Bacterial diversity and viral discovery in the invasive Argentine ant (Linepithema humile)

10.26686/wgtn.17014649 ◽

2021 ◽

Author(s):

◽

Alexandra Sébastien

Keyword(s):

Biological Control ◽

Invasive Species ◽

Population Dynamics ◽

New Zealand ◽

Bacterial Diversity ◽

Linepithema Humile ◽

Argentine Ant ◽

Invasive Ants ◽

Argentine Ants ◽

Species Population

Invasive species can lead to major economic and ecological issues. For this reason, biological controls are being developed in order to help with invasive species population management. Pathogenic bacteria and viruses offer good biological control opportunities as both micro-organisms have played a role in natural population declines. However, beneficial bacteria and viruses associated with the targeted invasive species may interfere with biological controls, by protecting their hosts from infections. Previous knowledge on both pathogenic and beneficial bacteria and viruses present in invasive species may then support the development of an active and efficient biological control. The Argentine ant, Linepithema humile, is a South American invasive ant species that has successfully spread over five continents. The ants were introduced to New Zealand after a complex invasion path, from Argentina their home range to Europe, then to Australia and finally to New Zealand. In their new environments, invasive Argentine ants affect species diversity and can cause agricultural losses. In the absence of any biological controls, the Argentine ant population is controlled by chemical sprays and poison baits. Management of these invasive ants in New Zealand is estimated to cost NZ$ 60 million a year. The Argentine ant population in New Zealand was reported to have unexpectedly declined. It was hypothesised that pathogens were the cause of this population collapse. In this study, bacteria and viruses present in the invasive ants were investigated using 454 sequencing and Illumina sequencing for future developments of possible biological controls for the Argentine ants, and a better understanding of the observed population decline in New Zealand. Bacterial diversity present in Argentine ants either declined or diminished along the invasion pathway. At the same time, the invasive ants maintained a core of nine bacteria genera, including Lactobacillus and Gluconobacter, two bacterial genera with members known for their beneficial associations with honey bees. The presence of these core bacteria may have participated in the success of Argentine ants in their new environments. In the laboratory, the use of ampicillin and gentamicin antibiotics on the ants increased bacterial diversity present in the ants. Furthermore, ampicillin, kanamycin and spectinomycin antibiotic treatments increased ant survival but did not affect the ant fitness or intra-species aggressiveness. Only spectinomycin treated ants presented a higher level of inter-species aggressiveness. Bacterial diversity may play an important role in the ant health and at length population dynamics. Finally, Argentine ants are the hosts of two viruses: the Deformed wing virus (DWV) involved in colony collapse disorder in honey bees, and Linepithema humile virus 1 (LHUV-1), a new virus related to DWV. Both viruses actively replicate within the ants, indicating a possible reservoir role of the ants. However, the effects of the viruses on the ants are not yet known. Further viral infection in the laboratory under different stress conditions and / or antibiotic treatment will give an insight in the role played by these viruses in the observed population collapse of Argentine ants in New Zealand. LHUV-1 may offer a possibility in the development of the first biological control for Argentine ants, depending on its specificity and its effects. This dissertation provides a first insight in the core bacteria as well as potential harmful viruses present in Argentine ants. These bacteria and viruses may play a role in the ant population dynamics. Invasive species may co-introduce harmful pathogens with them, and participate to the spread of local ones. The pathogens may affect both invasive ants and native species population dynamics.

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Invasive ants carry novel viruses in their new range and form reservoirs for a honeybee pathogen

Biology Letters ◽

10.1098/rsbl.2015.0610 ◽

2015 ◽

Vol 11 (9) ◽

pp. 20150610 ◽

Cited By ~ 30

Author(s):

Alexandra Sébastien ◽

Philip J. Lester ◽

Richard J. Hall ◽

Jing Wang ◽

Nicole E. Moore ◽

...

Keyword(s):

New Zealand ◽

Microbial Diversity ◽

Animal Species ◽

Linepithema Humile ◽

Argentine Ant ◽

Invasive Ants ◽

Argentine Ants ◽

Deformed Wing Virus ◽

Hymenopteran Species ◽

Exotic Animal

When exotic animal species invade new environments they also bring an often unknown microbial diversity, including pathogens. We describe a novel and widely distributed virus in one of the most globally widespread, abundant and damaging invasive ants (Argentine ants, Linepithema humile ). The Linepithema humile virus 1 is a dicistrovirus, a viral family including species known to cause widespread arthropod disease. It was detected in samples from Argentina, Australia and New Zealand. Argentine ants in New Zealand were also infected with a strain of Deformed wing virus common to local hymenopteran species, which is a major pathogen widely associated with honeybee mortality. Evidence for active replication of viral RNA was apparent for both viruses. Our results suggest co-introduction and exchange of pathogens within local hymenopteran communities. These viral species may contribute to the collapse of Argentine ant populations and offer new options for the control of a globally widespread invader.

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The widespread collapse of an invasive species: Argentine ants ( Linepithema humile ) in New Zealand

Biology Letters ◽

10.1098/rsbl.2011.1014 ◽

2011 ◽

Vol 8 (3) ◽

pp. 430-433 ◽

Cited By ~ 34

Author(s):

Meghan Cooling ◽

Stephen Hartley ◽

Dalice A. Sim ◽

Philip J. Lester

Keyword(s):

Climate Change ◽

Invasive Species ◽

New Zealand ◽

Argentine Ant ◽

Environmental Costs ◽

Argentine Ants ◽

Ant Communities ◽

Mean Survival Time ◽

Colony Collapse ◽

Increasing Temperature

Synergies between invasive species and climate change are widely considered to be a major biodiversity threat. However, invasive species are also hypothesized to be susceptible to population collapse, as we demonstrate for a globally important invasive species in New Zealand. We observed Argentine ant populations to have collapsed in 40 per cent of surveyed sites. Populations had a mean survival time of 14.1 years (95% CI = 12.9–15.3 years). Resident ant communities had recovered or partly recovered after their collapse. Our models suggest that climate change will delay colony collapse, as increasing temperature and decreasing rainfall significantly increased their longevity, but only by a few years. Economic and environmental costs of invasive species may be small if populations collapse on their own accord.

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Controlling invasive Argentine ants, Linepithema humile, in conservation areas using horizontal insecticide transfer

Scientific Reports ◽

10.1038/s41598-019-56189-1 ◽

2019 ◽

Vol 9 (1) ◽

Cited By ~ 3

Author(s):

Grzegorz Buczkowski ◽

Theresa C. Wossler

Keyword(s):

Horizontal Transfer ◽

Control Strategies ◽

Linepithema Humile ◽

Argentine Ant ◽

Environmental Benefits ◽

Effective Control ◽

Conservation Areas ◽

Invasive Ants ◽

Argentine Ants ◽

Management Tools

AbstractInvasive ants are major agricultural and urban pests and a significant concern in conservation areas. Despite long history of control and eradication efforts, invasive ants continue to spread around the globe driven by a multitude of synergistic factors. Lack of effective management tools is one of the biggest challenges in controlling invasive ants. The goal of the current study was to improve the efficacy and safety of ant management and to develop effective control strategies for sensitive conservation areas. We utilized the Argentine ant (Linepithema humile) as a model system to evaluate a target-specific pesticide delivery system that exploits the interconnected nature of social insect colonies to distribute a toxicant effectively within the colony. The approach, based entirely on horizontal transfer, takes advantage of various levels of social interactions in ant colonies to disseminate a toxicant throughout the colony. Results of laboratory studies coupled with LC/MS/MS analysis demonstrate that fipronil is toxic to Argentine ants in extremely small (nanogram) quantities and is efficiently transferred from a single treated donor to multiple recipients, causing significant secondary mortality. A field study was conducted in native fynbos plots invaded by Argentine ants. The study consisted of collecting naïve workers, treating them with fipronil, and releasing them within invaded plots. Results show that the release of fipronil-treated ants reduced Argentine ant abundance by >90% within 24 h. The horizontal transfer approach offers environmental benefits with regard to pesticide use in ecologically sensitive environments and appears ideally suited for ant management in conservation areas.

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Multi-host viruses in Argentine ants and honey bees: Increased viral disease in honey bees is associated with Argentine ants

10.26686/wgtn.16912519 ◽

2021 ◽

Author(s):

◽

Jana Dobelmann

Keyword(s):

Honey Bees ◽

Rna Viruses ◽

Population Control ◽

Argentine Ant ◽

Viral Dynamics ◽

Invasive Ants ◽

Argentine Ants ◽

Deformed Wing Virus ◽

Tomato Ringspot Virus ◽

Bee Health

Emerging infectious diseases threaten public health, livestock economies, and wildlife. Human-mediated species introductions can alter host and pathogen communities that shape the dynamics of infectious diseases. Several RNA viruses that have been linked to population declines in wild pollinators and losses of managed honey bees have been detected in multiple other species and are suspected to circulate within insect communities. Yet, we lack an understanding of how disease dynamics are affected by the introduction of novel species. These introduced species include invasive ants, which can disturb honey bees and become a pest in apiaries. The Argentine ant (Linepithema humile) is a globally successful invader that has been observed to attack bees and multiple bee-associated viruses have been detected in this ant species. Here, I studied interactions between Argentine ants and European honey bees (Apis mellifera) and how these interactions affect viral dynamics in beehives. I first tested a range of pollinators and associated insects for RNA viruses that are pathogenic to honey bees. Bee-associated viruses showed evidence for active viral replication in several pollinator species but also in species that cohabit in beehives such as ants, spiders, and cockroaches. Using phylogenetic analyses, I found that viral transmission within communities was shaped by geographic origin rather than being restricted by species barriers. Next, I used a longitudinal field study to test whether Argentine ant presence affected pathogen infections and survival in beehives. Argentine ants tested positive for three bee-associated viruses even before beehives were moved into ant-infested sites. Increased levels of deformed wing virus in beehives in autumn were associated with ant presence, although hive mortality was not affected by ants over the duration of this experiment. I used RNA sequencing on a subset of honey bee samples collected during autumn to study the RNA virome and identify transcriptomic responses associated with ant presence. Twelve RNA viruses were found in beehives, among those, three plant-associated viruses and an unclassified RNA virus that had not previously been observed in honey bees. Deformed wing virus showed the highest viral titres in most hives, but was only marginally affected by ant presence. Sacbrood virus and tomato ringspot virus levels were increased in hives with ants, however, both viruses are not known to infect Argentine ants and the plant-associated tomato ringspot virus seems unlikely to affect bee health. Lastly, I tested the feasibility of controlling Argentine ants in apiaries using a novel pest control strategy. RNA interference is a conserved cellular gene regulation mechanism that could be used to silence specific genes in ants. Using double-stranded RNA (dsRNA) to silence two immune-related genes in Argentine ants was expected to increase pathogen susceptibility, which could then lead to higher pathogen levels that reduce ant numbers. My results indicated that no consistent immune silencing could be achieved in the field. Immune gene expression changes were observed, but pathogen titres were not affected, and ant numbers stayed high. Argentine ant control using a conventional insecticide significantly increased bee survival, whereas many hives in the dsRNA and control group abandoned their hives due to ant attacks. Although population control was not successful using the two Argentine ant-specific dsRNAs, insights into ant immunity and ant-bee interactions could improve the development of novel control strategies. Bee-associated viruses have repeatedly been detected in ant species, yet, this is one of the first studies to investigate whether ants affect viral dynamics in honey bees. I showed that invasive Argentine ants are associated with increases in viral pathogens in honey bees. The mechanisms by which ants affect bee disease are unknown, although there is some evidence for ants transmitting viruses or causing stress responses in bees that affect immunity. The findings of this thesis highlight the risk of invasive ant species disrupting pollination services. New and environmentally-friendly methods to control invasive species are urgently needed to improve bee health and limit the spread of invasive ants, such as Argentine ants. The high prevalence of bee-associated viruses and viral diversity in ants suggests that pathogens that are suitable for population control might be present in ant populations, although risks of spillovers into other species need to be carefully considered.

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The interface between invasive species science and legal regulation, using Hymenopteran species and their pathogens as a model system

10.26686/wgtn.17131952.v1 ◽

2021 ◽

Author(s):

◽

Evan Brenton-Rule

Keyword(s):

Invasive Species ◽

New Zealand ◽

Biological Invasions ◽

Honey Bee ◽

Legal Regulation ◽

Argentine Ants ◽

Deformed Wing Virus ◽

Introduced Range ◽

The Impact ◽

Bee Virus

Biological invasions are one of the major causes of biodiversity decline on the planet. The key driver of the global movement of invasive species is international trade. As a response to trade driven invasive species risk, international and domestic regulations have been promulgated with the goal of managing the spread and impact of non-native species. My aims in this thesis were twofold. First, my goal was to review a subset of international and domestic regulations with a view to commenting on their fitness for purpose and suggesting potential improvements. Second, I used the example of non-native and invasive Hymenoptera, as well as their pathogens, to illustrate the risks posed by invasive species and gaps in their management. In order to assess international and domestic regulations, I reviewed the World Trade Organization’s (WTO) Agreement on Sanitary and Phytosanitary Measures, as well as associated disputes. I argue that the WTO’s regulatory system does, for the most part, allow domestic regulators to manage invasive species risk as they see fit. Subsequently, the focus of the thesis narrows to investigate New Zealand’s pre- and post-border regime managing invasive species. I argue that New Zealand’s pre-border approach represents international best practice, but the post-border management of species is fragmented. The power to manage invasive species has been delegated to sub-national and regional bodies, which typically approach invasive species management in different ways. This variation has led to regulatory inconsistencies in pests managed and funding allocated. There appears to be a substantial lack of planning in some spaces, such as the risk of aquatic invasions. I make recommendations to ameliorate these inconsistencies. My second aim involved the study of non-native and invasive Hymenoptera in New Zealand, as well as the pathogens they carry, in order to illustrate the risks posed by invasive species and gaps in their management. I show that the globally widespread invasive Argentine ant (Linepithema humile) may play a role in the pathogen dynamics and mortality of honey bee hives where the species occur sympatrically. Hives in the presence of Argentine ants suffered significantly higher mortality rates relative to hives without ants and always had higher levels of a honey bee pathogen Deformed wing virus. I demonstrate that honey bee pathogens are found in a range of invasive Hymenoptera in New Zealand. I amplify entire genomes of the honey bee virus Kashmir bee virus (KBV) from three species of non-native or invasive Hymenoptera (Argentine ants, common wasps and honey bees). I show that there is KBV strain variability within and between regions, but more between regions. Further, I demonstrate the result that as sampled KBV sequence length increases, so too does sampled diversity. These results highlight how ‘an’ invasive species is typically not alone: they carry a range of diseases that are almost always not considered in international and regional management plans. Patterns of non-native Hymenoptera carrying honey bee diseases were not restricted to New Zealand. I used mitochondrial DNA to find the likely origin of invasive populations of the globally distributed invasive German wasp. I demonstrate that German wasps show reduced genetic diversity in the invaded range compared to the native range. Populations in the introduced range are likely to have arrived from different source populations. In some regions there were likely multiple introductions. Other regions are genetically homogenous and represent potential areas for use of gene drive technologies. All four different honey bee pathogens assayed for were found in German wasp populations worldwide. These results highlight how the introduction of one exotic species likely brings a range of pathogens. This example of pathogens in Hymenoptera is likely to be true for nearly all non-native introductions. Many of the impacts of biological invasions, such as predation and competition, are relatively obvious and are frequently studied. However some, such as the impact of pathogens, are unseen and poorly understood. Legal regulation is often a post-hoc response implemented once a problem has already arisen. At a global level regulatory regimes operate relatively effectively. As the focus becomes more granular, such as the case of pathogens of Hymenoptera, fewer controls exists. This thesis helps to reduce uncertainty in this area as well as makes recommendations as to how these risks may be managed.

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Temperature-dependent development of the Argentine ant,Linepithema humile(Mayr) (Hymenoptera: Formicidae): a degree-day model with implications for range limits in New Zealand.

New Zealand Entomologist ◽

10.1080/00779962.2003.9722113 ◽

2003 ◽

Vol 26 (1) ◽

pp. 91-100 ◽

Cited By ~ 40

Author(s):

Stephen Hartley ◽

Philip J. Lester

Keyword(s):

New Zealand ◽

Linepithema Humile ◽

Argentine Ant ◽

Range Limits ◽

Temperature Dependent ◽

Dependent Development ◽

Degree Day

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Population dynamics of invasive Argentine ant Linepithema humile Mayr, 1868 (Hymenoptera: Formicidae) haplotypes in Kobe Port, Japan, and implications for the prediction of future dispersal and effective management

BioInvasions Records ◽

10.3391/bir.2021.10.2.24 ◽

2021 ◽

Vol 10 (2) ◽

pp. 467-476

Author(s):

Yugo Seko ◽

Yu Maebara ◽

Naoyuki Nakahama ◽

Takuya Nakamori ◽

Naoto Ishiwaka ◽

...

Keyword(s):

Population Dynamics ◽

Linepithema Humile ◽

Argentine Ant ◽

Effective Management

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Invasion Impact and Biotic Resistance by Invertebrate Communities

10.26686/wgtn.17003371.v1 ◽

2021 ◽

Author(s):

◽

Habteab Tsegai Habtom

Keyword(s):

Invasive Species ◽

New Zealand ◽

Walking Speed ◽

Biotic Resistance ◽

Interactive Effect ◽

Effect Of Temperature ◽

Beetle Species ◽

Resident Species ◽

Argentine Ants ◽

Arthropod Species

Invasive species have been recognized as one of the greatest threats to global biodiversity and can have dire economic consequences. Yet rates of invasion are increasing due to the fast and growing network of transportation across the globe. The establishment, spread and impact of invasive species are affected by environmental conditions as well as resident species. Species respond differently to the same abiotic factors and different native species can respond either positively or negatively to invasion. The interaction between invasive and resident species, as well as the effect of temperature on invasive species, has gained much attention. The synergistic effect of suboptimal temperature and biotic resistance could have a much stronger limiting or controlling effect on invasive species than either factor alone. Linepithema humile (Argentine ants) are invasive species originally from a Mediterranean climate, but successfully spreading into extra range habitats. The establishment and spread of these ants in temperate New Zealand represents an ideal model system for studying invasion biology in terms of temperature limits and biotic resistance effects. I investigated the changing distribution of the invasive species the Argentine ants over multiple years at five sites in New Zealand. To test whether their rate of spread corresponds with microclimate I investigated their fine-scare distribution patterns and evaluated the number of generations they may develop seasonally and annually in different microhabitat types. I also evaluated their impact on other arthropod species. I conducted a laboratory experiment to evaluate the effect of temperature on their aggression towards other species, walking speed, and foraging abundance. Similarly, I tested the effect of biotic resistance from other ant species (Monomorium antarcticum and Prolasius advenus) with varying colony sizes. I investigated whether there was any interactive effect of temperature and biotic resistance on the Argentine ants. The distribution of Argentine ants had declined across many invasion fronts over the past 7-8 years. They were more likely to be found in concrete, short grass and sandy habitats, which provide warm microsites. Degree-day calculations predicted that they could develop between 2.5 to 3 generations in each of the above microhabitats per year in urban and rural sites while they were predicted to be unable to develop one generation under tree habitats. In tall grass microhabitats they were predicted to develop between 1-1.5 generations per year. The Argentine ants were hypothesised to adversely affect many other arthropod species. Richness and abundance of resident beetle species were negatively correlated with the invasion of the Argentine ants. Areas invaded by the Argentine ants were also associated with a greater number of exotic beetle species, which may imply secondary invasion. Laboratory experiments showed that lowering temperatures below 17°C negatively affected the Argentine ants‟ walking speed, foraging abundance, aggression and their resource control. A high colony size of M. antarcticum (the competing ant species) affected the foraging success of Argentine ants, and the effect was stronger when coupled with unsuitable temperature (17°C and below). Therefore, Argentine ants are weak competitors at low temperature levels. The results of my thesis underline the importance of biotic and abiotic resistances, their interactive effect as well as the effect of the Argentine ants on other species. Based on climatic considerations and the habitat preferences of resident species it may be possible to predict future spread of the Argentine ants. More importantly, knowledge of microhabitat preferences and biotic resistance may help future control measures against Argentine ants based on management of vegetation structure and microhabitat availability.

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Multi-host viruses in Argentine ants and honey bees: Increased viral disease in honey bees is associated with Argentine ants

10.26686/wgtn.16912519.v1 ◽

2021 ◽

Author(s):

◽

Jana Dobelmann

Keyword(s):

Honey Bees ◽

Rna Viruses ◽

Population Control ◽

Argentine Ant ◽

Viral Dynamics ◽

Invasive Ants ◽

Argentine Ants ◽

Deformed Wing Virus ◽

Tomato Ringspot Virus ◽

Bee Health

Emerging infectious diseases threaten public health, livestock economies, and wildlife. Human-mediated species introductions can alter host and pathogen communities that shape the dynamics of infectious diseases. Several RNA viruses that have been linked to population declines in wild pollinators and losses of managed honey bees have been detected in multiple other species and are suspected to circulate within insect communities. Yet, we lack an understanding of how disease dynamics are affected by the introduction of novel species. These introduced species include invasive ants, which can disturb honey bees and become a pest in apiaries. The Argentine ant (Linepithema humile) is a globally successful invader that has been observed to attack bees and multiple bee-associated viruses have been detected in this ant species. Here, I studied interactions between Argentine ants and European honey bees (Apis mellifera) and how these interactions affect viral dynamics in beehives. I first tested a range of pollinators and associated insects for RNA viruses that are pathogenic to honey bees. Bee-associated viruses showed evidence for active viral replication in several pollinator species but also in species that cohabit in beehives such as ants, spiders, and cockroaches. Using phylogenetic analyses, I found that viral transmission within communities was shaped by geographic origin rather than being restricted by species barriers. Next, I used a longitudinal field study to test whether Argentine ant presence affected pathogen infections and survival in beehives. Argentine ants tested positive for three bee-associated viruses even before beehives were moved into ant-infested sites. Increased levels of deformed wing virus in beehives in autumn were associated with ant presence, although hive mortality was not affected by ants over the duration of this experiment. I used RNA sequencing on a subset of honey bee samples collected during autumn to study the RNA virome and identify transcriptomic responses associated with ant presence. Twelve RNA viruses were found in beehives, among those, three plant-associated viruses and an unclassified RNA virus that had not previously been observed in honey bees. Deformed wing virus showed the highest viral titres in most hives, but was only marginally affected by ant presence. Sacbrood virus and tomato ringspot virus levels were increased in hives with ants, however, both viruses are not known to infect Argentine ants and the plant-associated tomato ringspot virus seems unlikely to affect bee health. Lastly, I tested the feasibility of controlling Argentine ants in apiaries using a novel pest control strategy. RNA interference is a conserved cellular gene regulation mechanism that could be used to silence specific genes in ants. Using double-stranded RNA (dsRNA) to silence two immune-related genes in Argentine ants was expected to increase pathogen susceptibility, which could then lead to higher pathogen levels that reduce ant numbers. My results indicated that no consistent immune silencing could be achieved in the field. Immune gene expression changes were observed, but pathogen titres were not affected, and ant numbers stayed high. Argentine ant control using a conventional insecticide significantly increased bee survival, whereas many hives in the dsRNA and control group abandoned their hives due to ant attacks. Although population control was not successful using the two Argentine ant-specific dsRNAs, insights into ant immunity and ant-bee interactions could improve the development of novel control strategies. Bee-associated viruses have repeatedly been detected in ant species, yet, this is one of the first studies to investigate whether ants affect viral dynamics in honey bees. I showed that invasive Argentine ants are associated with increases in viral pathogens in honey bees. The mechanisms by which ants affect bee disease are unknown, although there is some evidence for ants transmitting viruses or causing stress responses in bees that affect immunity. The findings of this thesis highlight the risk of invasive ant species disrupting pollination services. New and environmentally-friendly methods to control invasive species are urgently needed to improve bee health and limit the spread of invasive ants, such as Argentine ants. The high prevalence of bee-associated viruses and viral diversity in ants suggests that pathogens that are suitable for population control might be present in ant populations, although risks of spillovers into other species need to be carefully considered.

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