BGBiogeosciencesBGBiogeosciences1726-4189Copernicus PublicationsGöttingen, Germany10.5194/bg-14-5313-2017Parallel functional and stoichiometric trait shifts in South American and
African forest communities with elevationBautersMarijnmarijn.bauters@ugent.beVerbeeckHanshttps://orcid.org/0000-0003-1490-0168DemolMiroBruneelStijnhttps://orcid.org/0000-0002-8226-8080TaveirneCysVan der HeydenDriesCizunguLandryBoeckxPascalIsotope Bioscience Laboratory – ISOFYS, Ghent University, Coupure Links 653, 9000 Ghent, BelgiumCAVElab, Computational and Applied Vegetation Ecology, Ghent University, Coupure Links 653, 9000 Ghent, BelgiumFaculty of Agronomy, Université Catholique de Bukavu, Avenue de la mission, BP 285, Bukavu, DR CongoMarijn Bauters (marijn.bauters@ugent.be)29November201714235313532111April201713April201712October201716October2017This work is licensed under the Creative Commons Attribution 3.0 Unported License. To view a copy of this licence, visit https://creativecommons.org/licenses/by/3.0/This article is available from https://bg.copernicus.org/articles/14/5313/2017/bg-14-5313-2017.htmlThe full text article is available as a PDF file from https://bg.copernicus.org/articles/14/5313/2017/bg-14-5313-2017.pdf
The Amazon and Congo basins are the two largest continuous blocks of tropical
forest with a central role for global biogeochemical cycles and ecology.
However, both biomes differ in structure and species richness and
composition. Understanding future directions of the response of both biomes
to environmental change is paramount. We used one elevational gradient on
both continents to investigate functional and stoichiometric trait shifts of
tropical forest in South America and Africa. We measured community-weighted
functional canopy traits and canopy and topsoil δ15N signatures. We
found that the functional forest composition response along both transects
was parallel, with a shift towards more nitrogen-conservative species at
higher elevations. Moreover, canopy and topsoil δ15N signals
decreased with increasing altitude, suggesting a more conservative N cycle at
higher elevations. This cross-continental study provides empirical
indications that both South American and African tropical forest show a
parallel response with altitude, driven by nitrogen availability along the
elevational gradients, which in turn induces a shift in the functional forest
composition. More standardized research, and more research on other
elevational gradients is needed to confirm our observations.
Introduction
A good understanding of the future response of tropical forest
ecosystems to global change is required because of their vital role in global
biogeochemical cycles and ecology. However, due to the long turnover times in
forest ecosystems, it is hard to acquire insight into these future responses.
As a result, empirical research has since long turned to studying ecosystems
along natural gradients, which can greatly advance our understanding of
ecosystem ecology and function in response to environmental shifts.
Elevational gradients in particular offer open-air space-for-time
experiments. Contrary to latitudinal gradients or elevational gradients in
the higher-latitude zones, they are not complicated by changes in
seasonality, and with careful interpretation can offer great insights into
tropical forest functioning (Körner, 2007; Malhi et al., 2010; Sundqvist
et al., 2013). Hence, elevational transects have been postulated as a viable
and useful setup to assess long-term ecosystem responses to environmental
changes, and serve as an empirical tool to assess future trajectories of
forest ecosystems under global change (Malhi et al., 2010; Sundqvist et
al., 2013). This has invoked research efforts on transects in South America,
but no such studies have been carried out in central African forests, leaving
the second-largest continuous block of tropical forest understudied.
Nevertheless, recent work has shown that African and South American tropical
forest currently show important differences in structure (Banin et al., 2012)
and species richness and composition (Slik et al., 2015). These differences
call for cross-continental empirical research in both the Amazon and the
Congo basins (Corlett and Primack, 2006), and in this context we can raise
questions about the universality of tropical forest biogeochemistry and
functioning across both continents, and subsequently their response to future
global change scenarios. Additionally, due to the central role of nutrient
availability that drives both net ecosystem productivity (NEP) and ecosystem
carbon use efficiency (CUEe) (Fernandez-Martinez et al., 2014), the effect of
climatic gradients on nutrient availability should be better understood.
Indeed, recent efforts have shown that biosphere–atmosphere carbon exchange
in forests is regulated by nutrient availability (Fernandez-Martinez et
al., 2014), and therefore, changes in nutrient bio-availability induced by
global change need to be accounted for. Canopy chemical traits are proxies
that are relatively easy to assess, and from which ecosystem functioning and
biogeochemistry can be inferred (Asner et al., 2015; Wright et al., 2004).
Nutrient ratios and concentrations in leafs, along with specific leaf area
(SLA), are traits that are known to cluster around the leaf economic
spectrum, which expresses a trade-off in photosynthetic efficiency and leaf
turnover. Indeed, canopy nutrients play key roles in photosynthesis, and are
hence vital for carbon exchange processes at the leaf level (Evans, 1989;
Reich et al., 2009). Consequently, species with high SLA, N and P are
associated with high photosynthesis rates (Poorter et al., 2009; Reich et
al., 1997; Wright et al., 2004), but have an “expensive” nutrient economy
(fast leaf turnover). Previous work has shown that these traits vary
systematically with landscape biogeochemistry (Asner et al., 2014, 2015), and
hence the functional canopy signature of forests across gradients express the
ecological response to changes in nutrient availability. Canopy chemistry has
received increasingly more attention because of its inherent link to the
plant strategy. Nevertheless, and as rightfully noted by Asner and Martin
(2016), there are only limited surveys on canopy functional signatures in the
tropics, while this information is vital for a landscape-scale understanding
of tropical forest assembly. In addition to leaf traits, both leaf and soil
δ15N are known integrators of the local N cycle and analysis of
natural abundance of stable N isotope ratios is a powerful and extensively
studied proxy for N cycling in ecosystems (Högberg, 1997). Previous
efforts have shown that shifts towards lower δ15N values indicate a
more closed N cycle with lower N availability, and vice versa (Brookshire et
al., 2012; Craine et al., 2015; Houlton et al., 2006). This shift in isotopic
ratios is caused by increased rates in fractioning processes such as
denitrification, where 14N is preferentially consumed, leaving the
source pool enriched with 15N (Hobbie and Ouimette, 2009). Hence
δ15N values have been used to infer shifts in N openness across
natural gradients (Martinelli et al., 1999; Menge et al., 2011; Vitousek et
al., 1989), and subsequently, combining both leaf traits and δ15N
values is an interesting approach to assess ecosystem responses to
environmental gradients.
In this study we address the existing lack of standardized cross-continental
research and assessed shifts in nutrient availability and forest functional
composition along two similar transects in Ecuador and Rwanda. We assessed
these shifts through indicative (i) community-level functional traits and
(ii) nitrogen isotope ratios in topsoil and canopy. We hypothesized that
(i) both these community-level traits and stable isotope signals would
indicate a shift in nitrogen availability with altitude, and that (ii) these
shifts would be similar on both continents in terms of direction and
magnitude, given a standardized research protocol and a similar adiabatic
lapse rate.
Materials and methodsField inventories, sampling and trait analyses
We selected plots at different altitudes on the west flank of the Andes in
Ecuador (ranging from 400 to 3200 m a.s.l.) and in the Nyungwe National
Park Rwanda (1600–3000 m a.s.l.), in the southern Great Rift Valley
(see Fig. S1 and Table S1 in the Supplement for location and overview maps). Due
to reduced accessibility, the gradient in Rwanda was shorter than the
South American transect. We delineated and inventoried plots following an
international standardized protocol for tropical forest inventories (RAINFOR;
Malhi et al., 2002), with an adapted plot size of 40 m by 40 m. In each
plot, the diameter of all live stems with a diameter larger than 10 cm was
measured at 1.3 m height and the trees were identified to species or genus
level. Besides diameters, also tree heights were measured, in order to
estimate the aboveground carbon storage (AGC) using pan-tropical allometric
relationships (Chave et al., 2014). The canopy of every plot was
characterized by selecting the most abundant tree species, aiming at a
sampling percentage of 80 % of the basal area of the plots. For the
selected species of all plots, we sampled mature leaves of a minimum of three
individuals per species per plot using tree climbers. For most of the
individuals we sampled fully sunlit leaves, but this was not always possible
for the safety of the climbers, in which case we sampled partly shaded leaves
under the top canopy. Previous work on elevational transects has shown that
the vertical profile of leaves within a canopy has little effect on the trait
values (Fisher et al., 2013). Additionally, composite samples of the topsoil
(0–5 cm) were collected at five different places within each plot, and
mixed per plot prior to drying. Soil and leaf samples were dried for 48 h at
60 ∘C. Roots were picked out of the soil samples before grinding and
subsequently carbon (C), nitrogen (N) content and δ15N of plant and
soil samples were analysed using an elemental analyser (automated nitrogen
carbon analyser; ANCA-SL, SerCon, UK), interfaced with an isotope ratios mass
spectrometer (IRMS; 20-20, SerCon, UK). Leaf samples were dry-ashed at
550 ∘C for 5.5 h; the ash was dissolved in 2 M HCl solution and
subsequently filtered through a P-free filter. The aliquots were then
analysed for total P by AAS method no. G-103-93 Rev.2 (Multitest MT7/MT8;
Ryan et al., 2001). SLAs were calculated by dividing the leaf areas of all
the sampled leafs per individual by their summed dry mass. Leaf areas were
determined by either photographing leafs on white paper with a reference
scale or by drawing leaf contours and scanning the drawings. Both the scans
and the pictures were processed using the ImageJ software (Schneider et
al., 2012). For one abundant species of the higher altitudes on the Rwandan
transect (Podocarpus latifolius (Thunb.) R.Br. ex Mirb.) we could
not obtain good area estimates, so we adopted SLA figures from the literature
(Midgley et al., 1995).
Statistical analysis
Average leaf trait values of SLA, leaf nitrogen content
on mass basis (LNC), leaf phosphorus content on mass basis (LPC), δ15N, C : N and N : P ratio were calculated for every selected
species, based on the sample values for the different individuals of the
species. Subsequently, to calculate community-level traits and leaf
δ15N per plot, we calculated a basal area weighted-average canopy
value and standard deviation using the species composition and the species
averages, following Asner et al. (2016b). Hence,
x‾w=∑i=1Nwi⋅xi∑i=1Nxi,
with xw the weighted value for trait x, xi the mean trait
value for species i and wi the basal-area based weight of that species
in the specific plot. Subsequently, for the weighted standard deviations
(σw),
σw=∑i=1Nwi⋅xi-x‾w2(N-1)∑i=1NwiN,
with N the number of nonzero weights.
The structure of the trait datasets was assessed qualitatively using Pearson
correlation statistics after log-transforming the trait data for normality.
Finally, we studied the relations between the different leaf traits and
elevation using mixed effects models for the different traits, with a random
error structure. The plots were spatially clustered around four altitudes on
both transects; hence we introduced these elevational clusters as a random
effect, and treated altitude and transect as fixed effects. Models were then
fitted using maximum likelihood methods in the “lme4” package in R (Bates
et al., 2007). P values of the fixed effects – elevation, transect and
their interaction – were determined based on the denominator degrees of
freedom calculated with the Satterthwaite approximation, in the lmerTest
package (Kuznetsova et al., 2014). The P values for the interaction term,
along with the Akaike information criterion for models with and without this
interaction term were used to decide whether or not to exclude the
interaction term. For reasons of linearity we used the inverse C : N
(hence rather N : C) in these analyses. Models for δ15N were
assessed for each transect, using mixed effects models, with elevational
cluster as a random effect. To explicitly determine divergence and
convergence of plant and soil δ15N with altitude, compartment (i.e.
canopy leaves or topsoil) was introduced as a fixed effect and the
interaction term was left in the model. For the statistical analysis, the R
software was used (R Development Core Team, 2014).
General characteristics, vegetation structure, climate (mean annual
temperature, MAT, and mean annual precipitation, MAP, WorldClim – Fick and
Hijmans, 2017) and soil characteristics of the elevational clusters on both
transects. Number of trees and species (in the 40 m by 40 m plots), basal
area (BA), mean tree height (MTH) and above-ground carbon (AGC) are averages
per plot ± the standard deviation on the plot-level results, based on the
inventories.
The pooled trait datasets from both transects showed a consistent and similar
correlation structure (Fig. S2), with both the separate and the pooled data
showing significant correlations between all traits, except SLA and
N : P. The structural vegetation parameters on both transects showed
important differences: for the same altitude range, we found a higher stem
density, but fewer species on the Rwandan transect (Table 1). Tree height and
basal area were comparable, and the carbon stocks showed high variability
along both transects. Climatic conditions were similar, with a highly
consistent temperature gradient (Fig. S3, Table 1), and similar mean annual
precipitation in the concurring elevational ranges. The linear mixed effects
models, with altitude as fixed effect, were able to explain a significant
proportion of variation in all traits. This is reflected by both the marginal
(m) and conditional (c) Radj2, respectively proxies for the
variation explained by the fixed effects and the random and fixed effects
together (Schielzeth and Nakagawa, 2013) (Table 2). The interaction term was
not significant in any case; hence the trait responses to altitude were
parallel on both continents. LNC, N : C, LPC and N : P significantly
decreased with altitude (Radj,m2 of respectively 0.83, 0.87,
0.68 and 0.60), with the Rwanda transect showing higher overall values. SLA
also decreased significantly, but with a slightly higher intercept for the
Ecuadorian transect (Radj,m2=0.83). δ15N
decreased on both continents with altitude, with a similar effect on both
continents (Table 3). There was a significant divergence between slope and
soil δ15N along the Ecuadorian transect, while Rwanda showed a
significant convergence (Radj,m2=0.93 and 0.55 for
respectively Ecuador and Rwanda).
Fixed effects estimates (altitude in km a.s.l.) for the different
canopy-level response variables; leaf nitrogen content (LNC), inverse
C : N ratio, specific leaf area (SLA), leaf phosphorus content (LPC) and
N : P ratio, along with the estimated marginal (m) and conditional (c)
Radj2 (sensu Nakagawa and Schielzeth, 2013). The interaction
term for altitude × transect was not significant in any case, and was
hence not retained in any model.
Fixed effects estimates (altitude in km a.s.l.) for δ15N
in both canopy and topsoil (compartment) on both transects, along with the
estimated marginal (m) and conditional (c) Radj2 (sensu
Nakagawa and Schielzeth, 2013).
Elevational transects are viable setups to assess long-term ecosystem
responses to environmental gradients. We assessed canopy chemistry,
functional composition and δ15N signals along one elevational
gradient in South America and one in central Africa. The measured traits are
indicative proxies for the underlying biogeochemistry of the forest
ecosystems. The shifts of these proxies along both transects were parallel in
both setups. They indicated a lowering N availability with increasing
altitude, with a subsequent parallel shift in functional forest composition
on both continents.
The vegetation structure was varying differently along both transects. The
high variability in the stem number, basal area and carbon stocks is
potentially caused by the relatively small plot size. Other research efforts,
targeting these variables specifically, use plot sizes of 1 ha, as set
forward by the RAINFOR protocol, in tropical forests worldwide (Phillips et
al., 2009). As such, the differing carbon stocks probably do not integrate
important stochastic events (e.g. tree fall) from the forest along both
slopes. However, interestingly enough we found a lower average carbon stocks
and higher number of trees in the upper two Rwandan clusters in comparison to
the Ecuadorian forests. This contrasts with what has been reported from
large-scale forest monitoring networks across the lowland forests of Amazon
and the Congo basins (Lewis et al., 2013). More research in larger plots,
including on dynamics and productivity, should establish whether this is a
consistent observation in highland forest on both continents. On the other
hand, the lower species number on the African transect fits well within the
recent findings of a pantropical study, reporting a lower tree species
diversity in the African tropical forest (Slik et al., 2015).
Trends in community-level functional traits and leaf (full line,
closed circles) and topsoil (dashed line, open circles) δ15N of the
elevation transects in Ecuador (red) and Rwanda (blue). Leaf nitrogen content
(LNC), leaf phosphorus content (LPC), specific leaf area (SLA), and leaf
N : C, P : C and N : P ratio decrease with increasing altitude on
both transects. Both transects showed decreasing values of δ15N,
providing additional evidence for a more closed N cycle with increasing
altitude. Lines represent the fixed altitude effects in the respective
statistical models for both Ecuador (red, 400–3200 m a.s.l.) and Rwanda
(blue, 1600–3000 m a.s.l.).
Different environmental variables are influenced by altitudinal changes, i.e.
atmospheric pressure, temperature, cloudiness, moisture, etc. (Körner,
2007). Accordingly, elevation is an indirect proxy for the related changes in
these variables. In this view, the air temperature decrease with elevation
was highly similar on both transects, which means that we can validly assess
similar temperature-driven responses of both forest functional composition
and the underlying nutrient dynamics. The high collinearity in the trait
datasets corresponds well to known trade-offs described as the “leaf
economics spectrum” (LES) – basically a leaf-level trade-off between leaf
construction cost, i.e. low SLA, LNC and LPC, and photosynthetic efficiency,
i.e. high SLA, LNC and LPC (Wright et al., 2004). LNC, LPC and SLA showed a
highly significant decrease with altitude (Fig. 1 and Table 2), indicating a
functional shift towards more nutrient-conservative species communities at
higher altitudes on both transects. Indeed, leaves at lower altitudes with
high LNC, LPC and SLA and hence a more efficient photosynthetic apparatus and
rapid turnover, are replaced by leaves with low LNC, LPC and SLA values at
higher altitudes. We have added previous published work of South America and
Southeast Asia, with similar temperature gradients by Asner et al. (2016b),
Kitayama and Aiba (2002) and Van de Weg et al. (2009) to our transects
(Fig. S3) to assess the consistency of our observed trends. We added the
limited amount of studies where community-weighted means were reported along
one “single mountain range system”, hence neglecting a recent and relevant
contribution from Asner and Martin (2016). Our comparison showed that the
decreasing trend in LNC was consistent with the other studies from South
America (Asner et al., 2016b; Van de Weg et al., 2009), but not with
Southeast Asia, where no significant trend was found (Kitayama and Aiba,
2002). However, leaf mass area (LMA; the inverse of SLA) of all studies
showed a similar, increasing trend with elevation. LPC shows a strong and
significant trend along both transects in this study, while the other studies
report no significant trend. This is consistent with the meta-analysis
presented by Tanner et al. (1998), which shows consistent negative LNC trends
on “same mountain” studies and inconsistent LPC trends. A recent effort on
a larger scale in Peru has shown that LES trade-off between LNC and LPC or
SLA and LPC is indeed decoupled by climatic and geophysical filters, while
the leaf SLA–LNC trade-off is more robust (Asner et al., 2016a). Regarding
the studies we included for comparison (Fig. S3), only Van de Weg et
al. (2009) assessed N : P ratio. Although no significant trend was found,
they reported that N : P ratio was lowest in the highest sites (Van de
Weg et al., 2009). Additionally, decreasing N : P ratios have also been
reported on other transects on the Andes (Fisher et al., 2013; Soethe et
al., 2008), and recently in Peru using airborne imaging spectroscopy (Asner
et al., 2016a).
In addition to the above community-level functional traits, the decreasing
δ15N values on both continents (Fig. 1) are another strong
indication of the decreasing N availability in the upper forests. Along the
transects, both topsoil and canopy leaves showed decreasing δ15N
values with increasing altitude (Fig. 1), indicating a more closed N cycle
with lower N availability at the higher altitudes of both transects. It has
been shown that lowland tropical rainforests exhibit high values of
δ15N mainly caused by the high gaseous nitrogen losses via
denitrification, a strongly fractionating process (Houlton et al., 2006). The
decreasing trends with altitude are interesting and seem to support the
existing paradigm that tropical forests shift from P-to-N limitation in
transition from lowland to montane tropical forest (Townsend et al., 2008).
This is also reflected in the stoichiometric shifts, as canopy N : P is
decreasing with increasing elevation (Fig. 1). Hence plants incorporate
relatively less N compared to P in canopies at higher altitudes. The higher
soil δ15N values along the lower part of the Rwanda transect
suggests a more open N cycle compared to the lower part of the Ecuadorian
transect. This corroborates a recent finding of very high N losses at
1900 m a.s.l. at the Rwanda site (Rütting et al., 2014), and the
observation of high retention potential of bio-available N in Chilean
Andisols (Huygens et al., 2008). Further research is needed to explain the
notable divergence in soil and foliage δ15N along the Ecuadorian
transect, mainly driven by the highest elevational cluster. As previously
reported, this can be due to different degrees of dependence upon
ectomycorrhizal fungi (EcM) (Hobbie et al., 2005), different mycorrhizal
association types (Craine et al., 2009) or shifts in the uptake of different
forms of nitrogen (Averill and Finzi, 2011; Kahmen et al., 2008).
EcM-associated plant species are expected to show more depleted isotopic
ratios, due to isotope fractionation during N transfer to the host plant.
This effect is obscured in lowland N-rich tropical forests and might just not
be detectable at lower altitudes, but might become apparent in N poorer
environments such as the higher altitude forests (Mayor et al., 2014).
Secondly, a study from a temperate elevational transect has shown that plants
increasingly switch to organic N sources with decreasing temperature, without
fractionation upon N transfer from EcM to plants (Averill and Finzi, 2011).
Resulting from that, they found that the δ15N from the canopy and that from the soil converged rather than diverged along altitude, because plants draw N increasingly from a source
pool close to the bulk isotopic signature. We have no data on EcM
colonization or δ15N of sporocarps in the study plots, so we are
not able to disentangle the mechanisms. However, by characterizing both
community functional traits and canopy and soil δ15N, the data of
these transects are consistent with a decreasing availability of soil N as
elevation increases. We suggest the reduced N availability to be caused by an
indirect temperature effect on the N cycle, consistent with observations from
a direct fertilization experiment (Fisher et al., 2013). Lower temperatures
slow down depolymerization and N mineralization processes, and hence also N
bio-availability, thereby invoking changes in the functional plant
communities along the transects (Coûteaux et al., 2002; Marrs et
al., 1988). Future global change will most likely distort N availability both
directly via increased reactive N deposition (Galloway et al., 2008; Hietz et
al., 2011) and indirectly via a temperature effect on N mineralization in
forest soils. This raises questions on the future of plant species within the
already threatened montane tropical forest biome, where higher N availability
and temperature increase might distort the existing ecological niches and in
turn also increase N losses. Further research should therefore focus on
process-based knowledge of N and P cycle dynamics along such transects to
further assess whether the availability is actually limiting the ecosystems.
These observations also have repercussions for carbon fluxes: since nutrient
availability exerts a stronger control on NEP than on gross primary
production (GPP) (Fernandez-Martinez et al., 2014), it is likely that the
CUEe will be lower at higher altitudes. It has been hypothesized
that this decrease in CUEe is due to an increased investment of
photosynthates into non-biomass components, such as root symbionts for
nutrient mining and root exudates, at the expense of net primary production
(Vicca et al., 2012). However, recent empirical evidence has shown for one
transect in the Andes, that a decrease in GPP with increasing altitude is not
accompanied by a trend in CUE (Malhi et al., 2016). More work on carbon
budgets along elevational transects is needed to fully understand the role of
N and P availability and its interaction with climate gradients for the
tropical forest carbon cycle.
Conclusions
Altogether, this study evidences parallel functional shifts with
a similar direction and magnitude along two comparable elevation gradients,
in tropical forests on two different continents. The data suggest, in two
different ways, that this shift is caused by temperature-driven response of
nutrient availability. With the first data on an elevational transect in
central Africa, this work adds to the existing set of elevational transects
in the tropics. However, more transects are needed, especially in Africa, to
validate a universal response of tropical forests to environmental change.
Furthermore, work on process-based nutrient dynamics is important to unravel
the importance of different global change factors for both forest basins.
The trait data will be made available via the TRY
database.
The Supplement related to this article is available online at https://doi.org/10.5194/bg-14-5313-2017-supplement.
MB, HV and PB developed the project; MB, MD, SB, CT and DV
carried out the field work and analysed the data. All authors contributed to
the ideas presented and edited the paper.
The authors declare that they have no conflict of
interest.
Acknowledgements
This research has been supported by the Belgian Development Cooperation
through VLIR-UOS. VLIR-UOS supports partnerships between universities and
university colleges in Flanders (Belgium) and the south looking for
innovative responses to global and local challenges. Visit
www.vliruos.be for more information. We also thank BOS+ Tropen, Mindo
Cloud Forest Foundation and the Rwanda Development Board for the logistical
support, as well as Fidel Nyirimanzi and Nicanor Mejía for their botanical
expertise. We also thank Jordan Mayor and an anonymous reviewer for their
suggestions and constructive comments on an earlier version of this
manuscript.
Edited by: Michael Bahn
Reviewed by: two anonymous referees
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