Management of Biological Invasions (2018) Volume 9, Issue 3: 259–265
Open Access
DOI: https://doi.org/10.3391/mbi.2018.9.3.08
© 2018 The Author(s).
This paper is published under terms of the Creative Commons Attribution License (Attribution 4.0 International - CC BY 4.0)
Research Article
A dip or a dab: assessing the efficacy of Virasure® Aquatic disinfectant to
reduce secondary spread of the invasive curly waterweed Lagarosiphon major
Ross N. Cuthbert 1, * , Neil E. Coughlan 1 , Kate Crane 1 , Joe M. Caffrey 2 , Hugh J. MacIsaac 3
and Jaimie T.A. Dick 1
1
Institute for Global Food Security, School of Biological Sciences, Queen’s University Belfast, Medical Biology Centre,
97 Lisburn Road, Belfast, BT9 7BL, Northern Ireland
2
INVAS Biosecurity, 6 Lower Ballymount Road, Walkinstown, Dublin 12, Ireland
3
Great Lakes Institute for Environmental Research, University of Windsor, Windsor, Ontario, N9B 3P4, Canada
Author e-mails: rcuthbert03@qub.ac.uk (RNC), neil.coughlan.zoology@gmail.com (NEC), kcrane02@qub.ac.uk (KC),
joecaffrey@invas.ie (JMC), hughm@uwindsor.ca (HJM), j.dick@qub.ac.uk (JTAD)
*Corresponding author
Received: 6 March 2018 / Accepted: 27 May 2018 / Published online: 5 July 2018
Handling editor: Calum MacNeil
Abstract
Aquatic alien invasive species (AIS) are a substantial and increasing threat to biodiversity and ecosystem function worldwide.
In particular, invasive aquatic macrophytes, such as the South African curly waterweed Lagarosiphon major ((Ridley) Moss
1928), induce major environmental change that often culminates in wide-ranging ecological and socio-economic impacts.
Currently, there is a lack of effective biosecurity protocols to mitigate against such invader spread. Here, we examine the
efficacy of a broad-spectrum aquatic disinfectant, Virasure® Aquatic, to induce mortality of L. major propagule stages. We
assessed the efficacy of Virasure® Aquatic at contact times of 1, 2 and 5 minutes, using 1% (10g L-1) and 4% (40g L-1)
concentrations. A necrosis scale was applied to visually assess tissue degradation. Necrosis increased with longer chemical
contact times, with fragment degradation optimised at 2 minutes at 1% concentration and 1 minute at 4% concentration.
Mode of application was also critical to treatment effectiveness, with spray treatments less effective than submersion treatments.
We recommend the use of Virasure® Aquatic via submersion for a minimum period of 2 minutes at 1% concentration or
higher. While spray applications should be applied when submersion is not feasible, such as with large water craft, increased
spray times beyond those assessed here should be examined. However, results presented suggest that Virasure® Aquatic can
effectively reduce the secondary spread of invasive L. major, and may thus form an integral part of biosecurity protocols. The
use of broad-spectrum disinfectants and other readily available treatments, that were not purposefully developed for aquatic
AIS control but nevertheless are emerging as effective in aquatic AIS management, is discussed and encouraged.
Key words: biosecurity, aquatic disinfectant, invasive species management, potassium peroxymonosulfate,
spread prevention, macrophyte
Introduction
Aquatic alien invasive species (AIS) are considered
a major driver of adverse change to freshwater
ecosystems (Simberloff et al. 2013; Piria et al. 2017).
In particular, many invasive aquatic plants (especially
invasive macrophytes) detrimentally affect freshwater
community dynamics and ecosystem function via
negative alteration of biotic and abiotic conditions
(Schultz and Dibble 2012; Hussner 2014; Kuehne et
al. 2016). In addition, the considerable biomass
associated with the presence of large monospecific
swards of invasive macrophytes can inhibit many
recreational and commercial activities, increase
flooding frequency, and result in substantial economic
costs (Williams et al. 2010; Lafontaine et al. 2013).
Novel methods for invader eradication and control,
which balance efficacy with cost, legislative barriers
and non-target effects, are thus urgently required.
Despite a restricted ability to self-disperse, many
aquatic AIS continue to successfully invade hydrologically unconnected sites (Hussner 2012; Caffrey et al.
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R.N. Cuthbert et al.
2016; Coughlan et al. 2017a). While vectors that
underpin the natural dispersal of aquatic AIS are
often not fully determined (Coughlan et al. 2017b),
freshwater systems remain highly vulnerable to
accidental invader introductions due to their interconnectedness and exposure to multiple transport
vectors, e.g. angling and boating (Rothlisberger et al.
2010; Banha et al. 2016). To date, various stakeholder
biosecurity campaigns (e.g. “Check, Clean, Dry”)
have attempted to reduce the spread of aquatic AIS
(Anderson et al. 2015) by creating awareness and
endorsing best practice. Moreover, recent European
Union (EU) legislation (Regulation 1143/2014)
requires EU Member States (MS) to enforce rapid
control, spread prevention and eradication of
damaging invaders that are listed as Invasive Alien
Species of Union Concern. Furthermore, recent United
States of America (USA) legislation (Safeguarding
the Nation from the Impacts of Invasive Species –
amendment to Executive Order 13112) seeks to
prevent, control and eradicate invasive species.
Currently, management options for the eradication
and control of established invader populations are
often complex, resource-intensive and costly, and
achieve only limited success (Hussner et al. 2017;
Piria et al. 2017). Indeed, there are relatively few
examples of successful reductions and/or eradications
where invaders have already established (Hussner et
al. 2017). As prevention of aquatic AIS introductions
is the most economical way to safeguard ecosystems,
the development of efficient and cost-effective biosecurity protocols that prevent invader spread is
essential (Barbour et al. 2013; Simberloff et al. 2013;
Caffrey et al. 2016; Hussner et al. 2017; Coughlan et
al. 2018a). Presently, however, there exists only a
limited understanding of the relative efficacies of
various biosecurity measures (Barbour et al. 2013;
Anderson et al. 2015; Piria et al. 2017; Coughlan et
al. 2018a). Chemical treatment has been suggested
as a suitable mechanism to control aquatic AIS
spread, as this is often more economical and widely
applicable when compared to other methods
(Getsinger et al. 2008; Richardson et al. 2016).
However, chemical treatments have hitherto been
predominantly applied in situ where invasive populations have already established (e.g. glyphosate,
Emerine et al. 2010; metsulfuron, Clements et al.
2014), often with inconsistent rates of success (see
Hussner et al. 2017). Thus, innovative measures to
reduce invasive species spread are urgently required
(e.g. Coughlan et al. 2018b). While alternative
broad-spectrum aquatic disinfectants may prove
effective at reducing secondary spread of invaders,
these chemicals have yet to be thoroughly considered
as aquatic AIS biosecurity agents.
260
Lagarosiphon major ((Ridley) Moss 1928) is a
canopy-forming submerged invasive macrophyte,
native to South Africa (Caffrey et al. 2010). In the
Northern Hemisphere, L. major displays over-winter
growth and can achieve substantial biomass under
conditions that are unsuitable for many native
species, including within eutrophic waters (Martin
and Coetzee 2014). Despite being listed as an EU
Invasive Alien Species of Union Concern, L. major
is still commonly sold as an oxygenating plant for
aquaria and artificial watercourses. Like many invasive
macrophytes, L. major predominantly reproduces and
spreads by vegetative propagation, particularly via
vegetative fragments which have been observed to
exhibit a high survival potential (Redekop et al.
2016; Coughlan et al. 2018a). Moreover, given the
high level of fragmentary propensity associated with
L. major, propagules are commonly observed to be
transferred via boat motors and fishing nets (Matthews
et al. 2012).
Here, we assess the efficacy of Virasure® Aquatic
as a biosecurity agent to reduce the secondary spread
of L. major fragments under varied chemical
concentrations, exposure times and modes of application. While aquatic disinfectants had previously
been developed for applications outside of invasive
species management, several have been observed to
effectively and rapidly induce aquatic AIS mortality
(e.g. Virkon®/Asian clam; Barbour et al. 2013), but
none have been previously tested upon invasive
macrophytes.
Methods
Cultivation of Lagarosiphon major
Shoot portions of L. major were harvested from an
artificial pond at Greenacres Golf Centre, Ballyclare,
Northern Ireland (N54º43′28.631; W06º00′10.908),
between February and April 2016. Substrate was also
sampled from the collection site for use in laboratory
cultures and the experiment using a spade. Vegetative
samples were rinsed and transported to Queen’s
University Belfast in dechlorinated tap water.
Lagarosiphon major was maintained in continuously
aerated aquaria within the laboratory at 13 ± 2 °C
under a 12:12 light:dark regime. All plants were
acclimatised for one week prior to experimentation.
Efficacy of Virasure® Aquatic as a biosecurity agent
for Lagarosiphon major
Healthy apical shoot sections of L. major were
selected for submersion and spray treatments with
Virasure® Aquatic (Fish Vet Group, 22 Carsegate Road,
Secondary spread reduction for invasive aquatic macrophytes
Table 1. Scale describing visual tissue degradation stages of Lagarosiphon.
Scale
0–10%
10–20%
20–30%
30–40%
40–50%
50–60%
60–70%
70–80%
80–90%
90–100%
Description
Tissue degradation at site of fragmentation
Pale brown leaf at apical tip
Pale brown leaf ends anywhere on plant
All leaf ends pale brown
Fragment collapse < 90°
Full leaves pale brown
All full leaves pale brown
Fragment collapse ≥ 90°
Full leaves dark brown/fragmenting at tips
Full fragment degradation: leaves fragmented and dark, flattened against stem
Figure 1. Mean (± SE) necrosis of
Lagarosiphon major propagule fragments
over a 28 day period post-exposure to 1%
Virasure® Aquatic for 1, 2 and 5 minutes
via submersion; to 4% Virasure® Aquatic
for 1 minute via submersion; and to 1%
Virasure® Aquatic for 1 minute via
continual spray, alongside control
submersion and spray treatments (n = 3).
Inverness, Scotland, IV3 8EX). A necrosis scale was
developed to monitor tissue degradation following
the various exposure treatments (see Table 1). Individual 5 cm apical fragments of L. major were either
submerged in a 1% Virasure® Aquatic (10 g L-1)
solution for 1, 2 or 5 minute exposure, or were
submerged in a 4% Virasure® Aquatic (40 g L-1)
solution for 1 minute exposure. Control samples were
submerged in dechlorinated tap water for 1 minute.
Other 5 cm fragments were concurrently sprayed
continually with 1% Virasure® Aquatic solution for
1 minute, while control samples were sprayed with
dechlorinated tap water for 1 minute. All treatments
were replicated three times. Following treatment,
each fragment was individually submerged in dechlorinated tap water in 0.15 litre cylindrical containers
measuring 8 cm diameter, with sufficient substrate to
cover the basal area to monitor recovery. Further,
comparative photographs were taken weekly to
support visual estimation of tissue degradation. All
experiments were conducted in a randomised design.
Statistical analyses
All data analyses were undertaken in R version 3.4.2.
(R Core Team 2017). We analysed categorically scaled
necrosis (Table 1) with repeated measures using
ordinal logistic regression. Experimental observations
for treatment effectiveness spanned 28 days at weekly
intervals, with explanatory variables “treatment” and
“time” incorporated as both single and interacting terms
in the model. Tukey’s comparisons were used to
perform post hoc analyses where terms yielded
significance.
Results
Minimal fragment degradation was observed for both
control treatments (Figure 1; Figure 2). However,
Virasure® Aquatic significantly increased fragment
tissue degradation (χ2 = 73.46, df = 6, P < 0.001;
Figure 1). Even submergence or spraying for 1 minute
in 1% Virasure® Aquatic resulted in significant fragment
degradation (submergence, z = 5.89, P < 0.001;
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R.N. Cuthbert et al.
Figure 2. Lagarosiphon major propagule fragments at 7 (A), 14 (B), 21 (C) and 28 (D) days post-treatment with Virasure® Aquatic. Top
row (L–R): control submerged 1 minute, submerged 1 minute (1%), submerged 2 minutes (1%). Middle row (L–R): submerged 5 minutes
(1%), control spray 1 minute, spray 1 minute (1%). Bottom: submerged 1 minute (4%). Photographs by RNC.
spraying, z = 5.86, P < 0.001). While there was no
difference between submergence or spray treatments
for 1 minute with 1% Virasure® Aquatic (z = 1.50, P
= 0.74), submergence for 2 minutes in 1% Virasure®
Aquatic was significantly more effective than both 1
minute submergence (z = 9.56, P < 0.001) and
spraying (z = 11.79, P < 0.001). However, there was
no significant difference between 2 minute submergence
and 5 minute submergence in 1% Virasure® Aquatic
(z = 1.08, P = 0.93), nor when compared to 1 minute
submergence in 4% Virasure® Aquatic (2 minutes,
z = 0.19, P = 0.99; 5 minutes, z = 1.20, P = 0.89).
262
Overall, necrosis increased with time after treatment
(χ2 = 86.82, df = 3, P < 0.001; Figure 2). There was a
significant difference between degradation observed
between all incremental observation periods (all
P ≤ 0.002). There was a significant “treatment ×
time” interaction (χ2 = 98.82, df = 18, P < 0.001),
which reflected the relatively rapid attainment of full
degradation with longer exposure time and greater
chemical concentration, whilst controls survived
(Figure 1). Although not accounted for quantitatively,
regrowth of shoots was observed within control
fragments and fragments treated with 1% Virasure®
Secondary spread reduction for invasive aquatic macrophytes
Aquatic via spray only, indicating sustained fragment
viability of control and spray treatments, but not
submersion treatments (Figure 2).
Discussion
Aquatic alien invasive species (AIS) continue to
spread at unprecedented rates, reducing biodiversity
and altering ecosystem function (Seebens et al. 2017,
2018). As aquatic ecosystems are highly susceptible
to aquatic AIS introductions, the identification and
integration of cost-effective and widely-applicable
protocols to reduce invader spread is essential.
Invasive aquatic plants have exerted particularly
profound negative impacts on recipient ecological
communities (Schultz and Dibble 2012; Hussner
2014; Kuehne et al. 2016). Virasure® Aquatic can
induce substantial necrosis, morbidity and mortality
of L. major fragmentary propagules. Accordingly,
biosecurity protocols can likely be improved with
the use of this broad-spectrum aquatic disinfectant.
To date, research has largely focused on the efficacy
of Virkon® Aquatic, a similar aquatic disinfectant, to
control aquatic AIS such as Asian clam, Corbicula
fluminea (Barbour et al. 2013), quagga mussel,
Dreissena rostriformis bugensis (Moffitt et al. 2015),
and the gastropod red-rimmed melania, Melanoides
tuberculata (Mitchell et al. 2007), all under varying
exposure times. Treatment of submerged plants
using herbicides is strictly prohibited across Europe
due to adverse environmental impacts, thus inherently
restricting management options for aquatic AIS
(Hussner et al. 2017). Accordingly, the use of aquatic
disinfectants outside of water, to reduce secondary
spread of invaders, is pertinent, timely and more
environmentally friendly.
A 2 minute submersion using 1% Virasure®
Aquatic solution can achieve full L. major fragment
degradation. However, longer exposure times and
greater chemical concentrations will likely increase
the rapidity of fragment mortality. When submersion
is not feasible, a spray treatment should be applied
using longer contact times than assessed within the
scope of the present study, and a higher concentration (≥ 4% solution) should be applied. The
limited efficacy of shorter submersion in, or spraying
treatments with, 1% Virasure® Aquatic solution may
result from a lack of adherence to plant tissue. These
results corroborate with those of Paetzold and
Davidson (2011), wherein an invasive sea squirt was
found to be largely unaffected by spray treatments
with Virkon® Aquatic.
In the present study, we examined relatively large
plant fragments as these are known to exhibit a
greater capacity for regrowth (Wu et al. 2007; Jiang
et al. 2009), and also reduce inhibition of lateral
growth driven through apical dominance (Cline
1991). Yet, the size of fragments examined is still
likely within the threshold of propagules which are
readily entangled with, and transported overland by,
anthropogenic vectors (Barrat-Segretain et al. 1998).
The lack of root growth observed here may be a
result of the timescale permitted, poor anchorage, or
potential apical dominance of samples (Cline 1991;
Wu et al. 2007). Critically, our results demonstrate
that the application of Virasure® Aquatic can induce
substantial and complete degradation of L. major
propagules. The working pH for the main oxidising
ingredient (potassium peroxymonosulfate) of Virasure®
Aquatic is strongly acidic (2.6) when diluted in a 1%
solution at 20 °C, facilitated through the presence of
two organic, malic and sulphamic, acids (see Fish Vet
Group 2015). However, L. major may only be
particularly susceptible to these compounds due to
the species’ characteristic tendency to induce and
tolerate high levels of alkalinity (Stiers et al. 2011).
Furthermore, negligible toxicities to non-target
vertebrate species following short-term exposure to a
compositionally-similar aquatic disinfectant have
been demonstrated (Stockton-Fiti and Moffitt 2017),
and therefore the focal product may be safe for use
proximal to water.
Our promising results suggest further experimental
examination of the efficacy of aquatic disinfectants
to reduce aquatic AIS spread to be critical.
Accordingly, additional trials investigating the impacts
of such chemical solutions on aquatic AIS propagule
stages should be considered, alongside assessments
for potential non-target effects on other native species,
particularly macroinvertebrates associated with aquatic
macrophytes. Further aquatic disinfectant efficacy
examinations towards other existing and emerging
floral and faunal aquatic AIS are urgently required.
Disinfectant trials should concurrently seek to examine
different contact times, recovery conditions and varied
chemical concentrations upon a variety of anthropogenic vectors, such as equipment associated with
angling and boating, in order to maximise the transparency of results. Finally, the incorporation of aquatic
disinfectants within biosecurity management protocols
requires urgent consideration by stakeholder groups.
Acknowledgements
RNC obtained funding support from Queen’s University Belfast
for this study. NEC and JTAD are supported by the Irish EPA
research grant 2015-NC-MS-4. KC is supported through
contributions from Queen’s University Belfast, the University of
Windsor and McGill University. We additionally acknowledge
funding received from NERC. We graciously thank Dr Matthijs
Metselaar at Fish Vet Group for providing Virasure® Aquatic. We
also thank all staff at the Greenacres Golf Centre.
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Author contributions
RNC, KC, JMC and JTAD designed the study; RNC conducted
the experiment and data analysis; RNC produced the first draft of
the manuscript; all authors contributed to writing the manuscript,
which was led by RNC.
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