Marine tropicalisation in response to climate change: what, why, where, who and the way forward

This presentation will examine marine tropicalisation in response to climate change. This first image is my attempt to show a vision of a very different future marine life for areas such as Sydney, which may result from climate change. It's a topic that I've become involved with pretty much by chance, and only fairly recently but I can see that museums have a really important place in this area, to make a real difference in understanding. This is because of the collections they hold, which represent historical databases, and their taxonomic resources, which include comparative specimens, literature, collegial networks, and most importantly, their staff expertise. So, my aim in this talk is to provide more detail on these points, as well as a definition of what marine tropicalisation is, indicate why it occurs, where it's happening, give some examples of organisms in which it's evident and demonstrate ways in which we can better understand what is happening and respond to it more effectively. And it's coming from an East Coast Sydney perspective, as in this image.

I'm using the term climate change in the current contemporary context of rapid and extreme heating of the environment, caused by human activities, principally through the burning of fossil fuels, combined with large scale deforestation since the 1800s. And I'm going ahead on the assumption this is not a controversial topic to this audience. The increased frequency and ferocity of storms, drought and fires, sea level rise and coastal erosion, coral bleaching and ice caps retreating are some of the highly publicised outcomes of climate change, and rightly so because of the catastrophic consequences. However, another outcome that I think has been a little more under the radar, and certainly in the mainstream media, but also has significant environmental and economic impacts is species range shifts. Range shifts can be defined as a change in the distribution of species from previous boundaries. This can involve a reduction in the area that a species lives in, which is often referred to as a range contraction. Another type of range shift is a range expansion, where the area that a species lives in increases. These definitions come from a website known as Redmap, which I'll come back to and talk about more in the presentation later on. So, to illustrate these concepts a little better in the climate change context I have first chosen some examples that are in an altitudinal dimension on land.

This initial example is from paper looking at alpine vegetation. The first image shows the scenario of a mountain, where the current condition has a forest at lower elevations, with a tree line at a particular altitude, a tree limit above this and large treeless alpine area at the highest elevation, which is occupied by other vegetation. The next image shows the expected outcome with warming due to climate change. The forest area, previously limited by colder conditions occurring at higher altitudes, is expected to advance upslope in a range expansion as climate warms, the tree line and tree limit also correspondingly advance upslope. Ultimately, this leads to reduced area and range contraction for the alpine species. So, from this theoretical example, we can look at a real example where something similar has happened for tropical bird populations. This data comes from a study that examined three species of birds in mountains of Peru using mist net surveys in 1985 and 2017. So, the image shows the results of the 1985 survey, which found three species that was distinctly distributed at different altitudes. The next image shows the 2017 situation. The antbird a low elevation species has benefited from warming expanding upslope to occupy a 17% larger area. However, the range or area occupied of the barbet that has shrunk by 66% and the antshrike originally occupying the highest elevations has disappeared from the area completely.

So, moving on to a marine example. This is some information from an Australian Museum factsheet for one of the most common sea urchins occurring around Sydney, the spiny sea urchin, Centrostephanus rodgersii. A couple of points to highlight. Firstly, the size of these animals: they're up to at least 17 centimetres in diameter, so reasonably large and certainly not small or insignificant. Secondly, the notes at the bottom indicate individuals can often be found in large numbers and impact the ecology of rocky reefs by grazing kelp to form barren areas known as white rock or urchin barrens. Also, this is a relatively long-lived species with ages up to 35 years recorded and sexual maturity is reached after only four to five years. Historically, the southern Australian distribution was restricted to the mainland, but now includes a relatively recent range expansion poleward across latitudes. This was first detected in the Kent Islands in Bass Strait in 1974. And subsequently at St. Helens in north-eastern Tasmania in 1978 and then later around the Tasmanian coast. The impacts of grazing by this species have been significant, with local loss of over 150 species that live among Tasmanian kelp beds recorded since the arrival of the urchin. So clearly, this poses a major threat to the structure and functioning of Tasmanian rocky reef ecosystems, and also to the productivity of lucrative fisheries for abalone and southern Rock Lobster that depend on this kelp habitat.

To provide some more perspective on the situation, this study from the University of Tasmania compares surveys from 2001 to duplicates in 2017, examining urchin density and associated barren reef along the Tasmanian east coast. In these surveys, there are 13 sites along the east coast, with replicate subsites and transects at each that were observed by scuba divers and using towed video. Major findings from it are that the abundance of Centrostephanus increased. This was particularly noticeable in the northern sites. In this northern area, average density increased to over 2,500 urchins per hectare. This represents a 75% increase in the survey period. Toward the south, the species remains relatively rare with less than 20 individuals per hectare. But scaling of these figures suggests the population of this species in Tasmanian waters is estimated to have exceeded 20 million individuals by 2017. Barren areas attributed to sea urchin grazing have similarly increased. Low density of both abalone and Rock Lobster were observed on urchin barrens. However, on a positive note, the study suggested that the annual increase of urchins has been at a scale where control through rebuilding of predators, or by upscaling or culling and harvesting would appear plausible. In particular, it found a decline in urchin abundance at St. Helens, where commercial fisheries have harvested them since 2009. In the fishery, the sea urchin gonads or roe, are extracted for sale in the food market, predominantly for export and notably to Japan.

So, to this point, I've touched on the what, who and where aspects of this topic. Moving on to the why in the marine situation with particular relevance to this sea urchin example. A fundamental process determining marine connectivity and distributions, at least for relatively shallow water species, are oceanic currents. Toward the water surface these currents are almost entirely wind driven, and combined with the rotation of the Earth, in the southern hemisphere ocean basins this results in counter clockwise gyres, in the northern hemisphere, clockwise gyres. Where these currents meet continental margins, they're constrained and formed boundary currents flowing along the continental margins. Famously as featured in the movie Finding Nemo, we have the East Australian Current, which is the western boundary current of the South Pacific Ocean gyre. This has long been recognised as being somewhat variable but brings warm tropical water south along the east coast into New South Wales, before turning East and leaving a trail of warm core eddie that peel off to the southeast. Under the climate change regimes we've seen over the last century, the southeast Australian region has become recognised as a global hotspot – pardon the pun there, with waters warming nearly four times faster than the international average. On the East Coast, this is largely due to in intensification of the East Australian Current, extending further south more regularly, with frequent large-scale eddies extending along the coastline of Eastern Tasmania. This warming has resulted in the mean winter water temperatures of Eastern Tasmania being elevated. And in the case of the sea urchin the temperature is consistently above the 12 degrees Celsius threshold, which would otherwise limit survivorship of the planktonic larval stage. This larval stage is produced from fertilisation after spawning of eggs and sperm directly into the water by the adult urchins. The larvae are known to survive for up to three months and genetic analysis has shown that recruitment of juvenile sea urchins in Tasmania had their origins from populations in New South Wales, rather than locally in Tasmania. I could provide a number of other examples where something similar has occurred. For instance, the octopus Octopus tetricus also found at Sydney has undergone a similar range expansion into Tasmania. Worldwide, because of the prevalence of these boundary currents moving warm water more consistently into areas where it was previously rare, there are many records of species beyond this historical poleward range edges, establishing populations in areas where minimum annual temperatures had previously prevented their persistence. This is the pattern which we term tropicalisation.

As I said, there are many marine examples of this that I could discuss, but I'll use two that I have been directly involved with to demonstrate a few points. Probably, firstly, about serendipity, but also about how the museum has an important role to play in recognising examples of this when they occur. The first one I'm going to talk about is the sea star Pentaceraster regulus and this initially came to my attention in early 2008 when I was approached by fisheries officers from Forster at Wallis Lake, which is an estuary a bit over 200 kilometres north of Sydney. They wanted to identify a large sea star that a member of the public had found in the local marina and was curious about. They sent photographs and the sea star certainly looked unusual for that area. But as with a lot of invertebrates, for a positive identification, fine scale features need to be consulted, so they sent us two specimens. Anna Murray here at the Australian Museum identified these as Pentaceraster regulus, a species that is otherwise found most closely to Wallis Lake, at Lord Howe Island about 600 kilometres offshore and known to receive a tropical influence via the East Australian Current. On the mainland, the closest record was also about 600 kilometres away at the north, at Stradbroke Island. We sent this information off to Fisheries and the reply was, “Oh, that's interesting. We get a lot of boats from Lord Howe Island, and perhaps someone brought them here and tossed them overboard in the marina.” Fast forward to 2020, and an email came to me via the Museum's inquiry centre Search & Discover, and this was from a high school teacher from the same area. He takes Year 9 marine and aquaculture technology students, snorkelling in the lake, and here a sea star they couldn't identify. I recognised that it's probably the same species and was able to get specimens to confirm this. It turns out, it was quite common in 2020 in the area, with specimens in a range of sizes from about eight centimetres in diameter, up to 26 centimetres, suggesting there's a population established with most, if not all of the lifecycle taking place there. And because in the intervening period I had become more aware of the importance of these records, and it was clear it wasn't a one-off situation, I contacted a sea star expert, Chris Mah, who was able to confirm the identification. We were then able to write it up and have the information peer reviewed and published as a further probable example of tropicalisation. Evidence that this is a relatively newly established range extension comes from museum specimen records that help to make up this map. Using data from these historical samples provides an important baseline to identify changes and long-term trends. The collections of the Australian Museum are particularly relevant in this situation, as they include specimens from the early review and study of Australian sea stars from the late 1800s and early 1900s through to the present. It's also the primary institution receiving these samples from New South Wales waters, including Wallis Lake. In this collection, we have about 2,500 registered samples of sea stars from Queensland, the state to the north, and a similar amount from New South Wales. Because of the longer coastline of Queensland, you could argue that New South Wales has actually been more intensively sampled. I know that wild animals don't have any knowledge of these political state boundaries but in this case, the state border is a useful geographic reference point. Prior to the records from Wallis Lake that I've discussed, the only New South Wales records are from Lord Howe Island whereas from Queensland there are records from 13 widely dispersed localities with dates from 1908 through to 1979. It's also worth noting that this is a large and spectacular species, it's not readily overlooked and that attention was drawn to it through members of the local community who were unfamiliar with it as an apparent recent arrival. So given this is also a large predatory species, I think we need to be concerned about this apparent range expansion. Additionally, I should point out that there are citizen science reports of it occurring around Sydney, which are fairly convincing from the images I've seen, but we haven't yet got specimens. So perhaps this is an interesting project for someone out there to follow up.

So, this brings me to the second example I've been involved with. This started with public inquiries Shane Ahyong and I received about an unusual jellyfish, again, appearing in Wallis Lake, but also in Lake Illawarra. And this was in 2013, in Lake Illawarra and 2014 in Wallis Lake, and they're both estuaries, Wallis Lake again north of Sydney and Lake Illawarra just south of Sydney. We were able to obtain specimens from both of these locations and identify them as two different species in the genus Cassiopea. Jellyfish in this genus are known to be fairly unusual because instead of spending most of their life in the water column, they actually settle on substrates in shallow water and become quite sedentary. In the image to the right, you can see my mouse pointer there, along the shoreline here you can see a bloom of these jellyfish in Brazil. They're all the white disks you can see along the shoreline here. These jellyfish have been reported to grow up to 49 centimetres in diameter and occur in densities of over 160 individuals per metre square. They are also predators that feed on plankton which they trap in mucus that is loaded with stinging cells. This mucus can be produced in such large quantities, that it's been implicated as the cause of discomfort reported by swimmers, which is known as stinging water that takes place in areas where Cassiopea also occur. Again, this is generally considered a tropically distributed taxon with the closest previously recorded locations at least 600 kilometres to the north in the vicinity of Moreton Bay in Queensland, around the Gold and Sunshine Coast. Shane and I also published these records in 2016 noting that this taxon is considered invasive in other locations, and it has the potential to have a significant negative ecological, and commercial impact in areas which it newly colonises. In 2017 reports came to me with a similar jellyfish in Lake Macquarie. Another estuary a bit under 100 kilometres north of Sydney as the crow flies. Shane and I were able to convince Claire Rowe to take on study this PhD project with Will Figueira at Sydney Uni as her current co-supervisor. Claire used a kayak to access populations of the jellyfish as shown in the bottom left image, as these jellyfish often occur in water depths as shallow as 30 centimetres. So access is difficult in a conventional boat and if you try and get to them on foot, you sink up to your knee or deeper in soft mud. She also supplemented this work with some drone studies as well, aerial drones.

Claire began her study in mid-2018, and submitted this year in March, and had just been accepted so you can safely call her Dr. Claire now, if you happen to see her. She's done a pretty amazing job and this is her work, which I'm hoping she'll talk about at the AMRI student forum in December. But I wanted to use it to highlight some of the ways in which you can learn quite a lot in a relatively short time with some concentrated study. So, when Claire started, there was practically nothing known about the Lake Macquarie population of this jellyfish. The red star there indicates that we only knew about one site where they occurred and we couldn't really readily identify this jellyfish to species. Through Claire’s survey work we now know that the jellyfish is widely dispersed in the lake being found initially in seven sites in the southern half separated by about 15 kilometres during 2018 through to early 2021. Two additional sites that started off as controls without any jellyfish being detected in 2018 subsequently were found to have jellyfish. And this suggests the distribution within the Lake may be expanding. From analysis of the CO1 gene and comparing populations from other localities and GenBank records, Claire was able to show that the material from Lake Macquarie is the same species that's found in Wallis Lake, and it's also found in Pelican Waters on the Sunshine Coast in Queensland. However, this clade also contains specimens from widely dispersed international localities, including Panama, Florida, Palau, Brazil, and Hawaii. So not only do we seem to have an example of tropicalisation, but also probably an invasive species to Australia. Additionally, Pelican Waters is the type locality for a species described in 2010. But it seems that this is a junior synonym of the overseas material identifiable as Cassiopea xamachana, which was described in 1892. Claire backed up these conclusions from genetic work with some morphometric analysis as well. Additionally, she looked seasonally over three years at environmental parameters that may impact the density of the jellyfish. This graph shows the mean density of Cassiopea for replicated seasonal sampling, during this period across multiple study sites in Lake Macquarie. The populations peaked in May to July each year but crashed by August and this could be correlated with water temperature in the field dropping to 12 degrees Celsius in winter, and lab studies confirmed that specimens exposed to temperatures approaching this had a lower physiological performance than those exposed to temperatures just two degrees Celsius warmer. However, in 2021, the May-June bloom failed to eventuate and this can be attributed to high rainfall event that occurred in March of that year, where salinities dropped below 13 parts per 1000. And prior to that the lowest salinity in which jellyfish have been detected, was 26 parts per 1000. So a general conclusion is that although there can be seasonal parameters, including water temperature that influenced the presence of jellyfish in Lake Macquarie on an annual basis, these can be overwritten by broader large scale weather patterns during some years.

So, moving on to the way forward with better documenting and better understanding these rate extensions, I wanted to bring this website Redmap to your attention. I mentioned it before. Redmap stands for range extension database and mapping project. So, as indicated in this slide, the project invites people to share sightings of marine species that are uncommon in their local areas. And the aim is to use the citizen science data to map which Australian marine species may be extending the range distribution and highlight regions that may be experienced the most change so that research can be focused there. Images and information can be uploaded to the site. There is a panel of experts to review submissions and follow it up. The site currently has a focus on fish and I know Mark McGrouther from the Australian Museum has been involved with providing records from his Australasian Fishes website to Redmap. However, algae, invertebrates, mammals and reptiles are also represented already.

So, using some of the data collected by Redmap, as well as search of the literature on the subject, this review of climate driven redistribution of marine species around Australia was published last year. Just to share some of the findings from it quickly. The review concluded that changes in the distribution of species are an accelerating impact of climate change. We lack a good understanding of patterns and processes at various scales, particularly in the southern hemisphere. This is particularly problematic in Australian waters, which encompass the world's third largest marine jurisdiction, and are warming at rates two to four times the global average. In Australia since 2003, 198 marine species from 9 phyla have been documented shifting their distribution and most of these shifts are poleward. Most documented shifts are of coastal fish species in subtropical and temperate systems with tropical systems in general poorly explored. Additionally, to this I’d add that invertebrates, other than perhaps corals, aren't receiving proportionally, the research attention they warrant. Another problem noted was that most distributional changes are often only described at the poleward boundary, with fewer studies considering the changes that are happening at the warmer limits. Results demonstrate the importance of historical data sets, underwater visual surveys and citizen science. Additionally, a number of extra ways to progress knowledge is suggested, including review of historical information, genetic sampling and predictive modelling. In particular, the study notes that environmental DNA is becoming increasingly used to detect the presence of rare or invasive species in an area and these approaches are now being incorporated into range shift studies.

So, in conclusion, I hope that I've made you alert but not alarmed. And for those of you who are in position to make marine observations you're aware of where you can take these if you're curious about them.