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.