Author/s Kevin A. Hughes (1)*, Katarzyna J. Chwedorzewska (2), Marco A. Molina Montenegro (3) and Luis R. Pertierra (4) (1) British Antarctic Survey, Natural Environment Research Council, Cambridge, United Kingdom. *[email protected] (2) Department of Botany, Warsaw University of Life Sciences, Warsaw, Poland (3) Centre for Integrative Ecology, Instituto de Ciencias Biológicas, Universidad de Talca, Talca, Chile (4) Universidad Rey Juan Carlos, Spain Brief Overview Non-native species introductions and establishment are having substantial and likely irreversible environmental impacts on Antarctic ecosystems and biodiversity. Non-native species, or species that live outside of their natural range, can spread inter-regionally (from outside the Antarctic) or intra-regionally (within the Antarctic). Inadvertent introductions may occur when propagules, such as seeds, soil, and invertebrate eggs, or whole organisms are transported to Antarctica. Transportation may occur in association with clothing and personal belongings of visitors, cargo, and fresh produce, transported to or within Antarctica by land vehicles, ships, or aircraft. Currently, the available data indicate that the Antarctic Peninsula region is the Antarctic Treaty area where most non-native species have been recorded. While Antarctic introductions are likely to increase, facilitated by climate change and increased human activity in the region, future rates of introduction and establishment could be reduced with the implementation of effective biosecurity mitigation and action. Despite some success in the eradication of non-native plants and insects inside buildings, some established invertebrate species have already begun to increase their distribution within Antarctica with largely unknown impacts upon native organisms and habitats. Detailed Overview General introduction Humans have spread organisms widely across the Earth, many of them unintentionally, through commerce, exploration, and travel. Some of these organisms are versatile and can adapt to and thrive in new environments. Globally, this movement of organisms by humans to areas beyond their natural ranges (often then referred to as non-native species) is responsible for major changes in ecosystem structure and functioning and reductions in biodiversity. Definitions Definitions relevant to the topic of non-native species are provided below. Some are taken from the Committee for Environmental Protection (2019), where further useful definitions and information may also be found. Native species: a species that occurs naturally in Antarctica (or part of Antarctica) and has not been introduced by humans either intentionally or unintentionally. Natural colonist: a species that undergoes natural range expansions through dispersal by natural means (e.g., ocean currents, wind, transport associated with other species such as migrating birds, etc.) Non-native species: an organism occurring outside its natural past or present range and dispersal potential, whose presence and dispersal in any biogeographic region of the Antarctic Treaty area is due to human (Synonyms include: alien species, non-indigenous species, exotic species) Invasive species: a subset of non-native species that are extending their range in the colonised Antarctic region, displacing native species and causing significant harm to biological diversity or ecosystem functioning. Invasion: The expansion of a non-native species into an area not previously occupied by it. Biogeographic region: a region of Antarctica that is biologically distinct from other regions. Non-native species risks to biodiversity and intrinsic values may arise if (1) native Antarctic species are moved by human activities between biogeographic regions, or (2) non-native species established in one Antarctic biogeographic region are distributed to other regions by human or natural mechanisms. Introduction/introduced: direct or indirect movement by human agency, of an organism outside its natural range. This term may be applied to intercontinental or intracontinental movement of species. In this information summary we focus predominantly on the introduction of non-native species due to human action rather than the introduction of natural colonists via natural pathways. It is estimated that the frequency of human-mediated introductions of non-native species to the broader Antarctic region may exceed natural colonisation rates by at least two orders of magnitude, with no evidence of a natural establishment event in the Antarctic in the time of human contract (i.e., the past c. 200 years) (Frenot et al., 2005). Once a non-native species, introduced to the Antarctic by human action, starts to have negative impacts upon native species it can be considered invasive. Current status in Antarctica Figure 1. Map of the Antarctic Peninsula region showing the distribution of known non- species, all of which are invertebrates due to earlier eradication of known plant introductions (see Resources for more details). Nevertheless, persistent seedbanks in Antarctic soils may still present a threat even following removal of plants. In Antarctica, relatively few terrestrial non-native species are known to have been established, largely due to the continent’s low connectivity to other parts of the globe and its extreme environment (Frenot et al., 2005). Currently, non-native species reports in Antarctica are mostly limited to flowering plants and invertebrates (Figures 1 and 2; Frenot et al., 2005; Hughes and Convey, 2010; Hughes et al., 2015; Leihy et al., 2023). The few monitoring activities that have occurred have increased our understanding of the number of non-native species and their distribution; however, it is apparent some non-native species may remain as yet undiscovered (Molina-Montenegro et al., 2012). In Antarctica, non-native species have been found mainly in the vicinity of research stations and visitor landing sites, highlighting that their presence, establishment, and increase in abundance are facilitated by human activities (Chown et al., 2012; Huiskes et al., 2014; Molina-Montenegro et al., 2014). Most Antarctic non-native species have been found within the Antarctic Peninsula region, but some have been reported from other areas of Antarctica (Figure 1; Frenot et al., 2005; Hughes et al., 2015). Non-native species distribution correlates strongly with areas predicted by modelling to be at the greatest risk of non-native species introductions due, for example, to high levels of national operator and tourist visitation and favourable climatic conditions (Chown et al., 2012; Huiskes et al., 2014). For example, Deception Island (South Shetland Islands) is one of the most frequently visited locations in Antarctica and is also the most invaded, with at least nine non-native invertebrate species recorded (Chown et al., 2012; Hughes and Convey, 2012; Greenslade et al., 2012; Hughes et al., 2015). The non-native grass, Poa annua (annual bluegrass), has repeatedly been introduced and established at Antarctic sites and has often been removed successfully. However, the grass continues to be invasive on the shores of Admiralty Bay, King George Island (South Shetland Islands) despite ongoing eradication efforts (Galera et al., 2017; 2019). Vectors and pathways There is evidence that terrestrial species are introduced inadvertently to Antarctica in significant numbers (Chown et al., 2012; Huiskes et al., 2014). In recent years, most non-native species have likely been introduced unintentionally through the importation of cargo, fresh foods, clothing, and personal effects via ships and aircraft (Whinam et al., 2005; Lee and Chown, 2009a,b; Hughes et al., 2010; 2011; Houghton et al., 2016; Lityńska-Zająć et al., 2012). Genetic studies of the non-native grass Poa annua from King George Island (South Shetland Islands) revealed that it was introduced on multiple occasions, from both European and South American sources (Chwedorzewska, 2008; Chwedorzewska and Bednarek, 2012). While most non-native species have been found in the vicinity of research stations, some have colonised Antarctic station buildings and hydroponic facilities (Frenot et al., 2005; Chwedorzewska et al. 2013; Bergstrom et al., 2017). For example, insects persist in some station sewage systems, despite eradication attempts, and have dispersed and may establish in the local environment (Hughes et al., 2015, Potocka and Krzemińska, 2018; Remedios-De Leon et al., 2021). Some non-native species have established and persisted for many years, while others have expanded their ranges and become invasive (Olech and Chwedorzewska, 2011; Pertierra et al., 2017b; 2020; Molina-Montenegro et al., 2019; Bartlett et al., 2023). Experience from environments around the world and from comparable environments in the Arctic and sub-Antarctic suggests that invasive species in Antarctica could have substantial environmental, economic, and irreversible impacts on Antarctic ecosystems (Frenot et al., 2005; Pejchar and Mooney, 2009). Movement of species within Antarctica Human activities may potentially transfer native Antarctic species to areas within Antarctica where they are not found naturally (intra-regional transfer) (Hughes et al., 2019; Bergstrom, 2022). Human-mediated dispersal of species could disrupt established terrestrial and freshwater ecosystems and alter the distinct biogeographic regions found within Antarctica (Hughes and Convey, 2010; Terauds and Lee, 2016; Hughes et al., 2019; Cukier et al., 2023). Furthermore, human movement within Antarctica may transfer existing non-native species to other Antarctic areas (Hughes et al., 2019). For example, laboratory research has shown that a flightless midge (Eretmoptera murphyi), accidentally introduced to Signy Island, South Orkney Islands, could survive and complete its life cycle c. 750 km further south on the Antarctic Peninsula and some grasses could survive beyond their current Antarctic distributions (Hughes et al., 2013; Pertierra et al., 2017a). Figure 2. [A] Nassauvia magellanica eradicated from Deception Island in January 2010 (Photo: K. A. Hughes). [B] Trichocera maculipennis found in Artigas Station (King George Island, South Shetland Islands) sewage system in 2006/07 (Photo: O. Volonterio). [C] Non-native potted plant in the window of an Antarctic research station (King George Island) (Photograph: K. A. Hughes]. [D] Poa annua on Deception Island which was subsequently removed (Photo: M. Molina-Montenegro). [E] Poa pratensis on Cierva Point, Antarctic Peninsula, where it was first introduced during transplantation experiments in 1954/55 and removed in 2015 (Photo: L. R. Pertierra). [F] Non-Antarctic soil inadvertently introduced to Rothera Research Station, Antarctic Peninsula, on vehicle wheels (Photo: K. A. Hughes). [G] Hull fouling of ships is a pathway for introduction of non-native marine species to Antarctica (Photo: K. A. Hughes). (H) The flightless chironomid midge Eretmoptera murphyi, introduced to Signy Island, South Orkney Island from South Georgia (Photo: P. Bucktrout). [I] Elephant seal (Mirounga leonina) resting in the drainage channel below the sewage treatment plant outfall at Rothera Research Station. Although the sewage is treated, microbial loads can still be high depending on the efficiency and performance of the sewage treatment plant. The effect of sewage ingestion by Antarctic marine mammals and avifauna is largely unknown. [Photograph: K.A. Hughes] Climate change Impacts resulting from the introduction of non-native species to Antarctica are in some cases likely to be exacerbated by climate change (Chown et al., 2012; 2022; Pertierra et al., 2020; 2021). Climate change may increase the availability of ice-free ground for colonisation by non-native species and make environmental conditions more favourable for new introductions thereby increasing the likelihood of establishment (Duffy and Lee, 2019; Bokhorst et al., 2021). As a result, new and established non-native species populations may increase their distribution and capacity to compete with native species (Molina-Montenegro et al., 2012; Duffy et al., 2017; Bokhorst et al., 2022). A continent-wide risk assessment for the establishment of non-native species in Antarctica demonstrated a substantial increase in the likelihood of establishment at locations subject to high levels of human activity in the future (Chown et al., 2012; see Figure 3). Non-native species biology and impacts The biology and traits of some non-native species enable them to survive under a wide range of environmental conditions, which may facilitate a rapid increase in their Antarctic distribution (i.e., become invasive in Antarctica) (Frenot et al., 2005; Pertierra et al., 2017a, Pertierra et al. 2022). Among vascular plants, the grass Poa annua is highly invasive in many other parts of the world and, as mentioned previously, is now also invasive in Antarctica (Frenot et al., 2005; Molina-Montenegro et al., 2012; 2014; Duffy et al., 2017; Atala et al., 2019; Ballesteros et al., 2022). Poa annua was reported from six locations on the Peninsula and South Shetland Islands, with the removal of populations at all sites, although seeds and other propagules still remain resulting in the potential for re-growth, such as has occurred on King George Island, South Shetland Islands (Molina-Montenegro et al., 2012, 2014; Chwedorzewska et al., 2015; Galera et al., 2017; 2019). On King George Island, the grass has spread from its initial introduction site around a research station into the local ecosystem (Molina-Montinegro et al., 2012; Galera et al., 2017). The variety of reproductive strategies available to this species as well as its wide climatic tolerance range may explain, in part, its colonisation success (Pertierra et al., 2017a). Soil disturbance can increase the abundance and germination of P. annua, but this is not the case for native plants, and P. annua can have negative effects on native plant species (Molina-Montenegro et al., 2014). The non-native grass Poa pratensis (also known as the smooth or common meadow-grass) was introduced inadvertently to Cierva Point, Danco Coast, Antarctic Peninsula, during transplantation experiments in 1954–55. Researchers reported that the grass was expanding beyond its original introduction plot, at the expense of local vascular plants and bryophytes, and its dense root system had a substantial impact on soil invertebrate densities. The plant was dug up and removed by an internationally coordinated team in 2015 (Pertierra et al., 2017b). For micro-invertebrates, Hypogastrura viatica is the most widely dispersed non-native springtail (Collembola) known in Antarctica, having been found at five locations on the Antarctic Peninsula, including popular visitor sites (Greenslade et al., 2012; Hughes et al., 2015). First reported on Deception Island in 1949, and now widespread across the island, its impact on native species is unknown. Other collembolan species are found in various parts of the Antarctic Peninsula, with Proisotoma minuta being the second most abundant locally and widespread on Deception Island (Enriquez et al., 2019; Pertierra et al., 2022; L.R. Pertierra, pers. obs.). Mesaphorura macrochaeta has been recorded recently in new localities of the South Shetland Islands, but its regional colonization status (see earlier definitions) remains uncertain (Pertierra et al. 2022). The colonization status of the latest alien Collembola reported in Antarctica, Ceratophysella succinea, remains uncertain but has been re-observed locally at two sites on Deception Island in recent years (Enriquez et al., 2019; Pertierra pers. obs.). Regarding insects, larvae of the midge Eretmoptera murphyi may be able to cycle soil nutrients many times faster than native invertebrates (Hughes et al., 2013; Pertierra et al., 2020; Bartlett et al., 2023). This species is currently confined to Signy Island and expanding locally at a slow rate. In contrast, the fly Trichocera maculipennis has rapidly colonised the sewage treatment plants of multiple stations on King George Island, although its ability to reproduce in the natural environment has not been confirmed (Potocka and Krzemińska, 2018; Remedios-De Leon et al., 2021). Current knowledge regarding the numbers and invasion status of non-native mites (Acari) is poor, with only two species minimally studied and inconsistently monitored (Pertierra et al., 2022). Information on non-native microorganisms, such as bacteria, fungi, and viruses, is very limited (Cowan et al, 2011). Introductions on wooden packaging have been reported and research from historical expedition sites in the Ross Sea and Deception Island describe introduced fungal species on the wood of huts (Held and Blanchette, 2017; Hughes et al., 2018). Management action The Protocol on Environmental Protection to the Antarctic Treaty largely prohibits the importation of non-native species into Antarctica without a permit. Consequently, to reduce the likelihood of inadvertent introductions, preventive measures are required by many national Antarctic operators and tourist companies, such as (i) cleaning of clothing, footwear, luggage, equipment, cargo, and means of transport before reaching Antarctica, and (ii) packing of fresh produce free of pests and diseases in closed containers (Hughes and Pertierra, 2016). Conscious of this need, the CEP has developed its Non-native Species Manual that provides information on biosecurity measures (ATS, 2019). Measures may also be required to prevent the distribution of species between biologically distinct ice-free regions of Antarctica which may be an area requiring future management attention by the international community (Hughes et al., 2019). Differentiating between new introductions transported through human activities (non-native species) and those naturally introduced by wind, ocean currents, or wildlife (natural colonists) can be challenging. For example, it was not possible to ascertain categorically if the South American aster Nassauvia magellanica on Deception Island was introduced by human or natural processes (Hughes and Convey, 2012). Correct differentiation is important for subsequent management as, according to the Protocol, non-native species should be eradicated while native species should be protected (for decision frameworks, see Figure 1 in Hughes and Convey, 2012, and Figure 2 in Bergstrom, 2022). From reports of non-native species eradication attempts in other continents, it is clear that a rapid response is key to their successful removal and management (Hughes and Pertierra, 2016). The CEP Non-native Species Manual states that ‘to be effective, responses to introductions should be undertaken as a priority, to prevent an increase in species’ distribution range and to make eradication simpler, cost-effective and more likely to succeed’ and encourages follow-up surveys to ensure management action is effective. Within the Antarctic Treaty area, several non-native plants have been removed (Molina-Montenegro et al., 2012, Hughes and Convey, 2012; Hughes et al., 2015; Pertierra et al., 2017b) although eradication of remaining propagules remains a longer-term technical challenge (Galera et al., 2019). Factors that may affect the likelihood of eradication success include: (i) the level of adaptation of the species to new environmental conditions, (ii) propagule longevity, (iii) the level of development of an abundant seed soil bank, (iv) the management reaction time and level of experience within the eradication team, and (v) the likelihood of reinvasion (Galera et al. 2021). In contrast, no attempts have been made to eradicate non-native invertebrates present in the natural environment, although some have been eradicated from within Antarctic stations and hydroponic facilities (Hughes et al., 2005; Bergstrom et al., 2017). The range expansion of existing non-native invertebrates may be minimized with effective control methods. In the case of the fly Trichocera maculipennis on King George Island, coordinated actions may prevent further dispersal while feasible eradication methods are being explored (Remedios-De Leon et al., 2021). Future Research Figure 1. The relative risk of alien vascular plants establishing in Antarctica. Visitor-free and ice free areas are allocated a small value because of the minor risk of species establishment in the absence of visitor landings. Insets show the risk index detail for the Antarctic Peninsula and the western Ross Sea, respectively. Ice-free areas are in dark grey, continental areas in light grey, and ice shelf or tongues in light blue. Source: Chown et al. 2012 PNAS 109, 4938-4943. Further scientific research could usefully investigate (i) surveillance and detection techniques, (ii) the rate and extent of microbial introductions, (iii) rates of transfer of non-native species into Antarctica (iv) rates of transfer of native and non-native species between Antarctica eco-regions, and (v) effective prevention and, ultimately, eradication methodologies. Risk assessments for globally invasive species and those that have already colonised the broader Antarctic region show that climatic barriers to non-native species establishment will weaken as warming continues across the region (Hughes et al., 2020). Research on invasions in other parts of the world, including the sub-Antarctic, may indicate which species present the greatest risk to ecosystems within the Treaty area (Leihy et al., 2023). The use of risk assessment methods could inform targeted surveillance of introduction pathways and sites that have the highest risk of establishment of invasive species (Greenslade et al., 2012; Duffy et al., 2017). Conclusion Increased pressures on Antarctic systems from increased human activity and climate change can increase the risk of non-native species introduction and range expansion. Therefore, (i) continued research into the impacts of non-native species, (ii) widespread adoption of practices to reduce their introduction and spread, and (iii) development of further methods to respond to introductions are integral to the protection of the Antarctic and its associated ecosystems.
