Received: 18 April 2024 | Accepted: 14 November 2024

DOI: 10.1111/1365-2745.14470

RESEARCH ARTICLE

Seasonal shifts in plant diversity effects on

above-­ground–below-­ground phenological synchrony

Ana E. Bonato Asato1,2 | Claudia Guimarães-­Steinicke1,3 | Gideon Stein1,4 |

Berit Schreck5 | Teja Kattenborn1,3 | Anne Ebeling6 | Stefan Posch5 |
Joachim Denzler1,4,7 | Tim Büchner4 | Maha Shadaydeh4 | Christian Wirth1,2 |
Nico Eisenhauer1,2 | Jes Hines1,2
1
German Centre for Integrative Biodiversity Research (iDiv) Halle-­Jena-­Leipzig, Leipzig, Germany; 2Institute of Biology, Leipzig University, Leipzig, Germany;
3
Remote Sensing Centre for Earth System Research (RSC4Earth), 04103, Leipzig University, Leipzig, Germany; 4Computer Vision Group, Faculty of Mathematics
and Computer Science, Friedrich Schiller University Jena, Jena, Germany; 5Institute of Computer Science, Martin Luther University Halle-­Wittenberg, Halle
(Saale), Germany; 6Institute of Ecology and Evolution, Friedrich Schiller University Jena, Jena, Germany and 7Michael Stifel Center Jena for Data-­Driven and
Simulation Science, Friedrich Schiller University Jena, Jena, Germany

Correspondence
Ana E. Bonato Asato Abstract
Email: [email protected]
1. The significance of biological diversity as a mechanism that optimizes niche
Present address breadth for resource acquisition and enhancing ecosystem functionality is well-­
Teja Kattenborn, Department for Sensor-­
established. However, a significant gap remains in exploring temporal niche
Based Geoinformatics, University of
Freiburg, Freiburg im Breisgau, 79104, breadth, particularly in the context of phenological aspects of community dynam-
Germany
ics. This study takes a unique approach by examining plant phenology, which has
Funding information traditionally been focused on above-­ground assessments, and delving into the
Deutsche Forschungsgemeinschaft,
relatively unexplored realm of below-­ground processes. As a result, the influence
Grant/Award Number: Ei 862/29-­1, FOR
5000, FZT 118, 202548816 and PANOPS of biological diversity on the synchronization of above-­ground and below-­ground
504978936
dynamics is brought to the forefront, providing a novel perspective on this com-
Handling Editor: Wentao Luo plex relationship.
2. In this study, community traits (including plant height and greenness) and soil pro-
cesses (such as root growth and detritivore feeding activity) were meticulously
monitored at 2-­week intervals over a year within an experimental grassland ex-
hibiting a spectrum of plant diversity, ranging from monocultures to 60-­species
mixtures.
3. Our findings revealed that plant diversity increased yearly plant height, root
growth and detritivore feeding activity, while enhancing the synchrony between
above-­ground traits and soil dynamics. Soil microclimate also played a role in
shaping the phenology of these traits and processes. However, plant diversity
and soil microclimate on above-­ground traits and soil dynamics effects varied

Christian Wirth, Nico Eisenhauer and Jes Hines contributed equally to this work.

This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction
in any medium, provided the original work is properly cited and is not used for commercial purposes.
© 2025 The Author(s). Journal of Ecology published by John Wiley & Sons Ltd on behalf of British Ecological Society.

Journal of Ecology. 2025;00:1–13.  wileyonlinelibrary.com/journal/jec | 1

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2 BONATO ASATO et al.

considerably in strength and direction across seasons, indicating a nuanced rela-

tionship between biodiversity, climate and ecosystem processes.
4. Notably, observations during the growing season unveiled a sequential pat-
tern wherein peak plant community height preceded the onset of greenness.
Meanwhile, root production commenced immediately after leaf senescence and
persisted throughout winter. Although consistent throughout the year, detriti-
vore activity exhibited pronounced peaks in the summer and late fall, albeit with
notable variability.
5. Synthesis. The study underscores the dynamic interplay between plant diversity,
above-­ground–below-­ground phenological patterns and ecosystem functioning.
It suggests that plant diversity modulates above-­ground–below-­ground interde-
pendence through intricate phenological dynamics, with the degree of synchrony
fluctuating in response to the varying combination of processes and seasonal
changes. Thus, by providing comprehensive within-­year data, the research elu-
cidates the fundamental disparities in phenological patterns across shoots, roots
and soil fauna activities, thereby emphasizing the pivotal role of plant diversity in
shaping ecosystem processes.

KEYWORDS
above-­ground–below-­ground interactions, biodiversity-­ecosystem functioning, biological
indicators, grasslands, soil ecology

1 | I NTRO D U C TI O N & Van Schaik, 1994), and has rarely been quantified as a response
to changes in biodiversity (but see Guimarães-­Steinicke et al., 2019;
Compelling evidence shows that biodiversity enhances essential Wolf et al., 2017).
ecosystem functions, such as productivity and decomposition rates Most ecosystem processes are soil-­related or even soil-­
(Cardinale et al., 2012; Hooper et al., 2005; Loreau & Hector, 2001). dependent (Bardgett & van der Putten, 2014; Schuldt et al., 2018;
One primary underlying reason may be that individual species or Soliveres et al., 2016). However, phenology tends to be monitored
groups of species in different functional groups may have dissimi- on easily observed above-­ground response variables (Albert et al.,
lar niches (niche complementarity effects) which allow diverse com- 2019; Huo et al., 2022), and evidence describing soil (below-­
munities to maximize resource utilization and minimize competition ground plant parts and soil organisms) phenology is mostly lacking
(Cardinale et al., 2011; Zuppinger-­Dingley et al., 2014). In theory, (Bonato Asato et al., 2023). Because shoots and roots are interde-
such niche differences include temporal variation in biological activ- pendent, tight synchrony of their responses to environmental driv-
ity (Ebeling et al., 2014). ers is often expected (Iversen et al., 2015; but see Blume-­Werry
If phenological niche differences are high enough, they can affect et al., 2016). However, the role of biotic and abiotic constraints
the phenology at the community level. For instance, if a plant com- on this synchrony seems to vary significantly among ecosystems
munity is composed of species that grow in early and late-­season, and plant types, ultimately affecting which organs grow first,
the above-­ground growing season will be extended, compared with a faster, or remain active and alive longer. Moreover, plant (roots
community lacking those species (Ebeling et al., 2014; Rudolf, 2019). and shoots) processes are often assumed to indicate ecosystem
Therefore, over time, differences among taxa can affect the timing functions driven by the activity of organisms at adjacent trophic
of community-­level productivity via temporal niche differentiation levels, such as soil fauna, but this may not necessarily be the case.
(complementarity effects) and/or increasing the probability of species Within-­year events inducing high activity in soil organism activity
with those traits to occur in the community (sampling effect) (Loreau depend, in part, on inputs from root exudates or pulses of detrital
& Hector, 2001). Those differences can be realized either as species inputs from senescent roots (Kuzyakov & Blagodatskaya, 2015).
diversity or functional group diversity. However, variation in phe- However, the limited evidence from the field does not always
nology is primarily monitored at the species rather than community confirm plant-­a ctivity-­b ased assumptions, such as expected high
level (Richardson et al., 2007; Yang et al., 2023). Moreover, pheno- growth and activity in spring and summer (Eisenhauer et al., 2018;
logical variation is typically attributed to changes in climate drivers, Siebert et al., 2018, 2019; Sünnemann et al., 2021). Instead, evi-
such as temperature and rainfall (Staggemeier et al., 2018; Wright dence suggests that investments in shoot and root production are
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BONATO ASATO et al. 3

commonly not synchronous (e.g. Blume-­Werry et al., 2016; Qu (Mommer et al., 2015) and detritivore feeding activity (Eisenhauer
et al., 2024; Sloan et al., 2016; Steinaker et al., 2010; Steinaker & et al., 2010).
Wilson, 2008), as well as the dynamics of soil organisms (Bonato 2. Does plant diversity visually affect seasonal above-­ground and
Asato et al., 2023; Eisenhauer et al., 2018). However, we lack ex- below-­ground phenological patterns? We predict that diversity
perimental evidence demonstrating whether changes in plant di- effects on plant community height and greenness will be con-
versity may influence the predictability and synchronization of the centrated in spring and summer, as usual in temperate regions
dynamics above and below the ground. (Staggemeier et al., 2018; Wang et al., 2023). Diversity effects
Presently, two predominant conceptual frameworks delineate on root production should last longer than that of shoots, as
the interplay between biodiversity and the (a)synchrony of ecosys- found in other studies (Blume-­Werry et al., 2016; Steinaker &
tem functions. On the one hand, ecosystem stability theory sug- Wilson, 2008), even though it is not clear if this longer activ-
gests that increasing biodiversity increases temporal asynchrony ity is driven by an earlier start of the production, a later end, or
among populations and functions, which would be one of the pri- both. For detritivore feeding activity, we expect diversity effects
mary mechanisms for positive diversity-­stability relationships within to peak in early spring due to high moisture and increased tem-
a trophic level (Cardinale et al., 2013; Loreau & de Mazancourt, perature and another peak in autumn, driven by the increased
2013). That is, temporal asynchrony is needed for a healthy (stable) availability of above-­ and below-­ground plant detritus and high
ecosystem functioning. However, ecosystem processes operate moisture.
across trophic levels. Therefore, ecosystem coupling, as defined by 3. Do changes in plant diversity affect the synchrony of shoot, root,
Ochoa-­Hueso et al. (2021) as ‘the orderly connections between the or detritivore feeding activity dynamics? We expect plant diver-
biotic and abiotic components of ecosystems across spaces and/or sity to enhance shoot, root and detritivore feeding activity, which
time’ presents a multi-­trophic alternative to evaluate efficient eco- could lead to either more or less synchronized patterns. If plant
system processes, cycles and transfer of energy and matter. A higher diversity enhances functioning at different time points (e.g., ad-
temporal coupling of populations and functions indicates more ef- vances plant growth and delays root senescence), we could see a
ficient ecosystem functioning. Moreover, monitoring the dynamics negative effect of diversity on phenological synchrony (e.g., be-
of one function or population can be used as an indicator of activity tween plant height and root growth).
in the other. In both cases, disruptions such as biodiversity change, 4. Does the season influence the strength and direction of direct
may affect key above-­ground or below-­ground processes, leading to and indirect relationships between plant diversity, microclimate
acceleration or delay of community phenology and asynchronization and shoot, root, or detritivore feeding activity? Because plant
of ecosystem functions. Despite the potential importance of above-­ shoots are only active for a restricted period, we expect plant di-
ground–below-­ground phenological synchrony, the current lack of versity effects to be most pronounced during the growing season
studies concurrently monitoring shoot, root and soil fauna dynamics (Guimarães-­Steinicke et al., 2019), while abiotic constraints might
has impeded a thorough understanding of the mechanisms by which mostly drive below-­ground dynamics out of the growing season
changes in biological diversity may influence the responses of these (Box 1).
affiliated processes.
Here, we examine how experimentally manipulated plant diver-
sity influences the phenological patterns of shoot, root and detri-
tivore feeding activity. In the framework of a long-­term grassland 2 | M ATE R I A L S A N D M E TH O DS
biodiversity experiment (the Jena Experiment; Roscher et al., 2004;
Weisser et al., 2017), using well-­established methods (LiDAR, phe- 2.1 | The Jena Experiment
nological cameras, minirhizotrons, bait-­lamina strips), we measured
the indicators of above-­ground–below-­ground ecosystem function- This study was conducted in the Jena Experiment (Roscher
ing and biological activity in annual plant communities (i.e., plant et al., 2004; Weisser et al., 2017), located in the floodplain of the
community height, greenness, root production and detritivore feed- River Saale in the north of Jena (Thuringia, Germany, 50°55′ N,
ing activity) every 2–3 weeks over four seasons (i.e., spring, summer, 11°35′ E, 130 m a.s.l.). The soil is classified as Eutric Fluvisol, devel-
autumn and winter) over a year. We used these data to calculate a oped from up to 2 m-­thick fluvial sediments that are almost free of
total yearly value for each response variable, phenological patterns stones. Soil texture changes from silty clay to sandy loam with de-
and synchrony between response variables. With this approach, we creasing distance from the river (Steinbeiss et al., 2008). During the
ask the following questions: sampling period of this study (March 2021 to Feb 2022), air and soil
characteristics were monitored daily at a meteorological station on
1. How does plant diversity affect above-­ground shoot, root, site (Figure 2).
or detritivore feeding activity as indexed by accumulation Following a gradient in soil characteristics, the experiment was
of values throughout an entire year? We expect that in- set up in four blocks containing an equal number of plots per plant
creasing plant diversity throughout the year enhances plant diversity treatment within each block to avoid any confounding
height (Weisser et al., 2017), plant greenness, root production effects of soil heterogeneity. In total, the study site consists of 80
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4 BONATO ASATO et al.

response variable is commonly related to an ecological process

BOX 1 Illustrated glossary of key concepts. (Table 1). We also present a simplified description of the sampling

Phenology. Although classic phenology is studied at the in- methods for each process. Please see the Supplemental Material for

dividual or populational level, biological events at the com- an extended version of the methods.

munity level, such as leaf or root growth and senescence,

flowering, or soil fauna activity can be monitored, predicted
and related to weather and climate at the community level 2.3 | Statistical analyses
(Richardson et al., 2007; Yang et al., 2023). Here, we only
use phenology as a community concept. This way, plant First, to understand the effects of plant species richness and plant

phenology refers to plant traits and/or activities of the plant functional group richness on ecosystem functioning (question 1),

community, while soil phenology refers to the activity of we fitted eight linear mixed models, using one predictor and one re-

below-­ground plant parts and/or soil organisms. sponse variable per model. For these analyses, the values of each
sampling time were compiled as the sum of each of all values for
Phenological synchrony. The temporal convergence of phe-
each response variable during the entire year. We treated the block
nological events (sensu Wang et al., 2016). Here, we use
as random factor and species richness were log-­transformed to en-
synchrony as a non-­numeric concept but as a general
compass the design of the experiment (Roscher et al., 2004).
evaluation based on the co-­variation between two curves
Then, we tested the relationship between plant diversity and
throughout the year. If two curves (e.g., plant greenness
phenological synchrony (question 3). As a measure of phenological
and plant height) co-­vary together over time, synchrony
synchrony, we calculated Pearson's correlation index (r) between
will be higher. If not (e.g., plant height and detritivore feed-
all possible pairs of activities by plot (six pairs in total). Correlations
ing activity), synchrony will be lower.
were calculated based on data collected during the maximum tem-
Phenological coupling. How biotic ecosystem components poral extent possible; that is, for above-­ground–above-­ground and
are orderly connected (adapted from Ochoa-­Hueso above-­ground–below-­ground correlations for the entire growing
et al., 2021). Contrary to synchrony, which is a general season, and below-­ground–below-­ground correlations, for the en-
concept throughout the year, we use coupling as a numeric tire year. Significant correlations are referred to here as positively or
concept to understand how much two phenologies are negatively coupled, when the direction of the correlation is positive
distant from each other at one point in time. If, at one and negative, respectively. We fitted individual linear mixed-­effect
point in time, two phenologies are distant from each other models with the correlation coefficients as response and plant spe-
(e.g., plant height and detritivore feeding activity), we have cies richness or plant functional group richness as predictors.
minor coupling. If not (e.g., when both points are high or To evaluate whether time of year altered plant diversity ef-
low), we have major coupling (Figure 1). fects on the strength, and direction of relationships among above-­
ground and below-­ground response variables (question 4), we fit
a series of mixed-­effect models into a structural equation model
(SEM; Grace, 2006; Lefcheck, 2015), following the conceptual
plots (~5.5 m × 6 m) that differ in levels of sown plant species richness framework depicted in Figure S1. Given that the response vari-
(1, 2, 4, 8, 16 and 60 species) and plant functional group richness ables were sampled across the entire year, and differed in pattern
(one to four of the functional groups grasses, small herbs, tall herbs (above-­ground shoot responses were unimodal, while below-­
and legumes). Following common management practices in temper- ground responses were bi-­ or multimodal), we subset the dataset
ate extensively used grasslands in Central Europe, where the Jena into three parts. The ‘spring’ dataset encompasses the beginning
Experiment is located, the experiment was mowed twice. Moreover, of the above-­ground measurements until the first mowing (14
the experimental plots were weeded three times during the study July). The ‘summer’ dataset encompasses the sampling after the
period to maintain the plot's target species composition. For de- first mowing until the second mowing, when the above-­ground
tailed information on the design of the experiment and how the plots measurements finished (Figure S1a). Finally, the ‘winter’ data-
were established, please see Roscher et al. (2004). set encompasses only below-­ground phenology, from the end of
September until February (Figure S1b). To simplify models and to
avoid multicollinearity, we ran a stepwise selection of variables for
2.2 | Temporal above-­and below-­ground sampling each mixed-­effect model within the SEM, using the ‘step’ func-
tion, prior to the inclusion in the SEM. The resulting models were
We sampled plant height, plant greenness, root production and de- then used to build the initial SEM, using the piecewiseSEM pack-
tritivore feeding activity biweekly (or every 3 weeks during winter). age (Lefcheck, 2015). We inspected the initial SEM model results
Even though the measurements' definitions differ, for example, plant according to the goodness-­of-­f it tests for both the SEM and in-
community height would be better defined as a biological feature, dividual causal relationships. We selected the final model by ex-
and detritivore feeding activity is an activity rate, each measured cluding the insignificant factors and adding missing relationships
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BONATO ASATO et al. 5

F I G U R E 1 Conceptual representation of the key terms used in this work. Three representative phenologies are presented, two with
similar patterns and another with a different pattern. In this example, plant greenness (depicted by the green solid line) and plant height
(green dashed line) show higher synchrony if compared to any of those with detritivore feeding activity (brown solid line). The degree of
coupling may vary depending on the sampling time (x-­axis). In June, plant greenness is at its peak, while detritivore feeding activity is at
its lowest, resulting in decreased phenological coupling. In November, however, both plant greenness and detritivore feeding activity are
low, leading to high phenological coupling between them. Similarly, high phenological coupling would occur if both plant greenness and
detritivore feeding activity were at their peaks.

F I G U R E 2 Ombrothermic diagram
of (a) air temperature at 2 m above
the ground (continuous red line) and
precipitation (dashed blue line) and (b)
soil temperature (continuous red line)
and soil moisture (dashed blue line) at
8 cm below the ground in 2021 and
January 2022. The blue vertical stripes
in June and September indicate the two
mowing periods (14–25 June and 13–24
September).
Data source: Local climatic station in the
Jena Experiment.

that significantly improved the model's global fit. We treated block into block, to account for the repeated measurements at plot level.
as random factor, allowing responses to vary randomly between The variables mean plant community height, root production and
blocks. Given that samples taken from closer sampling point times species richness were log-­t ransformed. Due to the relationship
are more alike, we also accounted for temporal autocorrelation fit- between species richness and functional group richness, we have
ting a ‘corCAR1’ term in each model, specifying it as plot nested also incorporated correlated errors between those variables. We
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6 BONATO ASATO et al.

TA B L E 1 Summary of sampling information and ecological meaning of each response variable.

Response variable Ecological meaning Sampling period Simplified description

Plant community height It is often correlated with leaf 31 March to 13 September Using a terrestrial laser scanner (TLS),
quality, longevity and life-­history 2021 we generated 3D point clouds of the
traits. It is often used as a proxy for plot centre. The 3D point clouds were
plant biomass (Guimarães-­Steinicke classified into soil and vegetation
et al., 2019) points, to further extract average
plant community height (Guimarães-­
Steinicke et al., 2019)
Plant greenness It can be related to vegetation 31 March to 13 September We installed one phenological camera
density, chlorophyll content and 2021 (Brinno TLC200) pointing to the
photosynthetic activity and is centre of each plot corner. For each
normally used to detect leaf greening picture, we calculated the Green-­Red
up and autumn colouring timing. Vegetation Index (GRVI) (Motohka
(Cleland et al., 2006; Motohka et al., 2010; Yin et al., 2022)
et al., 2010)
Root production It is often related to soil carbon 10 March 2021 to 03 February We scanned each plot using
content, cycle and capacity to 2022 minirhizotrons. We then identified
acquire water and nutrients. It usually the root pixels of each scan using a
correlates to net primary productivity Neural Network and calculated the
and soil fauna activity (McCormack number of root pixels per scan (Ma &
et al., 2014; Ravenek et al., 2014) Chen, 2016; Ravenek et al., 2014)
Detritivore feeding activity Bait consumption is used as a proxy 26 February 2021 to In-­situ decomposer feeding activity
of detritivores' feeding activity and 03 February 2022 was measured using bait lamina strips,
is correlated with root exudation, which are PVC sticks with 16 holes
decomposition rates and nutrient filled with cellulose-­based bait. In
mineralization each sampling period, old laminas
were removed from the soil. The
holes were rated as empty (all bait
material was consumed, indicating
high feeding activity), partly empty,
or filled. Then, new laminas were
inserted in the soil (Birkhofer
et al., 2011; Eisenhauer et al., 2014)

assessed the homogeneity of residuals with residuals vs. fitted July and August, and dropped suddenly in September (Figure 3b).
values plots and Q-­Q plots for data normality using ‘Pearson’ cor- Interestingly, plant greenness was not affected by the mowing
relation (Zuur et al., 2009) for each of the mixed-­effect equations events (see Figure S2 for a daily variation of greenness). Root pro-
used in the SEM. Statistical analyses were performed with R v. duction started in December, peaking in May and August, with a
4.2.2 (R Core Team, 2022). short but abrupt decrease in July (Figure 3c). Already in March,
root growth exceeded the values attained later during the summer
months after the first mowing. Detritivore feeding activity showed
3 | R E S U LT S two broad peaks—the first one in late spring and mid-­summer, and
a second one in early winter (Figure 3d). The below-­ground data
3.1 | Overall phenological patterns of showed that detritivore feeding activity was much more variable,
above-­ground and below-­ground processes probably due to higher sensitivity to short-­term climate fluctuation
(questions 1 and 2) than shoots.

In general, plant diversity increased total shoot (except greenness),

root and detritivore feeding activity (plant species richness only; 3.2 | Plant diversity effects on the synchrony of
Table S1). Shoots were active between May and September. Plant above-­ground–below-­ground phenology (question 3)
height and greenness peaked in mid-­spring but showed a slightly
asynchronous pattern (Figure 3). Plant height increased rapidly Plant species richness affected the phenological synchrony of
from May to June, until the first mowing. Plants re-­started growing several response variables (Figure 4), especially during the early
at a slower pace and reached a lower maximum height before the growing season in spring (pre-­mowing, Figure 4a,b). Plant species
second mowing in September (Figure 3a). In contrast, plant green- richness increased phenological synchrony between plant com-
ness increased slowly in March, reached a stable peak across June, munity height and greenness (p = 0.006), plant community height
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BONATO ASATO et al. 7

F I G U R E 3 Phenology of plant and soil processes in response to plant diversity treatments in the Jena Experiment. The phenology of (a)
plant height, (b) greenness, (c) root production and (d) detritivore feeding activity from March 2021 to September 2021 for above-­ground
activity, and to February 2022 for below-­ground activity. The lines show the average monthly value for each species-­richness level, with
darker shades of green (above-­ground) and brown (below-­ground) indicating higher plant species richness. The blue transparent stripes
indicate the two mowing periods (14–25 June and 13–24 September).

and root production (p = 0.026) and greenness and root produc- above and below the ground was markedly influenced by the inter-
tion (p = 0.042). In contrast, plant functional group richness reduced play of plant diversity and abiotic dynamics. However, across the
phenological synchrony between greenness and detritivore feeding seasons, these influences shifted in strength and direction.
activity (p = 0.046) and plant community height and detritivore feed- During spring (Figure 5a), richer communities showed higher
ing activity (p = 0.021). This can be seen as a change from negative r plants, with increased root growth and enhanced activity of detri-
values to r values around zero. During summer (post-­mowing period, tivores, but with less plant greenness. Instead, plant greenness
Figure 4b,e), increasing species richness shifted the synchrony be- increased with soil temperature, increasing root production and detri-
tween plant community height and greenness from non-­significant tivore feeding activity. Plant functional group richness and soil mois-
to positive (p < 0.001). However, increasing plant functional group ture did not explain significant variation in response variables during
richness shifted the correlation between greenness and detritivore spring. Plant community height was associated with all other activi-
feeding activity towards non-­significance (p = 0.046) (Figure 4e). No ties—positively with greenness and root production, and negatively
significant plant diversity effects on phenological synchrony were with detritivore feeding activity. Moving into summer (Figure 5b),
observed over winter (Figure 4c,f). Detailed results for each relation- higher plant species richness corresponded to enhanced root pro-
ship can be seen in Table S2. duction and detritivore feeding activity. However, increased plant
functional group richness was observed to directly decrease detri-
tivore feeding activity, but to indirectly increase it via soil moisture
3.3 | Seasonal effects of plant diversity and (Figure 5b, R2 = 0.052). Notably, the impacts of abiotic factors on all
abiotic factors on above-­ground and below-­ground studied ecosystem processes were predominantly negative. Root
responses (question 4) growth declined with rising soil temperature and moisture, while
detritivore feeding activity decreased with increasing soil moisture.
We tested the direct and indirect effects (via soil microclimate) of Communities with taller plants showed cooler soil temperatures and
plant diversity (i.e. species richness and functional group richness) higher soil moisture content. Interestingly, in contrast to spring obser-
on plants and soils. Across the seasonal cycle, the timing of events vations, taller plant communities favoured detritivore feeding activity
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8 BONATO ASATO et al.

F I G U R E 4 Plant species richness (above) and plant functional group richness (below) effects on the phenological synchrony above
and below-­ground dynamics. The first column (a, d) refers to the spring (pre-­mowing) period, the middle column (b, e) refers to the summer
(post-­mowing) period, and the third column (c, f) refers to the winter period. Only significant (p < 0.05) relationships are shown (solid lines).
Each point refers to one plot. For the full results, please see Table S2.

during summer while reducing plant greenness. Moreover, greenness terms increased explanatory power only slightly in winter (marginal
was found to affect detritivore feeding activity positively. As winter and conditional R 2 = 0.14 and 0.15, respectively).
approached (Figure 5c), richer plant communities showed enhanced
root growth and soil moisture retention. Conversely, increased root
growth and detritivore feeding activity were observed in colder soils. 4 | DISCUSSION
Surprisingly, root production decreased detritivore feeding activity
during this season. As in summer, plant diversity indirectly affected 4.1 | Plant diversity effects of above-­ground–
detritivore feeding activity via soil moisture, but this time from plant below-­ground processes are present
richness (Figure 5c, R2 = −0.037). throughout the year
All models fitted the data well (Fisher's C and p-­values in
Figure 5). Plant height was only explained by a fixed term in the The magnitude and/or direction of the plant diversity effects on
2
spring model (marginal R = 0.42), but its variation was also ex- plant and soil processes changed throughout the year. This pin-
plained by the random terms (conditional R 2 = 0.45). Greenness was points phenology as a key, yet often overlooked, component of re-
explained only by the fixed terms (marginal and conditional R 2 = 0.39 lationships between biodiversity and ecosystem functioning. Plant
in the spring and R 2 = 0.05 in the summer model). The variation of diversity effects on overall plant height, root production and detriti-
root production was greatly explained by fixed terms in all models vore feeding activity are consistent with previous works (Birkhofer
(marginal R 2 = 0.24, 0.32 and 0.20 for spring, summer and winter, et al., 2011; Liang et al., 2016; Ma & Chen, 2016). However, the lack
respectively). Still, the random terms increased explanatory power of plant diversity effects on overall greenness was unexpected,
greatly (conditional R 2 = 0.90, 0.75 and 0.64 for spring, summer which may be explained by several reasons. One possible expla-
and winter, respectively). The variation in detritivore feeding activ- nation is that the competitive environment in species-­rich plant
ity explained by random terms decreased along the year (marginal communities may be translated into enhanced flower production
R 2 = 0.06 and 0.30 for spring and summer; conditional R 2 = 0.23 and (Ebeling et al., 2008), decreasing greenness and suggesting the
0.37 for spring and summer, respectively), to the point that random need to include more flower-­related metrics to understand diversity
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BONATO ASATO et al. 9

see Muraoka et al., 2013). Furthermore, plant diversity effects on

plant shoot production were shown in the first phase of the grow-
ing season, when diverse communities started growing earlier
than previously observed (Guimarães-­Steinicke et al., 2019). Given
that other experiments are younger (as in the case of Guimarães-­
Steinicke et al., 2019), our results are consistent with the sugges-
tion that temporal niche partitioning and legacy effects strengthen
the relationship between biodiversity and ecosystem functioning
over time (Dietrich et al., 2021; Guerrero-­Ramírez et al., 2017; Reich
et al., 2012; Vogel et al., 2019).
Plant diversity effects on plant processes disappeared in sum-
mer when the positive effects of soil temperature were also ab-
sent. Instead, the plant community showed several effects on soil
temperature and moisture during this period, including a buffer ef-
fect by plant height on soil temperature, as shown before (Huang
et al., 2023). The direction of biotic-­abiotic relationships is a clas-
sical discussion in Ecology (Mori et al., 2017). Several authors have
debated whether biotic factors (e.g. plant structure) are driven by
abiotic factors (e.g. soil temperature and moisture) or whether abi-
otic factors regulate diversity (Mori et al., 2017). Our results support
both relationships and suggest that the strength and causal direction
may change over the year even in the same community.

4.2 | Below-­ground activity is high during winter

We found surprisingly high below-­ground activity in winter, re-

vealing the influence of plant species richness and plant functional
group richness on soil functioning. This is particularly important in
grasslands, where roots account for about 70% of plant biomass
(Jackson et al., 1996; Poorter et al., 2012). Such high asynchronyza-
tion with above-­ground phenology was not expected but is par-
tially in line with other studies that found decoupling between fine
root production and shoot growth (Abramoff & Finzi, 2015; Huo
et al., 2022; Qu et al., 2024; Tamura et al., 2022; Wang et al., 2023).
Root production in winter suggests that niche differences among
species allow diverse communities to initiate growth at low tem-
peratures, possibly resulting from a shift in carbon allocation to
roots when temperature decreases (Poorter et al., 2012; Reich
et al., 2014). Early onset of root production in a plant can convey
F I G U R E 5 The relationships between plant diversity, a competitive advantage and diversify carbon allocation strategies
environmental factors and plant and soil phenology in (a) spring, (b)
(Albert et al., 2019; Harris et al., 1977), which may, in turn, contrib-
summer and (c) winter. Only significant (p < 0.05) paths are shown.
The black arrows indicate positive effects, while the orange arrows ute to enhanced productivity of diverse plant communities during
indicate negative effects. The arrow width is proportional to the the above-­ground growing season. The winter peak in detritivore
strength of the effect, which is indicated by the standardized feeding activity was unexpected, given that other works found
coefficient in the boxes on the lines. Double-­arrowed arrows low activities during winter (Siebert et al., 2018, 2019; Sünnemann
indicate correlated errors.
et al., 2021, but see Gottschall et al., 2022). Plant diversity con-
tinuously enhanced detritivore feeding activity during spring and
effects on plant community production fully (Motohka et al., 2010; summer, but only functional group effects were observed in winter.
Schiefer et al., 2021). Another plausible explanation may be that Altogether, these results demonstrate that an accurate depiction of
greenness is in this case a better proxy of community structure as- winter activity is required for a mechanistic description of temporal
pects (Guimarães-­Steinicke et al., 2019), such as density and vol- niche dispersion and biodiversity effects on ecosystem functioning
ume, not representing photosynthetic activity well in our study (but (Gottschall et al., 2022).
 |

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10 BONATO ASATO et al.

4.3 | Above-­ground–below-­ground (a)synchrony (Ochoa-­H ueso et al., 2021). In the context of biodiversity and eco-
along the seasons is mediated by plant diversity system functioning, above-­ground–below-­ground phenology may
broadly advance the interpretation of species coexistence. It can
Plant diversity effects on above-­ground–below-­ground phe- help propose new mechanisms on whether and how biodiversity
nological synchrony shifted across seasons, with independent enhances ecosystem functioning. Overall, this work shows funda-
impacts of plant species richness and functional groups shown. mental differences in the phenological patterns of leaf and root
During spring, plant diversity generally increased phenological production and the activity of soil organisms, stressing the role of
synchrony. Plant species richness enhanced height-­greenness plant diversity in modulating the phenology of plant processes and
synchrony, indicating an optimal growth strategy, with the highest soil fauna activity.
photosynthetic capacity reaching the timing of the highest physi-
cal structure (Zhao et al., 2022). During summer (post-­m owing), AU T H O R C O N T R I B U T I O N S
height-­greenness dynamics were asynchronous on average but Ana Elizabeth Bonato Asato, Jes Hines, Nico Eisenhauer and
showed a tendency towards positive synchrony with increasing Christian Wirth conceptualized the paper. Ana Elizabeth Bonato
species richness. This indicates that species-­r ich plant communi- Asato, Claudia Guimarães-­Steinicke and Anne Ebeling collected the
ties regrow faster after mowing (i.e. higher resilience, van Moorsel data. Claudia Guimarães-­Steinicke and Teja Kattenborn processed
et al., 2021), then plant height matches the high greenness. Plant the above-­ground data, while Gideon Stein and Berit Schreck pro-
diversity strongly enhanced height-­root synchrony during spring, cessed the below-­ground data with input from Stefan Posch, Joachim
probably due to earlier shoot growth and extended root produc- Denzler, Tim Büchner, Maha Shadaydeh and Ana Elizabeth Bonato
tion in species-­r ich plant communities. Due to the high synchrony Asato. Ana Elizabeth Bonato Asato statistically analysed all data,
of height-­greenness, roots were also synchronous with greenness with input from all authors. Ana Elizabeth Bonato Asato drafted the
in the same period. Even though plant functional richness was not manuscript, with high inputs from Jes Hines. All authors revised and
a significant driver of above-­and below-­ground activities in spring, approved the final version of the manuscript.
it affected above-­ground–below-­ground phenological synchrony.
Specifically, greenness-­feeding and height-­feeding activity shifted AC K N OW L E D G E M E N T S
from asynchrony in lower diversity to a non-­correlation in higher We kindly acknowledge all the coordinators and the garden-
diversity. This was the opposite in summer, when communities ing team for their exceptional work in maintaining the Jena
with higher plant functional group richness showed no synchro- Experiment. We are enormously thankful to Carla María Silvar
nous greenness-­feeding activity dynamics. This may reflect the Fernández and Marina Baile Cardoso Ficker for the constant help
negative effect of functional group richness on detritivore feeding in the field sampling, as well as Roman Patzak, Rike Schwarz, Felix
activity alone in the same period, causing a mismatch with green- Zeh and Julius Quosh for emergency help. We immensely thank
ness that was still high. Even though detritivore feeding activity Laura-­F iona Heptner, Georg Hähn and Alfred Lochner for their
and root production were high in winter, their within-­winter dy- lab support. We also thank Kevin Mueller and Solveig Franziska
namics differed, resulting in non-­correlated root growth-­feeding Bucher for their enlightenment and critiques in the early stages
activity dynamics. of manuscript preparation. The Jena Experiment is funded by the
German Research Foundation (DFG, FOR 5000). Moreover, we ac-
knowledge the support of iDiv funded by the German Research
5 | CO N C LU S I O N S Foundation (DFG–FZT 118, 202548816).

The stimulating effects of plant diversity on plant biomass C O N FL I C T O F I N T E R E S T S TAT E M E N T

(Cardinale et al., 2013; Hooper et al., 2005; Liang et al., 2016; The authors declare no conflicts of interest.
Loreau & Hector, 2001), root productivity (Ma & Chen, 2016;
Oram et al., 2018; Ravenek et al., 2014) and soil fauna activity PEER REVIEW
(Birkhofer et al., 2011; Spehn et al., 2000) have been shown be- The peer review history for this article is available at https://​w ww.​
fore. However, our high temporal resolution data show that plant webof​s cien​ce.​com/​api/​g atew​ay/​wos/​p eer-­​review/​10.​1111/​1365-­​
diversity effects on plant and soil processes change throughout 2745.​14470​.
the year. Root production is initiated during winter, right after the
end of the above-­ground growing season. With this, the positive DATA AVA I L A B I L I T Y S TAT E M E N T
plant diversity effects on above-­ground processes may result from Data are available from the Jexis database at https://​doi.​org/​10.​
earlier plant diversity effects on the root system operating over 25829/​​C3BY-­​C712 (Bonato Asato et al., 2024).
winter. Unravelling the patterns of above-­ground–below-­ground
phenological synchrony offers a significant promise to advance un- ORCID
derexplored areas of plant and soil ecology by adding an essential Ana E. Bonato Asato https://orcid.org/0000-0002-6093-0483
layer to understanding above-­ground–below-­ground interactions Anne Ebeling https://orcid.org/0000-0002-3221-4017
 |

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BONATO ASATO et al. 11

Eisenhauer, N., Beßler, H., Engels, C., Gleixner, G., Habekost, M., Milcu,
REFERENCES A., Partsch, S. W., Sabais, A. C., Scherber, C., Steinbeiss, S., Weigelt,
Abramoff, R. Z., & Finzi, A. C. (2015). Are above-­and below-­ground phe- A., Weisser, W. W., & Scheu, S. (2010). Plant diversity effects on
nology in sync? New Phytologist, 205(3), 1054–1061. https://​doi.​ soil microorganisms support the singular hypothesis. Ecology, 91(2),
org/​10.​1111/​nph.​13111​ 485–496. https://​doi.​org/​10.​1890/​0 8-­​2338.​1
Albert, L. P., Restrepo-­Coupe, N., Smith, M. N., Wu, J., Chavana-­Bryant, Eisenhauer, N., Herrmann, S., Hines, J., Buscot, F., Siebert, J., & Thakur, M. P.
C., Prohaska, N., Taylor, T. C., Martins, G. A., Ciais, P., Mao, J., Arain, (2018). The dark side of animal phenology. Trends in Ecology & Evolution,
M. A., Li, W., Shi, X., Ricciuto, D. M., Huxman, T. E., McMahon, S. M., 33(12), 898–901. https://​doi.​org/​10.​1016/j.​tree.​2018.​09.​010
& Saleska, S. R. (2019). Cryptic phenology in plants: Case studies, Eisenhauer, N., Wirsch, D., Cesarz, S., Craven, D., Dietrich, P., Friese, J.,
implications, and recommendations. Global Change Biology, 25(11), Helm, J., Hines, J., Schellenberg, M., Scherreiks, P., Schwarz, B.,
3591–3608. https://​doi.​org/​10.​1111/​gcb.​14759​ Uhe, C., Wagner, K., & Steinauer, K. (2014). Organic textile dye im-
Bardgett, R. D., & van der Putten, W. H. (2014). Belowground biodiver- proves the visual assessment of the bait-­lamina test. Applied Soil
sity and ecosystem functioning. Nature, 55, 505–511. https://​doi.​ Ecology, 82, 78–81. https://​doi.​org/​10.​1016/j.​apsoil.​2014.​05.​0 08
org/​10.​1038/​natur​e13855 Gottschall, F., Cesarz, S., Auge, H., Kovach, K. R., Mori, A., Nock, C. A., &
Birkhofer, K., Diekötter, T., Boch, S., Fischer, M., Müller, J., Socher, S., & Eisenhauer, N. (2022). Spatiotemporal dynamics of abiotic and biotic
Wolters, V. (2011). Soil fauna feeding activity in temperate grass- properties explain biodiversity–ecosystem-­functioning relationships.
land soils increases with legume and grass species richness. Soil Ecological Monographs, 92, 78–81. https://​doi.​org/​10.​1002/​ecm.​1490
Biology and Biochemistry, 43(10), 2200–2207. https://​doi.​org/​10.​ Grace, J. (2006). Structural equation modeling and natural systems.
1016/j.​soilb​io.​2011.​07.​0 08 Cambridge University Press. https://​doi.​org/​10.​1017/​CBO97​
Blume-­Werry, G., Wilson, S. D., Kreyling, J., & Milbau, A. (2016). The 80511​617799
hidden season: Growing season is 50% longer below than above Guerrero-­Ramírez, N. R., Craven, D., Reich, P. B., Ewel, J. J., Isbell, F.,
ground along an arctic elevation gradient. New Phytologist, 209(3), Koricheva, J., Parrotta, J. A., Auge, H., Erickson, H. E., Forrester, D. I.,
978–986. https://​doi.​org/​10.​1111/​nph.​13655​ Hector, A., Joshi, J., Montagnini, F., Palmborg, C., Piotto, D., Potvin,
Bonato Asato, A. E., Ebeling, A., El-­Madany, T., & Eisenhauer, N. (2024). C., Roscher, C., Van Ruijven, J., Tilman, D., … Eisenhauer, N. (2017).
Aboveground and belowground phenology in the Jena Experiment in Diversity-­dependent temporal divergence of ecosystem functioning
2021 [dataset]. Jena Experiment Information System. https://​doi.​ in experimental ecosystems. Nature Ecology & Evolution, 1(11), 1639–
org/​10.​25829/​​C3BY-­​C712 1642. https://​doi.​org/​10.​1038/​s4155​9-­​017-­​0325-­​1
Bonato Asato, A. E., Wirth, C., Eisenhauer, N., & Hines, J. (2023). On the Guimarães-­Steinicke, C., Weigelt, A., Ebeling, A., Eisenhauer, N., Duque-­
phenology of soil organisms: Current knowledge and future steps. Lazo, J., Reu, B., Roscher, C., Schumacher, J., Wagg, C., & Wirth,
Ecology and Evolution, 13(4), e10022. https://​doi.​org/​10.​1002/​ece3.​ C. (2019). Terrestrial laser scanning reveals temporal changes in
10022​ biodiversity mechanisms driving grassland productivity. Advances
Cardinale, B. J., Duffy, J. E., Gonzalez, A., Hooper, D. U., Perrings, C., in Ecological Research, 61(September), 133–161. https://​doi.​org/​10.​
Venail, P., Narwani, A., Mace, G. M., Tilman, D., Wardle, D. A., 1016/​bs.​aecr.​2019.​06.​0 03
Kinzig, A. P., Daily, G. C., Loreau, M., Grace, J. B., Larigauderie, A., Harris, W. F., Kinerson, R. S., Jr., & Edwards, N. T. (1977). Comparison of
Srivastava, D. S., & Naeem, S. (2012). Biodiversity loss and its im- belowground biomass of natural deciduous forest and loblolly pine
pact on humanity. Nature, 486(7401), 59–67. https://​doi.​org/​10.​ plantations. Pedobiologia, 17, 369–381.
1038/​natur​e11148 Hooper, D. U., Chapin, F. S., Ewel, J. J., Hector, A., Inchausti, P., Lavorel,
Cardinale, B. J., Gross, K., Fritschie, K., Flombaum, P., Fox, J. W., Rixen, S., Lawton, J. H., Lodge, D. M., Loreau, M., Naeem, S., Schmid, B.,
C., Van Ruijven, J., Reich, P. B., Scherer-­Lorenzen, M., & Wilsey, B. Setälä, H., Symstad, A. J., Vandermeer, J., & Wardle, D. A. (2005).
J. (2013). Biodiversity simultaneously enhances the production and Effects of biodiversity on ecosystem functioning: A consensus of
stability of community biomass, but the effects are independent. current knowledge. Ecological Monographs, 75(1), 3–35. https://​doi.​
Ecology, 94(8), 1697–1707. https://​doi.​org/​10.​1890/​12-­​1334.​1 org/​10.​1890/​0 4-­​0922
Cardinale, B. J., Matulich, K. L., Hooper, D. U., Byrnes, J. E., Duffy, E., Huang, Y., Stein, G., Kolle, O., Kübler, K., Schulze, E. D., Dong, H.,
Gamfeldt, L., Balvanera, P., O'Connor, M. I., & Gonzalez, A. (2011). Eichenberg, D., Gleixner, G., Hildebrandt, A., Lange, M., Roscher, C.,
The functional role of producer diversity in ecosystems. American Schielzeth, H., Schmid, B., Weigelt, A., Weisser, W. W., Shadaydeh,
Journal of Botany, 98(3), 572–592. https://​doi.​org/​10.​3732/​ajb.​ M., Denzler, J., Ebeling, A., & Eisenhauer, N. (2023). Plant diversity
1000364 stabilizes soil temperature. bioRxiv, 2023.03.13.532451. https://​
Cleland, E. E., Chiariello, N. R., Loarie, S. R., Mooney, H. A., & Field, C. doi.​org/​10.​1101/​2023.​03.​13.​532451
B. (2006). Diverse responses of phenology to global changes in Huo, C., Gu, J., Yu, L., Wang, P., & Cheng, W. (2022). Temporal dynam-
a grassland ecosystem. Proceedings of the National Academy of ics of fine root production, mortality and turnover deviate across
Sciences of the United States of America, 103(37), 13740–13744. branch orders in a larch stand. Oecologia, 199(3), 699–709. https://​
https://​doi.​org/​10.​1073/​pnas.​06008​15103​ doi.​org/​10.​1007/​s0044​2-­​022-­​05206​-­​8
Dietrich, P., Cesarz, S., Liu, T., Roscher, C., & Eisenhauer, N. (2021). Effects Iversen, C. M., Sloan, V. L., Sullivan, P. F., Euskirchen, E. S., Mcguire, A.
of plant species diversity on nematode community composition and D., Norby, R. J., Walker, A. P., Warren, J. M., & Wullschleger, S.
diversity in a long-­term biodiversity experiment. Oecologia, 197(2), D. (2015). The unseen iceberg: Plant roots in arctic tundra. New
297–311. https://​doi.​org/​10.​1007/​s0044​2-­​021-­​04956​-1
­​ Phytologist, 205(1), 34–58. https://​doi.​org/​10.​1111/​nph.​13003​
Ebeling, A., Klein, A. M., Schumacher, J., Weisser, W. W., & Tscharntke, Jackson, R. B., Canadell, J., Ehleringer, J. R., Mooney, H. A., Sala, O. E.,
T. (2008). How does plant richness affect pollinator richness and Schulze, E. D., & Mooney-­, H. A. (1996). A global analysis of root
temporal stability of flower visits? Oikos, 117, 1808–1815. https://​ distributions for terrestrial biomes a global analysis of root distribu-
doi.​org/​10.​1111/j.​1600-­​0706.​2008.​16819.​x tions for terrestrial biomes. Oecologia, 108(3), 389–411.
Ebeling, A., Pompe, S., Baade, J., Eisenhauer, N., Hillebrand, H., Proulx, Kuzyakov, Y., & Blagodatskaya, E. (2015). Microbial hotspots and hot mo-
R., Roscher, C., Schmid, B., Wirth, C., & Weisser, W. W. (2014). A ments in soil: Concept & review. Soil Biology and Biochemistry, 83,
trait-­based experimental approach to understand the mechanisms 184–199. https://​doi.​org/​10.​1016/j.​soilb​io.​2015.​01.​025
underlying biodiversity–ecosystem functioning relationships. Basic Lefcheck, J. (2015). piecewiseSEM: Piecewise structural equation model-
and Applied Ecology, 15(3), 229–240. https://​doi.​org/​10.​1016/j.​ ing in R for ecology, evolution, and systematics. Methods in Ecology
baae.​2014.​02.​0 03 and Evolution, 7(5), 573–579.
 |

13652745, 0, Downloaded from https://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2745.14470 by CochraneAustria, Wiley Online Library on [11/01/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
12 BONATO ASATO et al.

Liang, J., Crowther, T. W., Picard, N., Wiser, S., Zhou, M., Alberti, G., Schmid, B., Weisser, W. W., Wirth, C., De Kroon, H., Weigelt, A., &
Schulze, E.-­D., McGuire, A. D., Bozzato, F., Pretzsch, H., De-­Miguel, Liesje, M. J. (2014). Long-­term study of root biomass in a biodiver-
S., Paquette, A., Herault, B., Scherer-­Lorenzen, M., Barrett, C. B., sity experiment reveals shifts in diversity effects over time. Oikos,
Glick, H. B., Hengeveld, G. M., Nabuurs, G.-­J., Pfautsch, S., … Reich, 123(12), 1528–1536. https://​doi.​org/​10.​1111/​oik.​01502​
P. B. (2016). Positive biodiversity-­productivity relationship pre- Reich, P. B., Luo, Y., Bradford, J. B., Poorter, H., Perry, C. H., & Oleksyn,
dominant in global forests. Science, 354(6309), aaf8957. https://​doi.​ J. (2014). Temperature drives global patterns in forest biomass
org/​10.​1126/​scien​ce.​aaf8957 distribution in leaves, stems, and roots. Proceedings of the National
Loreau, M., & de Mazancourt, C. (2013). Biodiversity and ecosystem Academy of Sciences of the United States of America, 111(38), 13721–
stability: A synthesis of underlying mechanisms. Ecology Letters, 13726. https://​doi.​org/​10.​1073/​pnas.​12160​53111​
16(S1), 106–115. https://​doi.​org/​10.​1111/​ele.​12073​ Reich, P. B., Tilman, D., Isbell, F., Mueller, K., Hobbie, S. E., Flynn, D. F.
Loreau, M., & Hector, A. (2001). Partitioning selection and comple- B., & Eisenhauer, N. (2012). Impacts of biodiversity loss escalate
mentarity in biodiversity experiments. Nature, 412(6842), 72–76. through time as redundancy fades. Science, 336(6081), 589–592.
https://​doi.​org/​10.​1038/​35083573 https://​doi.​org/​10.​1126/​scien​ce.​1217909
Ma, Z., & Chen, H. Y. H. (2016). Effects of species diversity on fine root Richardson, A. D., Hollinger, D. Y., Aber, J. D., Ollinger, S. V., & Braswell,
productivity in diverse ecosystems: A global meta-­analysis. Global B. H. (2007). Environmental variation is directly responsible for
Ecology and Biogeography, 25(11), 1387–1396. https://​doi.​org/​10.​ short-­but not long-­term variation in forest-­atmosphere carbon ex-
1111/​geb.​12488​ change. Global Change Biology, 13(4), 788–803. https://​doi.​org/​10.​
McCormack, M. L., Adams, T. S., Smithwick, E. A. H., & Eissenstat, D. 1111/j.​1365-­​2486.​2007.​01330.​x
M. (2014). Variability in root production, phenology, and turnover Roscher, C., Schumacher, J., Baade, J., Wilcke, W., Gleixner, G., Weisser,
rate among 12 temperate tree species. Ecology, 95(8), 2224–2235. W. W., Schmid, B., & Schulze, E.-­D. (2004). The role of biodiversity
https://​doi.​org/​10.​1890/​13-­​1942.​1 for element cycling and trophic interactions: An experimental ap-
Mommer, L., Padilla, F. M., Smit-­Tiekstra, A., & Berendse, F. (2015). proach in a grassland community. Basic and Applied Ecology, 5(2),
Diversity effects on root length production and loss in an exper- 107–121. https://​doi.​org/​10.​1078/​1439-­​1791-­​00216​
imental grassland community. Functional Ecology, 29(12), 1560– Rudolf, V. H. W. (2019). The role of seasonal timing and phenological
1568. https://​doi.​org/​10.​1111/​1365-­​2435.​12466​ shifts for species coexistence. Ecology Letters, 22, 1324–1338.
Mori, A. S., Osono, T., Cornelissen, J. H. C., Craine, J., & Uchida, M. (2017). https://​doi.​org/​10.​1111/​ele.​13277​
Biodiversity–ecosystem function relationships change through pri- Schiefer, F., Schmidtlein, S., & Kattenborn, T. (2021). The retrieval of plant
mary succession. Oikos, 126(11), 1637–1649. https://​doi.​org/​10.​ functional traits from canopy spectra through RTM-­inversions and
1111/​oik.​0 4345​ statistical models are both critically affected by plant phenology.
Motohka, T., Nasahara, K. N., Oguma, H., & Tsuchida, S. (2010). Ecological Indicators, 121, 107062. https://​doi.​org/​10.​1016/j.​ecoli​nd.​
Applicability of green-­red vegetation index for remote sensing of 2020.​107062
vegetation phenology. Remote Sensing, 2(10), 2369–2387. https://​ Schuldt, A., Assmann, T., Brezzi, M., Buscot, F., Eichenberg, D., Gutknecht,
doi.​org/​10.​3390/​rs210​2369 J., Härdtle, W., He, J.-­S., Klein, A.-­M., Kühn, P., Liu, X., Ma, K.,
Muraoka, H., Noda, H. M., Nagai, S., Motohka, T., Saitoh, T. M., Nasahara, Niklaus, P. A., Pietsch, K. A., Purahong, W., Scherer-­Lorenzen,
K. N., & Saigusa, N. (2013). Spectral vegetation indices as the indi- M., Schmid, B., Scholten, T., Staab, M., … Bruelheide, H. (2018).
cator of canopy photosynthetic productivity in a deciduous broad- Biodiversity across trophic levels drives multifunctionality in highly
leaf forest. Journal of Plant Ecology, 6(5), 393–407. https://​doi.​org/​ diverse forests. Nature Communications, 9(1), 2989. https://​doi.​org/​
10.​1093/​jpe/​r ts037 10.​1038/​s 4146​7-­​018-­​05421​
Ochoa-­Hueso, R., Delgado-­Baquerizo, M., Risch, A. C., Schrama, M., Siebert, J., Sünnemann, M., Auge, H., Berger, S., Cesarz, S., Ciobanu, M.,
Morriën, E., Barmentlo, S. H., Geisen, S., Hannula, S. E., Resch, M. Guerrero-­Ramírez, N. R., & Eisenhauer, N. (2019). The effects of
C., Snoek, B. L., & van der Putten, W. H. (2021). Ecosystem cou- drought and nutrient addition on soil organisms vary across taxo-
pling: A unifying framework to understand the functioning and re- nomic groups, but are constant across seasons. Scientific Reports,
covery of ecosystems. One Earth, 4(7), 951–966. https://​doi.​org/​10.​ 9(1), 1–12. https://​doi.​org/​10.​1038/​s 4159​8-­​018-­​36777​-­​3
1016/j.​oneear.​2021.​06.​011 Siebert, J., Thakur, M. P., Reitz, T., Schädler, M., Schulz, E., Yin, R., Weigelt,
Oram, N. J., Ravenek, J. M., Barry, K. E., Weigelt, A., Chen, H., Gessler, A., A., & Eisenhauer, N. (2018). Extensive grassland-­use sustains high
Gockele, A., de Kroon, H., van der Paauw, J. W., Scherer-­Lorenzen, levels of soil biological activity, but does not alleviate detrimental
M., Smit-­Tiekstra, A., van Ruijven, J., & Mommer, L. (2018). Below-­ climate change effects. Advances in Ecological Research, 60, 25–58.
ground complementarity effects in a grassland biodiversity experi- https://​doi.​org/​10.​1016/​bs.​aecr.​2019.​02.​0 02
ment are related to deep-­rooting species. Journal of Ecology, 106(1), Sloan, V. L., Fletcher, B. J., & Phoenix, G. K. (2016). Contrasting syn-
265–277. https://​doi.​org/​10.​1111/​1365-­​2745.​12877​ chrony in root and leaf phenology across multiple sub-­Arctic plant
Poorter, H., Niklas, K. J., Reich, P. B., Oleksyn, J., Poot, P., & Mommer, communities. Journal of Ecology, 104(1), 239–248. https://​doi.​org/​
L. (2012). Biomass allocation to leaves, stems and roots: Meta-­ 10.​1111/​1365-­​2745.​12506​
analyses of interspecific variation and environmental control. New Soliveres, S., van der Plas, F., Manning, P., Prati, D., Gossner, M. M.,
Phytologist, 193(1), 30–50. https://​doi.​org/​10.​1111/j.​1469-­​8137.​ Renner, S. C., Alt, F., Arndt, H., Baumgartner, V., Binkenstein,
2011.​03952.​x J., Birkhofer, K., Blaser, S., Blüthgen, N., Boch, S., Böhm, S.,
Qu, Z., Lin, C., Zhao, H., Chen, T., Yao, X., Wang, X., Yang, Y., & Chen, Börschig, C., Buscot, F., Diekötter, T., Heinze, J., … Allan, E. (2016).
G. (2024). Above-­ and belowground phenology responses of sub- Biodiversity at multiple trophic levels is needed for ecosystem
tropical Chinese fir (Cunninghamia lanceolata) to soil warming, multifunctionality. Nature, 536, 456–459. https://​d oi.​org/​10.​
precipitation exclusion and their interaction. Science of the Total 1038/​natur​e19092
Environment, 933(May), 173147. https://​doi.​org/​10.​1016/j.​scito​ Spehn, E. M., Joshi, J., Schmid, B., Alphei, J., & Körner, C. (2000). Plant di-
tenv.​2024.​173147 versity effects on soil heterotrophic activity in experimental grass-
R Core Team. (2022). R: A language and environment for statistical comput- land ecosystems. Plant and Soil, 224(2), 217–230. https://​doi.​org/​
ing. R Foundation for Statistical Computing. https://​w ww.R-​proje​ 10.​1023/A:​10048​91807664
ct.​org/​ Staggemeier, V. G., Camargo, M. G. G., Diniz-­Filho, J. A. F., Freckleton,
Ravenek, J. M., Bessler, H., Engels, C., Scherer-­Lorenzen, M., Gessler, A., R., Jardim, L., & Morellato, L. P. C. (2018). The circular nature of
Gockele, A., de Luca, E., Temperton, V. M., Ebeling, A., Roscher, C., recurrent life cycle events: A test comparing tropical and temperate
 |

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BONATO ASATO et al. 13

phenology. Journal of Ecology, 108(2), 393–404. https://​doi.​org/​10.​ Wright, J., & Van Schaik, C. P. (1994). Light and the phenology of tropical
1111/​1365-­​2745.​13266​ trees. The American Naturalist, 143(1), 192–199.
Steinaker, D. F., & Wilson, S. D. (2008). Phenology of fine roots and Yang, B., Deng, L., & Lin, Y. (2023). From species norms to communal
leaves in forest and grassland. Journal of Ecology, 96(6), 1222–1229. metrics: Advancing plant community-­level historical phenology and
https://​doi.​org/​10.​1111/j.​1365-­​2745.​2008.​01439.​x phenological ecology. Plant Ecology, 224(11), 1023–1035. https://​
Steinaker, D. F., Wilson, S. D., & Peltzer, D. A. (2010). Asynchronicity doi.​org/​10.​1007/​s1125​8-­​023-­​01359​-­​5
in root and shoot phenology in grasses and woody plants. Global Yin, G., Verger, A., Descals, A., Filella, I., & Peñuelas, J. (2022). A broad-
Change Biology, 16(8), 2241–2251. https://​doi.​org/​10.​1111/j.​1365-­​ band green-­red vegetation index for monitoring Gross primary pro-
2486.​2009.​02065.​x duction phenology. Journal of Remote Sensing, 2022, 1–10. https://​
Steinbeiss, S., Temperton, V. M., & Gleixner, G. (2008). Mechanisms of doi.​org/​10.​3 4133/​​2022/​9764982
short-­term soil carbon storage in experimental grasslands. Soil Zhao, Q., Zhu, Z., Zeng, H., Myneni, R. B., Zhang, Y., Peñuelas, J., & Piao,
Biology and Biochemistry, 40(10), 2634–2642. https://​doi.​org/​10.​ S. (2022). Seasonal peak photosynthesis is hindered by late canopy
1016/j.​soilb​io.​2008.​07.​0 07 development in northern ecosystems. Nature Plants, 8(12), 1484–
Sünnemann, M., Siebert, J., Reitz, T., Schädler, M., Yin, R., & Eisenhauer, 1492. https://​doi.​org/​10.​1038/​s 4147​7-­​022-­​01278​-­​9
N. (2021). Combined effects of land-­use type and climate change Zuppinger-­Dingley, D., Schmid, B., Petermann, J. S., Yadav, V., De Deyn,
on soil microbial activity and invertebrate decomposer activity. G. B., & Flynn, D. F. B. (2014). Selection for niche differentia-
Agriculture, Ecosystems & Environment, 318(August 2020), 107490. tion in plant communities increases biodiversity effects. Nature,
https://​doi.​org/​10.​1016/j.​agee.​2021.​107490 515(7525), 108–111. https://​doi.​org/​10.​1038/​natur​e13869
Tamura, A., Oguma, H., Fujimoto, R., Kuribayashi, M., & Makita, N. Zuur, A. F., Ieno, E. N., Walker, N. J., Saveliev, A. A., & Smith, G. M. (2009).
(2022). Phenology of fine root and shoot using high frequency tem- Mixed effects models and extensions in ecology with R. Springer.
poral resolution images in a temperate larch forest. Rhizosphere,
22(March), 100541. https://​doi.​org/​10.​1016/j.​rhisph.​2022.​100541
van Moorsel, S. J., Hahl, T., Petchey, O. L., Ebeling, A., Eisenhauer, N., S U P P O R T I N G I N FO R M AT I O N
Schmid, B., & Wagg, C. (2021). Co-­occurrence history increases Additional supporting information can be found online in the
ecosystem stability and resilience in experimental plant communi- Supporting Information section at the end of this article.
ties. Ecology, 102(1), 1–14. https://​doi.​org/​10.​1002/​ecy.​3205
Figure S1: Conceptual diagram of relationships informing structural
Vogel, A., Manning, P., Cadotte, M. W., Cowles, J., Isbell, F., Jousset, A.
L. C., Kimmel, K., Meyer, S. T., Reich, P. B., Roscher, C., Scherer-­ equation models.
Lorenzen, M., Tilman, D., Weigelt, A., Wright, A. J., Eisenhauer, Figure S2: Daily variation of greenness (Green-­Red Vegetation
N., & Wagg, C. (2019). Lost in trait space: Species-­poor communi- Index, GRVI) in the growing season 2021.
ties are inflexible in properties that drive ecosystem functioning.
Figure S3: Spearman's correlations among response variables in
Advances in Ecological Research, 61, 91–131. https://​doi.​org/​10.​
spring (A), summer (B), and winter (C).
1016/​BS.​AECR.​2019.​06.​0 02
Wang, C., Tang, Y., & Chen, J. (2016). Plant phenological synchrony in- Table S1: Effects of plant species richness and plant functional group
creases under rapid within-­spring warming. Nature Publishing Group. richness on the total activities.
https://​doi.​org/​10.​1038/​srep2​5460 Table S2: Effects of plant species richness and plant functional group
Wang, X., Pan, J., Liu, F., Chen, H., Jiao, Z., Liu, S., & Wang, C. (2023).
richness on coupling in each season.
Seasonal asynchrony in above-­ and below-­ground phenology in a
temperate forest: Carbon allocation trade-­off and plant-­microbe
interactions. Plant and Soil, 492(1–2), 573–586. https://​doi.​org/​10.​
1007/​s1110​4-­​023-­​06200​-­​6
Weisser, W. W., Roscher, C., Meyer, S. T., Ebeling, A., Luo, G., Allan, How to cite this article: Bonato Asato, A. E., Guimarães-­
E., Beßler, H., Barnard, R. L., Buchmann, N., Buscot, F., Engels, Steinicke, C., Stein, G., Schreck, B., Kattenborn, T., Ebeling,
C., Fischer, C., Fischer, M., Gessler, A., Gleixner, G., Halle, S.,
A., Posch, S., Denzler, J., Büchner, T., Shadaydeh, M., Wirth,
Hildebrandt, A., Hillebrand, H., de Kroon, H., … Eisenhauer, N.
(2017). Biodiversity effects on ecosystem functioning in a 15-­year C., Eisenhauer, N., & Hines, J. (2025). Seasonal shifts in plant
grassland experiment: Patterns, mechanisms, and open questions. diversity effects on above-­ground–below-­ground
Basic and Applied Ecology, 23, 1–73. https://​doi.​org/​10.​1016/j.​baae.​ phenological synchrony. Journal of Ecology, 00, 1–13. https://
2017.​06.​0 02
doi.org/10.1111/1365-2745.14470
Wolf, A. A., Zavaleta, E. S., & Selmants, P. C. (2017). Flowering phenology
shifts in response to biodiversity loss. Proceedings of the National
Academy of Sciences of the United States of America, 114(13), 3463–
3468. https://​doi.​org/​10.​1073/​pnas.​16083​57114​