Seized by a sneeze - more from Kristie Cobb Hacke

AD - Its clear to me that Kristie is a repressed zoologist!  Her pure joy at the sight of dozens of tiny brittle stars attached to a sea fan is the kind of emotion that drove many of us into marine science in the first place.  But don’t take my word for it…

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When I was a kid I used to spend hours thinking about how small we are in a really big world. I would often ponder “what is at the end of the universe?” I would amuse myself by thinking things like “it’s a brick wall” and then assume if you walked around or knocked it over there was always something on the other side. I would have this same thought again and again sometimes stopping to pause and wonder if it is something just like a big brick wall and there is no other side. When I was in high school these thoughts were shared by some of my friends as we circulated and chatted about Douglas Adams and his version of the universe and the restaurant at the end.

Another popular thought of mine was that earth was created by a giant sneeze. Sometime in middle school biology a teacher posed the thought that there could be whole universes in something as small as a pin-head. I had this great vision of the giant humans, one standing in front of another being seized by a sneeze. This uncontrollable sneeze produced projectile droplets that landed on the other person’s glasses. Although the term “yuck” is the first thing that comes to mind the second was always….”what if that just created a whole universe?” Would some small organism in that universe consider the edge of the droplet the end of the universe? Would they push on to see what was on the other side? Would they live and die a whole lifetime in the instant between the sneeze and the inevitable wiping of the lens?

From the collection boxes of the Sea Link II the scientists brought up a bio-box of goodies. Their samples included a beautiful gorgonian sea fan. As they unloaded, documented and photographed the various items, they pointed out many beautiful teeny-tiny brittle stars on the single fan sample. One of the researchers suggested that the sample piece contained more than 30 of the sea stars. Each of the sea stars was amazingly blended to hide themselves among the thin fan structure of the coral. Their fragile thin legs curled around the fan and, when coupled with their patterning, it created the perfect camouflage. The researchers were amazingly accommodating and allowed me to touch and handle one of the sea stars and a piece of the coral. As I carefully unwound an arm I had a stunning flashback to the brick wall and the sneeze. I wondered instantly if to these sea stars is the edge of their universe the single fan, the whole coral colony, the structure to which it is attached or some expanse of sea floor?

Camouflaged brittle star attached to a gorgonian

When you consider the ocean as a whole it is amazing to think about all the millions of places that are yet to be discovered. Not to mention the uncountable species yet to be recorded. There are new depths known only through scans just waiting to be explored by humans. This journey has allowed time for conversations about new technology being created and innovative ways to use existing technologies or commercial vessels for research applications. As each of these becomes available and is applied it will undoubtedly lead to new discoveries. As this continued, in our lifetimes alone, there are bound to be millions if not trillions of questions to be asked and hopefully answered. Although I doubt the answer to life the universe and everything is as simple as “42” and I certainly cannot claim to know if there is a brick wall waiting at the bottom of challenger deep just waiting to be knocked over. What I do know is that research and its concrete ability to pose and then answer questions is incredibly important to our full comprehension of both the universe and the deep.

AD - This relationship between the brittle star and the sea fan is a great example of how little we know about symbioses in the oceans.  Clearly the two organisms are living in close association, but in what manner?  Is it pure parasitism, whereby the brittle star benefits and the sea fan is damaged?  Or is it commensalism, where the brittle star benefits and the sea fan is indifferent to its passenger?  Is it maybe possible that there is some sort of mutual benefit that we are unaware of?  As a parasitologist by training, how little we know about the these associations makes it hard for me to define my own field.  So, while Kristie’s vision is a little broader than mine (scaling up from brittle stars to the edge of the known universe!), I mostly grapple with smaller questions of who makes out better in this little biological transaction, and how does the sum of those transactions across the diversity of animal groups serve to reinforce or undermine stability in the whole ecosystem.

Everything's just peachy

I have another guest post over at Parasite-of-the-Day today about Peachia.  What’s that, exactly? Well, you’ll just have to go over there and find out.

Six fish parasites you don't want to miss...or catch

Are you one of those people who just can’t stand the idea of parasites? You find the idea of some slimy  critter living in or on you and feeding on your very flesh just repulsive?  If so, this post may be best viewed through a crack between fingers clamped tight across your eyes.  If, on the other hand, you’re more like me and find the idea just fascinating (enough in my case to study them for grad school), then enjoy the following, which comprise a six-pack of the some of the best parasites you’ll find in fish.  I’m not just restricting it to fish because this is a marine science blog, but because fish truly get some of the worst (best?) parasites around.  Its probably got a lot to do with the diversity of available hosts (28,000+ species of fish = parasite smorgasboard!) and the supportive medium in which they live.  Here they are then, six fish parasites you don’t want to miss.

1. Bite my tongue

Delightful little critters, tongue biters are a type of isopod, vaguely related to the pill bug/roly poly/slater bug you might see in a wood heap from time to time.  They’re actually crustaceans more related to shrimp and crabs than to insects, so in a sense the common pill bug is more of a weirdo than the tongue biter; at least tongue biters have the decency to be truly aquatic, but I digress.  Cymothoid isopods live on all sorts of fish in both fresh and salt water.  They have a tick-like life-cycle where they periodically jump on and off the fish, taking a meal of blood or tissue each time they are on, and moulting each time they are off.  Lots live on the skin or gills, and some even invade the body cavity, but the most famous are those that live in the mouth and hang onto the bottom lip, peering out over the teeth like a motorcyclist peeking over the windshield.  They have quite good eyes, so they can probably see whats going on pretty well.  Why live on the tongue?  Not sure - oxygenated water supply perhaps?  Maybe they just like the view.  Whatever the reason, it would be a bit like you or I carrying a rhinoceros beetle around in your mouth all the time.

Image credit: Australian Museum

 2. Size does matterImage: NOAA

Your typical free-living planktonic copepod looks like the thing on the right here: tiny (<1mm or 1/20th in.), clearly crustacean, with delicate swimming antennae and one or two simple egg clumps hanging off the abdomen.  Not so their parasitic cousins.  In a pattern repeated often in the evolution of various parasite groups (parasitism having arisen in practically every phylum), the parasitic ones are much bigger than their free-living relatives.  Why?  It could be many reasons, like predator evasion, reproductive efficiency or just a result of living la dolce vita off some other poor sod.  Whatever the reason, pennellid copepods take this size disparity to the extreme.  In a group where the average size is less than 1mm, adult pennellids can be 30cm or more in length, even longer if you count the strands of eggs that trail behind them in the water like a string of pearls, popping little parasitic progeny off the end like pez.  That’s three and half orders of magnitude in body size, and there aren’t many animal groups that can claim that sort of range.  The largest  pennellids look like big brown toilet bImage:Oceansunfish.orgrushes sticking out of the flesh of their hosts, which tend to be large pelagic things like sunfish, marlin and sharks (sometimes even dolphins!).  The brush bit is the tail end and serves as a sort of gill, with countless tiny filaments to provide a high surface area and thereby facilitate oxygen exchange.  If the brush is the back end, then that means the head is - you guessed it - buried deep in the flesh, usually T-ing into a blood vessel like a wall anchor and providing the copepod with a continuous source of food to fuel those ever-lengthening egg strands. 

There’s a great scene in the BBC series Blue Planet (that paragon of marine biologist porn!) where a sea gull valiantly tries to remove pennellids from the skin of a basking sunfish, but in vain.  It proves nicely that a large body size confers on a parasite both robustness and protection from predators.  Its one of the best and most remarkable scenes in the entire film series.

 3. Going to great lengths

This isn’t Nematobibothrioides, but a similar species from Hawaiian jobfish. Image:HIMBThe ocean sunfish, Mola mola, is also host to the third in our set: the didymozoid Nematobibothrioides histoidii.  I know, awful names, right?  Didymozoids (pronounced like P-Diddy) are a family of parasitic flatworms in the digenean (“fluke”) group.  Most digeneans live in the gut, but didymozoids have invaded the flesh.  That’s not what makes this worm special, though, there are lots of worms that live in flesh.  No, its the length of N. histoidii that sets it apart.  In the best paper on the subject Glenn Noble (1975) describes finding them up to 12 meters long!  That’s a 40 foot worm, as Noble says “snaking” its way through the tissues, leaving a trail of eggs in its wake.  Chances are, N. histoidii may even grow larger than that.  Scientists don’t know, partly because dissections of Mola aren’t all that common and partly because dissecting an entire sunfish to extract the fragile, threadlike worm in one piece is practically impossible.  Didymozoids have incredibly complex life cycles that likely involve flaoting snails and copepods and all sorts of other intermediate hosts.  Despite this, or perhaps because of it, they’ve been very successful in infecting a wide range of pelagic fishes.  I probably shouldn’t tell you that a significant proportion of the tuna you’ve ever eaten probably hosted didymozoids somewhere in its body when it was alive.  Oh wait, I just did…

 4. Beauty in the beast

Trichodina is my favourite protistan (single-celled) parasite; it’s one that parasitology students and researchers alike are drawn to for its spectacular marriage of form and function and for the startling and beautiful complexity inherent in a single cell.  Trichodinids are ciliated parasites of the skin, fins and gills (mostly) of fishes (mostly) in both fresh and salt water, and they’re shaped as discs or hemispheres, sucking onto the surface of the fish with their flattened underside.  Everyone always shouts “Scubbing bubbles!” when I show them in parasitology classes, and I guess I can see why:

Trichodina and Scrubbing Bubbles - separated at birth?

What makes Trichodina so amazing is a ring of interlocking structures just under the cell membrane, called denticles, that are used to aid in attachment to wet fish skin, which is pretty slippery stuff.  When the pins in the middle of the denticle pull up, the blades on the outside bite down into the skin, with the added bonus of creating suction on the underside.  The blades are revealed by staining the cells in silver nitrate and then exposing them to UV light to develop them, exactly like a photograph, and their structure is very important for telling species apart, which is good, because there’s over 150 in the genus!  Some of them are definitely parasitic and can cause nasty disease, but most are probably commensals, which means they’re just using the host as a home and means of conveyance while they feed on bacteria and other detritus suspended in the water.  One of the most captivating things I ever saw was a trichodinid cell dividing, under a microscope.  The way a single-cell could disengage all those blades (each daughter cell gets half), successfully divide and then replicate the missing denticles and reassemble their intricate structure was just mesmerizing.

 5.  Stop it, or you’ll go blind

 Diplostome metacercariae in a fish’s lens. http://www.thefishsite.com/ Eyes are sensitive things, so the thought of some freeloading bug making a home in your precious orbits is just creepy, and yet parasites in the eyes are pretty common.  Why?  There’s several possibilities, but the two best are, firstly, that the eye is a relatively inactive place as far as the immune response goes (not a lot of blood inside your eyeball, normally anyway) and that, secondly, infecting the eyes can help you get where you’re going next.  If we, ahem, focus on the second reason for a minute, I can tell you about diplostomes.  These are another family of digenean flatworms, but unlike Nematobibothrioides in the Mola, these mature in birds - fish-eating birds to be exact.  The stage that infects fish is an immature form that lives in the lenses of the eye.  They’re very common, almost ubiquitous, among freshwater fishes, but nearly always only in one eye.  If we, um, look at some fish and find that a third of individuals have diplostomes in the left eye and third of fish have them in the right eye, then a ninth of fish (1/3 x 1/3 = 1/9) should have it in both eyes, but this is not what we, ahem, see.  Where are the dual infections?  You guessed it - nailed, um, in the blink of an eye by one of the aforementioned piscivorous birds.  A fish, it seems, can get by with being functionally blinded in one eye, but being blind in both makes you, er, a sight for sore eyes to your average heron.  In this way the parasite is playing probability statistics to get its life-cycle completed; worms are good at math, who knew?

6. When the worm turns

Our first 5 candidates were all parasites OF fish, but the title of the post was “Six fish parasites” and that could just as easily mean the fish IS the parasite.  I thought about doing the male anglerfish, which parasitises his mate so intimately that their circulatory systems fuse, or the candiru, that tiny terror of the Amazon: a catfish that swims into the human urethra and locks its spines erect, making removal a matter for a skilled surgeon.  But in the, um, end, I had to go with the pearlfish (I’m sorry, I’ll stop now, promise).  Thats because this delightful fish, rather humourously called Carapus, chooses to live in the lower digestive system of sea cucumbers, a lumbering sausage-like relative of urchins and starfish that spends its days lazily sifting food particles from sand on coral reefs.  Pearlfish may not, strictly speaking, be parasites, since it seems that they feed while on day-trip excursions out of the sphincter, rather than on the cucumber itself, but I’m told they can and do feed on the respiratory tree of the host if the need arises.  Its a good thing sea cucumbers are masters of regeneration.  I’ve never actually seen one, but then again I dont spend a lot of time peering into beche-de-mer butts

Image: Claude Rives/Fishbase

Its often said that parasitism is the most common lifestyle on the planet, and nowhere is this better seen than among fish hosts.  From forty foot flukes to tongue-biting isopods, fish are home to the most amazing variety of parasitic symbionts.  Estimates of how many species of fish parasites there are run into the hundreds of thousands; vastly more than the diversity of fish, which are themselves the most diverse vertebrate phylum.   Next time you look at a fish, then, try to see it for what it really is: a little swimming city, replete with enclaves of surprising parasite diversity in practically every tissue.

What's THIS now?

I have a guest blog post today over on Susan Perkin’s fine AMNH blog “Parasite of the Day”, regarding this fascinating cirtter.  What on earth is it?  You’ll just have to roll on over there and check it out

Tampa - brace yourselves...

Next week I will be in sunny Tampa for the 6th International Symposium on Aquatic Animal Health, a great meeting that happens every four years covering the gamut of AAH from aquaculture to fisheries to aquariums and even marine mammals (they’re OK too, ‘spose).  The energetic Andy Kane from UF and the lovely and talented Sarah Poynton from Johns Hopkins are chairing the program and it looks to be a great set of folks attending. They’ve got me co-chairing a session about parasites in molluscs, which should be fun, and my own talk will be about metabolomics in whale sharks, a collaboration with colleagues at Georgia Tech.  What’s metabolomics, I hear you say?  Well, perhaps I’ll post about it while I’m there (you know, AFTER I make the powerpoint.  I should probably start that…).

The AGM for the Fish Health Section of the American Fisheries Society will also be there, so we’ll be mixing hundreds of science talks with some serious chit-chat about the state of fish health science in this country, which has evolved significantly of late, in part because of new disease epizootics (VHSV anyone?), the National Aquatic Animal Health Plan and the increasing role of veterinarians in fish health research (the more the merrier, I say).

Should be a great meeting.  Anyone got any “must hit” spots while I am there? or want to meet up for a cuban sandwich, or better yet, a couple of cervezas?

More on sharky parasites

I have a guest post over at the aforementioned Parasite-a-Day blog today. 

Why should sharks get all the glory? - its shark *PARASITE* week too

 Everytime you sit down to watch a premiere in this weeks Discovery Channel shark week, I want you to imagine something: every single shark you see is loaded with parasites.  All of them.  On the gills, sometimes on the skin, and especially in their unique spiral valve intestine, live a myriad critters that make their living off the top predators in the ocean.  Which makes you wonder, are they really the top?  Hmmmm….

In celebration of this carnival of diversity that exploits our toothy friends, AMNH curator/blogger Susan Perkins (ably supported by a veritable Who’s Who of fish parasitologists from around the world) is hosting a parade of bugs for shark week on her blog Parasite-a-Day. Here’s what she’s had so far:

August1. Anthobothrium, an elegant tapeworm.  Yes, I said elegant.  You got a problem with that?

August 2. Gnathiid isopods.  The ticks of the marine realm, blood meal anyone?

August 3. Branchotenthes robinoverstreeti.  A six-suckered monogenean from the guitarfish

August 4. Pandarus rhincodonicus.  A parasitic copepod that likes to hitch a ride on the lips oif whale sharks.

Keep an eye on the blog for the rest of the week and beyond.  Its a fantastic showcase of parasite diversity

One of the bizarrest parasitic relationships you will ever see

My good colleague Janine Caira wrote a paper way back in 1997 about one of the strangest parasites ever recorded in an animal.  This paper has stuck with me ever since, I think because I saw the original photos when I visited the lab of one of the other co-authors George Benz, when he was with Tennessee Aquarium (he's now at Middle Tennessee State U.).  So, I thought I'd revive it for you guys; the story goes like this:

Janine and her co-author Nancy Kohler had received a report from a longliner of a really big foul-hooked shortfin mako caught near Montauk, NY.  (a shortfin is shown at right, from discovery.com, this one with plenty of parasitic copepods on the dorsal fin - it sucks to be a shark sometimes).  Now, Janine is the queen of tapeworm taxonomy in sharks and rays - believe it or not, there's lots of them - and had visited Montauk before to collect parasites during catch-and-kill shark tournaments held there.  To make the most of the unfortunate death of this mako, they raced across the sound from Connecticut to collect parasites from the beast.  It was a huge animal, nearly 900lbs, and during necropsy, as they say in the paper, they "were astonished to find two anguilliform fish in the lumen of the heart".  Thats right, eels; this shark had two eels living in the chambers of the heart!  These particular eels, called pugnose eels or Simonchelys parasitica, have been recorded before burrowing into the flesh of halibut and other large North Atlantic fishes (hence their species name), but never completely internal and certainly not in the lumen of the heart, so this was a truly remarkable find. 

Janine and her colleagues were unable to determine the path of entry, but they showed good evidence that the eels were alive in the heart prior to the shark being killed and put in the fridge, because their guts were full of blood and there were pathologic changes to the heart.  Their conclusion?  That this was a facultatively parasitic relationship.  In other words, the eels didn't need to be living in the sharks heart (that would be obligate parasitism), rather they took advantage of an opportunity to get a meal.  They proposed that the eels probably attacked the shark after it had been hooked and was dangling, distressed, from the longline.  They had some evidence that the shark was probably resting on the bottom, which may have made it easier for the eels to find.  The pugnoses somehow gained entry (hypothesised to be through the gills) and made their way to the heart, where they dined on the beasts blood up until it died.  Maybe they would have burrowed out again after the animal expired, maybe they would have suffocated (remember - the eels had be swimming in and breathing the sharks blood once they were inside, how bizarre is that?).  We'll never know because the carcass went in the fridge, which ended things for the eels, but also led to this amazing discovery.

The horrifying part is that the shark was almost certainly alive as the eels made their way into its flesh and began to consume its life blood from the inside.  It would have been a long, slow and nasty way to go out.  It just goes to show that even when you are at the top of the food chain, you're never really at the top of the food chain...

Caira, J., Benz, G., Borucinska, J., & Kohler, N. (1997). Pugnose eels, Simenchelys parasiticus (Synaphobranchidae) from the heart of a shortfin mako, Isurus oxyrinchus (Lamnidae) Environmental Biology of Fishes, 49 (1), 139-144 DOI: 10.1023/A:1007398609346

The water is ALIVE!

Its easy to get discouraged about the plight of marine ecosystems and the future of all those incredible marine species that we love so much. This is especially so of late, with all the bad news about the oil spill in the northern Gulf of Mexico and the impacts that it may well have on several habitats. Consider this post, then, as your good news story for the week. I am here to tell you that there is still amazing stuff to see in the ocean. Incredible stuff. Stuff that will blow your mind. I can tell you this with supreme confidence, because for the last two days, that’s exactly what I have been seeing. As part of the research program at Georgia Aquarium, I am with colleagues in Quintana Roo, Mexico, studying whale sharks and other species that live in the azure waters of the Yucatan peninsula. Jeff Reid, who is the aquarium’s dive safety officer, is here and our main colleague in Mexico is Rafael de la Parra of Project Domino, who has been working on whale sharks and other marine species in the area for many years. This is a remarkable part of the world, with a lot of great terrestrial activities (can you say Cenotes, anyone? No? How about Mayan ruins?), exceeded only by the marine life, which is truly spectacular.

Yesterday Jeff and Raffa and I spent the day boating around the northeastern tip of the Yucatan along with videographer Jeronimo. Now, when you’re on a boat, you can only see a small strip of ocean either side of the vessel, and yet over the course of the day we saw lots of mobula (devil rays), turtles, flying fish, manta rays, spotted dolphins and whale sharks. We snorkeled alongside some of these animals and, in the case of whale sharks and mantas, took samples of their food for later analysis. They dine on the rich plankton soup of this tropical upwelling area, much of which consisted of fish eggs, which hints at other fish species – yet unseen – taking advantage of the plankton to start their next generation by spawning in the surface waters. Snorkeling next to a whale shark in the natural setting was a special thrill; I’ve been lucky enough to work with the animals in the collection at Georgia Aquarium since 2006, but this was my first encounter with them in the wild. Except for the slightly different “faces” (we do get to know our animals pretty well) and the parasitic copepods visible on the fins of the wild animal, it could have easily been the very same sharks Jeff and I have been working with in Atlanta.

Today, Jeff and Raffa and I joined Lilia (from the Mexican department of protected areas CONANP) and pilot Diego for an aerial survey of the waters around the northeastern tip of the Yucatan. In contrast to the boat, you can’t get in the water from a plane (its not advisable anyway), but you can see a whole lot more at once and cover a much greater area in a relatively shorter time. From the air, lots of sharks, cownosed rays, manta, dolphins, fish schools and whale sharks were all visible, and I am told that flamingos and manatees can be seen at other times too. The manta rays, which numbered in the hundreds, were especially impressive and included at least two species (see my post about taxonomy of mantas). The sheer number of cownosed rays, called chuchas in the local slang, was staggering (muchas chuchas, if you will). They formed huge schools that looked for all the world like the rafts of sargassum weed that accumulate on the wind-lines at the water’s surface offshore. Many of the turtles and mobula seemed to be in the mood for love; most turtles were in pairs (or a pair being followed by other hopeful males), whereas the mobula followed each other in lazy tandems, their wingtips breaking the surface with every stroke. Whale sharks were also there – lots of them – with their attendant flotilla of tourist boats and tiny orange specks of snorkelers in life-vests, doing their best (and largely failing) to keep up with the gentle giants.

When you have experiences such as those I have shared with my colleagues over the last two days, you are reminded why we do this stuff in the first place. Its not just for the papers, or the salary or the glory of new discovery (yeah, right!), its for those moments working with animals when you and a colleague become friends because you shared an experience of the oceans that most folks will never have. We should seek to share and recreate those moments with everyone we can, whether its in an aquarium or on the open ocean. I am pretty sure that if we could all do that, then public empathy for the plight of the oceans would skyrocket, and many of the threats that face them would be addressed quick smart.

A Parasite a Day, keeps the Doctor in pay

My colleague Susan Perkins at AMNH has a most excellent blog that features a different parasite every day for a year.  Since the oceans have more parasites than anywhere else by far, many of her feature critters are marine.  Check out some of these marine beasties, then enjoy the rest of the collection.  There's a new one every day.

Crepidostomum cooperi - a digenean (fluke) parasite of fish
Nasitrema globicephalae - a digenean parasite of the sinuses of whales
Cyamus ovalis - isopod parasites often called "whale lice"
Maritrema novaezealandensis - an important model digenean from New Zealand mudflat animals
Polypodium hydriforme - a weird parasitic jellyfish relative that lives on sturgeon eggs, and:
Dolops sp., -  a type of Branchiuran (related to crustaceans) parasitic on piranha

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

SAC's revisited

A little while back I wrote about how we can use Species Accumulation Curves to learn stuff about the ecology of animal, as well as to decide when we can stop sampling and have a frosty beverage. There’s a timely paper in this month’s Journal of Parasitology by Gerardo Pérez-Ponce de Leon and Anindo Choudhury about these curves (let’s call them SACs) and the discovery of new parasite species in freshwater fishes in Mexico. Their central question was not “When can we stop sampling and have a beer?” so much as “When will we have sampled all the parasites in Mexican freshwaters?”. They conclude, based on “flattening off” of their curves (shown below, especially T, C and N), that researchers have discovered the majority of new species for many major groups of parasites and that we can probably ease up on the sampling.

Trying to wrap your arms (and brain) around an inventory of all the species in a group(s) within a region is a daunting task, and I admire Pérez-Ponce de Leon and Choudhury for trying it, but I have some problems with the way they used SACs to do it, and these problems undermine their conclusions somewhat.

In their paper, the authors say “we used time (year when each species was recorded) as a measure of sampling effort” and the SACs they show in their figures have “years” on the X-axis. Come again? The year when each species was recorded may be useful for displaying the results of sampling effort over time, but its no measure of the effort itself. Why is this a problem? For two reasons. Firstly, a year is not a measure of effort, it’s a measure of time; time can only be used as a measure of effort if you know that effort per unit of time is constant, which it is clearly not; there’s no way scientists were sampling Mexican rivers at the same intensity in 1936 that they did in 1996. To put it more generally: we could sample for two years and make one field trip in the first year and 100 field trips in the next. The second year will surely return more new species, so to equate the two years on a chart is asking for trouble. Effort is better measured in number of sampling trips, grant dollars expended, nets dragged, quadrats deployed or (in this case) animals dissected, not a time series of years. The second problem is that sequential years are not independent of each other, as units of sampling effort are (supposed to be). If you have a big active research group operating in 1995, the chances that they are still out there finding new species in 1996 is higher than in 2009; just the same as the weather today is likely to bear some relationship to the weather yesterday.

OK, so what do the graphs in this paper actually tell us? Well, without an actual measure of effort, not much, unfortunately; perhaps only that there was a hey-day for Mexican fish parasite discovery in the mid-1990’s. It is likely, maybe even probable, that this pattern represents recent changes in sampling effort, more than any underlying pattern in biology. More importantly, perhaps, the apparent flattening off of the curves (not all that convincing to me anyway), which they interpret to mean that the rate of discovery is decreasing, may be an illusion. I bet there are tons of new parasite species yet to discover in Mexican rivers and lakes, but without a more comprehensive analysis, it’s impossible to tell for sure.

There is one thing they could have done to help support their conclusion. If they abandoned the time series and then made an average curve by randomizing the order of years on the x-axis a bunch of times, that might tell us something; this would be a form of rarefaction. The averaging process will smooth out the curve, giving us a better idea of when, if ever, they flatten off, and thereby allowing a prediction of the total number of species we could expect to find if we kept sampling forever. Sometimes that mid-90’s increase will occur early in a randomised series, sometimes late, and the overall shape for the average curve will be the more “normal” concave-down curve from my previous post, not the S-shape that they found.  After randomizing, their x-axis would no longer be a “calendar” time series, just “years of sampling” 1, 2, 3… etc.  There's free software out there that will do this for you: EstimateS by Robert Colwell at U.Conn.

The raw material is there in this paper, it just needs a bit more work on the analysis before they can stop sampling and have their cervezas.

Perez-Ponce de León, G. and Choudhury, A. (2010). Parasite Inventories and DNA-based Taxonomy: Lessons from Helminths of Freshwater Fishes in a Megadiverse Country Journal of Parasitology, 96 (1), 236-244 DOI: 10.1645/GE-2239.1

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)