Lake to land subsidies: experimental addition of aquatic insects increases terrestrial arthropod densities

Aquatic insects are a common and important subsidy to terrestrial systems, yet little is known about how these inputs affect terrestrial food webs, especially around lakes. Myvatn, a lake in northern Iceland, has extraordinary midge (Chironomidae) emergences that result in large inputs of biomass and nutrients to terrestrial arthropod communities. We simulated this lake-to-land resource pulse by collecting midges from Myvatn and spreading their dried carcasses on 1-m2 plots at a nearby site that receives very little midge deposition. We hypothesized a positive bottom-up response of detritivores that would be transmitted to their predators and would persist into the following year. We sampled the arthropod community once per month for two consecutive summers. Midge addition resulted in significantly different arthropod communities and increased densities of some taxa in both years. Detritivores, specifically Diptera larvae, Collembola, and Acari increased in midge-addition plots, and so did some predators and parasitoids. Arthropod densities were still elevated a year after midge addition, and two years of midge addition further increased the density of higher-order consumers (e.g., Coleoptera and Hymenoptera). Midge addition increased arthropod biomass by 68% after one year and 108% after two years. By manipulating the nutrient pulse delivered by midges we were able to elucidate food web consequences of midge deposition and spatial and temporal dynamics that are difficult to determine based on comparative approaches alone. Resources cross ecosystem boundaries and are assimilated over time because of life-history strategies that connect aquatic and terrestrial food webs and these systems cannot be fully understood in isolation from each other.     

The use of radioactive isotopes to measure the transfer of materials in aquatic food chains

Radioisotopes have been misused extensively by ecologists in transfer studies within food chains. Unless it is known that no recycling of isotope has occurred during the experiment, the assumption of linear uptake when in fact the system is not linear, even over short periods, can lead to significant errors in the estimation of ingestion or feeding. If recycling occurs, at least a 3 or 4-compartment, hydraulic-type model is necessary to even approximate the complicated kinetics of isotopic transfer in a simple aquatic feeding experiment. In any event, it is essential to follow the uptake or loss of an isotope (change in specific activity) as a function of time in at least 1 compartment before deciding on an appropriate model. If experiments are designed so that the maximum number of rate processes are summed or integrated by the animal, the kinetics can be considerably simplified. If the food supply is uniformly labelled, the rate of change of tracer can be used to give a rate of ingestion (grazing). If the predator is labelled with a suitable isotope before starting the experiment, the rate of loss of its isotope burden under different experimental conditions can be used to determine respiration or excretion rates, turnover rates, ingestion, and the size and number of major compartments in the transfer system.Bedford Institute Contribution. Woods Hole Oceanographic Institution Contribution No. 2690.     

Response of complex food webs to realistic extinction sequences

Although an ecosystem's response to biodiversity loss depends on the order in which species are lost, the extinction sequences generally used to explore such responses in food webs have been ecologically unrealistic. We investigate how several extinction orders affect the minimum number of secondary extinctions expected within pelagic food webs from 34 temperate freshwater lakes. An ecologically plausible extinction order is derived from the geographically nested pattern of species composition among the lakes and is corroborated by species' pH tolerances. Simulations suggest that lake communities are remarkably robust to this realistic extinction order and highly sensitive to the reverse sequence of species loss. This sensitivity is not well explained by the known sensitivity of networks to the loss of highly connected species but appears to be better explained by our observation that trophic specialists preferentially consume widely distributed species at low risk of extinction. Our results highlight an important aspect of community organization that may help to maintain biodiversity amidst changing environments.     

Origin of compartmentalization in food webs

The response of an ecosystem to perturbations is mediated by both antagonistic and facilitative interactions between species. It is thought that a community's resilience depends crucially on the food web--the network of trophic interactions--and on the food web's degree of compartmentalization. Despite its ecological importance, compartmentalization and the mechanisms that give rise to it remain poorly understood. Here we investigate several definitions of compartments, propose ways to understand the ecological meaning of these definitions, and quantify the degree of compartmentalization of empirical food webs. We find that the compartmentalization observed in empirical food webs can be accounted for solely by the niche organization of species and their diets. By uncovering connections between compartmentalization and species' diet contiguity, our findings help us understand which perturbations can result in fragmentation of the food web and which can lead to catastrophic effects. Additionally, we show that the composition of compartments can be used to address the long-standing question of what determines the ecological niche of a species.     

Nutrient subsidies to belowground microbes impact aboveground food web interactions

Historically, terrestrial food web theory has been compartmentalized into interactions among aboveground or belowground communities. In this study we took a more synthetic approach to understanding food web interactions by simultaneously examining four trophic levels and investigating how nutrient (nitrogen and carbon) and detrital subsidies impact the ability of the belowground microbial community to alter the abundance of aboveground arthropods (herbivores and predators) associated with the intertidal cord grass Spartina alterniflora. We manipulated carbon, nitrogen, and detrital resources in a field experiment and measured decomposition rate, soil nitrogen pools, plant biomass and quality, herbivore density, and arthropod predator abundance. Because carbon subsidies impact plant growth only indirectly (microbial pathways), whereas nitrogen additions both directly (plant uptake) and indirectly (microbial pathways) impact plant primary productivity, we were able to assess the effect of both belowground soil microbes and nutrient availability on aboveground herbivores and their predators. Herbivore density in the field was suppressed by carbon supplements. Carbon addition altered soil microbial dynamics (net potential ammonification, litter decomposition rate, DON [dissolved organic N] concentration), which limited inorganic soil nitrogen availability and reduced plant size as well as predator abundance. Nitrogen addition enhanced herbivore density by increasing plant size and quality directly by increasing inorganic soil nitrogen pools, and indirectly by enhancing microbial nitrification. Detritus adversely affected aboveground herbivores mainly by promoting predator aggregation. To date, the effects of carbon and nitrogen subsidies on salt marshes have been examined as isolated effects on either the aboveground or the belowground community. Our results emphasize the importance of directly addressing the soil microbial community as a factor that influences aboveground food web structure by affecting plant size and aboveground plant nitrogen.     

Using stable isotopes to monitor anthropogenic nitrogen inputs to estuaries

Use of stable nitrogen isotope ratios is one method that has been proposed to indicate anthropogenic nutrient enrichment in estuarine systems. However, the role of stable isotopes as a tool in long-term ecosystem monitoring has not been fully developed. Resident producer and consumer species were collected from marshes dominated by Spartina alterniflora and subject to a range of anthropogenic impacts in Cape Cod, Massachusetts, and in Great South Bay and Jamaica Bay, New York. Tissue isotope ratios of Spartina alterniflora, Ulva lactuca, Fundulus heteroclitus, and Geukensia demissa were analyzed in order to determine which organisms are the most sensitive indicators of changes in anthropogenic nitrogen source and loading. Power analysis was used to determine the sample sizes necessary to detect change in nutrient source using the species sampled. Relationships between the delta15N values of the species sampled and watershed population density and residential development were evaluated. Population density was a better indicator of anthropogenic nitrogen impact than residential development, since most anthropogenic nitrogen in the study marshes was derived from wastewater. Consumer species demonstrated lower within-site variability than producer species and would therefore require smaller sample sizes to detect changes in nitrogen source and loading.     

Diverging response patterns of terrestrial and aquatic species to hydromorphological restoration

Although experiences with ecological restoration continue to accumulate, the effectiveness of restoration for biota remains debated. We complemented a traditional taxonomic analysis approach with information on 56 species traits to uncover the responses of 3 aquatic (fish, macroinvertebrates, macrophytes) and 2 terrestrial (carabid beetles, floodplain vegetation) biotic groups to 43 hydromorphological river restoration projects in Germany. All taxonomic groups responded positively to restoration, as shown by increased taxonomic richness (10–164%) and trait diversity (habitat, dispersal and mobility, size, form, life history, and feeding groups) (15–120%). Responses, however, were stronger for terrestrial than aquatic biota, and, contrary to our expectation, taxonomic responses were stronger than those of traits. Nevertheless, trait analysis provided mechanistic insights into the drivers of community change following restoration. Trait analysis for terrestrial biota indicated restoration success was likely enhanced by lateral connectivity and reestablishment of dynamic processes in the floodplain. The weaker response of aquatic biota suggests recovery was hindered by the persistence of stressors in the aquatic environment, such as degraded water quality, dispersal constraints, and insufficient hydromorphological change. Therefore, river restoration requires combined local- and regional-scale approaches to maximize the response of both aquatic and terrestrial organisms. Due to the contrasting responses of aquatic and terrestrial biota, the planning and assessment of river restoration outcomes should consider effects on both components of riverine landscapes.     

A simulation analysis of continental shelf food webs

Energy flow through continental shelf food webs was examined using a simulation model. The model structure expands the two traditional marine food chains of phytoplankton-zooplankton-pelagic fish and benthos-demersal fish into a complex web which includes detritus, dissolved organic matter (DOM), bacteria, protozoa, and mucus net feeders. Simulation of energy flux for different shelf systems using the expanded web revealed that heterotrophic microorganisms and their predators account for a significant component of the energy flux in the continental shelf ecosystem. Contrary to previous models, where all phytoplankton were considered to be grazed by zooplankton, our simulation results indicate that only slightly more than 50% of the annual net primary production is grazed. A substantial quantity of the phytoplankton production directly becomes detritus. Bacteria mineralize detritus and DOM produced by phytoplankton and other components of the food web, converting these to biomass with high efficiency. Consequently, the model predicts that planktonic bacterial production is equivalent to zooplankton production. Exclusion of the bacteria requires the assumption that all DOM is either exported from the system or consumed by another component of the food web. Neither of these assumptions can be supported by present knowledge of the dynamics of DOM in the sea. Model simulations were also employed to test the hypothesis that production exceeds consumption on continental shelves, resulting in exports of 50% of the annual primary production. Simulations of shelves with high rates of primary production resulted in a particulate export of 27% and realistic estimates of secondary production. Results of other simulations suggest that shelves with lower primary production cannot export production and still maintain the macrobenthos and their predators. General properties about continental shelves can also be inferred from the model. From simulations of shelves of differing primary production, nanoplankton are predicted to account for a greater proportion of the primary production in nutrient limited systems. Benthic production appears to be related to both the quantity of primary production and the sinking rates of the phytoplankton. The model indicates that zooplankton fecal inputs to the shelf benthos are only a small portion of the total detrital flux, leading to the prediction that fecal pellets are of little significance in determining benthic production. Finally, the model generates production efficiencies that are highly variable depending on the type of system and kind of populations involved. We argue that the assumed ecological efficiency of 10% should be abandoned for continental shelves and other ecosystems.     

Historical metal concentrations in lacustrine food webs revealed using fossil ephippia from Daphnia.

Metal contamination of freshwater ecosystems is increasingly prevalent due to anthropogenic activities such as metal smelting and fossil fuel combustion. While toxicological studies focus on aqueous metal concentrations that result in lethal or sublethal responses, currently the only method for reconstructing a lake's metal contamination history is through an examination of the sedimentary deposits. In this paper, we suggest that cladoceran diapausing eggs (ephippia), which are abundant in nature and accumulate maternally derived metals, can be used to measure historical variations in biologically relevant metals that derive from the water column (water, diet). Linear regressions of total metal content against ephippia density or mass were strong (R2 > 0.80, P < 0.04) and revealed that metals were incorporated into ephippia with little contamination from the sediment matrix. Comparison of metal concentrations in ephippia and bulk sediments from three lakes demonstrated that some metals associated with urban sources (Cd, Cr, Mo) were preferentially concentrated in ephippia, whereas concentrations of other metals indicating landscape erosion (Al, Ca, Fe, Mn) exhibited greater concentrations in bulk sediments than in diapausing eggs. Because historical changes in metals within fossils and bulk sediments were uncorrelated in most instances, past variation in the metal content of ephippia provided a unique history of food web exposure to metals in the water column.     

Coupling stable isotopes with bioenergetics to estimate interspecific interactions.

Interspecific interactions are often difficult to elucidate, particularly with large vertebrates at large spatial scales. Here, we describe a methodology for estimating interspecific interactions by combining stable isotopes with bioenergetics. We illustrate this approach by modeling the population dynamics and species interactions of a suite of vertebrates on Santa Cruz Island, California, USA: two endemic carnivores (the island fox and island spotted skunk), an exotic herbivore (the feral pig), and their shared predator, the Golden Eagle. Sensitivity analyses suggest that our parameter estimates are robust, and natural history observations suggest that our overall approach captures the species interactions in this vertebrate community. Nonetheless, several factors provide challenges to using isotopes to infer species interactions. Knowledge regarding species-specific isotopic fractionation and diet breadth is often lacking, necessitating detailed laboratory studies and natural history information. However, when coupled with other approaches, including bioenergetics, mechanistic models, and natural history, stable isotopes can be powerful tools in illuminating interspecific interactions and community dynamics.     

Bat-cave catchment areas: using stable isotopes (deltaD) to determine the probable origins of hibernating bats

The application of stable hydrogen isotope (deltaD) techniques has swiftly advanced our understanding of animal movements, but this progression is dominated by studies of birds and relatively long-distance, north-south migrants. This dominance reflects the challenge of incorporating multiple sources of error into geographic assignments and the nature of spatially explicit deltaD models, which possess greater latitudinal than longitudinal resolution. However, recent progress in likelihood-based assignments that incorporate multiple sources of isotopic error and Bayesian approaches that include additional sources of information may advance finer-scale understanding of animal movements. We develop a stable-isotope method for determining probable origins of bats within hibernacula and show that this method produces spatially explicit, continuous assignments with regional resolution. We outline how these assignments can be used to infer hibernacula connectivity, an application that could inform spatial modeling of white-nose syndrome. Additionally, estimates of seasonal and annual flight distances for many cave-dwelling bat species can be derived from this approach. We also discuss how this application can be used in general to provide insights into variable migratory and foraging strategies within bat populations.     

Multiple anthropogenic stressors and the structural properties of food webs

Coastal environments are among the most productive on the planet, providing a wide range of ecosystem services. Development and exploitation mean that they are faced with stresses from a number of anthropogenic sources. Such stresses are typically studied in isolation, but multiple stressors can combine in unexpected ways to alter the structure of ecological systems. Here, we experimentally explore the impacts of inorganic nutrients and organic matter on a range of food web properties. We find that these two stressors combine additively to produce significant increases in connectance and mean food chain length. Such increases are typically associated with enhanced robustness to secondary extinctions and productivity, respectively. Despite these apparent beneficial effects, we find a simplification of web structure in terms of taxon richness and diversity, and altered proportions of basal and top species. These effects are driven by a reduction in community assembly and lower consistency in a range of system properties as a result of the multiple stressors. Consequently, impacted food webs are likely to be more vulnerable to human- or climate-induced perturbations in the long-term.     

Using stable isotopes to reveal shifts in prey consumption by generalist predators.

The effectiveness of generalist predators in biological control may be diminished if increased availability of alternative prey causes individual predators to decrease their consumption of crop pests. Farming practices that enhance densities of microbidetritivores in the detrital food web can lead to increased densities of generalist predators that feed on pest species. The ability to predict the net biocontrol impact of increased predator densities depends upon knowing the extent to which individual predators may shift to detrital prey and feed less on crop pests when prey of the detritus-based food web are more abundant. We addressed this question by comparing ratios of stable isotopes of carbon (delta13C) and nitrogen (delta15N) in generalist ground predators and two types of prey (crop pests and microbidetritivores) in replicated 8 x 8 m cucurbit gardens subjected to one of two treatments: a detrital subsidy or no addition of detritus (control). Small sheet-web spiders (Linyphiidae) and small wolf spiders (Lycosidae) had delta13C values similar to those of Collembola in both the detrital and control treatments, indicating that small spiders belong primarily to the detrital food web. In control plots the larger generalist predators had delta13C values similar to those of the major insect pests, consistent with their known effectiveness as biocontrol agents. Adding detritus may have caused delta13C of one species of large wolf spider to shift toward that of the microbi-detritivores, although evidence is equivocal. In contrast, another large wolf spider displayed no shift in delta13C in the detrital treatment. Thus, stable isotopes revealed which generalist predators will likely continue to feed on pest species in the presence of greater densities of alternative prey.     

Trophic structure of coastal Antarctic food webs associated with changes in sea ice and food supply

Predicting the dynamics of ecosystems requires an understanding of how trophic interactions respond to environmental change. In Antarctic marine ecosystems, food web dynamics are inextricably linked to sea ice conditions that affect the nature and magnitude of primary food sources available to higher trophic levels. Recent attention on the changing sea ice conditions in polar seas highlights the need to better understand how marine food webs respond to changes in such broad-scale environmental drivers. This study investigated the importance of sea ice and advected primary food sources to the structure of benthic food webs in coastal Antarctica. We compared the isotopic composition of several seafloor taxa (including primary producers and invertebrates with a variety of feeding modes) that are widely distributed in the Antarctic. We assessed shifts in the trophic role of numerically dominant benthic omnivores at five coastal Ross Sea locations. These locations vary in primary productivity and food availability, due to their different levels of sea ice cover, and proximity to polynyas and advected primary production. The delta15N signatures and isotope mixing model results for the bivalves Laternula elliptica and Adamussium colbecki and the urchin Sterechinus neumeyeri indicate a shift from consumption of a higher proportion of detritus at locations with more permanent sea ice in the south to more freshly produced algal material associated with proximity to ice-free water in the north and east. The detrital pathways utilized by many benthic species may act to dampen the impacts of large seasonal fluctuations in the availability of primary production. The limiting relationship between sea ice distribution and in situ primary productivity emphasizes the role of connectivity and spatial subsidies of organic matter in fueling the food web. Our results begin to provide a basis for predicting how benthic ecosystems will respond to changes in sea ice persistence and extent along environmental gradients in the high Antarctic.     

Quantitative approaches to the analysis of stable isotope food web data

Ecologists use stable isotopes (delta13C, delta15N) to better understand food webs and explore trophic interactions in ecosystems. Traditionally, delta13C vs. delta15N bi-plots have been used to describe food web structure for a single time period or ecosystem. Comparisons of food webs across time and space are increasing, but development of statistical approaches for testing hypotheses regarding food web change has lagged behind. Here we present statistical methodologies for quantitatively comparing stable isotope food web data. We demonstrate the utility of circular statistics and hypothesis tests for quantifying directional food web differences using two case studies: an arthropod salt marsh community across a habitat gradient and a freshwater fish community from Lake Tahoe, USA, over a 120-year time period. We calculated magnitude and mean angle of change (theta) for each species in food web space using mean delta13C and delta15N of each species as the x, y coordinates. In the coastal salt marsh, arthropod consumers exhibited a significant shift toward dependence on Spartina, progressing from a habitat invaded by Phragmites to a restored Spartina habitat. In Lake Tahoe, we found that all species from the freshwater fish community shifted in the same direction in food web space toward more pelagic-based production with the introduction of nonnative Mysis relicta and onset of cultural eutrophication. Using circular statistics to quantitatively analyze stable isotope food web data, we were able to gain significant insight into patterns and changes in food web structure that were not evident from qualitative comparisons. As more ecologists incorporate a food web perspective into ecosystem analysis, these statistical tools can provide a basis for quantifying directional food web differences from standard isotope data.     

Sources of primary production supporting food webs in an arid coastal embayment

Penaeid shrimp can be useful ecological indicators of linkages between shallow tropical coastal habitats, acting as integrators of carbon and nitrogen sources due to their generalist feeding habits and their mobility between habitats and with tidal cycles. In the current study, the contribution of mangrove, seagrass and microbial mat to the nutrition of two penaeid shrimp species, Penaeus semisulcatus and Metapeneus ensis, in a shallow arid embayment in the Arabian Gulf was assessed through a combination of analysis of stomach contents and dual carbon and nitrogen stable isotope signatures. Shrimp tissue stable isotope signatures identified seagrass as a major source of carbon and nitrogen for both species, contributing 21–38?% (1–99?‰). Microbial mat was also detected as a significant nutritional source for early-stage Metapenaeus affinis postlarvae (1–27?%). However, mangroves were not identified as a significant source, with the range of results including the possibility of a zero contribution. Moreover, the greatest possible contribution of mangroves as source of carbon was less than for the other primary producers. This may be due the high salinity and wide temperature range limiting mangrove productivity as well as the low export of dissolved and particulate organic material out of the mangroves due to low rainfall.     

Regulation of intertidal food webs by avian predators on New England rocky shores

Although there is a large body of research on food webs in rocky intertidal communities, most of the emphasis has been on the marine benthic components. Effects of avian predation on highly mobile predators such as crabs, remains practically unstudied in rocky shore ecosystems. The crab, Cancer borealis, is an important component of the diet of gulls (Larus marinus, L. argentatus) at the Isles of Shoals, Maine, USA. C. borealis prey include the predatory gastropod Nucella lapillus L., the herbivore Littorina littorea, and mussels Mytilus edulis L. We hypothesized that gulls reduce abundance of C. borealis in the low intertidal and shallow subtidal, thereby allowing C. borealis prey to persist in high numbers. A study of crab tidal migration showed that C. borealis density nearly doubled at high tide compared to low tide; thus, crabs from a large subtidal source population migrate into the intertidal zone during high tides and either emigrate or are removed by gulls during low tides. Results from a small-scale (1 m2) predator caging experiment in the low intertidal zone indicated that enclosed crabs significantly reduced L. littorea abundance when protected from gull predation. In a much larger-scale gull exclusion experiment, densities of C. borealis increased significantly during low and high tides in exclosures relative to the controls. C. borealis density was inversely correlated with changes in the abundance of two mesopredators Carcinus maenas and Nucella lapillus, and with the space-occupier M. edulis. There was a similar negative correlation between abundance of C. borealis and the change in abundance of the herbivore L. littorea, but the trend was not significant. Mortality of tethered L. littorea was associated with C. borealis density across sites. However, preferred algae did not change in response to L. littorea density during the experiment. Thus, we found suggestive, but not conclusive, evidence for a three-level cascade involving gulls, crabs, and L. littorea. Our studies strongly suggest that gulls, as apex predators, generate three-level trophic cascades in rocky intertidal food webs by preventing the highly mobile subtidal predator, C. borealis, from establishing substantial populations in the low-mid intertidal zone thereby indirectly enhancing densities of two key mesopredators (N. lapillus, Carcinus) and blue mussels (M. edulis).