VERTICAL VS HORIZONTAL DIVERSITY
Our study demonstrated that trophic energy flows defined by thei TP increase in more diverse communities of coastal benthic
macroinvertebrates, supporting the VDH in real food webs with
multitrophic interactions. When consumer biomass was used as an
indicator of ecosystem productivity, in contrast, the positive BEF
relationship was less clear. This may be due to the multitrophic nature
of aquatic food webs showing strong top-down effects on prey biomass
combined with Lindeman’s (1942) law on consumer biomass progressively
decreasing across TLs. FCL showed no significant biodiversity effects.
Although the positive relationship between biodiversity and FCL has
previously been reported in a comparative study, in which species
richness and FCL scales were extended across a wide range of ecosystem
sizes (Rossiter et al., 2017; Vander Zanden et al., 1999), empirical
studies have often failed to highlight these relationships for
individual ecosystems (Schriever & Lytle, 2020; Schriever & Williams,
2013). In open systems, whether predators with the highest TP are
sampled for analysis is often random owing to their high mobility and
low abundance, which may generate uncertainty when estimating the
realized FCL. Therefore, to empirically test the VDH for multitrophic
systems, the i TP can be a more reliable indicator for energy
flow-based ecosystem functioning than FCL as it is more robust to the
presence/absence of top predators.
In the multitrophic model testing the VDH, Wang & Brose (2018)
demonstrated that trophic transfer indicated by nutrient flows increases
when nutrient availability is high. In contrast, our observational data
revealed that basal resource availability signified by algal biomass
exerted no bottom-up effects on the i TP, as well as on consumer
biomass, except for deposit-feeding chironomids. In aquatic ecosystems,
high primary productivity is crucial to benthic macroinvertebrates as it
causes organic matter loading and consequently oxygen depletion in
benthic habitats (Paerl et al., 1998; Wolowicz et al., 2007). This is
the reason why the abundance and richness of hypoxia-sensitive grazers
decreased with increasing phytoplankton biomass in the present study. In
general, productive conditions favor hypoxia-tolerant deposit feeders
because algae-derived organic matters are embedded within detrital food
webs in the sediment (Sokolowski et al., 2012). Combined, trophic energy
flows may show a non-linear response to overall primary productivity in
benthic food webs (Vadeboncoeur et al., 2002).
Our within-lake comparison of meta-community also revealed that thei TP was affected by the relative biomass of deposit feeders
rather than top predators. The dominance of deposit feeders implies that
trophic energy is retained into a functional group with lower TPs,
decreasing both H ’ and i TP. This is simply a
phenomenological explanation for the observed correlation betweenH ’ and i TP; here, further research is needed to explain
the reason why i TP is higher for more diverse communities. In our
study, two carnivorous taxa with the highest TPs more frequently
appeared in communities with higher prey taxonomic richness. Theoretical
models demonstrated that prey–predator interactions become stable where
predators have prey options, allowing for predator biomass to persist in
the diverse community (Kondoh, 2003; Post et al., 2000). In laboratory
experiments manipulating both prey and predator diversity, Gamfeldt et
al. (2005) also demonstrated that prey richness can increase predator
biomass via prey consumption by multiple predators. These studies
provide circumstantial evidence that prey–predator diversity can
enhance trophic energy flows to higher TLs. In mesocosms with
tri-trophic interactions, Duffy et al. (2005) conducted prey diversity
manipulation to explore how the presence of predators alters the prey
diversity effects on biomass distribution. They found that prey
diversity increased prey biomass only in the presence of predators but
did not show topological changes in food webs throughout the experiment.
Future experiments to manipulate functional diversity in multitrophic
systems will further leverage the i TP to test the VDH.
More interestingly, Ishikawa et al. (2017) reported that the i TP
decreases in more diverse communities of stream benthic
macroinvertebrates in a tributary river of our study lake. To explain
such a negative BEF relationship, Ishikawa et al. (2017) proposed
alternative, but not mutually exclusive, hypotheses, i.e., variance in
edibility and trophic omnivory hypotheses, although these hypotheses
were not empirically tested. On the one hand, the former hypothesis
assumes that the relative biomass of inedible prey increases with
increasing prey diversity (Wilby & Orwin, 2013). This hypothesis is
true if inedible preys have lower TPs. In our study communities,
however, anti-predator armored gastropods, i.e., snails and bivalves,
which were among the most dominant in the biomass abundance, had
intermediate TPs, sometimes exceeding TP = 3 (Table S5). Therefore, the
dominance of these inedible preys does not always decrease thei TP in coastal macroinvertebrate communities, rejecting the
variance in edibility hypothesis.
Conversely, the trophic omnivory hypothesis assumes that predators’
omnivory decreases their TPs (Bruno & O’Connor, 2005), as reported for
well-studied food webs where 12%–43% of consumers are omnivores
(Williams & Martinez, 2004). In our study communities, the trophic
omnivory hypothesis is applicable to carnivorous insects, which
exhibited lower TPs than expected from their carnivorous habits (Table
S5). In fact, predatory stoneflies can undergo a seasonal niche shift
from carnivory to omnivory in winter, which results in lower TPs than
carnivores (Miyasaka & Genkai-Kato, 2009). This type of trophic
omnivory has a potential to decrease the i TP. Considering that
their relative biomass is negligible (0.00 ± 0.01; Table S2), however,
their trophic omnivory should only marginally affect the i TP in
coastal macroinvertebrate communities. In conclusion, the trophic
omnivory hypothesis can be rejected for our study communities.
When comparing coastal and stream benthic communities, the most critical
difference is the diversity of basal resources and consumer functional
feeding groups (FFGs), i.e., the former is characterized by the
dominance of autochthonous algal products supporting deposit feeders and
the latter by a combination of autochthonous algal and allochthonous
terrestrial products supporting a variety of FFGs (Allan, 2008; Horne &
Goldman, 1994). Within the study watershed, for instance, coastal
communities harbored more abundant hypoxia-tolerant deposit feeders
(pi = 0.45 ± 0.28 for oligochaetes and 0.24 ±
0.25 for chironomids; Table S1) than their stream counterparts
(pi = 0.09 ± 0.15 and 0.20 ± 0.18, respectively;
Ko et al., 2021). In contrast, in stream communities, EPT taxa (i.e.,
Ephemeroptera, Plecoptera, and Trichoptera), which are considered the
dominant FFGs, account for 45.7% of species richness (75/164; Ko et
al., 2021), which is much greater than their coastal counterparts
(25.9% = 7/27; Table S1). Even within a given EPT taxon, species
diversity can enhance basal resource use via the interspecific
complementarity effects (Cardinale et al., 2002). When compared with our
coastal cases, the stream benthic food webs are characterized by the
functional diversity of primary consumers.
Duffy et al. (2007) proposed a conceptual framework in which BEF
relationships are altered by interactions between horizontal and
vertical diversities in complex ways. Developing this framework, Kato et
al. (2018) constructed a theoretical model to define complex food webs,
in which biodiversity (H ’) can be broken down into three
components, namely, horizontal diversity (DH ),
vertical diversity (DV ), and range diversity
(DR ), defined as functional diversity within a
TL, diversity of TLs, and degree of trophic omnivory, respectively, with
a formula of H ’ = DH +
DV – DR . From a
comparative analysis of three riverine systems, Kato et al. (2018)
concluded that DH can explain spatiotemporal
variations in the diversity of stream macroinvertebrate communities.
This may also hold true for stream communities in our study watershed
(Ishikawa et al., 2014). Negative BEF can be observed through
between-community comparisons if more diverse primary consumers (TP = 2)
increase their relative biomass, leading to a lower i TP. In
contrast, for vertical diversity, the spatial variation in i TP is
much greater for our coastal communities (range = 1.69) than the stream
counterparts (0.40; Ishikawa et al. 2017). Therefore, it is likely that
positive BEF in coastal communities can be explained by vertical
diversity and negative BEF in stream communities by horizontal diversity
of primary consumers, resulting in contrasting BEF patterns.