5.1. Water availability and soil nutrients
Climate changes are strongly related to changes in rainfall patterns
worldwide, involving reductions in the total amount of annual
precipitation and/or increase in the dry season duration (Grossiord et
al. 2016). Furthermore, at local scales, soil water availability is
highly variable along topographic gradients, with wetter valleys and
drier ridges (Fig. 3, Gibbons & Newbery 2002). Both changes in soil
moisture and reduced precipitation strongly drive changes in
physiological traits (Pezzola et al. 2017). For instance,
drought-induced water stress decreases photosynthesis rate, which leads
to slow and reduced plant growth (McDowell et al. 2008). In addition,
low water availability decreases the physiological mechanisms (secondary
metabolites) related to plant defense and favors the reproduction of
insects (Mattson and Haack 1987, McDowell et al. 2011), increasing woody
species vulnerability to death (Das et al. 2016). Water availability
also plays a vital role in forest recovery, increasing the growth rate
of plant tissues during post-drought periods (Poorter et al. 2016,
Álvarez-Yépiz et al. 2018). Due to its strong spatial and temporal
variations, water availability is the most important driver of
resistance and recovery rates.
Soil nutrients also play an essential role in plant communities
distributed across topographic gradients (Fig. 3, Guan et al. 2015).
Soil nutrients are key factors of photosynthesis, which is an essential
mechanism of plant survival and growth (Fatichi et al. 2014). Nutrient
stoichiometry can change across topographic gradients due to the
unidirectional fluxes from ridges to valleys and of the consequent loss
of nutrients in the ridges (Werner and Homeier 2015). Therefore,
nutrient limitation can lead to high nutrient competition in ridges
(Werner and Homeier 2015). Nitrogen (N), phosphorus (P) and carbon (C)
are the main elements required to plant growth and survival, and change
in their ratios can have strong consequences for tropical forest
communities (Zhang et al., 2012, 2017). For instance, P of tropical
forest soil is positively correlated with growth rate and negatively
related with mortality rate (Soong et al. 2020). Tropical plants in
valleys may require large amounts of leaf N to deal with the intense
shading of forest understory (Torres-Leite et al. 2019). Droughts can
alter N and P cycles in ecosystems, either directly through changes in N
mineralization and P sorption (Mariotte et al. 2017) or indirectly
through changes in plant nutrient uptake and growth (Mariotte et al.
2020). Changes in litter N, P and C content alter decomposition rates
because decomposers require nutrients from either litter or soil for
their functioning (Gartner and Cardon 2004). Deficiency in
plant-available nutrients in ridge is enhanced through a positive
feedback driven by poor litter decomposability (Werner and Homeier
2015). Furthermore, more frequent droughts slow down litter
decomposition and reduce plant-available nutrients (da Silva et al.
2020).
Microclimate variation across topographic gradients
Vegetation structure (e.g., height, stem density, and canopy biomass)
and local topography (e.g., elevation, slope and aspect) strongly
influence the microclimate (Hardwick et al. 2015). Understory and canopy
species are under different microclimatic conditions due to the vertical
structuration in tropical forests. For instance, canopy cover of larger
trees regulate the irradiance and light intensity entering the
understory layer (Nepstad et al. 2002, Wright et al. 2010). Thus, the
light availability is more variable and limiting for understory species
than for large trees (Wright et al. 2010). The high drought-induced
mortality of large trees can change the microclimate of the understory
(Redmond et al. 2018, Zellweger et al. 2020). Small forest fragments
have lower abundance of large trees due to high edge effects (Dantas de
Paula et al. 2011) and lack suitable microclimatic sites for the
persistence of species during drought periods (Hardwick et al. 2015,
Laurance et al. 2018). During a water stress period, the low leaf area
of large deciduous trees lead to high light availability in the
understory (Smith et al. 2019). In turn, the increase in light
availability induces high rates of photosynthesis in the understory,
thus affecting species adapted to shaded conditions (Guan et al. 2015).
Other microclimate variables, such as air temperature and humidity, are
controlled by light availability that reaches the understory stratum.
For example, in the valleys with dense forest canopy, air humidity is
higher and temperature is lower than ridges with open forest canopy
(Fig. 3, Jucker, Hardwick, et al. 2018). The high humidity and low
temperature in valley can protect plant species during drought periods.
However, the opening of forest canopies during droughts due to leaf loss
can affect species adapted to low temperatures and high air humidity
(Smith et al. 2019). The high transpiration rates are strongly related
to high air moisture in the understory layer (Hardwick et al. 2015). In
addition, ridges can show different microclimate conditions depending on
the topographic aspect. For example, west facing ridges are warmer due
to higher exposure to afternoon sun than east facing ridges that are
exposed to morning sun (Stephenson 1990). Therefore, microclimate
variables, controlled by topography and vegetation structure, are
strongly related to plant growth and mortality, especially for
understory species.
Biotic factors
Drought resilience of dominant and low abundance species
Plant tropical communities are complex systems due to high diversity and
large differences in species abundances. The most basic classification
of species in a plant community is based on abundance patterns and it
separates species into dominants, subordinates and transients (Whittaker
1965, Grime 1998). In a plant community, few species are classified as
dominant species, which are the most abundant, and account for a higher
proportion of the overall biomass of the community. On the other hand,
low abundance species (subordinates and transients) represent lower
amount of biomass, but are the main determinants of plant diversity
(Whittaker 1965, Grime 1998, Mariotte 2014). Dominant and low abundance
species differ in their functional traits and play different roles in
the ecosystem (Mariotte 2014). In general, dominant species are
competitively superior (Mariotte 2014) and respond to environmental
filtering, while low abundance species respond to niche differentiation
(Maire et al. 2012). Low abundance species can promote the diversity of
climbing plants (Garbin et al. 2012) and affect ecosystem functioning
(Mariotte et al. 2015). Dominant species play an important role in
structuring the species distributions (Wei et al. 2020) due to its
homogenous distribution pattern (Mariotte 2014). For example, in a
topographic gradient, they can occur in valleys and ridges (Hollunder et
al. 2014). On the other hand, as low abundance species have a more
aggregated spatial distribution (Mariotte 2014, Garbin et al. 2016), it
is expected that they occur in specific habitats and not across a whole
topographic gradient (Hollunder et al. 2014). The response to drought
depends on species and their spatial distribution and thus, taking into
account both habitats (valleys vs. ridges) and species groups (dominant
vs. low abundance species) can improve our understanding of the
processes that drive the response of tropical forests to severe
droughts.
Low abundance species are less numerous, making populations of these
species more vulnerable to local extinction induced by climate change
(Greenwood et al. 2017). Furthermore, populations of low abundance
species that occur with few individuals and with an aggregated spatial
pattern (Mariotte 2014) can be even more reduced due to habitat loss. On
the other hand, dominant species are expected to be more resistant to
local extinction due to their higher number of individuals (Greenwood et
al. 2017). Therefore, locally, and perhaps even globally, species
diversity can decrease under the future climate scenarios due to the
role of low abundance species as main determinants of plant diversity.
Dominant species play important roles on ecosystem functioning because
of their large amount of biomass (Grime 1998) and thus, they can act as
a biotic filter in the establishment and survival of low abundance
species (Khalil et al. 2019). The mortality of dominant species during
droughts can also affect the performance of low abundance species.
Therefore, understanding how dominant and low abundance species respond
to drought events will highlight their roles in promoting resilience of
tropical plant communities.
Use of traits to unravel drought resilience mechanisms
A functional trait is any feature which impacts fitness indirectly via
effects on growth, reproduction and survival at individual and species
level (Diaz and Cabido 2001, Violle et al. 2007). Traits are classified
based on responses to the environment and/or common effects on ecosystem
processes (Lavorel and Garnier 2002). There are traits related to
responses to environmental variables, such as resources and disturbances
(i.e., response traits), and traits that determine the effects of
plants on ecosystem functions (i.e., effect traits), such as
biogeochemical cycling and disturbance resistance (Lavorel and Garnier
2002). Furthermore, species may exhibit intraspecific variation in
functional traits, which can represent an important strategy to resist
and recover from drought impacts (Hof et al. 2011). For instance, small
forest fragments sustain smaller populations with low phenotypic
variability in traits, making them more sensitive to climate change
effects (Hof et al. 2011). Trait-based approaches can help to understand
the physiological mechanisms of drought tolerance in different species,
as well as how forests will respond to future climate scenarios. Thus,
ecologists have to include key traits directly and mechanistically
relevant to plant survival and growth. For instance, carbon
sequestration, water use efficiency and photosynthesis rate are
mechanisms related to plant growth and mortality that can be assessed by
measuring plant traits.
Traits can be measured at different levels, from tissue (e.g. stomatal
and vein density), organ (e.g., specific leaf area [SLA],
leaf dry matter content [LDMC], woody density [WD]) to
whole-plant level (e.g., height, root to shoot ratio)
(Pérez-Harguindeguy et al. 2013). Plant ecologists have been using
trait-based approaches in order to understand mechanisms that explain
resilience mechanisms. On one hand, at the community level, functional
diversity can enhance resource use and increase the potential for
facilitative interactions, which decrease the negative impacts of
droughts (Gazol and Camarero 2016). On the other hand, at smaller
levels, individual and species are able to change their traits to
tolerate droughts. For example, trees can increase chlorophyll
concentration in their leaves during El Niño periods (Nunes et al.
2019).
Trait combinations have the potential to explain the growth-mortality
and resistance-recovery trade-offs. Traits that are linked to resource
capture (e.g., leaf area), photosynthetic capacity (e.g.,specific leaf area and leaf nitrogen content) and nutrient and water
uptake (e.g., root length and diameter) generally have positive
relationships with growth and negative relationships with mortality
(Pérez-Harguindeguy et al. 2013). In turn, traits that are related to
structural safety (e.g., wood density) or longevity (e.g.,leaf dry-matter content and leaf thickness) have negative relationships
with growth, but are often positively related to survival (Poorter and
Bongers 2006). However, the growth–trait relationships can exhibit
inconsistences among species group, biomes, and spatial scales. For
instance, although WD is widely used to predict drought impacts, it has
been suggested that this trait does not provide a mechanistic
understanding of drought-induced mortality (O’Brien et al. 2017).
Recently, it was found that low wood density is a strong predictor of
mortality for angiosperms, but not for gymnosperms (Anderegg et al.
2016). Furthermore, high wood density can be associated to high
mortality rate caused by hydraulic failure (Hoffmann et al. 2011).
Therefore, the use of specific key traits directly related to growth and
mortality is essential to investigate physiological mechanisms of
resilience.
The importance of tree size
Tree size is one of the most used traits to understand drought effects
on plants (Meakem et al., 2017; Prado-Junior et al., 2017; Shenkin et
al., 2018). Tree size is an effect trait, due to its key role in
controlling light availability and heterogeneity, and in influencing the
structure of understory species communities (Sercu et al. 2017). Tree
size is also a response trait related to light competition due to the
greater access to light that larger trees can have when compared to
understory plants (Laughlin 2014). Plant size can be negatively related
to stand density across topographic gradients, from valleys with low
stem density and bigger trees (in height and diameter) to ridges with
high stem density and smaller trees (Werner and Homeier 2015). This
trait can be helpful to understand which trees are more vulnerable to
mortality, but its use in drought studies is still limited in tropical
forest.
Most studies showed that larger trees are more sensitive to drought
effects due to their higher demands for water comparing to smaller
trees, which are expected to be more resistant (Phillips et al. 2010,
Moser et al. 2014). Nevertheless, small trees can face more water
limitation due to their shallower roots (Gibbons and Newbery 2002) and
thus they also show higher mortality rates (Rocha et al. 2020) and a
more accentuated growth-mortality trade-off pattern than larger trees
(Zhu et al. 2017). Trees with a
single stem may be more vulnerable to drought effects than shrubs with
multiple stems, which can leave one or more viable as an insurance to
survive (Tanentzap et al. 2012). In addition, older and taller trees can
show high resistance to precipitation variations (Giardina et al. 2018).
These findings suggest that small and big trees are more vulnerable to
droughts and trees with intermediate sizes (e.g. understory individuals)
are more resistant to drought events. Indeed, tree mortality may
increase, decrease, or show a U-shaped curve with increasing tree size
(Zhu et al. 2017). Although tree size is a common trait used in drought
studies, we do not know clearly if there is a size-dependency in
mortality.
The importance of hydraulic traits
Traits can be classified according to their responses to different
factors (Li et al. 2015): leaf economic traits (e.g., SLA and WD)
and hydraulic traits (e.g., stomata density and water-use
efficiency). Leaf economic traits are related to light use and carbon
sequestration while hydraulic traits are related to gas exchange and
water transport capacity (Li et al. 2015). Variation in hydraulic traits
is independent of variation in economic traits in tropical forests
(Powell et al. 2017), but hydraulic traits are strongly influenced by
plant size and water availability (Liu et al. 2019). Plants can reduce
water loss by shedding their leaves or closing their stomata to maintain
plant water potential and avoid or reduce the risk of xylem cavitation
(Vitória et al. 2019). The sensitivity of trees to drought is best
predicted by hydraulic traits (Anderegg et al. 2016, Li et al. 2020) and
forests with higher diversity in hydraulic traits are more resistant to
drought impacts (Anderegg et al. 2018). Hydraulic failure was the main
mechanism explaining tree mortality during the 2015/2016 drought, while
wood density, SLA, tree size and foliar nutrients were poorly correlated
with drought vulnerability in a seasonally dry tropical forest in Costa
Rica (Powers et al. 2020). Hydraulic failure occurs when the water
transport to the canopy is decreased, resulting in desiccation and death
of plant tissues (Hoffmann et al. 2011). In addition, tropical
rainforests showed high water use efficiency to deal with the negative
impacts of 2015/2016 drought (Nunes et al. 2019). Therefore, the use of
hydraulic traits and leaf economic traits, as well as their
relationships, can help to understand the cause of mortality and reduced
growth.
Deciduousness is a phenological but also a hydraulic trait related to
drought avoidance strategy for trees from dry tropical trees (Wolfe et
al. 2016), but it is rarely used in drought studies. Deciduous species
lose their leaves during drought periods to reduce transpiration and
maintain water balance (Wolfe et al. 2016). When the water is available
again, these species show high stomatal conductance and photosynthesis,
both important mechanisms to grow and increase canopy cover (Lambers et
al. 2008). The duration of the deciduousness strongly affect carbon
sequestration by tropical deciduous and it has the potential to indicate
the magnitude of the drought
(Singh and Kushwaha 2016).
Deciduousness can explain why the recovery is faster in ridges and in
dry forests. However, most of the studies investigating drought response
mechanism focused on leaf economic traits, and not on hydraulic traits.
Repeated droughts can act as filter selecting tolerant species
(Aguirre-Gutiérrez et al. 2020) and increasing the abundance of
drought-tolerant deciduous species (Fauset et al. 2012). Focusing on
traits related to water use and balance is a way to fill most of the
remaining mechanistic gaps regarding drought effects (Martinez-Vilalta
et al. 2019).
Conclusion
This literature review summarizes the role of abiotic and biotic factors
mediating drought resilience in tropical forests. Our synthesis
highlights that the regional climate conditions shape the forest types,
and the topography controls biotic and abiotic factors at a local scale
in different forest types. Both
dry tropical forests and ridges are more sensitive to droughts than
moist tropical forest and valleys but the mechanisms explaining these
patterns remain unknown. Field studies are essential to identify local
and regional differences in drought resilience and to predict the future
of tropical forests. This
literature review also highlights the main gaps in drought resilience
research, which are: 1) to identify mechanisms explaining both the
growth-mortality and resistance-recovery trade-offs; 2) to understand
how different functional groups (dominant vs. subordinate species,
shade-species vs. sun-species, trees vs. shrubs) deal with droughts; 3)
to describe the physiological mechanisms explaining the forest
resilience of different habitats (valley versus ridge), forest
types (moist versus dry forests) and successional stages
(secondary versus primary forests); 4) to understand how droughts
change the microclimate in different habitats.