The effect of the alternative prey, Paramecium caudatum (Peniculida: Parameciidae), on the predation of Culex pipiens (Diptera: Culicidae) by the copepods Macrocyclops albidus and Megacyclops viridis (Cyclopoida: Cyclopidae)

Biological control can be an effective tool to combat public health risks associated with mosquito-borne disease. However, target impacts of biological control agents may be reduced by biotic contexts such as the presence of alternative prey. In turn, this can impede our ability to realistically assess biocontrol agent efficacy. Here, we examine the effects of alternative ciliate prey on the predation potential of two cyclopoid copepods, Macrocyclops albidus Jurine (Cyclopoida: Cyclopidae) and Megacyclops viridis Jurine (Cyclopoida: Cyclopidae), towards larvae of the West Nile virus vector mosquito Culex pipiens Linnaeus (Diptera: Culicidae). Using functional responses (FRs; resource use under different resource densities), we demonstrate that both copepods exhibit potentially destabilising Type II FRs towards mosquito prey. However, where the alternative prey was present, we observed species-specific modulations to FR form and magnitude. For M. albidus, FRs remained Type II where ciliate prey were present, however, maximum feeding rates on mosquito larvae were reduced. Conversely, for M. viridis, FRs moved towards more stabilising Type III, whilst maximum feeding rates on mosquito larvae were not significantly reduced. Whilst both species of cyclopoid copepod were able to effectively target and consume larval mosquitoes in the presence of alternative prey, we demonstrate that overall efficacies may be reduced in aquatic habitats which contain multiple prey types. We thus advocate that biotic contexts such as prey selectivity should be integrated into predatory biocontrol agent examinations for mosquitoes which vector pathogens and parasites, to more holistically assess their efficacy

Differential interaction strengths and prey preferences across larval mosquito ontogeny by a cohabiting predatory midge

Abstract Understandings of natural enemy efficacy are reliant on robust quantifications of interaction strengths under context-dependencies. For medically important mosquitoes, rapid growth during aquatic larval stages could impede natural enemy impacts through size refuge effects. The identification of biocontrol agents which are unimpeded by ontogenic size variability of prey is therefore vital. We use functional response and prey preference experiments to examine the interaction strengths and selectivity traits of larvae of the cohabiting predatory midge Chaoborus flavicans (Meigen 1830) (Diptera: Chaoboridae) towards larval stages of the Culex pipiens (Diptera: Culicidae) mosquito complex. Moreover, we examine the influence of search area variation on selectivity traits, given its importance in consumer-resource interactions. Chaoborids were able to capture and consume mosquito prey across their larval ontogeny. When prey types were available individually, a destabilizing Type II functional response was exhibited towards late instar mosquito prey, whereas a more stabilizing Type III functional response was displayed towards early instars. Accordingly, search efficiencies were lowest towards early instar prey, whereas, conversely, maximum feeding rates were highest towards this smaller prey type. However, when the prey types were present simultaneously, C. flavicans exhibited a significant positive preference for late instar prey, irrespective of water volume. Our results identify larval chaoborids as efficacious natural enemies of mosquito prey, with which they frequently coexist in aquatic environments. In particular, an ability to prey on mosquitoes across their larval stages, coupled with a preference for late instar prey, could enable high population-level offtake rates and negate compensatory reductions in intraspecific competition through size refuge

Ecological impacts of invasive alien species along temperature gradients: testing the role of environmental matching

Invasive alien species (IAS) can cause substantive ecological impacts, and the role of temperature in mediating these impacts may become increasingly significant in a changing climate. Habitat conditions and physiological optima offer predictive information for IAS impacts in novel environments. Here, using meta-analysis and laboratory experiments, we tested the hypothesis that the impacts of IAS in the field are inversely correlated with the difference in their ambient and optimal temperatures. A meta-analysis of 29 studies of consumptive impacts of IAS in inland waters revealed that the impacts of fishes and crustaceans are higher at temperatures that more closely match their thermal growth optima. In particular, the maximum impact potential was constrained by increased differences between ambient and optimal temperatures, as indicated by the steeper slope of a quantile regression on the upper 25th percentile of impact data compared to that of a weighted linear regression on all data with measured variances. We complemented this study with an experimental analysis of the functional response - the relationship between predation rate and prey supply - of two invasive predators (freshwater mysid shrimp, Hemimysis anomala and Mysis diluviana) across relevant temperature gradients; both of these species have previously been found to exert strong community-level impacts that are corroborated by their functional responses to different prey items. The functional response experiments showed that maximum feeding rates of H. anomala and M. diluviana have distinct peaks near their respective thermal optima. Although variation in impacts may be caused by numerous abiotic or biotic habitat characteristics, both our analyses point to temperature as a key mediator of IAS impact levels in inland waters and suggest that IAS management should prioritize habitats in the invaded range that more closely match the thermal optima of targeted invaders

Salinity tolerance and geographical origin predict global alien amphipod invasions

Invasive alien species are driving global biodiversity loss, compromising ecosystem function and service provision, and human, animal and plant health. Habitat characteristics and geographical origin may predict invasion success, and in aquatic environments could be mediated principally by salinity tolerance. Crustacean invaders are causing global problems and we urgently require better predictive power of their invasiveness. Here, we compiled global aquatic gammarid (Crustacea: Amphipoda: Gammaroidea) diversity and examined their salinity tolerances and regions of origin to test whether these factors predict invasion success. Across 918 aquatic species within this superfamily, relatively few gammarids (n = 27, 3%) were reported as aliens, despite extensive invasion opportunities and high numbers of published studies on amphipod invasions. However, reported alien species were disproportionately salt-tolerant (i.e. 32% of brackish-water species), with significantly lower proportions of aliens originating from freshwater and marine environments (both 1%). Alien gammarids also significantly disproportionally originated from the Ponto-Caspian (20% of these taxa) when compared with all ‘other' grouped regions (1%), and principally invaded Eurasian waters, with translocations of salt-tolerant taxa to freshwaters being pervasive. This suggests habitat characteristics, alongside regional contexts, help predict invasibility. In particular, broad environmental tolerances to harsh environments and associated evolutionary history probably promote success of aliens globally

Biological control agent selection under environmental change using functional responses, abundances and fecundities; the Relative Control Potential (RCP) metric

We currently lack the capacity to rapidly and reliably predict the efficacy of biological control agents due to inadequate consistency in derivations of functional and numerical responses and potential effects of context-dependencies. Here, we propose and apply a novel metric, Relative Control Potential (RCP), which combines the functional response (FR, per capita effect) with proxies for the numerical response (NR, agent population response) to compare agent efficacies, where RCP = FR × abundance (or other proxies e.g. fecundity). The RCP metric is a comparative ratio between potential biocontrol agents, where values > 1 indicate higher relative control efficacy. Further, RCP can compare the efficacy of agents under environmental contexts, such as temperature change. We thus derived the RCP for two predatory cyclopoid copepods, Macrocyclops albidus (Cyclopoida: Cyclopidae) and Megacyclops viridis (Cyclopoida: Cyclopidae), towards larvae of the mosquito Culex pipiens (Diptera: Culicidae) under temperatures representative of current and future climate. Both copepods exhibited potentially population destabilising Type II FRs, with increasing temperatures inducing greater magnitude FRs through increased attack rates and decreased handling times. Attack rates by M. albidus were higher than M. viridis, yet handling times and maximum feeding rates were similar between the species across all temperatures. The inclusion of abundance data drives an elevated RCP of M. albidus and the integration of fecundity drives greater RCP of M. albidus at peak temperatures. Q10 values are indicative of increased feeding activity by both copepods with temperature increases, however relative feeding level increases of M. viridis slowed towards the peak temperature. We present RCP calculations and biplots that represent the comparative efficacies of the two biological control agents across temperatures. The Relative Control Potential (RCP) metric thus provides a new tool for practitioners to better assess the potential efficacy of biocontrol agents before their integration into management approaches for pests, vectors and invasive species

Combining resource population dynamics into impact assessments of native and invasive species under abiotic change

Predicting future changes in interspecific interactions continues to be a challenge for environmental managers. This uncertainty is exacerbated by increasing biological invasions and the likelihood that the strength of trophic interactions among native species will change. Abiotic variables influence predator resource utilisation and abundance as well as resource population dynamics. Currently no practical metric or impact prediction methodology can adequately account for all of these factors. Functional Response (FR) methods successfully incorporate resource utilisation rates with regards to resource density to quantify consumer-resource interactions under varying abiotic contexts. This approach has been extended to create the Relative Impact Potential (RIP) metric to compare invader vs native impact. However, this does not incorporate resource abundance dynamics, which clearly can also change with abiotic context. We propose a Resource Reproduction Qualifier (RRQ) be incorporated into the RIP metric, whereby RRQ is the reciprocal of the fraction or proportion to which reproduction (e.g. of prey species) changes under an environmental context. This modifies the RIP score to give a more informative RIPq value, which may be contextually increased or decreased. We empirically demonstrate the utility and benefits of including RRQ into impact potential predictions with an invasive species (the lionfish Pterois volitans) and two European native species (shanny fish Lipophyris pholis and lesser spotted dogfish Scyliorhinus canicula) under different abiotic contexts. Despite high FR and abundance, lionfish impacts were reduced by increasing prey recruitment at higher temperatures, however, remained high impact overall. Shanny predatory impact increased with increasing temperature and was exacerbated by decreasing prey fecundity. Two population increase scenarios (50% and 80%) were assessed for lesser spotted dogfish under predicted temperature increases, preying upon E. marinus. Both scenarios indicated heightened predatory impact with increasing predator FR and decreasing prey fecundity. Our new metric demonstrates that accounting for resource reproductive responses to abiotic drivers, in tandem with the consumer per capita and abundance responses, better estimate the magnitudes of predicted inter-species interactions and ecological impacts. This can be used in stock assessments and predictions, as well as invasive species risk assessments in a comprehensive yet user-friendly manner

The influence of microplastics on trophic interaction strengths and oviposition preferences of dipterans

Microplastic (MP) pollution continues to proliferate in freshwater, marine and terrestrial environments, but with their biotic implications remaining poorly understood. Biotic interactions such as predation can profoundly influence ecosystem structuring, stability and functioning. However, we currently lack quantitative understandings of how trophic interaction strengths and associated behaviours are influenced by MP pollution, and how transference of MPs between trophic levels relates to consumptive traits. We also lack understanding of key life-history effects of MPs, for example, reproductive strategies such as oviposition. The present study examines the predatory ability of non-biting midge larvae, Chaoborus flavicans, towards larvae of Culex pipiens mosquitoes when the latter are exposed to MPs, using a functional response (FR) approach. Transfer of MPs occurred from larval mosquitoes to larval midges via predation. Microplastics transfer was significantly positively related to predation rates. Predation by C. flavicans followed a Type II FR, with average maximum feeding rates of 6.2 mosquito larvae per hour. These and other FR parameters (attack rates and handling times) were not significantly influenced by the presence of MPs. Further, C. pipiens adults did not avoid ovipositing in habitats with high concentrations of MPs. We thus demonstrate that MPs can move readily through freshwater food webs via biotic processes such as predation, and that uptake correlates strongly with consumption rates. Further, as MPs do not deter adult mosquitoes from ovipositing, our experiments reveal high potential for MP exposure and transference through ecosystems

On the context-dependent scaling of consumer feeding rates

The stability of consumer-resource systems can depend on the form of feeding interactions (i.e. functional responses). Size-based models predict interactions - and thus stability - based on consumer-resource size ratios. However, little is known about how interaction contexts (e.g. simple or complex habitats) might alter scaling relationships. Addressing this, we experimentally measured interactions between a large size range of aquatic predators (4-6400 mg over 1347 feeding trials) and an invasive prey that transitions among habitats: from the water column (3D interactions) to simple and complex benthic substrates (2D interactions). Simple and complex substrates mediated successive reductions in capture rates - particularly around the unimodal optimum - and promoted prey population stability in model simulations. Many real consumer-resource systems transition between 2D and 3D interactions, and along complexity gradients. Thus, Context-Dependent Scaling (CDS) of feeding interactions could represent an unrecognised aspect of food webs, and quantifying the extent of CDS might enhance predictive ecology. © 2016 John Wiley & Sons Ltd/CNRS