., H. Mustaparta, and J. G. Hilderbrand. 1989. Discrimination of sex pheromone blends in the olfactory system of the moth. Chemical Senses 14:463-477.
14. Clark, T. 1999. Evolution and adaptive significance of larval midgut alkalinization in the insect superorder Mecopterida. Journal of Chemical Ecology 25:1945-1960.
15. Coley, P. D. 1980. Effects of leaf age and plant life history patterns on herbivory. Nature 284:2.
16. Coley, P. D., J. P. Bryant, and F. S. Chapin III. 1985. Resource availability and plant antiherbivore defense. Science 230:895-899.
17. Crutsinger, G. M., M. D. Collins, J. A. Fordyce, Z. Gompert, C. C. Nice, and N. J. Sanders. 2006. Plant genotypic diversity predicts community structure and governs an ecosystem process. Science 313:966-968.
18. Farrand, L., J. Y. Kim, S. Byun, A. Im-aram, J. Lee, J. Y. Suh, K. W. Lee, H. J. Lee, and B. K. Tsang. 2014. The diarylheptanoid hirsutenone sensitizes chemoresistant ovarian cancer cells to cisplatin via modulation of apoptosis-inducing factor and X-linked inhibitor of apoptosis. Journal of Biological Chemistry 289:1723-1731.
19. González-Hernández, M. P., E. E. Starkey, and J. Karchesy. 2000. Seasonal variation in concentrations of fiber, crude protein, and phenolic compounds in leaves of red alder (Alnus rubra): nutritional implications for cervids. Journal of Chemical Ecology 26:293-301.
20. González-Laredo, R. F., R. F. Helm, J. Chen, and J. J. Karchesy. 1998. Two acylated diarylheptanoid glycosides from red alder bark. Journal of Natural Products 61:1292-1294.
21. Hunter, M. D., and J. N. McNeil. 1997. Host-plant quality influences diapause and voltinism in a polyphagous insect herbivore. Ecology 78:977-986.
22. Ives, A. R., and S. R. Carpenter. 2007. Stability and diversity of ecosystems. Science 317:58-62.
23. Jackrel, S. L., and J. T. Wootton. 2014. Local adaptation of stream communities to intraspecific variation in a terrestrial ecosystem subsidy. Ecology 95:37-43.
24. Jackrel, S. L., and J. T. Wootton. 2015. Cascading effects of induced terrestrial plant defences on aquatic and terrestrial ecosystem function. Proceedings of the Royal Society of London B: Biological Sciences 282:20142522.
25. Karonen, M., J. Parker, A. Agrawal, and J.-P. Salminen. 2010. First evidence of hexameric and heptameric ellagitannins in plants detected by liquid chromatography/electrospray ionisation mass spectrometry. Rapid Communications in Mass Spectrometry 24:3151-3156.
26. Kind, T., and O. Fiehn. 2007. Seven Golden Rules for heuristic filtering of molecular formulas obtained by accurate mass spectrometry. BMC Bioinformatics 8:105.
27. Kinney, K. K., R. L. Lindroth, S. M. Jung, and E. V. Nordheim. 1997. Effectts of CO2 and NO3-availability on deciduous trees: phytochemistry and insect performance. Ecology 78:215-230.
28. Knight, T. M., M. W. McCoy, J. M. Chase, K. A. McCoy, and R. D. Holt. 2005. Trophic cascades across ecosystems. Nature 437:880-883.
29. Lankau, R. A. 2007. Specialist and generalist herbivores exert opposing selection on a chemical defense. New Phytologist 175:176-184.
30. Mason, C., K. Rubert-Nason, R. Lindroth, and K. Raffa. 2015. Aspen defense chemicals influence midgut bacterial community composition of gypsy moth. Journal of Chemical Ecology 41:75-84.
31. Mattson, W. J. 1980. Herbivory in relation to plant nitrogen content. Annual Review of Ecology and Systematics 11:119-161.
32. McCutcheon, A. R., S. M. Ellis, R. E. W. Hancock, and G. H. N. Towers. 1994. Antifungal screening of medicinal plants of British Columbian native peoples. Journal of Ethnopharmacology 44:157-169.
33. Moilanen, J., and J.-P. Salminen. 2008. Ecologically neglected tannins and their biologically relevant activity: chemical structures of plant ellagitannins reveal their in vitro oxidative activity at high pH. Chemoecology 18:73-83.
34. Moilanen, J., J. Sinkkonen, and J.-P. Salminen. 2013. Characterization of bioactive plant ellagitannins by chromatographic, spectroscopic and mass spectrometric methods. Chemoecology 23:165-179.
35. Muilenburg, V. L., P. L. Phelan, P. Bonello, and D. A. Herms. 2011. Inter-and intra-specific variation in stem phloem phenolics of paper birch (Betula papyrifera) and European white birch (Betula pendula). Journal of Chemical Ecology 37:1193-1202.
36. Nakagawa, S., and H. Schielzeth. 2013. A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods in Ecology and Evolution 4:133-142.
37. Nakano, S., and M. Murakami. 2001. Reciprocal subsidies: dynamic interdependence between terrestrial and aquatic food webs. Proceedings of the National Academy of Sciences USA 98:166-170.
38. R Development Core Team. 2014. R version 3. R Project for Statistical Computing, Vienna, Austria. http://www.r-project.org
39. Rice, W. R., and S. D. Gaines. 1994. The ordered-heterogeneity family of tests. Biometrics 50:746-752.
40. Salminen, J.-P., and M. Karonen. 2011. Chemical ecology of tannins and other phenolics: we need a change in approach. Functional Ecology 25:325-338.
41. Sati, S. C., N. Sati, and O. P. Sati. 2011. Bioactive constituents and medicinal importance of genus Alnus. Pharmacognosy Reviews 5:174-183.
42. Schimel, J., R. Cates, and R. Ruess. 1998. The role of balsam poplar secondary chemicals in controlling soil nutrient dynamics through succession in the Alaskan taiga. Biogeochemistry 42:221-234.
43. Schweitzer, J. A., J. K. Bailey, B. J. Rehill, G. D. Martinsen, S. C. Hart, R. L. Lindroth, P. Keim, and T. G. Whitham. 2004. Genetically based trait in a dominant tree affects ecosystem processes. Ecology Letters 7:127-134.
44. Schweitzer, J., et al. 2008. From genes to ecosystems: the genetic basis of condensed tannins and their role in nutrient regulation in a populus model system. Ecosystems 11:1005-1020.
45. Stevens, M., A. Gusse, and R. Lindroth. 2014. Root chemistry in Populus tremuloides: effects of soil nutrients, defoliation, and genotype. Journal of Chemical Ecology 40:31-38.
46. Stout, R., W. Taft, and R. Merrit. 1985. Patterns of macroinvertebrate colonization on fresh and senescent alder leaves in two Michigan streams. Freshwater Biology 15:7.
47. Sunnerheim, K., and K. Bratt. 2004. Identification of centrolobol as the platyphylloside metabolite responsible for the observed effect on in vitro digestibility of hay. Journal of Agricultural and Food Chemistry 52:5869-5872.
48. Teece, M. A., and M. L. Fogel. 2007. Stable carbon isotope biogeochemistry of monosaccharides in aquatic organisms and terrestrial plants. Organic Geochemistry 38:458-473.
49. Thompson, J. N. 2005. The geographic mosaic of coevolution. University of Chicago Press, Chicago, Illinois, USA.
50. Vannote, R. L., G. W. Minshall, K. W. Cummins, J. R. Sedell, and C. E. Cushing. 1980. The river continuum concept. Canadian Journal of Fisheries and Aquatic Sciences 37:8.
51. Violle, C., B. J. Enquist, B. J. McGill, L. Jiang, C. H. Albert, C. Hulshof, V. Jung, and J. Messier. 2012. The return of the variance: intraspecific variability in community ecology. Trends in Ecology & Evolution 27:244-252.
52. Whitham, T. G., et al. 2006. A framework for community and ecosystem genetics: from genes to ecosystems. Nature Reviews Genetics 7:24.
53. Wright, M. S., and A. P. Covich. 2005. Relative importance of bacteria and fungi in a tropical headwater stream: leaf decomposition and invertebrate feeding preference. Microbial Ecology 49:536-546.