Michio Kondoh

Unifying the relationships of species richness to productivity and disturbance

Although species richness has been hypothesized to be highest at ‘intermediate’ levels of disturbance, empirical studies have demonstrated that the disturbance-diversity relationship can be either negative or positive depending on productivity. On the other hand, hypothesized productivity–diversity relationships can be positive, negative or unimodal, as confirmed by empirical studies. However, it has remained unclear under what conditions each pattern is realized, and there is little agreement about the mechanisms that generate these diverse patterns. In this study, I present a model that synthesizes these separately developed hypotheses and shows that the interactive effects of disturbance and productivity on the competitive outcome of multispecies dynamics can result in these diverse relationships of species richness to disturbance and productivity. The predicted productivity–diversity relationship is unimodal but the productivity level that maximizes species richness increases with increasing disturbance. Similarly, the predicted disturbance–diversity relationship is unimodal but the peak moves to higher disturbance levels with increasing productivity. Further, these patterns are well explained by the opposite effects of productivity and disturbance on competitive outcome that are suggested by the change in community composition along these two environmental gradients: higher productivity favours superior competitors while higher disturbance levels favour inferior competitors.

Diversity of Interaction Types and Ecological Community Stability

Diversity of Interactions The diversity in interactions that occur between different species—such as predation, competition, and mutualism—is a fundamental feature of natural ecological systems. Using a theoretical model, Mougi and Kondoh (p. 349; see the Perspective by Boyd) show that the diversity of ecological relationship helps a biological community to be stable and thus may be key to the maintenance of biodiversity itself. A theoretical model incorporating multiple interactions shows how ecological complexity leads to ecosystem stability. Ecological theory predicts that a complex community formed by a number of species is inherently unstable, guiding ecologists to identify what maintains species diversity in nature. Earlier studies often assumed a community with only one interaction type, either an antagonistic, competitive, or mutualistic interaction, leaving open the question of what the diversity of interaction types contributes to the community maintenance. We show theoretically that the multiple interaction types might hold the key to understanding community dynamics. A moderate mixture of antagonistic and mutualistic interactions can stabilize population dynamics. Furthermore, increasing complexity leads to increased stability in a “hybrid” community. We hypothesize that the diversity of species and interaction types may be the essential element of biodiversity that maintains ecological communities.

MiFish, a set of universal PCR primers for metabarcoding environmental DNA from fishes: detection of more than 230 subtropical marine species

We developed a set of universal PCR primers (MiFish-U/E) for metabarcoding environmental DNA (eDNA) from fishes. Primers were designed using aligned whole mitochondrial genome (mitogenome) sequences from 880 species, supplemented by partial mitogenome sequences from 160 elasmobranchs (sharks and rays). The primers target a hypervariable region of the 12S rRNA gene (163–185 bp), which contains sufficient information to identify fishes to taxonomic family, genus and species except for some closely related congeners. To test versatility of the primers across a diverse range of fishes, we sampled eDNA from four tanks in the Okinawa Churaumi Aquarium with known species compositions, prepared dual-indexed libraries and performed paired-end sequencing of the region using high-throughput next-generation sequencing technologies. Out of the 180 marine fish species contained in the four tanks with reference sequences in a custom database, we detected 168 species (93.3%) distributed across 59 families and 123 genera. These fishes are not only taxonomically diverse, ranging from sharks and rays to higher teleosts, but are also greatly varied in their ecology, including both pelagic and benthic species living in shallow coastal to deep waters. We also sampled natural seawaters around coral reefs near the aquarium and detected 93 fish species using this approach. Of the 93 species, 64 were not detected in the four aquarium tanks, rendering the total number of species detected to 232 (from 70 families and 152 genera). The metabarcoding approach presented here is non-invasive, more efficient, more cost-effective and more sensitive than the traditional survey methods. It has the potential to serve as an alternative (or complementary) tool for biodiversity monitoring that revolutionizes natural resource management and ecological studies of fish communities on larger spatial and temporal scales.

Building trophic modules into a persistent food web

Understanding what maintains species and perpetuates their coexistence in a network of feeding relationships (the food web) is of great importance for biodiversity conservation. A food web can be viewed as consisting of a number of simple subunits called trophic modules. Intraguild predation (IGP), in which a prey and its predator compete for the same resource, is one of the best-studied trophic modules. According to theory, there are two ways to yield a large persistent system from such modules: (i) to use persistent subunits as building blocks or (ii) to arrange the subunits in a way that externally supports the nonpersistent subunits. Here, I show that the complex food web of the Caribbean marine ecosystem is constructed in both ways. I show that IGP modules, which convey internal persistence because of the fact that prey are superior competitors for the resources, are overrepresented in the Caribbean ecosystem. The other modules, consisting of competitively inferior prey, are not persistent in isolation. However, competitively inferior prey in these modules tend to receive more advantage from extra-module interactions, which allows persistence of the IGP module. In addition, those exterior interactions tend to be provided by intrinsically persistent IGP modules to prevent cascading extinction of interacting IGP modules. The food web can be viewed as a set of interacting modules, nonrandomly arranged to enhance the maintenance of biodiversity.

The Release Rate of Environmental DNA from Juvenile and Adult Fish

The environmental DNA (eDNA) technique is expected to become a powerful, non-invasive tool for estimating the distribution and biomass of organisms. This technique was recently shown to be applicable to aquatic vertebrates by collecting extraorganismal DNA floating in the water or absorbed onto suspended particles. However, basic information on eDNA release rate is lacking, despite it being essential for practical applications. In this series of experiments with bluegill sunfish (Lepomis macrochirus), we examined the effect of fish developmental stage on eDNA release rate. eDNA concentration reached equilibrium 3 days after the individual fish were introduced into the separate containers, enabling calculation of the eDNA release rate (copies h−1) from individual fish on the assumption that the number of eDNA released from the fish per unit time equals total degradation in the container (copies h−1). The eDNA release rate was 3–4 times higher in the adult (body weight: 30–75 g) than in the juvenile group (0.5–2.0 g). Such positive relationship between fish size and eDNA release rate support the possibility of biomass rather than density estimation using eDNA techniques. However, the eDNA release rate per fish body weight (copies h−1 g−1) was slightly higher in the juvenile than the adult group, which is likely because of the ontogenetic reduction in metabolic activity. Therefore, quantitative eDNA data should be carefully interpreted to avoid overestimating biomass when the population is dominated by juveniles, because the age structure of the focal population is often variable and unseen in the field. eDNA degradation rates (copies l−1 h−1), calculated by curve fitting of time-dependent changes in eDNA concentrations after fish removal, were 5.1–15.9% per hour (half-life: 6.3 h). This suggests that quantitative eDNA data should be corrected using a degradation curve attained in the target field.

Functional diversity of microbial decomposers facilitates plant coexistence in a plant–microbe–soil feedback model

Theory and empirical evidence suggest that plant–soil feedback (PSF) determines the structure of a plant community and nutrient cycling in terrestrial ecosystems. The plant community alters the nutrient pool size in soil by affecting litter decomposition processes, which in turn shapes the plant community, forming a PSF system. However, the role of microbial decomposers in PSF function is often overlooked, and it remains unclear whether decomposers reinforce or weaken litter-mediated plant control over nutrient cycling. Here, we present a theoretical model incorporating the functional diversity of both plants and microbial decomposers. Two fundamental microbial processes are included that control nutrient mineralization from plant litter: (i) assimilation of mineralized nutrient into the microbial biomass (microbial immobilization), and (ii) release of the microbial nutrients into the inorganic nutrient pool (net mineralization). With this model, we show that microbial diversity may act as a buffer that weakens plant control over the soil nutrient pool, reversing the sign of PSF from positive to negative and facilitating plant coexistence. This is explained by the decoupling of litter decomposability and nutrient pool size arising from a flexible change in the microbial community composition and decomposition processes in response to variations in plant litter decomposability. Our results suggest that the microbial community plays a central role in PSF function and the plant community structure. Furthermore, the results strongly imply that the plant-centered view of nutrient cycling should be changed to a plant–microbe–soil feedback system, by incorporating the community ecology of microbial decomposers and their functional diversity.

Anti-predator defence and the complexity–stability relationship of food webs

The mechanism for maintaining complex food webs has been a central issue in ecology because theory often predicts that complexity (higher the species richness, more the interactions) destabilizes food webs. Although it has been proposed that prey anti-predator defence may affect the stability of prey–predator dynamics, such studies assumed a limited and relatively simpler variation in the food-web structure. Here, using mathematical models, I report that food-web flexibility arising from prey anti-predator defence enhances community-level stability (community persistence and robustness) in more complex systems and even changes the complexity–stability relationship. The model analysis shows that adaptive predator-specific defence enhances community-level stability under a wide range of food-web complexity levels and topologies, while generalized defence does not. Furthermore, while increasing food-web complexity has minor or negative effects on community-level stability in the absence of defence adaptation, or in the presence of generalized defence, in the presence of predator-specific defence, the connectance–stability relationship may become unimodal. Increasing species richness, in contrast, always lowers community-level stability. The emergence of a positive connectance–stability relationship however necessitates food-web compartmentalization, high defence efficiency and low defence cost, suggesting that it only occurs under a restricted condition.

Environmental DNA as a 'Snapshot' of Fish Distribution: A Case Study of Japanese Jack Mackerel in Maizuru Bay, Sea of Japan.

Recent studies in streams and ponds have demonstrated that the distribution and biomass of aquatic organisms can be estimated by detection and quantification of environmental DNA (eDNA). In more open systems such as seas, it is not evident whether eDNA can represent the distribution and biomass of aquatic organisms because various environmental factors (e.g., water flow) are expected to affect eDNA distribution and concentration. To test the relationships between the distribution of fish and eDNA, we conducted a grid survey in Maizuru Bay, Sea of Japan, and sampled surface and bottom waters while monitoring biomass of the Japanese jack mackerel (Trachurus japonicus) using echo sounder technology. A linear model showed a high R2 value (0.665) without outlier data points, and the association between estimated eDNA concentrations from the surface water samples and echo intensity was significantly positive, suggesting that the estimated spatial variation in eDNA concentration can reflect the local biomass of the jack mackerel. We also found that a best-fit model included echo intensity obtained within 10–150 m from water sampling sites, indicating that the estimated eDNA concentration most likely reflects fish biomass within 150 m in the bay. Although eDNA from a wholesale fish market partially affected eDNA concentration, we conclude that eDNA generally provides a ‘snapshot’ of fish distribution and biomass in a large area. Further studies in which dynamics of eDNA under field conditions (e.g., patterns of release, degradation, and diffusion of eDNA) are taken into account will provide a better estimate of fish distribution and biomass based on eDNA.

Food webs are built up with nested subwebs

Nested structure, in which specialists interact with subsets of species with which generalists interact, has been repeatedly found in networks of mutualistic interactions and thus is considered a general feature of mutualistic communities. However, it is uncertain how exclusive nested structure is for mutualistic communities since few studies have evaluated nestedness in other types of networks. Here, we show that 31 published food webs consist of bipartite subwebs that are as highly nested as mutualistic networks, contradicting the hypothesis that antagonistic interactions disfavor nested structure. Our findings suggest that nested networks may be a common pattern of communities that include resource-consumer interactions. In contrast to the hypothesis that nested structure enhances biodiversity in mutualistic communities, we also suggest that nested food webs increase niche overlap among consumers and thus prevent their coexistence. We discuss potential mechanisms for the emergence of nested structure in food webs and other types of ecological networks.

Habitat fragmentation resulting in overgrazing by herbivores.

Habitat fragmentation sometimes results in outbreaks of herbivorous insect and causes an enormous loss of primary production. It is hypothesized that the driving force behind such herbivore outbreaks is disruption of natural enemy attack that releases herbivores from top-down control. To test this hypothesis I studied how trophic community structure changes along a gradient of habitat fragmentation level using spatially implicit and explicit models of a tri-trophic (plant, herbivore and natural enemy) food chain. While in spatially implicit model number of trophic levels gradually decreases with increasing fragmentation, in spatially explicit model a relatively low level of habitat fragmentation leads to overgrazing by herbivore to result in extinction of the plant population followed by a total system collapse. This provides a theoretical support to the hypothesis that habitat fragmentation can lead to overgrazing by herbivores and suggests a central role of spatial structure in the influence of habitat fragmentation on trophic communities. Further, the spatially explicit model shows (i) that the total system collapse by the overgrazing can occur only if herbivore colonization rate is high; (ii) that with increasing natural enemy colonization rate, the fragmentation level that leads to the system collapse becomes higher, and the frequency of the collapse is lowered.