Discussion
Phylogeny explains most of trait
variations
Linking patterns to processes in community ecology is often challenging,
especially in field-based studies. Several authors have suggested to use
trait variations to infer community assembly mechanisms (McGill, 2008;
Taudiere & Violle, 2016; Violle et al., 2007, 2012). To tease apart the
multiple factors that drive community assembly in aquatic systems, we
partitioned the variance of several traits among three distinct, yet
interacting, scales, i.e. space, time, and phylogeny.
Importantly, studies simultaneously taking different scales into account
remain rare (but see e.g. Henn et al., 2018; R. Liu et al., 2018;
Luo et al., 2016), and to our knowledge, none of them have so far
considered an interannual effect over several years.
In the present study, variance partitioning among tested scales is
uniform among traits, indicating that the processes determining these
different trait values are similar. Community assembly mechanisms
operating through time (year) and space (regional scale) are responsible
for a low percentage of total trait variance, in line with the
observations formerly reported by Fu et al. (2013). These authors also
partitioned trait variance, but across spatial scales only, and they
found that large spatial scale (i.e. regional scale including
different lakes) does not account much for the root/shoot ratio, and
leaf number variations in the macrophyte species Potamogeton
maackianus . In our work, trait distributions are fairly conserved among
sites and suggests a filter operating on the overall distribution of
trait values within the region. Then, we showed that intra-site
variations (inter and intraspecific scales) were overwhelmingly dominant
in comparison with inter-site variations, for all traits. In other
words, the trait means were variable among species in each site, and
among individuals in each species. Thus, a mechanism participated in
spreading trait values around the optimum values within sites. This
observed pattern can arise from several non-exclusive hypotheses. First,
adaptation to habitat heterogeneity within sites can lead to different
optimal trait values depending on the micro-site considered. Second,
biotic interactions can disperse trait values to limit the similarity
between individuals, thus reducing competition. As highlighted by
Messier et al. (2010), both niche and neutral theory can play a role in
community assembly, since a filter select individuals based on their
trait values rather than their species identity, finally constraining
trait values at regional scale.
Interestingly, phylogeny accounted for the most of all trait variations,
with in particular intraspecific trait variations being higher (56.29%
on average) than interspecific variations in most traits. However, the
relative importance of interspecific versus intraspecific trait
variability was trait-depend which is consistent with previous studies
showing that the relative amount of interspecific versusintraspecific trait variability differ among studies and traits (see
Albert, Thuiller, Yoccoz, Douzet, et al., 2010; Fajardo & McIntire,
2010; Roche et al., 2004). We found LDMC and specific internode mass to
vary more between species than within species. This indicates that
traits related to resources conservation are highly conserved among
species, allowing different species to specialize and co-occur along
habitat gradients (different conditions among ponds). However, growth
and resources acquisition traits (height, SLA, internode length, maximum
root length) varied more within species than between species, in line
with Siefert et al. (2015) who found that “whole-plant traits”
(i.e. plant height, and architecture) were more variable within
population than between species in a global-scale meta-analysis. This
high amount of intraspecific trait variability allows individuals to
better resist to filters, and the environmental heterogeneity at very
fine scale (within-pond habitat variations) can lead to high variation
in phenotypic trait values. Another non-exclusive hypothesis is that, in
case of macrophytes, architectural traits can display multiple trait
values since individuals are much less constrained by gravitational
force than terrestrial species (Fu et al., 2013).
We confirmed that partitioning trait variance is a relevant approach to
detect at which scale operate the most decisive processes in plant
community assembly without scale dependency issues (McGill, 2008).
Moreover, we underlined the strong importance of ITV in shaping
community assembly (Jiang et al., 2016; Violle et al., 2012), and we
then argue that not only species mean and community-aggregated trait
values (Schamp et al., 2007; Stubbs & Bastow Wilson, 2004) but also
trait distributions have to be analyzed when studying community dynamics
and structure (de la Riva et al., 2016; Henn et al., 2018). Including
ITV in community ecology can improve the detection of processes
underlying species coexistence at local scale (Doudová & Douda, 2020;
Fu et al., 2014; Violle et al., 2009).
Intraspecific trait variation in response to both biotic and
abiotic variables
Trait based approaches are widely used in the literature to investigate
individual responses to abiotic and biotic filters separately (Violle et
al., 2007), although individuals usually cope with both types of filters
within plant communities. As a consequence, our vision of ITV in a
context of multiple constraints remains partial. In our study, we
propose to fill this literature gap by simultaneously testing trait
responses to different abiotic and biotic variables.
Contrary to our expectations, in pond living individuals, all traits did
not respond to both abiotic and biotic variables. Height, SLA, and
internode length on the one hand, and specific internode mass on the
other hand, were respectively influenced by abiotic or biotic variables
only, although these traits are known to usually respond to these two
types of variables (Bittebiere & Mony, 2015; Loughnan & Gilbert, 2017;
Rusch et al., 2011; Santamaría, 2002). However, all other traits
variations (i.e. LDMC, maximum root length, and specific root
mass) were due to both biotic and abiotic variables, as predicted. These
different patterns of trait responses indicate that, in a context of
multiple constraints, individual plant does not respond as a whole, but
instead, each trait has a singular role. This finding challenges the
validity of conclusions that assume responses at a whole-plant level (De
Kroon et al., 2005), and suggests that survival within multi-constrained
habitat, relies on low phenotypic integration (Murren, 2002) allowing
the expression of multivariate phenotypes. Overall, our study thus
underlines the relevance of multi-traits approaches integrating both
biotic and abiotic variables, as also stated by Chalmandrier et al.
(2022), to efficiently capture plant response strategies, and ultimately
identify mechanisms of species coexistence at local scale. Besides, our
observations suggest that patterns of trait variations measured in
situ should be carefully interpreted as they may not reflect responses
to one type of filter only, either biotic or abiotic (Duarte et al.,
1986; Kõrs et al., s. d.; Su et al., 2019).
In the ponds of the Iles Kerguelen, each trait category was involved in
the response to specific habitat variables. First, traits related to
nutrient acquisition and light acquisition as SLA did respond to water
nutrients. More precisely, SLA decreased when water nutrients increased,
suggesting that macrophyte species may be plastic to either maximize the
capture of light when higher nutrient concentrations stimulate
phytoplankton growth reducing light penetration in water (Rabalais,
2002), or maximize the capture of nutrients (Lavorel & Garnier, 2002).
Root length, also involved in nutrient acquisition, was positively
impacted by species abundances. Competition for nutrient acquisition
would favor root traits divergence and force plants to optimize resource
uptake (Ferguson et al., 2016; Manschadi et al., 2006). This result
indicates that root trait variations can be useful in detecting
responses to biotic competition, although they are poorly considered in
field studies due to the difficulty of sampling (Colom & Baucom, 2020).
Secondly, traits related to resources conservation, as LDMC, specific
internode, and root masses were negatively impacted by competition.
Indeed, resource storage decreased within connection internodes and
roots in response to species abundance and/or phytoplankton biomass,
perhaps reflecting an escape strategy towards less competitive
micro-sites for nutrients. To a lesser extent, LDMC also responded to
sediment nutrients, which is consistent with the literature (Fu, 2020;
Garnier et al., 2001). Previous studies suggested indeed that an
increase in nutrient availability may induce leaf trait variability
towards a low conservation of nutrients, as a decrease in LDMC for
instance (Poorter & Garnier, 2007). Lastly, internodes elongated with
water depth, probably as part of harsh conditions avoidance strategy
(Bittebiere & Mony, 2015; Callaghan et al., 1992; Louâpre et al.,
2012).
As a result, while many previous studies focused on the effects of one
or few variables on species, we argue to consider several biotic and
abiotic variables in future studies to better understand the effects of
environmental changes on plant communities (Cavieres et al., 2014; Crain
et al., 2004; Klanderud et al., 2015; Mitchell et al., 2017; Morris et
al., 2020; Wood et al., 2012).
Effects of trait values and their relationships on
macrophyte
performance
The SEM approach allowed us to highlight that all traits, except LDMC,
had either direct or indirect effects on individual performance. This
observation is especially important as most published studies neglect
the relationships between traits when dealing with their influence on
individual performance (Engbersen et al., 2022; Pywell et al., 2003), in
particular in aquatic ecosystems (Fu et al., 2014; Ma et al., 2022). Our
study thus supports the current view in functional ecology underlying
the relevance of multi-traits approaches taking trait relationships into
account (Albert, Thuiller, Yoccoz, Douzet, et al., 2010; Bittebiere et
al., 2019; Blonder et al., 2014; Gustafsson & Norkko, 2019).
As traits are interrelated, adjustments in trait values must be
coordinated to produce a properly functioning organism, also meaning
that patterns of trait correlations can greatly change across
environments (Murren, 2002). To maintain optimal fitness, it is expected
that plant individual should present high correlations among
functionally related traits (high integration within functional unit),
and lower correlations among functionally different traits (among
functional units), conferring flexibility yet coordination to
individuals (Nicotra et al., 1997). This is consistent with our results
where the highest correlations were found among traits related to
resource storage (specific internode mass, specific root mass), or
traits related to resource acquisition/conservation strategies (SLA,
LDMC).
Comparing the respective effects of traits on individual performance, we
observe that clonal traits act more intensely and more directly on
performance than expected, suggesting their crucial importance for
individual survival. These traits allow to forage for suitable
micro-habitats (Suzuki & Stuefer, 1999) and store resources (Dong et
al., 2010), which is essential to maintain within constrained habitats.
Pooling direct and indirect effects, growth and storage traits
(i.e. height, specific internode mass, and specific root mass)
have stronger positive effects than architectural traits (root and
internode length), which is consistent with the results presented in
Wildová et al. (2007). Individual growth and storage traits are directly
related to individual size, subsequently affecting individual biomass,
whereas architectural traits are more related to colonization ability
and allocations between organs, thus affecting more indirectly the
individual performance (Wildová et al., 2007). Besides, traits related
to resource storage have here stronger effects (amplified by the
correlation between specific internode mass and specific root mass) than
traits related to resource acquisition (SLA), probably implying a
priority in investing in resource conservation within constrained
habitats like ponds of the sub-Antarctic region.
Finally, abiotic variables can have cascading effects on individual
performance through their influence on trait variations. Indeed, changes
in abiotic values from season to season and from year to year, within
constrained habitats like polar ponds, would greatly impact plant trait
values. For example, an increase in water temperature reduces root
length, indirectly and negatively affecting individual performance.
Thus, although rising water temperatures can stimulate macrophyte
performance within the optimum thermal range (Dar et al., 2014), it may
present a negative impact within sub-Antarctic ponds, suggesting that
this optimal thermal range can be overpassed (Frenot et al., 2006).
Similarly, variations of water depth affect plant performance, through
its effects on internode length. As water temperatures keep warming up
and precipitations keep decreasing (Walther et al., 2002), one can
predict that the consequences for the macrophyte community structure and
its productivity will be severe.