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

Identifying potential emerging invasive non-native species from the freshwater pet trade

1. An increasingly globalised world has facilitated the movement of non-native species (NNS) via the poorly regulated international pet trade. While focus is increasingly being placed on preventative action to combat invasive NNS—often cheaper and less difficult than the management of established populations—successful prevention requires controlling potential pathways and obtaining baseline knowledge of species' availability. 2. Here we performed an in-depth analysis of the freshwater pet trade as one major vector of NNS, compiling its species inventory and deriving threats of NNS release and establishment in the wild. With Germany as our study region, we surveyed pet stores, websites and the country's largest online classified portal, eBay Kleinanzeigen, recording the taxa encountered. For each species, we determined the likelihood of release based on availability and price (cheaper and/or more readily available species have been shown to be of greater risk), and the likelihood of establishment based on ecological niche breadth and niche overlap with environmental conditions in Germany. 3. The survey revealed 669 species, of which 651 were non-native to Germany. Looking at release likelihood, more readily available species in pet stores and on websites proved to be cheaper. For websites, there was a significant effect of occurrence status (i.e. released, not released, native) on price, with released and native species being significantly cheaper. Species previously released in Germany and elsewhere demonstrated greater niche breadths and greater niche overlaps between their source regions and Germany; and for species released in Germany, there was a significantly positive relationship between the magnitude of niche overlap and the number of documented occurrences. 4. Finally, we combined our release and establishment likelihood findings under ‘Release Risk’ metrics to highlight the species most worthy of prioritisation. We propose these metrics as proactive methods for screening species in the trade, which can inform future policy direction and intervention

Current temperatures limit the potential impact of a commonly traded predatory gastropod

The pet trade has facilitated the spread of invasive alien species (IAS) globally, with negative consequences for biodiversity. The prediction of impacts is a major goal for invasion ecologists, and is especially crucial in an industry often lacking knowledge about traded species. We focused on the predatory gastropod Anentome helena, a species originating in south-east Asia and traded around the world, but with taxonomic uncertainty. We first set out to determine where our study organism fell within the A. “helena” species complex, known to comprise at least four cryptic species, before assessing the effect of temperature on the number of prey, the pulmonate snail Physella acuta, killed per predator via functional response experiments at two temperatures. We used 22 °C as a recommended temperature for housing the species in captivity, and 18 °C as a representative summer lake temperature in temperate climates of Europe. We also assessed the role of predator group size (1×, 2×, 3×) on predation (total consumption and average per capita consumption) at the experimental temperatures with fixed densities of prey, as well as the effect of these temperatures on prey activity. Our organisms belonged to a cryptic species originating from Thailand (Anentome sp. A), matching the findings of aquarium trade samples in other continents. In the functional response experiments, we found maximum feeding rate to be significantly reduced at the lower temperature. A similar result ensued from group feeding, with total consumption significantly reduced and the reduction in average per capita consumption approaching significance at the lower temperature. There was no significant effect of group size on the average per capita consumption in the group trial, indicating neutral conspecific interactions. No significant effect of temperature on the activity of the prey species was found, suggesting decreased consumption was mainly driven by predator, rather than prey. These results suggest limited A. helena impacts in the short-term, but increasing temperatures with climate change may facilitate greater consequences from releases. We suggest future studies assess other potential predatory impacts and survival across relevant abiotic conditions, and encourage the use of similar methods to assess the impacts of other commonly traded species

Understanding divergent zoochorous dispersal

The mechanisms which underpin passive dispersal (zoochory) of organisms (or propagules) by other, usually more mobile animals (vector species), are frequently poorly understood. While certain dispersal networks have received considerable scientific interest, basic questions concerning the relative importance of vector species, propagule survival, and likely dispersal distances, often remain unanswered. Here, we propose and apply a series of novel metrics, the Dispersal Potential (DP), the Relative Dispersal Potential (RDP) and the Combined Dispersal Potential (CDP), to predict and classify likely dispersal and vector importance. In essence, DP = Np × Tv, whereby Np is the per capita propagule load (e.g. mean, minimum, or maximum abundance) or species richness of propagules carried per individual vector species, while Tv is the total number of possible vectors (e.g. individuals of a single species at a source site, local scale abundances, or entire continental populations). Further, the ratio based metric RDP allows for DP comparison between species, while the CDP accumulates the DP of a variety of vector species. An additional Relative CDP (RCDP) metric facilitates comparison between the CDP for multiple vectors to that of one or more additional vectors. The proposed metrics can also be used to assess intraspecific differences (e.g. ontogeny or reproductive status). Accordingly, we examine a variety of case studies and present calculations to ascertain the usefulness of our proposed metrics. Finally, we argue that adoption of these metrics and variants thereof, will enhance understanding of zoochory within and across dispersal networks

More than we bargained for: Zebra mussels transported amongst European native freshwater snails

The international pet trade is a major driver of non-native species spread, including species both sold in the trade, and organisms incidentally transported alongside. Here, we document the discovery of invasive zebra mussels, Dreissena polymorpha, in Germany, transported alongside a commonly traded garden pond snail and European native, Viviparus viviparus, ordered from a German pet website. We highlight that the trade poses yet another way in which zebra mussels and other invasive species can expand their invaded range into novel ecosystems. We call for stricter biosecurity enforcement towards sellers, and encourage raising awareness amongst customers to inhibit the further spread of invasive species through the pet trade

Behavioural traits of rainbow trout and brown trout may help explain their differing invasion success and impacts

Animal behaviour is increasingly recognised as critical to the prediction of non-native species success and impacts. Rainbow trout and brown trout have been introduced globally, but there appear to be differences in their patterns of invasiveness and ecological impact. Here, we investigated whether diploid rainbow trout and diploid and triploid brown trout differ among several key behavioural measures linked to invasiveness and impact. We assessed activity, boldness, aggression, and feeding, using open field, novel object, shelter, mirror, feeding, and functional response experiments. We also tested within each fish type for behavioural syndromes comprising correlations among activity, boldness and aggression. Rainbow trout were more active and aggressive but less bold than diploid and triploid brown trout. In small groups, however, rainbow trout were bolder than both types of brown trout. Diploid brown trout were more active and bolder than triploids when tested individually, and had a higher functional response than both rainbow trout and triploid brown trout. In terms of behavioural syndromes, there was no association between activity and boldness in rainbow trout, however, there was in both brown trout types. The increased activity and aggression of rainbow trout may reflect an increased stress response to novel situations, with this response reduced in a group. These results suggest that rainbow trout do not manage their energy budgets effectively, and may explain why they have limited survival as invaders. In addition, the lower functional response of rainbow trout may explain why they are implicated in fewer ecological impacts, and the triploidy treatment also appears to lower the potential impact of brown trout. Comparative analyses of multiple behaviours of invasive species and genetic variants may thus be key to understanding and predicting invader success and ecological impacts

When worlds collide: Invader-driven benthic habitat complexity alters predatory impacts of invasive and native predatory fishes

Interactions between multiple invasive alien species (IAS) might increase their ecological impacts, yet relatively few studies have attempted to quantify the effects of facilitative interactions on the success and impact of aquatic IAS. Further, the effect of abiotic factors, such as habitat structure, have lacked consideration in ecological impact prediction for many high-profile IAS, with most data acquired through simplified assessments that do not account for real environmental complexities. In the present study, we assessed a potential facilitative interaction between a predatory invasive fish, the Ponto-Caspian round goby (Neogobius melanostomus), and an invasive bivalve, the Asian clam (Corbicula fluminea). We compared N. melanostomus functional responses (feeding-rates under different prey densities) to a co-occurring endangered European native analogue fish, the bullhead (Cottus gobio), in the presence of increased levels of habitat complexity driven by the accumulation of dead C. fluminea biomass that persists within the environment (i.e. 0, 10, 20 empty bivalve shells). Habitat complexity significantly influenced predation, with consumption in the absence of shells being greater than where 10 or 20 shells were present. However, at the highest shell density, invasive N. melanostomus maximum feeding-rates and functional response ratios were substantially higher than those of native C. gobio. Further, the Relative Impact Potential metric, by combining per capita effects and population abundances, indicated that higher shell densities exacerbate the relative impact of the invader. It therefore appears that N. melanostomus can better tolerate higher IAS shell abundances when foraging at high prey densities, suggesting the occurrence of an important facilitative interaction. Our data are thus fully congruent with field data that link establishment success of N. melanostomus with the presence of C. fluminea. Overall, we show that invader-driven benthic habitat complexity can alter the feeding-rates and thus impacts of predatory fishes, and highlight the importance of inclusion of abiotic factors in impact prediction assessments for IAS

Driver's Seat: Understanding Divergent Zoochorous Dispersal of Propagules

The functional role, relative importance, and the spatial and temporal parameters of different vector species, which underpin the passive dispersal (zoochory) of organisms (or their propagules), are frequently poorly understood. Accordingly, a conceptual framework capable of providing a rigorous and unified assessment for the dispersal capacity of vector species is required. Here, we propose and apply a series of novel metrics, the Dispersal Potential (DP), the Relative Dispersal Potential (RDP), and the Combined Dispersal Potential (CDP), to predict and classify likely dispersal and vector importance. In essence, DP = Np × Tv, whereby Np is the per capita propagule load (e.g., mean, minimum, or maximum abundance) or species richness of propagules carried per individual vector species, while Tv is the total number of possible vectors (e.g., individuals of a single species at a source site, local scale abundances, or entire continental populations). Further, the ratio based metric RDP allows for DP comparison between species, while the CDP accumulates the DP of a variety of vector species. An additional Relative CDP (RCDP) metric facilitates comparison between the CDP for multiple vectors to that of one or more additional vectors. The proposed metrics can also be used to assess intraspecific differences (e.g., ontogeny). Accordingly, we examine a variety of case studies and present calculations to ascertain the usefulness of our proposed metrics. Overall, the metrics can be used to quantify and rank the prominence of different dispersers that facilitate biological connectivity. Finally, we argue that adoption of these metrics and variants thereof, will provide a more realistic measure of species' functional roles than examination of interaction intensities alone, which will enhance understanding of zoochory within and across dispersal networks