Discussion
In our meta-food-web approach, we show that spatial processes related to
plant resource exploitation and animal movement strongly affect plant
diversity-productivity relationships. Positive relationships arise only
when plant resource access overlaps spatially (‘spatial resource
overlap’) at the cost of exploitative competition. Herbivore movement
introduces apparent competition between plants, which can reduce plant
productivity in diverse communities, yielding negative
diversity-productivity relationships. However, a realistic body mass
scaling of animal home range sizes moves apparent competition motifs up
the food chain. The reduced plant competition together with the spatial
integration of sub-food webs through the movement of top predators lead
to the most positive effects of plant diversity on productivity,
suggesting animal movement as a crucial driver of plant
diversity-productivity relationships.
Plant-resource
interactions
A spatial resource overlap between neighbouring plants has two important
implications for plants. While it allows each plant to access a larger
share of resources available in the ecosystem, it also forces them to
engage in exploitative competition. In diverse plant communities,
however, plants will differ in their resource requirements and thus in
their competitive ability. Different resource requirements are usually
accompanied by low competition (Tilman et al. 1997) and suggest a
stoichiometric complementarity between neighbouring plants (Gonzálezet al. 2017) that is likely to have positive impacts on plant
productivity. We find this mirrored in our results, where, in the
absence of animals, even a weak spatial resource overlap is enough to
maximize productivity in diverse plant communities of species with
different resource requirements. Accessing small amounts of otherwise
inaccessible resources can therefore already suffice to lift resource
limitations, leading to positive diversity-productivity relationships
due to a stoichiometric complementarity.
Differences in competitive abilities across pairs of plant species are
rarely associated with such performance enhancements. Instead, they
should lead to local extinctions of the weaker competitor (Tilman 1982),
which we find mirrored in a loss of plants when the spatial resource
overlap increases. Surprisingly, this does not come at the cost of a
reduced productivity. Instead, plants with a competitive advantage,
either due to a higher efficiency in resource acquisition (i.e.
exploitative competition) or favourable multi-trophic interactions (i.e.
apparent competition), can maximize their resource uptake and thereby
increase their biomass (Wang & Brose 2018). This has the positive side
effect of reducing energy requirements for metabolic processes relative
to their mass (Enquist et al. 1998), contributing to a more
energy efficient plant community. Our findings suggest that this is
enough to counterbalance the loss of plants as well as the associated
diversity loss.
When plants have a spatial resource overlap, diversified resource
requirements create complementarity whereas selection (sensuLoreau 2000) due to competitive differences shift the community to be
more energy efficient (Wang & Brose 2018), leading to an optimized
resource uptake in both cases. Consistent with our hypothesis (H1), this
increases productivity and leads to positive diversity-productivity
relationships. The consistency of those relationships paired with the
shifts in plant community composition additionally implies that the
contribution of complementarity and selection processes to maximizing
productivity varies depending on the strength of the competitive
interaction between plants.
Plant-animal interactions
When embedded in complex food webs, the response of plant productivity
to varying plant biodiversity is rooted in food-web topology. As the
number of plant species increases, there is an increasing number of
apparent competition motifs in which two plant species are coupled by a
shared herbivorous consumer population. In this motif, the plant species
with a higher resource acquisition efficiency achieves a higher biomass
density, leading to higher herbivore densities, which in turn has
negative top-down effects on other plant species with lower resource
acquisition efficiencies (Holt 1977). Accordingly, our simulations of
spatially non-nested food webs have shown that as plant species richness
increases, plant productivity decreases, which is, consistent with our
hypothesis (H2), reflected in negative diversity-productivity
relationships. However, when compared to scenarios without animals, the
added apparent competition does not foster competitive exclusion.
Instead, it seems to buffer some of the negative effects of an increased
exploitative competition (i.e. increased spatial resource overlap) as
more plant individuals and species are able to coexist when embedded in
a food web (see also Brose 2008; Albert et al. 2022).
While the high levels of maintained plant individuals and species are
similar between spatially nested and non-nested food webs, the effects
of apparent competition on productivity are not. Specifically, our
simulations of spatial non-nested food webs assume a well-mixed system
without any differences in local biomass densities of animal species.
Ignoring such differences results in herbivore populations that can feed
simultaneously on different plants regardless of their location. In
nature, however, animal communities have a complex spatial organization
(e.g. Gonçalves-Souza et al. 2015). While almost all animal
species move between resource patches, larger species travel longer
distances and have larger habitats (Tucker et al. 2014;
Tamburello et al. 2015; Hirt et al. 2021). As a result,
meta-food webs have a structure in which smaller species from local food
webs are spatially integrated within the home ranges of larger species.
Apparent competition between plants in spatially nested food webs is
therefore spatially constrained depending on the home range size of the
herbivore. In addition, an increased amount of apparent competition
motifs between sub-populations of herbivores reduces their top-down
control on plants. Hence, instead of the negative plant
diversity-productivity relationships found in spatially non-nested food
webs, relationships in spatially nested food webs are the most positive,
peaking at levels similar to plant communities without animals.
Apart from the positive effects of an altered spatial topology (i.e.
effects of apparent competition) on diversity-productivity relationships
in spatially nested food webs, the spatial integration of sub-food webs
has additional dynamic benefits. In particular, biomass overshooting and
unstable dynamics leading to local extinctions are buffered in spatially
nested food webs by large top predators that stabilize biomass minima of
populations in the local food webs away from critically low values
(McCann et al. 2005). This is reflected in the relatively stable
plant diversity of spatially nested food webs despite differences in the
spatial resource overlap of plants. Consistent with our hypothesis (H3),
we thus conclude that a spatial integration of sub-food webs associated
with spatially nested food webs has positive effects on plant
diversity-productivity relationships. The clear dynamic and topological
differences between spatially nested and non-nested food webs, which may
be negligible for biodiversity maintenance, can therefore have strong
implications for plant productivity, leading to vastly different plant
diversity-productivity relationships.
BEF: from multi-trophic to meta-food
webs
BEF research has evolved from focusing on single functional groups (e.g.
plant communities) to the complex multi-trophic structure of natural
communities (e.g. Schuldt et al. 2019; Barnes et al. 2020;
Albert et al. 2022). This development has shown that
multi-trophic interactions can facilitate plant coexistence and thereby
increase productivity. In our study, we extended this development by
applying meta-ecosystem (i.e. plant-resource exploitation bridges
between local habitats) and meta-food web approaches (i.e.
spatially-explicit structure of the food webs). Some of our results on
the effects of multi-trophic interactions differ significantly from
previous conclusions. While prior studies reported generally positive
effects of multi-trophic interactions on plant coexistence and
diversity-productivity relationships (Thébault & Loreau 2003; Brose
2008; Albert et al. 2022), we found that under the assumption of
spatially segregated plants (i.e. each plant inhabits its own local
habitat) this is not necessarily the case. Spatially non-nested animal
communities paired with spatially segregated plants instead result in
negative relationships, which finds an explanation in the systematic
increase in apparent competition motifs. In contrast, the spatially
nested structure of animal communities yields strongly positive
diversity-productivity relationships due to the positive effects of an
apparent competition shift up the food chain (i.e. from between plants
to between herbivores) and the spatial integration of sub-food webs by
top predators.
By relaxing the classic assumption of well-mixed systems (e.g. Schneideret al. 2016; Albert et al. 2022), we gained accuracy in
the description of the processes that drive ecosystems and their
functioning. The assumption of a well-mixed system is also at the core
of BEF research, as it usually compares the functioning of entire
communities of varying diversity. While this helped to identify
complementarity mechanisms as the main driver of positive BEF
relationships, it remains difficult to identify their concrete causes
(Barry et al. 2019), which may be related to focusing on the
wrong spatial scale. Indeed, competition and the associated BEF
processes (i.e. complementarity and selection; Loreau 2000) act between
a few organisms and are thus spatially constrained. Our work
demonstrates that a multi-trophic investigation of spatially-explicit
plant-resource interactions additionally requires a spatially-explicit
consideration of the entire food web. Moreover, our simulations show
that the sign and strength of diversity-productivity relationships
depends on the joint effects of animal movement and spatial resource
overlap of plants. This renders the spatial organisation of
multi-trophic communities, which can vary across landscapes, an
important but often neglected aspect that can help to explain the
variation observed in empirical BEF relationships (Cardinale et
al. 2007). Overall, our findings on diversity-productivity
relationships clearly demonstrate the importance of spatial community
structure and animal movement in driving BEF relationships in meta-food
webs.
Future directions
The development of accounting for spatial processes in BEF relationships
can be progressed in multiple ways. We have advanced this field in one
dimension by synthesizing spatially-explicit processes related to animal
foraging movement with spatially-explicit plant-resource exploitation.
Our model is flexible to also include other aspects of community
structure across spatial scales, including (1) local factors and species
traits influencing exploratory movement during foraging (Hirt et
al. 2017), (2) neighbouring habitats coupled by lateral nutrient flows
in meta-ecosystems (Loreau et al. 2003; Gounand et al.2018), (3) meso-scale landscape structures in community assembly models
(Bannar‐Martin et al. 2018; Saravia et al. 2022),
including plant and animal dispersal (Ryser et al. 2021), and (4)
biogeographic differences between species pools (e.g. of plants;
Sabatini et al. 2022). In this vein, merging our
spatially-explicit meta-food web approach with food web assembly models
(Bauer et al. 2022; Saravia et al. 2022) offer a
particularly exciting avenue of future research as it allows to
understand how local spatial processes scale to the diversity and
ecosystem functioning patterns observed at larger spatial scales.
Conclusion
Despite its variability, the positive effects of diversity on
productivity in plant communities are a widely recognized pattern that
is consistent across ecosystems (Cardinale et al. 2007). To date,
the most prominent among the proposed mechanisms driving these patterns
and their variability is complementarity in the resource-use of plants
(Barry et al. 2019), which has more recently been supplemented by
multi-trophic complementarity (Poisot et al. 2013; Albertet al. 2022). To better understand their differences, we
explicitly modelled the different spatial scales at which both
mechanisms operate in a simulated biodiversity experiment. We could show
that a spatial overlap in resource access between neighbouring plants is
a fundamental requirement for positive plant diversity-productivity
relationships, highlighting the tight association of exploitative
competition with resource-use complementarity and plant compositional
shifts due to selection. The realistic, spatially-explicit
representation of meta-food webs that integrate nested local sub-food
webs stabilizes plant coexistence and yields the strongest
diversity-productivity relationships we observe. Our modelling framework
can serve as a foundation to further enhance our mechanistic
understanding of multi-trophic processes in driving plant
diversity-productivity relationships. It provides a novel approach to
managing biodiversity while explicitly accounting for the spatial
processes that underpin the ecosystem functions that are the basis of
our human society. Advancing in this direction is therefore crucial for
guiding conservation efforts to maintain biodiversity and the
functioning of ecosystems.