INTRODUCTION
Since Tilman & Downing (1994)’s pioneering work, many studies have so
far investigated biodiversity–ecosystem functioning (BEF) relationships
and demonstrated that ecosystem productivity often increases with
increasing biodiversity (Tilman et al., 2014). These results attract
ecological and societal interests as biodiversity loss leads to a
decline in ecosystem goods and services for humanity by decreasing
ecosystem productivity (Balvanera et al., 2006; Harrison et al., 2014;
Millennium Ecosystem Assessment, 2005), stimulating biodiversity
conservation and restoration. In the assessment of BEF relationships,
biomass is often used as a proxy for productivity due to difficulties inin situ measurements (e.g., Duffy et al., 2015; Gamfeldt et al.,
2015; Scurlock et al., 2002). Despite unclear causal mechanisms,
positive relationships between biodiversity and biomass are found in
many observational studies in nature (Duffy et al., 2017). From a
meta-analysis on non-experimental and experimental data, Waide et al.
(1999) concluded that such a positive BEF is commonly found for
terrestrial consumers, whereas the dominant pattern is unimodal or
non-significant for aquatic consumers.
There are two possible explanations for the scarcity of positive BEF in
aquatic consumer communities. One is the dominance of top-down effects
on consumer biomass in aquatic food webs, i.e., the negative effect of
predators on herbivore biomass is stronger in aquatic than in
terrestrial systems (Shurin et al., 2002; Strong, 1992). Another is the
difference in vertical diversity between these two systems, i.e., a
greater number of trophic levels (TLs) in aquatic than in terrestrial
food webs due to wider body size distribution and higher metabolic
efficiency in aquatic systems that permits more extended trophic links
(Rossiter et al., 2017). Since the energy entering consumer communities
becomes progressively attenuated with increasing TLs (Lindeman, 1942),
we may underestimate ecosystem productivity if substituted with
community biomass measurements in systems with multitrophic
interactions.
Recently, multitrophic perspectives have provided new insights into
empirical studies on BEF (Eisenhauer, 2017; Eisenhauer et al., 2019;
Soliveres et al., 2016). In multitrophic systems, a comprehensive
understanding of BEF relationships requires the measurement of energy
flows but not community biomass in food webs because the former can be a
common currency for ecosystem productivity across a variety of ecosystem
types (Barnes et al., 2018; Hines et al., 2015). Supported by size-based
food web models, the vertical diversity hypothesis (VDH) states that
functional diversity across TLs can enhance energy flows within a
community (Schneider et al., 2016; Wang & Brose, 2018). However, this
hypothesis has been poorly tested empirically (Hines et al., 2015;
Thompson et al., 2012a). Although experimental approaches are effective
in testing the VDH, simplified experimental systems with small species
pools and few TLs may lack the power needed to demonstrate that more
energy travels to higher TLs in real food webs with high species
richness and trophic network complexity. Barnes et al. (2016) employed
the energy-based approach to explore BEF relationships in
non-manipulative terrestrial food webs with multitrophic interactions,
classifying consumers into given trophic groups based on ecological
traits. However, realized consumer trophic positions (TPs) vary broadly
depending on the ecological context, as is often the case for aquatic
consumers (Nakazawa et al., 2010). Such flexibility in TPs can generate
analytical uncertainty in energy-based BEF.
Stable isotope analysis is a powerful tool for accurately estimating
consumer TPs (Chang et al., 2014; Jennings et al., 2002b; Post, 2002b).
Using this technique, many ecologists measure food chain length (FCL)
defined as top predator TPs (Post, 2002a). FCL is a convenient indicator
for empirical studies but may not accurately capture the overall energy
flow within a food web as not all energy flow distributions among
trophic links are fully considered (Figure 1). To overcome this
limitation, Ishikawa et al. (2017) recently proposed an alternative
indicator to characterize food web topology, integrated trophic position
(hereafter, i TP), which is defined as the summed TPs of all
consumer species in a focal food web weighed by the relative biomass of
each species (see Eq. 5 for details). The i TP indicates how many
times consumer biomass undergoes metabolic turnover, on average, as a
whole community. Moreover, it reflects dynamical changes in the biomass
pyramid via trophic interactions, e.g., a decrease in prey
biomass due to predation can be offset by increasing predator TP and
predator biomass. Therefore, the i TP can provide more appropriate
and quantitative estimates of tropic energy flows within a food web
(Figure 1).
Here, we test the VDH, i.e., whether and how functional diversity can
enhance overall trophic energy flow, by applying the i TP to
complex real food webs. We focus on spatial variation in a
meta-community of coastal benthic macroinvertebrates in the ancient Lake
Biwa, which exhibits high biodiversity with endemism (Kawanabe et al.,
2012; Timoshkin et al., 2011). Its huge lake basin has hundreds of
tributary rivers, which greatly vary in land use and local human
population sizes (Kohzu et al., 2009; Ohte et al., 2010). Thus, its
coastal habitats have high spatial heterogeneity in nutrients and basal
resource availability (Karube et al., 2010; Sakai et al., 2013). Because
benthic macroinvertebrates are sedentary or less mobile, we comparei TP across a wide variety of local communities that share the
species pool within a meta-community but greatly vary in species
composition in response to local environments (Shibata et al., 2014).
Since land use can be a strong driver that alters species composition, a
between-community comparison provides an opportunity to explore
ecosystem consequences of biodiversity change across anthropogenically
induced environmental gradients at the landscape level (Barnes et al.,
2014; Gossner et al., 2016; Thompson et al., 2012b). Comparing our
results with previous findings that the i TP decreases in more
diverse communities of stream benthic macroinvertebrates (Ishikawa et
al., 2017), we discuss a possible mechanism to explain such a negative
BEF in contrast to the VDH. To deepen our mechanistic understanding of
observed patterns in biodiversity and i TP for the coastal
meta-community, we finally employed a size-based food web approach,
which enables us to link size-specific community properties, such as
abundance, biomass, and TP, to ecosystem functioning based on the
scaling theory (Cohen et al., 2003; Jennings & Mackinson, 2003;
Jennings et al., 2002b).