Tilting the three-way tango - disease as a loss of diversity

Disease is a funny old thing.  We're taught from very early on that disease agents are "bad" and that, by contrast, the infected are somehow poor and unfortunate victims of nasty evil bugs.  This is clearly a cultural bias, wherein we project our own concerns about getting sick onto all other animals; there's no real reason to think that a bacterium or virus has any less right to be here or any less important role in the ecological processes of the world than does the dolphin it infects, or the fish or the lobster.  We have all survived eons while avoiding extinction, which makes us winners in the great game of evolution, the microbes every bit as much (or more) than their hosts.

Still, biases run deep.  This is important because sometimes they cloud our perceptions of whats really going on.  Consider coral diseases for a moment.  What, you didn't know that coals get diseases?  That's OK, neither did most folks, including many scientists, until fairly recently.  Lets picture a nice reef coral, maybe a handsome Porites, infected with one of the many "band"-causing agents (diseases that march across the surface of the coral, destroying tissue along a coloured front that gives the disease its name).  Most folks would perceive that the coral (good) was quietly minding its own business when it was "infected" by the microbe (bad), causing disease.  But actually it took at least three players to tango in this case; the coral had to be susceptible to the pathogen, the pathogen had to be infectious to the coral, and the environment had to set the scene that made the interaction swing in favour of the pathogen.  This simple "disease triad" is the most basic model of how infectious processes take place, but its just that: a basic model.

These days, disease studies are becoming a lot more nuanced, and its revealing a whole new world of how diseases start and stop.  Rocco Cipriano, a microbiologist colleague of mine at the National Fish Health Labs in Leetown WV, has been promoting a model lately where an infectious disease of fish (furunculosis) is caused by a disruption to the natural community of bacteria on the skin of fish; a community in which pathogens have no place normally.  The furunculosis agent (Aeromonas) is excluded from these communities by bacteria better adapted to living in normal fish skin and its associated mucus layer.  That is, until an environmental modulator, like a temperature spike or pollutant, shakes things up a bit; what ecologists would call disturbance.  And what is the first outcome of disturbance in most systems? Loss of diversity, in this case among the normal bacterial community.  Some bacteria disappear from the skin of the fish, freeing up resources (space, food) that are exploited by other bacteria - opportunists that can come in and pounce on the new space or food.  When that space and food consists of the fish itself, we call those bacteria pathogens.  This same process happens after any ecological disturbance, like a hurricane on a reef or a tree falling in a rainforest: opportunists come in and pounce on a newly-available resource; then as things settle down a succession takes place, until the early colonisers are displaced by more typical fauna.  In this view, disease is nothing more than a byproduct of disturbance and loss of diversity in the normal microbial community.

Which brings me back to corals and to the recent paper by Mao-Jones and colleagues in PLoS Biology.  These folks used a mathematical model to show that much the same holds true for the diseases of corals, which, like fish, rely heavily on a surface layer of mucus as their first line of defence.  It seems that in both corals and fish, the mucus is important, but even more important are the normal bacteria that live there, continually excluding pathogens and acting as a protective guard against disease.  In a very anthropomorphic sense, the corals (and fish) are using the surface bacteria as a biological weapon against the potential pathogens, at the expense of having to produce all that mucus for the bacteria to live and feed on.  Importantly, Mao-Jones and friends show us that the derangement of the mucus community can persist for a really long time after the initial disturbance.  This is important, because you often come along and see disease starting, but you may well have missed the initial insult that got the ball rolling, which may have occurred some time ago.

I really like this idea of infectious disease as an ecological disturbance and of many pathogens as simply early colonisers in the succession back towards health (or towards death, if the disturbance was too severe).  As a model, it doesn't work for everything, though.  There are many "primary pathogens" that are specifically adapted to invade healthy animals, but its not in the best interests of those organisms to invest so much energy in adaptations to invasion, only to kill the host, thus many of those are fairly benign.  For more "opportunistic" agents, however, I suspect it holds true much of the time, and that group includes many or most of the really virulent diseases.  I dare say many of the "emerging" diseases fall in this category, and we can expect to see more of this as the global climate continues to tilt the tango in favour of the pathogens.

Mao-Jones, J., Ritchie, K., Jones, L., & Ellner, S. (2010). How Microbial Community Composition Regulates Coral Disease Development PLoS Biology, 8 (3) DOI: 10.1371/journal.pbio.1000345

Q: When is a ship like a tree?

A: When you can't see the forest for it.

You may have followed some press in the last week or so about a Chinese coal ship, Shen Neng 1, that ran aground on the Great Barrier Reef and spilled some of its fuel oil.  This has caused a regular frenzy in the Aussie media and the global conservation and environmental news-o-sphere.  There have been all sorts of calls for prosecution of the shipping company and new stringent regulations for the transport industry and so on, along with dramatic accounts of the damage the ship did and the risky salvage operation that came next.  But you know what?  I am not worried in the slightest about this incident.  Not that its a good thing - far from it - but this accident is nothing more than a tree, obscuring us from seeing one big and scary forest.

The main reasons I am not especially bothered by the Shen Neng accident are that (1) it affected a very limited area - the G.B.R. is really B.I.G. and one ship can only damage so much of it; and (2) it was a single event in time - this was not a process or an ongoing problem, but a singular disturbance.  Science shows us that the GBR, and reefs in general, are amazingly resilient to violent disturbances like this; a decent cyclone can literally turn a reef upside down, and a couple of years later you'd never know the difference.  Indeed, periodic disturbances may  be really important for maintaining a healthy reef ecosystem.

No, the Shen Neng is just a tree, obscuring us from seeing the forest that really threatens the future of the GBR and all reefs.  Its not the 2km gash that the hull cut in the reef, nor is it the tons of fuel oil leaked into the water; it's the very concept of burning that fuel oil, and burning the thousands of tons of coal that the Shen Neng 1 was carrying.  When you consider all the other ships and all the coal and fuel they were carrying that day and every day, and all the cars in the world, the power plants and so on ... ach, you get my point.  THAT'S what we ought to be worried about, because both of the main effects of increased atmospheric CO2 - warming and ocean acidification - will likely result in unrecoverable damage to All reefs. Everywhere. In our lifetime.  Warming is directly linked to lethal bleaching events, while acidification disrupts the ability of reefs to lay down their skeleton and grow.   Oh yeah, and lets not forget the drowning effects of sea level rise, too.  The more I think about it, the more it seems that jumping up and down about the Shen Neng is hypocritical (coal is one of Australia's biggest exports, after all) and akin to complaining about the deck chair arrangements of another, even bigger, ill-fated ship.  (Ironically, if Titanic sailed today, she probably wouldn't have to worry about icebergs...)

Of course, its a false dichotomy, we should be worried about BOTH the Shen Nengs of the world AND the global climate change/ocean acidification.  But I only have so much energy/capacity for worrying about these things, so with a limited anxiety budget, I feel compelled to focus on the bigger issue and what (if anything) we can do about it - to try to reduce consumption and to try to make sensible decisions that are mindful of how much energy is involved and what the broader impacts might be.

In other words, to worry about the forests - and let the trees take care of themselves.

Field locations you have loved

In this thread I want to hear about field locations YOU have loved, and WHY.  Here's a couple of mine to get the ball rolling:

Kedron Brook, Brisbane, Australia.  A choked little stretch of suburban creek on the north east side of Brisbane Australia was a key field location for my PhD research, which was all about introduced (exotic) species and their parasites in rivers and streams in Australia.  At one point just above the tidal influence - stylishly named KB216 for its map reference - this creek is basically completely exotic: plants, invertebrates, fish, the whole shebang.  There aren't many parasites there, but those that were present were introduced hitchhikers.  Not sexy, but a veritable Shangri-La for a student on the hunt for ferals...

Heron Island, Queensland, Australia.  Where I met and fell in love with marine biology.  A patch of sand and guano-reeking Pisonia forest 800m long, on a reef 10 times that size, crawling with noddies, shearwaters, turtles, grad students and squinting daytrippers or more wealthy sunburned resort guests.  Too many firsts for me there to even list (but no, not that one - get your mind out of the gutter!).  Absolute heaven, hands-down.  How do I get back?

Throgs Neck, NY, USA.  You generally wouldn't think of the junction of Queens and the Bronx as a biologically interesting in any way (except maybe on the subway), but actually the western part of Long Island Sound was the epicenter of a lobster holocaust that started in (well, before, if you ask me) 1999.  When we were out on the RV Seawolf, the Throgs Neck bridge marked your entry into the East River and the start of one of the most unique and strangely beautiful urban research cruises around, right down the East side of Manhattan, past the Statue of Liberty and out into the Lower NY bays.  We would pass through on our way to do winter flounder spawning surveys off the beach at Coney Island (its that or go around Montauk).  Proof that not all interesting biology takes place in Peruvian rainforests...

In the comments, tell us about a field location YOU have loved and why.  Post links if you can find them.

When can we stop sampling and have a beer?

Yesterday I got a very kind email from a fellow scientist, Eric Seabloom at Oregon State University, letting me know that a paper I wrote with my PhD advisor Tom Cribb (University of Queensland) a few years ago had influenced a recent publication of his.  My paper was about one of those patterns in nature that just seem to be universal.  They're called species accumulation curves and, at the heart of it, they represent the "law of diminishing returns"* as it applies to sampling animals in nature. Basically, they show that when you first start looking for animals - maybe in a net, a trap or a quadrat - pretty much everything you find is new to you, but as you go along, you find fewer and fewer new species, until eventually you don't find any more new species.  Simple, maybe even obvious, right?  Well it turns out that that simple observation has embedded within it all sorts of useful information about the way animal diversity is spread around, and even about how animals interact with each other in nature.  Consider the figure on the above right, which represents two sets of 5 samples (the tall boxes), containing different animal species (the smaller coloured boxes).  The first thing to note is that both set (a) and set (b) consist of 5 samples, and both have a total diversity of 5 species (i.e. 5 different colours).  In set (a), all the diversity is present in every sample, but in set (b) there's only one species per sample, so you have to look at all 5 samples before you find all 5 species.  If you were to plot a graph of these findings, you'd get very different species accumulation curves; they would both end at 5 species, but they would be shaped differently.  They'd look much like what you see below:

 Set (a) would be more like the curve on the left (in fact, it would be a perfect right angle), while set (b) would be more like the curve on the right (in fact, it would be a straight diagonal line).  You can see some other properties on the two types of curves above also, for the more ecologically inclined, but the gist is, the shape of the curves means something about the communities they describe.

Tom and I wrote our paper after many nights in the field spent dissecting coral reef fishes to recover new species of parasitic worms - a time consuming and sometimes tedious process (sometimes thrilling too, depending on what you do or don't find).  We were often motivated by another far more important factor too - when can we stop all this bloody sampling so that we can go and have a beer on the beach?!?   Species accumulation curves therefore have a very practical aspect to them - they tell you when its OK to stop sampling because you've either sampled all the available species, OR, you've sampled enough to extrapolate a good estimate of how many species there might be.

Back to Eric Seabloom.  He and his colleagues wrote a paper about the diversity of aphid-borne viruses infecting grasses of the US Pacific northwest and Canada.  While the environment that they sampled was about as far away as its possible to be from the coral reefs that Tom and I looked at, the patterns of saturated and unsaturated communities they observed were the same. I get a huge buzz out of that, and that out of the morass of published science out there, Dr. Seabloom found a scientific kindred spirit who had had the same thoughts and ideas about nature, however different the specific areas of study.  While Tom and I sipped beers on the beach and watched the sunset over the reef, I wonder if Eric and his colleagues blew the froth off a few while they watched the wind waves spread across the grasslands.  There's something so unifying about science; it can give you common ground with someone you never would have otherwise known, and that's just one reason why I love it so much.

*The tendency for a continuing application of effort or skill toward a particular project or goal to decline in effectiveness after a certain level of result has been achieved. Answers.com 

DOVE, A., & CRIBB, T. (2006). Species accumulation curves and their applications in parasite ecology Trends in Parasitology, 22 (12), 568-574 DOI: 10.1016/j.pt.2006.09.008

ERIC W. SEABLOOM, ELIZABETH T. BORER, CHARLES E. MITCHELL, & ALISON G. POWER (2010). Viral diversity and prevalence gradients in North American Pacific Coast grasslands Ecology, 91 (3), 721-732 (doi:10.1890/08-2170.1)

Lionfish - more spectacular than your average invasive, but still a right pest.

When we think of invasive species, flamboyant fish from coral reefs are not usually the first thing that comes to mind.  Indeed, if you put together a list of characteristics of successful invasive species (like this one), "boring" would probably be close to the top, along with being quick to reproduce, not fussy about what you eat, having a large natural range, a great tolerance for extremes in the environment, and lacking natural enemies such as predators or parasites.  Think of some of the most successful invaders and decide for yourself if these predictions hold true: carp, starlings, mosquitofish, rats, sparrows, mice, rabbits, dogs, cane toads, cats, foxes, kudzu, chickweed... 

All this makes the invasion of the Atlantic seaboard by the Pacific lionfish, Pterois volitans, all the more remarkable.  Lionfish are flat-out spectacular!  Long prized as an aquarium specimen, they have bold stripes that spill over onto their fantastically long and showy fins; their scientific name even means "fluttering wings".  The sheer beauty of lionfish doubtless plays a role in how they came to invade the Atlantic in the first place; most likely they were an escaped or released aquarium species that found itself able to survive quite nicely in the conditions of the coastal Atlantic.  The beauty of lionfish conceals a dangerous secret - venomous spines on their dorsal (back) and pelvic (bottom) fins.  While they won't kill a person; they cause excruciating pain.  I've never been stung by one, but I have been stung by related scorpionfish (most recently the short-spined wasp fish) and the feeling is not one I'd care to go through again!

Over the course of just a few years, mostly since 2000, lionfish have spread dramatically along the coast of the Atlantic, from North Carolina down to the southern Caribbean and Mexico's beautiful Yucatan peninsula.  Typically considered to be a rocky or coral reef species, they've now been found swimming in the intracoastal waterway; that labyrinth of salt-marshes, channels and estuaries, engineered to allow safe passage of boats along the US coast in wartime.  This is sort of an unusual location, but it speaks to the adaptability of this remarkable fish.

So, what to do about such an animal??  Well, that's a tough one.  Invasive species (or more accurately, moving species around) are one of the greatest impacts humanity has had on natural environments, and there are very few cases where we have successfully eradicated or controlled an invasive (but see prickly pear in Australia), more often they just become part of the furniture and we get used to their impacts on the local ecosystem.  Introducing natural enemies (diseases, predators) like they did for prickly pear is a dangerous game; if you tried to get the Cactoblastus moth introduced to Australia in these days of stricter biosecurity, you'd almost certainly be denied.  You can easily get into a "spider to catch the fly" situation too; in fact that's how cane toads were introduced to many places - to control sugar cane beetles (which they suck at).  Perhaps the best approach is to do what we do best - create a market that will promote human efforts to exploit them, and then rely on the Tragedy of the Commons to do the work for you.  This has already been proposed with Asian carp.  Fortunately, it turns out that lionfish are not only spectacular aquarium fish, but also delicious in a white wine sauce.  I am sure that if we set our minds to it, we could do as good a job wiping out this species as we have with so many others.  So c'mon everyone and grab a fork; Save a reef - eat a lionfish, today!

(Photo and graphic from NOAA)

Ului inches closer

Looks like Ului will cross the coast right over the Whitsunday Islands.  Good luck to the folks in Proserpine and Bowen.

This picture from the Australian Bureau of Meteorology

Cyclone Ului approaching the Queensland coast

Cross your fingers for the people of Queensland, Australia, who are facing an impending cyclone, Ului.  It was just downgraded to a Category 2, but you never relax with these things right?  Tourists and researchers have been evacuated from Heron Island and several others, but it looks like it might cross a little further north.  Here's hoping it avoids major populated areas.

Whale sharks arrive early at Ningaloo Reef, Australia

I have never been to Ningaloo (great name, right?) - its WAY on the other side of Australia from where I grew up - but its a fascinating place.  Whale sharks gather there every year, and this year it looks like they turned up earlier than usual.  Whale shark aggregations are amazing events and the one at Ningaloo is one of the biggest.  Why gather? Why Ningaloo?  Why then?  How do they know where to go?  These are just some of the great mysteries of whale shark gatherings; its amazing that we know so little about the worlds largest fish.