Microclimate modulation: An overlooked mechanism influencing the impact of plant diversity on ecosystem functioning

Changes in climate and biodiversity are widely recognized as primary global change drivers of ecosystem structure and functioning, also affecting ecosystem services provided to human populations. Increasing plant diversity not only enhances ecosystem functioning and stability but also mitigates climate change effects and buffers extreme weather conditions, yet the underlying mechanisms remain largely unclear. Recent studies have shown that plant diversity can mitigate climate change (e.g. reduce temperature fluctuations or drought through microclimatic effects) in different compartments of the focal ecosystem, which as such may contribute to the effect of plant diversity on ecosystem properties and functioning. However, these potential plant diversity‐induced microclimate effects are not sufficiently understood. Here, we explored the consequences of climate modulation through microclimate modification by plant diversity for ecosystem functioning as a potential mechanism contributing to the widely documented biodiversity–ecosystem functioning (BEF) relationships, using a combination of theoretical and simulation approaches. We focused on a diverse set of response variables at various levels of integration ranging from ecosystem‐level carbon exchange to soil enzyme activity, including population dynamics and the activity of specific organisms. Here, we demonstrated that a vegetation layer composed of many plant species has the potential to influence ecosystem functioning and stability through the modification of microclimatic conditions, thus mitigating the negative impacts of climate extremes on ecosystem functioning. Integrating microclimatic processes (e.g. temperature, humidity and light modulation) as a mechanism contributing to the BEF relationships is a promising avenue to improve our understanding of the effects of climate change on ecosystem functioning and to better predict future ecosystem structure, functioning and services. In addition, microclimate management and monitoring should be seen as a potential tool by practitioners to adapt ecosystems to climate change.


| INTRODUC TI ON
The profound impacts of changing climate and biodiversity on ecosystem functioning and stability are widely acknowledged (IPBES, 2019;Pörtner et al., 2021).These threats extend to the key ecosystem services that sustain human populations (IPCC, 2021;Pörtner et al., 2021), particularly as climatic extremes like heatwaves, droughts and floods become more frequent, pushing ecosystems toward critical thresholds and potential collapse (Duffy et al., 2021;MacDougall et al., 2013).
The intricate relationship between ecosystem functioning and climatic conditions holds on the climate dependency of the sum of biological processes that contribute to ecosystem functioning.Net ecosystem carbon exchange (NEE), for instance, depends on air temperature, radiation and soil water availability (Niu et al., 2012).
Similarly, organic matter recycling responds to changes in temperature and water availability (Joly et al., 2023;Xiao et al., 2014).
With changing climatic conditions, these processes move along a climate response curve that is rarely linear, and the net outcome on ecosystem properties and services becomes a focal point of concern.
The climatic conditions experienced (i.e.temperature, light availability, concentrations of greenhouse gasses and humidity) by organisms may deviate substantially from those measured by using conventional meteorological standards characterizing macroclimate under highly standardized conditions (Haesen et al., 2023;Lembrechts, 2023;Lembrechts et al., 2020).The climatic niche experienced by an organism is therefore defined by microclimatic conditions that can differ substantially from macroclimatic conditions, potentially altering the real shape of the species response curve against a given climatic parameter like temperature (Haesen et al., 2023).Unsurprisingly, incorporating microclimate data, rather than macroclimate data, into species distribution models has proven highly valuable for advancing our understanding of ecosystem properties (Kemppinen et al., 2023;Lembrechts, 2023;Stark & Fridley, 2022), as well as our ability to better predict the activity and survival of species (Colinet et al., 2015;Dingman et al., 2013).
The physical structure of ecosystems and their species composition, above all that of the vegetation compartment contributing to most of the biomass and controlling the key ecosystem processes like the fluxes of energy and matter, play a critical role in influencing differences between macro-and microclimate conditions (de Frenne et al., 2019(de Frenne et al., , 2021;;Gril et al., 2023;Milling et al., 2018).
Consequently, manipulating the species composition and canopy structure of a given ecosystem offers a promising strategy to modulate microclimate, and thus, the overall functioning of the focal ecosystem.Indeed, recent research highlighted the potential of plant diversity, and thus ecosystem structure, to influence microclimatic fluctuations (Huang et al., 2023;Ray et al., 2023;Schnabel et al., 2023;Zhang, 2022).This included the further reduction in temperature extremes experienced underneath a vegetation canopy that is composed of more species (Huang et al., 2023;Schnabel et al., 2023), and changes in sensible heat flux and evapotranspiration resulting in higher ecosystem CO 2 uptake (Milcu et al., 2016).
Higher plant diversity also promotes ecosystem functioning and stability by increasing and securing essential functions such as productivity and carbon storage (Beugnon et al., 2023;Huang et al., 2018;Liang et al., 2016Liang et al., , 2022;;Schnabel et al., 2019).However, the nexus between biodiversity, microclimate and ecosystem functioning remains relatively unexplored, also lacking a unified framework.
The aim of this study is to better understand the biodiversitymicroclimate-ecosystem functioning relationships by exploring the cascading effects of biodiversity-induced changes on microclimatic processes and ecosystem functioning.While climate encompasses various environmental factors, such as temperature, air pressure, humidity, precipitation, solar radiation, cloudiness and wind, in this study, we specifically concentrate on the effects of temperature.
To address this, we take a fourfold approach (Figure 1).First, we emphasize the climate dependency of ecosystem functions across organizational levels.Second, we examine the evidence supporting the effect of plant diversity on microclimate.Third, through the implementation of a common simulation framework, we quantify the potential consequences of increased plant diversity for temperature-dependent ecosystem functions.Finally, we discuss the implications of our findings for the general understanding of the biodiversity-ecosystem functioning (BEF) relationship and their practical applications.

| CLIMATE CONTE X T DEPENDEN CIE S OF PRO CE SS R ATE S ACROSS ORG ANIZ ATIONAL LE VEL S
Formulated by Brown et al. (2004), 'the metabolic theory of ecology' proposes a temperature dependency of biological processes across organizational levels, from specific processes at the molecular scale to integrated processes at the ecosystem scale.Beyond its primary emphasis on temperature, this theory proposes that similar causal de-France; Ministère de l'Enseignement Supérieur et de la Recherche; European Fund for Regional Economic Development should be seen as a potential tool by practitioners to adapt ecosystems to climate change.

K E Y W O R D S
biodiversity-ecosystem functioning, climate change, ecosystem services, microclimate, plant species richness, thermal tolerance relationships exist for other climatic parameters, such as humidity and light, all influencing the performance of organisms and ultimately their contribution to ecosystem functioning (Brown et al., 2004).
At the molecular level, temperature acts as a strong driver of enzymatic activity due to the strong dependence of the reaction rate on temperature.The temperature dependence of enzyme catalytic reactions shows a reaction-specific optimum and an upper-temperature limit that is ultimately reached when thermal inactivation of enzymes occurs (Alster et al., 2016;Peterson et al., 2007).This temperature-enzyme activity relationship has historically been modelled with the Arrhenius law, although recently proposed models better represent the experimentally observed bell-shaped response curve (Alster et al., 2020).Concurrently, other climatic variables also impact enzyme functioning, for instance, changes in soil moisture alter substrate diffusion and the likelihood of substrate-enzyme encounters and the production of microbial extracellular enzymes, ultimately leading to changes in enzyme activity, as observed for the extracellular beta-glucosidase enzyme, a key player in soil organic carbon decomposition (Puissant et al., 2015(Puissant et al., , 2018;;Wallenstein & Weintraub, 2008;Zhang et al., 2011).Changes in microclimate can also affect substrate concentration, such as an increase in CO 2 concentrations that enhance the activity of the photosynthetic enzyme Rubisco (Galmés et al., 2019).
The climate, or more generally the environmental control of enzymatic kinetics, affects individual performance and the functions the organisms have in the ecological context via the organism's metabolic activities.This holds particular significance for species unable to regulate their body temperature, such as ectotherms.For instance, insects, being ectotherms, demonstrate an increase in activity with rising temperatures, reaching an optimal point before experiencing a drastic decline (Colinet et al., 2015;Khelifa et al., 2019;Sinclair et al., 2016;Terlau et al., 2023).Although primarily assessed at the microbial community scale, the temperature response of microbes plays a critical role in nutrient recycling and ecosystem functioning (Bradford et al., 2019;Dacal et al., 2019).The temperature dependency of microbes is a subject of intense debate, representing a major uncertainty in the projections of carbon cycle models in response to climate warming (Duffy et al., 2021;García-Palacios et al., 2021).Consequently, microclimate buffering could emerge as a critical factor in regulating the rate of soil carbon decomposition.Such control over specific activities of organisms is also exerted by other environmental factors such as light availability.When light penetrates a plant canopy, it is increasingly absorbed following the Beer-Lambert law (Larcher, 2003) affecting, for example, leaf functional traits and microclimatic conditions along the vertical profile (Govaert et al., 2023;Messier et al., 2017;Niinemets & Valladares, 2004), growth of understorey plants, as well as their composition and cover in the understorey (Messier et al., 1998;Tinya & Ódor, 2016).

Climate responses of individual organisms ultimately transition
to the community level by impacting their survival (Allen et al., 2010;Dingman et al., 2013;McDowell et al., 2022), phenology (Cleland et al., 2007;Møller et al., 2023) and productivity (Huang et al., 2019), which all determine competitive interactions and community composition.Through its influence on individuals, biotic interactions and communities, climate effects also transcend trophic levels and food web structure and dynamics (Sentis et al., 2014).
Collectively, these responses to climate variables across various organizational levels from single biochemical reactions to organisms, communities and food web structure may have cascading effects on ecosystem-level processes such as photosynthesis (Crous et al., 2022;Kirschbaum, 2004), evapotranspiration (Kirschbaum, 2004), organic matter recycling (Bradford et al., 2017;Xiao et al., 2014) and soil respiration (Jones et al., 2006).A notable example is the temperature dependence of the net ecosystem CO 2 exchange (NEE) that can vary between net C influx at average temperatures to net C efflux at extreme temperatures (Figure 2; Niu et al., 2012;Yuan et al., 2011).Other climate-related variables such as atmospheric CO 2 concentrations and water availability additionally or interactively affect NEE (Milcu et al., 2014).Similarly, net ecosystem nitrous oxide (N 2 O) emissions are contingent upon soil moisture and temperature (Schindlbacher et al., 2004).It is particularly important to better understand all these ecosystem-level responses to climate variables with ongoing climate change (IPBES, 2019;IPCC, 2021;Pörtner et al., 2021), especially since the responses across organizational levels span different time scales, ranging from immediate reactions to long-lasting effects.

| THE CLIMATE-MODULATING IMPACT OF PLANT DIVERSITY
The dominating contribution of primary producers in terms of biomass in terrestrial ecosystems confers to plants a particularly with ongoing succession is a well-documented example of how plants reshape environmental properties (Northup et al., 1995;Rahmonov et al., 2021;Wardle & Ghani, 1995).Specific plant species can alter environmental conditions for associated species through facilitation by 'nursing' and can indirectly modify biodiversity, then making it less exposed to climate extremes (Bulleri et al., 2016) and sometimes improving access to limited resources such as water (hydraulic lift, Caldwell et al., 1998) or nitrogen for Nfixing plants.Due to their large size, trees often have a particularly strong influence on both their proximal and distal environments by modifying biogeochemical cycles and providing food and shelter for many other species in their environment.Coniferous trees, for example, typically reduce litter and soil pH in forests where they dominate with far-ranging consequences for soil microbial and fauna communities, nutrient availability and associated plant species in the understorey (Burgess-Conforti et al., 2019;Phillips et al., 2013;Wardle & Ghani, 1995).The tree canopies of forests as a whole have been shown to substantially alter microclimatic conditions underneath (de Frenne et al., 2019), generally providing climatically more favourable conditions to understorey plants by alleviating climate extremes (Bertrand et al., 2011;de Frenne et al., 2021).Forest tree canopies affect microclimate via different mechanisms, such as shading, reducing air movement that diminishes mixing between air layers and active cooling by alive foliage through transpiration (Geiger et al., 1995;Zellweger et al., 2020).
Increasing canopy thickness and structural complexity consequently enhances the strength of the buffering capacity of the upper canopy layer (Ehbrecht et al., 2019;Gril et al., 2023).
Plant diversity was found to foster canopy thickness and complexity (Peng et al., 2017;Perles-Garcia et al., 2021;Williams et al., 2017), potentially also enhancing the buffering capacity of vegetation cover on microclimatic processes in the understorey.Results from experiments manipulating plant diversity in the field (BEF experiments) indicate that microclimatic conditions are even more stable with increasing plant species richness (Huang et al., 2023;Schnabel et al., 2023;Zhang, 2022) and that microclimate interacts with stand complexity in promoting forest productivity (Ray et al., 2023).Similar effects by more diverse plant communities on microclimatic conditions via thicker canopies were also observed in grasslands (Huang et al., 2023), yet empirical evidence in grassland ecosystems remains limited, particularly F I G U R E 2 Climate dependencies of various processes across different levels of organization, here using temperature dependency as an example: (1) Net ecosystem CO 2 exchange (NEE, Niu et al., 2012), (2) soil respiration (Jones et al., 2006), (3) tree seedlings survival (Dingman et al., 2013), (4) insect activity (Colinet et al., 2015) and (5) Rubisco activity (Galmés et al., 2019).The present, still limited, evidence suggests that higher plant diversity potentially modifies ecosystem functioning through climate-dependent ecosystem properties.Among the possible (and non-exclusive) mechanistic hypotheses proposed to explain the effect of plant diversity on ecosystem properties (e.g.hydraulic lift, architecture complementarity leading to canopy packing), microclimatic processes appear as a promising explanation allowing a direct link with physiology-based mechanisms.However, the effects of plant diversity on microclimate dynamics depend on seasons (Huang et al., 2023;Schnabel et al., 2023;Zhang, 2022), owing to structural mediation in winter (e.g.branch structure in forests) and leaf mediation in summer (Schnabel et al., 2023).Consequently, the impact of plant diversity on climate-dependent ecosystem functions is anticipated to be dynamic over time.It still could accumulate over larger time scales, because increase in productivity with species-rich communities is expected to increase with time (Dietrich et al., 2023;Huang et al., 2018;Perles-Garcia et al., 2021;Weisser et al., 2017).

| CON S EQUEN CE S FOR ECOSYS TEM FUN C TIONING AND S ERVICE S
Plant diversity effects on microclimate have the potential to influence ecosystem functioning and services through climate-dependent processes across various levels of organization (Figure 2).However, the extent of these effects remains largely unexplored, partly because they are not easy to experimentally tease apart microclimatic processes from other mechanisms of diversity effects.Therefore, it is unclear how diversity-driven climate modulation cascades through different levels of organization and how large the resulting consequences on ecosystem functioning may be.For instance, some studies on litter decomposition indicate a positive influence of tree species richness on leaf litter decomposition through microclimate modulation (Gottschall et al., 2019;Joly et al., 2017;Makkonen et al., 2013).However, the quantification of these causal relationships remains limited and the resulting consequences on ecosystem carbon and nutrient cycling are untested.
Here, we chose a different approach to experimental testing in an attempt to move forward with this critically important question.
We employed a simple simulation approach to assess the effects of species diversity on ecosystem functioning via microclimate, using temperature as an example for a microclimate variable and soil respiration as a temperature-dependent ecosystem process (Figure 3a, for details on the workflow see Data S1).Initially, we simulated soil temperature for grasslands with various plant species richness scenarios (bare soil, monoculture and 60-species mixtures), using air temperature records from central Germany (2017( -2019, ERA5 , ERA5 hourly data, Copernicus Climate Change Service, 2019) and the soil temperature-grassland species richness relationship from Huang et al. (2023).Subsequently, based on the soil respiration-temperature relationship from Jones et al. (2006), we predicted soil respiration for each scenario and calculated cumulative soil respiration (Figure 3b).Our simulation illustrated the potential of plant species diversity to modulate soil respiration by modifying microclimate.We demonstrated that diversity primarily affects soil respiration during warm hours, days and months, rapidly increasing the divergence between scenarios during these periods.Despite the fact that the magnitude of this climate-mediated effect of diversity on soil respiration varied among different time periods, it accumulated over time with an increasing difference in total respiration between the low and high plant diversity scenarios (Figure 3b).The simulations that illustrate how soil respiration depends on microclimate highlight the possible effects of climate modulation on ecosystem functioning.However, these simulations oversimplify the relationship by considering only temperature as the factor affecting soil respiration's dependence on microclimate.In reality, the relationship between soil respiration and microclimate is multifaceted and is modulated by additional factors such as soil humidity (Wood et al., 2013), nutrient availability and CO 2 diffusivity (Davidson et al., 2012;Skopp et al., 1990).To accurately predict long-term trends in soil respiration, it is imperative to consider these various aspects, their interactions and the direct effects of plant diversity on soil quality (Weisser et al., 2017).
These simulations underscore the potential of plant diversity to influence ecosystem processes through microclimate modulation, particularly when considering cumulative processes such as carbon fluxes that occur not only during soil respiration but also during organic matter decomposition or through biomass production, which can greatly accentuate overall effects beyond the slight differences measured at specific points in time.Given that numerous ecosystem functions across various organizational levels are contingent on climatic conditions, the vegetation-microclimate-ecosystem functioning nexus may play a pivotal role in overall ecosystem functioning.This simulation exercise emphasizes the necessity for empirically measuring the vegetation-microclimate-ecosystem functioning nexus to better understand the consequences at the ecosystem level.A way forward to tackle the issue of confounding mechanisms influencing ecosystem functions at a yearly extent could then be to increase the temporal resolution of sampling allowing to identify potential mechanisms and their temporality.

| PER S PEC TIVE FOR RE S E ARCH AND MANAG EMENT
Microclimate is an ecologically important environmental parameter that regulates ecosystem functioning to an important degree (e.g.Gottschall et al., 2019;Joly et al., 2017;Kemppinen et al., 2023), which can be co-determined by plant diversity and canopy structure (Huang et al., 2023;Schnabel et al., 2023;Zhang, 2022).Thus, integrating microclimate into the BEF relationship seems critically important and promises an enhanced understanding of the mechanisms underlying BEF relationships, particularly given the multitude of climate-dependent processes at different organizational levels ultimately determining ecosystem functions.The mediation of microclimate in the relationship between biodiversity and ecosystem functioning, coupled with its direct correlation to macroclimate fluctuations, could offer an explanation for the observed climate and context dependency in the strength of the BEF relationship (Cesarz et al., 2022;Liu et al., 2022;Spohn et al., 2023).Incorporating microclimate mediation into the BEF framework may advance our understanding of ecosystem functioning by providing mechanistic insights.
Microclimate spans a continuum from the top of the canopy to the soil layers, with specific microclimates affecting distinct processes.For example, the soil microbial community will respond to variations in the topsoil microclimate rather than to variations in the microclimate within the plant canopy (Kemppinen et al., 2023).
Consequently, microclimate variations will have to be quantified in space and time simultaneously with the assessment of how plant diversity affects microclimate dynamics in space and time.
Additionally, there is a growing need to quantify the climate responses of ecosystem functions over time, particularly when considering functions that integrate temporal dynamics in microclimate effects.The impact of plant diversity on microclimate acts primarily through modifications of canopy parameters such as thickness and structural complexity (Ehbrecht et al., 2019;Gril et al., 2023).
It is therefore critical to include stand age and structure beyond the diversity of species composing the canopy for a detailed understanding of plant diversity control over microclimate (Au et al., 2022).
Recognizing the importance of plant diversity in promoting ecosystem functioning and services, as well as their stability, has been emphasized to ecosystem managers (Messier et al., 2021), particularly in the context of climate change (Beugnon et al., 2021;Pires et al., 2018).Understanding the biodiversity-microclimate-ecosystem functioning nexus offers new perspectives.
Microclimate monitoring becomes a valuable non-invasive tool for assessing climate change mitigation, allowing stakeholders to quantify the effects of plant diversity, both taxonomic and structural diversity, on ecosystem functioning (Figure 4).Microclimate monitoring, being low-cost, effortless and non-invasive (Kemppinen et al., 2023), emerges as an important approach for tracking ecosystem functioning, given its influence on numerous functions across all organizational levels.

| CON CLUS IONS
We showed that the influence of plant diversity on microclimate is promising for advancing our understanding of the relationship be-

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I G U R E 1 Conceptual framework linking the nexus between plant diversity, microclimate and ecosystem functions.Examples of pairwise relationships from the scientific literature: (1) Bertrand et al. (2011) and Lembrechts (2023), (2) Pörtner et al. (2021), (3) Beugnon et al. (2021) and Messier et al. (2021), (4) Huang et al. (2023), Schnabel et al. (2023) and Zhang (2022), (5) and (6) Gottschall et al. (2019), Huang et al. (2019) and Joly et al. (2017).important role in structuring and engineering their proximal environment.The soil development during successional dynamics with a continuous modification of soil properties resulting from plant colonization in early successional stages and the accumulation of organic matter and nitrogen (through symbiotic N fixation) regarding comprehensive global quantification across various ecoregions.Further, in situ measurements are necessary to fully understand the scope of this relationship on a global scale, especially, long-term measurements are essential to quantify the potential mitigation of climatic extremes within the context of climate change.Such diversity-driven canopy feedbacks may be particularly important in mitigating effects on soil temperature that have recently been shown to be more frequently affected by temperature extremes than air temperature (García-García et al., 2023) at a global extent.

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I G U R E 3 Climate-mediated biodiversity-ecosystem functioning (BEF) relationships: (a) simulation framework and (b) outputs.(a) Simulation framework tested on soil temperature mediation: microclimate simulations using air temperature records and plant species diversity effects on soil temperature from Huang et al. (2023), and prediction of soil respiration using Jones et al. (2006) soil respiration temperature dependency (holding all other parameters to a constant value).(b) Simulation outputs: soil respiration and cumulative respiration over time (Data S1).
tween biodiversity and ecosystem functioning, especially considering the climate dependency of ecosystem functions and services.Therefore, future research should strengthen our understanding of biodiversity-microclimate-ecosystem functioning by developing and testing these connections theoretically as much as experimentally.Consequently, the manipulation of microclimate, through plant diversity, both in terms of taxonomic and structural diversity, presents an opportunity to effectively manage ecosystems functioning in the face of climate change.AUTH O R CO NTR I B UTI O N S Rémy Beugnon: Conceptualization; data curation; formal analysis; methodology; validation; visualization; writing -original draft.Nolwenn Le Guyader: Conceptualization; data curation; formal analysis; visualization; writing -review and editing.Alexandru Milcu: Conceptualization; validation; writing -review and editing.Jonathan Lenoir: Conceptualization; validation; writing -review and editing.Jérémy Puissant: Conceptualization; validation; writing -review and editing.Xavier Morin: Conceptualization; validation; writing -review and editing.Stephan Hättenschwiler: Conceptualization; validation; writing -review and editing.ACK N OWLED G M ENTS This research was funded by the Saxon State Ministry for Science, Culture and Tourism (SMWK)-3-7304/35/6-2021/48880.We gratefully acknowledge the support by the German Centre for Integrative Biodiversity Research (iDiv) funded by the German Research Foundation (DFG-FZT 118, 202548816).JL acknowledges funding from the Agence Nationale de la Recherche (ANR), under the framework of the collaborative research program funding scheme (Grant No. ANR-21-CE32-0012-03: MaCCMic project) and the young researcher funding scheme (ANR-19-CE32-0005-01: IMPRINT project).JL also acknowledges the Région Hauts-de-France, the Ministère de l'Enseignement Supérieur et de la Recherche and the European Fund for Regional Economic Development for their financial support to the CPER ECRIN program.JP was supported by funding from the European Union's Horizon 2020 research and innovation program under the Marie Sklodowska-Curie grant agreement No 892654.Open Access funding enabled and organized by the Projekt DEAL.

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Perspectives and consequences for biodiversity-ecosystem functioning research and ecosystem management.