Linkages between stream and forest food webs: Shigeru Nakano's legacy for ecology in Japan

Adaptive foragers and community ecology: linking individuals to communities and ecosystems

In a replicated field experiment we studied the effects of natural densities of two exotic consumers, the predatory and herbivorous signal crayfish (Pacifastacus leniusculus) and the predatory rainbow trout (Oncorhynchus mykiss), on multiple trophic levels of a pond community. The goals were to: (1) determine the individual and combined effects of predators on macroinvertebrates, macrophytes, and periphytic algae; (2) evaluate the strength of direct and indirect interactions in a food web influenced by omnivores; and (3) evaluate the relative importance of direct and indirect predator effects on mortality and growth of a native frog species, Rana temporaria. The experiment showed that both signal crayfish and rainbow trout had strong effects on multitrophic levels of a littoral pond community, through direct consumption and indirect effects on lower trophic levels. Crayfish had weak but significant negative effects on the biomass of predatory invertebrates and greatly reduced the biomass of snails, the most abundant invertebrate grazers. Although the number of active herbivorous tadpoles tended to be higher in crayfish cages relative to control cages, the proportion of surviving froglets was lower in crayfish cages than in control cages, possibly due to crayfish predation on injured tadpoles. The size of surviving froglets did not differ from controls, but tadpoles in crayfish cages often suffered tail injuries. Macrophyte coverage decreased as a result of crayfish consumption and nonconsumptive fragmentation. However, the biomass of periphyton increased in crayfish cages relative to controls, probably due to reduced grazing from snails. In contrast, trout had strong negative effects on the biomass of both predatory invertebrates and insect grazers, whereas trout had less effect on snail biomass than did crayfish. Also, in contrast to crayfish cages, the number of active tadpoles in trout cages was lower than in controls, probably due to a combination of trout predation and trout-induced reduced tadpole activity. Trout had a strong negative impact on froglet survival, and froglets in trout cages metamorphosed at a smaller size and had reduced growth rates compared to froglets in crayfish and control cages. As with crayfish, the biomass of periphyton increased in trout cages relative to controls, which may be due to a combination of both density and trait-mediated trout effects on tadpole grazing. In treatments with multiple predators the effects of crayfish and trout on caged communities were independent, and there were few interactions. Mostly effects of combined predators reflected those in single predator cages. Our results demonstrate that noninteracting, introduced multiple predators can have strong direct and indirect effects on multiple trophic levels in pond communities. Trophic cascades may develop in aquatic food webs even with omnivores such as crayfish, and in complex habitats with trout. These strong indirect effects are mediated through both predation on important grazers (i.e., the crayfish-snail-periphyton link) and a combination of density and behavioral responses of grazers to predators (i.e., the trout-tadpole-periphyton link). When two noninteracting predators have strong but different effects on prey survival or activity, their combined effects on intermediate trophic levels reflect responses to the more dangerous predator. (Less)

Nearly all ecosystems are contaminated with highly toxic methylmercury (MeHg), but the specific sources and pathways leading to the uptake of MeHg within and among food webs are not well understood. In this study, we report stable mercury (Hg) isotope compositions in food webs in a river and an adjacent forest in northern California and demonstrate the utility of Hg isotopes for studying MeHg sources and cross-habitat transfers. We observed large differences in both δ(202)Hg (mass-dependent fractionation) and Δ(199)Hg (mass-independent fractionation) within both food webs. The majority of isotopic variation within each food web could be accounted for by differing proportions of inorganic Hg [Hg(II)] and MeHg along food chains. We estimated mean isotope values of Hg(II) and MeHg in each habitat and found a large difference in δ(202)Hg between Hg(II) and MeHg (∼2.7‰) in the forest but not in the river (∼0.25‰). This is consistent with in situ Hg(II) methylation in the study river but suggests Hg(II) methylation may not be important in the forest. In fact, the similarity in δ(202)Hg between MeHg in forest food webs and Hg(II) in precipitation suggests that MeHg in forest food webs may be derived from atmospheric sources (e.g., rainfall, fog). Utilizing contrasting δ(202)Hg values between MeHg in river food webs (-1.0‰) and MeHg in forest food webs (+0.7‰), we estimate with a two-source mixing model that ∼55% of MeHg in two riparian spiders is derived from riverine sources while ∼45% of MeHg originates from terrestrial sources. Thus, stable Hg isotopes can provide new information on subtle differences in sources of MeHg and trace MeHg transfers within and among food webs in natural ecosystems.

1.2 - Food web science: Moving on the path from abstraction to prediction

Understanding food webs is important and useful for planning environmental conservation, management and restoration. However, research on food webs is not uniform globally; it tends to be concentrated in specific areas or ecosystem types, and would hinder our understanding of food webs and ecosystem processes. This study examined the trends in food web research over the past decades by analysing publication data from Web of Science; in particular, it focused on the ecosystem types studied, countries in which the studies were done, and which countries collaborated on the studies. A total of 20,239 publications were examined. The results showed that research on food webs has dramatically increased since the 1990s. Most publications related focused on aquatic ecosystems. North American and European countries contributed much more in terms of research productivity than those from Africa and South America. Collaboration among individual authors and countries has become increasingly intensive. The USA and Canada were consistently the top two productive countries, and had the most frequent collaborations. Our study indicates that food webs from ecosystems other than aquatic ones, such as terrestrial ecosystems, also require more attention in the future; in particular those that exist within countries from Africa and South America.

Shigeru Nakano was a Japanese ecologist whose work crossed boundaries among subdisciplines in ecology, between aquatic and terrestrial habitats, and between different languages and cultures. He published his first paper in 1985 while still an undergraduate, and is well known for his early research on the individual behavior of stream salmonids in dominance hierarchies. Shortly after completing his Master’s degree in 1987 he began collaborating with many graduate students and other scientists, including those from the US, and expanded his research to include factors controlling stream salmonid distribution and abundance across spatial scales ranging from local to landscape levels. In 1995 he moved to a research station in southwestern Hokkaido and began new collaborative research on interactions between forest and stream food webs. Nakano pioneered large-scale field experiments using greenhouses to sever the reciprocal fluxes of invertebrate prey between stream and riparian food webs. The strong direct and indirect effects of isolating these food webs from each other on organisms ranging from stream algae to fish, riparian spiders, and bats have revealed new linkages and explained phenomena that were previously unexplained. When combined with similar results from other investigators, they have created a paradigm shift in ecology. Shigeru Nakano was lost at sea in Baja California on March 27, 2000 at the age of 37, but key papers from his 15-year career set new standards for rigor, detail, and synthesis. They continue to be highly cited and inspire new research, and to foster new collaborations among Japanese and western scientists.

Summary1. Dramatic advances have been made recently in the study of biodiversity–ecosystem functioning (B‐EF) relations and food web ecology. These fields are now starting to converge, and this fusion has the potential to improve our understanding of how environmental stressors modulate ecosystem processes and the supply of ‘goods and services’.2. Food web structure and dynamics can exert particularly strong influences on B‐EF relations in fresh waters, as consumer–resource interactions (e.g. trophic cascades) are often more important than horizontal interactions within trophic levels. For instance, many freshwater food webs are size structured, with large organisms tending to occupy the higher trophic levels and often exerting powerful effects on ecosystem processes. However, because they are also vulnerable to perturbations, non‐random losses of these large taxa can alter both food web structure and ecosystem functioning profoundly.3. Recently, the focus of food web research has shifted away from exploring patterns, towards developing an understanding of processes (e.g. quantifying fluxes of individuals, biomass, energy, nutrients) and how the two interact. Many of the best‐characterized food webs are from fresh waters, and these ecosystems are now being used to address some of the shortcomings of earlier B‐EF studies. I have identified several key gaps in our current knowledge and highlighted potentially fruitful avenues of future B‐EF and food web research.4. A major challenge for this newly emerging research is to place it within a unified theoretical framework. The application of metabolic theory and ecological stoichiometry may help to achieve this goal by considering biological systems within the constraints imposed upon them by physical and chemical laws.

Changes to the community ecology of hosts for zoonotic pathogens, particularly rodents, are likely to influence the emergence and prevalence of zoonotic diseases worldwide. However, the complex interactions between abiotic factors, pathogens, vectors, hosts, and both food resources and predators of hosts are difficult to disentangle. Here we (1) use 19yr of data from six large field plots in southeastern New York to compare the effects of hypothesized drivers of interannual variation in Lyme disease risk, including the abundance of acorns, rodents, and deer, as well as a series of climate variables; and (2) employ landscape epidemiology to explore how variation in predator community structure and forest cover influences spatial variation in the infection prevalence of ticks for the Lyme disease bacterium, Borrelia burgdorferi, and two other important tick-borne pathogens, Anaplasma phagocytophilum and Babesia microti. Acorn-driven increases in the abundance of mice were correlated with a lagged increase in the abundance of questing nymph-stage Ixodes scapularis ticks infected with Lyme disease bacteria. Abundance of white-tailed deer 2 yr prior also correlated with increased density of infected nymphal ticks, although the effect was weak. Density of rodents in the current year was a strong negative predictor of nymph density, apparently because high current abundance of these hosts can remove nymphs from the host-seeking population. Warm, dry spring or winter weather was associated with reduced density of infected nymphs. At the landscape scale, the presence of functionally diverse predator communities or of bobcats, the only obligate carnivore, was associated with reduced infection prevalence of I.scapularis nymphs with all three zoonotic pathogens. In the case of Lyme disease, infection prevalence increased where coyotes were present but smaller predators were displaced or otherwise absent. For all pathogens, infection prevalence was lowest when forest cover within a 1km radius was high. Taken together, our results suggest that a food web perspective including bottom-up and top-down forcing is needed to understand drivers of tick-borne disease risk, a result that may also apply to other rodent-borne zoonoses. Prevention of exposure based on ecological indicators of heightened risk should help protect public health.

Many features of a food web are semi‐ to fully quantitative and are subject to uncertainty. Various techniques have been developed to describe these features. Others have been developed to model food web dynamics for purposes that include prediction. Yet, few approaches facilitate systematic, unified conclusions to be readily drawn about the food web's characteristics. Even fewer address the uncertainty that is inherent in the behavior of organisms within the web and in the surrounding environment. Recently, statistical modeling techniques have been adapted to food web research; they allow the investigator to simultaneously address multiple questions about the food web of interest under a unified quantitative framework, while fully exploiting the important role that uncertainty plays in food web ecology. This article reviews some conventional methods for drawing insights into food webs, and discusses recent statistical developments in food web research. Some details of the latter on network flows are provided.

Trophic cascades, or indirect effects of predators on non-adjacent lower trophic levels, are a classic phenomenon in ecology, and are thought to be strongest in aquatic ecosystems. Most research on freshwater trophic cascades focused on temperate lakes, where fish are present and where Daphnia frequently dominate the zooplankton community. These studies identified that Daphnia often play a key role in facilitating trophic cascades by linking fish to algae with strong food web interactions. However, Daphnia are rare or absent in most tropical and subtropical lowland freshwaters, and fish are absent from small and temporary water bodies, where invertebrates fill the role of top predator. While invertebrate predators are ubiquitous in freshwater systems, most have received little attention in food web research. Therefore, we aimed to test whether trophic cascades are possible in small warmwater ponds where Daphnia are absent and small invertebrates are the top predators. We collected naturally occurring plankton communities from small fishless water bodies in central Texas and propagated them in replicate pond mesocosms. We removed zooplankton from some mesocosms, left the plankton community intact in others, and added one of two densities of the predaceous insect Neoplea striola to others. Following an incubation period, we then compared biomasses of plankton groups to assess food web effects between the trophic levels, including whether Neoplea caused a trophic cascade by reducing zooplankton. The zooplankton community became dominated by copepods which prefer large phytoplankton and exhibit a fast escape response. Perhaps due to these qualities of the copepods and perhaps due to other reasons such as high turbidity impairing predation, no evidence for food web effects were found other than somewhat weak evidence for zooplankton reducing large phytoplankton. More research is needed to understand the behavior and ecology of Neoplea, but trophic cascades may generally be weak or absent in fishless low latitude lowland water bodies where Daphnia are rare.

The gypsy moth is considered one of the most harmful invasive forest insects in North America. It has been suggested that gypsy moth may indirectly impact native caterpillar communities via shared parasitoids. However, the impact of gypsy moth on forest insect food webs in general remains unstudied. Here we assess such potential impacts by surveying forest insect food webs in Ontario, Canada. We systematically collected caterpillars using burlap bands at sites with and without histories of gypsy moth outbreak, and then reared these caterpillars until potential parasitoid emergence. This procedure allowed us to generate quantitative food webs describing caterpillar-parasitoid interactions. We estimated the degree of parasitoid sharing between gypsy moth and native caterpillars. We also statistically modeled the effect of gypsy moth outbreak history and current gypsy moth abundance on standard indices of quantitative food web structure and the diversity of parasitoid communities. Rates of gypsy moth parasitism were very low and gypsy moth shared very few parasitoids with native caterpillars, suggesting limited potential for indirect interactions. We did not detect any significant effects of gypsy moth on either food web structure or parasitoid diversity, and the small amount of parasitoid sharing strongly implies that this lack of significance is not merely due to low statistical power. Our study suggests that gypsy moth has limited impact on native host-parasitoid food webs, at least for species that use burlap bands. Our results emphasize that extrapolations of theoretical and experimental conclusions on the impacts of invasive species should be tested in natural settings.

The quantitative mapping of food web flows based on empirical data is a crucial yet difficult task in ecology. The difficulty arises from the under-sampling of food webs, because most data sets are incomplete and uncertain. In this article, we review methods to quantify food web flows based on empirical data using linear inverse models (LIM). The food web in a LIM is described as a linear function of its flows, which are estimated from empirical data by inverse modeling. The under-sampling of food webs implies that infinitely many different solutions exist that are consistent with a given data set. The existing approaches to food web LIM select a single solution from this infinite set by invoking additional assumptions: either a specific selection criterion that has no solid ecological basis is used or the data set is artificially upgraded by assigning fixed values to, for example, physiological parameters. Here, we advance a likelihood approach (LA) that follows a different solution philosophy. Rather than singling out one particular solution, the LA generates a large set of possible solutions from which the marginal probability density function (mPDF) of each flow and correlations between flows can be derived. The LA is exemplified with an example model of a soil food web and is made available in the open-source R-software. Moreover, we show how stoichiometric data, stable isotope signatures, and fatty acid compositions can be included in the LIM to alleviate the under-sampling problem. Overall, LIM prove to be a powerful tool in food web research, which can bridge the gap between empirical data and the analysis of food web structures.

Food web research is rapidly expanding through study of natural fractional abundance of 15N in individual amino acids. This paper overviews the principles of this isotope approach, and from my perspective, reanalyzes applications, and further extends the discussion. It applies kinetic isotope effects that enriches 15N in certain amino acids associated with the metabolic processes, which was clearly demonstrated by observations of both natural ecosystem and laboratory experiments. In trophic processes 'trophic amino acids' such as glutamic acid that significantly enrich 15N, whereas 'source amino acids' such as phenylalanine and methionine show little 15N enrichment. Through various applications conducted over the years, the principles of the method have shown to operate well and disentangle complex food webs and relevant problems. Applications include food chain length estimate, nitrogen resource assessment, tracking fish migration, and reconstruction of paleodiet. With this approach, considerations of a wide range of classical issues have been reinvigorated, while in the same time, new challenging frontiers are emerging.

Although more consensus is now emerging on the magnitude and frequency of cascading trophic effects in aquatic communities, the debate over their terrestrial counterparts continues. We used meta-analysis to analyze field experiments on trophic cascades in terrestrial arthropod-dominated food webs to evaluate the overall magnitude of trophic cascades and conditions affecting their occurrence and strength. We found extensive support for the presence of trophic cascades in terrestrial communities. In the majority of experiments, predator removal led to increased densities of herbivorous insects and higher levels of plant damage. Cascades in which removing predators led to decreased herbivory also were detected but were less frequent and weaker, suggesting a predominantly three-trophic-level behavior of arthropod-dominated terrestrial food webs. Despite the clear evidence that cascades often decreased plant damage, residual effects of predation produced either no or only minimal changes in overall plant biomass. Agricultural systems and natural communities exhibited similarly strong effects of predation on herbivore abundance. However, resulting effects on plant damage and community-wide effects of trophic cascades on plant biomass usually were highly variable, and only in the managed agricultural systems did predators occasionally have strong indirect effects on plant biomass. Our meta-analysis suggests that the effects of trophic cascades on the biomass of primary producers are weaker in terrestrial than aquatic food webs.

Ecologists seek to understand the ways that human activities are altering the structures and processes that support biodiversity and nature's contributions to people. Food web research at the interface of community and ecosystem ecology is promising in this regard. An industry of studies has utilized stable isotopes in recent decades to rapidly characterize energy and material transfer among organisms in freshwater food webs. Nevertheless, these efforts have been somewhat siloed and mainly locally-based, and lack of a centralized database has limited efforts to tackle questions about food web change using isotopes at a global scale. Here we present IsoFresh, a freshwater food web database that contains species-level carbon (δ13C) and nitrogen (δ15N) stable isotope values for 15343 organisms, representing 1001 food webs and including > 1600 fish species and associated potential prey, from 65 countries around the globe. Our hope is that IsoFresh is used to explore fundamental and applied food web questions, contributing new knowledge about global environmental change so that human societies can better conserve and manage freshwater ecosystems along desirable future trajectories.