The origin of species: the Australian connection

The Great Barrier Reef: Designed to survive (built to last?)

6 February 2007

Professor Terry Hughes
Director, ARC Centre of Excellence for Coral Reef Studies
James Cook University
Townsville, Queensland

Professor Terry Hughes

Professor Hughes has made outstanding contributions to marine biology and coral reef ecology. His work includes the first detailed account of the mechanisms underlying the long-term degradation of coral reefs. His research on the Great Barrier Reef examines regional-scale processes, and will help to predict the effects of global warming on coral reefs.

In recent years, his research has evolved in a new direction: moving from an ecological focus to a broader evaluation of the linkages between coral reef systems, the goods and services they provide to people and the welfare of human societies. The focus is on finding solutions for managing resilience and for coping with change and uncertainty in complex social-ecological systems.

Terry's profile at the ARC Centre of Excellence for Coral Reef Studies
www.coralcoe.org.au/research/terryhughes.html

Great Barrier Reef Marine Park Authority
www.gbrmpa.gov.au

CRC Reef Research Centre
www.reef.crc.org.au

Coral bleaching - will global warming kill the reefs? (Nova: Science in the news)
www.science.org.au/nova/076/076key.htm

Introduction

Professor Kurt Lambeck: Good evening. I am Kurt Lambeck, President of the Australian Academy of Science, and I welcome you this evening. This is the fourth lecture in the series 'The origin of species: the Australian connection'. Shortly I will introduce our speaker for tonight, Professor Terry Hughes.

The lecture series is intended to highlight the contribution Australian material has made to the development of Charles Darwin's ideas on evolution. Darwin visited Australia for an extended period during the voyage of the Beagle, and during his time here he made numerous observations that contributed to his subsequent development of The origin of species.

This in itself is a cause for celebration, but we have a second reason for holding these lectures: our concern about Intelligent Design creeping into schools as a scientific alternative to evolution. One of the reasons for these lectures is to try to get the story of evolution, and the way science works, out into the broader community. The lectures try to illustrate that, while scientific ideas may be imperfect, they are subject to testing, and that, as a result of this testing, further developments of the theory occur et cetera. So there is a basis for testing everything we do.

The lectures have tended to follow that pattern. The first lecture was on the position of Australia's mammals in the evolutionary scheme, the second one was on proteas and the drifting of continents, and the third one was on the evolution of the complex social system of Australian birds. This evening's lecture turns to the marine environment and to coral reefs, specifically, how reefs respond to rapid climate change.

Our speaker tonight is Professor Terry Hughes from James Cook University, where he is Director of the ARC Centre of Excellence for Coral Reef Studies. Terry is a Fellow of the Academy, but more importantly, he is one of Australia's foremost experts on marine biology and coral reef ecology. His research has included the underlying mechanisms of long-term resilience of corals to environmental change. It is important to note that he also applies his research to understanding the linkage between reef welfare and human welfare and trying to find solutions for managing this linkage.

So without further ado I hand over to Terry Hughes.

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Professor Terry Hughes: Thank you very much. It is a great pleasure to be here.

Today I will talk about the Great Barrier Reef and discuss the evolutionary history of corals and reef fishes. I will spend time talking about the ecology of reefs, particularly in the context of threats to reefs from climate change.

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I will use this outline as a roadmap throughout the talk. I will start off by talking about evolutionary history. I will also talk about some weird and wonderful adaptations by corals. After that I will talk about some contemporary threats to coral reefs, and what we can do about it. And finally I will talk about some of the management issues, particularly in the context of climate changes and the Great Barrier Reef.

Let's start out by looking at some evolutionary aspects of coral reefs. One of the great embarrassments to people who denounce evolution is the fossil record. In Darwin's time there was even a theory that fossils were placed there by the Devil, because they did not conform to the contemporary model.

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Coral reefs, as it happens, have a wonderful fossil record. This photograph shows fossil reefs from the Huon Peninsula, in Papua New Guinea. This part of the world is tectonically unstable and you can actually see fossil reefs that have been lifted up out of the ocean. Today there are modern reefs under the water and inland from them there are fossil reefs.

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Looking at the fossil reefs more closely, at the accretion of the reefs, we can measure reef growth and determine dates. The older portions of the reef are found at the bottom of this geological sequence, which is very young, and younger deposits are at the top.

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If we take an even closer look at this deposit, we can see that there are lots of fossilised corals. In fact, because this is a very young geological feature, these are actually contemporary corals that are found on modern reefs today. The state of preservation is such that we can distinguish individual features of coral skeletons and we can identify these corals at the species level.

In this photograph, one of our students has run a transect tape along the fossil reef and is measuring the abundance and sizes of the corals.

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In much the same way, a diver can do a similar study on modern reefs. So there are a lot of parallel questions that can be investigated using fossil coral reefs as well as contemporary ones.

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Corals are not the only group of organisms on reefs that are well preserved. Fossil fish from coral reef habitats are found around the world, and we can look at the fossil representatives alongside their modern counterparts. The fossil fish in these photographs are exquisitely preserved. We can see individual features of their rays and we can even, in some cases, look at what they ate for breakfast before they were fossilised.

This information tells us a lot about patterns of speciation and extinction during the long geological history of fossil reefs.

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Another way to look at the evolutionary history of coral reef organisms is to use a phylogenetic approach. Using molecular techniques, or sometimes morphological data, we look at who is related to whom and which branch of the tree of life, if you like, gave rise to other, more recent branches.

This work was done by my colleague David Bellwood, from Townsville, and is actually an independent reconstruction of evolutionary history that we can confirm with the fossil record.

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By combining the data from two sources - fossils and phylogenetic data - we can determine when these divergences took place. These patterns of evolution, speciation and extinction are the basic processes that gave rise to the modern-day patterns of biodiversity across the globe.

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If we look at a map of the world today we can see three different regions where coral reefs are currently found. Each of the three regions has a very different geological history. For instance, the east Pacific coral reefs were isolated from the Caribbean, with the merger of South America and North America, relatively recently. So this region is now very depauperate - it has lost a lot of species in recent geological time, as indeed has the Atlantic province.

The current biodiversity hotspot for coral reefs is in our part of the world, particularly in the triangular region up to the Philippines in the north and down to the Great Barrier Reef. Generally, there are between 10 and 15 times more species - depending on the taxonomic group - in this part of the world than there are in the Atlantic.

So why does that matter?

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Patterns of biodiversity, it turns out, can have a huge impact on the resilience of coral reefs to issues such as climate change, and this relates to the issue of what ecologists call functional diversity. So this pattern is important because biodiversity affords some degree of insurance against extinction of functional groups. Let me explain what that means.

Traditional taxonomy is based on genetic relatedness of taxa. So we classify taxa into species, genera, families and so on. But there is an alternative way to cluster or lump species, based on their function. If you have a particular function that is performed by, say 20 species, then if one or two of those species become extinct that function will remain, compare this with a more depauperate place where a function may be undertaken by a single species.

So let's look at some functions on coral reefs. The main ecological function of corals is providing the three-dimensional structure and reef accretion. If we look at fishes, we can categorise them on the basis of whether they are predators, herbivores or detritivores and so on.

If we compare functional groups of corals, by classifying them into different morphological categories, in the Great Barrier Reef versus the Caribbean, we get a very different picture, and that is what is shown here.

The number of coral species is shown on the vertical axis and the functional group - specifically growth morphology - is on the horizontal axis. The blue bars represent the number of species in the Great Barrier Reef and the red bars represent the species in the Caribbean. For every functional group there are fewer species in the Caribbean, and in some cases far fewer species, than on the Great Barrier Reef.

Let's look at a couple of examples. Staghorn and tabular corals, which are the most three-dimensional corals on a reef, are very important in terms of the habitat structure that they provide to other organisms, like fishes. There is only one staghorn and one tabular coral in the Caribbean and unfortunately both of these species are now listed, by the US EPA, as threatened. In contrast, in our part of the world we have about 35 species of highly three-dimensional corals and that affords some level of insurance or protection in this more speciose portion of the coral reef world, as compared with the Caribbean.

Later on I will show you some information about the extent of degradation on Caribbean reefs and I will put the changes to the Great Barrier Reef in that broader context.

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That was a very brief outline of the evolutionary history of coral reefs and how diversity has been generated through a long history of speciation and extinction. I would like to move on now and talk about adaptations by corals.

Corals are unusual animals, in that most studies by biologists are on more familiar mobile organisms, like mammals, reptiles and fishes. Corals are also unusual in that they are colonial organisms: their bodies are made up of replicated building blocks - the polyps - and that design constraint gives them a number of characteristics, which I will try to explain.

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So what are some of the consequences of being sessile? 'Sessile' means stuck to the bottom, literally glued to the bottom for the vast majority of your life. Most sessile organisms have a very brief planktonic phase, which is the only part of their life cycle where they are mobile. The larvae move around, carried by the water column; they have some limited ability to move during this phase. They then undergo metamorphosis: they glue themselves to the bottom and they spend the rest of their life as a sessile organism.

So we can think of a continuum - from being very vagile, or mobile, to being glued onto the substrate.

Let's consider some of the consequences. I'd like you to imagine that you have just completed a brief planktonic phase, you have selected the habitat that you are going to spend the rest of your life in and your bottom is now very firmly glued to your seat for the next 50 years or so. What are the consequences of this?

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Well, in an hour or so, depending on how many glasses of wine you have had, you might need to go to the bathroom, or you might get hungry. Energy intake and the disposal of waste are taken care of in the marine environment because of the hydrodynamics of the water medium.

Here we have a picture of a tunicate, or a sea squirt, with green dye that has been injected into the water, by a scientist, to show the movement of that water. In addition to the ambient current, this organism generates its own currents, which bring it food and take away its waste products. This is very different from mobile organisms, which have complex foraging behaviours and predator-prey relationships and so on.

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If you have ever travelled on an overcrowded plane and had to wrestle with somebody over who got use of the armrest, then you would be aware of another consequence of being sessile - coping with crowding. Healthy coral reefs can be very crowded; this particular patch of reef probably has coral cover of around 80 per cent, with very little free space available. As a consequence, neighbouring organisms compete with each other for space, which sometimes gets very vicious.

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In this photograph, a solitary sea anemone is competing for space with the colonial coral in the background. The white zone here is a zone of death and destruction, where the sea anemone has digested away the soft tissues of the coral, exposing the hard calcium carbonate skeleton that lies underneath.

These organisms are in constant warfare over the limited space available. I will just show you a couple more pictures.

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The soft coral at the bottom is competing for space with a brain coral. Notice the no-man's-land between them.

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Here is another example: in the centre of the picture a small brain coral is competing with a tabular Acropora coral, with a zone of interaction clearly visible between them. This photograph was taken in the daytime, so it looks fairly peaceful, but at night the tentacles of the brain coral come out and are about as long as the width of the zone of interaction. It has succeeded in keeping the faster growing tubular coral at bay, but in the meantime the tubular coral is trying to encircle it by growing out at the sides.

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There are ongoing battles for space.

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Another consequence of being sessile is that you can't run away from predators, you have to deal with predators that come to you. Sessile organisms have evolved a number of defences, typically involving toxins or mechanical defences: being too rubbery or too crunchy or - in this case these are the spicules of a sponge - too spiky for many predators.

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What about sex? If you are stuck to your seat for the rest of your life, how are you going to reproduce?

Mobile organisms have involved courtship behaviour that usually involves a lot of mobility - in humans this usually means going to nightclubs and the like. Sessile organisms don't have these mobile options because they are stuck in their seats.

This is a Grecian urn depicting a scene referred to in a very famous poem, which I will get to in a moment. The urn shows some of the problems with being sessile: the male and female are too far apart to reproduce. So Keats wrote a poem, which is all about the problems of reproducing if you are sessile:

Bold lover, never, never canst thou kiss,
Though winning near the goal - yet, do not grieve;
She cannot fade, though thou hast not thy bliss,
For ever wilt thou love, and she be fair!

You probably weren't anticipating hearing some classic poetry tonight! But the words 'never, never canst thou kiss' and 'though thou hast not thy bliss' show that Keats was aware of the constraints on reproductive systems of being sessile.

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So how do sessile organisms deal with this issue? There are several solutions, one of which is to breed on your own. Many sessile organisms are colonial: they have so-called asexual modes of reproduction. Many of them are also hermaphroditic - in other words, they have male and female organs for reproduction and that raises at least the possibility of self-fertilisation.

Another option is to have a very large penis. Barnacles utilise this option: they have the longest penis in the world, relative to their body size. They keep it inside their shell, rolled up in an apparatus a bit like those things you use to wind up your garden hose. So even if they haven't settled beside their ideal partner, it is possible for them to reproduce with someone in the back row.

But, the most common option is to have what is called broadcast spawning. Unlike more familiar animals like mammals and so on, many marine organisms release their eggs and sperm into the water column and fertilisation takes place externally.

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The following photographs show coral spawning. You see here the individual polyps that make up the coral colony and an egg-sperm bundle which is being released during the spawning period on the Great Barrier Reef. These egg-sperm bundles float to the surface where they break apart and fertilisation takes place a few hours later.

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This is another photograph of a coral colony spawning, taken a little bit further away. Obviously, a lot of energy is put into this annual reproduction event to produce these coral spawns.

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The coral spawning can be seen from the air. This is a coral slick, almost a kilometre long, a day or two after the annual mass spawning of corals.

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The whole issue of dispersal, breeding success and habitat selection at the end of the planktonic phase, comprise reproductive aspects which are key issues for the future resilience of coral reefs. Remember that when Darwin described evolution as 'survival of the fittest' he only had half the story, because evolution is more about leaving more offspring in future generations than other people in the same population. These issues about reproductive success are really crucial, from an evolutionary perspective and from the perspective of resilience of reefs in response to climate change - which is what I would like to get to next.

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There are basically three major threats to coral reefs: over-harvesting, declining water quality and climate change. Although I have listed these as three separate things, I want to make the point, here and later, that they are not separate issues. They are in fact very intimately interconnected.

Over-harvesting is often referred to as a top-down effect, while declining water quality is a bottom-up effect. This terminology comes from the influence of these two issues on the structure of foodwebs, which I will explain now.

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This is a somewhat idealised, simplified foodweb for a coral reef. At the top are top predators and at the bottom are primary producers - which include corals, because they get a lot of energy from photosynthesis, algae for seaweeds and some sponges. In the middle we have second-tier predators and, lower down, herbivores.

The arrows depict the flow of energy, who eats whom, and also the flow of materials within the foodweb.

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The foodweb of virtually every coral reef in the world today has been altered by human activity, and I will show you, again in an idealised fashion, the sort of top-down impacts that can occur through overfishing, through the depletion of predators and large herbivores. They can have spill-on effects down through the food chain.

I didn't bring a picture today, but we can also envisage bottom-up effects whereby added nutrients promote algal blooms and so on that have trickle-on effects up the food chain.

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Climate change is also an issue of increasing concern. I would like to make the point that climate change impacts on reefs are not some distant threat in future decades; climate change has been happening to reefs now for the past 20 years or so, and there is quite a lot of information available on the types of changes that are likely to increase in the future.

This slide shows a landscape photograph of a reef that has been severely bleached. Just by way of background: bleaching occurs when the symbiosis between the coral host and the algal symbiont contained within its tissue breaks down. In this case, the host is stressed by water that is unusually warm and so the zooxanthellae, the symbiotic algae, are expelled. This weakens the coral and significantly increase the mortality rate.

This photograph happens to be dominated by a single species - this is one very large colony, several tens of metres across - and this happens to be a species that is particularly susceptible to climate change.

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A more typical photograph might look like this, which relates to functional redundancy and how having multiple species performing a similar function can give you some insurance against threats to reefs.

This reef is in French Polynesia and we see a sort of checkerboard, some corals have been bleached while others have not. French Polynesia is interesting because the reefs there have been bleached about eight times since the mid-1980s. The coral cover is still very high, but the coral species composition today - this photograph was taken last year - is completely different from the species composition when I was a PhD student (which isn't that long ago).

One point about climate change that I think is important to make is that it is incredibly selective as to which corals are impacted and which ones are not, or at least not to the same extent.

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We can quantify the impact of climate change by running some transects across a landscape and looking at the response of different species - which for simplicity I have labelled as A, B, C, et cetera. The vertical axis shows the proportion of each of the species that bleached during a particular bleaching event.

Species A is obviously very susceptible: every colony we found was bleached. But look at species G, H, I and J: much smaller proportions of them have bleached.

The evidence we have so far implies that bleaching, and bleaching mortality, is actually quite selective. We are beginning to see evidence of very rapid shifts in species composition, rather than just wholesale degradation without replacement of coral reefs.

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I mentioned earlier that the Caribbean fauna is very depauperate - there are very few species. There is only one tabular coral, Acropora palmata and one staghorn coral, Acropora cervicornis. I took this photograph in 1979 and at that time these two corals were the spatial dominants on this reef. In fact, the classical studies of coral reef zonation in the Caribbean describe the shallow part of the reef as the Acropora palmata zone and the deeper part as the Acropora cervicornis zone. The cover by these corals at this location today is very close to zero and as I mentioned earlier, they are now regarded as threatened species by the US EPA.

The danger with any mortality event that kills a lot of corals is that instead of corals reorganising and rebuilding a coral dominated community over subsequent years, something else might recolonise that reef and create an entirely different community. What we are seeing, particularly in the Caribbean, is a regime-shift from one set of species to a completely different set of species, and most people would make a value judgment that this is now a degraded system, as compared with the earlier one. Certainly I don't think a tourist would pay as much money to explore a seaweed dominated 'coral reef' as compared with a coral dominated reef.

In the Caribbean we are seeing a lot of degradation of coral reefs. Certainly we haven't seen that level of disruption on the Great Barrier Reef, but I think this is a warning of the sorts of things that could happen if we don't maintain our current management practices, particularly in regard to climate change.

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A question I am often asked is: are gloom-and-doom stories from overseas, primarily developing, countries relevant for 'our' Australian reefs?

The first argument is usually that overseas evidence is flawed or it doesn't apply. I don't accept that argument. It is a bit like saying, 'Well, we know that smoking causes lung cancer in Germany and it kills Canadians in Canada, but do we know that smoking kills Australians?' I think we do.

Another argument used against the relevance of overseas stories is that our fisheries are the best managed in the world. Well, perhaps they are, but many of the fisheries that we had 100 or 150 years ago are today ecologically extinct. We are dealing with marine systems that are very much altered.

Some people argue that our reefs are pristine, however, I will show you some evidence in a moment that they are not.

And people often exclaim the opinion that threats to reefs are exaggerated. I will present you some evidence and you can make up your own mind.

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Let's have a look at the health of the Great Barrier Reef. How are we doing in Australia?

The Great Barrier Reef is not pristine. We know, for instance, that run-off from land onto near-shore reefs increased substantially after about 1850, when cattle and sheep were moved into the catchment of the Great Barrier Reef. This is evidenced from coral banding studies done by my colleague Malcolm McCulloch, at the Australian National University. We also know that wild stocks of many marine species have dramatically reduced over the last 150 or so years, so stocks of many of these organisms are today very severely depleted.

For example, if we look at dugongs, we find that in the last 30 years - which is quite a short time - there has been a 98 per cent decline in the number of dugongs on the lower two-thirds of the Great Barrier Reef. That is about a thousand kilometres of coastline. We are down to 2 per cent, compared with the 1970s, and presumably the 1970s was a small fraction of the 1870s.

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Here are some data that document the accumulating damage to the Great Barrier Reef, over the past 40 years or so, from two different threats - coral bleaching and crown-of-thorns starfish outbreaks. The vertical axis shows the cumulative number of reefs that have been impacted by these two threats.

The first outbreaks of crown-of-thorns were recorded in about 1959, near Cairns, and since then there have been three major outbreaks that have so far affected about 200 reefs. To put that in perspective: depending on how you classify a 'reef', there are about a thousand reefs on the Great Barrier Reef.

If we look at the data for bleaching we see that bleaching is a much more modern phenomenon and the biggest bleaching event to date, affecting about 400 reefs on the Great Barrier Reef, was an event in about 2002. That followed just two years after the second biggest bleaching event on the Great Barrier Reef, which occurred in 1998.

Some of the reefs have been hit more than once by crown-of-thorns, or by crown-of-thorns and bleaching, but the point I want to make here is that a significant proportion of the reefs on the Great Barrier Reef have had substantial losses of corals over this 40-year period.

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Modern monitoring of the health of the Great Barrier Reef only stretches back a few years, but the first and second generation of coral reef scientists, working from the late 1950s through the '60s and '70s, gathered a lot of high quality data, and we can look at that information for a shift in the health of the Great Barrier Reef. I have tried to do that in these graphs.

These graphs are a summary of how coral cover on the Great Barrier Reef has changed when we compare the information available before 1980 and after 2000 - again we are not exactly talking the Pleistocene here, just a couple of decades. About 50 reefs were surveyed prior to 1980, and these are graphs of the frequency distribution of coral cover.

If we look at the older data we see that about half of the reef had between 41 and 50 per cent coral cover, which is a pretty healthy amount. Some had more than that and quite a few had less. But, if we look at the distribution today, we see that there has been a huge increase in the proportion of reefs that have less than 10 per cent coral cover. The average amount of coral cover, from the earlier data set to the later one, has declined by about half, which is quite significant.

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If we look at the reef today, we can certainly find lots of places that are still gorgeous. This is a picture I took near Lizard Island last year. There is very high coral cover in this picture, about 80 per cent - it's very diverse, very three-dimensional, a beautiful reef that people pay a lot of money to go to.

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This is a reef near the Keppel Islands, just a few months ago, which has undergone a regime-shift and is now dominated by fleshy algae. It is very difficult to reverse the regime-shifts once they occur. The alternative suite of species is locked in and I think most people would make the value judgment that this is a degraded reef, compared with what was there before.

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Here is another reef, intermediate between the two previous examples. This picture comes from a reef near Orpheus Island, which was quite severely damaged by the bleaching event in 1998 - about 90 per cent of the corals around Orpheus Island were killed by that bleaching event. There is a lot of bare space around here: due to the coral which was recently-killed in that bleaching event.

But we can see newly recruited corals that settled on the reef shortly after the 1998 bleaching event, so they are about five or six years old - teenage corals. This reef has managed to maintain its resilience to bleaching. An important part of that is the continued ability of larvae to come out of the water column after their planktonic phase, select the site as a good place to grow up and establish themselves on the reef. This site, this substrate, is being maintained in a suitable condition for colonisation by these corals because of the grazing activities of parrot fish and surgeonfish. I now want to look at the importance of herbivory, and fishes in general, in the response of coral reefs to climate change.

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I want to look at the management options for trying to maintain the ability of corals to cope with what is almost certainly going to be an increased frequency of coral bleaching in the future.

In particular, I am going to show you a study that looks at the consequences of loss of large fishes from coral reefs. I mentioned at the beginning, that although we can categorise threats to reefs and list them as fishing, pollution and climate change, the three threats are very intimately interrelated. I will try to explain that now. In particular, I want to look at whether overfishing reduces reef resilience to climate change.

The information I will show you is from a study which will be released at noon on Thursday [8 March].

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We undertook a fish exclusion experiment. This photograph shows the site at high tide. The tidal range here is close to four metres - quite large. We placed these cages on the reef crests, which is the zone on the reef where herbivory - grazing by fish - is at its maximum. Any time a baby algae, baby seaweed, pokes its head above the substrate on a reef crest, it is immediately removed by herbivorous fish - providing the herbivorous fish have not been removed due to overfishing.

This location is a no-take area, one of the Great Barrier Reef Marine Park's 'green zones' where fishing is prohibited, so it has an intact fish fauna, which is unusual when compared with most coral reefs around the world, where chronic overfishing - usually subsistence fishing - is ongoing.

At high tide we can census what is going on in these cages by jumping into them from a boat.

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These are the cages at low tide. Each cage has a door which allows us to get out of the cage at low tide; you can't scale them wearing a tank, because they are too tall. They are quite large, roughly the size of a squash court each.

This is a large-scale fishing experiment which we started soon after the 1998 bleaching event that killed most of the corals here.

We had three experimental treatments: full cages with doors, which excluded large fish; partial cages that controlled for any shading or impact of the structures on water flow and so on; and the third treatment was no structure at all, just open plots. The total area of this experiment was 300 square metres and over the three-year course it enclosed something like 12,000 coral colonies, which we censused individually.

We were interested in the ability of this reef to bounce back from the '98 bleaching event and how that resilience is influenced by the activities of fish.

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This movie was taken inside one of the partial cages to show you the activities of herbivorous fish. In the movie you can see a surgeonfish and a parrot fish, and you might just be able to make out a juvenile Acropora coral which has settled onto this substrate. The substrate is kept reasonably bare of algae by the grazing activities of the fish.

There is no sound track to this movie, but if there was it would sound a bit like Bugs Bunny, 'Crunch, crunch,' because of the grazing activities of these larger parrot fish. There are lots of big fish removing algae and making space for juvenile corals.

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This is an example of a parrot fish, actually an endangered parrot fish from the Caribbean.

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If you look on the substrate of any coral reef in the world where there are parrot fish present, you will see grazing marks from their jawlike 'beaks', hence the name parrot fish. (This one obviously doesn't use floss.)

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These are the scrape marks from the parrot fish. The grooves are a nice structure for recruiting tiny corals and algae is kept at bay by the feeding activities of the fish.

Slide 50
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This second movie was taken just outside one of the full cages where the fish are being excluded. I have opened the door so I can swim through it, and this is what the reef crest looked like, three years after we set up the cages. If you take away the grazers you create a forest of seaweed - this is called Sargassum. There is so much of it that I am actually having trouble moving around in the cage.

Slide 51
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Some of the Sargassum was around three metres tall, so we created Sargassum heaven, and a new science of Sargassum aquaculture, simply by excluding herbivorous fish. In the background you might be able to make out the mesh; this photograph is taken inside the cage, looking out through the mesh.

Slide 52
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We took away the mesh, just to prove that it was the fish that were responsible for keeping the algae at bay, and we had in situ cameras recording what happened next. After only two weeks the vast majority of the algae had been grazed down to a sort of stubble and after four weeks it was completely removed. So the effect was reversible, at least on the scale of this experiment.

Slide 53
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We looked at lots of different responses to this algal bloom, but I am just going to show you one - probably the most important one. This graph depicts what happened to coral recruitment - that is, the arrival of new coral into space that was damaged in 1998 by bleaching - in these three treatments.

There was no difference in recruitment into the partial cages and open plots, where herbivory was ongoing. In the full cages, where the algal bloom took place, recruitment by corals was reduced by about two-thirds compared with the other two treatments. Also, the species composition of the coral recruits inside the full cages, underneath the dense shading of the Sargassum, was a completely different assemblage of coral.

The trajectory of recovery from bleaching was completely different because of the grazing activities of these large fishes.

Slide 54
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The point I want to make is that loss of biodiversity which has accumulated through evolutionary time - generally loss through destructive human practices - is a big deal. It is important to maintain fish biodiversity, not just for maintaining fish stocks in their own right, but also from the perspective of maintaining the ecological function that various types of fish perform.

I spoke today about the critical role of herbivorous fish in the dynamics of a reef: if you exclude herbivorous fish, you get huge macroalgal blooms. The algae have a big impact on coral recruitment, which impairs the resilience of the reef when recovering from processes that kill corals, particularly coral bleaching.

Another conclusion is that managing fisheries, and also water quality, can help prevent phase-shifts from coral dominated systems to algal dominated systems, and help maintain reef resilience with future climate change. I think that is an important conclusion from this experiment because there are a lot of people out there saying that in 30 years' time coral reefs will be dead. I think that is an exaggeration. I talked earlier about the filtering effect and shifts in species composition of corals that we are already seeing. If it is true that coral reefs will all be dead in 30 years, then why would you bother? Let's go save some rainforest instead. I think that's a dangerous message.

Certainly it is very difficult to respond to a global threat like climate change and we are all familiar with the difficulties of the Australian and US governments in signing up to Kyoto. Getting global action is difficult but there are things we can do locally to maintain reef resilience - for example controlling the input of nutrients and managing local fish stocks - through to much larger-scale activities for threats like climate change.

Slide 55
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But it's all about getting the right balance. I hope I have convinced you that reefs are threatened but they are not doomed. I believe that the future condition of the Great Barrier Reef should be part of the public debate on how Australia confronts climate change. At the moment, it appears largely to be an economic debate and there is a lot of concern about the cost of a carbon tax, of building nuclear power plants and so on, but let's not forget the economic value of the goods and services provided by ecosystems. The Great Barrier Reef is worth more than $5 billion every year to the Australian economy, through tourism and fisheries. And unlike coal, which you dig up and then it's not there any more, this is a potentially ongoing source of income to Australia.

Also, let's not forget the aesthetic, social and cultural values. This debate that we are having now should not solely be about economics, although obviously that is important.

And I think we should let Keats have the last word: 'For ever wilt thou love (the Great Barrier Reef), and she be fair!'

Thanks very much.

Discussion

Question 1: One of the impacts of global warming is expected to be a change in sea-level. How will that affect the reef?

Terry Hughes: My opinion is that rises in sea-level are the least of the problems. Compared with thermal stress that can kill huge amounts of corals, an extra 30 or 50 centimetres of water on top of a reef is pretty much a sideline issue.

Another issue, I think, that is much more important than sea level rises but that I didn't mention today is changes in ocean chemistry - shifts in alkalinity. As the partial pressure of carbon dioxide rises in the atmosphere, the ocean will become less favourable for calcifying organisms like corals. Their growth may slow down and their latitudinal extent may shift or shrink, in ways that we don't fully understand.

But, to answer your question, I don't think modest shifts in sea-level will have much impact on reefs. After all, they have coped reasonably well with the 130- or 140-metre rise at the end of the last Ice Age, when the Great Barrier Reef was recolonised by corals. So I think another foot or so (in the imperial system) of water is going to be more of a problem to coastal real estate than it will be to corals.

Kurt Lambeck: It will presumably be beneficial, in fact, because it is going to give space for the corals to move up into.

Terry Hughes: That's right. Many reefs on the Great Barrier Reef are sufficiently mature now, that they have grown very close to sea-level. So they may actually get a bit more breathing space. In the scheme of things, among threats from various aspects of climate change, sea-level is not the issue.

Question 2: I have two questions. By 2050, or in 30 or 40 years [inaudible] if the reef is not there. Can you give us a picture [inaudible]? Secondly, have you presented this information to tourism associations and businesses, and what was their reaction?

Terry Hughes: Those are big questions. To tackle the first one: the big uncertainty, of course, is the extent of climate change. Depending on whether you take a conservative scenario or a very warm scenario, you get completely different trajectories. We do know that a 0.7 °C rise so far has had a detrimental impact on reefs, particularly reefs that are polluted and overfished. The 1998 bleaching event was the largest regional-scale bleaching event ever and it coincided with a strong El Niño event. The bleaching affected the Great Barrier Reef, most of the Western Pacific and almost all the Indian Ocean, and it killed roughly 12 per cent of the world's coral reefs in a single season. So that is the scale of a very large bleaching event.

The frequency of disturbances of that magnitude that could be sustained by coral reefs is largely guesswork, but we can look at recovery rates from cyclones. It generally takes about a decade or so for a reef to resemble its former self after a large amount of mortality. The big unknowns are: how warm is it going to get and how frequent will bleaching events be?

If it gets so warm that there are annual bleaching events, then we will be looking at a very, very depauperate system, with only a small subset of species being able to cope with that level of physiological stress.

More optimistically, if the warming is not as great, we may be able to see some short-term evolutionary responses. We do know that many corals have very large geographic ranges and within those ranges there is a broad spectrum of maximum summer temperatures. For example, Lord Howe Island is at the southern extremity of geographic ranges for about 110 species, and 35 of those 110 species are found in the Persian Gulf. The difference in maximum summer temperature between the Persian Gulf and Lord Howe Island is somewhere around 9 °C, but the same species have adapted to the local conditions.

That poses the question: if they can adapt locally, how quickly can they do it and how quickly can the zooxanthellae do it? And how quickly can they migrate? So in coming decades, we may see movement polewards, beyond the current southern and northern limits of coral reefs.

It is a complex issue and I have only partially answered your question but those are some of the issues.

The other question you asked me was whether we are getting this message across to the tourism industry. I think we are. Our new ARC Centre of Excellence has given us visibility through our web site and through new media capabilities that we did not have in the past. We have hired a media adviser, Julian Cribb, and in our first year of operation we had 700 media stories on issues like this. We have also had close to a million hits on our web site. So we are trying to get these messages out to as broad an audience as possible.

Question 3: My question is about the difference in biodiversity between sites here and in the Caribbean. Is this a function of overall size of the area, or are there other factors, particularly in the Indo-Pacific region?

Terry Hughes: Size is certainly a factor but it is more complicated than that. One issue for the Caribbean is that it is a relatively small, enclosed area and the corals don't have anywhere to 'hide' geographically because it is hemmed in by unfavourable habitat - the east coast of the United States and the major river systems coming out from South America.

The Indo-Pacific is a much larger place and we have more geographic refugia from climate change events and so on. But there is a lot more to the story than that.

And I only briefly alluded to the history of plate tectonics and the role that that has played in the accumulation of species in different parts of the world.

Question 4: In the Caribbean there is a history of dust storms spreading viruses carrying coral disease. I recently heard a talk about similar effects south of the Gulf of Carpentaria. Is there any evidence on the Great Barrier Reef of a similar effect from dust storms carrying disease?

Terry Hughes: Not that I am aware of. The issue of coral disease is an interesting one because it is very new. Coral reef science dates back to the 1950s and certainly by the late '60s and '70s there was a lot of research being undertaken. Coral disease is rampant in the Caribbean today; I have worked there for 30 years but in the first half of that I never saw a diseased coral. So a lot of people view coral disease as an emergent issue, which may be associated with dust storms, as you mentioned, or with climate change. It has not, however, been the cause of destruction of corals in the Caribbean because it arrived too late. It is certainly killing off remnant corals but most of the destruction of corals in the Caribbean actually pre-dates what is a relatively new phenomenon.

Question 5: You talked about water quality as having a significant impact there [inaudible]. To what distance offshore is there an impact on the Great Barrier Reef, how significant is the impact, and how important is it relative to other factors?

Terry Hughes: I mentioned water quality in the context of bottom-up effects as well as top-down effects. Basically, if you want to convert a reef from coral dominance to algal dominance, the best way to do it is to wait for something to kill the corals, then fertilise it and take away the herbivorous fish.

To answer your question: we have just had about a metre of rain in North Queensland over the last two weeks, so the Burdekin River, which you can jump over in the dry season, is now a couple of kilometres wide. When it is in flood I think it is the fourth biggest river in the world, by volume discharged. And that discharge, on the surface at least, can go out to about 40 or 50 kilometres. Perhaps Malcolm McCulloch can confirm that.

Malcolm McCulloch: Several hundred kilometres along the coast.

Terry Hughes: So it is no accident that most of the Great Barrier Reef is offshore. And if you look at Ningaloo Reef, on the west coast, which of course is fringing, you see that the corals are growing on the beach because it is a desert and there is no run-off.

Kurt Lambeck: Thank you very much, Terry, for a splendid lecture and for continuing a tradition that has developed with our lecture series here on evolution.