Biology – Page 23 – Science Sushi

Playing in Tide Pools | Scientist in vivo

Here at Science Sushi, I often talk about the great work being done by other scientists, but I rarely turn the focus around and talk about my life as a scientist. This is a shame because I really love my job. So, starting today I’m going to try and take you out in the fiels and into the lab in a series I’ve titled “Scientist in vivo“. I hope that, through this series, you’ll get to learn what it’s like to be a scientist, what I actually do for a living and what makes my job so rewarding. Enjoy!

As a scientist, one of the most important parts of my job is outreach. I consider this blog and other outreach activities as an integral part of my profession. So every year, I wrangle grad students from the Ecology, Evolution and Conservation Biology (EECB) Specialization at the University of Hawaii to help a local elementary school teach their students about the ecology of tide pools. The partnership between EECB and Mililani-Mauka Elementary school is one of those rare gems in outreach where both sides get a tremendous amount out of the relationship. The school gets trained scientific experts that fascinate and amaze the kids with tales of slimy defenses and odd partnerships between crabs and anemones. In turn, the graduate students get to take a day off, get out of the lab, and act like kids playing in tide pools. Sometimes, I think the overworked grad students are more excited to catch critters than the kids!

What can you find in a tide pool on the coast of Oahu? Well, let’s find out…

Hexabranchus saguineus – Spanish Dancer

Kingdom: Animalia

Phylum: Mollusca

Class: Gastropoda

Family: Hexabranchidae

Genus: Hexabranchus

Species: H. sanguineus

One of my favorite finds was a Spanish Dancer nudibranch – a name that aptly fits the beautiful undulating motion of this colorful animal while it swims which looks like the swirling of a flamenco dancer’s skirt. It’s the largest species of nudibranch in Hawaii, and can get over a foot long!

The term “nudibranch” means “nude/naked gills,” and refers to the frilly, external gills found in these species (they look almost like feathers sticking out of the dancer’s back). The scientific name for this species, Hexabranchus sanguineus, refers specifically to the number of gills (six) and to its blood-like red coloring. Nudibranchs are often brilliantly colored and found in many sizes and shapes, which may serve to warn predators as many species are toxic. Unlike other sea critters, toxic nudibranchs don’t make their own defenses – they steal them from species they eat, like sponges and Portuguese man-of-war.

Dardanus gemmatus – Jeweled Anemone Crab

Kingdom: Animalia

Phylum: Arthropoda

Class: Malacostraca

Order: Decapoda

Family: Diogenidae

Genus: Dardanus

Species: D. gemmatus

This beautiful little crab is a specialized kind of hermit crab known as an anemone crab. The frilly bits on its shell aren’t just for show – they’re a kind of sea anemone, Calliactis polypus. For the crab, the anemones provide protection. Their painful stinging cells make the crab’s predators think twice about what they snack on. Those pretty pink strands are actually specialized stinging threads called acontia which help protect both the anemone and the crab. In turn, the crab provides the anemones with movement, thus granting them access to better food resources. This kind of you-pat-my-back-I’ll-pat-yours relationship is what is known in as symbiosis or mututalism.

Dolabella auricularia – Wedge or Eared Sea Hare

Kingdom: Animalia

Phylum: Mollusca

Class: Gastropoda

Family: Aplysiidae

Genus: Dolabella

Species: D. auricularia

Ok, so you can’t really see the sea hare in these pictures. But you can see what it produces when it’s scared – a thick batch of bright purple slime! Sea hares – also known as sea slugs – are relatives of snails and other shelled animals, but like slugs on land, they haven’t had a shell for millions of years, thus making them more vulnerable to predators. But the sea hares aren’t defenseless, as you can see from the goo in the pictures. When they feel threatened, they are able to produce large amounts of a thick slime which confuses their would-be predator, allowing the slug to slither away unharmed. The purple color for the slime from the red algae the hares feed on.

Echidna nebulosa – Snowflake Moray

Kingdom: Animalia

Phylum: Chordata

Class: Actinopterygii

Order: Anguilliformes

Family: Muraenidae

Genus: Echidna

Species: E. nebulosa

Tide pools are important nursery habitats, even for active predators like this snowflake moray. These scary hunters can grow up to 3 feet long and pack one heck of a bite, but this young eel is as vulnurable to predators as other small fish. The tide pools provide him and other young fish a place free of large predators where they can grow large enough to try and make it on their own on the exposed reefs. Snowflake morays don’t often eat fish, though they will if the opportunity arises. Their teeth are flatter than other species of eel, and are more suited to crushing shelled prey items like as shrimps, crabs, and sea urchins.

Octopus cyanea – Day Octopus

Kingdom: Animalia

Phylum: Mollusca

Class: Cephalopoda

Order: Octopoda

Family: Octopodidae

Genus: Octopus

Species: O. cyanea

By far one of the kid’s favorite finds was this small day octopus. Popular here in Hawaii as a food item (known as tako), day octopus are heavily fished. As daytime hunters, day octupus have incredible camouflage abilities. Let me point out that the two photos above are of the same octopus – those color differences are just a couple of the wide variety of elaborate color patterns and skin textures that the octopus displayed in our short time with it. Octopus have complex brains with a highly developed nervous system capable of changing their skin almost instantly as they move over different substrates. Roger Hanlon, an octopus biologist, once recorded a single day octopus changing patterns 1,000 times over a 7 hour period!

Scorpaenopsis diabolus – Devil Scorpionfish

Kingdom: Animalia

Phylum: Chordata

Class: Actinopterygii

Order: Scorpaeniformes

Family: Scorpaenidae

Genus: Scorpaenopsis

Species: S. diabolus

Last but not least, however, was by far my favorite catch of the week – this small devil scorpionfish, now named Stumpy. You see, this guy is one of the species that I study. I’m investigating the toxins in the entire order to get a better understanding of how toxins evolved in fish, and this little cutie is one of the many fishes whose spines possess a potent and painful sting. It’s easy to see why this particular species might be mistaken for a rock covered in algae. Because of exceptional camouflage, scorpionfish like this one are often unnoticed by tide pool goers, swimmers and divers until it’s too late and they find out the hard way exactly how strong the toxins they produce are. My goal is to better understand why other member of the order – groupers, for example – aren’t as toxic, even though they possess the ability to produce a similar protein toxin. Do they not express it? Or is the toxin itself altered to be less painful? Given that the toxins have strong effects on our bodies, it’s possible they may provide clues to new drugs or insights into how our cells work.

Stumpy here has come back with me so I can study his toxins as a part of my dissertation research. He currently resides in a tank at my house, where he has been eating like a glutton all week. The speed with which these ambush predators gulp a fish right out of the water never ceases to amaze me. Other cool fact: he glows orange in UV light. Yeah. Orange. How neat is that? I study the coolest animals EVER.

Check out more photos from this year’s tide walks on Facebook!

Mounting Evidence Suggests Sharks Are In Serious Trouble

Can you imagine oceans without sharks? We may soon have to, as new research suggests may already be 90% of the way there.

Studying shark populations can be tricky. As David Shiffman explains well, while there are a number of methods that can be used to study shark populations, quantifying just how far their numbers have fallen can be difficult. However, recent research out of the University of Hawaii suggests that the presence of humans has a severe and strong negative impact on sharks, driving down numbers by over 90%.

Sharks play a vital role in coral reef ecosystems. Yet every year, millions are killed for asian delicacies and disproven cancer cures. There is no question our shark fishing habits have devastated their populations; the only questions that remain are how much of an effect are we having, and can the sharks recover.

In an effort to answer the first, the research team crunched data from 1607 surveys from the NOAA Coastal Reef Ecosystem Division (CRED) to calculate the effect of human habitation on shark populations. The CRED team counted sharks throughout the Pacific using towed diver surveys, the most efficient and effective way to study open ocean creatures on a large spatial scale, and compared their counts with local human population numbers. Their results were clear – and sobering.

“Around each of the heavily populated areas we surveyed — in the main Hawaiian Islands, the Mariana Archipelago and American Samoa — reef shark numbers were greatly depressed,” said Marc Nadon, lead author of the study. “We estimate that less than 10% of the baseline numbers remain in these areas.”

The team also looked at other factors that might be affecting shark populations, including temperature and reef productivity. However, while sharks preferred warmer waters full of potential prey, the negative impact of humans dwarfed these effects. “Our results suggest humans now exert a stronger influence on the abundance of reef sharks than either habitat quality or oceanographic factors,” the authors wrote.

The team estimated that less than 100 people is enough to cut shark populations by 20%. Even 1,000 people – which is much less than the population of many small islands in the Pacific – was enough to decrease shark populations by 60%. As Nadon put it, “In short, people and sharks don’t mix.”

The findings are consistent with other research in the field. A 2003 paper, for example, found that shark populations in the Northwestern Atlantic dropped over 65% between 1986 and 2000. Similarly, a 2010 paper estimated that shark populations in the Chagos Archipelago had declined 90% since the 1970s. The more we study sharks, the worse the picture becomes, and the stronger the case becomes for conservation efforts. We simply cannot continue to treat these animals the way we do now, for all scientific evidence suggests the day is fast approaching when there will be no sharks left to exploit.

Reference: Nolan et al. Re-Creating Missing Population Baselines for Pacific Reef Sharks. Conservation Biology; DOI: 10.1111/j.1523-1739.2012.01835.x

Reflections On The Gulf Oil Spill: Conversations With My Grandpa | Observations

Two years ago, an explosion on the Deepwater Horizon oil platform led to the spilling of almost five million barrels of oil in just a handful of months. I wrote the following post in June of that year, two months after the spill began. Even now, we still don’t really know how much of an effect the oil spilled and the subsequent cleanup efforts will have on the Gulf ecosystem. At least, as I conclude in this post, I hope we have learned our lesson.

Oil supplies the United States with approximately 40% of its energy needs. Billions upon billions of gallons are pumped out of our wells, brought in from other countries, and shipped around to refineries all over the states. 1.3 million gallons of petroleum are spilled into U.S. waters from vessels and pipelines in a typical year. Yes, it would be great if we never spilled a drop of oil. No matter how hard we may try, though, the fact is that nobody is perfect, and oil spills are an inevitable consequence of our widespread use of oil. The question is, once the oil is out there, how do we clean it up?

Nowehere is this issue more glaring than in the Gulf of Mexico right now, where 35,000 to 60,000 barrels of oil are spewing out of the remains of the Deepwater Horizon drilling rig every day. The spill has enraged an entire nation. But perhaps my grandfather put it best, when I asked him what he thought about how BP and the US is responding to the spill.

“They’re friggin’ idiots.”

My grandfather, Ralph Bianchi, knows a thing or two about oil spills. He spent thirty years in the oil spill cleanup business. His company, JBF Scientific (now a part of Slickbar), developed new technologies for cleaning up spills, including a skimming method called the Dynamic Inclined Plane (DIP). In 1970, they sold their first skimmer to the U.S. Environmental Protection Agency. The next year, the U.S. Navy purchased forty $250,000 DIP skimmers and stationed them at major naval installations throughout the world. When word of how well his designs worked for the government, private oil companies started buying DIP skimmers, too.

In 1987, my grandfather’s company, JBF Scientific, received a call from the Alyeska Pipeline Service Company. The company, based in Alaska, was formed in 1970 and charged with the duty of designing, constructing, operating and maintaining the pipeline which transports oil from the fields in Alaska. It is owned by the major oil companies that operate the Trans-Alaska Pipeline System, including a couple you may have heard of: BP and Exxon Mobil.

The DIP Skimming System

Part of Alyeska’s job is to clean up any spills which occur in the process of the movement of oil to, from and through the pipeline. What they wanted from my grandfather was a DIP skimmer larger than he’d ever constructed – a boat over 120 feet long. JBF drew up plans for a massive DIP skimmer capable of removing 2,500 barrels of oil per hour. But when my grandfather told them how much it would cost – an estimated $4 to $5 million at the time – Alyeska instead decided to try another company’s cheaper model, which turned out to be close to useless in the kelp-filled waters of the Northwest.

Of course, everyone knows what happened next. In 1989, the Exxon Valdez ran aground on Prince William Sound’s Bligh Reef and spilled an estimated 250,000 barrels of crude oil, creating one of the worst environmental disasters in history. The spill itself was bad enough, but Alyeska, Exxon and the country were entirely unprepared to deal with a cleanup of that nature. Despite months of cleanup efforts, less than 10% of the spilled oil was recovered, and 20 years later, the ecosystems in the area had still yet to recover.

After the spill, Alyeska bought my grandfather’s skimmer. The boat, called the Valdez Star, still operates in that area today. If another spill the size of the Exxon Valdez occurred now, picking up that volume of oil would only be a few days’ work for the Valdez Star and two aluminum oil recovery boats the company also bought. Only a few days work.

If only the cooperative in Alaska had been willing to spend a little more on their cleanup equipment! Other areas, however, were and are much better about their cleanup planning. One of the first privately owned groups to embrace the DIP skimmers was the oil cooperative in Puget Sound. Puget Sound and the Northwest Straits are among the busiest shipping lanes in the world, with billions of gallons of oil moving across the waters of Puget Sound every year. The Sound may have many environmental issues, including stormwater runoff and pollution, but it kicks butt at cleaning up oil spills.

Despite the fact that oil spills occur there fairly frequently, you don’t hear about them much. That’s because in Puget Sound, they have what my grandfather calls a “firehouse mentality.” The cooperative bought the first privately owned DIP skimmer, The North Sounder, from JBF in the late 1980s. After the Exxon spill, they purchased three more similar skimmers, and a 600 ton skimmer like the Valdez Star called The Shearwater. These skimmers are among a fleet of equipment and trained personnel ready at a moment’s notice to deal with any spill. They run drills to practice different methods of cleanup. They know the currents and wind data and predict where and when the oil will hit. They’ve identified sensitive shore areas like shell fish beds, bird feeding and nesting ground and yachting harbors, and have stationed containment and deflecting booms, storage barges, and skimmers at those areas. And all of it is funded by the state and the oil companies and other shippers whose oil could be spilled. In Washington, the state Ecology Department has a budget of $16 million, while companies spend roughly $41 million a year there preparing for spills.

Oil spill cleanup using my grandpa’s technology in 1972; my uncle Robert Bianchi on the left, a family friend Mark Mendano in the center, and my uncle Raimond Bianchi on the right.

In Puget Sound, when a spill happens, they jump into action. Just like firefighters responding to an alarm, trained teams of workers immediately assess the situation and combat the spreading problem. They contain the oil if they can, and if they can’t, they protect the areas that are most vulnerable to oil’s damaging effects. Similar oil cleanup crews are now in place in a number of harbors around the country.

So I asked my grandfather how many skimmers he sold to companies in the Gulf.

“None.”

BP now claims that 400 or so skimmers are now working to clean up the oil spilling in the gulf. One of their spokesmen, Mark Proegler, says skimmers are only able to collect about 10-15 percent of the oil. “They essentially scoop up the oil and water mix in the water for later separation,” he explained, “and that mix is about 10 percent oil and 90 percent water.”

But that’s because they aren’t using DIP skimmers, or other, better skimming technologies that have been developed over the past few decades. The resultant oil percentage of the fluids that are picked up by these skimmers is more than five times higher. When deciding how well prepared an area is for an oil spill, the government tends to operate on a 20% rule of thumb (33 CFR 155, Appendix B, Section 6) – that is, they assume that any skimmer will operate at only 20% the efficiency that the manufacturer claims. For JBF DIP models, however, they assume 74% to 94% efficiency.

What my grandfather wants to know is why the Valdez Star and the Shearwater, as well as the other large, high-quality skimmers, aren’t in the Gulf right now. Better boats are out there, which could clean up more oil and faster.

It’s not just that BP and other Gulf companies hadn’t embraced the newer, better cleanup technologies before this disaster occurred. It’s that they aren’t prepared at all for any kind of large spill. That’s what the US government discovered when they performed exercises in the early 2000s to see how companies would respond to a major spill. The After Action report of the 2004 Spill of National Significance (SONS) exercise concluded that, in the Gulf of Mexico:

Oil spill response personnel did not appear to have even a basic knowledge of the equipment required to support salvage or spill cleanup operations…. There was a shortage of personnel with experience to fill key positions. Many middle-level spill management staff had never worked a large spill and some had never been involved in an exercise.

What’s even more sobering is that of the oil spills within the Coast Guard’s jurisdiction (i.e., marine and coastal areas), approximately 50% of the incidents, both in number and the volume of oil spilled, occur in the Gulf of Mexico and its shoreline states.

Why doesn’t the Gulf have the “firehouse mentality” of areas like Puget Sound? Why haven’t they identified the most vulnerable areas and stationed cleanup equipment there, provided up to date training for cleanup personnel, and generally prepared for this kind of disaster?

The answer is simple. As my grandpa phrased it, “they’re cheap bastards.”

The lack of foresight and constant corner cutting by BP led to this disaster. But what’s worse is that they continue to botch the containment and cleanup of the billions of gallons of oil that their mistakes have spilled.

“The real issue,” my grandfather explained to me, “is that they don’t care about solving the problem.” By they, he wasn’t just referring to BP. He was referring to all of the oil companies in the Gulf and the government regulators that are supposed to be ensuring that oil drilling and transport occurs safely. “They throw dispersants on the oil. Do you know what dispersants do? They make the oil neutrally buoyant. Dispersed oil winds up in the water column and, therefore, cannot be deflected by floating booms or harvested with oil skimmers. They make the surface look cleaner, but they don’t do a damned thing to actually clean up the oil.”

Essentially, dispersants are soaps. They emulsify oil, breaking up up and allowing it to mix into water. The idea behind dispersants is that by breaking up the oil and putting it in the water column, it will be degraded faster by the microorganisms that naturally degrade oils and keeping the oil from coating the shoreline.

Starting in May, the US has been spraying oil dispersants at the spill like mad, despite concerns raised by many related to potential dispersant impact on wildlife and fisheries, environment, aquatic life, and public health. The EPA further approved injection of these dispersants directly at the the leak site to break up the oil before it reaches the surface. By the end of may, over 600,000 gallons of dispersants have been applied on the surface, with another 55,000 gallons applied underwater. The two main dispersants being used, Corexit EC9500A and EC9527A are neither the least toxic, nor the most effective, among the dispersants approved by the Environmental Protection Agency. In fact, the UK has banned their use entirely. When BP was asked why they aren’t using better dispersants, they said that Corexit was ‘what they had available.’

The bigger question, though, is why are they using dispersants at all. Multiple studies after the Exxon Valdez spill found that dispersants, detergents, and hot water cleaning of shoreline cause substantially more mortality than oil itself. Even before the Exxon spill, scientists knew that “dispersant-oil mixtures are more toxic than the dispersant alone, and many-fold more toxic than the crude oil.” While better and safer detergents are being developed, their long-term toxicity and effectiveness is still completely unknown, making them risky to use in such high quantities as BP is.

The way my grandpa sees it, the so-called cleanup of the Deepwater Horizon Oil Spill isn’t about being effective or safe, it’s about looking like they’re doing something. The goal is to make it less visible so the public forgets that it’s happening. It’s all about PR.

I think he’s right.

What needs to happen, in the Gulf of Mexico and throughout the United States, is a change of mindset. We’ve already started moving away from oil to other, more responsible and sustainable energy technologies, but that is only a small part of the solution. The truth is, we’re likely never going to have a zero demand for oil. We certainly won’t do it in the next fifty or a hundred years – it’s just not feasible. While we need to continue to research alternatives, we need to deal with how we handle and regulate oil now, too.

Oil companies have been taking advantage of loose regulations for too long. They need to be forced to prepare for the damage their products can cause. You would think that after the disaster in Alaska that we would have learned our lesson – that anywhere where oil is drilled, pumped or transported would have put in place well trained emergency response teams and extensive equipment ready to react to large spills. But apparently, we haven’t learned from our mistakes. This time, I hope that we do.

This post has been chosen as a Research Blogging Editor’s Selection, featured in the 33^rd edition of Scientia Pro Publica, and now won the Post with the Most!

PS: For amazing coverage of the oil spill in general, check out my blog-buddies over at Deep Sea News and the growing list of fantastic posts/feeds/etc from Southern Fried Science

Citations:

Jonathan L. Ramseur (2010). Oil Spills in U.S. Coastal Waters: Background, Governance, and Issues for Congress Congressional Research Service , 7-5700 (RL33705)
USCG Spill Compendium (2005). Cumulative Data And Graphics For Oil Spills (1973-2004)
Ralph A. Bianchi, Edward E. Johanson, & James H. Farrell (1973). The Application of Skimmers, Piston Films,and Sorbents for Open Water Spills Offshore Technology Conference
U.S. Department of Homeland Security, & U.S. Coast Guard (2004). California SONS 2004 After Action Report
Paine, R., Ruesink, J., Sun, A., Soulanille, E., Wonham, M., Harley, C., Brumbaugh, D., & Secord, D. (1996). TROUBLE ON OILED WATERS: Lessons from the Exxon Valdez Oil Spill Annual Review of Ecology and Systematics, 27 (1), 197-235 DOI: 10.1146/annurev.ecolsys.27.1.197
SWEDMARK, M., GRANMO, A., & KOLLBERG, S. (1973). Effects of oil dispersants and oil emulsions on marine animals Water Research, 7 (11), 1649-1672 DOI: 10.1016/0043-1354(73)90134-6
CM Tarzwell (1971). Toxicity of oil and oil dispersant mixtures to aquatic life. Water pollution by oil. London, The Institute of Petroleum. P. Hepple (Ed.) , 263-272

Parasite Insights: Using Lice To Map Socialization

Weighing in at only 40 grams, brown mouse lemurs are one of the smallest species of primate in the world. Their diminutive size as well as their nocturnal, tree-dwelling lifestyle makes them difficult to track and observe. It would have been completely understandable if Sarah Zohdy, a graduate student at the University of Helsinki, had simply given up her quest to understand the social structure of these elusive creatures — but she didn’t. Instead, she and her colleagues came up with an ingenious way to study the interactions of these small lemurs: they followed their lice.

mouse lemur and lice — A mouse lemur and a close-up shot of lice on its ear. Photos by Sarah Zohdy

For as long as there have been mammals, there have been lice. Though it’s hard to find lice in the fossil record, scientists have estimated that the group originated at least 130 million years ago, feeding off feathered dinosaurs, though they now live on just about all species of birds and mammals. Lice tend to be very host-specific, meaning they only live and feed on one species or a set of closely related species. Furthermore, lice can only survive a limited time without their hosts, and must quickly find a new one if they leave or are forcibly removed. This means that for lice to reproduce and spread, their hosts have to be in fairly close contact (like, as many parents know, kids in a kindergarden classroom). In wild species, lice rarely switch hosts unless the animals interact physically, whether through wrestling, nesting together or mating.

It was that requirement for close contact that made Zohdy and her colleagues think they might be an ideal proxy for investigating social interactions that can’t be viewed directly. They had already been collecting data on the mouse lemur populations in Madagascar using traps to monitor their movement. But while the researchers knew certain lemurs spent a lot of time together if they were caught together in traps, the researchers figured they were probably missing a good amount of social interaction. So, they decided to follow the lemur’s lice as well.

Mouse lemurs are parasitized by a particular species of louse, Lemurpediculus verruculosus, which feed off the lemurs’ blood. The researchers were able to track the transfer of these lice between lemurs by tagging lice with a unique color code using nail polish, so they could tell what lemur each louse started on. Over time, they continued to trap lemurs and look at their lice to see if any of the tagged ones had switched hosts.

In total, they tracked 76 transfers between 14 animals — all males — over the course of a month, which happened to be during the breeding season. The researchers hypothesized that the male-only transfers likely occurred during fights over females. But perhaps more interestingly, the lice data only supported 8 of the 28 expected social interactions predicted by trapping data, and found 13 new ones, suggesting the louse marking technique was able to uncover lemur social activity that the researchers have never observed. They also found that some animals shared more lice than others. Sarah Zohdy explained, “The youngest male in the study had the worst louse infestation, but only donated one louse, indicating a low number of interactions, while the eldest male, who also had a heavy infestation, appeared to be more sociable, collecting lice from many donors. Other males appeared to be ‘superspreaders’ donating but not collecting lice.”

The lice also revealed that lemurs travel more than the researchers had thought. “Most of the louse transfers occurred between lemurs over 100 m from each other, and one transfer spanned over 600 m,” the authors write. “The transfers therefore demonstrate a degree of lemur ranging far greater than anticipated.”

Overall, these data provide new insights into the social interaction of mouse lemurs as well as the relationship between the lice and their hosts. This isn’t the first study that used lice to look at a bigger scientific picture. Because of their host-specific nature, scientists have used them to map ancient speciation events, and even determine when humans first wore clothes. But never before have lice been used to study behavior in a living wild species, though the team hopes their study shows the usefulness of this technique. “The approach developed here has potential for application in any species parasitized by sucking lice, including the many trappable species of cryptic, nocturnal, subterraneous or otherwise elusive mammals in which host social contact and parasite exchange data are difficult to obtain.”

Reference: Zohdy S., Kemp A.D., Durden L.A., Wright P.C. & Jernvall J. (2012). Mapping the social network: tracking lice in a wild primate (Microcebus rufus) population to infer social contacts and vector potential., BMC ecology, PMID: 22449178

Native Hawaiians Provide Lessons In Fisheries Management

Roughly three-quarters of the Earth’s surface is covered with water. As I stand on a beach in Hawaii and look out over the vast, blue expanse in front of me, I am overwhelmed by the immensity of the Pacific Ocean. My brain wrestles with numbers far beyond its capacity to visualize. In that moment, it is incomprehensible that even seven billion humans could deplete such a boundless and unimaginable resource. Yet, I know that we are. We are emptying the oceans of their fish, one species at a time.

Today, 85 percent of the world’s fisheries are either fully exploited, overexploited or have already collapsed. Combined, the world’s fishermen catch 2.5 times the sustainable number of fish every year. Scientists predict that if current trends continue, world food fisheries may collapse entirely by 2050. “We are in the situation where 40 years down the line we, effectively, are out of fish,” explains Pavan Sukhdev, special advisor to the UN Environment Programme.

What we need are better management strategies. Now, researchers from the Center for Ocean Solutions at Stanford University are turning to the past for advice. Loren McClenachan and Jack Kittinger used historical records to reconstruct fish catches for the past seven hundred years to see if earlier civilizations did a better job than we are at managing their fisheries. The authors were able to characterize historical catch rates in the Florida Keys and Hawaii by reviewing a variety of historical sources, including species-specific catch records from the 1800s and archaeological reconstructions of population densities and per-capita fish consumption.

“Seven hundred years of history clearly demonstrate that management matters,” said Loren McClenachan, co-author of the study and assistant professor of environmental studies at Colby College. In Florida, fisheries were characterized by years of boom and bust through sequential collapse of high-value species, many which are still endangered or extinct today. The Keys fisheries were set up for failure – unlike other historical island communities, the Keys were highly connected to other markets, increasing fisheries demand. Furthermore, they have historically lacked a centralized management system. But, while fisheries in the Florida Keys have always been poorly supervised, fisheries in Hawaii were once far better than they are today.

fisheries_catch_historical_hawaii_Florida — Annual fisheries catch per reef area for the Florida Keys and Hawaii over time.

“Before European contact, Native Hawaiians were catching fish at rates that far exceed what reefs currently provide society,” said Kittinger, co-author and early career fellow at the Center for Ocean Solutions. Native Hawaiians pulled in over 15,000 metric tons of fish per year, and these high yields were sustained over several hundred years, despite a dense Hawaiian population. “These results show us that fisheries can be both highly productive and sustainable, if they’re managed effectively.”

Much of the management system in Hawaii was tied to class and gender. For example, most offshore fishing was done by a professional fishing class who were familiar with their local environment. If they wanted to fish, they had to ask their chiefs, who regulated the fishing gear and canoes. The most valuable (and vulnerable) species like turtles and sharks were reserved for high chiefs and priests, reducing fishing pressure.

The key to the Hawaiian’s success lay in using a diverse suite of management measures. Many of the methods they used are similar to strategies employed in fisheries management today, including protected areas, community-based management, regulation of gear and effort, aquaculture, and restrictions on vulnerable species.

Perhaps the greatest difference between management then and now, however is that in native Hawaiian society, rules were strictly enforced. “Rules were accompanied by robust sociocultural institutions,” the authors write. The ancient Hawaiians did not hesitate, and punished transgressors with corporal punishment. “Clearly, we don’t recommend this,” said Kittinger, “but it’s easy to see there’s room to tighten up today’s enforcement efforts.”

He’eia Fishpond in Kane’ohe Bay, Hawaii. Image c/o Paepae O He’eia

Other differences exist as well. For example, while aquaculture was used by the native Hawaiians, these fishponds were maintained for different reasons than we farm fish today. Fishponds did not contribute substantially to total fish production, but instead served as food security during tough times. As such, Hawaiians stocked fishponds with very different species than modern farms. Fishponds contained small, algae-eating species, requiring little from the sea to support them. Modern aquaculture, in contrast, relies heavily on wild-caught feeder species to support lucrative, luxury species like salmon. Five pounds of wild-caught fish are needed to produce one pound of farmed salmon, and instead of acting as a backup for when wild fish are scarce, fish farms make up a whopping 50% of our consumed fish production.

Kittinger and McClenachan hope that understanding successful management strategies by historical societies will lead to better management of our current resources. “The evidence we present from historical reconstructions shows that reef fishery sustainability has been achieved in the past,” they write, “which can guide actions for a more sustainable future for reefs and the communities that depend on them.”

Reference: McClenachan, L & JN Kittinger (2012). Multicentury trends and the sustainability of coral reef fisheries in Hawai‘i and Florida. Fish and Fisheries, doi: 10.1111/j.1467-2979.2012.00465.x

Image of fishing c/o Flickr user dennistanay

Sexually deprived Drosophila become bar flies

“He caresses every bottle like it’s the first one he’s had, saying it ain’t love, but it ain’t bad.”

– Ani DiFranco

Rejection stinks. It literally hurts. But worse, it has an immediate and negative impact on our brains, producing withdrawal symptoms as if we’re quitting a serious addiction cold turkey. It’s no wonder, then, that we are tempted to turn to drugs to make ourselves feel better. But we’re not the only species that drowns our sorrows when we’re lonely – as a new study in Science reveals, rejected Drosophila do, too. Scientists have found not only will these sexually frustrated flies choose to consume more alcohol than their happily mated peers, sex and alcohol consumption activate the same neurological pathway in their brains.

Drosophila melanogaster males sure know how to woo a lady. When placed in the same container as a potential mate, a male fly will play her a delicate love song by vibrating one wing, caress her rear end, and gently nuzzle her most private of parts with his proboiscis to convince her that he is one heck of a lover. But even the most romantic fly can’t convince an already mated female Drosophila to give up the goods, so scientists were able to use the girls’ steely resolve to see how rejection affects fly drinking behavior.

“Alcohol is one of the most widely used and abused drugs in the world,” explains lead author Galit Shohat-Ophir. “The fruit fly Drosophila melanogaster is an ideal model organism to study how the social environment modulates behavior.” Previous studies have found that Drosophila melanogaster exhibit complex addiction-like behaviors. So in the controlled setting of Ulrike Heberlein’s lab at the University of California San Francisco, researchers paired male fruit flies with three types of females: 1) unmated females, which were willing and happy to mate; 2) mated females, which actively rejected the men; and 3) decapitated females, which didn’t actively reject the guys but, well, weren’t exactly willing partners either. After the flies were satisfied or frustrated, they were offered regular food and food spiked with ethanol, and the researchers measured which type they preferred to see if there was any connection between sex and drinking.

The flies that were rejected drank significantly more than their satisfied peers, but so did the ones paired with incapacitated girls, suggesting that it wasn’t the social aspect of rejection but sexual deprivation that drives male flies to increase their ethanol consumption (see the video at the end!). This alcoholic behavior was very directly related to the guy fly ever getting laid, for even after days of blue balls, if he was allowed to spend some time with a willing woman, he no longer preferred the spiked food.

What the scientists really wanted to understand, though, was why. What drives a frustrated fly to the flask? So to look at the underlying mechanism of this phenomenon, the scientists examined the flies’ brains. A body of scientific literature has connected one particular neurotransmitter, neuropeptide F (NPF), to ethanol-related behaviors in Drosophila, so it was a logical place to start. A very similar neurotransmitter in our brains, called neuropeptide Y (NPY), is linked to alcoholism.

Screen Shot 2012-03-13 at 12.03.14 AM — Increased expression of NPF in mated male brains, as shown through immunochemistry.

The team found that sexual frustration caused an immediate decrease in the expression of NPF, while sex increased expression. Furthermore, when they used genetics to artificially knock down NPF levels in the satisfied flies, they drank as much as their not-so-satisfied friends. Similarly, when the researchers artificially increased NPF levels, flies stayed sober. This is the first time NPF levels have connected sexual activity to drinking. Clearly, NPF levels controlled the flies’ desire to drink, so the team further explored how NPF works in the fly’s brain.

Many animals, including ourselves, possess a neurological reward system which reinforces good behavior. Through this system, we ascribe pleasure or positive feelings to things we do that are necessary for species survival, including sex, eating, and social interaction. Drugs tap into this system, stimulating pleasure which can lead to addiction. Previous studies have shown that flies find intoxication rewarding, so the researchers hypothesized that NPF may play a role in the reward system.

Preference tests showed that artificially increasing NPF levels in the absence of sex or ethanol was rewarding to the flies, confirming the scientists’ hypothesis. This was further supported by the discovery that constantly activating NPF abolished the flies’ tendency to consider ethanol rewarding.

“NPF is a currency of reward” explains Shohat-Ophir. High NPF levels signal good behavior in Drosophila brains, thus reinforcing any activities which led to that state. This is a truly novel discovery, for while NPF and the mammal version, NPY, have been linked to alcohol consumption, no animal model has ever placed NPF/NPY in the reward system.

Understanding the role of NPF in reward-seeking behaviors may lead to better treatments for addicts. “In mammals, including humans, NPY may have a similar role [as NPF],” says Shohat-Ophir. “If so, one could argue that activating the NPY system in the proper brain regions might reverse the detrimental effects of traumatic and stressful experiences, which often lead to drug abuse.” Already, NPY and drugs that affect the function of its receptors are in clinical trials for anxiety, PTSD, mood disorders and obesity. This study suggests that perhaps they should be tested as treatment for alcoholism, too, as well as other reward-based addictions.

Research: Shohat-Ophir, G, KR Kaun & R Azanchi (2012). Sexual Deprivation Increases Ethanol Intake in Drosophila. Science 335: 1351-1355.

Flies turn to drinking after sexual refusal

This sequence of three videos shows a male fly courting and successfully mating with a female fly, another male fly being rejected by a female, and a male choosing to consume an alcohol-infused solution over a non-alcohol solution. Video © Science/AAAS

Images:

Fruit fly from Wikimedia Commons, posted by Thomas Wydra, edited in Photoshop.

Immunochemistry reproduced from Shohat-Ophir, G, KR Kaun & R Azanchi. Science 335: 1351-1355 (2012).

Hydra Watch What They Eat

Upon first glance, hydra seem like remarkably simple creatures. The basic description of a hydra would be a tube closed at one end with tentacles surrounding a mouth on the other, made of fragile tissue that can be as slim as two cells thick. No gills, no heart, no brain, no eyes – of course, it would be hard to pack all those organs into a creature a few millimeters long, and hydra certainly seem to do well enough without them. These small relatives of jellyfish are found worldwide, and are some of the only members of the phylum Cnidaria to be found in fresh water.

Yet their modest body plan is misleading. Hydra have fascinated scientists for centuries, for they have a phenomenal capacity to regenerate and may even be immortal. In 1744, Swiss naturalist Abraham Trembly was one of the first to be entranced by these simple animals and reflected, “It seemed to me from the start of my observations that knowledge of the remarkable properties of the polyps could bring pleasure to the inquisitive and contribute something to the progress of natural history.”

The hydra’s simple nature is also belied by their tentacles, which inject a potent neurotoxin into unsuspecting prey using extremely sophisticated cells called cnidocytes. For decades, scientists have sought to understand how these specialized attack cells are triggered. Now, evidence published in BMC Biology suggests these primitive creatures may ‘see’ more than we realized, as the firing of these prey-catching stinging cells is regulated by the same chemical pathway used in our eyes.

Ever since the genome for Hydra magnipapillata was published in 2010, it was known that hydra possess the genes for opsins, the photosensitive protein family found in all animals that can see, but no one knew exactly what they do with them. Unlike other animals, hydra don’t have eyes or eye spots, or any kind of centralized visual sensory area, although they have behavioral responses to light. When David Plachetzki teamed up with Caitlin Fong and Todd Oakley’s lab at UC Santa Barbara, they found that these light-sensitive proteins were clustered on the hydra’s tentacles and around the hydra’s mouth, suggesting that they might be involved in feeding behavior.

fluorescent hydra tentacle — Fluorescent picture of hydra tentacle bulbs; Musculature is stained green, neurons, including cnidocytes, are stained red and nuclei are stained blue

In hydra, potent stinging cells are grouped with other neurons in what are called “battery complexes” on the hydra’s tentacles, forming one of the most intricate systems of neurons in an organism that lacks a central nervous system. Using fluorescent molecular probes, the researchers were able to show that opsins are expressed in the same locations. They also discovered that other proteins that are part of the response to light, cyclic nucleotide gated (CNG) ion channel and arrestin, are found in these battery complexes, too. In other words, the stinging arsenals are completely equipped to react to changes in light.

Just because they have the parts, however, doesn’t mean they use them. So to see if the stinging cells themselves, the cnidocytes, are regulated by light, the researchers exposed hydra to LED lights of different intensities, then prodded the animals’ tentacles with gelatin-coated fishing wire as if they were being touched by potential prey. After, the team was able to count how many cnidocytes were embedded in the line as a way of measuring whether the stinging cells were triggered.

They found that bright light decreased the firing of stinging cells – which makes sense, really. “Cnidocytes are expensive to make for a hydra; a significant proportion of their cellular mass is comprised by these cell types. Therefore, it is important these austere animals to discharge them in an economical manner,” explains Plachetzki. Hydra and their relatives in the phylum Cnidaria are known to feed in daily patterns, becoming especially active at dawn or dusk, so it’s logical that they would be less inclined to feed in bright light, which might be perceived as day. Of course, there is an even more straightforward explanation as to why cnidocytes fire when the lights go out – shadows. “It could be that hydra use this sensory function to detect the shadows cast by prey on feeding tentacles, just when the moment is right to strike.” The researchers were able to directly connect the opsin signaling cascade to this change in feeding behavior by introducing a blocker of opsin signaling, cis-diltiazem. In the presence of the blocker, light had no affect, confirming that opsin-based signaling is required for this light-mediated change in cnidocyte firing.

Since hydra have been extensively studied for centuries, it is a bit surprising that we are only now learning how light affects their feeding. “It is strange that nobody had discovered this before,” remarked Plachetzki. “Folks have been playing around with hydra and their photobehavior for greater than 200 years, why didn’t they notice this?” But, he says, when you look at some of the older observations of these creatures, “you get the impression that others might have had this hypothesis as well, but there were until now never any data to support it.”

These findings reveal one of the earliest uses of the chemical pathways that were co-opted to create vision. By learning more about these signaling cascades, we can begin to glimpse back at the very beginnings of sight, and slowly learn more about the evolutionary steps that led to our eyes. Aside from the interesting evolutionary implications, this research may also lead to more direct benefits to humans. Cnidarians, including hydra, jellies and corals, are responsible for tens of thousands of stings every year, a handful of which are fatal. The more we know about how these stinging cells are triggered, the better we can prevent these stings, or even develop a way of protecting swimmers against them.

Reference: David C Plachetzki, Caitlin R Fong and Todd H Oakley (in press). Cnidocyte discharge is regulated by light and opsin-mediated phototransduction. BMC Biology

Social Media for Scientists Part 4: On The Road

A couple weeks ago, I braved the freezing north to speak at the University of Washington for a workshop focusing on Social Media for Scientists. The event was co-sponsored by AFSUW, Washington Sea Grant, and COSEE OLC as a part of the Beyond the Ivory Tower series, a set of free public lectures that hopes to provide researchers with tools and techniques to reach audiences and broaden the impacts of their work. I was teamed up with the effortlessly incredible Liz Neeley, COMPASS’ super ninja of science communication, to try and convince a room full of hardy Seattle scientists that, indeed, every lab should tweet.

I truly do believe that Facebook, Twitter, and other social media are essential for every scientist to use. Not only are they the communication platforms of the future, they hold the potential to revolutionize how we do science in the first place. It seems foolish at best that in scientific circles we deride the use of these networks that, literally, two thirds of the world’s population are connecting through. I’ve laid out the arguments before (see the post list below), and will surely continue to talk about this topic until I go hoarse. Simply put, it’s not a question that scientists need to increasingly engage with new media platforms to stay relevant in this digital age. The question is how.

For that, I’m going to point you toward the freshly launched Social Media for Science Google+ Page and the workshop wiki, which is an evolving collection of information and resources, as well as the Storify of the afternoon by Jessica Rohde. You can also download my slides from slideshare, or watch the video of my talk:


Science and Social Media--Christie Wilcox from AFSUW on Vimeo.

More Social Media for Scientists:

Who said cells aren’t romantic?

Happy Valentine’s Day!

From: Heinz Kutzner (2001). For Valentine’s Day: Epithelial Sheath Neuroma Cancer, 91 (4)

Darwin’s Degenerates – Evolution’s Finest | Observations

153 years ago on November 24th a naturalist named Charles Darwin published a book with a rather long and cumbersome title. It was called On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life (for its sixth edition in 1872, the title was cut short to simply The Origin of Species, which was found to be much more manageable to say in conversation). It was inspired by an almost five year journey around the world on a ship named for a small, floppy eared canine during which Darwin did his best to catalog and understand geology and the diversity of life he found.

It’s incomprehensible, now, to think of someone writing a single volume that could equally change science as we know it. The two simple ideas that Darwin fleshed out in his first publication were earth shattering at the time. He has since been called both a genius and a heretic for these two theories – both titles equally deserved. But whatever you call him, his vision has changed the world irrevocably. Today, on what would have been his 203 birthday, we celebrate the life and scientific contributions of this man. In honor of the occasion, I am reposting my first Darwin Day post ever, from way back in 2009. Enjoy!

If I ask you what group of organisms is an exhibition of evolution at its finest, what would you say? Most people, I think, would say human beings, or at least apex predators. After all, we have staggering intellect compared to our prey items and clearly dominate the planet, eat what we will, etc. Not only that, we’re insanely complex. Ask some scientists, and they might give you any number of answers. Cockroaches are likely to exist long after we do, as are rodents, so maybe they get the title. Or, being scientists, they might be biased to whatever organism they study. Maybe algae and plants, as the sustenance for all other life. But all of you, in my humble opinion, are wrong. That is, unless you choose parasites.

It’s ok if you don’t believe me yet. Darwin wouldn’t have, either. He and his contemporaries viewed parasites as degenerates who, at best, violated the progressive nature of evolution. Even in The Origin of Species, Darwin refers to parasites as regressive instead of progressive. But truly, no group of species is a better choice for evolution’s finest.

An ant being attacked by a parasitoid phorid fly. Photo Credit: Bernardo Segura

First off, let’s talk numbers. Parasitism is the most popular lifestyle on earth – over 40% of all known species are parasitic, and the number of parasitic species rises daily¹. Sure, you might say, but they tend to be small. In that case, let’s talk biomass – weight, just to be clear. One group of parasites, the flukes, have been found to be equal in weight to fish in estuarine habitats, and three to nine times the weight of the top predators, the birds – estimates which are thought to be conservative for the earth as a whole². Though they’re largely ignored when we study food webs, they’ve been estimated to be involved in over 75% of inter-species interactions¹. Clearly, by the numbers, they are the most prolific and successful organisms on earth.

But even that is not why I would argue they are evolution’s finest. They, more than any other group out there, both exhibit extreme evolutionary adaptations and spur them onward in other species.

No matter how complex or how impressive any other species may be, it has parasites. We do – lots, actually. Every species we might hold as a masterpiece of evolutionary complexity cannot out maneuver their parasites. Not one. Even parasites, marvelous as some are, have parasites – like a crazy russian doll. They have evolved amazing abilities to survive host defense systems, manipulate host behavior and boost heir own reproductive success. They’ve even been implicated in major cultural differences in people. It turns out that a rat parasite, Toxoplasma gondii, needs to be eaten by a cat to complete its lifestyle. Somehow it developed a trick to make rats unafraid of cat smells. When it accidentally ends up in people, it does the same kind of mind-altering, making people more guilty and insecure, even more frugal, mild-tempered, and complacent³. Other parasites do far more intricate manipulations of behavior, turning males into females, creating walking zombies, even forcing suicide. If parasites can not only break into and survive the most complex assortments of systems available, even with modern medicine fighting against them, and manipulate those complex organisms to slave to their bidding, how can we not credit them as masters at what they do?

But even more impressively, I would argue, is that no other group has so dramatically impacted how other species have evolved. They don’t just affect their hosts immune systems, either. If you read much into evolutionary theory, you realize it’s riddled with parasites. Why are some birds very colorful? Oh, because if they’ve got a lot of parasites they can’t be, so it’s a signal of a healthy male⁴. Why are we attracted to certain people? Because their immune genes are different from ours, giving our children the best chance to fight off the next generation of parasites. Almost everywhere you look, evolutionary changes are spurred on by parasites. It’s even suggested that sex itself evolved as a response to parasites. It’s a way of better shuffling our genes so that we have better odds at fighting off parasites.

Even we, as “ideal” or “complex” as we are, owe much to parasites. Some even argue that we are worse off without them. The argument, as it goes, is that our immune system evolved in the presence of unkillable parasites, particularly the parasitic worms. These worms, or Helminths as they are called as a group, were too costly to try and eradicate. Attacking foreign invaders, after all, is energetically expensive, and always runs the risk of over-activating our immune system, leading to self-inflicted injuries and diseases. So the best strategy, instead, was to have an immune system that functioned optimally against other issues, like the fatal viruses or bacteria, despite the mostly benign worm infections⁵. Since worms secrete anti-inflammatory compounds to fight off our defenses, we were better off with systems that overcompensated for that. Now, since we have drugs which kill them off, our immune system is out of balance. Many cite the rising rates of auto-immune and inflammatory diseases like allergies, arthritis, irritable bowel, type 1 diabetes, and even cancer in developed nations as evidence that ridding ourselves of helminths has damaged our health⁶. They’re backed up with multiple studies that show unexpected results, like that mice genetically predisposed to diabetes never develop it if infected with flukes at an early enough age.⁷

Parasites are uniquely capable of out-evolving their hosts and adapting to whatever changes go on in them. Simply put, they evolve better. They change their genes faster and keep up with a barrage of host defense systems, often like it’s effortless, spurring onward dramatic changes in other species. If Darwin had only known how amazingly complex the barriers these creatures have to overcome and the extent to which they have affected the species he’d encountered on his travels, he would not have labeled them “degenerates”.

As far as evolution is concerned, no group of species demonstrates it, causes it, and is so capable of it as the parasites. While disgusting or even cruel, they are truly evolutionary masterpieces. So while you may find them vile or detestable, you have to admit they’re good at it. Can you really argue that some other group is more deserving of the title of Evolution’s Finest?

Cited:
1. A. Dobson, K. D. Lafferty, A. M. Kuris, R. F. Hechinger, W. Jetz (2008). Colloquium Paper: Homage to Linnaeus: How many parasites? How many hosts? Proceedings of the National Academy of Sciences, 105 (Supplement_1), 11482-11489 DOI: 10.1073/pnas.0803232105
2. Armand M. Kuris, Ryan F. Hechinger, Jenny C. Shaw, Kathleen L. Whitney, Leopoldina Aguirre-Macedo, Charlie A. Boch, Andrew P. Dobson, Eleca J. Dunham, Brian L. Fredensborg, Todd C. Huspeni, Julio Lorda, Luzviminda Mababa, Frank T. Mancini, Adrienne B. Mora, Maria Pickering, Nadia L. Talhouk, Mark E. Torchin, Kevin D. Lafferty (2008). Ecosystem energetic implications of parasite and free-living biomass in three estuaries Nature, 454 (7203), 515-518 DOI: 10.1038/nature06970
3. Kevin D. Lafferty (2006). Can the common brain parasite, Toxoplasma gondii, influence human culture? Proceedings of the Royal Society B: Biological Sciences, 273 (1602), 2749-2755 DOI: 10.1098/rspb.2006.3641
4. Jesús Martínez-Padilla, François Mougeot, Lorenzo Pérez-Rodríguez, Gary R. Bortolotti (2007). Nematode parasites reduce carotenoid-based signalling in male red grouse Biology Letters, 3 (2), 161-164 DOI: 10.1098/rsbl.2006.0593
5. Joseph A. Jackson, Ida M. Friberg, Susan Little, Janette E. Bradley (2009). Review series on helminths, immune modulation and the hygiene hypothesis: Immunity against helminths and immunological phenomena in modern human populations: coevolutionary legacies? Immunology, 126 (1), 18-27 DOI: 10.1111/j.1365-2567.2008.03010.x
6. Joel V. Weinstock, David E. Elliott (2009). Helminths and the IBD hygiene hypothesis Inflammatory Bowel Diseases, 15 (1), 128-133 DOI: 10.1002/ibd.20633
7. Anne Cooke (2009). Review series on helminths, immune modulation and the hygiene hypothesis: How might infection modulate the onset of type 1 diabetes? Immunology, 126 (1), 12-17 DOI: 10.1111/j.1365-2567.2008.03009.x