Sources of Canopy Chemical and Spectral Diversity in Lowland Bornean Forest
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- Asner, G.P., Martin, R.E. & Suhaili, A.B. Ecosystems (2012) 15: 504. doi:10.1007/s10021-012-9526-2
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Sources of variation among the chemical and spectral properties of tropical forest canopies are poorly understood, yet chemical traits reveal potential ecosystem and phylogenetic controls, and spectral linkages to chemical traits are needed for remote sensing of functional and biological diversity. We analyzed 21 leaf traits in 395 fully sunlit canopies, representing 232 species and multiple growth forms, in a lowland mixed dipterocarp forest of Sarawak, Malaysia. Leaf traits related to light capture and growth (for example, photosynthetic pigments, nutrients) were up to 55% lower, and defense traits (for example, phenols, lignin) were 15–40% higher, in the dominant family Dipterocarpaceae and in its genus Shorea, as compared to all other canopy species. The chemical variation within Dipterocarpaceae and Shorea was equivalent to that of all other canopy species combined, highlighting the role that a single phylogenetic branch can play in creating canopy chemical diversity. Seventeen of 21 traits had more than 50% of their variation explained by taxonomic grouping, and at least 16 traits show a connection to remotely sensed spectroscopic signatures (RMSE < 15%). It is through these chemical-to-spectral linkages that studies of functional and biological diversity interactions become possible at larger spatial scales, thereby improving our understanding of the role of species in tropical forest ecosystem dynamics.
Keywordscanopy chemistrymixed dipterocarp forestleaf chemistryMalaysia remote sensingSarawakspectranomics
Humid tropical forests are comprised of thousands of plant species, of which a substantial fraction can acquire upper canopy position, thereby accessing direct-beam solar radiation. These canopy species play a major role in the uptake of carbon from and release of water to the atmosphere, as well as myriad biogeochemical interactions. They also provide sub-canopy conditions and habitat for the entire food web.
Canopy species diversity and ecosystem function are linked through a variety of pathways; one in particular is canopy foliage, and the chemicals contained with leaves. Leaf chemicals can be partitioned functionally into major groups related to light capture and growth, longevity and defense, and maintenance and metabolism. Leaf nitrogen (N), phosphorus (P), water, and chlorophyll-a and -b (chl-a, chl-b), as well as leaf mass per area (LMA), adjust to regulate physiological processes including carbon (C) fixation (Field and Mooney 1986; Poorter and Evans 1998). Secondary metabolites such as lignin, cellulose, phenols, and tannins contribute to foliar defense and longevity (Dudt and Shure 1994). Maintenance-metabolism elements are those required in small quantities to support and mediate multiple functions within the leaf (Schlesinger 1991). Along with carbon fractions such as lignin, foliar concentrations of N, P, and base cations (Ca, K, Mg) are tied to ecosystem-level nutrient cycling and decomposition rates (Vitousek 1984; Aerts 1997). Although regional variation in climate, soils and other factors impart variation in many foliar traits (Vitousek and Sanford 1986), species composition is another determinant of spatial variation in tropical forest canopy chemistry (Townsend and others 2008). Despite the suggestion of a link between biological and chemical trait diversity in tropical forest systems, the nature of that connection remains unclear, because floristic composition also varies within and among different forest types, which may affect the degree to which species dictate canopy chemical patterns.
In recent work from lowland Amazonia, leaf chemical traits ranging from growth-related nutrients, to defense and maintenance compounds, were explicitly linked to variation in species composition across contrasting sites (Fyllas and others 2009; Asner and Martin 2011). Both studies considered substrate controls over canopy chemical traits and LMA, finding that site fertility is expressed in foliar chemical concentrations, but that taxonomy remains an important factor within a site. However, these studies were Neotropical, and thus may not be the representative of other regions or of distant phylogenies. Tropical forest canopies of SE Asia and Oceania are often dominated by species in the Dipterocarpaceae (Ashton 1987; Ashton and others 1988), a family not found in the Neotropics. In a study of lowland Bornean rainforest, Paoli (2006) had uncovered a differential effect of environment and phylogeny on leaf chemical and trait variation: Within the common Dipterocarpaceae genus Shorea, foliar P and LMA variation was influenced more by soil fertility than was foliar N, which more closely tracked phylogeny. Like many studies, however, this one included plants in their sapling stage, and shade variation in the forest understory imparts major foliar chemical variation that, although an important contribution to ecosystem processes, can trump phylogenetic- or environment-based chemical patterns, observed when lighting conditions are held constant (Dudt and Shure 1994; Kitajima and others 2005; Poorter and others 2009). In Sarawak, Kurokawa and Nakashizuka (2008) did control for canopy illumination conditions, while seeking linkages between foliar herbivory and decomposition rates, finding that total N and C display a significant degree of phylogenetic structure. Furthermore, Kenzo and others (2004) found that inter-specific differences in leaf traits were on par with variation linked to light availability determined by tree height (Kenzo and others 2006). Other than a few studies focused on inventories of some canopy chemicals in Bornean forests (Breulmann and others 1998; Breulmann and others 1999), we are aware of no work that evaluates sources of multichemical variation among canopy species in the region, and this information is needed to improve our understanding of whole-canopy and ecosystem function.
Ecological patterns in leaf properties may be measureable well beyond chemical traits, such as in the spectral optical properties of the foliage (Curran 1989; Jacquemoud and others 1995; Sanchez-Azofeifa and others 2009). Imaging spectroscopy, which can resolve contiguous optical reflectance signatures (for example, 400–2,500 nm) of vegetation from aircraft and spacecraft, has proven the most effective means to remotely estimate canopy chemical properties (reviews by Kokaly and others 2009; Ustin and others 2009). However, the strength of a chemical-to-spectral link remains unknown for most vegetation types, and has proven particularly challenging to ascertain in biologically diverse canopies of the humid tropics. Even as remote sensing of leaf traits stands to provide an essential tool to extend chemical information to spatial scales relevant to ecosystem dynamics, we are aware of no studies to quantify relationships between foliar chemical and spectral traits among Bornean forest canopy taxa, which might subsequently advance the role of remote sensing for use in studies of these ecosystems.
Here, we report on the chemical and spectral variation among 395 lowland humid tropical forest canopies in Borneo. We sought to quantify variation in leaf traits within and among canopy species, and to develop a quantitative link between those traits and remotely sensed data. We considered variation in 20 chemical properties, ranging from photosynthetic pigments to carbon compounds and micro-nutrients, as well as LMA, within species, among plant growth forms, and taxonomically. We then determined the relationship between these traits and canopy reflectance spectroscopy using a combination of measurement and modeling techniques. We focused effort at the top of canopy where sunlight control could be applied. We did not measure leaf traits within the canopy vertical profile because changes in leaf properties generally follow light gradients within canopies, and although these relationships vary across species, they can be accounted for when modeling of canopy chemistry and reflectance based on top-of-canopy foliar traits (Poorter and others 1995; Bondeau and others 1999; Asner 2008).
Materials and Methods
The study was conducted in the Lambir Hills National Park in the Malaysian state of Sarawak, on the Island of Borneo. Vegetation is classified as lowland mixed dipterocarp forest (Ashton 2005), and as moist lowland tropical forest in the Holdridge system. Soils are classified as Ultisols, with sub-order variation from sandy humults to clayey udults based on highly localized terrain variation on the order of meters (Seng Lee and others 2004). Mean annual precipitation and temperature are 2,450 mm y−1 and 26.3°C, respectively.
Sample collection was carried out over an area of about 100 ha neighboring the Lambir 52-ha plot, that is, part of the Center for Tropical Forest Science (CTFS) network (Condit and others 2005). The canopy ranges in height from 30 to 60 m. The 52-ha plot census data show the canopy to be dominated by individuals in the Dipterocarpaceae, representing more than 40% of the stand-level basal area for all stems larger than 1 cm in diameter (Seng Lee and others 2004). Based on CTFS plot data, we estimate that 300 tree species occupy the upper, sunlit canopy in and around the 52-ha plot, with an additional 25–50 liana species likely to be present (Putz and Chai 1987).
To capture the diversity of sunlit canopies throughout the site, while also maintaining statistical power for replication at the family, genus, and species levels, we sampled 395 individual canopies (tree = 377; liana = 18) from 232 unique species. The 232 species were partitioned into 108 genera and 49 families, including 96 samples for 36 species in 6 genera within the dominant family Dipterocarpaceae and 16 species in 8 genera from the second most important family Euphorbiaceae (Table S1). Of the total, 86 species were selected for replication. Different levels of replication were based on the requirements of the various statistical analyses employed in the study (Supplemental Information online). Overall, our sampling structure captured the most common species, with repeat measurements among them (19% of the species with three or more representatives), as well as the less common species, and as a result, our partitioning approximates the relative abundance of canopy individuals on a basal area basis (Seng Lee and others 2004).
Strict measures were taken to collect samples from fully sunlit canopies. Vouchers were collected from all selected individuals and matched by local expert taxonomists to type specimens kept at the Sarawak Herbarium, Forest Research Centre. We also matched genus names to information provided by Kew Botanic Gardens and revised the family-level taxonomy to follow the Angiosperm Phylogeny Group III (Stevens 2010). Project reference vouchers are kept at the Carnegie Institution facility, and reference photos of all specimens can be viewed at http://spectranomics.ciw.edu.
Leaf Chemical Traits
Leaf collections were conducted using tree climbing techniques and the Sarawak canopy crane facility (Kumagai and others 2004). Only fully sunlit branches of mature leaves were taken and transported to a local site for processing within 15 min of collection. A chemical profile, including 20 chemical elements and compounds as well as LMA, was developed for each sample. Statistical analyses included general linear modeling, nested random-effects analysis of variance (ANOVA) modeling, principal components analysis (PCA), and stepwise linear discriminant analysis (LDA). Detailed methodologies are provided in the Supplementary Information online, and laboratory protocols are downloadable from the Carnegie Spectranomics website (http://spectranomics.ciw.edu).
Leaf and Canopy Spectroscopy
Hemispherical reflectance and transmittance spectra spanning the 400–2,500 nm wavelength range were measured on 12 leaf surfaces immediately after acquiring each branch in the field. The spectral measurements were taken at or close to the mid-point between the main vein and the leaf edge, and approximately half-way from petiole to leaf tip. Care was taken to avoid large primary or secondary veins, while allowing for smaller veins to be incorporated into the measurement. The spectra were collected with a field spectroradiometer (FS-3 with custom detectors and exit slit configuration to maximize signal-to-noise performance; Analytical Spectra Devices, Inc., Boulder, Colorado USA), an integrating sphere designed for high-resolution spectroscopic measurements, and a custom illumination collimator (Supplemental Information). Twenty-five spectra per sample were averaged and calibrated for dark current and stray light, then referenced to a calibration block within the integrating sphere (Spectralon, Labsphere Inc., Durham, New Hampshire USA).
We projected the measured leaf reflectance and transmittance spectra to the canopy level using a radiative transfer model described by Asner and Martin (2008) and in the Supplemental Information online. The model simulates top-of-canopy spectral reflectance based on the measured leaf spectra and incorporates variation of leaf area index (LAI), leaf angle distribution, and other crown geometric-optical properties as they are distributed throughout the canopy. For each field-based sample, a randomly-selected combination of canopy structural parameters based on growth habit was used to generate a canopy reflectance signature. Ranges for LAI and other structural parameters for each growth habit (tree, liana, hemi-epiphyte, palm, vine) were taken from Asner and others (2003) and Asner and Martin (2008). This was repeated 250 times per sample, and the mean reflectance signatures were recorded for subsequent analyses.
Canopy Chemical Variation
Descriptive Statistics for Leaf Traits, Arranged by Broad Functional Group, Collected from Sunlit Canopies in Lambir Hills National Park, Sarawak
Light capture and growth
Chl-a (mg g−1)
Chl-b (mg g−1)
Carotenoids (mg g−1)
LMA (g m−2)
Longevity and defense
Soluble C (%)
Phenols (mg g−1)
Tannins (mg g−1)
Maintenance and metabolism
Zn (μg g−1)
Mn (μg g−1)
B (μg g−1)
Fe (μg g−1)
Inter-relationships Among Leaf Properties
Principal Components Analysis (PCA) Results for Different Combinations of Leaf Properties
Variance explained (%)
Chl a, Chl b and carotenoids
LMA, N, and P
N, P, Ca, K, and Mg
Soluble C, cellulose, hemi-cellulose, and lignin
i + ii + iii + iv above
Remote sensing properties1
All leaf properties
We also considered other leaf trait combinations, beginning with photosynthetic pigments alone, for which PC1 accounted for more than 96% of the variation (Table 2). Among three of the ‘leaf economics spectrum’ traits of LMA, N and P (Reich and Oleskyn 2004; Wright and others 2004), we found that PC1 accounted for nearly 70% of the variability. However, PCA indicated weaker explanatory power among combinations of C fractions (58%). Again, similar patterns were found when limiting the analysis to the Dipterocarpaceae (data not shown). Correlation analyses supported the PCA results, indicating weak correlations, with r values less than 0.40 for more than 90% of the trait pairs (Table S4). Major exceptions included inter-correlations among photosynthetic pigments (r = 0.95–0.97), which were expected based on our PCA results (Table 2), and which are well understood biologically (Sims and Gamon 2002).
Taxonomic Partitioning of Chemical Traits
Families alone accounted for an average 27% variation in chemical traits, although at this deeper phylogenetic level, we found weak family-level organization of pigments, LMA, and some C fractions, and oppositely, strong accounting of Zn, K and water variation (Figure 4A). When excluding Dipterocarpaceae from the analysis, nested taxonomic organization accounted for an average 55% of the variance among chemicals, with a high of 76% for cellulose. Family-level organization varied by only a small amount, and the strongest control was found for Zn, K, and water (Figure 4B). Removal of the genus Shorea led to an increase in the genus-level organization of carotenoids and LMA, as well as soluble C, cellulose, hemi-cellulose, lignin and phenols.
Regression analyses supported results from the nested ANOVA tests (Table S5): Family, genus and species accounted for an average 20, 29 and 52%, respectively, of the variation in leaf chemicals and LMA (adjusted-r2, p < 0.01). A total of 14 of 21 traits had species-level regression adjusted-r2 values exceeding 0.50, and the strongest results were 0.70 for cellulose, 0.68 for water, and 0.67 for total C. Rerunning the analyses without the Dipterocarpaceae or without Shorea indicated the same overall pattern, at times increasing or decreasing the power of the regression by small amounts (Table S5).
The Cumulative Order in which Leaf Traits Enter a Stepwise Linear Discriminant Analysis (LDA) for Canopy Taxonomic Classification
Spectroscopic Estimation of Leaf Chemical Properties and Leaf Mass per Unit Area (LMA) Using Modeled Canopy Reflectance Signatures (Figure 6A)
Sources of Chemical Diversity
This dipterocarp forest harbors co-existing species with very wide ranging values for most leaf traits, but how does this variation compare to published compilations? LMA ranged from 51.4 to 244.1 g m−2 in the upper canopy at Lambir, which nearly equals the range reported for global humid tropical forests (Asner and others 2011b) and other biomes (Poorter and others 2009). A similar result held for N, which varied from 0.72 to 3.53% at Lambir, approaching the global range reported by Wright and others (2004). However, we also found that foliar P was held to a much narrower range in the Lambir canopy, 0.02–0.15%, compared to Wright and others’ (2004) global compilation. Foliar N:P ratios are often used as an index of site fertility (Hedin 2004), and we found that canopies at Lambir have a mean N:P of 25.6 (s.d. = 5.5), which is two standard deviations greater than the threshold of 14–16 said to indicate substrate-driven P limitation (McGroddy and others 2004). P limitation has a cascading effect on patterns of plant nutrient supply and demand, as well as decomposition processes, resulting in ecosystem-level feedbacks that can promote or limit primary production (Vitousek 1982; Vitousek and Sanford 1986; Vitousek and Walker 1987). Despite broad patterns of canopy chemistry associated with site fertility, there also often exists taxonomic pattern in chemical traits (Townsend and others 2008), suggesting an additional role of evolution in maintaining biogeochemical processes.
Where exactly does the chemical trait variability reside in the Lambir canopy? For many traits, we found major differences by growthform (Figure 1). Concentrations of P and other rock-derived nutrients (Ca, K, Mg, Zn, Mn, B and Fe) were 14–82% higher in lianas, as were pigment concentrations (17–18%). Although we did not assess whether localized variation in soil nutrients were correlated with liana presence-absence (Schnitzer and Bongers 2011), Paoli and others (2006) did find associations between soil conditions and both canopy chemistry and composition among dipterocarp trees. We thus suspect that there are similar niche partitioning processes at work for lianas. Nonetheless, there is a clear growthform effect by which lianas concentrate growth chemicals (nutrients, pigments), while maintaining lower concentrations of longevity and defense chemicals (LMA, lignin, phenols, tannins).
Beyond the pattern based on growthforms, we found that the Dipterocarpaceae maintains systematically lower concentrations of nutrients and photosynthetic pigments, and higher concentrations of secondary metabolites, than do trees in other families (Figure 2). We found a similar pattern within the genus Shorea (Figure 2). Moreover, intra-specific variation in most leaf traits within the Dipterocarpaceae, and even within the genus Shorea, was equivalent to what is found among all other species in the forest (Figure 3). That a single family or genus can strongly diverge in foliar chemical make-up from other canopy species is surprising, but given the observed dominance of Shorea and the dipterocarps at Lambir and in similar Bornean forests (Ashton 1987; Condit and others 2005), the results suggest that these chemical trait divergences are advantageous in a life strategy context affecting growth, longevity and defense. An alternative explanation might be that limits to migration (biogeography) and evolutionary processes have produced a forest dominated by a family that has subsequently undergone chemical trait radiation based on community-scale interactions such as competition and plant-pest dynamics (sensu Janzen 1970; Coley and Barone 1996). This will be difficult to assess prior to the development of a quantitative phylogeny for dipterocarps and other species found in the system, as well as an improved knowledge of host-specific interactions across trophic levels.
Taxonomic partitioning of chemical traits is ultimately a function of intra-specific variation and phylogenetic distance among taxa. We did not consider distance in the formal sense because we do not have genetic (for example, barcode) data. Instead, we focused on relative distance for each trait, which is an approach used by others to assess broad taxonomic patterns in plant traits at regional (Fyllas and others 2009) and global scales (Chave and others 2009). With nested random-effects ANOVA models that incorporate intra-specific variation, we found that taxonomic assignment (family-genus-species) accounts for a low of 32% (chl-a) to a high of 75% (Zn) of the chemical variance among canopies (Figure 4). However, the relative contribution of family, genus and species organization varied widely for each trait. For example, pigment variation, although the weakest in terms of taxonomic partitioning of variance, was almost entirely organized at the species level (Figure 4). In contrast, several micronutrients (K, Mg, and Zn) fell under mostly family-level organization. Still others such as the secondary metabolites (soluble C, cellulose, and lignin) displayed mostly genus- and species-level organization, without a pattern among families. Chemical partitioning at differing taxonomic levels suggests differential patterns and controls over chemical trait evolution. This also suggests that traits may be queuing to different selective forces over time, such as Zn with a deeper and older evolutionary history versus chlorophyll with a more recent species-level radiation.
What effect, if any, does a dominating family or genus have on patterns in taxonomically-grouped chemical traits throughout a forest canopy? Although species in the Dipterocarpaceae or Shorea maintain chemical concentrations that are very different from other taxa in the canopy (Figure 2), the stand-level taxonomic partitioning of chemicals is nearly invariant whether or not this most common family or genus is included in the ANOVA (Figure 4B, C). This suggests a common set of evolutionary processes at work in creating the observed chemical partitioning among all canopy taxa, which would go against the argument that dipterocarps have somehow undertaken a different pathway of trait evolution.
Environmental constraints, such as strong P limitation, may affect phylogenetic partitioning of canopy chemical traits in a system such as Lambir. Compared to a site in western Amazonia with relatively high P availability (N:P = 18.1 ± 5.4) but in similar climate conditions (Asner and Martin 2011), the Bornean canopy had up to 117% lower concentrations of leaf P and Ca. Foliar longevity and defense traits including LMA, lignin, phenols and tannins were up to 22% higher in Borneo. Although the Bornean site maintains a canopy of lower nutrient concentrations and greater investment in tougher foliage than in the Amazonian site, taxonomy still explains a substantial fraction of the chemical trait variability at both sites—72% in the Amazon and 57% in Borneo. The main difference is that a maximum of 6% of the floristic composition is explained by a single family in Amazonia, whereas more than 40% is driven by dipterocarps at Lambir. So although strong P infertility may limit the diversity of families found at a site like Lambir, both the chemical variation and the taxonomic partitioning of that variation appears to be maintained independent of the number of dominating families present. This supports the hypothesis that chemical trait variation is driven by evolutionary radiation based on species interactions (for example, competition, allelopathy) and host-specific defense (Fine and others 2004; Kursar and others 2009).
Linking Chemical and Biological Diversity
Although individual canopy traits may display differing levels of intra-specific variation, and have differing degrees and patterns of taxonomic organization, combining them into chemical signatures tends to improve the differentiation of taxa on a chemical basis. However, the dimensionality of the foliar chemical signatures depends upon the degree of correlation among leaf properties. We found that most leaf properties at Lambir are uncorrelated, and that at least 14 axes of variation exist among 21 leaf traits (Table 2, Table S4). Although LMA, N and P forms a highly inter-correlated, growth-related leaf ‘economics spectrum’ (Reich and others 1997; Wright and others 2004), our data indicate that adding chemical constituents, many of which are acquired and synthesized by plants to manage metabolism, longevity and defense, creates a rather unique portfolio for many canopy species. This is strongly evidenced in the LDA results, which showed that 81% of the multi-chemical trait variation (including intra-specific variation) was explained at the species level. About 42% of the variation was explained at the family level. These results suggest the existence of a wide variety of strategies among coexisting canopies in humid tropical forests, expressed in chemical signatures.
Prospects for Remote Sensing of Biological Diversity
Until recently, the possibility of remotely sensing canopy functional or biological diversity in tropical forests seemed out of reach, but advances in imaging spectroscopy have opened new doors that may allow for an improved mapping of canopy traits (Castro-Esau and others 2004; Clark and others 2005; Carlson and others 2007; Sanchez-Azofeifa and others 2009; Papeş and others 2010). These and other studies provide novel links between spectral data and species composition, yet a more general approach to combining canopy taxonomy and spectroscopy might best be made via the chemical properties of canopies. Asner and Martin (2009) developed the spectranomics concept to link spectroscopic remote sensing to canopy diversity via differences in the leaf chemical signatures found among many species. The approach was tested in a lowland Amazon forest (Asner and Martin 2011), revealing that the majority of species, spread among a large number of families, had unique chemical and thus spectral signatures. However, intra-specific variation in chemical attributes and the diversity of chemical signatures among co-existing canopy taxa each influences whether spectroscopic signals might indicate the richness and abundance of species (Asner and others 2009). Our remote sensing goal in Borneo was thus to assess whether these chemical-to-spectral linkages made in a community dominated by one family would be different from that of the Amazon site harboring a more even distribution of families.
Compared to the Amazon site and to most other tropical forest systems we have assessed (Asner and others 2011a), we found the Lambir forest to have high inter-specific and low intra-specific spectral variability (Figure 6). This variability was about the same among the Dipterocarpaceae, and within the genus Shorea (Figure 6D), as it was at the site level among hundreds of species (Figure 6B). The strong spectroscopic variability within this dominant family or genus is commensurate with the pronounced chemical variation measured among their chemical traits. The formal link between spectral and chemical properties was made using PLSR analysis, a technique which treats the spectrum as a single, contiguous measurement, rather than as a series of spectral bands. In the past, particular spectral regions or bands have been singled out for analysis of canopy chemical traits (Curran 1989). However, the entire spectrum can now be analyzed as a contiguous measurement, which greatly improves accuracy and transferability of the new relationships to other ecosystems (Boulesteix and Strimmer 2006; Feilhauer and others 2010). And new evidence suggests that treatment of the spectrum as a contiguous signal is more in line with the way that plants invest in and make trade-offs among the multitude of chemical compounds affecting vegetation–light interactions (Ustin and Gamon 2010; Ollinger 2011). With current computing technology, it is no longer necessary to discard spectral information by selection of narrow wavelength regions for processing, and an increasing number of studies are showing the advantage of using the full spectrum for remotely-sensed chemical analysis (for example, Martin and others 2008; Skidmore and others 2010; Knox and others 2011).
With this in mind, our PLSR results establish that 16 leaf traits can be remotely estimated in the Lambir canopy (Table 4), including traits characterized in past studies—pigments, N, water, and C fractions such as cellulose and lignin (see reviews by Kokaly and others 2009; Ustin and others 2009). Moreover, we found that about 76 and 33% of species and families, respectively, can be classified with these remotely sensible chemical signatures (Figure S1). The subset of chemical traits most important to developing the classification included C, hemi-cellulose, phenols and tannins (Table S6). Our analyses indicated that these four chemical traits have particularly unique values within the Dipterocarpaceae, as compared to other taxa, hence their important contributions to these combined chemical signatures. And finally, we found that phenols were a key contributor to the remotely sensed classification of species at the Bornean site, highlighting the value of defense compounds in the development of ecological remote sensing approaches for biological diversity.
This study provides new insight into sources of spectral and chemical variation among canopy species in lowland Bornean forests. We drew a connection between chemical and biological diversity, and between chemical and spectral properties among canopies. Our approach is unique because it allows for quantitative linkage between these otherwise disparate areas of study, yet we still view these techniques as needing refinement. Ripe areas for increased effort range from improving models of canopy reflectance based on sunlight foliage and vertical light attenuation gradients, to integrating quantitative remote sensing and phylogenetic methods (for example, barcodes and distance matrices). Such efforts will be essential to upscaling what are ultimately limited field-based measurements to scales commensurate with ecosystem-level processes.
Despite the limitations of our current techniques, we found the chemical diversity of lowland mixed dipterocarp forest to be very high, and that this high chemical diversity is expressed through a suite of elements and compounds regulating growth, defense, longevity, and other vital plant and ecosystem functions. Some of the chemical ranges observed among full sunlight canopies in this single Bornean forest nearly matched the global variability within and among different biomes. However, we also found that much of the chemical diversity resides in the dominant family Dipterocarpaceae, and in the genus Shorea, highlighting the role that a single phylogenetic branch can play in creating chemical variation. These findings suggest that chemical diversity is not simply a function of biological diversity at low taxonomic levels (for example, families or genera present at the site), but rather it reflects the variation among co-existing species. This may indirectly suggest over-dispersion (low phylogenetic signal) of foliar chemical traits (Kursar and others 2009), a topic warranting further research. Independent of the underlying evolutionary causes and the present distribution of species, chemical diversity in canopies such as those found in lowland Borneo are measurable using high-fidelity spectroscopic remote sensing techniques. Through these chemical-to-spectral linkages, studies of functional and biological diversity interactions will become increasingly possible at larger spatial scales, thereby improving our knowledge of how species mediate and are affected by ecosystem and evolutionary processes.
We thank D. Knapp, F. Sinca, L. Carranza, C. Anderson, M. Houcheime, K. Smith, and A. Enjah, and colleagues from the Forest Department Sarawak, University Malaysia Sarawak, and University Putra Malaysia for assistance with logistics, field work and laboratory analyses. We thank S. Davies and the Center for Tropical Forest Science (CTFS) for programmatic assistance. The Carnegie Spectranomics Project (http://spectranomics.ciw.edu) is supported by the John D. and Catherine T. MacArthur Foundation, and activities in the field campaign were made possible through the development project of the Ministry of Natural Resources and Environment (NRE), Malaysia.