The spirit of Antarctic invasions future?

Dickens wrote A Christmas Carol during a change in how Victorian England viewed the Christmas holiday. It’s clearly not Christmas … and certainly isn’t a jolly time. But, taking some artistic liberty from how Dickens outlined the five chapters of A Christmas Carol, there’s been a small flurry of papers published on the future of invasions in Antarctica.

Biological invasions, as one consequence of global change, have very real implications for biodiversity on a global scale. Invasions of fungi, terrestrial plants, invertebrates, and vertebrates have occurred over the last 200 years on the Antarctic continent and its surrounding islands (Frenot et al. 2005), but these are largely terrestrial invasions.

Marine invaders have wreaked havoc throughout the world’s oceans and near shore marine communities … is Antarctica the final frontier for invasive marine species?

STAVE ONE

The great White Continent is one of the most remote places on Earth. For marine species, in particular, the shallow benthos has remained a last, pristine ecosystem due to physical distance (>1000 km), the Antarctic Polar Front, and the constantly near-freezing waters.

While species have breached this barrier naturally (see this #StudentSciComm post here about kelp rafts), it would take a very long time to disperse to the islands of the Antarctic Peninsula (but see Stave Four below). Nevertheless, biological invasions are increasingly a concern in the Anthropocene with increased tourism (42,000 tourists landed in the 2017/2018 season, Hughes et al. 2020) and ever-increasing temperatures.

There are strict rules on the dumping of ballast water, but what about organisms hitching a ride on the hull of a ship? Or, on the boot of a tourist taking the trip of a life time? Or, on an alga?

Temperatures have acted as a formidable barrier to marine benthic species invading from less extreme environments whether they arrive naturally or by some anthropogenic means. With increasing temperatures, there’s more than just massive ice sheets breaking free. Thermal barriers may become porous.

Certain taxa that are good hull foulers, let’s say, may be able scoot over what were previously rather insurmountable obstacles and become established in Antarctic waters.

STAVE TWO

In other regions of the globe, we are often playing catch up with species invasions. We use an arsenal of tools to figure out where a species came from (i.e., the source), how it got to this new area (i.e., the vector), the probability that it will be established (though for many marine species they’re already there before they’re noticed), and, finally, the longer-term consequences of establishment.

In Antarctica, there are no confirmed population of non-native marine species (McCarthy et al. 2019). Nevertheless, as these waters have high levels of endemism (>50% of marine taxa) and unique combos of species, understanding and preserving Antarctica biodiversity is a major conservation priority.

Cataloguing species is a must. Not only because invasions could arise from a fouled hull of a tourist ship, but because invasions could happen from a species native or endemic to one region in Antarctica arriving in another:

Six distinct biogeographic regions have been identified within the APR, alongside another 10 regions in continental Antarctica, and at least a further 10 comparable distinct areas can be recognized in the various sub‐Antarctic islands (from Hughes et al. 2020).

An example of different bioregions around Antarctica – Updated version of the Antarctic Conservation Biogeographic Regions from Terauds and Lee (2016).

Given that many marine invasions have happened under the very noses of researchers out looking for invaders, it’s perhaps not unsurprising that monitoring protocols are lacking in Antarctica where researchers aren’t out and about year as ‘easily’ or frequently as in other parts of the world.

Hughes et al. (2020) report the consensus of a working group composed of experts from nine nations that met in Cambridge in 2018 to asses the risk of invasion in the Antarctic Peninsula region over the next 10 years. They established thematic groups and made a list of potentially invasive non-native species that had a high risk of arrival, but excluded the following:

  1. Species that might arrive from their native range by natural spread without intervention even though this might be a consequence of global change (but, see Stave Four)
  2. Parasites (le sigh … parasites never get their due, do they?)
  3. Microorganisms and macroscopic fungi

The working group identified 103 species that warranted further review. From this list, there were 13 species that had a high risk of invading the Antarctic Peninsula region and causing adverse effects for biodiversity and the ecosystem in general. The authors did note that this is only for the next 10 years … what changes may come beyond that with a ‘business as usual’ approach to mitigating the effects of climate change?

Hughes et al. (2020) found eight marine invertebrates, one alga, two terrestrial inverts, and two vascular plants.

The alga in question is wakame, or the kelp Undaria pinnatifida. Being an algal enthusiast, I was disappointed Undaria didn’t merit more of a discussion. It is found all over the world and has spilled out of marinas and aquaculture facilities into nearby rocky shores and subtotal zones. In its native range in Russia, the coldest sea surface temperature is -0.6 C where it can survive (Skriptsova et al. 2004), but, for sporulation and completion of the complex, haplodiplontic life cycle, temperatures need to be above 13 C (Thornber et al. 2004). Thus, for the time being, it might be impossible for Undaria to recruit if its propagules can’t be produced or survive in the cold waters of the Peninsula.

Curiously, there were three species of Mytlius, a genus that includes several notorious invaders around the world. They live quite happily on hulls, but can they survive in frigid waters?

STAVE THREE

Whereas a few non-indigenous invertebrates have been occasionally found in the field, these records have been limited to observations of one or two adult individuals, colonies, or several larval stages, none of which have been known to successfully settle and establish, a necessary step in the invasion process … (from Cárdenas et al. 2020).

Mussel invasions are commonplace throughout coastal regions of the world and there’s no debate about the roles mussels play in structuring these communities, both in freshwater and marine ecosystems.

Published a few short weeks ago, Cárdenas et al. (2020) found the first settlement of a cohort of Mytilus cf. platensis in a shallow subtidal habitat in the South Shetland Islands (Figure 1).

Here, the authors found teeny tiny mussels growing on a sponge in Fildes Bay (or also known as Maxwell Bay). Because they were so tiny, they had to barcode them in order to determine which species they were … apparently the mytilids are a giant taxonomic mess – a story for another day.

Figure 1 from Cárdenas et al. (2020) showing A) dense aggregations of Mytilus spp. in the Straight of Magellan, B) small recruits shown growing on an endemic sponge, and C) the haplotype network based on CO1 assigning the collections in Fildes Bay to the Southern Patagonian clade of Mytilus cf. platensis.

This clade of mytilids were able to disperse to the Kerguelen Islands on strong eastward currents in the late Tertiary era, though the Antarctic Polar Front poses a barrier to dispersal to the South Shetlands today.

Today, ship traffic is the most likely vector, but it’s unclear whether adults hitched a ride on a hull or larvae escape from ballast water. Due to the legalities associated with dumping ballast water, it’s more likely adults spawned. Worryingly, that means that early life stages were able to complete metamorphosis … the pretty strong environmental filters that were thought to prevent mussels from completing their life cycle seem to not apply here. Why is a question that needs rather immediate experimentation.

Can mussels complete their life cycles at the chilly temps found in these waters?

If they can, what will the ecological and evolutionary implications be? Could Fildes Bay serve as a stepping stone to a full fledged Antarctic invasion?

The Antarctic constitutes a distinct biogeographic realm, and global warming will not only put charismatic native species at risk, but also lower dispersal and physiological barriers to NIS in intertidal and shallow waters. (from Cárdenas et al. 2020).

STAVE FOUR

Ships might bring invaders, but so can ‘natural’ dispersal that may be enhanced by changing environmental conditions. Marine organisms are more than happy to hitch a ride on kelps. And, kelps drifting toward Antarctica isn’t something that was just discovered recently (see here).

Avila et al. (2020) have followed up on the work by Fraser et al. (2018) about kelp rafting their way to the Antarctic and what wee beasties may be along for the joy ride across the Drake Passage.

On the shores of Deception and Livingston Islands, fresh specimens of Macrocystis pyrifera and Durvillaea antarctica (no, it’s not a native) have been found with a host of animal and algal passengers (see figure below from Avila et al. (2020)).

Rafting kelp and passengers. Macrocystis pyrifera (A) with passengers found at Deception Island, and Durvillaea antarctica (B) with cirripeda from Livingston Island, South Shetland Islands, Antarctica. (CF) Passengers found on M. pyrifera at DI: the red alga Ballia callitricha (C); the bryozoan Membranipora membranacea (D); the cirripeda Lepas australis (E); and the cirripeda L. anatifera (F) on D. antarctica from Livingston Island. from Avila et al. (2020)

Significantly, Membranipora membranacea, an encrusting bryozoan, was found. This species has been implicated in kelp losses in the Northwest Atlantic. It’s grows quickly, can undergo both sexual and asexual reproduction, and can eat under a wide range of flow conditions … basically it’s a great invader. It might be able to survive in colder waters and use the ‘warmer’ waters of Deception Island (there’s an active volcano) as a bridgehead. Yet, it’s not one of the top 13 species identified by Hughes et al. (2020), nor in their list of 103 species of concern.

Could a species like M. membranacea be a harbinger of what is to come? Avila et al. (2020) argue that

these species may be useful indicators of climate change in Antarctic habitats and should be carefully monitored during the next years.

STAVE FIVE

Species along the coastline of Antarctica have been effectively cut off from the rest of the world, but our world is connected as never before (as we are all no doubt aware sitting working remotely at the present time).

While drifting brown algae showing up in the Antarctic has been documented for over 100 years (Zaneveld 1993), what if crossing frequency is increasing as environmental conditions change throughout the Southern Hemisphere? What if crossing time is also occurring more quickly?

Certainly ships can make it across the Drake more quickly than a kelp and in their recommendations Hughes et al. (2020) point out that

[m]echanisms and practices to reduce the risk of marine non‐native species introductions on ship hulls are likely to be minimal if present at all.

Indeed, 56% of the vessels arriving in the South Shetland Islands had sailed directly from the Straight of Magellan and the Beagle Channel, genetically the source of the teeny mussels found in Fildes Bay (Cárdenas et al. 2020).

Thus, effective biosecurity measures and more widespread surveillance is necessary. Invasive marine species have gone undetected right next to marine labs due to issues with confused taxonomy where native species look very similar to recent invaders.

Ecological and environmental change, including increasing water temperature, decreasing ice cover, and increasing ship activity, may aid the arrival, establishment, and spread of non-native species in the coming decades (McCarthy et al. 2019).

What can we do, especially now for those that frequently head to the ice, but are at home?

McCarthy et al. (2019) recommended that researchers:

[p]erform detailed analyses of records in databases such as OBIS and GBIF of species with distributions that include but are notlimited to the Southern Ocean.

Some species may already have records in Antarctica, sub‐Antarctic islands, and the Southern Ocean. Maybe not a bad idea to hunt around these databases while stuck at home dreaming of being in the field?

References

Avila C, Angulo-Preckler C, Martín-Martín RP, et al. (2020) Invasive marine species discovered on non-native kelp rafts in the warmest Antarctic island. Scientific Reports 10: 1639.

Cárdenas L, Leclerc J-C, Bruning P, et al. (2020) First mussel settlement observed in Antarctica reveals the potential for future invasions. Scientific Reports 10: 5552.

Fraser CI, Morrison AK, Hogg AM, et al. (2018) Antarctica’s ecological isolation will be broken by storm-driven dispersal and warming. Nature Climate Change 8: 704-708.

Frenot Y, Chown SL, Whinam J, et al. (2005) Biological invasions in the Antarctic: extent, impacts and implications. Biological Reviews 80: 45–72.

Hughes KA, Pescott OL, Peyton J, et al. (2020) Invasive non-native species likely to threaten biodiversity and ecosystems in the Antarctic Peninsula region. Global Change Biology 26: 2702-2716.

McCarthy AH, Peck LS, Hughes KA, Aldridge DC (2019) Antarctica: the final frontier for marine biological invasions. Global Change Biology 25: 2221-2241.

Skriptsova AV, Khomenko V, Isakov V (2004) Seasonal changes in growth rate, morphology and alginate content in Undaria pinnatifida at the northern limit in the Sea of Japan (Russia). Journal of Applied Phycology 16: 17-21.

Terauds A, Lee JR (2016) Antarctic biogeography revisited: updating the Antarctic Conservation Biogeographic regions. Diversity and Distributions 22: 836-840.

Thornber CS, Kinlan BP, Graham MH, Stachowicz JJ (2004) Population ecology of the invasive kelp Undaria pinnatifida in California: environmental and biological controls on demography. Marine Ecology Progress Series 268: 69–80.

Zaneveld JS  (1993)  Iconography of Antarctic and Sub-Antarctic Benthic Marine Algae. Part II. Phaeophycophyta. Stuttgart, Gustav Fischer Verlag

About Stacy Krueger-Hadfield

I am a marine evolutionary ecologist interested in the impacts of seascapes and complex life cycles on marine population dynamics. I use natural history, manipulative field experiments and population genetic and genomic approaches with algal and invertebrate models in temperate rocky shores,estuaries and the open ocean.
This entry was posted in blogging, community ecology, comparative phylogeography, conservation, DNA barcoding, ecology, evolution, mini-review, natural history, phylogeography, Science Communication and tagged , , , , , , , , , . Bookmark the permalink.