Introduction
Understanding how tree growth responds to changes in temperature and
precipitation along latitude is crucial for an accurate prediction of
future changes in forest dynamics caused by global climate change,
especially in Northern boreal ecosystems (Huang et al. 2020; Zhang,
Belien, Ren, Rossi, and Huang 2020). A latitudinal gradient is
associated with consistent temperature changes, which acts as a
potential natural laboratory to help infer forest responses to global
warming (De Frenne et al. 2013). Although there are many studies on tree
growth response to latitude, most of them have focused on ring width and
latewood density in the context of specific regions and/or species. For
instance, using a tree ring database from a dozen species and 762 sites
in the International Tree-Ring Data Bank (ITRDB), Wettstein et al.
(2011) showed that high-latitude ring-width series were more likely to
positively correlate with summer temperature while low-latitude sites
commonly showed negative correlations; different species respond
differently to temperature and precipitation anomalies (Wettstein,
Littell, Wallace, and Gedalof 2011). Björklund et al. (2017) analyzed
the latewood density parameters from 27 species and 349 sites in ITERDB
and found that correlations between density and width shifted from
negative to positive when moving from earlywood to latewood, and
temperature response of density varied intra-seasonally in strength and
sign (positive or negative correlation coefficients) (Björklund et al.
2017).
Although wood density and ring width are sensitive indicators of a
tree’s response to climate, the changes might be driven by traits at the
cell level or lower (i.e. micro-structure of cell wall). Conduit
dimensions of xylem are accepted as important traits in respect to plant
hydraulics and adaptation for both angiosperms and gymnosperms (Baas,
Ewers, Davies, and Wheeler 2004). Similar to angiosperm vessels,
tracheid characteristics can provide us with valuable information about
how conifer species adapt to diverse habitats and their possible
responses to global climate change. For instance, stem heating and water
manipulation experiments were carried out to study tree growth based on
timing and kinetics of the tracheid development process, which showed
that xylem traits responded to a significant change in temperature and
water availability (Begum, Nakaba, Yamagishi, Oribe, and Funada 2013;
Vieira, arvalho, and Campelo 2020). However, latitudinal patterns of
tracheids have been surprisingly understudied when compared to vessel
traits (Brodribb, Pittermann, and Coomes 2012).
Conifer xylem consists of two types of cells: tracheid (approx. 90-93%
xylem surface area) and parenchyma (approx. 7-10% surface area), which
is more uniform in pattern and has less cellular diversity than
angiosperm xylem (Panshin and Zeeuw 1980; Hacke 2015). Temperate conifer
tree rings are mainly composed of two types of tracheid: large and
thin-walled earlywood cells that are produced early in the growing
season (i.e. springwood) and primarily responsible for water transport,
and small but thick-walled latewood tracheids (i.e. summerwood) that are
produced after the earlywood cells and serving primarily in mechanical
support (Fonti et al. 2013). Therefore, tracheid diameter, length and
wall thickness represent useful proxies to examine tracheid cell
profiles within a growth rings and across xylem. Understanding the
temporal pattern of these traits and how the environment shapes them is
of high importance for forest management.
Recent studies on wood formation dynamics have greatly increased our
understanding of xylogenesis, i.e. xylem formation (Rossi et al. 2013;
Cuny, Rathgeber, Frank, Fonti, and Fournier 2014; Cuny and Rathgeber
2016; Rathgeber, Cuny, and Fonti 2016; Rossi et al. 2016). In short,
cell enlargement and secondary cell wall deposition and lignification
(wall thickening) are the two fundamental sub-processes of xylogenesis
that shape xylem cell dimensions and the resulting tree-ring structure
(Cuny et al. 2014). The complex interplay between the duration and rate
of xylogenesis determines the changes in cell features, e.g., cell and
lumen diameter, lumen area and wall thickness, etc., which in turn
creates the anatomical structure driving the wood density profile (Cuny
et al. 2014; Cuny and Rathgeber 2016). A recent study on Larixsp. and Picea sp. showed that tracheid cell size and tracheid
wall thickness drive variability of earlywood and latewood density in
the Northern Hemisphere (Björklund et al. 2017). However, whether this
conclusion can be applied to most conifer species remains unknown,
especially pertaining to those distributed in humid tropical forests of
the Southern Hemisphere (Leslie et al. 2012).
Although tracheid cell development across a tree ring follows a sequence
in cell division from cell enlargement, secondary cell wall thickening
to cell maturation, the duration and rate of the latter sub-processes
are influenced by different climatic factors during their specific
developmental periods (Castagneri Fonti, von Arx, and Carrer 2017;
Ebisuya and Briscoe 2018). For instance, using a micro-core data set
including members of Pinaceae belonging to four genera (i.e.,Abies, Larix, Picea, and Pinus ) from 39
sites in the Northern Hemisphere, Rossi et al. (2016) found that the
timing of xylem phenology events and mean annual temperature of the
sites were related linearly, with spring and autumn events being
separated by constant intervals across the temperature range. The latter
authors suggested that the uniformity of the process in wood formation
was mainly determined by the environmental conditions occurring at the
time of growth resumption (Rossi et al. 2016). In a three-year study on
the kinetics of tracheid development of three conifer species (i.e.,Picea abies , Pinus sylvestris , and Abies alba ),
Cuny et al. (2014) found that the amount of lumen wall material per cell
was quite constant along growth rings, which challenges the widespread
understanding that wall thickness is mainly driven by the
wall-thickening duration (Cuny et al. 2014). Hence, there is no
consensus on the role of the duration and rate of cell enlargement and
wall thickening phases on final tracheid cell traits, such as cell size
and cell wall area or thickness, while the effects of climatic factors
on xylogenesis are often species-specific and site-dependent (Cuny et
al. 2014; Rossi et al. 2016; Buttò, Rossi, Deslauriers, and Morin 2019).
Tree growth and xylem structure could be influenced by various climatic
conditions along a latitudinal gradient. Towards the colder upper-end of
the gradient, low temperatures limit tree growth and ultimately prevent
the growth, reproduction, and survival of trees at the tree line (Körner
1998; Lyu et al. 2017). By contrast, at lower regions of latitude, the
higher temperatures increase evapotranspiration, raising the level of
drought stress on tree growth and changing tree phenology (Lian et al.
2020). Therefore, in such environments, tree growth is typically
negatively correlated with temperature but positively with
precipitation. Previous dendrochronology studies showed that tree growth
of Picea abies responded to temperature and precipitation changes
along latitudinal gradients; however, the effect of precipitation was
dependent on temperature-induced water stress (Mäkinen et al. 2003). In
addition to the gradually changing relationship between temperature and
growth, the period of cambial activity and xylem cell growth gradually
shortens towards colder areas owing to thermal limitations in wood
formation (Rossi Deslauriers, Anfodillo, and Carraro 2007; Huang et al.
2020). The time window in which climatic conditions affect cell
development and tree growth, tends to change most with increasing
latitude (Körner 1998; Briffa et al. 2002; Henttonen et al. 2014).
However, there are relatively few interspecific studies on the effect of
climate on xylem anatomical traits compared to the tree ring width for
conifer species.
Although previous research suggests that hydraulic traits are correlated
with both precipitation and temperature (Martínez-Vilalta et al. 2004),
temperature is increasingly recognized as the primary driver of growth
reactivation in a cold climate. Both direct observations and controlled
experiments have demonstrated that cambial activity is limited by low
air temperatures in a cold climate (Rossi et al. 2012; Begum et al.
2013). However, most studies have only focused on temperate or boreal
ecosystems where snowmelt provides abundant water especially at the
beginning of spring and summer, and is therefore not a limiting factor
for xylem formation (Cuny and Rathgeber 2016, Rathgeber et al. 2016,
Rossi et al. 2016). Given that xylem cell expansion is a turgor-driven
process depending on cellular water uptake and solute accumulation,
water availability can affect xylogenesis (Kozlowski and Pallardy,
2002). Researchers have shown that both cell division and expansion are
sensitive to water potential (Fonti et al. 2010), and that water deficit
is the primary constraint for xylogenesis of Pinus pinaster in a
Mediterranean climate (Vieira, Rossi, Campelo, Freitas, and Nabais 2014;
Vieira Carvalho, and Campelo 2020). The large range in the thermal
thresholds for the onset of xylogenesis in Juniperus przewalskiiprovides additional evidence that temperature was not the only factor
initiating xylem growth under such cold and dry conditions (Ren Rossi,
Gricar, Liang, and Cufar 2015; Ren et al. 2018). These results suggest
that wood formation and xylem structure of various conifer species along
a large latitudinal gradient are an interplay between genetics and
multiple climatic factors. Therefore, an interspecific study within a
phylogenetic context and along a wide latitudinal gradient could shed
light on the role of temperature and precipitation on conifer xylem
structure.
The global distribution of conifers is as wide as that of angiosperms.
Boreal forests in high latitudes consist of a limited number of conifer
species (low diversity), whereas at lower latitudes conifer species
generally occur on mountains. The latter observations indicate that some
conifer species are more adapted to stresses such as cold and drought
than angiosperm trees, and therefore could occupy habitats that most
angiosperm trees could not (Condamine Silvestro, Koppelhus, and
Antonelli 2020), and their adaptation might be attributed to some
characteristics of their xylem structure. Furthermore, adaptation to
various climatic conditions along a wide latitudinal range should be
reflected in the xylem structure, especially in tracheid cell and cell
wall dimensions in early-and-latewood owing to construction costs and
water transportation constraints of tracheids. To-date, the latitudinal
patterns of conifer xylem anatomy has been understudied, and climatic
factors driving the variance of xylem structure traits were shown to be
ambiguous.
We hypothesize that the xylem structure of conifer species is mainly a
consequence of adaptation to cold or drought, thus, differences in
tracheid dimensions between early-and latewood would become stronger at
higher latitudes, which could be viewed as an ecological strategy of
adaptation to changing climate conditions. Among climatic factors, we
predict that temperature and precipitation could both impact the xylem
structure of conifers under cold or dry conditions, along with
elevation. Specifically, we address the following questions: 1) Does a
contrast of tracheid dimension between earlywood and latewood persist
when accounting for phylogeny? 2) Are there clear trends in xylem
structure along a latitudinal gradient? 3) Is temperature the main
driver of xylem structure under a monsoonal climate or does xylogenesis
depend on the interaction between temperature and precipitation? 4) How
much of the xylem structure variance can be explained by climate and
phylogeny respectively? To the best of our knowledge, there are no
existing cross-species studies that include up to 80 coniferous tree
species making this study an important contribution to our knowledge of
conifer adaptation.