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Pathways for the Introduction of Terrestrial Non-Native species

Ad H.L. Huiskes (1), Marc Lebouvier (2), Marco A . Molina Montenegro (3), Luis R. Pertierra (4), Megumu Tsujimoto (5)

(1) Royal Netherlands Institute for Sea Research, Yerseke, The Netherlands. ad.huiskes[at]nioz.nl
(2) Station Biologique, Unité Mixte de Recherche Ecobio, Centre National de la Recherche Scientifique–Université de Rennes, Paimpont, France
(3) Instituto de Ciencias Biológicas, Universidad de Talca, Talca, Chile
(4) Universidad Rey Juan Carlos, Departamento de Biología y Geología, Madrid, Spain
(5) National Institute of Polar Research, Tokyo, Japan

Non-native organisms are relatively rare in Antarctica and the Southern Ocean. This is probably attributable to the comparatively recent human presence and to protection afforded by the Protocol on Environmental Protection to the Antarctic Treaty, which prohibits deliberate introductions. Inadvertent introductions do occur, as clothing and luggage of visitors, cargo, fresh produce, vehicles, ships and other means of transport can inadvertently entrain propagules or complete organisms. Because of steadily growing human activities on the continent and climate change trends, the risk of non-native organisms arriving and establishing is likely to increase.

Antarctic ecosystems are under increasing pressure from the introduction of non-native species (1). Non-native species introductions in terrestrial and freshwater environments in Antarctica are rare compared to introductions occurring elsewhere in the world, largely due to its low connectivity to other parts of the globe, its extreme environment and its protection under the Protocol on Environmental Protection to the Antarctic Treaty (2). While natural introductions into the Antarctic appear to occur very rarely, they have been documented (3). Up to 2015, most non-native species introductions of both plants and invertebrates have been predominantly due to human activities. These have occurred in the Antarctic Peninsula region and on the sub-Antarctic and Southern Cold Temperate islands (4, 5) (Table 1).

Table 1 – Records of known alien species in the Antarctic Peninsula terrestrial environment prior to January 2015 (after 5).

Information on microbes and fungi is very limited but research from historical expedition sites in the Ross Sea and Deception Island describe introduced fungal species on wood of huts (6).

Non-native plants reported from the Antarctic continent have been subsequently eradicated at several sites (Puccinellia sp. near Syowa station, Dronning Maud Land, and Alopecurus geniculatusPuccinellia distans, Rumex pulcher, Stellaria media and Chenopodium rubrum near Progress II station, Larsemann Hills, Princess Elizabeth Land) (5). Non-native invertebrates have so far not been reported from terrestrial Antarctica outside the Peninsula region, apart from a number of invertebrates found in station buildings (5).
Knowledge on marine species introductions in the Southern Ocean, south of the 60°S, is still scarce (2, 10); vessels may carry marine non-native organisms predominantly associated with fouling assemblages and anthropogenic marine debris (7, 8, 9).

Various important vectors of introduction have been identified by previous studies, which provide guidance to the areas where biosecurity efforts should be focused. These include:

  • cargo containers (packing crates) and contents (10, 11)
  • cargo for infrastructure works (station construction or renovation including earthmoving and excavation machinery) (10, 12)
  • fresh produce (13)
  • visitors: clothing and gear (1)
  • means of transport and landing (ships, planes, helicopters) (7, 8, 9).

Fig. 1: Soil imported on the unwashed wheels of a vehicle arriving at an Antarctic station (Photo: K Hughes).

Visitors (including scientists and operational and logistic support staff) traveling to Antarctica primarily depart from South America, South Africa, Australia and New Zealand. Ships and planes also depart from other ports and airports worldwide to Antarctic research stations and tourist sites. These ships and planes are all potential carriers of propagules including seeds, other plant propagules and invertebrates (14, 15). Of the 35,973 tourists landing in 2017-18 the largest number were concentrated in the Peninsula, followed by the McMurdo Sound region of the Ross Sea (https://iaato.org/tourism-statistics). Cargo importation is one of the main pathways for non-native species introductions into Antarctica. Numerous propagules have been found attached to cargo, including packing crates, contents, machinery and vehicles (Figure 1), transported mainly from the cargo facilities of the national programme operators to the Antarctic research stations (11, 12, 14, 16, 17).

The importation of fresh produce such as eggs, fresh fruit and vegetables (Figure 2) and meat products could also inadvertently transport non-native species such as microorganisms and invertebrates primarily from the departing port into Antarctica (13). However, some modes of transport, especially planes and helicopters, have not yet been studied in great detail as possible vectors. Additionally, there have not been particular pathways of intra-regional transport of non-native species identified within the Antarctic although they are of great concern for the conservation of the Antarctic ecosystems.

Fig. 2: Fresh food may be contaminated. 89% of fresh fruit and vegetables examined for Australian stations were clean but some items were either infected with fungi (9%) as was this onion, or had evidence of the presence of insects (2%) (Photo: K. Kiefer).

Non-native species introductions can be classified in four categories (2, 5):
a. transient, i.e. those surviving for a short time period, dying out by natural causes (e.g. unfavorable environment) or being eradicated by humans;
b. persistent, those surviving wintering and locally established in a small area for several years (for example, Poa pratensis colony persisting in Cierva Point for over 60 years (18)); and
c. invasive, those that are firmly established and start expanding and significantly disturbing any native communities (for example Poa annua) (19).
d. synanthropic non-native species, which are only associated with humans in Antarctica – e.g living inside Antarctic buildings, in sewage treatment plants and in hydroponic facilities (5). These species listed (5) are all Diptera (true flies and mosquitos): Lycoriella ingenua in Casey Station (eradication attempt unsuccessful), Lycoriella sp. in Rothera Research Station (eradication successful), Trichocera maculipennis in Artigas Station (eradication unsuccessful, species now also found in the surrounding environment), unidentified mosquito Frei Station (larvae persistent in sewage plant).

The Antarctic climate, which is adverse to the majority of aliens, is likely to continue to be mitigated by climate change, particularly in the Antarctic Peninsula (20). Recent studies show also that the number of potential niches available for colonization by alien species in the Antarctic Peninsula is higher than anticipated (21). Impact of invasive aliens in other biomes of the world have proven to be detrimental to the biodiversity of the native communities. Research on the invasive plant species Poa annua in Antarctica has shown that a detrimental impact is very likely to occur in Antarctica as well (19).

The Protocol on Environmental Protection to the Antarctic Treaty prohibits import of alien organisms into Antarctica without a permit. This means that preventive measures are required by national operators and tourist companies to avoid inadvertent introductions. Studies on the possible vectors and pathways for non-native species, have identified key elements for minimizing the risk of transferring non-native species to Antarctica. These included cleaning of clothing (Figure 3), boots (Figure 4), luggage, equipment, cargo, and means of transport by washing or vacuuming before reaching Antarctica, and packing of fresh produce free of pests and diseases in closed containers.

Fig. 3: Passenger’s clothing being checked by expedition staff for propagules, on an Antarctic cruise ship before landing in Antarctica (Photo: DWH Walton).

Fig. 4: Rigorous boot washing needs to be enforced before and after each Antarctic landing to limit the potential for the spread of propagules (Photo: A. Herbert).

A recent paper evaluates non-native species policy development and implementation by the Antarctic Treaty Parties and provides useful guidance on some of the more effective biosecurity procedures (22).
Further research is required on the pathways for non-native species introductions which should include intra-regional transport and the pathways for marine species introductions.

Other information:

1. S. L. Chown, A. H. L. Huiskes, N. J. M. Gremmen, J. E. Lee, A. Terauds, K. Crosbie, et al, Continent-wide risk assessment for the establishment of non-indigenous species in Antarctica. Proceedings of the National Academy of Sciences 109, 4938-4943 (2012). doi: 10.1073/pnas.1119787109

2. Y. Frenot, S. L. Chown, J. Whinam, P. M. Selkirk, P. Convey, M. Skotnicki, et al, Biological invasions in the Antarctic: impacts and implications. Biological Reviews 80, 45–72 (2005). doi: 10.1017/S1464793104006542

3. R. I. L. Smith, M. Richardson, Fuegian plants in Antarctica: natural or anthropogenically assisted immigrants? Biological Invasions  13, 1-5 (2011). doi: 10.1007/s10530-010-9784-x

4. M. A. McGeoch, J. D. Shaw, A. Terauds, J. E. Lee, S. L. Chown, Monitoring biological invasion across the broader Antarctic: a baseline and indicator framework. Global Environmental Change  32, 108-125 (2015). doi: 10.1016/j.gloenvcha.2014.12.012

5. K. A. Hughes, L. R. Pertierra, M. A. Molina-Montenegro, P. Convey, Biological invasions in terrestrial Antarctica: what is the current status and can we respond? Biodiversity and Conservation  24, 1031-1055 (2015). doi: 10.1007/s10531-015-0896-6

6. B. W. Held, R. A. Blanchette, Deception Island, Antarctica, harbors a diverse
assemblage of wood decay fungi. Fungal Biology  121, 145 – 157 (2017). doi: 10.1016/j.funbio.2016.11.009

7. K. A. Hughes, G. V. Ashton, Breaking the ice: the introduction of biofouling organisms to Antarctica on vessel hulls. Aquatic conservation  27, 158-164 (2016). doi: 10.1002/aqc.2625

8. J. E. Lee, S. L. Chown, Mytilus on the move: transport of an invasive
bivalve to the Antarctic. Marine Ecology Progress Series  339, 307-310 (2007). doi: 10.3354/meps339307

9. J. E. Lee, S. L. Chown, Temporal development of hull-fouling assemblages associated with an Antarctic supply vessel. Marine Ecology Progress Series  386, 97-105 (2009). doi: 10.3354/meps08074

10. K. A. Hughes, P. Convey, A. H. L. Huiskes, Global movement and homogenization of biota: challenges to environmental management of Antarctica? In: T. Tin, D. Liggett, P. T. Maher, M. Lamers (eds), Antarctic Futures. Human Engagement with the Antarctic environment. Springer: Dordrecht, Heidelberg, New York, London, 113-137 (2014). doi: 10.1007/978-94-007-6582-5_5

11. M. Tsujimoto, S. Imura, Does a new transportation system increase the risk of importing non-native species to Antarctica? Antarctic Science 24, 441–449 (2012). doi: 10.1017/S0954102012000272

12. J. E. Lee, S. L. Chown, Quantifying the propagule load associated with the construction of an Antarctic research station. Antarctic Science  21, 472-475 (2009). doi: 10.1017/S0954102009990162

13. K. A. Hughes, J. E. Lee, M. Tsujimoto, S. Imura, D. M. Bergstrom, C. Ware, et al, Food for thought: risks of non-native species transfer to the Antarctic region with fresh produce. Biological Conservation  144, 1682-1689 (2011). doi: 10.1016/j.biocon.2011.03.001 

14. A.H.L. Huiskes, N.J.M. Gremmen, D.M. Bergstrom, Y. Frenot, K.A. Hughes, S. Imura, et al, Aliens in Antarctica: assessing transfer of plant propagules by human visitors. Biological Conservation 171, 278-284 (2014). doi: 10.1016/j.biocon.2014.01.038

15. J.E. Lee, S.L. Chown, Breaching the dispersal barrier to invasion: quantification and management. Ecological Applications 19, 1944–1959 (2009). doi: 10.1890/08-2157.1

16. K.A. Hughes, P. Convey, N.R. Maslen, R.I.L Smith, Accidental transfer of non-native soil organisms into Antarctica on construction vehicles. Biological Invasions 12, 875–891 (2010). doi: 10.1007/s10530-009-9508-2

17. M. Houghton, P.B. McQuillan, D. Bergstrom, L. Frost, J. van den Hoff, J. Shaw, Pathways of alien invertebrate transfer to the Antarctic region. Polar Biology  39, 23-33 (2016). doi: 10.1007/s00300-014-1599-2

18. L. R. Pertierra, F. L. J. Benayas, K. A. Hughes, Poa pratensis L., current status of the longest-established non-native vascular plant in the Antarctic. Polar Biology  36, 1473–1481 (2013). doi: 10.1007/s00300-013-1367-8

19. M. A. Molina-Montenegro, F. Carrasco-Urra, C. Rodrigo, P. Convey, F. Valladares, E. Gianoli, Occurrence of the non-native annual Bluegrass on the Antarctic mainland and its negative effects on the native plants. Conservation Biology  26, 717–723 (2012). doi: 10.1111/j.1523-1739.2012.01865.x

20. M. J. Amesbury, T. P. Roland, J. Royles, D. A. Hodgson, P. Convey, H. Griffiths, et al, Widespread biological response to rapid warming on the Antarctic Peninsula. Current Biology  27, 1616-1622 (2017). doi: 10.1016/j.cub.2017.04.034

21. L.R. Pertierra, P. Aragón, J. D. Shaw, D. M. Bergstrom, A. Terauds, M. A. Olalla-Tarraga, Global thermal niche models of two European grasses show high invasion risk in Antarctica. Global Change Biology (2017). doi: 10.1111/gcb.13596

22. K. A. Hughes, L. R. Pertierra, Evaluation of non-native species policy development and implementation within the Antarctic Treaty area. Biological Conservation 200, 149 – 159 (2016). doi: 10.1016/j.biocon.2016.03.011