INTRODUCTION
Compelling evidence shows that biodiversity enhances essential ecosystem
functions, such as productivity and decomposition rates (Loreau &
Hector 2001; Hooper et al., 2005; Cardinale et al., 2012). One primary
underlying reason may be that individual species or groups of species in
different functional groups may have dissimilar niches (niche
complementarity effects ) which allow diverse communities to maximize
resource utilization and minimize competition (Cardinale et al., 2011;
Zuppinger-Dingley et al., 2014). In theory, such niche differences
include temporal variation in biological activity (Ebeling et al.,
2014), and species in a community can adjust the timing of their
biological activity in such a way that they cover the longest possible
time and/or use the resources from the largest possible space in the
habitat. If phenological niche differences are high enough, they can
affect the shape of the phenology at the community level. For instance,
if a plant community is composed of species that grow in early spring,
the aboveground growing season will be extended, compared with a
community lacking those species (Ebeling et al., 2014; Rudolf, 2019).
Therefore, species and functional group diversity can affect the timing
of community-level productivity (i.e. community phenology) via
temporal niche differentiation and/or increasing the probability of
species with those traits to occur in the community (selection
effect ) (Loreau & Hector 2001). However, variation in phenology is
primarily monitored at the species rather than community level.
Moreover, phenological variation is typically attributed to changes in
climate drivers, such as temperature and water supply (Wright and van
Schaik 1994; Staggemeier et al., 2018), and has rarely been quantified
as a response to changes in biodiversity (but see Wolf et al., 2017 and
Guimarães-Steinike et al., 2019).
Most ecosystem processes are soil-related or even soil-dependent
(Bardgett & van der Putten, 2014; Soliveres et al., 2016; Schuldt et
al., 2018). However, phenology tends to be monitored on easily observed
aboveground response variables, and evidence describing soil phenology
is mostly lacking (Bonato Asato et al., 2023). This knowledge gap leads
to uncertainty about how well soil properties and belowground processes
(i.e. root growth and activity of soil organisms) are predicted by
aboveground phenological strategies (Eisenhauer, 2012; Blume-Werry et
al., 2015; Eisenhauer et al., 2018). Because shoots and roots are
interdependent, tight synchrony of their responses to environmental
drivers is often expected (Iversen et al., 2015; but see Blume-Werry et
al., 2016). However, the role of biotic and abiotic constraints on this
synchrony seems to vary significantly among ecosystems and plant types,
ultimately affecting which organs grow first, faster, or remain active
and alive longer. Moreover, plant (roots and shoots) processes are often
assumed to indicate ecosystem functions driven by the activity of
organisms at adjacent trophic levels, such as soil fauna, but this may
not necessarily be the case. Hot moments (within-year events inducing
high activity) in soil organism activity depend, in part, on inputs from
root exudates or pulses of detrital inputs from senescent roots
(Kuzyakov & Blagodatskaya 2015). However, the limited evidence from the
field does not always confirm plant-activity-based assumptions. For
example, phenological monitoring of detritivore feeding activity during
the growing season in oaks has shown both a negative and no correlation
between feeding activity and oak branch production (Eisenhauer et al.,
2018). In an experimental grassland, feeding activity rates decreased
during the summer, when plant growth is usually high (Siebert et al.,
2019; Sünnemann et al., 2021). Evidence suggests that investments in
shoot and root production are commonly not synchronous (e.g. Steinaker
& Wilson 2008; Steinaker et al. 2010; Sloan et al. 2016; Blume-Werry et
al. 2016), as well as the dynamics of soil organisms (Bonato Asato et
al., 2023; Eisenhauer et al., 2018). However, we lack experimental
evidence demonstrating whether changes in biodiversity may influence the
predictability and synchronization of the dynamics above and below the
ground.
Presently, two predominant conceptual frameworks delineate the interplay
between biodiversity and the synchronization of ecosystem functions. On
the one hand, ecosystem stability theory suggests that increasing
biodiversity increases temporal asynchrony among populations and
functions, which would be one of the primary mechanisms for positive
diversity-stability relationships (Cardinale et al., 2013; Loreau & de
Mazancourt 2013). In other words, temporal asynchrony is needed for a
healthy (stable) ecosystem functioning. On the other hand, ecosystem
coupling, as defined by Ochoa-Hueso et al. (2021) as ”the orderly
connections between the biotic and abiotic components of ecosystems
across spaces and/or time”, suggests the opposite: for more efficiently
process, cycle, and transfer of energy and matter, a higher temporal
coupling of populations and functions is needed. Under this point of
view, temporal synchrony is required for more efficient ecosystem
functioning, and monitoring the dynamics of one function or population
can be used as an indicator of activity in the other. In both cases,
disruptions such as biodiversity change, may affect key aboveground or
belowground processes, leading to acceleration or delay of community
phenology and desynchronization of ecosystem functions. Despite the
potential importance of aboveground-belowground phenological synchrony,
the current lack of studies concurrently monitoring shoot, root, and
soil fauna dynamics has impeded a thorough understanding of the
mechanisms by which changes in biological diversity may influence the
responses of these affiliated processes.
Here, we examine how experimentally manipulated plant diversity
influences the phenological patterns of shoot, root, and soil fauna
dynamics (responses). In the framework of a long-term grassland
biodiversity experiment (the Jena Experiment; Roscher et al. 2014;
Weisser et al. 2017), using well-established methods (LiDAR,
phenological cameras, minirhizotrons, bait-lamina strips), we measure
ecosystem response variables that are often used to evaluate
aboveground-belowground ecosystem functioning and biological activity in
annual plant communities (e.g. plant community height, greenness,
root production, and detritivore feeding activity) every two to three
weeks over four seasons (one full year). We used these data to calculate
yearly values for each response variable, phenological patterns, and
synchrony between response variables. With this approach, we ask the
following questions:
1) How does plant diversity affect the yearly accumulated values of
aboveground plant traits and belowground activity? We expect that
increasing plant diversity throughout the year enhances all response
variables (Weisser et al. 2017; Mommer et al., 2015; Eisenhauer et al.,
2010).
2) Does plant diversity affect intra-annual aboveground and belowground
phenological patterns? We predict that plant community shoot dynamics
will be concentrated in spring and summer, as usual in temperate
regions. Root production should last longer than that of shoots, as
found in other studies (Steinaker & Wilson 2008; Blume-Werry et al.
2016), even though it is not clear if this longer activity is driven by
an earlier start of the production, a later end, or both. For
detritivore feeding activity, we expect a peak in early spring due to
high moisture and increased temperature and another peak in autumn,
driven by the increased availability of resources by above- and
belowground plant-derived inputs and high moisture.
3) Do changes in plant diversity affect the synchrony of shoot, root, or
soil organism dynamics? We expect plant species richness and functional
group richness to enhance aboveground-belowground activity, which could
lead to either more or less synchronized patterns. If plant diversity
drives enhanced functioning at different time points (e.g. advances
plant growth and delays root senescence), we could see a negative
diversity effect on synchrony.
4) Does the time of year influence the strength/direction/predictability
of relationships between aboveground-belowground response variables?
Because plant shoots are only active for a restricted period, we expect
plant diversity effects to be most pronounced during the growing season
(Guimarães-Steinike et al., 2019), while abiotic constraints might
mostly drive belowground dynamics out of the growing season.