Discussion
Most biodiversity-ecosystem-functioning studies address the effect of
diversity within a trophic level, such as plants, on functions such as
primary productivity (e.g., Isbell et al. 2015). We have introduced an
integrated model of producer species richness and resource-use
complementarity that yields positive diversity-productivity
relationships consistent with patterns found in experimental (Isbell et
al. 2015) and natural communities (Duffy et al. 2017; van der Plas
2019). When introducing resource-use complementarity by creating
dissimilarities in how producer species access resource-pool
compartments, monocultures generally become less productive than species
mixtures as they utilize a smaller proportion of the total resource pool
(Tilman et al. 1997; Loreau 2001). By increasing this resource-use
dissimilarity across primary producers, we could enhance such net
diversity effects through bottom-up mechanisms. However, trophic
interactions can affect diversity-productivity relationships in producer
communities in similar ways. We find that adding animal communities
embedded in food-webs of multi-trophic interactions strengthened the net
diversity effect on primary production. This similarly results from a
reduction in monoculture productivity. Such top-down reductions due to
herbivory can be compensated in more species-rich producer communities
(e.g., Jactel et al. 2021), where trophic interactions shape the
composition and interactions among producer species (e.g., Naeem et al.
1994; Thébault & Loreau 2003; Brose 2008; Zhao et al. 2019). By
addressing the interplay of resource-use complementarity and
multi-trophic interactions, our study synthesizes bottom-up and top-down
drivers of BEF relationships. While both create complementarity to
create positive net diversity effects, our model suggests that diversity
across trophic levels can additionally change selection mechanisms and
thereby producer community composition. Specifically, a dominance of
highly productive monoculture species (positive selection effects) at
low animal richness shifts to a community that also includes the less
productive monoculture species (negative selection effects) as animal
richness increases. An increased complementarity among producer species
at high animal richness therefore allows more species to coexist. In
consequence, complementarity effects increase with animal richness and
overcompensate the negative selection effects. To which degree
multi-trophic mechanisms can increase net diversity effects is
determined by resource-use dissimilarity. At high levels of resource-use
dissimilarity, multi-trophic interactions show only weak effects,
whereas lower levels of resource-use dissimilarity allow top-down
mechanisms to enhance net diversity effects more. Hence, our results
suggest that multi-trophic interactions and resource-use complementarity
among producers shape diversity-productivity relationships
interactively. This finding implies that processes across trophic levels
are strongly interwoven, which renders the integration of multi-trophic
mechanisms in the analysis of diversity effects in complex communities
highly important.
In simple communities without animals, we tested for the consequences of
resource-use dissimilarities between producer species. It promotes
coexistence, creates complementarity and consequently positive net
diversity effects, thereby confirming findings of earlier theoretical
studies (Vandermeer 1981; Tilman 1982; Loreau 2004). Further,
resource-use dissimilarity can create a range of different shapes of
diversity-productivity relationships (e.g., exponential, sigmoidal, or
saturating on a log2-scale of producer richness), as
found in experimental and natural studies (Balvanera et al. 2006; Duffy
et al. 2017). Our simulated producer communities show how at low levels
of resource-use dissimilarity (i.e., substantial overlap in the resource
compartments used by different producer species), saturating
diversity-productivity relationships emerge where only a few species are
necessary to maximize primary production. On the contrary, at high
levels of resource-use dissimilarity (i.e., producer species mostly
exploit different compartments of the total resource pool), the majority
of producer species is necessary to maximize productivity. This
highlights how an increasing resource-use dissimilarity not only
increases complementarity between species but also reduces their
functional redundancy in resource-use (Loreau 2004). When producer
species are lost, communities with a low functional redundancy are more
prone to become less productive and thus show weaker net diversity
effects. Resource-use dissimilarity that enhances complementarity and
thus drives net diversity effects in producer communities can therefore
also be responsible for weakening such effects as species are lost.
In ecosystems with animal species, our results confirm that
multi-trophic interactions can create positive net diversity effects
even without any resource-use dissimilarity amongst producers (Thébault
& Loreau 2003). As long as producer species are not limited to access
distinct resource compartments, multi-trophic interactions consistently
enhance net diversity effects. Whether herbivores are predominantly
specialists or generalists determines if such effects are strong or
negligible, respectively (Thébault & Loreau 2003; Jactel et al. 2021).
In our simulations, generalism is constraint by predator-prey body-mass
ratios known from aquatic and belowground ecosystems (Schneider et al.
2016). Regardless, they are sufficient to reproduce the decreasing
influence of herbivores on primary production as producer diversity
increases that is common to forests, grasslands, and agroecosystems
alike (Barnes et al. 2020; Wan et al. 2020; Jactel et al. 2021). We find
that animals largely influence net diversity effects by reducing primary
production in monocultures (Barry et al. 2018). In mixtures, reductions
in productivity can be compensated by producers that access the same
resource compartments (i.e., functional redundancy in resource-use;
Naeem 1998). The potential of compensatory effects therefore scales with
resource-use dissimilarity and producer species richness. When animals
are present, a lack of compensation inevitably leads to a reduced
primary production in mixture. Even though this may weaken the positive
impact of multi-trophic interactions on net diversity effects, our
results suggest that it is rarely the case.
Our findings show that enhanced net diversity effects in multi-trophic
ecosystems can largely be attributed to complementarity mechanisms
(Thébault & Loreau 2003; Barry et al. 2018), which reduce interspecific
competition among producer species. Apart from competing for resources,
animals can shift the competitive interaction to being additionally
mediated by consumers and their trophic interactions (Holt 1977; Loreau
2010). For example, multi-trophic interactions reduce competition
between producer species by limiting productivity and thereby inhibiting
the dominance of single species (Brose 2008). As a result, producer
species can coexist even if their resource-niches overlap entirely
(Brose 2008; Loreau 2010). Similar to an increased vertical diversity
(Wang & Brose 2018), we found that an increased animal richness can
enable more producer species to coexist, which is indicative for the
higher complementarity among them. In addition, a complementarity in
herbivorous feeding links sorts producer species into different trophic
groups common to our simulated and natural food-webs alike (Gauzens et
al. 2015; Schneider et al. 2016). This top-down aspect of trophic
complementarity can enhance net diversity effects similar to the
bottom-up complementarity of resource-use (Thébault & Loreau 2003;
Poisot et al. 2013). Despite the increased complementarity, a limited
resource availability caps primary productivity in multi-trophic
ecosystems to not exceed primary production in ecosystems without
animals.
While multi-trophic interactions determine net diversity effects in
producer communities largely through complementarity mechanisms,
selection effects draw a less conclusive picture. Differences in the
functional expression of producer species in monoculture are a
fundamental requirement for non-neutral selection effects (Loreau &
Hector 2001). In our simulations, the maximum productivity of all
producer species is largely determined by their access to resource
compartments, which is the same for all co-occurring species. Their
functional expression in monoculture (i.e., primary production without
competition) is therefore equal in the absence of animal consumers.
Hence, we do not find selection effects in simple producer communities.
This model simplification disregards processes such as associations
between competitive ability and productivity that can determine
selection in producer communities (Tilman et al. 1997), but it enables
us to isolate multi-trophic selection mechanisms. Specifically, we find
that the productivity of large producer species is less susceptible to
herbivory. The low mass-specific metabolic rates of large species may
play an important role in minimizing losses to herbivory (Brown et al.
2004; Schneider et al. 2016). The ability of large species to better
cope with herbivory also increases their chances to persist in mixtures
(Schneider et al. 2016; Wang & Brose 2018), which should lead to
positive selection effects. However, we find negative selection effects
at high animal richness and resource-use dissimilarity, which both tend
to enhance complementarity. Because complementarity mechanisms reduce
interspecific competition, the small producer species that are excluded
when complementarity is low can persist in mixtures. Once in the
mixture, a disproportionally strong effect of herbivores on strong
competitors (Brose 2008) elevates the productivity of the otherwise
excluded, small and less productive producer species. Even though this
does not imply their dominance, it alters community composition enough
to turn selection effects negative in response to an increasing
complementarity. This interdependence of complementarity and selection
effects in multi-trophic ecosystems becomes apparent in our findings of
their inverse relationship to realized producer richness. However, not
all complementarity mechanisms have to be linked to selection mechanisms
that influence net diversity effects (e.g., resource-use dissimilarity
as defined in this study). Identifying causes of selection can therefore
serve as an important tool to disentangle drivers of diversity effects.
Despite the evidence that multi-trophic interactions (Thébault & Loreau
2003) and resource-use complementarity (Tilman et al. 1997) can create
positive net diversity effects on primary production independently, how
they interact has remained speculative (Tilman et al. 2014; Barry et al.
2018). We find that both mechanisms create positive net diversity
effects by lowering primary production in monoculture. Hence, an already
low monoculture primary production at high resource-use dissimilarity,
which leads to high net diversity effects on its own, cannot be reduced
much further by animals before driving the single producer species and
thus the entire food-web extinct. A high resource-use dissimilarity
therefore limits the ability of multi-trophic interactions to enhance
net diversity effects. Similarly, it promotes the coexistence of
producer species by reducing competition but simultaneously limits the
ability of multi-trophic mechanisms to alter competition in favor of a
more diverse producer community (Brose 2008). In both cases, bottom-up
forces fundamentally limit the strength of top-down mechanisms to
improve either net diversity effects or species coexistence. Plastic
responses in resource-use to changes in producer diversity (Von Felten
et al. 2009; Mueller et al. 2013), consumer diversity, or vertical
diversity (Zhao et al. 2019) might affect such limitations but should
not change our conclusion that multi-trophic interactions become
especially important when the resource-use dissimilarity of producers is
low.
The interactive effect of resource-use complementarity and multi-trophic
interactions creates positive net diversity effects that generally
exceed their independent effects. Both mechanisms jointly support
diverse communities of complementary producer species. However,
multi-trophic interactions determine the community composition of the
producer species depending on the animal diversity of the multi-trophic
ecosystem, whereas selection in simple producer communities is solely
driven by resource competition. Hence, different mechanisms can
similarly create complementary communities, but the associated selection
mechanisms may differ. To identify drivers of positive diversity effects
common to natural ecosystems, instead of focusing on identifying causes
of complementarity it may therefore be more expedient to identify causes
of selection and understand how they relate to complementarity
mechanisms. In bridging the gap between food-web and BEF theory, our
novel simulation-framework can guide such efforts as it integrates
effects of diversity within and across trophic levels on functions of
complex, multi-trophic ecosystems. Its results highlight the interplay
between bottom-up and top-down forces in these ecosystems, emphasizing
the need to adopt a multi-trophic view on BEF relationships.