1. Introduction
Isoprenoids are volatile organic compounds (VOCs) that are emitted to
the atmosphere mostly by plants. They have diverse functional roles at
multiple scales, from cellular protection and defense at the foliar
level, through chemical signaling within and among plants, up to the
regulation of large-scale biogeochemical processes, such as the effect
on atmospheric chemical composition and contribution to aerosol
formation (Laothawornkitkul, Taylor, Paul & Hewitt 2009). Volatile
isoprenoids are represented by isoprene
(C5H8), monoterpenes
(C10H16), and sesquiterpenes
(C15H24), and their largest source is
from tropical trees that contribute ca. 80% of global emissions
(Guenther et al. 2012). With half of the world’s tropical
forests, Amazonia is recognized as the most important global source of
isoprenoids to the atmosphere (Sindelarova et al. 2014). Since
the early 1980s, multiple investigations have studied canopy flux,
canopy concentrations, and to a lesser degree, leaf-level emissions of
isoprenoids. These studies have reported meaningful insights into the
emission drivers and how these compounds are involved in subsequent
atmospheric processes (Yáñez‐Serrano et al. 2020). These combined
findings contributed to developing and optimizing an isoprenoid emission
model (Guenther et al. 2012). Despite this effort, emission
estimates from tropical vegetation still carry a high uncertainty due to
a poor understanding of the biological controls that determine thecapacity of emission and its plasticity in response to ecological
and environmental conditions, as well as of the environmental controls
that determine rates of emissions (Alves et al. 2018).
The constitutive emission capacity of isoprenoids is determined by the
emission at leaf standard conditions (1000 𝜇mol m-2s-1photosynthetically active radiation, 30 ˚C), and
this is a physiological property that may vary plastically (across
individuals) under different ecological and physiological conditions.
Actual emission rates are a function of emission capacity and variation
in light and temperature (Niinemets et al. 2011). This implies
that, for modeling isoprenoid emissions, first it is necessary to
quantify emission capacities across species, and their plasticity across
individuals, to then quantify the emission variation driven by
environmental factors such as light and temperature (Duhl, Helmig &
Guenther 2008; Niinemets et al. 2011; Guenther et al.2012). For several practical reasons, such as the remoteness and high
plant species diversity of Amazonia, most studies so far have only
investigated isoprenoid emission rates at the ecosystem level and how
they vary with environmental factors. The majority of these studies
measured canopy concentration or flux of isoprenoids, focusing on
isoprene, known to be the strongest emitted compound (Eerdekens et
al. 2009). Only a few studies measured monoterpenes, and very few
studies quantified sesquiterpenes (Yáñez‐Serrano et al. 2020).
A first attempt to address isoprene emission capacities at the leaf
level and the upscaling to ecosystems was made by Harley et al.(2004). Knowing that not all plant species emit isoprene (Monson, Jones,
Rosenstiel & Schnitzler 2013), the aforementioned study aimed at
quantifying the isoprene emission capacity for multiple plant species
from different Amazonian regions, and a method was created to impute the
isoprene trait to other non-measured trees by using species
identification and phylogenetic proximity; then, results were used to
upscale the isoprene emission capacity to the ecosystem level based on
the trees fraction of isoprene emitters. Subsequent work has further
expanded the number of species measured (Jardine et al. 2020;
Taylor et al. 2021). Recent work has derived more mechanistic approaches
to scaling isoprene emission across the landscape by determining how the
fraction of emitters relates to mean climate conditions (Taylor et
al. 2018) due to differential performance between isoprene-emitting and
non-emitting species (Taylor, Smith, Slot & Feeley 2019). These studies
were important as they identified the emission capacity of isoprene, and
in a few cases also of monoterpenes, and certainly contributed to the
overall body of work from nearly 30 years of research on modeling
isoprenoid emission in Amazonia.
Yet, it is also known that isoprenoid composition is conserved within
plant species, but that these compounds’ emission capacity may vary
significantly within species and individuals with photosynthetic
capacity, carbon and nutrient investment tradeoffs, habitat, and the
environment (Harrison et al. 2013). This variability in emission
capacities is an essential factor to explain why we observe seasonal
variation in isoprenoid emission (see a synthesis of studies in
Yáñez‐Serrano et al. 2020), which does not entirely follow the
seasonal variation in solar radiation and temperature in central
Amazonia (Alves et al. 2016, 2018).
Seasonal factors such as leaf demography and phenology are important
drivers of variability in leaf emission capacities and the composition
of emitted isoprenoids. During early leaf development, young leaves
synthesize less isoprene and more monoterpenes and sesquiterpenes
(Gershenzon & Croteau 1991; Kuhn et al. 2004b), and the opposite
occurs with leaf maturation (Alves, Harley, Gonçalves, Silva & Jardine
2014). This shift in emission composition results from physiological and
ecological factors, which cannot be explained by atmospheric
observations and direct abiotic effects alone. Variation in leaf
physiology with ontogeny scales up through leaf age distributions —
with a higher proportion of young leaves during the dry season (Lopeset al. 2016; Wu et al. 2016 ) — to influence seasonal
variation in isoprenoid emission capacities and total ecosystem
emissions (Alves, Harley, Gonçalves, Silva & Jardine 2014; Alveset al. 2016, 2018).
Faced with these reports, we can infer that most of the studies in
Amazonia were focused on emission rates — canopy-level
sensitivity concerning environmental factors and landscape-level
sensitivity to leaf quantity and emitter fraction. Relatively little
work has focused on mechanisms of variation in emission capacity,either within or between species, and these have focused exclusively on
leaf age, and primarily on isoprene (Alves et al. 2014, 2016,
2018). There is still a lack of understanding of the different
physiological roles of the other light-dependent isoprenoids, and, by
measuring all of them across habitats and seasons within species, we can
begin to infer conditions under which one or the other compound is
favored and how this can be more accurately scaled to the ecosystem.
Therefore, the determination of intraspecific variation in emission
capacities of different isoprenoids is a critical knowledge gap that
this study intends to address.
In this study, we present a uniquely comprehensive set of leaf-level
isoprenoid emission measurements to characterize variation in emission
capacities and chemical compositions within species, across habitats,
and across seasons. We performed our measurements on trees of three
hyperdominant species from central Amazonia — Protium hebetatum,
Eschweilera grandiflora, and Eschweilera coriacea (ter
Steege et al. 2013) — distributed along a topographic and
edaphic environmental gradient at the Amazon Tall Tower Observatory
(ATTO) site, during the wet and the dry seasons. Simultaneous
measurement of photosynthesis and emissions allowed us to assess
shifting isoprenoid investments in the context of the leaf carbon
balance and the inferred availability of photosynthetic substrates for
isoprenoid synthesis.