You are what your host eats: The trophic structure and food chain length of a symbiont community are coupled with the plastic diet of the host ant.

Food chain length provides key information on the flow of nutrients and energy in ecosystems. Variation in food chain length has primarily been explained by environmental drivers such as ecosystem size and productivity. Most insights are obtained from theory or aquatic systems, but the importance of these drivers remains largely untested in terrestrial systems. We exploited red wood ant nests markedly differing in size as natural experiments to quantify the drivers of trophic structure and food chain length of their symbiont arthropod communities. Using stable isotopes, we explored the variation in the trophic positions of four symbiont species with the trophic position of the top predator as a proxy for food chain length of the symbiont community. Nest size did not affect food chain length, nor trophic distance between the symbionts. Instead, food chain length and the trophic positions of the symbionts were strongly affected by the host's foraging decisions. When the host diet shifted from predominantly herbivorous to more predacious, the trophic position of the symbionts and food chain length strongly increased. We show for the first time that a food web can be structured by biotic interactions with an engineering species rather than by abiotic environmental variables.

Moving apart together: co-movement of a symbiont community and their ant host, and its importance for community assembly.

BACKGROUND: Species interactions may affect spatial dynamics when the movement of one species is determined by the presence of another one. The most direct species-dependence of dispersal is vectored, usually cross-kingdom, movement of immobile parasites, diseases or seeds by mobile animals. Joint movements of species should, however, not be vectored by definition, as even mobile species are predicted to move together when they are tightly connected in symbiont communities. METHODS: We studied concerted movements in a diverse and heterogeneous community of arthropods (myrmecophiles) associated with red wood ants. We questioned whether joint-movement strategies eventually determine and speed-up community succession. RESULTS: We recorded an astonishingly high number of obligate myrmecophiles outside red wood ant nests. They preferentially co-moved with the host ants as the highest densities were found in locations with the highest density of foraging red wood ants, such as along the network of ant trails. These observations suggest that myrmecophiles resort to the host to move away from the nest, and this to a much higher extent than hitherto anticipated. Interestingly, functional groups of symbionts displayed different dispersal kernels, with predatory myrmecophiles moving more frequently and further from the nest than detritivorous myrmecophiles. We discovered that myrmecophile diversity was lower in newly founded nests than in mature red wood ant nests. Most myrmecophiles, however, were able to colonize new nests fast suggesting that the heterogeneity in mobility does not affect community assembly. CONCLUSIONS: We show that co-movement is not restricted to tight parasitic, or cross-kingdom interactions. Movement in social insect symbiont communities may be heterogeneous and functional group-dependent, but clearly affected by host movement. Ultimately, this co-movement leads to directional movement and allows a fast colonisation of new patches, but not in a predictable way. This study highlights the importance of spatial dynamics of local and regional networks in symbiont metacommunities, of which those of symbionts of social insects are prime examples.

Monoculture-based consumer-resource models predict species dominance in mixed batch cultures of dinoflagellates.

Global change will disturb the frequency, scale and distribution of harmful algal blooms (HABs), but we are unable to predict future HABs due to our limited understanding of how physicochemical changes in the environment affect interspecific competition between dinoflagellates. Trait-based mechanistic modelling is an important tool to unravel and quantify various direct and indirect interactions between species. The present study explores whether MacArthur's consumer-resource model can be used as a viable base model to predict dinoflagellate growth in closed multispecies systems. To this end, two batch culture experiments (294 cultures in total) with monocultures and multispecies cultures of Alexandrium minutum, Prorocentrum lima, P. micans, Protoceratium reticulatum and Scrippsiella trochoidea were performed. Despite changes to the relative (different nitrate concentrations) and absolute nutrient availability (dilutions of L1 medium), P. micans outcompeted all other species in mixed cultures. Consumer-resource modelling parameterized using monoculture growth correctly predicted this species dominance (R² between 0.80 and 0.95). Parameter estimates revealed that P. micans had a faster uptake of nitrogen when compared to its competitors, but did not differ in resource efficiency and natural mortality rate. Yet, while the model accurately predicted community dynamics during the growth phase, it was not able to predict their dynamics beyond the point of quiescence. Consumer-resource modelling was shown to differentiate the roles of resource assimilation, resource efficiency, and natural mortality rates in batch culture experiments with minimal data requirements beyond common measurements. The results suggest that consumer-resource models provide a promising basis for trait-based modelling of interspecific competition between (harmful) algae.

Contrasting indirect effects of an ant host on prey-predator interactions of symbiotic arthropods.

Indirect interactions occur when a species affects another species by altering the density (density-mediated interactions) or influencing traits (trait-mediated interactions) of a third species. We studied variation in these two types of indirect interactions in a network of red wood ants and symbiotic arthropods living in their nests. We tested whether the ant workers indirectly affected survival of a symbiotic prey species (Cyphoderus albinus) by changing the density and/or traits of three symbiotic predators, i.e., Mastigusa arietina, Thyreosthenius biovatus and Stenus aterrimus, provoking, respectively, low, medium and high ant aggression. An ant nest is highly heterogeneous in ant worker density and the number of aggressive interactions towards symbionts increases with worker density. We, therefore, hypothesized that varying ant density could indirectly impact prey-predator interactions of the associated symbiont community. Ants caused trait-mediated indirect effects in all three prey-predator interactions, by affecting the prey capture rate of the symbiotic predators at different worker densities. Prey capture rate of the highly and moderately aggressed spider predators M. arietina and T. biovatus decreased with ant density, whereas the prey capture rate of the weakly aggressed beetle predator S. aterrimus increased. Ants also induced density-mediated indirect interactions as high worker densities decreased the survival rate of the two predatory spider species. These results demonstrate for the first time that a host can indirectly mediate the trophic interactions between associated symbionts. In addition, we show that a single host can induce opposing indirect effects depending on its degree of aggression towards the symbionts.

Theoretically exploring direct and indirect chemical effects across ecological and exposure scenarios using mechanistic fate and effects modelling.

Predicting ecosystem response to chemicals is a complex problem in ecotoxicology and a challenge for risk assessors. The variables potentially influencing chemical fate and exposure define the exposure scenario while the variables determining effects at the ecosystem level define the ecological scenario. In absence of any empirical data, the objective of this paper is to present simulations by a fugacity-based fate model and a differential equation-based ecosystem model to theoretically explore how direct and indirect effects on invertebrate shallow pond communities vary with changing ecological and exposure scenarios. These simulations suggest that direct and indirect effects are larger in mesotrophic systems than in oligotrophic systems. In both trophic states, interaction strength (quantified using grazing rates) was suggested a more important driver for the size and recovery from direct and indirect effects than immigration rate. In general, weak interactions led to smaller direct and indirect effects. For chemicals targeting mesozooplankton only, indirect effects were common in (simple) food-chains but rare in (complex) food-webs. For chemicals directly affecting microzooplankton, the dominant zooplankton group in the modelled community, indirect effects occurred both in food-chains and food-webs. We conclude that the choice of the ecological and exposure scenarios in ecotoxicological modelling efforts needs to be justified because of its influence on the prevalence and magnitude of the predicted effects. Overall, more work needs to be done to empirically test the theoretical expectations formulated here.

The ChimERA project: coupling mechanistic exposure and effect models into an integrated platform for ecological risk assessment.

Current techniques for the ecological risk assessment of chemical substances are often criticised for their lack of environmental realism, ecological relevance and methodological accuracy. ChimERA is a 3-year project (2013-2016), funded by Cefic's Long Range Initiative (LRI) that aims to address some of these concerns by developing and testing mechanistic fate and effect models, and coupling of these models into one integrated platform for risk assessment. This paper discusses the backdrop against which this project was initiated and lists its objectives and planned methodology.

Migration and opportunistic feeding increase PCB accumulation in Arctic seabirds.

It is widely accepted that body concentrations of persistent organic pollutants (POPs) tend to increase with trophic level (TL). Yet, little attention has been paid to the causes in the underlying differences in POP body concentrations between species occupying similar TLs. In this paper we use two modeling approaches to quantify the importance of migration and opportunistic feeding, relative to that of trophic level, in explaining interspecific differences in polychlorinated biphenyl (PCB) body concentrations between 6 Arctic seabird species breeding in the Barents Sea: Little Auk (Alle alle), Black Guillemot (Cepphus grylle), Brünnich's Guillemot (Uria lomvia), Common Eider (Somateria mollissima), Black-legged Kittiwake (Rissa tridactyla), and Glaucous Gull (Larus hyperboreus). As a first approach, we use additive models to analyze two independent data sets (n = 470 and n = 726). We demonstrate that migration, opportunistic feeding, and TL significantly (p < 0.001) increase PCB body concentrations by a factor 3.61-4.10, 2.66-20.95, and 2.38-2.41, respectively. Our second approach, using a mechanistic bioaccumulation model, confirmed these positive effects on the body burdens but suggested lower effects of migration, opportunistic feeding, and TL (1.55, 2.39, and 2.38) than did our statistical analysis. These two independent approaches demonstrate that the effects of migration and opportunistic feeding on seabird body burdens can be similar to that of an increase of one TL and should therefore be accounted for in future analyses.

Toxicity data for modeling impacts of oil components in an Arctic ecosystem.

Ecological impact assessment modeling systems are valuable support tools for managing impacts from commercial activities on marine habitats and species. The inclusion of toxic effects modeling in these systems is predicated on the availability and quality of ecotoxicology data. Here we report on a data gathering exercise to obtain toxic effects data on oil compounds for a selection of cold-water marine species of fish and plankton associated with the Barents Sea ecosystem. Effects data were collated from historical and contemporary literature resources for the endpoints mortality, development, growth, bioaccumulation and reproduction. Evaluating the utility and applicability of these data for modeling, we find that data coverage is limited to a sub-set of the required endpoints. There is a need for new experimental studies for zooplankton focused on the endpoints development and bioaccumulation and for larvae and juvenile fish focused on growth and development.

Using additive modelling to quantify the effect of chemicals on phytoplankton diversity and biomass.

Environmental authorities require the protection of biodiversity and other ecosystem properties such as biomass production. However, the endpoints listed in available ecotoxicological datasets generally do not contain these two ecosystem descriptors. Inferring the effects of chemicals on such descriptors from micro- or mesocosm experiments is often hampered by inherent differences in the initial biodiversity levels between experimental units or by delayed community responses. Here we introduce additive modelling to establish the effects of a chronic application of the herbicide linuron on 10 biodiversity indices and phytoplankton biomass in microcosms. We found that communities with a low (high) initial biodiversity subsequently became more (less) diverse, indicating an equilibrium biodiversity status in the communities considered here. Linuron adversely affected richness and evenness while dominance increased but no biodiversity indices were different from the control treatment at linuron concentrations below 2.4 µg/L. Richness-related indices changed at lower linuron concentrations (effects noticeable from 2.4 µg/L) than other biodiversity indices (effects noticeable from 14.4 µg/L) and, in contrast to the other indices, showed no signs of recovery following chronic exposure. Phytoplankton biomass was unaffected by linuron due to functional redundancy within the phytoplankton community. Comparing thresholds for biodiversity with conventional toxicity test results showed that standard ecological risk assessments also protect biodiversity in the case of linuron.

Biodiversity of freshwater diatom communities during 1000 years of metal mining, land use, and climate change in central Sweden.

We subjected a unique set of high-quality paleoecological data to statistical modeling to examine if the biological richness and evenness of freshwater diatom communities in the Falun area, a historical copper (Cu) mining region in central Sweden, was negatively influenced by 1000 years of metal exposure. Contrary to ecotoxicological predictions, we found no negative relation between biodiversity and the sedimentary concentrations of eight metals. Strikingly, our analysis listed metals (Co, Fe, Cu, Zn, Cd, Pb) or the fractional land cover of cultivated crops, meadow, and herbs indicating land disturbance as potentially promoting biodiversity. However, correlation between metal- and land-cover trends prevented concluding which of these two covariate types positively affected biodiversity. Because historical aqueous metal concentrations--inferred from solid-water partitioning--approached experimental toxicity thresholds for freshwater algae, positive effects of metal mining on biodiversity are unlikely. Instead, the positive relationship between biodiversity and historical land-cover change can be explained by the increasing proportion of opportunistic species when anthropogenic disturbance intensifies. Our analysis illustrates that focusing on the direct toxic effects of metals alone may yield inaccurate environmental assessments on time scales relevant for biodiversity conservation.

Combining monitoring data and modeling identifies PAHs as emerging contaminants in the arctic.

Protecting Arctic ecosystems against potential adverse effects from anthropogenic activities is recognized as a top priority. In particular, understanding the accumulation and effects of persistent organic pollutants (POPs) in these otherwise pristine ecosystems remains a scientific challenge. Here, we combine more than 20,000 tissue concentrations, a food web bioaccumulation model, and time trend analyses to demonstrate that the concentrations of legacy-POPs in the Barents/Norwegian Sea fauna decreased 10-fold between 1985 and 2010, which reflects regulatory efforts to restrict these substances. In contrast, concentrations of fossil fuel derived PAHs in lower trophic levels (invertebrates and fish) increased 10 to 30 fold over the past 25 years and now dominate the summed POP burden (25 POPs, including 11 PAHs) in these biota. Before 2000, PCBs dominated the summed POP burden in top predators. Our findings indicate that the debate on the environmental impacts of fossil fuel burning should move beyond the expected seawater temperature increase and examine the possible environmental impact of fossil fuel derived PAHs.

Functional redundancy and food web functioning in linuron-exposed ecosystems.

An extensive data set describing effects of the herbicide linuron on macrophyte-dominated microcosms was analysed with a food web model to assess effects on ecosystem functioning. We showed that sensitive phytoplankton and periphyton groups in the diets of heterotrophs were gradually replaced by more tolerant phytoplankton species as linuron concentrations increased. This diet shift--showing redundancy among phytoplankton species--allowed heterotrophs to maintain their functions in the contaminated microcosms. On an ecosystem level, total gross primary production was up to hundred times lower in the treated microcosms but the uptake of dissolved organic carbon by bacteria and mixotrophs was less sensitive. Food web efficiency was not consistently lower in the treated microcosms. We conclude that linuron predominantly affected the macrophytes but did not alter the overall functioning of the surrounding planktonic food web. Therefore, a risk assessment that protects macrophyte growth also protects the functioning of macrophyte-dominated microcosms.

Uncertainties in ecological, chemical and physiological parameters of a bioaccumulation model: implications for internal concentrations and tissue based risk quotients.

Bioaccumulation models predict internal contaminant concentrations (c(i)) using ecological, chemical and physiological parameters. Here we analyse the effect of uncertainties on these parameters on bioaccumulation model predictions. Simultaneously considering the uncertainties on all these parameters in a bioaccumulation model resulted in uncertainty ranges of c(i) that increased with the octanol water partition coefficient K(ow) and reached maxima of up to 1.25 log units for mesozooplankton and up to 1.45 log units fish at logK(ow)=8. A global sensitivity analysis (SA) was performed to rank the contribution of different parameters to the observed uncertainty. The SA demonstrated that this interspecies difference resulted predominantly from uncertain production rates of fish. The K(ow), the water concentration and organic carbon-octanol proportionality constant were important drivers of uncertainty on c(i) for both species. A tissue based risk quotient (RQ(tissue)) combining uncertainty on c(i) with realistic tissue based effect thresholds indicated that fish were up to 10 times more probable to have RQ(tissue)>1 than mesozooplankton, depending on the considered threshold value. Conventional exposure based risk quotients were up to 5 times less probable to exceed one than were corresponding RQ(tissue), and this for both species.

Non-simultaneous ecotoxicity testing of single chemicals and their mixture results in erroneous conclusions about the joint action of the mixture.

The ecotoxicity of binary chemical mixtures with a common mode of action is often predicted with the concentration addition model. The assumption of concentration addition is commonly tested statistically based on results of toxicity experiments with the two single chemicals and their binary mixture. The present simulation study shows that if not all these experiments are performed simultaneously, one has a 20-80% chance of concluding synergism or antagonism while the mixture is actually additive (false positive rate). Truly synergistic or antagonistic mixtures have a 10-50% chance of being falsely categorized as additive (false negative rate). Additionally, false positive rates decrease with increasing experimental error, while false negative rates increase with increasing experimental error. Based on these results, we put forward a number of recommendations for future mixture ecotoxicity evaluation.

An ecosystem modelling approach for deriving water quality criteria.

Ecological effects of chemicals on ecosystems are the result of direct effects of the chemical, determined in single-species toxicity testing, and indirect effects due to ecological interactions between species. Current experimental methods to account for such interactions are expensive. Hence, mathematical models of ecosystems have been proposed as an alternative. The use of these models often requires extensive calibration, which hampers their use as a general tool in ecological effect assessments. Here we present a novel ecosystem modelling approach which assesses effects of chemicals on ecosystems by integrating single-species toxicity test results and ecological interactions, without the need for calibration on case-specific data. The methodology is validated by comparing predicted ecological effects of copper in a freshwater planktonic ecosystem with an experimental ecosystem data set. Two main effects reflected by this data set (a decrease of cladocerans and an increase of small phytoplankton) which were unpredictable from single-species toxicity test results alone, were predicted accurately by the developed model. Effects on populations which don't interact directly with other populations, were predicted equally well by single-species toxicity test results as by the ecosystem model. The small amount of required data and the high predictive capacity can make this ecosystem modelling approach an efficient tool in water quality criteria derivation for chemicals.

[The development of epidemiological surveillance systems for smallpox and poliomyelitis: changing concepts in operational categories]. / Desenvolvimento dos sistemas de vigilância epidemiológica da varíola e da poliomelite: a transformação de conceitos em categorias operacionais.

This article describes the process by which some concepts of epidemiological surveillance are elaborated and turned into operational categories to comprise the so-called epidemiological surveillance system for two specific diseases. The authors describe some epidemiological concepts and categories which were elaborated over the course of the smallpox eradication program and more recently in the poliomyelitis eradication program. Such concepts and categories as outbreak containment, cross-notification, and case definitions are described as they fit into a series of actions which make up the epidemiological surveillance system. Finally, it is worth noting that the description developed in this article is based on personal observations, since the authors participated in the smallpox eradication program in Bangladesh and Somalia as well as in the regional poliomyelitis eradication program in the Americas.

Randomised trial of alternative formulations of oral poliovaccine in Brazil.

In February to July, 1986, an outbreak of type 3 poliomyelitis occurred in north-east Brazil that was linked to type-specific failure of trivalent oral polio vaccine (TOPV). To see if alternative vaccines would improve seroconversion to type 3, 441 children less than 5 years of age who had previously received no or up to four doses of TOPV were randomly assigned to receive one dose of standard TOPV (1,000,000, 100,000, and 300,000 median tissue culture infection doses [TCID50] of types 1, 2, and 3, respectively); a new formulation of TOPV containing twice the dosage of type 3 (600,000 TCID50); or a monovalent vaccine containing 300,000 TCID50 of type 3. While rates of seroconversion to types 1 or 2 were equivalent following vaccination with either formulation of TOPV, children who received the new formulation were 2.7 times more likely to seroconvert to type 3. Similar differences for type 3 were observed when monovalent vaccine was compared with standard TOPV, though both groups had received the same dose of type 3 antigen. The low rate of seroconversion to type 3 in the standard TOPV group was associated with a higher rate of reinfection with type 2, which also appeared to interfere to some extent with seroconversion to type 1. These findings extend earlier observations that interference from Sabin type 2 virus may be an important contributory cause of type-specific TOPV failure, and suggest that interference can be overcome with alterations in the formulation.