Spread of invasive species into Scotland: study

Discussion

Much of Scotland is relatively distinct from the rest of Great Britain in terms of climate, with colder winter temperature minima and many fewer frost-free days in winter and spring. This limits the establishment of cold-sensitive invasive non-native species (INNS) from tropical, sub-tropical and Mediterranean regions, some of which have been able to establish in southern England. This limiting effect is likely to be greatest for terrestrial plants and animals, with freshwater INNS, such as submerged plants, fish and terrapins, more buffered against extreme cold air temperatures. North-south gradients in average monthly surface water temperatures are less extreme, and lag behind those in air temperature by several weeks because water heats up and cools down more slowly than land. The natural nutrient status and pH values of freshwaters within Scotland mirror those of the rocks and soils in the catchments. Scotland’s freshwater environment shares greater similarity with that of Wales compared with that of England (Abell, Thieme et al. 2008). Open access legislation, especially to boating and watersports, does however, potentially increase the spread of INNS that are generally introduced through recreational pathways. This may be a particular threat to the arrival of freshwater INNS in Scotland (Chapman et al., 2020). Recent tourism developments in Scotland, such as the promotion and development of the North Coast 500, have led to exceptional increases in the number of visitors to this region of northern Scotland, which could intensify pathways for INNS transported through vehicles, boats, equipment and clothing.

The top 10 and top 30 lists include a diverse range of INNS spanning all environments. Five freshwater species are present in the top 10: three molluscs and two submerged plant species. Freshwaters are considered to be one of the most vulnerable habitats, affected greatly by multiple pressures, such as climate change, overexploitation, sewage, nutrient pollution and recreation which can act synergistically with pressures from INNS (Birk, Chapman et al. 2020). Indeed, there is increasing attention on the interactions amongst drivers of biodiversity change including climate change and biological invasions. Some of the UK’s rarest fish, such as the cold-water loving species, the Arctic charr (Salvelinus alpinus) and powan (Coregonus lavaretus), are found in Scottish lochs. These species are vulnerable to the effects of climate change, which may, in turn, facilitate the expansion of INNS that could outcompete them for resources. A good example of where this has already occurred is in Loch Lomond, with the introduction of the non-native perch-like fish, the ruffe (Gymnocephalus cernuus) , in the early 1980s as live bait by anglers. Subsequently, the ruffe population expanded and was implicated in the decline of the native powan in one of its only two natural sites in Scotland (Winfield, Fletcher et al. 2011).

Freshwater biodiversity is also culturally and economically important in Scotland, with salmon and trout angling in particular contributing significantly to some rural Scottish economies (Marine Scotland 2017). The two freshwater invasive non-native plant species (floating pennywort, Hydrocotyle ranunculoides, and parrot’s feather, Myriophyllum aquaticum) are widely distributed in England and Wales but have only been recorded (and removed) from one site each in northern Scotland. They can colonise vegetatively through the introduction of stem fragments and are very competitive, forming dense emergent stands that can outcompete native flora, impact water quality and alter natural flow regimes. The latter impact can lead to social and economic impacts through exacerbating flood risk.

Of the three invasive non-native mollusc species, only one, zebra mussel (Dreissena polymorpha), has been recorded in Scotland previously, where it was present in the Forth & Clyde Canal and Union Canal and in Perth Docks (a brackish habitat). It is thought to have been lost from these sites in the 1970s, due to a severe deterioration in water quality. There have only been three records of zebra mussel (D. polymorpha) in Scotland in recent decades, relating to interceptions of overland transport of canal boats, and these did not establish. Quagga mussel (D. bugensis) has also been intercepted in Scotland before it was able to enter the canal network. Given this evidence, and the fact that it is locally distributed in many English rivers and canals, D. polymorpha is considered to be a priority species because of its imminent potential for arrival, and clear introduction pathway through boat traffic in the canal network. The other two mussel species are considered to be high priority because they are spreading quickly in England. D. bugensis has also been intercepted in Scotland before it was able to enter the canal network and both Dreissena species have been intercepted simultaneously. All three species have also established in Ireland in recent decades, illustrating their ongoing range expansion. In terms of biodiversity impact, all three mussels have the capacity to outcompete native molluscs and alter freshwater benthic habitats (Sousa, Novais et al. 2014, Modesto, Dias et al. 2021), facilitating establishment of other INNS (Gallardo and Aldridge 2015).

There is evidence from long-term lake data that indicates that Dreissena invasion in lakes can lead to greater dominance by harmful algal blooms of cyanobacteria, due to selective feeding. This can have consequent impacts on biodiversity, economic interests and health. The Dreissena species are grouped together in the top 10 list for communication purposes, in part because they have previously demonstrated a shared introduction pathway and because for recording purposes the public are asked to look out for stripey mussels. The targeting of control actions may vary for the two species due to their respective habitat requirements/impacts, particularly when it comes to engaging with knowledgeable audiences. The invasion capacity of Corbicula fluminea appears to be particularly high due to its life strategy traits (rapid growth, early sexual maturity, short life span, high fecundity, extensive dispersal capacities). For these reasons, its rapid spread in England, and its possible role in the apparent loss of a critically endangered mussel species (Sphaerium solidum) from the UK fauna, it has been the focus for a rapid risk assessment by the GB Non-native Species Secretariat^[10].

Crepidula fornicata, commonly known as the American slipper limpet was the only marine species included in the top 10 priority list. This mollusc arrived on the south coast of the UK between 1887 and 1890, with American oysters imported from North America (Bohn, Richardson et al. 2012). It has since spread throughout the north-east Atlantic and is now established as far north as Belfast Lough in the UK. This species attaches to other slipper limpets and can form long chains of up to 12 individuals. It also readily attaches to commercially important bivalve species, such as oysters, mussels and scallops. The intentional movement of these commercial species for stocking purposes has been identified as the primary pathway for the spread of C. fornicata throughout Europe. The slipper limpet has no species-specific predators, it is long-lived and has high reproductive viability and fecundity. It can occupy a wide range of habitats, including harbours, marinas, inlets, bays, estuaries and open coast, settling on substrates ranging from rocks and stones to artificial surfaces. This species can form dense populations (up to 10,000 individuals m^-2), to the extent that in certain regions, commercial oyster grounds require regular clearing before new seed is sown. It can also readily alter the nature of the sediment substrata and smother areas previously dominated by native bivalves. A number of records exist for C. fornicata in Scotland, but to date none of these have been verified. With the possible spread through fishing and culture practices and/ or through natural dispersal of the pelagic planktonic larval stage, it is highly likely, therefore, that this species will become established in Scottish waters within the next 10 years.

Alongside the two aquatic plant species (floating pennywort, Hydrocotyle ranunculoides, and parrot’s feather, Myriophyllum aquaticum) one terrestrial plant species was also included in the top 10 INNS, the northern highbush blueberry (hereafter blueberry), Vaccinium corymbosum, and its hybrids (Vaccinium corymbosum x angustifolium). It is a deciduous shrub reaching a height of 1.8–3.7 m and can form dense thickets through vegetative growth (suckering). The species is a member of the Ericaceae (heather) family and is found in open and wooded areas mostly on acidic soils in its native range of eastern North America (from Florida in the south to Ontario and Nova Scotia in the north). This species and its hybrids are already established elsewhere in Europe. For example, in northern Germany, plants have spread from hybrid commercial crop plantations to peat bog and planted Scots pine (Pinus sylvestris) habitats (located within 3 km of plantations). The fruits, each fruit containing multiple seeds, are likely to be bird-dispersed. This means that spread potential within landscapes with open commercial plantations is likely to be high. Blueberry is not able to self-pollinate, which may serve to limit its reproduction and establishment when populations are small. However, the ability to spread to and form thickets in important habitats that occur within Scotland means that the potential for biodiversity and ecosystem impacts is high, through outcompeting lower-growing plant species, and possibly through altering water content of bog soils due to increased rates of evapotranspiration.

Another notable invasive non-native plant species included within the top 30 is Anemanthele lessoniana (synonym: Stipa arundinacea) or pheasant’s tail (or sometimes called New Zealand wind grass). Pheasant’s tail is a fast-growing perennial, clump-forming grass with short rhizomes, introduced and widely planted as an ornamental in gardens within Britain, including Scotland. Pheasant’s tail is easy to grow and has received the Royal Horticultural Society (RHS) award of garden merit; according to the RHS, it has a hardiness level of H4, which means the species is hardy throughout most of Britain (withstanding minimum temperatures of -10 to -5° C). This grass produces large numbers of seeds which germinate easily and has already been recorded as established in England and Wales. The species may already be on the verge of escaping plantings and establishing in Scotland. While the species is known to be introduced to Britain, there is little information available on its introduction and invasion history elsewhere. However, this grass tends to produce a large amount of thatch, representing a potential fire risk in fire-prone habitats. Production of thatch could also alter litter inputs into soils and prevent germination of seeds of other species, though concrete evidence of impacts is lacking. The prolific production of small seeds that could be wind-dispersed means that spread potential from plantings to semi-natural and natural habitats is likely to be high.

The top 10 list included two vertebrates: Reeve’s muntjac (Muntiacus reevesi) and raccoon (Procyon lotor) although there was considerable discussion around the other non-native vertebrates included within the top 30. The Reeve’s muntjac is a small deer that can have a big impact. Introduced from Asia, muntjacs have been very successful in colonising much of England and parts of Wales, thriving in woodland, farmland and even suburban and garden habitats. They are able to breed throughout the year and reach densities of over 100 animals per square kilometre; where muntjacs become abundant they can have a serious impact on native vegetation through browsing pressure. Woodland herbs, understorey shrubs and tree regeneration can be seriously damaged, changing the habitat structure and vegetation composition to the detriment of native flora and fauna. Muntjacs would be a significant threat to Scotland’s existing woodlands and goals for woodland expansion. Raccoons are highly adaptable omnivores that originate from North America but have established large populations in Germany (estimated at 200 000–400 000 individuals) and smaller populations in France, Belarus and Azerbaijan (Roy, Peyton et al. 2014). Raccoons pose a threat to biodiversity through predation and disease transmission (Roy, Tricarico et al. 2022).

Four species of geoplanid flatworms, Australoplana sanguinea, Caenoplana bicolor, Kontikia andersoni and Obama nungara, are listed among the top 10 on the basis of impact studies in other parts of their range or the equivalence in the biology to other well-studied species (Boag & Yeates 2001). Flatworms are voracious top-level predators in soil communities. With the exception of C. bicolor, the other three species are known to predate, among other groups, on lumbricid earthworms that are widely recognised as key ecosystem engineers. Thus, the main impact of the flatworms is likely to be indirect, but would affect soil structure, nutrient cycling and ultimately plant communities, while also having a direct predatory impact on native soil invertebrates such as gastropods (Keith et al. 2018). The flatworms listed here are known from invaded ranges south of Scotland in the UK, but also from the European continent (e.g., France, Germany, Italy) and elsewhere in the world. Once established there is currently no known method of removal or control (Justine et al. 2020, Mori et al. 2021). These invasive non-native flatworm species are thought to be moved with horticultural materials and ornamental plants, as most records are from urban environments, such as gardens and parks. However, the native and other invaded ranges of these flatworms suggest that there is the potential that they could move into non-urban environments.

The impact of beetles, similarly to that of the flatworms, is mostly indirect, damaging and removing trees, which are foundation species, with often well-defined communities associated with them. A notable potential invader is Agrilus planipennis, the emerald ash borer. Known to cause significant damage to its hosts, Fraxinus spp., in other parts of its invaded range, such as North America, the trees in Europe are already highly impacted by ash dieback, Hymenoscyphus fraxineus, a non-native fungal disease. While a small proportion, estimated to be 1–3% of the ash trees in the UK, show signs of disease tolerance, a dual challenge by pest and disease would make any management harder (Broome et al. 2019).

It is important to mention two species not included in the Top Ten priority list, despite their predicted high biodiversity and economic impact. Both are not yet recorded from Great Britain or Ireland, but are already recognised in plant and animal health legislation in Scotland because of their potential for severe economic impact. They are, therefore, already a focus of legislation to prevent their establishment and spread. Agrilus planipennis, the emerald ash borer, is a beetle that can cause extensive mortality of ash trees in regions where it has been introduced, including eastern North America, the European part of Russia, and more recently eastern Ukraine. A. planipennis is listed as a priority quarantine pest in Schedule 1 of The Plant Health (Amendment etc.) (EU Exit) Regulations 2020/1482 and as such its introduction into and movement within Great Britain is banned with a detailed Plant Health Response Plan in place to prevent its establishment and spread. Gyrodactylus salaris (salmon fluke) is a small parasitic flatworm. In Norway, catastrophic losses of Atlantic salmon (Salmo salar) occurred following the introduction of G. salaris to the country in the 1970s on imported live fish. Many Norwegian rivers were infected, and their salmon populations decimated (Marine Scotland, 2019). Although the most severely affected species is Atlantic salmon, G. salaris has been reported on other native fish species, such as Arctic char (Salvelinus alpinus), grayling (Thymallus thymallus) and brown trout (Salmo trutta). Because of the severe economic and biodiversity impacts this species poses, the Scottish Government has introduced strict provisions under the Aquatic Animal Health (Scotland) Regulations 2009 to eradicate, prevent or limit the spread of G. salaris in Scotland.

From the pathway analysis, horticultural and ornamental pathways emerged as the most important potential ways of introduction of INNS. This result is due to the high number of plants within all the lists assessed. Additionally, as these two pathways can be difficult to separate for many species, this could have compounded the high representation of these pathways. The pet pathway is considered important for introducing species on the horizon scanning long list but was not ranked as high for already established non-native species. Pathways in the contaminant category have historically been important in introducing non-native species. It is likely that this will continue to be the case as is evident from the analysis of the pathways considered relevant to the horizon scanning long list derived in this study. Contaminant of animals, seed contaminant and contaminant of habitat material are associated with a number of the non-native species listed. Furthermore, the natural dispersal of species from an existing invaded range into Scotland is considered an important pathway of arrival of INNS.

The results from the horizon scanning study coupled with the pathway analysis provide detailed information to prioritise actions to prevent the establishment of new INNS in Scotland, including action plans for priority pathways of introduction and spread. Noting the importance of pathways such as the ornamental and horticultural pathways, there are opportunities to further promote biosecurity campaigns such as Be Plant Wise. However, the pathway analysis also highlights a diverse range of pathways including the importance of contaminant pathways.