Assessing the vulnerability of Antarctic marine ecosystems to invasive non-native species

Invasive non-native species are a major threat to global biodiversity. For at least 15 million years coastal Antarctica has been poorly connected to nearby temperate ecosystems due to physical and physiological barriers. Yet, Antarctica is experiencing significant environmental change and becoming increasingly exposed to ship-borne human activity that crosses the physical barriers. These factors may facilitate the establishment of non-native marine species. This doctoral research adds insight into the risk of non-native marine species being transported to Antarctica via ships’ hulls and internal seawater systems, with particular focus on pathways of introduction and species found within those pathways. To begin my research, I assessed the current knowledge of non-native marine species in the Antarctic region: the physical and physiological factors that resist establishment of non-native marine species; changes to resistance under climate change; the role of legislation in limiting marine introductions; and the effect of increasing human activity on vectors and pathways of introduction. Evidence of non-native marine species was limited: up to 2019 just four marine non-native and one cryptogenic species that were likely introduced anthropogenically had been reported free-living in Antarctica or in the sub-Antarctica islands, but no established populations have been reported. An additional six species had been observed in pathways to Antarctica that are potentially at risk of becoming invasive. I estimated there may be approximately 180 vessels and 500+ voyages in Antarctic waters annually. However, these estimates are necessarily speculative because relevant data are not recorded comprehensively. In response to the scarcity of data on ship movements into the Southern Ocean, I obtained data on ship activity in the Southern Ocean from 2014-2018 inclusive and developed a ship traffic network for Antarctic-going vessels. I analysed the ship movements and conducted a spatially-explicit assessment of introduction risk for non-native marine species in all Antarctic waters. I found that vessels connect Antarctica via an extensive network of ship activity to all global regions, and especially South Atlantic and European ports. Ship visits were more than seven times higher to the Antarctic Peninsula and the South Shetland Islands than elsewhere around Antarctica. I found that, while the five recognised ‘Antarctic Gateway cities’ are important last ports of call, an additional 53 ports had vessels directly departing to Antarctica from 2014-2018. I identified ports outside Antarctica where biosecurity interventions could be most effective and the most vulnerable Antarctic locations where monitoring programmes for high-risk invaders should be established. Biofouling communities within the major pathway to Antarctica from Europe via the South Atlantic, identified in the network analysis, became my next focus. I obtained biofouling samples from the polar research vessel RRS James Clark Ross and found that niche (protected) areas of the hull represent significantly greater colonisation (species richness) and propagule pressure (individual abundance) than exposed areas of the hull. The composition of the biological communities did not differ among exposed and niche areas, but did change significantly among the three surveys conducted. Only six species were found on the ship’s hull in Antarctica, but they included a known invasive bryozoan, Tricellaria inopinata, and barnacles that have no counterparts in Antarctica. While the role of hull fouling is recognised as a globally important vector for introductions of non-native marine species, the role of a vessel’s internal pipework has been overlooked. I conducted the first comprehensive study of biofouling macrofauna living inside an Antarctic vessel’s internal seawater systems, finding breeding communities of Jassa marmorata (Amphipoda) and mytilid mussels throughout the internal pipework system. I found fouling communities that occluded ~9-17% of a pipe’s cross-sectional area, increasing running costs for ships. Since ships are constantly pumping their water through their pipework, they are likely to be releasing propagules at all stages of their voyages, including in polar regions. Before I started my research, Antarctic operators and policy-makers were unaware of the total number of vessels that visit Antarctica. Now, I have provided comprehensive insight into the most traversed routes to Antarctica and identified Antarctic locations that are the most likely recipient locations for non-native marine species. I found that non-native species from temperate regions can survive passages through polar areas and that sheltered sections of the hull and internal systems are especially important sites for both propagule and colonisation pressure. Together, these results demonstrate that Antarctica is well connected to worldwide marine ecosystems and that biofouling on ships poses an important and growing introduction risk to Antarctica.General Sir John Monash Foundation, Whitten Studentship (Zoology Department, University of Cambridge), WEJ Craig Travelling Scholarship (University of Melbourne), St John's College Cambridg