Published in June 2020
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Research articles
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Frances E. Lucy, Eithne Davis, Roy Anderson, Olaf Booy, Ken Bradley, J. Robert Britton, Colin Byrne,
Joseph M. Caffrey, Neil E. Coughlan, Kate Crane, Ross N. Cuthbert, Jaimie T.A. Dick, James W.E. Dickey, Jeffrey Fisher, Cathal Gallagher,
Simon Harrison, Matthew Jebb, Mark Johnson, Colin Lawton, Dave Lyons, Tim Mackie, Christine Maggs, Ferdia Marnell, Tom McLoughlin, Dan Minchin,
Oonagh Monaghan, Ian Montgomery, Niall Moore, Liam Morrison, Rose Muir, Brian Nelson, Art Niven, Colette O’Flynn, Bruce Osborne, Ruth M. O’Riordan,
Neil Reid, Helen Roy, Rory Sheehan, Dorothy Stewart, Monica Sullivan, Paula Tierney, Paula Treacy, Elena Tricarico and Wayne Trodd
Horizon scan of invasive alien species for the island of Ireland (pp 155–177) |
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Ireland, being an island situated on Europe’s western seaboard, has a fewer number of native species than mainland European Union Member States (MS).
Increased numbers of vectors and pathways have reduced the island’s biotic isolation, increasing the risk of new introductions and their associated
impacts on native biodiversity. It is likely that these risks are greater here than they are in continental Member States, where the native biodiversity
is richer. A horizon scanning approach was used to identify the most likely IAS (with the potential to impact biodiversity) to arrive on the island
of Ireland within the next ten years. To achieve this, we used a consensus-based approach, whereby expert opinion and discussion groups were utilised
to establish and rank a list of 40 species of the most likely terrestrial, freshwater and marine IAS to arrive on the island of Ireland within
the decade 2017–2027. The list of 40 included 18 freshwater invaders, 15 terrestrial IAS and seven marine species. Crustacean species (freshwater
and marine) were taxonomically dominant (11 out of 40); this reflects their multiple pathways of introduction, their ability to act as ecosystem
engineers and their resulting high impacts on biodiversity. Freshwater species dominated the top ten IAS (seven species out of ten), with the signal
crayfish (Pacifastacus leniusculus) highlighted as the most likely species to arrive and establish in freshwaters, while roe deer
(Capreolus capreolus) (second) and the warm-water barnacle (Hesperibalanus fallax) (fifth), were the most likely terrestrial and marine
invaders. This evidence-based list provides important information to the relevant statutory agencies in both jurisdictions in Ireland to prioritise
the prevention of the most likely invaders and aid in compliance with legislation, in particular the EU Regulation on Invasive Alien Species
(EU 1143/2014). Targeted biosecurity in both jurisdictions is urgently required in order to manage the pathways and vectors of arrival, and is vital
to maintaining native biodiversity on the island of Ireland.
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Mikhail O. Son, Alexander A. Prokin, Pavel G. Dubov, Alicja Konopacka, Michał Grabowski, Calum MacNeil and Vadim E. Panov
Caspian invaders vs. Ponto-Caspian locals – range expansion of invasive macroinvertebrates from the Volga Basin results in high biological pollution of the Lower Don River (pp 178–200) |
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Until the 2000s, faunal exchange between endemic faunas of the Caspian Sea basin and the Azov-Black Sea (aka Pontic) basin was asymmetrical, with fauna heading towards the Volga Delta
and Caspian Sea from or via the Black and Azov Seas and little exchange in the opposite direction. This study is based on a hydrobiological survey of the Don River Basin conducted
in August 2011 and reflects a period when three new Caspian invaders (Dikerogammarus caspius, Adacna glabra, and Theodoxus major) were already widely distributed
in the study area. At the time of the expedition, of all the invasive species present, these three caused the greatest impact on local species and communities in the Don Basin.
The greatest biological contamination was found in areas which had already had relatively favorable conditions for existing resident Ponto-Caspian communities. In contrast, those stations
devoid of invaders were those under the most severe anthropogenic pressure or subject to estuarine conditions. This pattern was confirmed by biocontamination indices being significantly
correlated with standard water quality indices. The situation in the studied area, involving both the Azov-Caspian exchange via the Volga-Don Canal and the eastward invasion of exotic
species, such as Ferrissia californica and Potamopyrgus antipodarum, clearly identifies a single Ponto-Caspian Invasion Corridor that connects all three marine basins
of the Ponto-Caspian region. The importance of recognising and accounting for regional differences when considering the monitoring of aquatic invasions is discussed.
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Francis LeBlanc, Valérie Belliveau, Erica Watson, Chantal Coomber, Nathalie Simard, Claudio DiBacco, Renée Bernier and Nellie Gagné
Environmental DNA (eDNA) detection of marine aquatic invasive species (AIS) in Eastern Canada using a targeted species-specific qPCR approach (pp 201–217) |
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Aquatic invasive species (AIS) represent a significant threat to aquatic ecosystems, and early detection is a crucial step in mitigating risks
of establishment and spread. In this study, we designed and/or optimized species-specific qPCR assays for 9 marine invertebrates considered invasive
in Eastern Canada for use in conjunction with environmental DNA (eDNA) sampling. All qPCR assays showed high analytical sensitivity with theoretical limit
of detection (LOD) ranging from 0.045 to 9.24 picogram (pg) of DNA. Comparison of two eDNA water sampling methods showed an increased detection sensitivity
using the grab sample approach. eDNA AIS detections were also compared to results obtained using a traditional in situ biofouling monitoring method
(i.e., biofouling monitoring lines), and a high concordance between the two was observed. We also determined temporal variability in the amount of DNA found
in the environment for some of the targeted AIS, which will help target seasonal monitoring efforts. The results provided herein clearly demonstrate
the usefulness of including eDNA for early AIS detection in ongoing monitoring, rapid response investigations and mitigation/eradication efforts.
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Rosetta C. Blackman, Marco Benucci, Robert C. Donnelly, Bernd Hänfling, Lynsey R. Harper, Graham S. Sellers and Lori Lawson Handley
Simple, sensitive and species-specific assays for detecting quagga and zebra mussels (Dreissena rostriformis bugensis and D. polymorpha)
using environmental DNA (pp 218–236) |
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Early detection is paramount for attempts to remove invasive non-native species (INNS). Traditional methods rely on physical sampling and morphological
identification, which can be problematic when species are in low densities and/or are cryptic. The use of environmental DNA (eDNA) as a monitoring tool
in freshwater systems is becoming increasingly acceptable and widely used for the detection of single species. Here we demonstrate the development
and application of standard PCR primers for the detection of two freshwater invasive species which are high priority for monitoring in the UK and elsewhere:
the Dreissenid mussels; Dreissena rostriformis bugensis (Andrusov, 1987) and D. polymorpha (Pallas, 1771). We carried out a rigorous validation
process for testing the new primers, including DNA detection and degradation experiments in mesocosms, and a field comparison with traditional monitoring
protocols. eDNA from single individuals of both mussel species could be detected within four hours of the start of the mesocosm experiment. In field trials,
the two mussel species were detected at all sites where the species are known to be present, and eDNA consistently outperformed traditional kick-net sampling
for species detection. These results demonstrate the applicability of standard PCR for eDNA detection of freshwater invasive species.
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Amit Savaya, Giulio De Leo, Emilius Aalto, Tom Levy, Ohad Rosen, Rivka Manor, Eliahu D. Aflalo, Elena Tricarico and Amir Sagi
The IAG gene in the invasive crayfish Procambarus clarkii – towards sex manipulations for biocontrol and aquaculture (pp 237–258) |
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The red swamp crayfish Procambarus clarkii (Girard, 1852) is considered a voracious invasive species that gained this reputation through
the displacement of native crustaceans and is threatening the biodiversity of many freshwater ecosystems through Europe, Africa and Asia. At the same
time, this crayfish is an important aquaculture species since it is easy to grow and has high production rates. It is crucial to develop tools to control
and prevent invasive populations to reconcile conservation objectives with aquaculture goals. Thanks to recent biotechnological progress in crustacean
monosex aquaculture, we present here novel insights in crayfish reproductive biology that might pave the way for the production of monosex populations
through “IAG-switch”-manipulation based on the identification of the P. clarkii insulin-like androgenic gland hormone (IAG) encoding gene.
Our data indicate that this manipulation can be used to create “neo-females”, which produce all-male progeny. This approach is a promising avenue
for increasing food production in regions where crayfish is cultured, while greatly reducing risk of invasion in case of accidental release in the wild.
We also explored potential use of stocking neofemale crayfish to control invasive populations by generating a strong bias in male-to-female sex-ratio.
Specifically, we developed a simple demographic model and used it to investigate whether and under what assumptions stocking neofemale P. clarkii
can cause the eradication of an invasive population. Our work suggests that all-male crayfish production could be further developed towards an effective
control of wild invasive populations as part of an integrated pest management approach.
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Kim T. Fredricks, John A. Tix, Justin R. Smerud and Aaron R. Cupp
Laboratory trials to evaluate carbon dioxide as a potential behavioral control method for invasive red swamp (Procambarus clarkii)
and rusty crayfish (Faxonius rusticus) (pp 259–278) |
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Few effective strategies are available to control invasive crayfishes. Carbon dioxide (CO2) acts as a behavioral deterrent for invasive fishes
and could be a useful crayfish control tool. The objective of this laboratory study was to quantify CO2 concentrations that caused red swamp crayfish
(RSC; Procambarus clarkii) and rusty crayfish (RYC; Faxonius rusticus) avoidance behavior, altered emergence behavior, and caused loss
of equilibrium. Behavioral endpoints were quantified under light and dark conditions and at 10 and 24 °C. Avoidance responses from both species varied
widely. Under light conditions, 35 mg/L CO2 was needed to induce the first avoidance shuttle in both crayfish species at 10 °C. CO2 concentrations
of 42 mg/L for RYC and 46 mg/L for RSC were required for first shuttle at 24 °C. The first avoidance shuttle was induced at 37 mg/L CO2
for RYC and 54 mg/L CO2 for RSC at 10 °C in the dark. At 24 °C, 44 mg/L CO2 was required for first shuttle for both species. Less CO2 was needed
to cause the last avoidance shuttle in RYC compared to RSC at both temperatures and under both lighting conditions. RSC emergence occurred
at 418 ± 77 mg/L CO2, and loss of equilibrium occurred for both species at 1,231 ± 201 mg/L CO2. RYC appeared to be more sensitive than RSC to CO2,
but behavior did not differ among light and water temperature treatments. These results demonstrate that CO2 alters crayfish behavior.
The CO2 concentrations identified during this study may inform field testing to develop CO2 as a potential control tool for invasive crayfishes.
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Paul A. Bzonek, Jaewoo Kim and Nicholas E. Mandrak
Short-term behavioural response of common carp, Cyprinus carpio, to acoustic and stroboscopic stimuli (pp 279–292) |
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Deterrents that limit the dispersal of non-native fishes into waterways are important tools for managing aquatic invasions. Acoustic and stroboscopic stimuli may be used to limit the dispersal of common carp
(Cyprinus carpio), a widely invasive species. This study exposed mature, wild-caught common carp to stroboscopic, acoustic, or combined-stimuli treatments, and observed changes made in the duration of active
movement, and in the number of passes made across the deterrent. Mixed-effects models determined that common carp spent more time moving actively during the stimulus and post-stimulus periods than during the control
period for all treatments. Common carp deterrent passes differed according to treatments. In the stroboscopic treatment, passes only increased during the post-stimulus period, in the acoustic treatment there were
no significant differences across stimulus periods, and in the combined treatment passes decreased during the stimulus period. These results indicate that stimulus-induced behavioural changes may be sustained
for short periods of time (> 30 min) after the deactivation of a stimulus deterrent. Our study also found a muted avoidance response in comparison to other acoustic deterrent studies, likely due to the lack
of sufficient stimulus refuge. Finally, individuals exposed to both stimuli did not express additive behavioural responses in comparison to individuals exposed to only one stimulus type. Our findings highlight
important considerations for deterrent technologies and directly quantify the behavioural response of combined deterrent stimuli.
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Simona Strgulc Krajšek, Erazem Bahčič, Urban Čoko and Jasna Dolenc Koce
Disposal methods for selected invasive plant species used as ornamental garden plants (pp 293–305) |
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Invasive alien plant species are frequently grown as ornamental plants in gardens. Until recently, in Slovenia, there were neither specific collection centres
for a safe disposal of invasive plant species, nor any legislation that defined procedures for their removal and disposal. We investigated in two experiments
how to dispose of pieces of selected invasive plant species, with the aim to prevent their survival and further dispersion. In the first experiment, we chose
eight species that are known for spreading by either growing from pieces of cut stem (Cornus sericea, Parthenocissus quinquefolia,
Buddleja davidii) or through subterranean rhizomes and tubers (Solidago canadensis, Solidago gigantea, Rudbeckia laciniata,
Helianthus tuberosus, Symphyotrichum novae-angliae). The plant fragments were exposed to three different storage treatments: drying, composting
on an open compost heap, and storage in black bin liners, all of which can be used in the home garden. After 5 months of storage, the materials were planted
in box planters, and their development was monitored. Drying and composting was highly efficient for disposal, as the conditions destroyed the majority
of the plant material. However, storage in a bin liner was inefficient because it did not kill any of the plant species tested, and did not delay their growth
of new roots. In the second experiment we investigated selected woody invasive plants (Cornus sericea, Parthenocissus quinquefolia,
Buddleja davidii, Acer negundo, Forsythia × intermedia) to determine whether their branch fragments can sprout new roots, and whether
shredding of their branches represents an efficient dispersal pathway. These dried fragments did not grow roots under any circumstances, while freshly shredded
fragments rooted in some cases. Therefore, the use of mulch that has not been treated properly might allow dispersal of woody invasive plants.
We can conclude that not all recommended treatments for invasive plant disposal are equally successful to prohibit plant survival and further spread.
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Emi Yamaguchi, Mutsuyo Kadohira, Kei Fujii, Kohei Kobayashi and Mayura B. Takada
Utilization of municipality records for the early-stage management of introduced raccoons in Japan (pp 306–324) |
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Rapid response is critical for management of invasive alien species (IAS). However, lack of ecological information at early stages of invasion
is a challenge for development of management strategies. To facilitate development of an IAS management strategy, we investigated the stages of invasion
and habitat preferences of raccoons (Procyon lotor) believed to be in the early stage of invasion at Tokachi, Hokkaido, Japan. We obtained raccoon
records from local municipalities in Tokachi including trapping and individual biological data (2006–2014), necropsies conducted on 161 carcasses
collected as roadkill or by traps (2009–2014), and track surveys (August–November, 2010). Female raccoon reproductive statuses indicated populations
are established and actively breeding in Tokachi. Relative population densities (based on catch per unit effort) and annual changes in raccoon capture
sites revealed raccoon expansions, which were likely localized to the western region, indicating district-level variation in invasion stages.
The distribution of livestock farms may have positively influenced raccoon occurrence and body sizes. Half of sampled raccoons had recently eaten corn
(Zea maize), presumably obtained from livestock feed. Therefore, livestock farms may represent preferred raccoon habitats and could facilitate
raccoon establishment. In Tokachi, IAS management strategies (i.e., prevention, eradication, and impact mitigation) should be tailored to stage
of invasion at the local level. In particular, increased monitoring and capture efforts in areas with many livestock farms might retard raccoon
establishment. More broadly, at early stages of invasion, IAS data from local municipalities may facilitate development of management strategies.
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Letters to Management of Biological Invasions
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Jeffrey E. Hill, Gordon H. Copp, Scott Hardin, Katelyn M. Lawson, Larry L. Lawson Jr., Quenton M. Tuckett, Lorenzo Vilizzi and Craig A. Watson
Comparing apples to oranges and other misrepresentations of the risk screening tools FISK and AS-ISK – a rebuttal of Marcot et al. (2019) (pp 325–341) |
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Marcot et al. (2019) recently described the risk analysis process by which the U.S. Fish and Wildlife Service (USFWS) chooses species for listing as injurious wildlife.
They further compared the Fish Invasiveness Screening Kit (FISK) and the Aquatic Species Invasiveness Screening Kit (AS-ISK), generally unfavorably, with their process/components.
We assert that FISK and AS-ISK were largely misrepresented. The USFWS process is a risk analysis framework, whereas FISK and AS-ISK are hazard identification/risk screening tools,
addressing only the initial step of a risk analysis scheme. Thus to avoid an apples-to-oranges comparison as done in that paper, FISK/AS-ISK should be compared to the equivalent USFWS tool,
the Ecological Risk Screening Summaries (ERSS). The remaining issues that we address concerning FISK/AS-ISK include: (1) need for expert opinion, (2) subjective climate matching,
(3) need for regional calibration, and (4) narrower range of information inputs; and concerning the ERSS process: (5) peer-review. Both systems clearly use expert opinion,
the FISK/AS-ISK arguably in a more structured and transparent manner. Guidance for FISK/AS-ISK recommends a climate-matching program, but allows for use of Köppen-Geiger climate types
or physiological tolerances, potentially increasing subjectivity in some cases but improving climate-match quality in others. Calibration of FISK/AS-ISK follows from the regional nature
of invasiveness risk and the use of questions unrelated to climate that are tailored to the risk assessment (RA) area. Climate match is the only element that the ERSS applies specifically to the RA area.
The FISK and AS-ISK actually use a much wider range of information than does the ERSS, a system based on invasion history and climate match only. The peer review of ERSS consisted of a five-member expert
panel that evaluated the method, whereas the ERSS reports posted online are not peer reviewed. Conversely, FISK applications have resulted in 37 peer-reviewed journal articles, including assessments
from over 70 experts in 45 countries. We welcome constructive criticism and improvement of these decision-support tools, but we are concerned that managers may dismiss well-established approaches
in favor of a framework that possesses its own method-specific limitations. We recommend that managers evaluate risk-based approaches and adopt systems to support decisions and improve invasive species management.
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Craig D. Martin, Susan D. Jewell, Michael H. Hoff, Carrie E. Givens and Bruce G. Marcot
Comparing Invasive Species Risk Screening Tools FISRAM, ERSS, and FISK/AS-ISK as a response to Hill et al. (2020) (pp 342–355) |
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The U.S. Fish and Wildlife Service (USFWS) developed an invasive species risk assessment procedure, presented in Marcot et al. (2019), consisting of an existing rapid assessment process for plants and animals
(Ecological Risk Screening Summary; ERSS) and a new probability-based Bayesian network model (Freshwater Fish Injurious Species Risk Assessment Model; FISRAM), that may be used to help prioritize invasive
freshwater fish species for Federal injurious wildlife listing evaluation by USFWS under the Lacey Act. Hill et al. (2020) provided a rebuttal letter of Marcot et al. (2019) but did not critique FISRAM,
the main subject of that paper. They focused instead on the ERSS process and on our characterization of several other existing risk assessment models and procedures. Here we provide our reciprocal rebuttal
by addressing their criticisms. Hill et al. (2020) implied that we equate the Fish Invasiveness Screening Kit (FISK) and Aquatic Species Invasiveness Screening Kit (AS-ISK) to the USFWS risk analysis process
for listing species as injurious, their “apples to oranges.” However, the USFWS process for evaluating species to list is an extensive risk analysis process explained in our paper that follows laws and standards
and optionally includes ERSS as a rapid screen in an early stage. Their interpretation that we compared our rigorous listing process to the risk screening tools FISK and AS-ISK was incorrect. We explain
how we use expert opinion and reiterate that the information inputs for the ERSS reports, primarily climate match and invasiveness history, are good predictors of species invasion and are appropriate
for a rapid screen for use in many situations. Their criticism of a lack of regional calibration of ERSS is answered by the ERSS climate-matching heat maps that show a color-calibrated continuum of climate
match for the contiguous United States. We further explain our comprehensive peer review process and why their suggestion to have each ERSS report peer reviewed is infeasible. We also discuss their letter’s
misrepresentation of the injurious wildlife listing process, which can use ERSS and FISRAM to advise prioritization and to provide documentation and decision support. All models described in our paper have value,
and management entities should review the literature published by the respective developers to learn of their individual utility.
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