Introduction
Tropical forests contain more than half of the Earth’s terrestrial
species, store one quarter of the global terrestrial carbon and account
for one-third of net primary productivity (Bonan, 2008; Wright, 2010).
Therefore, any alteration in the structure or functioning of tropical
forests has important consequences for biodiversity conservation,
productivity and global carbon budgets. Currently, one of the most
eminent changes occurring over the last three decades in tropical
forests is the increase in liana abundance and biomass (Schnitzer &
Bongers, 2011; Yorke et al., 2013; Schnitzer, 2018). Lianas (woody
climbers) are non-self-supporting plants which rely on trees as supports
to grow and to gain access to the forest canopy (Schnitzer & Bongers,
2002; Gerwing et al., 2006). They are a prominent growth form across
lowland tropical forests where they may represent up to 40% of the
woody stems and more than 25% of the woody species (Gentry, 1991).
Lianas invest proportionally more in leaf mass than in stem
cross-sectional area than trees, thus, deploying a large canopy of
leaves on the host trees that they infest (Putz, 1984; Gerwing &
Farias, 2000). Intense competition for above- and below-ground resources
with lianas may limit tree recruitment, growth, reproduction and
survival (Putz, 1984; Stevens, 1987; Clark & Clark, 1990; Schnitzer et
al., 2000; Ingwell et al., 2010). Moreover, the negative effect of
lianas is greater on late-successional- than on pioneer tree species
(Schnitzer & Carson, 2010); this has enormous consequences for
community richness and composition, as well as for ecosystem-level
dynamics such as carbon storage (Schnitzer & Bongers, 2011; Schnitzer,
2018). Currently, at least eight studies have provided evidence for
increases in liana abundance or biomass, or both, across Neotropical
forests (Schnitzer & Bongers, 2011). However, not all studies support
the liana increase hypothesis. For instance, only two studies have
evaluated the lianas’ growth rates for the African continent and these
did not find an increase in their abundance or biomass (Schnitzer &
Bongers, 2011; Schnitzer, 2018, Bongers et al. 2020). One possible
explanation for these different results across the tropics may be due to
taxonomic and functional trait differences among the species present in
each of those continents. In fact, Gallagher & Leishman (2012), in a
global analysis for climbing plants, found a difference in the
proportion of species having tendril or twining climbing mechanisms in
Africa and the Americas. However, whether these taxonomic differences
are related to specific morphological and physiological traits is still
not clear. One reason is that most of the studies investigating the
morphological and physiological traits in lianas have contrasted them
with trees, while few have addressed differences amongst lianas
differing in their climbing mechanisms (Carter & Teramura, 1988;
Durigon et al., 2013). Consequently, the current predominant view
considers lianas as a uniform group and, so far, no comprehensive work
has been carried out to test if different climbing strategies may also
account for functional trait variability among liana species (Medina et
al., 2021). Recognizing functional and morphological differences among
liana climbing mechanisms may be essential for understanding their
spatial and temporal patterns of abundance across tropical forests,
particularly if the increase in liana abundance and biomass is driven by
taxa with a specific climbing mechanism and growth strategy. Therefore,
if differences between groups of lianas exist and are not accounted for,
this may lead to a misrepresentation of the role of lianas role in
forest successional dynamics, which, in turn, will have important
implications for our understanding of forest responses to climate
change.
Lianas have long been attracting the interest of botanists because of
their distinctive climbing mechanisms and growth strategies (Darwin,
1875; Isnard & Silk, 2009) (see Box 1). The vertical growth of lianas
is facilitated via a large diversity of attaching systems (Putz, 1984;
Nick & Rowe, 2004; Isnard & Silk, 2009; Speck & Burgert, 2011). Each
type of climbing mechanism (see Fig. 1) may differ in carbon allocation
and the mechanical support requirements necessary for vertical growth,
consequently determining the differences in life history among the liana
species. For example, it has been proposed that each type of climbing
mechanism determines the maximum distance between supports and that
climbing success depends on the maximum stem diameter support that they
can colonize (Putz & Holbrook, 1991; Isnard & Silk, 2009; Rowe &
Speck, 2004). Darwin, in his book “The climbing movement of plants”
(1875) (the first study to investigate the ecological behavior of
climbing plants), did not consider species which merely scramble over
vegetation without any special organ. He described hook-climbers as
having the least efficient climbing mechanism, followed by hook and root
climbers, while he considered the more widespread twining and tendril
climbers to be the most efficient. Those early observations are in
accordance with modern-day measured mechanical properties of wood from
different types of climbers. For instance, tendril and twining species
generally have more flexible stems, while hook-climbers and scramblers
retain relatively stiff stems throughout their lives (Isnard & Silk,
2009; Speck & Burgert, 2011; Rowe & Speck, 2004). Considering the
lianas life history, one emerging question is whether an active climbing
mechanism, which facilitates easier access to the upper canopy, is
associated with a resource-acquisitive strategy via functional traits.
The theoretical basis for this hypothesis relies on the fact that the
type of climbing mechanism limits the maximum size of the support used
for vertical growth (e.g., the stem diameter to which a specific
climbing mechanism can attach and, consequently, climb on), as well as
the light environment that can be explored (Darwin, 1875; Putz, 1984;
Holbrook & Putz, 1991). Therefore, the success of certain types of
climbing mechanisms will differ according to the forest structure and
successional stages (Putz & Chai, 1987; DeWalt et al., 2000). Likewise,
there is evidence that the proportion of species with different climbing
mechanisms differ significantly between continents (Gallagher and
Leishman, 2012), but the main drivers (climate, soil and forest
structure) of these patterns are still not explored.
Plant functional types have been used by ecologists to aggregate the
enormous number of plant species into a tractable number of functionally
similar classes (Ustin & Gamon, 2010). This classification implies an
ecological basis to differentiate between groups of plants responding
similarly to changes in their environments (Diaz & Cabido, 1997;
Lavorel & Garnier, 2002), while there is also strong support for
significant differences in key traits among plants of different
functional types (Wright et al., 2004, 2005; Verheijen et al., 2016);
such classification is necessary in order to reduce the need for
specific knowledge about each underlying species functional trait. Plant
traits are suitable tools for describing the different functional
aspects of plants and their relationships to environmental conditions.
The various growth and survival strategies of plants in response to
abiotic and biotic determinants are reflected by their set of trait
values (Westoby et al., 2002; Reich, 2014; Verheijen et al., 2016). An
increasing number of global overviews have been reported for various
functional groups of plants (e.g., Wright et al., 2005a, b; Poorter et
al., 2012; Verheijen et al., 2016) and it becomes clear that several
questions characterizing lianas as a group still need to be answered
(Wylka et al., 2013; Schnitzer, 2018; Medina et al., 2021). Although the
morphology, anatomy and physiology of the climbing organs used by lianas
to reach the canopy have been relatively well studied (for a review see
Isnard & Silk, 2009), much less effort has been made to understand if
there is a relationship between the type of climbing mechanism and the
functional traits related to whole-plant performance, such as the leaf
and wood economic spectra traits (Wright et al., 2004; Chave et al.,
2009; Reich, 2014). If such links exist, this information would be
especially needed to properly account for the role of lianas in forest
dynamics via Dynamic Global Vegetation Models (DGVMs) (Verbeeck et al.,
2016; Schnitzer et al., 2016, Meunier et al., 2021). Similarly, the few
studies which have characterized the drivers of liana abundance and
species richness have focused on only a few environmental variables and
have mainly compared lianas to trees (Schnitzer, 2005), focused on
specific liana clades and biogeographical realms such as the Neotropics
(Meyer et al., 2020), or on a particular type of climbing mechanism
(Durigon et al., 2013). Therefore, we still do not know how the
environment (e.g., climate and soil) and the forest structure drive the
proportion of species (richness) and abundance (density) of lianas
regarding their main climbing strategies across the large spatial
scales.
Classifications of the climbing mechanisms used by lianas may vary
substantially throughout literature, ranging from three categories
(Vaughn & Bowling, 2011) to as high as nine in some cases
(Addo-Fordjour & Rahmad, 2015), as recently reviewed by Sperotto et al.
(2020). In this study, we followed the recently proposed classification
of climbing mechanisms from Sperotto et al. (2020) to establish a
framework which considers a continuum from highly-specialized obligate
lianas (active climbing) to species with an intermediate behavior
(passive climbing) and devoid of highly specialized attachment systems
(Fig. 1). Here we analyzed the functional strategies and distribution of
lianas, classifying lianas into two main types of climbing mechanisms:
active and passive. In general, active climbing comprises twining,
tendrils, prehensile branches, twining petioles and prehensile peduncles
and inflorescences, while passive climbing comprises scrambling (or
clambering, leaning), hooks or grapnels and adhesive roots.
The current perspective regarding
the ecology of lianas remains somewhat limited because previous analyses
of liana ecology have largely focused on the differences between lianas
and trees and, so far, no major synthesis has considered the life
history differences among lianas in terms of their climbing mechanisms.
Here we synthesize data for lianas regarding the main functional traits
used to characterize plant form and function and, thus, classify the
liana species according to their main type of climbing mechanisms (Fig.
1, Box 1): active and passive climbing. Furthermore, we integrate the
liana species climbing mechanism data with a standardized pantropical
plot sampling of the species richness and abundance, in addition to
remote sensing data (climate and soil) to explore the following
hypotheses:
(1) There is an association between the climbing mechanism and
functional traits, therefore, we expect that functional traits differ
between active and passive climbing lianas. More specifically, we expect
that species with active climbing, that forage vertically through a
short-term vigorous growth, show functional traits towards the
acquisitive end of the global trait spectra.
(2) The magnitude and direction of the associations between the main
drivers (climate, soil and forest structure) of the relative abundance
and richness of lianas differ between active and passive climbing
species (Table 1). We expect that taller forests will favor active
climbers, whereas shorter forests will favor passive climbers. We expect
that climate and soil fertility show a positive relationship to species
richness for both active and passive climbing, while abundance may
respond differently to those variables because recruitment is also
affected by forest structure (availability of suitable supports).
Here, we first show that functional trait differences are significant
between the two main categories of liana climbing mechanisms: active and
passive climbing (Sperotto et al., 2020). Subsequently, we show that the
factors driving abundance and species richness of lianas across tropical
forests differ significantly between active and passive climbing
species. Finally, we discuss the need of reconsidering the view of
lianas as a single, plant functional type, given the importance of the
climbing mechanism to the life history and ecology of lianas.
Box 1. The definition of climbing mechanisms and their
importance in the life-history of liana.
Lianas are a particular type of
climbing plant that develop woody stems and have a non-self-supporting
habit so they rely upon an external support for vertical growth towards
the canopy (Rowe and Speck, 2004; Schnitzer & Bongers, 2002). In
general, the ontogeny of lianas is marked by two distinct phases:
firstly, the erect phase, where, after germinating, they can grow
vertically adopting a self-supporting habit and can reach up to 2 m
height without the need for an external support and, secondly, the
climbing phase (Putz & Holbrook, 1991), which is marked by a rapid
increase in the internode distance with low investment in ramification
and foliar expansion until a suitable support is found (Hegarty, 1991;
Isnard & Silk, 2009; Ichihashi and Tateno, 2015). This marked
plasticity in response to the availability of support is associated with
several changes in the anatomy, morphology and physiology of the leaves,
stems and branches; this is a key feature in the life history of many
liana species (Putz, 1984; Gentry,
1991; Isnard & Silk, 2009; Chen et al., 2014). The need for finding a
support for vertical growth is also an important determinant of the
spatial distribution of lianas inside forests (Putz, 1984; Putz &
Holbrook, 1991; Schnitzer & Bongers, 2002). For example, tendril
species are restricted to attach to trees with smaller diameters than
twiner species (Putz, 1984; Putz and Chai, 1987), therefore, in forests
with high rates of fragmentation or gap formation, where more small
trees are present, tendril species tend to show higher abundance (DeWalt
et al., 2005; Letcher & Chazdon, 2009).
The transition between the self- and non-self-supporting phase described
above is also heavily dependent on the type of climbing mechanism that
lianas can use to attach to the support structures. Lianas exhibit a
diversity of morphological and anatomical variation (Putz & Holbrook,
1991; Isnard & Silk, 2009; Rowe & Speck, 2004) related to the type of
attachment and the organs (e.g., leaf, branch or stem) used to adhere to
the support structures (climbing strategy). In part, this diversity
results from the unique demand to maintain stems that are both flexible
to twist, but also strong enough to climb and span across different
hosts without breaking during the search for light (Rowe & Speck, 2004;
Isnard & Silk, 2009).
Species
with an active climbing mechanism display a support-searching behavior
such as circumnutation, an endogenous growth-related rhythmic movement
in which leader shoots (i.e., shoots produced to search for supports)
sweep through the air in arcs (Darwin, 1875; Hegarty, 1991; Carlquist,
1991; Putz et al., 1991; Isnard & Silk, 2009). This greatly increases
the possibility of the plant finding suitable supports. On the other
hand, species with a passive climbing mechanism do not actively search
for support, rather, they merely grow over the host plants without any
searching movements such as circumnutation. Additionally, species with a
passive climbing mechanism may have adhesive roots or specialized
grapnels or hooks to ensure their attachment to supports.