The survival of mature (L4) E. murphyi larvae in 100% seawater for as long as 21 days indicates that seawater exposure alone would not necessarily be a barrier to this species’ dispersal. However, whilst mature larvae tolerated prolonged submergence, the small L1 larvae were unable to survive even very brief seawater exposure if they successfully hatched from the immersed eggs (Figs. 1, 2).
Most dipteran larvae cannot tolerate prolonged seawater submergence (Bayley 1972). However, larvae of B. antarctica, Antarctica’s only endemic chironomid (and E. murphyi’s closest relative), can withstand extensive osmotic dehydration, with 50% survival after 10 days in 100% seawater (Elnitsky et al. 2009). As predicted, E. murphyi L4 larvae also showed considerable tolerance to seawater immersion, with no difference in survival between 100% seawater, freshwater or soil treatments over 21 days (Fig. 1). This is consistent with the findings of a recent, related study of the possibility of using seawater as a biosecurity measure, where E. murphyi larvae survived all seawater dilution treatments trialled over a 7 days period (Bartlett et al. 2020a). The mortality recorded in the current, longer, study is also consistent with previous findings relating to E. murphyi’s life cycle and development under field and controlled conditions (Bartlett et al. 2018). Survival of E. murphyi L4 larvae declined rapidly under prolonged hyperosmotic sea water (200%) exposure, with time to 50% mortality (LT50) of just 2 days. While B. antarctica survival also declined rapidly under these conditions, 25% of larvae survived 6 d submerged in 200% sea water (Elnitsky et al. 2009), suggesting a greater tolerance of hyperosmotic stress in the more southern species. This lower tolerance may limit the ability of the E. murphyi larvae to survive in some habitats currently occupied by B. antarctica, such as supralittoral habitats that can experience hypersaline conditions resulting from tidal spray and evaporation (Elnitsky et al. 2009).
The ability of E. murphyi L4 larvae to survive periods of at least 21 days in seawater opens the possibility of oceanic dispersal to adjacent islands. Providing hyperosmotic conditions are not experienced for longer than a few days, this could occur through rafting (most likely with debris such as mosses washed into the sea, as larvae alone would sink rather than float) or via zoochoric association with seabirds or seals. Given E. murphyi is found in habitats with close association with elephant and fur seals on Signy Island (Bartlett et al. 2019) as well as various nesting seabirds, animal transport of larvae is certainly possible. There is also the potential that eggs may be carried in the fur or feathers of the animals, especially as egg sacs have a sticky outer membrane (Bartlett et al.2018), and thus could enter the ocean via this route. Whilst exposure to seawater appears to prevent successful hatching, our data indicated that eggs can continue development while submerged, and thus, both egg sacs and L4 larvae could represent potentially viable oceanic dispersal stages (Fig. 2). This would be especially likely if egg sacs are returned to terrestrial environments within the egg development period, such as is possible if transported through ectozoochory. Within this study, we only examined eggs, and consequently L1 hatchlings, as well as the mature L4 larvae; it is possible that L2 and L3 instars are not as vulnerable to seawater as are L1, given their more robust response to other stressors, such as cold (Bartlett et al. 2020b).
Buoyancy of the midge larvae was variable within this experiment, with some sinking and others not. However, we did not explicitly examine buoyancy. Even early stage pupae have a hydrophobic cuticle (J. Bartlett pers. obs), as well as later pupal stages and adults, likely as a result of the development of microtrichia during metamorphosis as is seen in several intertidal Chironomidae (Neumann and Woermann 2009). Based on this knowledge we speculate that pupae or adults might be capable of physically floating on the surface, although we also note that adults, in particular, are very short lived, thus limiting the dispersal potential of this stage relative to water transfer times. Egg sacs and larvae would, rather, likely be reliant on vectors such as animals, or rafts/debris.
Drifter currents crossing the South Orkney Plateau move material into open ocean (Fig. 3c), posing little risk of transporting the midge beyond the South Orkney Islands. The available drifter data did not include tracks from within the South Orkney Island group, so the details of currents around Signy Island and its neighbouring islands remain unknown. However, we did identify several currents that could potentially allow dispersal of E. murphyi among islands along the Antarctic Peninsula, should the midge be initially transferred to this region—as has happened in the past (Hughes et al. 2010). The South Shetland Islands are a well frequented archipelago north-west of the tip of the Antarctic Peninsula, with 26 international research stations located across several islands, as well as many field research and tourist landing sites (Bender et al. 2016); King George Island alone hosts the facilities of ten different national operators (COMNAP 2019). The geography of the South Shetland Islands means that distances between islands are small, and available coastlines large. Figure 3d shows how the midge could potentially disperse among the islands of the archipelago, including to Elephant Island in the north, and from Livingston Island southwards into the Palmer Archipelago, via smaller islands en route that could act as stepping stones. If transferred to Rothera Research Station (Adelaide Island) via anthropogenic means, there are potential pathways from there towards the mainland of the Antarctic Peninsula and its offshore islands (Fig. 3b), and transfer could occur well within the survival period of E. murphyi larvae in seawater (Fig. 3b, blue drifter).
To date, aeolian transport has most commonly been invoked in the colonisation of islands and remote areas by terrestrial invertebrates (e.g. Peck 1994; Hogg and Stevens 2002). Hughes and Worland (2010) considered that E. murphyi could potentially be wind dispersed on Signy Island, or via the feet of birds. However, the detailed distribution mapping of Bartlett et al. (2019) found that the species’ current distribution on the island is effectively explained through dispersal via human movement. Passive aeolian dispersal of adult Chironomidae has previously been suggested as a form of trans-oceanic movement (Krosch et al. 2011). Epizoochory has also been proposed as a dispersal mechanism that could help explain the distribution of some Antarctic Acari (Pugh 1997). Given the potential of both E. murphyi and B. antarctica to survive prolonged periods of seawater exposure, and the pattern of ocean currents in the region, it is reasonable to infer that the distribution of B. antarctica along the Antarctic Peninsula could be explained, in part, by oceanic drifting/rafting, and that this cannot be excluded as a potential distribution pathway for seawater tolerant invertebrate species, now including E. murphyi. Belgica antarctica is currently distributed throughout the coastal regions of the western Antarctic Peninsula to southern Marguerite Bay (Allegrucci et al. 2005; Gantz et al. 2018). With its known ecophysiological pre-adaptations, given opportunity, E. murphyi could in principle occupy the same distribution (Pertierra et al. 2020). Both E. murphyi and B. antarctica have similar life cycles, physiological tolerances and, potentially, diets (Baust and Edwards 1979). However, a key difference is that E. murphyi is parthenogenetic and able to emerge over a much more extended period in the summer, rather than in a more time-constrained event as is the case for B. antarctica [compare Bartlett et al. (2018) with Sugg et al. (1983)]. This may give E. murphyi a competitive advantage and allow it to increase in population numbers more rapidly. Similar scenarios in temperate invertebrates have seen parthenogenetic species invade twice as rapidly as sexual species, and invading species often outcompete native organisms they may share a niche with (e.g. Vorburger et al. 2003).