Disturbance is the primary determinant of food chain length when the top predator is constant

The number of trophic transfers occurring between basal resources and top predators, food chain length (FCL), varies widely in the world's ecosystems for reasons that are poorly understood, particularly for stream ecosystems. Available evidence indicates that FCL is set by energetic constraints, environmental stochasticity, or ecosystem size effects, although no single explanation has yet accounted for FCL patterns in a broad sense. Further, whether environmental disturbance can influence FCL has been debated on both theoretical and empirical grounds for quite some time. Using data from sixteen South Island, New Zealand streams, we determined whether the so-called ecosystem size, disturbance, or resource availability hypotheses could account for FCL variation in high country fluvial environments. Stable isotope-based estimates of maximum trophic position ranged from 2.6 to 4.2 and averaged 3.5, a value on par with the global FCL average for streams. Model-selection results indicated that stream size and disturbance regime best explained across-site patterns in FCL, although resource availability was negatively correlated with our measure of disturbance; FCL approached its maximum in large, stable springs and was <3.5 trophic levels in small, fishless and/or disturbed streams. Community data indicate that size influenced FCL, primarily through its influence on local fish species richness (i.e., via trophic level additions and/or insertions), whereas disturbance did so via an effect on the relative availability of intermediate predators (i.e., predatory invertebrates) as prey for fishes. Overall, our results demonstrate that disturbance can have an important food web-structuring role in stream ecosystems, and further imply that pluralistic explanations are needed to fully understand the range of structural variation observed for real food webs.

食物链长度远因与近因研究进展综述

Disturbance and productivity are potentially interacting factors often thought to underlie the complexity of aquatic food webs. We tested predictions about the effects of disturbance (bed movement, total water column freezing) and productivity (as indicated by primary consumer biomass) on the structure of 19 stream food webs in arctic Alaska. We predicted that food webs subject to high levels of disturbance would have low connectance, low linkage density, and short food chains, while food webs of streams with more benign disturbance regimes would be more complex (i.e., a test of the “dynamic stability hypothesis”). We further predicted that food chain length would increase with productivity (i.e., testing the “resource‐availability hypothesis”). Connectance and linkage density were negatively related to bed movement but not to freezing. Food chain length was related to freezing but not to bed movement or productivity. The relationships among food chain length, freezing, and productivity were driven by the occurrence of fishless streams, which all froze during winter. Streams containing fish had longer food chains than fishless streams, and food chain length was positively related to productivity only when fishless streams were removed from analyses. Our results show that disturbance and productivity are codeterminants of stream food web complexity in the Arctic. Our data further suggest that colonization dynamics are an important factor controlling food web structure, highlighting the importance of idiosyncratic habitat and life history related factors that are often overlooked in theoretical studies.

食物链长度理论研究进展

There are three hypothesized controls on food-chain length (FCL): energy supply (or "resource availability"), ecosystem size and disturbance (or "environmental variation"). In this article, the evidence for controls on FCL in freshwater ecosystems is evaluated. First, the various ways FCL can be measured are defined. Food-chain length typically is estimated as (1) connectance-based FCL--an average connectance between basal resources and top consumers, (2) functional FCL--by experimental determination of functionally significant effects of a top predator on lower trophic-level biomass patterns, and (3) realized FCL--an average connectance measure weighted by energy flow between basal consumers and the consumer occupying the maximum trophic position in the food web. Second, all evidence for relationships between the three hypothetical controls and FCL in freshwater ecosystems are evaluated. The review includes studies from streams, lakes, ponds, wetlands, phytotelmata, and experimental containers. Surprisingly, few studies of FCL in freshwaters that test the same suite of controls using the same methods are found. Equally compelling results arise from case studies based on functional, realized, and connectance-based measures of FCL. Third, 10 rules of thumb that could increase similarity of future studies, thereby facilitating synthesis across systems, are suggested. Fourth, it is discussed how FCL influences the concentration of contaminants in large-bodied animals (many of which are consumed by humans) as well as the efficacy of biocontrol applications in agriculture. Finally, there is a discussion of the potential relationships between global climate change, hydrology, and FCL in freshwaters.

Food web structure is paramount in regulating a variety of ecologic patterns and processes, although food web studies are limited by poor empirical descriptions of inherently complex systems. In this study, stable isotope ratios (δ15N and δ13C) were used to quantify trophic relationships and food chain length (measured as a continuous variable) in 14 Ontario and Quebec lakes. All lakes contained lake trout as the top predator, although lakes differed in the presumed number of trophic levels leading to this species. The presumed number of trophic levels was correlated with food chain length and explained 40% of the among‐lake variation. Food chain length was most closely related to fish species richness ($$r^{2}=0.69$$) and lake area ($$r^{2}=0.50$$). However, the two largest study lakes had shorter food chains than lakes of intermediate size and species richness, producing hump‐shaped relationships with food chain length. Lake productivity was not a powerful predictor of food chain length ($$r^{2}=0.36$$), and we argue that productive space (productivity multiplied by area) is a more accurate measure of available energy. This study addresses the need for improved food web descriptions that incorporate information about energy flow and the relative importance of trophic pathways.

Food web structure is paramount in regulating a variety of ecologic patterns and processes, although food web studies are limited by poor empirical descriptions of inherently complex systems. In this study, stable isotope ratios (δ15N and δ13C) were used to quantify trophic relationships and food chain length (measured as a continuous variable) in 14 Ontario and Quebec lakes. All lakes contained lake trout as the top predator, although lakes differed in the presumed number of trophic levels leading to this species. The presumed number of trophic levels was correlated with food chain length and explained 40% of the among-lake variation. Food chain length was most closely related to fish species richness ([Formula: see text]) and lake area ([Formula: see text]). However, the two largest study lakes had shorter food chains than lakes of intermediate size and species richness, producing hump-shaped relationships with food chain length. Lake productivity was not a powerful predictor of food chain length ([Formula: see text]), and we argue that productive space (productivity multiplied by area) is a more accurate measure of available energy. This study addresses the need for improved food web descriptions that incorporate information about energy flow and the relative importance of trophic pathways.

Food chain length (FCL) represents a fundamental metric within ecology because it has implications for ecosystem function and responses to environmental change. Omnivory between linked food chains situated within large ecosystems can increase FCL, whereas overlap of food chains within small or spatially compressed ecosystems is generally thought to decrease FCL. Yet FCL varies widely in small ecosystems and the mechanisms underlying determinants of FCL in these systems is unclear. In small shallow lakes, littoral structure is a predictor of FCL but it is unclear whether this is due to productivity or refuge mechanisms. Here we provide evidence, using consumer resource food web modules parameterized with empirical data, that refuge in spatially compressed ecosystems has the ability on its own to increase the trophic position of top predators by increasing the biomass of top and intermediate predators across a range of common food web module structures. Our results suggest that refuge is an important driver of FCL in small ecosystems, which has implications for determining responses of these systems to environmental change.

The determinants of food chain length (FCL), a crucial aspect of biodiversity due to its effects on ecosystem functioning, have long been debated. Previous studies proposed resource availability, disturbance, and ecosystem size as environmental drivers. However, studies using stable isotope approaches have shown inconsistent results, indicating missing links between environmental drivers and FCL. Here, we hypothesized that species richness and motifs (i.e. three‐species subgraphs) modulated environmental effects on FCL. Combining empirical food webs with our N‐species food web model, we found that FCL disproportionately changed at low species richness, with saturation at high species richness. This functional response was essential to the interdependent effects of disturbance and ecosystem size in our model. Disturbance more strongly regulated FCL in smaller ecosystems, where species richness was low. Similarly, increasing ecosystem size enhanced FCL under strong, but not weak, disturbance regimes. Our study suggests that internal food web structure should deepen our understanding of how FCL changes over environments.

The trophic structure of pelagic communities in lakes of glaciated regions is highly variable due to restricted dispersal of glacial relict taxa and recent species introductions. Much of the enormous between-lake variability in PCB levels in lake trout flesh (15–10 000 ng/g) from the St. Lawrence system results from differences in the length of pelagic food chains. Ontario Ministry of the Environment data (1978–81) on PCB concentrations in lake trout flesh indicate that PCB concentrations increased with the length of the food chain and tissue lipid content, and decreased with distance north of urban-industrial centres. Each trophic level contributed about a 3.5-fold biomagnification factor to the PCB concentrations in the trout, and the lipid content of the trout flesh increased by a factor of 1.5 for each additional trophic level. An empirical model capable of predicting PCB levels in pelagic salmonids and forage fish (smelt and coregonids) indicated that biomagnification of small atmospheric inputs of persistent lipophilic contaminants can explain the frequent occurrence of high levels of contaminants in some biota from remote areas, and that species introductions that lengthen food chains will lead to significant increases in levels of atmospherically dispersed persistent organic contaminants in top predators.

Mercury biomagnification in three geothermally-influenced lakes differing in chemistry and algal biomass

The effects of energy on food web structure have been debated for at least 80 years. Nevertheless, the empirical evidence is meager, especially from terrestrial ecosystems. We analyzed long‐term temporal variation in food chain length in a semiarid continental ecosystem, where productivity shows large interannual variations. Incidence of nonherbivorous prey in predator diet was used as a proxy of trophic position, allowing us to analyze the effect of productivity on food chain length within the assemblage of top predators (which comprises the most abundant and persistent top predators in the system) and to compare observed patterns at the species and assemblage levels. At the species level, the relationship between trophic position and productivity took different forms, varying in magnitude and shape. This pattern contrasts with the consistent increase in food chain length, with productivity observed at the assemblage level. Our results indicate that productivity can be a main determinant of food chain length, but not necessarily because of energy limitation. Further, the increase in food chain length with available energy probably represents an aggregate attribute, driven to a large extent by predators with higher consumption rates, rather than being the result of compensatory responses among predators.

The effects of energy on food web structure have been debated for at least 80 years. Nevertheless, the empirical evidence is meager, especially from terrestrial ecosystems. We analyzed long-term temporal variation in food chain length in a semiarid continental ecosystem, where productivity shows large interannual variations. Incidence of nonherbivorous prey in predator diet was used as a proxy of trophic position, allowing us to analyze the effect of productivity on food chain length within the assemblage of top predators (which comprises the most abundant and persistent top predators in the system) and to compare observed patterns at the species and assemblage levels. At the species level, the relationship between trophic position and productivity took different forms, varying in magnitude and shape. This pattern contrasts with the consistent increase in food chain length, with productivity observed at the assemblage level. Our results indicate that productivity can be a main determinant of food chain length, but not necessarily because of energy limitation. Further, the increase in food chain length with available energy probably represents an aggregate attribute, driven to a large extent by predators with higher consumption rates, rather than being the result of compensatory responses among predators.

Food chain length provides insights into how ecosystems function and respond to global change. A recent synthesis has shown that food chain length is significantly related to both ecosystem productivity and ecosystem size. Relaxation of energetic constraints on top predators has been advanced as the primary mechanism explaining the importance of ecosystem productivity whereas the significance of ecosystem size may be related to the fact that larger ecosystems provide more refuge that stabilizes intermediate predators. Given that submerged macrophytes in lakes are known to enhance both ecosystem productivity and the amount of available refuge, we hypothesized that food chain lengths, measured as the trophic positions of top predators, would be significantly related to macrophyte biomass. We tested our hypothesis by conducting a field survey of shallow lakes across a strong macrophyte but limited morphometric gradient using a hierarchical mixed effect modeling approach. We determined that macrophyte biomass was positively related to the trophic position of numerous piscivores and to food chain length across lakes. Both lake volume and macrophyte biomass were retained as fixed predictors in our model with lowest AICc, and this model explained 85% of the variation in piscivorous fish trophic positions considering both fixed and random effects (i.e., lake and species‐specific responses to lake volume). Macrophyte biomass explained 29% of the residual variation in food chain length when the effect of lake volume was removed. These results are the first to directly relate macrophyte biomass to piscivore trophic positions and food chain length. We conclude that shallow lakes with higher macrophyte biomass support longer food chains independent of ecosystem size and nutrient concentration. We suggest that loss of macrophytes largely driven by human activities reduces food chain length, with potential consequences for ecosystem function.

Streams experience frequent natural disturbance and are undergoing considerable anthropogenic disturbance due to dam construction and water diversion. Disturbance is known to impact community structure, but its effect on food chain length is still a matter of considerable debate. Theoretical models show that longer food chains are less resilient to disturbance, so food chain length is predicted to be shorter following a disturbance event. Here we experimentally test the effect of disturbance on food chain length in streams by diverting stream flow. We found that our experimental low-flow disturbance did not alter food chain length. We did see an effect on body-size structure in our food webs suggesting that food chain length may be an insensitive indicator of disturbance. We suggest that habitat heterogeneity and food web complexity buffer the effect of disturbance on food chain length. The theoretical predictions of disturbance on food chain length are only likely to be seen in homogeneous systems that closely approximate the linear food chains the models are based upon.