Imaging spectroscopy links aspen genotype with below-ground processes at landscape scales

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 369, Issue 1643, 2014, Pages

  Madritch, Michael D ^a   Kingdon, Clayton C ^b   Singh, Aditya ^b   Mock, Karen E ^c   Lindroth, Richard L ^b   Townsend, Philip A ^b  

^a APPALACHIAN STATE UNIVERSITY   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UTAH STATE UNIVERSITY   (United States)

Author keywords

Above and belowground linkages; Intraspecific diversity; Plant chemistry

Indexed keywords

AVIRIS; BIODIVERSITY; DATA SET; DECIDUOUS FOREST; ECOSYSTEM FUNCTION; GENOTYPE-ENVIRONMENT INTERACTION; IMAGING METHOD; INTRASPECIFIC VARIATION; LANDSCAPE ECOLOGY; OPTICAL PROPERTY; PHYTOCHEMISTRY; REMOTE SENSING; SPATIAL ANALYSIS; SPECTRAL ANALYSIS; SPECTROSCOPY; TANNIN;

NORTH AMERICA;

EID: 84898449139     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2013.0194     Document Type: Article

References (123)

1. Pereira HM et al. 2010 Scenarios for global biodiversity in the 21st century. Science 330, 1496-1501. (doi:10.1126/science.1196624)
2. Vitousek PM, Mooney HA, Lubchenco J, Melillo JM. 1997 Human domination of earth's ecosystems. Science 277, 494-499. (doi:10.1126/science.277.5325.494)
3. Haberl H, Erb KH, Krausmann F, Gaube V, Bondeau A, Plutzar C, Gingrich S, Lucht W, Fischer-Kowalski M. 2007 Quantifying and mapping the human appropriation of net primary production in earth's terrestrial ecosystems. Proc. Natl Acad. Sci. USA 104, 12942-12945. (doi:10.1073/pnas.0704243104)
4. Sgro CM, Lowe AJ, Hoffmann AA. 2011 Building evolutionary resilience for conserving biodiversity under climate change. Evol. Appl. 4, 326-337. (doi:10.1111/j.1752-4571.2010.00157.x)
5. Cardinale BJ et al. 2012 Biodiversity loss and its impact on humanity. Nature 486, 59-67. (doi:10. 1038/nature11148)
6. Naeem S, Duffy JE, Zavaleta E. 2012 The functions of biological diversity in an age of extinction. Science 336, 1401-1406. (doi:10.1126/science. 1215855)
7. Joppa LN, Visconti P, Jenkins CN, Pimm SL. 2013 Achieving the convention on biological diversity's goals for plant conservation. Science 341, 1100-1103. (doi:10.1126/science. 1241706)
8. Hughes AR, Inouye BD, Johnson MTJ, Underwood N, Vellend M. 2008 Ecological consequences of genetic diversity. Ecol. Lett. 11, 609-623. (doi:10.1111/j. 1461-0248.2008.01179.x)
9. Cadotte MW, Cavender-Bares J, Tilman D, Oakley TH. 2009 Using phylogenetic, functional and trait diversity to understand patterns of plant community productivity. PLoS ONE 4, e5695. (doi:10.1371/ journal.pone.0005695)
10. Cadotte MW, Carscadden K, Mirotchnick N. 2011 Beyond species: functional diversity and the maintenance of ecological processes and services. J. Appl. Ecol. 48, 1079-1087. (doi:10.1111/j.1365- 2664.2011.02048.x)
11. Connolly J, Cadotte MW, Brophy C, Dooley A, Finn J, Kirwan L, Roscher C, Weigelt A. 2011 Phylogenetically diverse grasslands are associated with pairwise interspecific processes that increase biomass. Ecology 92, 1385-1392. (doi:10.1890/10- 2270.1)
12. Flynn DFB, Mirotchnick N, Jain M, Palmer MI, Naeem S. 2011 Functional and phylogenetic diversity as predictors of biodiversity-ecosystem- function relationships. Ecology 92, 1573-1581. (doi:10.1890/10-1245.1)
13. Madritch MD, Hunter MD. 2002 Phenotypic diversity influences ecosystem functioning in an oak sandhills community. Ecology 83, 2084-2090. (doi:10.1890/0012-9658(2002)083[2084:PDIEFI]2.0.CO;2)
14. Madritch M, Donaldson JR, Lindroth RL. 2006 Genetic identity of Populus tremuloides litter influences decomposition and nutrient release in a mixed forest stand. Ecosystems 9, 528-537. (doi:10. 1007/s10021-006-0008-2)
15. Bailey JK et al. 2009 From genes to ecosystems: a synthesis of the effects of plant genetic factors across levels of organization. Phil. Trans. R. Soc. B 364, 1607-1616. (doi:10.1098/rstb.2008.0336)
16. Hargrave CW, Hambright KD, Weider LJ. 2011 Variation in resource consumption across a gradient of increasing intra- and interspecific richness. Ecology 92, 1226-1235. (doi:10.1890/09-1948.1)
17. Schweitzer JA, Fischer DG, Rehill BJ, Wooley SC, Woolbright SA, Lindroth RL, Whitham TG, Zak DR, Hart SC. 2011 Forest gene diversity is correlated with the composition and function of soil microbial communities. Popul. Ecol. 53, 35-46. (doi:10.1007/s10144-010-0252-3)
18. Genung MA, Bailey JK, Schweitzer JA. 2013 Belowground interactions shift the relative importance of direct and indirect genetic effects. Ecol. Evol. 3, 1692-1701. (doi:10.1002/ece3.582)
19. Secretariat of the Convention on Biological Diversity. 2010 Global Biodiversity Outlook 3. Montréal, Canada: Secretariat of the Convention on Biological Diversity.
20. Ustin SL, Roberts DA, Gamon JA, Asner GP, Green RO. 2004 Using imaging spectroscopy to study ecosystem processes and properties. Bioscience 54, 523-534. (doi:10.1641/0006-3568(2004)054 [0523:UISTSE]2.0. CO;2)
21. Kokaly RF, Asner GP, Ollinger SV, Martin ME, Wessman CA. 2009 Characterizing canopy biochemistry from imaging spectroscopy and its application to ecosystem studies. Remote Sens. Environ. 113, S78-S91. (doi:10. 1016/j.rse.2008.10.018)
22. Ustin SL, Gamon JA. 2010 Remote sensing of plant functional types. New Phytol. 186, 795-816. (doi:10.1111/j.1469-8137.2010.03284.x)
23. Martin ME, Aber JD. 1997 High spectral resolution remote sensing of forest canopy lignin, nitrogen, and ecosystem processes. Ecol. Appl. 7, 431-443. (doi:10.1890/1051-0761(1997)007[0431:HSRRSO]2. 0.CO;2)
24. Ollinger SV, Smith ML, Martin ME, Hallett RA, Goodale CL, Aber JD. 2002 Regional variation in foliar chemistry and N cycling among forests of diverse history and composition. Ecology 83, 339-355.
25. Townsend PA, Foster JR, Chastain RA, Currie WS. 2003 Application of imaging spectroscopy to mapping canopy nitrogen in the forests of the central Appalachian Mountains using Hyperion and AVIRIS. IEEE Trans. Geosci. Remote Sens. 41, 1347-1354. (doi:10.1109/TGRS.2003.813205)
26. Martin ME, Plourde LC, Ollinger SV, Smith ML, McNeil BE. 2008 A generalizable method for remote sensing of canopy nitrogen across a wide range of forest ecosystems. Remote Sens. Environ. 112, 3511-3519. (doi:10.1016/j.rse.2008.04.008)
27. Ollinger SV. 2011 Sources of variability in canopy reflectance and the convergent properties of plants. New Phytol. 189, 375-394. (doi:10.1111/j.1469- 8137.2010.03536.x)
28. Asner GP, Martin RE. 2011 Canopy phylogenetic, chemical and spectral assembly in a lowland Amazonian forest. New Phytol. 189, 999-1012. (doi:10.1111/j.1469-8137.2010.03549.x)
29. Gillespie TW, Foody GM, Rocchini D, Giorgi AP, Saatchi S. 2008 Measuring and modelling biodiversity from space. Prog. Phys. Geogr. 32, 203-221. (doi:10.1177/0309133308093606)
30. Schimel DS, Asner GP, Moorcroft P. 2013 Observing changing ecological diversity in the Anthropocene. Front. Ecol. Environ. 11, 129-137. (doi:10. 1890/120111)
31. Stoms DM, Estes JE. 1993 A remote-sensing research agenda for mapping and monitoring biodiversity. Int. J. Remote Sens. 14, 1839-1860. (doi:10.1080/ 01431169308954007)
32. Turner W, Spector S, Gardiner N, Fladeland M, Sterling E, Steininger M. 2003 Remote sensing for biodiversity science and conservation. Trends Ecol. Evol. 18, 306-314. (doi:10.1016/S0169-5347(03) 00070-3)
33. Rocchini D et al. 2010 Remotely sensed spectral heterogeneity as a proxy of species diversity: recent advances and open challenges. Ecol. Inf. 5, 318-329. (doi:10.1016/j.ecoinf.2010.06.001)
34. Asner GP, Martin RE. 2008 Spectral and chemical analysis of tropical forests: scaling from leaf to canopy levels. Remote Sens. Environ. 112, 3958-3970. (doi:10.1016/j.rse.2008.07.003)
35. Martin ME, Newman SD, Aber JD, Congalton RG. 1998 Determining forest species composition using high spectral resolution remote sensing data. Remote Sens. Environ. 65, 249-254. (doi:10.1016/ S0034-4257(98)00035-2)
36. Key T, Warner TA, McGraw JB, Fajvan MA. 2001 A comparison of multispectral and multitemporal information in high spatial resolution imagery for classification of individual tree species in a temperate hardwood forest. Remote Sens. Environ. 75, 100-112. (doi:10.1016/S0034-4257(00)00159-0)
37. Clark ML, Roberts DA, Clark DB. 2005 Hyperspectral discrimination of tropical rain forest tree species at leaf to crown scales. Remote Sens. Environ. 96, 375-398. (doi:10.1016/j.rse.2005.03.009)
38. Carlson KM, Asner GP, Hughes RF, Ostertag R, Martin RE. 2007 Hyperspectral remote sensing of canopy biodiversity in Hawaiian lowland rainforests. Ecosystems 10, 536-549. (doi:10.1007/s10021-007-9041-z)
39. Asner GP, Martin RE. 2009 Airborne spectranomics: mapping canopy chemical and taxonomic diversity in tropical forests. Front. Ecol. Environ. 7, 269-276. (doi:10.1890/070152)
40. Mitton JB, Grant MC. 1996 Genetic variation and the natural history of quaking aspen. Bioscience 46, 25-31. (doi:10.2307/1312652)
41. Kanaga MK, Ryel RJ, Mock KE, Pfrender ME. 2008 Quantitative-genetic variation in morphological and physiological traits within a quaking aspen (Populus tremuloides) population. Can. J. For. Res. 38, 1690-1694. (doi:10.1139/X08-012)
42. DeWoody J, Rowe CA, Hipkins VD, Mock KE. 2008 'Pando' lives: molecular genetic evidence of a giant Aspen clone in central Utah. Western North Am. Nat. 68, 493-497. (doi:10.3398/1527-0904-68.4.493)
43. Barnes BV. 1966 Clonal growth habit of American aspens. Ecology 47, 439-447. (doi:10.2307/1932983)
44. Mock KE et al. 2012 Widespread triploidy in western North American aspen (Populus tremuloides). PLoS ONE 7, e48406. (doi:10.1371/journal.pone.0048406)
45. Mock KE, Rowe CA, Hooten MB, Dewoody J, Hipkins VD. 2008 Clonal dynamics in western North American aspen (Populus tremuloides). Mol. Ecol. 17, 4827-4844. (doi:10.1111/j.1365-294X.2008.03963.x)
46. Michaelian M, Hogg EH, Hall RJ, Arsenault E. 2011 Massive mortality of aspen following severe drought along the southern edge of the Canadian boreal forest. Glob. Change Biol. 17, 2084-2094. (doi:10.1111/j.1365-2486.2010.02357.x)
47. Worrall JJ, Rehfeldt GE, Hamann A, Hogg EH, Marchetti SB, Michaelian M, Gray LK. 2013 Recent declines of Populus tremuloides in North America linked to climate. For. Ecol. Manage. 299, 35-51. (doi:10.1016/j.foreco.2012.12.033)
48. Shields WJ, Bockheim JG. 1981 Deterioration of trembling aspen clones in the Great-Lakes region. Can. J. For. Res. 11, 530-537. (doi:10.1139/x81-073)
49. Frey BR, Lieffers VJ, Hogg EH, Landhausser SM. 2004 Predicting landscape patterns of aspen dieback: mechanisms and knowledge gaps. Can. J. For. Res. 34, 1379-1390. (doi:10.1139/x04-062)
50. Worrall JJ, Egeland L, Eager T, Mask RA, Johnson EW, Kemp PA, Shepperd WD. 2008 Rapid mortality of Populus tremuloides in southwestern Colorado, USA. For. Ecol. Manage. 255, 686-696. (doi:10. 1016/j.foreco.2007.09.071)
51. Lindroth RL, Hwang SY. 1996 Clonal variation in foliar chemistry of quaking aspen (Populus tremuloides Michx). Biochem. Syst. Ecol. 24, 357-364. (doi:10.1016/0305-1978(96)00043-9)
52. Donaldson JR, Lindroth RL. 2007 Genetics, environment, and their interaction determine efficacy of chemical defense in trembling aspen. Ecology 88, 729-739. (doi:10.1890/06-0064)
53. Bennett RN, Wallsgrove RM. 1994 Secondary metabolies in plant defense mechanisms. New Phytol. 127, 617-633. (doi:10.1111/j.1469-8137.1994.tb02968.x)
54. Kraus TEC, Dahlgren RA, Zasoski RJ. 2003 Tannins in nutrient dynamics of forest ecosystems: a review. Plant Soil 256, 41-66. (doi:10.1023/A:1026206511084)
55. Hattenschwiler S, Vitousek PM. 2000 The role of polyphenols in terrestrial ecosystem nutrient cycling. Trends Ecol. Evol. 15, 238-243. (doi:10.1016/ S0169-5347(00)01861-9)
56. Haettenschwiler S, Coq S, Barantal S, Handa IT. 2011 Leaf traits and decomposition in tropical rainforests: revisiting some commonly held views and towards a new hypothesis. New Phytol. 189, 950-965. (doi:10.1111/j.1469-8137.2010.03483.x)
57. Joanisse GD, Bradley RL, Preston CM, Bending GD. 2009 Sequestration of soil nitrogen as tanninprotein complexes may improve the competitive ability of sheep laurel (Kalmia angustifolia) relative to black spruce (Picea mariana). New Phytol. 181, 187-198. (doi:10.1111/j.1469-8137.2008.02622.x)
58. Madritch MD, Lindroth RL. 2011 Soil microbial communities adapt to genetic variation in leaf litter inputs. Oikos 120, 1696-1704. (doi:10.1111/j.1600-0706.2011.19195.x)
59. Madritch MD, Greene SL, Lindroth RL. 2009 Genetic mosaics of ecosystem functioning across aspendominated landscapes. Oecologia 160, 119-127. (doi:10.1007/s00442-009-1283-3)
60. Madritch MD, Donaldson JR, Lindroth RL. 2007 Canopy herbivory can mediate the influence of plant genotype on soil processes through frass deposition. Soil Biol. Biochem. 39, 1192-1201. (doi:10.1016/j.soilbio.2006.12.027)
61. Schweitzer JA 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. (doi:10.1007/s10021-008-9173-9)
62. Schweitzer JA, Bailey JK, Hart SC, Whitham TG. 2005 Nonadditive effects of mixing cottonwood genotypes on litter decomposition and nutrient dynamics. Ecology 86, 2834-2840. (doi:10.1890/04-1955)
63. Schweitzer JA, Bailey JK, Rehill BJ, Martinsen GD, Hart SC, Lindroth RL, Keim P, Whitham TG. 2004 Genetically based trait in a dominant tree affects ecosystem processes. Ecol. Lett. 7, 127-134. (doi:10.1111/j.1461-0248.2003.00562.x)
64. Cardinale BJ, Matulich KL, Hooper DU, Byrnes JE, Duffy E, Gamfeldt L, Balvanera P, O'Connor MI, Gonzalez A. 2011 The functional role of producer diversity in ecosystems. Am. J. Bot. 98, 572-592. (doi:10.3732/ajb.1000364)
65. Wolter PT, Mladenoff DJ, Host GE, Crow TR. 1995 Improved forest classification in the northern Lake- States using multitemporal Landsat imagery. Photogramm. Eng. Remote Sens. 61, 1129-1143.
66. Wolter PT, Townsend PA. 2011 Multi-sensor data fusion for estimating forest species composition and abundance in northern Minnesota. Remote Sens. Environ. 115, 671-691. (doi:10.1016/j.rse.2010.10.010)
67. Reese HM, Lillesand TM, Nagel DE, Stewart JS, Goldmann RA, Simmons TE, Chipman JW, Tessar PA. 2002 Statewide land cover derived from multiseasonal Landsat TM data: a retrospective of the WISCLAND project. Remote Sens. Environ. 82, 224-237. (doi:10.1016/S0034-4257(02)00039-1)
68. Townsend PA, Walsh SJ. 2001 Remote sensing of forested wetlands: application of multitemporal and multispectral satellite imagery to determine plant community composition and structure in southeastern USA. Plant Ecol. 157, 129-149A. (doi:10.1023/A:1013999513172)
69. Smulders MJM, Van Der Schoot J, Arens P, Vosman B. 2001 Trinucleotide repeat microsatellite markers for black poplar (Populus nigra L.). Mol. Ecol. Notes 1, 188-190. (doi:10.1046/j.1471-8278.2001.00071.x)
70. Tuskan GA et al. 2006 The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313, 1596-1604. (doi:10.1126/science.1128691)
71. Callahan CM, Rowe CA, Ryel RJ, Shaw JD, Madritch MD, Mock KE. 2013 Continental-scale assessment of genetic diversity and population structure in quaking aspen (Populus tremuloides). J. Biogeogr. 40, 1780-1791. (doi:10.1111/jbi.12115)
72. Porter LJ, Hrstich LN, Chan BG. 1986 The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry 25, 223-230. (doi:10. 1016/S0031-9422(00)94533-3)
73. Hagerman AE, Butler LG. 1989 Choosing appropriate methods and standards for assaying tannin. J. Chem. Ecol. 15, 1795-1810. (doi:10.1007/BF01012267)
74. Bruce RJ, West CA. 1989 Elicitation of lignin biosynthesis and isoperoxidase activity by pectic fragments in suspension-cultures of castor bean. Plant Physiol. 91, 889-897. (doi:10.1104/pp.91.3.889)
75. Suzuki S, Suzuki Y, Yamamoto N, Hattori T, Sakamoto M, Umezawa T. 2009 High-throughput determination of thioglycolic acid lignin from rice. Plant Biotechnol. 26, 337-340. (doi:10.5511/plantbiotechnology.26.337)
76. Mulvaney R. 1996 Nitrogen: inorganic forms. In Methods of soil analysis. Part 3. Chemical methods (ed. J Bartels), pp. 1123-1184. Madison, WI: Soil Science Society of America.
77. Doane TA, Horwath WR. 2003 Spectrophotometric determination of nitrate with a single reagent. Anal. Lett. 36, 2713-2722. (doi:10.1081/AL-120024647)
78. Sinsabaugh RL, Moorhead DL. 1994 Resourceallocation to extracellular enzyme-production: a model for nitrogen and phosphorus control of litter decomposition. Soil Biol. Biochem. 26, 1305-1311. (doi:10.1016/0038-0717(94)90211-9)
79. Sinsabaugh RL, Reynolds H, Long TM. 2000 Rapid assay for amidohydrolase (urease) activity in environmental samples. Soil Biol. Biochem. 32, 2095-2097. (doi:10.1016/S0038-0717(00)00102-4)
80. Saiya-Cork KR, Sinsabaugh RL, Zak DR. 2002 The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol. Biochem. 34, 1309-1315. (doi:10.1016/S0038-0717(02)00074-3)
81. Allison SD. 2012 A trait-based approach for modelling microbial litter decomposition. Ecol. Lett. 15, 1058-1070. (doi:10.1111/j.1461-0248.2012.01807.x)
82. Caldwell BA. 2005 Enzyme activities as a component of soil biodiversity: a review. Pedobiologia 49, 637-644. (doi:10.1016/j.pedobi.2005.06.003)
83. Montes MJJ, Fusina RA, Donato TF, Bachmann CM, Bo-Cai G. 2004 The effects of atmospheric correction schemes on the hyperspectral imaging of littoral environments. In IGARSS 2004 Proc., Science for Society: Exploring and Managing a Changing Planet, 20-24 September, 2004, Anchorage, Alaska (IEEE cat. no. 04CH37612), vol. 4186, pp. 4187-4190. Piscataway, NJ: IEEE.
84. Soenen SA, Peddle DR, Coburn CA. 2005 SCS {thorn} C: a modified sun-canopy-sensor topographic correction in forested terrain. IEEE Trans. Geosci. Remote Sens. 43, 2148-2159. (doi:10.1109/TGRS. 2005.852480)
85. Roujean JL, Leroy M, Deschamps PY. 1992 A bidirectional reflectance model of the Earth's surface for the correction of remote-sensing data. J. Geophys. Res. Atmos. 97, 20455-20468. (doi:10.1029/92JD01411)
86. Lucht W, Schaaf CB, Strahler AH. 2000 An algorithm for the retrieval of albedo from space using semiempirical BRDF models. IEEE Trans. Geosci. Remote Sens. 38, 977-998. (doi:10.1109/36.841980)
87. Penuelas J, Gamon JA, Fredeen AL, Merino J, Field CB. 1994 Reflectance indexes associated with physiological changes in nitrogen-limited and water-limited sunflower leaves. Remote Sens. Environ. 48, 135-146. (doi:10.1016/0034-4257(94)90136-8)
88. Dormann CF et al. 2007 Methods to account for spatial autocorrelation in the analysis of species distributional data: a review. Ecography 30, 609-628. (doi:10.1111/j.2007.0906-7590.05171.x)
89. Terbraak CJF. 1986 Canonical correspondence analysis: a new eigenvector technique for multivariate direct gradient analysis. Ecology 67, 1167-1179. (doi:10.2307/1938672)
90. Perez-Enciso M, Tenenhaus M. 2003 Prediction of clinical outcome with microarray data: a partial least squares discriminant analysis (PLS-DA) approach. Hum. Genet. 112, 581-592.
91. Barker M, Rayens W. 2003 Partial least squares for discrimination. J. Chemometr. 17, 166-173. (doi:10.1002/cem.785)
92. Wold S, Ruhe A, Wold H, Dunn WJ. 1984 The collinearity problem in linear-regression: the partial least-squares (PLS) approach to generalized inverses. SIAM J. Sci. Stat. Comput. 5, 735-743. (doi:10.1137/0905052)
93. Geladi P, Kowalski BR. 1986 Partial least-squares regression: a tutorial. Anal. Chim. Acta 185, 1-17. (doi:10.1016/0003-2670(86)80028-9)
94. Wolter PT, Townsend PA, Sturtevant BR, Kingdon CC. 2008 Remote sensing of the distribution and abundance of host species for spruce budworm in Northern Minnesota and Ontario. Remote Sens. Environ. 112, 3971-3982. (doi:10.1016/j.rse.2008.07.005)
95. Wold S, Sjostrom M, Eriksson L. 2001 PLSregression: a basic tool of chemometrics. Chemometr. Intell. Lab. Syst. 58, 109-130. (doi:10. 1016/S0169-7439(01)00155-1)
96. Kuhn M. 2008 Building predictive models in R using the caret package. J. Stat. Softw. 28, 1-26.
97. Venables WN, Ripley BD. 2002 Modern applied statistics with S, 4th edn, pp. 331-338. New York, NY: Springer.
98. Mantel N. 1967 Detection of disease clustering and a generalized regression approach. Cancer Res. 27, 209.
99. Legendre P, Fortin MJ. 1989 Spatial pattern and ecological analysis. Vegetatio 80, 107-138. (doi:10.1007/BF00048036)
100. Oksanen J et al. 2013 vegan: community ecology package. R package version 2.0-9.
101. Bruvo R, Michiels NK, D'Souza TG, Schulenburg H. 2004 A simple method for the calculation of microsatellite genotype distances irrespective of ploidy level. Mol. Ecol. 13, 2101-2106. (doi:10. 1111/j.1365-294X.2004.02209.x)
102. Dray S, Dufour A-B. 2007 The ade4 package: implementing the duality diagram for ecologists. J. Stat. Softw. 22, 1-20.
103. Smith ML, Martin ME, Plourde L, Ollinger SV. 2003 Analysis of hyperspectral data for estimation of temperate forest canopy nitrogen concentration: comparison between an airborne (AVIRIS) and a spaceborne (Hyperion) sensor. IEEE Trans. Geosci. Remote Sens. 41, 1332-1337. (doi:10.1109/TGRS. 2003.813128)
104. Asner GP, Knapp DE, Kennedy-Bowdoin T, Jones MO, Martin RE, Boardman J, Hughes RF. 2008 Invasive species detection in Hawaiian rainforests using airborne imaging spectroscopy and LiDAR. Remote Sens. Environ. 112, 1942-1955. (doi:10. 1016/j.rse.2007.11.016)
105. Gamon JA, Bond B. 2013 Effects of irradiance and photosynthetic downregulation on the photochemical reflectance index in Douglas-fir and ponderosa pine. Remote Sens. Environ. 135, 141-149. (doi:10.1016/j.rse.2013.03.032)
106. Gamon JA, Penuelas J, Field CB. 1992 A narrowwaveband spectral index that tracks diurnal changes in photosynthetic efficiency. Remote Sens. Environ. 41, 35-44. (doi:10.1016/0034-4257(92) 90059-S)
107. Curran PJ. 1989 Remote-sensing of foliar chemistry. Remote Sens. Environ. 30, 271-278. (doi:10.1016/0034-4257(89)90069-2)
108. Elvidge CD. 1990 Visible and near-infrared reflectance characteristics of dry plant material. Int. J. Remote Sens. 11, 1775-1795. (doi:10.1080/ 01431169008955129)
109. Ferwerda JG, Skidmore AK, Stein A. 2006 A bootstrap procedure to select hyperspectral wavebands related to tannin content. Int. J. Remote Sens. 27, 1413-1424. (doi:10.1080/01431160500497119)
110. Rubert-Nason KF, Holeski LM, Couture JJ, Gusse A, Undersander DJ, Lindroth RL. 2013 Rapid phytochemical analysis of birch (Betula) and poplar (Populus) foliage by near-infrared reflectance spectroscopy. Anal. Bioanal. Chem. 405, 1333-1344. (doi:10.1007/s00216-012-6513-6)
111. Whitham TG, Gehring CA, Lamit LJ, Wojtowicz T, Evans LM, Keith AR, Smith DS. 2012 Community specificity: life and afterlife effects of genes. Trends Plant Sci. 17, 271-281. (doi:10.1016/j.tplants.2012. 01.005)
112. Osier TL, Lindroth RL. 2006 Genotype and environment determine allocation to and costs of resistance in quaking aspen. Oecologia 148, 293-303. (doi:10.1007/s00442-006-0373-8)
113. Cornwell WK et al. 2008 Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecol. Lett. 11, 1065-1071. (doi:10.1111/j.1461-0248.2008.01219.x)
114. Ustin SL, Gitelson AA, Jacquemoud S, Schaepman M, Asner GP, Gamon JA, Zarco-Tejada P. 2009 Retrieval of foliar information about plant pigment systems from high resolution spectroscopy. Remote Sens. Environ. 113, S67-S77. (doi:10.1016/j.rse.2008.10.019)
115. Gamon JA, Serrano L, Surfus JS. 1997 The photochemical reflectance index: an optical indicator of photosynthetic radiation use efficiency across species, functional types, and nutrient levels. Oecologia 112, 492-501. (doi:10.1007/s004420050337)
116. Lewis P, Disney M. 2007 Spectral invariants and scattering across multiple scales from within-leaf to canopy. Remote Sens. Environ. 109, 196-206. (doi:10.1016/j.rse.2006.12.015)
117. Baldeck CA, Asner GP. 2013 Estimating vegetation beta diversity from airborne imaging spectroscopy and unsupervised clustering. Remote Sens. 5, 2057-2071. (doi:10.3390/rs5052057)
118. Scioneaux AN, Schmidt MA, Moore MA, Lindroth RL, Wooley SC, Hagerman AE. 2011 Qualitative variation in proanthocyanidin composition of populus species and hybrids: genetics is the key. J. Chem. Ecol. 37, 57-70. (doi:10.1007/s10886-010-9887-y)
119. Merila J, Crnokrak P. 2001 Comparison of genetic differentiation at marker loci and quantitative traits. J. Evol. Biol. 14, 892-903. (doi:10.1046/j.1420-9101.2001.00348.x)
120. Wardle DA, Bardgett RD, Klironomos JN, Setala H, van der Putten WH, Wall DH. 2004 Ecological linkages between aboveground and belowground biota. Science 304, 1629-1633. (doi:10.1126/science.1094875)
121. van der Putten WH et al. 2013 Plant-soil feedbacks: the past, the present and future challenges. J. Ecol. 101, 265-276. (doi:10.1111/1365-2745.12054)
122. Townsend PA, Serbin SP, Kruger EL, Gamon JA. 2013 Disentangling the contribution of biological and physical properties of leaves and canopies in imaging spectroscopy data. Proc. Natl Acad. Sci. USA 110, E1074-E1074. (doi:10.1073/pnas.1300952110)
123. Gamon J. 2008 Tropical remote sensing: opportunities and challenges. In Hyperspectral remote sensing of tropical and subtropical forests (eds M Kalacska, GA Sanchez-Azofeifa), pp. 297-305. New York, NY: CRC Press.