Author/s Kevin A. Hughes (1) *, Katarzyna J. Chwedorzewska (2), Luis R. Pertierra (3) and Justine D. Shaw (4) (1) British Antarctic Survey, Natural Environment Research Council, Cambridge, United Kingdom. *kehu[at]bas.ac.uk (2) Department of Agronomy, Warsaw University of Life Sciences, Warsaw, Poland (3) Universidad Rey Juan Carlos, Spain (4) Centre for Biodiversity & Conservation Science, The University of Queensland, St Lucia, Australia Brief Overview Antarctic biodiversity and ecosystems are under threat from introduced non-native species. Currently the Antarctic Peninsula and off shore islands are the most invaded areas. Invasions are likely to increase, facilitated by climate change and increased human activity in the region. Despite success in eradication of non-native plants, established non-native invertebrate species have already begun to increase their distribution within Antarctica with largely unknown impacts upon native organisms and habitats. Further scientific research could usefully investigate surveillance and detection techniques, the rate and extent of microbial and marine introductions, rates of transfer of native and non-native species between Antarctica eco-regions, and devise optimal prevention and ultimately eradication methodologies. Detailed Overview 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. Invasive non-native species have caused substantial negative impacts on biodiversity and ecosystem structure and function in many areas of the Earth. In contrast, Antarctica has relatively few known established terrestrial non-native species, with those reported mostly limited to flowering plants and invertebrates (Figure 1 and 2; 1-3). Nevertheless, the few monitoring activities that have occurred so far have increased our understanding of the number of non-native species, their distribution and it is apparent some introduced species may remain as yet undiscovered (4). 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 (5,6). Most known Antarctic non-native species have been found within the Antarctic Peninsula region but some have been reported from other areas of Antarctica (Figure 1; 1,3). This distribution correlates strongly with areas predicted to be at greatest risk of non-native species introductions due to high levels of national operator and tourist visitation and favourable climatic conditions (5). For example, Deception Island (South Shetland Islands) is one of the most frequently visited locations in Antarctica, and also the most invaded, with nine non-native invertebrate species recorded (3,5,7,8). 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] Since the Environmental Protocol was agreed, most non-native species have been introduced unintentionally through importation of cargo, fresh foods, clothing and personal effects (1,2,5,9,10). Genetic studies of the non-native Poa annua (annual bluegrass) from King George Island (South Shetland Islands) revealed that it was introduced on multiple occasions, from both European and South American sources (11). Some non-native species have colonised Antarctic station buildings and hydroponic facilities (1,12), for example, insects persist in some station sewage systems, despite eradication attempts, and may disperse to establish in the local environment (3,7). Climate change and human footprint Climate change and expanding human footprint put the whole of Antarctica at increased risk of invasion (5,13). Climate change may increase availability of ice-free ground, make environmental conditions more favourable for new introductions and increase the likelihood that established non-native populations will increase their distribution and capacity to compete with native species (2,4,13,14). Human movement between Antarctic regions may transfer existing non-native species to other Antarctic areas (4). For example, 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 (15). Human activities may potentially also transfer native Antarctic species to areas within Antarctica where they are not found naturally, which could disrupt established ecosystems and lead to homogenization of the biota (2). Non-native species biology and impacts The biology of some invasive species enables them to survive under a wide range of environmental conditions, which may facilitate a rapid increase in their Antarctic distribution (1,5,15,16). Among vascular plants, Poa annua is highly invasive in many other parts of the world and has the potential to become invasive in Antarctica (1,4,6,13). Poa annua was reported from six locations on the Peninsula and South Shetland Islands, with the successful removal of populations at all sites, although seeds and other propagules may still remain (4,6,17). On King George Island, it spread from its initial introduction site around a research station into the local ecosystem (4,17). The variety of reproductive strategies available to this species as well as its wide climatic tolerance range may explain, in part, its colonisation success (16). Soil disturbance can increase the abundance and germination of P. annua, but not native plants (6) and P. annua can have negative effects on native plant species (4). Poa pratensis was expanding at the expense of local vascular plants and bryophytes prior to its eradication, and its dense root system had a substantial impact on soil invertebrate densities (16). For micro-invertebrates, Hypogastrura viatica is the most widely dispersed non-native springtail (Collembola) in Antarctica having been found at five locations on the Antarctic Peninsula, including popular visitor sites (3,8). With a preference for disturbed ground, the species may out-compete native species (8). First reported on Deception Island in 1949, it is now found there in densities of over 5,500 individuals per litre of soil with unknown impacts on native species. Regarding insects, on Signy Island, larvae of the midge Eretmoptera murphyi may be able to cycle soil nutrients up to nine times faster than native invertebrate populations and, if dispersed, could alter terrestrial habitats across the Peninsula (15). This species is expanding locally at a slow rate, but it is confined to Signy Island. In contrasts, the fly Trichocera maculipennis has rapidly colonised the sewage treatment plants of multiple stations on King George Island, although it ability to reproduce in the natural environment has not been confirmed (19). Management action 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. Use of risk assessment methods could inform targeted surveillance of introduction pathways and sites that have the highest risk of establishment of invasive species (8,13). Differentiating between new introductions transported through human activities (non-native species) and those introduced by wind, ocean current or wildlife (natural colonists) can be difficult (7). 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 (7). Using the sub-Antarctic islands as model systems for natural species colonisation rates, the likelihood of two new species reaching Antarctica by natural processes and establishing in this time frame is very low. Correct differentiation is important for subsequent management as non-native species should be eradicated, according to the Protocol (7). Within the Antarctic Treaty area, several non-native plants have been removed (3,4,7,16) although eradication of remaining propagules remains a longer-term technical challenge. 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 (12). The expansion of non-native invertebrates may be minimized with effective control methods. In the case of Trichocera maculipennis on King George Island, coordinated actions may prevent further dispersal while feasible eradication methods are being explored. Marine introductions Little is known about levels of non-native species introductions to Antarctic marine environments (1). However, species could be imported in ballast water or on ship hulls (1,20). Although hull abrasion by sea ice may be effective in removing adhering species, marine organisms may persist within ship sea chests (21), and hull intake ports, increasing the risk of marine introductions (22). What non-native species have been found in Antarctica to date? This paper reviews available knowledge on possible pathways, impacts and management approaches. Key Events 1962 ATCM II –WP3 Draft of Agreed Measures including first mention of prohibition on importation of non-native species 1964 Recommendation III-8 Agreed Measures for the Conservation of Antarctic Fauna and Flora which includes prohibition on bringing into Treaty area and non-indigenous animals or plants except under permit. 1991 Protocol on Environmental Protection to the Antarctic Treaty. Annex II Conservation of Antarctic Fauna and Flora Article 4 re-iterates the prohibition on non-native species 1998 ATCM XXII – IP 53 IUCN paper on non-native species which covered pathogens, pets, household plants as well as accidental introductions around stations. 1999 ATCM XXIII – WP 32 Report on outcomes from the Workshop on Diseases of Antarctic Wildlife. 2001 Reports from an ICG provided a review and risk assessment (ATCM XXIV- WP 10) and practical measures to reduce the risks of introducing wildlife diseases (ATCM XXIV – WP 11). 2003 Lewis et al. (20) investigated ships used in support of Antarctic science and tourism and demonstrate that non-native marine species could be transported to the Antarctic on the hulls of such vessels. 2005 ATCM XXVIII – WP 28 Suggested six measures to address the unintentional introduction and spread of non-native biota and disease to the Antarctic Treaty area ATCM XXVIII – IP 97 Provided information on decontamination procedures for tourists. Frenot et al. (1) publish a review on: “Biological invasions in the Antarctic: extent, impacts and implications”. Whinam, Chilcott and Bergstrom publish “Subantarctic hitchhikers: Expeditioners as vectors for the introduction of alien organisms”. Biological Conservation 121, 207-219 (2005) doi: 10.1016/j.biocon.2004.04.020 reporting on the potential for scientists on national Antarctic programmes to act as vectors for the introduction of Non-native Species to Antarctica. 2006 ATCM XXIX – WP 5 Rev. 1 Provided Practical Guidelines for Ballast Water Exchange to limit marine introductions, and leads to Resolution 3 (2006). ATCM XXIX – IP 44 Details on how to manage quarantine. ATCM XXX – IP 49 Aimed to quantify the transfers and validate the pathways for introductions ATCM XXIX – WP 13 and ATCM XXIX – IP 46 Reports of the workshop in New Zealand on non-native species that provided several recommendations. 2007 ATCM XXX – IP37 Reporting on hull fouling as a source of marine invasions in the Antarctic, noting that recent studies have shown hull fouling to be an important vector for non-native species introductions. 2008 ATCM XXXI – WP 16 CEP endorsed proposal to use the existing Australian Antarctic Alien Species Database for recording non-native species ATCM XXXI – IP 17 Proposed measures to keep the Larsemann Hills free of introductions ATCM XXXI – IP 98 COMNAP report on existing procedures to control the introduction of non-native species through logistics 2009 ATCM XXXII-IP4 SCAR included non-native species introductions in its environmental code of conduct for terrestrial scientific field research in Antarctica ATCM XXXII – IP 12 and ATCM XXXII – WP 33. Proposed provisions for inclusion in management plans for protected and managed areas ATCM XXXII – SP 11 Secretariat topic summary of previous discussions ATCM XXXII – WP 5 . Work Program for CEP Action on Non-native Species was agreed 2010 ATCM XXXIII – WP 4 and ATCM XXXIII – WP 6 . An evidence-based approach to reducing the risks of introductions ATCM XXXIII – WP 15 Suggestions on how to deal with the discovery of new non-native introductions ATCM XXXIII – WP 14 The risks of intra-regional transfer of species in terrestrial Antarctica ATCM XXXIII – IP 42 Provided details of known non-native colonists ATCM XXXIII – IP 44. Suggested framework to determine the colonisation status of newly discovered species 2011 The CEP adopted the Non-native Species Manual (Manual) providing guidance on preventive measures to limit accidental introductions and listing a wide range of resources already published for further information. ATCM XXXIV – WP12 COMNAP checklist for supply chain managers to ensure cargo is clean before shipping ATCM XXXIV – WP 53 Suggestions on how to reduce risks of introductions from contaminated food ATCM XXXIV – WP25. Proposals on how to minimise risks from hydroponic facilities ATCM XXXIV – IP50. Summary of the status of all know non-native species 2012 ATCM XXXV – WP5 . Summary of the outcomes of the IPY Aliens in Antarctica Project provided by SCAR including risk assessment. Terauds and Lee (23) publish an analysis of the best available biodiversity data, which for the first time allows for the delineation of 15 biologically distinct ice free regions in Antarctica 2013 ATCM XXXVI- WP19 Biosecurity measures for preventing the introduction of non-native soil organisms ATCM XXXVI – WP35 Highlighted the negative impacts of non-native microbial introductions on scientific and environmental values 2014 ATCM XXXVII – IP23 Provided up to date details of known non-native colonist 2015 ATCM XXXVIII – IP 46 Update on distribution of known non-native species ATCM XXXVIII – IP 29 Report of the successful eradication of Poa pratensis from Cierva Point, Danco Coast, Antarctic Peninsula. 2016 The CEP adopted the revised Non-native Species Manual (Manual) providing guidance on preventive measures to limit accidental introductions and listing a wide range of resources already published for further information. Resolution 4 (2016) – ATCM XXXIX – CEP XIX, Santiago. Revision of the Non-native Species Manual. https://www.ats.aq/devAS/ats_meetings_meeting_measure.aspx?lang=e ATCM XXXIX – WP13 Report of the intersessional contact group on revision of the CEP Non-native Species Manual. ATCM XXXIX – WP52. Report of the non-native fly, Trichocera maculipennis, in several sewage treatment plants on King George Island, South Shetland Islands ATCM XXXIX – IP27. Report of the risks of introduction of biofouling organisms to Antarctica on vessel hulls. 2017 ATCM XL – WP 46. Report of an internationally agreed action plan to manage the non-native flies on King George Island, South Shetland Islands ATCM XL – IP 47. Report of the eradication of the non-native grass Poa annua L. from ASPA No 128 Western Shore of Admiralty Bay, King George Island, South Shetland Islands ATCM XL – IP 128 rev. 1. Report on the Argentine Antarctic Program Operations Manual on prevention of the introduction of non-native species to the Antarctic continent.