Wednesday, 23 April 2014

Life, Death and Rebirth of a Coral Reef: Witnessing ecosystem change over the past 42 years

1972 St. Croix -- I'm getting ready to dive into a career in marine science (but with a clipboard and a spear?)


At first light on March 18th we departed the Grenadines for St. Croix.  It’s a 370 nautical mile run that took most of three days.  The first 24 hours we had 20-knot winds on our beam and we sailed over 7 knots the entire time…. Terrific!

Approaching St. Croix from the south.
St. Croix and its coral reefs.  Our focus was on the reefs around Buck Island and on St. Croix's northeast shore.
Logistics dictated that St. Croix (U.S. Virgin Islands) would be the last research site of the Antilles Expedition.  Ironically, it happened to also be the place where I was first introduced to coral reefs as an undergraduate student in 1972.

Students at West Indies Laboratory 1972 - I'm reclining shirtlessly


The coral reefs surrounding the east half of St. Croix including Buck Island are among the best developed of the eastern Caribbean.  The Tague Bay Reef along the northeast shore reef runs nearly 6 kilometers without a break.  It is also one of the best-studied coral reefs in the Caribbean.  My first job after I graduated from college in 1973 was to assist Dr. Walter Adey of the Smithsonian Institution in drilling through St. Croix’s coral reefs and algal ridges to determine how thick they are and how long they took to develop that thickness.  What we learned was that these reefs are 30’ (10 m) thick and they developed mostly over the past 7,000 to 10,000 years.  Reefs were mostly built by the remarkably large branching elkhorn coral (Acropora palmata).  So, this is a wonderful site to study because we know it was a great place for coral reefs to grow for millennia (the same cannot be said for some of the rocky reefs we studied in places like St. Maarten and St. Lucia).
Studying the algal ridges at Isaacs Bay 1973
For younger reef scientists, it is hard to imagine the structure of coral reefs of the 1970s.  The shallow reefs were an expansive tangle of complexly branched elkhorn coral that went on for miles and miles.  The reef fish used the branching habitat for the food and myriad “hidey holes” it provided.

Buck Island elkhorn coral reef in 1973. In the center of the photo lurks a large barracuda
On a few occasions I would get my Nikonos I camera with only enough film to take 36 black and white photos of the coral reef.  I would often photograph large predators such as barracuda, groupers and large snappers. 
Tiger grouper on Tague Bay reef 1973
Everything made sense.  I was taught as a student that highly complex ecosystems such as coral reefs were highly stable.  Scientists of the 1970s published articles speculating that the only thing that could change this coral-dominated state would be another Ice Age over the next 10,000 years.  This was the widely held consensus among most coral reef scientists at the time.  As the famous coral reef scientist, Jeremy Jackson, has frequently pointed out – most of the world’s best coral reef scientists were using the best scientific methods available at the time but none predicted the widespread collapse that we have observed in recent decades.

Speaking for myself, I was studying the St. Croix’s coral reefs for my PhD dissertation (with Jeremy Jackson as my advisor).  I set up experiments on the Tague Bay fore reef in 1979 and continued to follow the dynamics of change there until 1995 (so this included period after I was hired by the University of Maine in 1982).  Over that short period of a decade, I saw the coral reefs of St. Croix collapse into an unrecognizable wasteland.

My 2 and 5 meter sites on Tague Bay forereef collapsed from 1980 to 1990
The 1980s was the disastrous decade for Caribbean coral reefs.  Two diseases hit about the same time but the rate of their impacts were very different.  Chronologically, the first disease was the White Band disease that infected the elkhorn and staghorn corals beginning in the late 1970s.  It was easy to spot.  It attacked the elkhorn and staghorn corals at the base and progressed slowly upward.  The lethal white band spread considerably faster than these corals can grow.  It created a wave of death visible from low flying airplanes. Bill Gladfelter, a scientist working at St. Croix’s West Indies Lab, published a paper in 1982 showing the elkhorn coral mortality and suggesting that if this disease continued, it could eliminate the dominant coral of Caribbean reefs.  His paper was largely ignored until late in the 1990s when it dawned on reef scientists that he was right.  The elkhorn and staghorn corals had died throughout most of the Caribbean.
The black-spined sea urchin Diadema and its well grazed reef.
The second disease attacked the black-spined sea urchin “Diadema” (Diadema antillarum).  This sea urchin had attained remarkable population densities throughout the Caribbean.  In St. Croix on the Tague Bay reef I was studying, we documented over 17 per square meter at my 15’ (5m) site.   So, imagine your desk is about 3’ by 3’ or one square meter.  Now imagine that desk with over 17 large sea urchins with long spines packed with poison.  Until 1983 these were the bane of most coral reef scientist’s existence.  Most scientists and tourists at the time had close encounters of the most unfortunate kind.  Although these urchins hurt, scientists such as Bob Carpenter, Paul Sammarco and John Ogden were conducting experiments to see how they functioned in coral reefs.   All the studies pointed out that Diadema keeps coral reefs and the surrounding areas ‘mowed’ down so no seaweed was present on most Diadema dominated coral reefs.  Studies of experimental removal of all the Diadema showed a very rapid shift to harmful seaweed.

My experiment (coral settlement plates) at 5 m in 1980 with Diadema nestled around the base of the corals.
Suddenly everything changed.  Starting in 1983 and progressing to 1984, Diadema suffered a mass mortality from a disease.  The disease began in Panama so speculation is high that a pathogen from the eastern Pacific caused this outbreak but to this date we simply do not know how the disease started or where it came from.  Nevertheless, what we do know is that the early experiments showing how important this sea urchin is as an herbivore was absolutely correct.  Within a month of the sea urchin disease outbreak, coral reefs throughout the Caribbean were overgrown by seaweeds.  The earlier sea urchin removal experiments were spot-on.  This was an important grazer that kept the coral reefs of the 1970s healthy and free of seaweed.

Because Diadema was so abundant and when the disease hit a reef all of the urchins died in a day or two, there was no mistake that a serious epidemic had struck the Caribbean coral reefs.   The slowly creeping White Band Disease (WBD) was often conflated with the effect of the Diadema mass-mortality (I published a paper in 1994 pointing out the impact of herbivore loss without mentioning that the coral decline was likely from WBD).

The combined effects of herbivore loss and increase in area where seaweed can grow (due to WBD of the dominant coral) effectively diluted the grazing pressure from the remaining herbivorous reef fish such as parrotfish.  With such low levels of herbivory the coral reef “flipped” into becoming a seaweed reef.

By the end of the 1980s none of the reef scientists were saying complex and diverse coral reefs were stable.  What we had all witnessed was one of the World’s most rapid and widespread collapse of a complex ecosystems.


As I’ve been studying reefs of the eastern Caribbean, I’ve come to recognize the alternative state of coral reefs is one dominated by seaweed.  It is an alternative state from which it is difficult to recover.   Based on all of my surveys at 30’ (10m) depth from this expedition, the abundance of seaweed still exceeds the abundance of coral.  Arguably, these should no longer be called “coral reefs” and since it has been 30 years since coral-dominated reefs became seaweed-dominated reefs, this could now be considered an “alternative stable state”.

Returning to St. Croix for perhaps the last time in my professional career had me thinking that this was going to be just another example of a fully collapsed coral reef ecosystem.  The only reason it was worth studying is that I was revisiting the exact same reef sites using the same methods over the decades before, during and after reef collapse.


We revisited the exact area of the Tague Bay reef where I conducted my PhD research starting in 1978.  That was before we had “global positioning systems” (GPS) so I had used distinct houses on the shore to line up my study sites.  Remarkably, they were still there so I was on my old study site!

Swimming up the reef from 30’ depth, the reef hadn’t changed much but then I started to see Diadema and coral.  At 5 and 2 m (15 and 6’) it was clear that the grazing Diadema were back, seaweed was relatively rare, coral was more abundant (so were the baby corals).  To me, it seemed I was witnessing a rebirth of a coral reef.

Trends in abundance of corals, diadema and seaweed from 1980 to 2014 at 2, 5 and 10 m (6, 15 and 30 feet).  Note that the trends are positive at shallow two depths.
Make no mistake, the reef had a long way to go.  While there was some elkhorn coral scattered about, it was nothing like the elkhorn that was here in 1980.  But all of the shallow water trends were positive!

Tague Bay forereef at 5 m (15')  1980.
Tague Bay forereef at 5 m 2014 (same site as the photo above from 1980)

Nevertheless, seeing large proud elkhorn coral at my 2 m site and also seeing lots of baby elkhorn coral indicated to me that the real reef builder could be coming back

Tague Bay forereef at 2 m 1980 - 1988.  No elkhorn coral was alive in 1988.

Tague Bay forereef at 2 m 2014 (same place as above) with numerous live elkhorn coral!
We then travelled to Buck Island National Monument.  This is now a no-take reserve where fishing is illegal (they started enforcing the no-take regulation around 2003).  While some of the coral I had seen in 2003 had died, in the shallow zone, was the most extensive stand of elkhorn coral I’ve seen in the last 30 years.

An elkhorn coral reef on the southern bank barrier reef on St. Croix's Buck Island.   This is the densest stand of elkhorn coral that I've seen anywhere in the Caribbean in over 30 years!

Elkhorn coral is among the fastest growing corals in the Caribbean.  At this Buck Island site, I had placed coral settlement plates for Park scientists to study but that hadn’t happened.  So, the plates were still there.  It was a great opportunity for me to see what had happened to them in the past 12 years.  Some large corals had overgrown the settlement plates.  Baby corals that had attached to them were now adult corals.   It is amazing what you can learn from accidentally leaving an experiment for more than a decade!

Terracotta coral settlement plates I deployed in 2002 (left) and how corals have grown on and over them in the past 12 years

 However, the biggest surprise was coming upon a plate that was completely enveloped by the base of an elkhorn coral.  The coral had grown 60 cm and and across 1 m (24”, 39”, respectively).  That’s an impressive amount of growth.  As I looked around and saw how many baby elkhorn coral I could see, I thought I was in fact seeing the rebirth of a coral reef!

Elhorn coral growing over a terracotta settlement plate (plate is 10 cm or 4").

Elkhorn coral that grew up and over a coral settlement plate (coral is 60 cm high and 100 cm wide or 24" and 39")

THE RETURN OF THE KING!  ..... maybe?

The biggest source of despair among Caribbean coral reef scientists has been the loss of elkhorn coral because it has produced far more coral reef rock than all other species of coral combined.  It grows fastest, it has the capacity to produce coral reefs best able to keep up with rapidly rising sealevel (which is predicted to occur in the next century).  So, the ample evidence that elkhorn corals are proliferating here in St. Croix is great news and offers renewed optimism for the future of Caribbean coral reefs.

I sure hope an assessment of these coral reefs 40 years from now is as positive as this entry.

Sunday, 23 March 2014

Coral reef oases in the eastern Caribbean

Alaria at Tobago Cays Marine Park
Coral reef at Tobago Cays Marine Park

After Mustique, we sailed south to the drop-dead gorgeous Tobago Cays Marine Park (“TCMP”).  There, the Park Rangers took us to reefs they have been monitoring for some time. We spent a week there before we sailed on to Union Island from which we traveled to Petite St. Vincent again courtesy of the TCMP Rangers and their fast boats.  Finally, we sailed to Carriacou in the country of Grenada.  This was our most southern station where we surveyed the island’s reefs along its windward east coast and south coast.  So after over 170 coral transects and nearly 500 fish transects we had surveyed most of the coral reefs we had targeted in the eastern Caribbean.  Now, we can consider what, if any, patterns we’ve found.

The Grenadines with the most extensive coral reefs (right inset)
Fig. of eastern Caribbean Islands including Grenadines


Living coral comprised less than 20% of the hard surfaces we surveyed from Anguilla to Carriacou.  This is a low number but it is comparable with most coral reefs of the Caribbean today.  Nevertheless, three regions -- St. Lucia, Mustique and Tobago Cays -- had higher than average coral cover and a higher than average abundance of baby corals.   Similarly, two of those three regions had lower than average abundance of harmful seaweed.  Grazing fish such as parrotfish and surgeonfish were most abundant at Mustique but they were either average of above average at those three regions.  The most prized reef fishes to eat are groupers and they were most abundant at both Mustique and Tobago Cays.

The relatively healthy reef at Mustique
Relatively healthy reef at Tobago Cays Marine Park
In short, it appears that all of the reefs with better than average conditions for coral reef health (abundant coral, baby corals, little seaweed, many and grazers and relatively abundant predators) were all found in no fishing “marine reserves” with effective enforcement.  In the larger view this included St. Maarten, St. Lucia (Soufriere Marine Management Area), Mustique and Tobago Cays Marine Park.

Average coral, seaweed and baby coral abundance.  The blue horizontal line represents the Antilles average.  Note that St. Maarten, St. Lucia, Mustique and Tabago Cays have enforced marine protected areas.

There are, of course caveats to the pattern that reefs with less fishing are “healthier”.  For example, it is possible that areas with high coral cover were targeted for protection.  That certainly happened in St. Lucia and possibly Tobago Cays Marine Park.  However, Mustique’s protection was established with little specific knowledge of what coral reefs existed there.

Specific reefs within managed sites vary greatly.  Sometimes this is due to natural variability found in any ecosystem.  However, in some places we think we see some patterns that may have caused the local variations.  To address why adjacent reefs differ, we targeted a few sites for more detailed studies with some more expertise.


For help on why reef fishes and seaweed abundances vary so much among local coral reefs Dr. Peter Mumby (University of Queensland) and Ms. Natalia Rincón Díaz (Universidad Nacional de Colombia) joined our team.  Both of these scientists will spend a month working on these problems from Alaria. 

Dr. Pete Mumby (reef fish ecologist) sailing to our study site on Alaria.

Natalia Rincon Diaz (a seaweed expert) joins our group.
In the way of introductions, Dr. Peter Mumby is an Australia Research Council, Laureate Fellow and heads the University of Queensland’s Marine Spatial Ecology Lab.  He is the President of the Australian Coral Reef Society but most of his research over the past few decades has been on coral reefs of the Caribbean.  He is one of the world’s leading experts on the ecology of coral reef fishes (Google him if you are curious).   Natalia is a masters student at her university who is studying the relationship between herbivorous fishes and the algae they eat.  I saw this a great opportunity to help advance her career while helping us with our studies.  She will have full access to all of our data to help her in her masters thesis research.

Science discussions intensify during our sunset chats.

While it is great that there are areas with higher than average coral cover and fish abundance, it is also interesting to consider why another reef nearby is different.  We suspect there are two big factors affecting reefs.  One is one is the variability of reef structure (that is, its habitat architecture), the other is how fishing pressure changes from place to place.  These are by no means the only factors causing the variability we observed but we think they may be factors contributing to the differences.

Corals create the architecture of reefs.  This includes those corals alive today and the skeletons of corals past.  This architecture may take centuries to develop but it provides places for fish and other critters to live or to hide.  The habitat architecture of reefs increases the surface area on which seaweed can grow and herbivores such as parrotfish can graze.  So, we wondered if differences in habitat architecture may explain the differences we see among adjacent and nearby coral reefs.

A simple and relatively featureless reef in Barbuda.
A complex elkhorn coral reef at Tobago Cays Marine Park.
To examine these questions in greater depth we set out to measure habitat architecture by measuring the length of coral structure under each meter along a 10 meter transect.  With our measurements we learn how high and how dense the coral structures thrust into the overlying water.  We get a sense of how much reef surface area there is in any given space.

Bob measuring spatial complexity of the coral reef (photo Pete Mumby).

We also measure how the topography of the reef is being used by grazing fishes.  We watch for 5 minute periods and via small video cameras, the bite rates on the reef by parrotfishes and tangs.   As the surface area of reefs increase, so to does the area on which seaweed can grow. So it may be necessary in high complexity areas for more parrotfishes grazing just to keep the reef clean of harmful seaweed.

Natalia quantifying the rate at which herbivorous parrotfish and tangs bite tops, sides and bottoms of complex reef surfaces.
Because it is also possible that fish behave differently on these reefs, Peter Mumby documented the grazing behavior of the dominant parrotfish including juveniles and adults.  We also deploy video cameras to film fish grazing at sites that range from high to low complexity

Pete quantifying bite rates for different size and species of grazing parrotfish.
One of several compact GoPro video cameras quantifying fish grazing without a human presence.
We will need to considerable analyses beyond what I’ve presented here.  However, we are beginning to see patterns that make sense.  This is also information that reef managers will want to know.  In a future blog I’ll describe how we have been meeting with managers at each of the islands we are studying.  All of them are eager to hear what we have learned.

The beauty of coral reefs today.  All these photos happen to be from reef protected areas.

Elhorn coral in TCMP

Neon gobies on a star coral.
Sponges in the Soufriere Marine Management Area

A green moray in Mustique's Lagoon reef.

Wednesday, 19 February 2014

The Grenadine archipelago: Bequia and Mustique a study of contrasts

Alaria sailing to Bequia
Rain squalls over St. Vincent
With a brisk wind across our beam, Alaria sailed due south past the verdant mountainous island of St. Vincent to the small island of Bequia over 50 miles south of St. Lucia.  We had all of our sails up so we travelled much faster than we could with the engine.  There is something extremely satisfying sailing to your next study area powered entirely by the Trade Winds!

Alaria under full sail arriving at Bequia
Islands of Bequia and Mustique showing our survey sites
Port Elizabeth is Bequia’s major port and it is where we cleared customs to enter the country of St. Vincent and the Grenadines (actually only the northern Grenadines since the southern Grenadines are the country of Grenada).  Port Elizabeth’s Admiralty Bay has both anchorages and moorings.  We decided to anchor to keep costs down but it was a lovely spot where we watched the sun set into the sea each night.

It is obvious after just walking around for a Bequia for a little while that it is a very friendly place.  When I first went ashore to clear customs, I asked a fellow where the customs house was and he insisted on walking me to the building.  The small town of Port Elizabeth has a ‘light’ feel to it.  It is not crowded, there are enough tourists to keep shops and eateries going.  The open air market is well stocked with nice local produce.

Bequia's Port Elizabeth
In Bequia, we arranged to see Mr. Herman Belmar who is Deputy Director of Grenadines Affairs.  He was eager to have us survey the reefs in the region and especially the Tobago Cays Marine Park.  We went over the charts considering where we could work and where we can anchor.  It was clear he knew the waters around Bequia like the back of his hand.  He knew where reefs were best developed and where fishing pressure will likely be highest.  He also called over to the island of Mustique to arrange for us to work there after a bit.

Mr. Herman Balmar pointing out keep coral reefs in the Grenadines
The Grenadines are really different from anything we’ve experienced so far.  It is an archipelago of small to tiny islands that stretch about 50 miles from St. Vincent to Grenada.  Bequia is one of the larger islands but it is only a bit over 5 miles long. 

The people of Bequia have a tradition of building boats, fishing and whaling.  They have a permit from the International Whaling Commission to take up to four whales a year but often they don’t get one.  They use traditional methods.  They sail to the whale, harpoon it with a hand-thrown harpoon and then float it to a small whaling station on a tiny island off the east coast of Bequia for processing.

Bequia's whaling station
Fishing is important in Bequia.  We saw lots of folks fishing both the inshore reefs and going offshore to catch some of the larger pelagic fish such as wahoo, mahi mahi, Spanish mackerel and small tuna.  Those are the fish I saw landed at the dock.  Pelagic fish are the best choice of fish to eat because they can be fished sustainably.  Unlike reef fish these pelagic fish grow rapidly, they reproduce early and often, and they are abundant. 

Bequia's colorful fleet of fishing boats
Nice catch of fish being filleted. 
Only some fishermen can venture offshore for the larger pelagic fish.  Many people fish with spears, traps and nets the inshore reefs.  Gillnets are particularly destructive because they drape over reefs for considerable distances.  Fish try to swim through the net but their gills get caught. Chancey happened upon one such gillnet as he did his fish surveys.  He photographed lots of large parrotfish caught and dead in the nets.  These nets fish for as long as they are deployed.  If they are left too long the caught fish will rot and not be suitable to sell or eat.   Because there is not much of a market for parrotfish in Bequia,  many (or most) are discarded dead.  The site where the gillnet below was deployed had lower than average parrotfish abundance on the reef according to our fish surveys.

Gillnet strung across a coral reef (photo Chancey Macdonald)
Dead parrotfish caught in the gillnet (photo Chancey Macdonald)
Bequia’s coral reefs are modest in extent (to be generous).  Chancey and I dived on two widely separated of reefs on opposite shores of Admiralty Bay (Port Elizabeth) and then we took Alaria around to Friendship on the eastern side of the island.  There the Trade Winds blow incessantly. We anchored in a corner of Friendship cove but had to set the stern anchor to minimize our roll from a constant swell.

Alaria at anchor in Friendship Bay. 
Because we were on Bequia’s exposed coast, wave action was high on the reef we wanted to study.  So we had to take particular care on how we anchored the inflatable boat, just out of the breaking waves, and we checked the anchor at the start and end of our dive.

This was a high-energy reef so conditions were ideal for seaweed growth.  Normally we wouldn’t see much seaweed because parrotfish and other grazers would keep it mowed down.  However, this is a heavily fished reef according Mr. Balmar and grazing fish densities were low and seaweed was luxuriant.

Fishermen of Friendship Bay
Seaweed dominated reef at Friendship Bay
Overall, Bequia’s reefs were about average for the region.  Areas like Friendship that are heavily fished and where conditions for seaweed growth is good, there is a carpet of seaweed that limits baby corals so the reef is likely to remain degraded for some time.

We had learned from Mr. Balmar, that the reefs around the neighboring island of Mustique are protected from fishing and they are patrolled regularly by Mustique’s security force.  We knew we had to sail over to see if reefs were in fact different there.

Alaria viewed from the groomed shoreline of  Mustique Harbor 
Mustique is unlike any island I’ve visited.  It is a private island owned and operated by the Mustique Company.  It has a board of directors (including folks like Mick Jagger, who is also part of the environmental committee); it is where Britain’s royal family goes when they want a break from the winter chill.  The week before we arrived the Duchess of Cornwall (Kate Middleton) and her baby had been on the island for the baby’s first overseas trip.  The head of security told me in jest that “no photos were taken of them, so I get to keep my job”.

The tiny island of Mustique (only 2.5 miles long) has by far the highest per capita income of any island in the region.  Its economy comprises one quarter of the gross domestic product of the country of St. Vincent and the Grenadines!  When a powerful Christmas Eve rainstorm flooded St. Vincent (as it did in St. Lucia while I was there), Mustique donated a million dollars for the big island’s restoration.

We met with Mr. Simon Humphrey who holds several important positions within the Company but importantly he is the island’s Conservation Officer.  He has a broad view of what is happening on land and in the sea.  He worries about how the island runoff may affect the reefs.  The island has banned pesticides and landscaping looks to minimize erosion. The reefs are all currently protected from fishing.  He also wants to see the protection of the island’s coastal zone extended one kilometer offshore (he knows that will be hard but he’d love to see that happen).

Mr. Simon Humphrey explains the conservation challenges of Mustique
Mr. Humphrey arranged for us to dive from the island’s security force boat while Brian, the dive manager, was busy.  Afterwards, we dived with Brian and the dive team.  On our first dive we saw the value of Mustique’s protected area.  Parrotfish and grouper abundance (biomass) were an order of magnitude higher than the average for Bequia and the entire eastern Caribbean. 

A school of striped parrotfish swim over Mustique's coral reef

Pillar coral and fish along my transect line on a Mustique coral reef. 
We spent the week diving other sites and none quite matched up to our first dive but the average for Mustique.  However, coral cover, juvenile coral abundance, parrotfish and carnivorous fish abundance were all well above average for the region and for the eastern Caribbean.  We intend to return to Mustique to follow up a bit on what might be driving coral reefs around this island.  However, the bigger picture that is emerging is that the socio-economic status of the local area creates the need to fish the coral reefs.  Arguably, Mustique can afford to be conservative but Bequia may not.

The value of coral reefs, as with any commodity, is what the market can bear.  There are some dive operations in Bequia but there are many more fishers so the incentive to conserve the coral reefs is low.  However, truly unique and expansive coral reefs exist around Tobago Cays and there they have the Tobago Cays Marine Park, a fully protected ecotourist magnet.  There we can study reefs where the overwhelming value comes from having healthy and abundant reef fish as opposed to those sold in fish markets.

Chancey looking from Bequia to neighboring islands of the Grenadines