Taming the terminological tempest in invasion science.

Standardised terminology in science is important for clarity of interpretation and communication. In invasion science - a dynamic and rapidly evolving discipline - the proliferation of technical terminology has lacked a standardised framework for its development. The result is a convoluted and inconsistent usage of terminology, with various discrepancies in descriptions of damage and interventions. A standardised framework is therefore needed for a clear, universally applicable, and consistent terminology to promote more effective communication across researchers, stakeholders, and policymakers. Inconsistencies in terminology stem from the exponential increase in scientific publications on the patterns and processes of biological invasions authored by experts from various disciplines and countries since the 1990s, as well as publications by legislators and policymakers focusing on practical applications, regulations, and management of resources. Aligning and standardising terminology across stakeholders remains a challenge in invasion science. Here, we review and evaluate the multiple terms used in invasion science (e.g. 'non-native', 'alien', 'invasive' or 'invader', 'exotic', 'non-indigenous', 'naturalised', 'pest') to propose a more simplified and standardised terminology. The streamlined framework we propose and translate into 28 other languages is based on the terms (i) 'non-native', denoting species transported beyond their natural biogeographic range, (ii) 'established non-native', i.e. those non-native species that have established self-sustaining populations in their new location(s) in the wild, and (iii) 'invasive non-native' - populations of established non-native species that have recently spread or are spreading rapidly in their invaded range actively or passively with or without human mediation. We also highlight the importance of conceptualising 'spread' for classifying invasiveness and 'impact' for management. Finally, we propose a protocol for classifying populations based on (i) dispersal mechanism, (ii) species origin, (iii) population status, and (iv) impact. Collectively and without introducing new terminology, the framework that we present aims to facilitate effective communication and collaboration in invasion science and management of non-native species.

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.

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.

Breathing space: deoxygenation of aquatic environments can drive differential ecological impacts across biological invasion stages.

The influence of climate change on the ecological impacts of invasive alien species (IAS) remains understudied, with deoxygenation of aquatic environments often-overlooked as a consequence of climate change. Here, we therefore assessed how oxygen saturation affects the ecological impact of a predatory invasive fish, the Ponto-Caspian round goby (Neogobius melanostomus), relative to a co-occurring endangered European native analogue, the bullhead (Cottus gobio) experiencing decline in the presence of the IAS. In individual trials and mesocosms, we assessed the effect of high, medium and low (90%, 60% and 30%) oxygen saturation on: (1) functional responses (FRs) of the IAS and native, i.e. per capita feeding rates; (2) the impact on prey populations exerted; and (3) how combined impacts of both fishes change over invasion stages (Pre-invasion, Arrival, Replacement, Proliferation). Both species showed Type II potentially destabilising FRs, but at low oxygen saturation, the invader had a significantly higher feeding rate than the native. Relative Impact Potential, combining fish per capita effects and population abundances, revealed that low oxygen saturation exacerbates the high relative impact of the invader. The Relative Total Impact Potential (RTIP), modelling both consumer species' impacts on prey populations in a system, was consistently higher at low oxygen saturation and especially high during invader Proliferation. In the mesocosm experiment, low oxygen lowered RTIP where both species were present, but again the IAS retained high relative impact during Replacement and Proliferation stages at low oxygen. We also found evidence of multiple predator effects, principally antagonism. We highlight the threat posed to native communities by IAS alongside climate-related stressors, but note that solutions may be available to remedy hypoxia and potentially mitigate impacts across invasion stages. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s10530-021-02542-3.

Using functional responses and prey switching to quantify invasion success of the Pacific oyster, Crassostrea gigas.

Invasive alien species continue to proliferate and cause severe ecological impacts. Functional responses (FRs) have shown excellent utility in predicting invasive predator success, however, their use in predicting invasive prey success is limited. Here, we assessed invader success by quantifying FRs and prey switching patterns of two native predators, the common sea star, Asterias rubens, and the green crab, Carcinus maenas, towards native blue mussels, Mytilus edulis, and invasive Pacific oysters, Crassostrea gigas. Asterias displayed destabilising type II FRs, whereas Carcinus displayed stabilising type III FRs towards both prey species. Both predators exhibited greater search efficiencies and maximum feeding rates towards native compared to invasive prey. Both predators disproportionately consumed native mussels over invasive oysters when presented simultaneously, even when native mussels were rare in the environment, therefore indicating negligible prey switching. We demonstrate that invasion success may be mediated through differential levels of biotic resistance exerted by native predators.

Resistance is futile: lack of predator switching and a preference for native prey predict the success of an invasive prey species.

Invasive species continue to severely impact biodiversity, yet predicting the success or failure of introduced species has remained elusive. In particular, the relationship between community invasibility and native species diversity remains obscure. Here, we apply two traditional ecological concepts that inform prey population stability and hence invasibility. We first show that the native predatory crustacean Gammarus duebeni celticus exhibited similar type II (destabilizing) functional responses (FRs) towards native mayfly prey and invasive amphipod prey, when these prey species were presented separately. However, when the two prey species were presented simultaneously, the predator did not exhibit prey switching, instead consuming disproportionately more native prey than expected from the relative abundance of native and invasive species. These consumptive propensities foster reductions of native prey, while simultaneously limiting biotic resistance against the invasive species by the native predator. Since our theoretical considerations and laboratory results match known field invasion patterns, we advocate the increased consideration of FR and prey switching studies to understand and predict the success of invasive species.

Winning the arms race: host-parasite shared evolutionary history reduces infection risks in fish final hosts.

Parasite manipulation of intermediate hosts evolves to increase parasite trophic transmission to final hosts, yet counter selection should act on the final host to reduce infection risk and costs. However, determining who wins this arms race and to what extent is challenging. Here, for the first time, comparative functional response analysis quantified final host consumption patterns with respect to intermediate host parasite status. Experiments used two evolutionarily experienced fish hosts and two naive hosts, and their amphipod intermediate hosts of the acanthocephalan parasite Pomphorhynchus tereticollis The two experienced fish consumed significantly fewer infected than non-infected prey, with lower attack rates and higher handling times towards the former. Conversely, the two naive fish consumed similar numbers of infected and non-infected prey at most densities, with similar attack rates and handling times towards both. Thus, evolutionarily experienced final hosts can reduce their infection risks and costs via reduced intermediate host consumption, with this not apparent in naive hosts.