Barnacle Evolution: A Tribute to Alan J. Southward (1928-2007)

Its a brand new year! Thats means I get to have 2008 in my Endnote catalogue! So what was the first paper of the year that I downloaded?

Perez-Losada, M., M. Harp, J. T. Hoeg, Y. Achituv, D. Jones, H. Watanabe, and K. A. Crandall. 2008. The tempo and mode of barnacle evolution. Molecular Phylogenetics and Evolution 46:328-346.

This was tempered by the news of the passing of one the world's great barnacle biologists, Alan J. Southward. I never got a chance to meet him, though I heard from several people he was great guy. The Liverpool Daily Post's obituary gives a brief example:

"At a more homely level, he was a kind and humorous man, white-haired and bushy-browed, who devoted his immense intellect to discovering more about simple creatures, which, though unseen and unsung, experience the precious gift of life on Earth."

But I have gotten known his research since 2003 when I became interested in stalked barnacles from hydrothermal vents at the East Pacific Rise. Relishing an opportunity to go on board a research expedition with a boat full of taxonomists (though I came with a small geology contingent), I saw for the first time in my life the stalked barnacle, Neolepas zevinae. Barnacles on stalks were a new concept for me. N. zevinae was described in 1979 by Bill Newman from Scripp's Institute for Oceanography. He is still alive and was a colleague of Dr. Southward. The poster below describes them well (from a newspaper by Sam Hinton in 1981).

Alan Southward was more than just a barnacle biologist. Like Charles Darwin, the foremost authority on barnacles, Dr. Southward studied biogeographic patterns and isolating barriers using barnacle distributions. He studied the damage to the marine ecosystem by pollutants in the 1950s, showing how long it took for ecosystems to recover. Additionally, he was one of the first to study the effects of environmental temperature increases on marine invertebrate fauna, way before global warming was a hotbed issue. Alan Southward worked with other marine organisms, most notably Pogonophorans, but limpets and fish as well as being an accomplished marine biologist. He worked 19 beyond his retirement, focusing heavily on hydrothermal vent organisms.

For further information about this naturalist who exemplified a lifetime of learning, I encourage you to look up his publications. I'm happy to provide some from my personal library too! Paul Dando, a researcher at the Marine Biological Station who worked with Dr. Southward, wrote an excellent obituary article in this week's Nature. It is well worth the read. With that being said, this post on barnacle evolution is dedicated to the memory of Alan J. Southward. Cheers!
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Lepas anatifera from Washington state, USA. Photo credit: David Cowles 1997.

Perez-Losada et al. (2008) published a MEGA barnacle data set using 3 nuclear genes and 44 morphological characters for 91 taxa in the superorders Thoracica and Rhizocephala. They rewrote barnacle evolution by rejecting some of the hypotheses that were the foundation for barnacle biology and systematic, while giving statistical and phylogenetic support for others and creating new hypotheses. This study forms the new basis for understanding barnacle evolution and basic biology. This has many implications for other fields. In particular, barnacles are the marine industry's most wanted. They foul docks, boats, and anything else with a part in the seawater, including other animals! Whales, sea turtles, other crustaceans and just about anything else can become a barnacle colonization substrate.

Though Linnaeus, and/or his students, certainly described barnacles, the real authority was Charles Darwin. He spent over 8 years cataloging, describing and monographing every barnacle he could get his hands on from every part of the world. This resulted in 4 comprehensive tomes that are still referenced and cited today. Darwin Online has the complete works freely available over the internet: Living Cirripedia Volumes 1 & 2 and Fossil Cirripedia of Great Britain Volumes 1 & 2. Darwin based much of his taxonomy on shell characteristics, though he certainly studied the internal "soft" parts.

The cirripede shell is formed by plates secreted by the cuticle. They are not molted, or shed, like in other arthropods but increase in size circumferentially and in height. The number of shell plates were traditionally hypothesized to increase from a thoracican ancestor with 4 or 5 plates during the course of evolution. Other groups in the Thoracica with more plates are thus more derived. It is uncertain to what the selective pressure was to develop different numbers of plates. Perhaps more smaller plates offer greater protection than fewer larger plates. What Perez-Losada et al. found out though was there were no clear patterns with plate enumeration. Clades with no plates are mixed in with clades with 5 plates, while a clade with more than 12 plates is sister to a clade with a last common ancestor that had no more than 7 plates. The theory of shell plate evolution is clearly debunked in this analysis, though they can say with some degree of certainty that the last common ancestor to the Thoracica had no more than 4 plates. Another interesting point is that asymmetry (Verrucomorpha) has evolved independently at least twice in the thoracican lineage. I believe this highlights the plasticity in biomineral characters, such as shell characteristics. This is seen in many molluscan clades where general shell characteristics are misleading, sometimes due to external parameters (erosion) and sometimes due to phenotypic plasticity in the mechanisms that construct biomineral structures. Thus, the soft parts and larval characteristics are more important (though often more difficult to study and they leave no fossil trace).

Figure 3 from Perez-Losada et al. (2008): "Thoracican divergence time chronogram estimated using the 50% majority-rule consensus BMCMC tree of morphological and molecular data under mix-models..." See paper for more details.

On a sytematic level they uncovered several polyphyletic clades, such as the Heterlepadomorpha (those that have no shell plates). This clade appears to have evolved at least twice, independently, and in both cases are more derived (within clades that have more than 5 plates) and a more recent radiation. The previously well established clades of the Verrucomorpha, Scalpellomorpha and Sessilia are no more, while the Iblomorpha and Balanomorpha have gained unequivocal support. One grouping that caught my attention is the clade below (magnified from above).


Especially everything under and including the clade marked 'Verrucomorpha (7s)'. All those barnacles - Neoverruca, Ashinkailepas, Vulcanolepas, Leucolepas and the aforementioned Neolepas are - are hydrothermal vent barnacles from the Pacific Ocean. I am very surprised to see this neat and well supported grouping. In particular, the stalked barnacle Vulcanolepas osheai is known the farm chemoautotrophic bacteria on its cirri. The more vent scientists look, the more it seems that vent organisms tend to form clades despite geographic distance, barriers or classical taxonomic ranks. We are seeing similar grouping in anemones, caridean shrimp, bythograeid crabs, and of course all the chemoautotrophic taxa: siboglinid annelids, bathymodiolin mussels, and vesicomyid clams. The habitat appears to be a unifying factor. I wonder what else in this phylogeny groups together by habitat? I know I've found Arcoscapellum sp. hanging off the antenna of an anomuran crab (Eumunida picta), perhaps it is related to other crab hitchhiking barnacles.

This study is a great study for many reasons, partly because it answers some questions, but mostly because it rearranges our thinking about the taxa in question and gives us more avenues to explore. I didn't highlight all the major discoveries from this article, such as the fine-tuning of the tempo of evolution, but I hope to see future papers addressing the evolutionary ecology of barnacles in light of the new systematic rearrangement. Taxonomy is at the point now where they needs to be substantial revolutions to be made in order to progress from stagnancy. This study and others like it using 'total evidence' (i.e. combining morphological characters, life history traits and genetics) will pave the way to understanding animal evolution and give systematics the credit it deserves, both financially and publicly. So cheers Dr. Southward, I'm sure you are resting well in the cirri of your loved organisms.

Mr. Arthrobalanus

Today, Charles Darwin is mostly remembered for the theory of evolution, natural selection and his four most famous books"The Voyage of the Beagle", "On the Origin of Species", "The Descent of Man" and "The Expression of the Emotions in Man and Animals". Few realize he published some 21 major books (one he was a writer an editor of a multi-volume set which I have counted as one book) and numerous papers. Even without the theory of evolution and the four most popular works, Charles Darwin was an eminent scientist, well published in geology, general zoology and in the area that most concerns us... invertebrates.

Of the many books he published, one was about the structure of coral reefs, two were about the interactions of plants and insects; five were completely about invertebrates. Of those only one, "The Formation of Vegetable Mould, through the Actions of Worms, with Observations on Their Habits" was not about barnacles. He spent 8 years and published four monographs on the barnacles.



First the back story. Barnacles were, when Charles Darwin went off to university, understood to be molluscs. Linneaus and Cuvier both reasoned they were molluscs because of the morphology of their shells and the presence of a sea water filled "mantle" cavity. In 1830 John Thompson showed they were related to crustaceans when he published the results of watching the metamorphosis of a nauplius into a cyprid larvae and then into and adult barnacle.

By 1844 Charles had almost completed the description of the specimen collected on the Voyage of the Beagle, and he had completed the first draft of On the Origin of Species. 1844 was also the year that Vestiges came out, which caused Darwin to rethink publishing "On the Origin" in its current form, and which prompted his friend Hooker to remark in 1845: "no one has the right to examine the question of species who has not minutely described many."

Darwin returned to writing "Geological Observations on South America" and by 1846 had cleared his desk, except that "illformed little monster" he would later come to call Mr. Arthrobalanus, a microscopic barnacle. Darwin figured it would take a few months, at most a year to examine, describe and publish the results. Then he could return to the issue of revising and publishing "Origins". 8 Years later he finished with the barnacles, having written 4 monographs on them.

I had originally intended to have described only a single abnormal Cirripede, from the shores of South America, and was led, for the sake of comparison, to examine the internal parts of as many genera as I could procure.

Unfortunately Mr. Arthrobalanus turned out to be a vexing character – a microscopic, parasitic barnacle. Darwin requested barnacles from friends and colleagues around the word to try and understand how arthrobalaus fit in. He began looking at life histories and larval forms. With each new species loaned to him, he sank deeper into the world of Cirripedia. Loius Agassiz called out for someone to revise the group, since had not been evaluated since becoming part of the crustaceans, a move which required a complete re-evaluation of their anatomy. In Darwin he found a willing patsy author.

For years he studied barnacles from around the world. The modern barnacles he dissected, the fossils he disarticulated. Yep, he did the fossils too, since no complete re-examination of the barnacles would be complete without re-examining the multitude of fossilized species. Darwin both suffered and enjoyed the challenge of the work. He suffered from eye and mental fatigue dissecting each day, but he made discoveries that kept him excited:

I believe Arthrobalanus has no ovisac at all!, & that the appearance of one is entirely owing to the splitting, & tucking up to the posterior penis, of the inner membrane of sack.— I have just found a Cirripede with an indisputably abortive anterior penis; so that this chief anomalous feature (viz two penes) in Arthrobalanus is in some degree brought within bounds.—

In short order Darwin had trained himself to become a taxonomist. He relied on homology and embryology for both description and as a key to the evolutionary relationships between group members lines of descent. In the 8 years he worked on Barnacles he soon became the worlds leading authority on the subject and quickly met his friend Hooker's objection to Vestiges, since he had now described many indeed, in creating the first modern taxonomic description of the Cirripedia. This "detour" actually provided time to rethink "On the Origin" and provided him with invaluable experience describing species and their relations to create a more compelling argument of evolution.

Soon after publishing the first monograph on living cirripedia, Charles Darwin was awarded the Royal Medal of the Royal Society of London, for his work. Clearly Mr. Darwin was a friend of the invertebrates.

Oh, Darwin renamed Mr. Arthrobalanus to be Cryptophialus minutus a burrowing or boring barnacle, a rather curious and unusual group of barnacles that includes sexual dimorphism and reduced males.

The sources for all of this post are Darwin Online and the Darwin Correspondence Project, a pair of excellent resources for studying anything Darwin, especially with the PDF's of his Ciripedia Monographs (PDF files)!

What Google Says

In an interesting Navel Gazing and Social experiment Rick MacPherson of Malaria, Bedbugs, Sea Lice & Sunsets came up with a meme finding a number of search terms (other than the blog title) that result in a #1 google ranking for the blog. Somewhat predictably MBSLS came up # 1 on such searches as “coral reefs, conservation, queer” and "moray, rick". Somehow it also came up as the number one place to turn for “zelnio, conservation, blog, coral, drunk”.

I know Kevin and I long ago evolved into more or less responsible drinkers, but this is devastating news. Even though he is a friend, that's some important territory we need to win back from Rick. Kevin, we gotta do more drunk blogging about inverts and conservation! ;-)

Ok, while the scallop beer and lobster vodka chill, I'll respond to Rick's meme tag. It's a great excuse to procrastinate doing mindless GIS exercises.

First search is the obvious one:

1. "zelnio heupel" or is that "heupel zelnio" #1 either way (yes, with google sometimes word order does matter)


2. "chaetognath phylogeny" beat out some heavy hitters like the Tree of Life, Springerlink, and Oxford Journals.


3. "barnacle evolution" scored another top spot with Kevins awesome tribute to Alan J. Southward and summary of a great paper on Barnacle Evolution


4. "whale lice conservation" gets a nod as number one for the Quixotic mission to get Right Whale Lice listed as an endangered species


5. the "Nobel Jelly" surprised me with a number 1 spot as well

But then things get a bit weird:

6. "sea squirt porn" a search phrase that also consistently shows up in our logs...weird! There must be a lot of lonely sea squirts out there tapping into the lab computers, or desperate tunicate researchers, or.. well I really don't want to know if it's not the one of the first two.


7. "ostracod penis" got a top result, but not "ostracode penis" which only got a #2 result.


8. "squirt en masse" was a number one result that I really don't even think I want to know about


9. "sperm races" Beg pardon?! What? Oh, but that reminds me I need to set up the video to record those urchins, last time it was a photo finish

Looking through our logs some time ago I noticed "porn" was one of the top words that led people from Google to us so on a whim...I added "porn" to the end of a number of species we talk about and found out TO95% owns:
"whale lice porn" and "snail porn" with top ten results for "chaetognath porn", "mollusc porn", "cephalopod porn" and "arthropod porn". Interestingly Pharyngula beat us out on all of those except "arthropod porn" where Blackwell Synergy stomped our telsons.

So to be a meme it has to be self replicating...so if they would like to participate, I'm asking The Brine Queen, Bobbie and Jerry, Jason and Peter to gaze into their navels through Google and see what floats to the top.

A World Inside a Coconut

In November 2003, while an undergrad at University of California at Davis I was asked by my 2 of my Geology professors if I wanted to help them out on an expedition to hydrothermal vents on the East Pacific Rise. They knew of my interest in vents because they were teaching a 1 credit seminar on Hydrothermal Vents that I was participating in. My undergraduate major in Evolution and Ecology though and was planning on double majoring in Geology. It never happened though, mostly because I didn't want to stay an extra semester and take the two classes I needed to finish the major (coincidentally the same classes I would have needed to get a minor too - Paleoclimatology and Mineralogy).

This expedition was headed by the Field Museum of Chicago as more or less a collecting expedition and other parties with funding came along to share the cruise time. We used the famous Alvin submersible and sailed aboard the R/V Atlantis. Our role as the "geology contingent" was to oversee the night operations which included mapping the seafloor and flying TowCam, the towed camera system the we basically keep from crashing too may times into the seafloor or a cliff or something. It takes a photo every 30 seconds and also has equiptment to measure the alitude off the seafloor, distance of something in front it, particle scatter in the water column, conductivity and temperature. Except for the photographs, all this information is relayed up the cable to the control room where someone has to constantly have their hand on the controls to adjust the feed of the cable, keeping the camera at about 3-5 meters off the bottom. Not an easy task, but needlessness to say the graduate student and undergrad (myself) never crashed while the 2 professors who have done this for years... lets just say the close-ups were awesome!

Being that this was mainly a biology cruise was the real reason I was asked to go. I'm not really a geologist, just a biologist with a good deal of geological training. Being the least senior out of just about everybody on board I was affectionately referred to one French participant (whom I now work with on various projects) as the "ship's bitch". I was in charge of making a "best of" video for the expedition to show off to the Museum's patrons. Basically pulling out highlights and cool video from each dive. I also found my passion was sorting through rocks, sediment, snot, you name it and finding critters. I seemed to be very good at it as the Chief P.I. and other biologists seemed pretty please with my findings! Sorting is still something I take great pleasure in. I get all giggly when a box full of crap comes up from the seafloor, filled with various worms, gastropods, amphipods... its the "what new thing might I find if I keep looking?" that keeps my interests peaked. Other duties were as requested by whomever wanted help (like bleeding the giant tubeworm Riftia pachyptila). I reveled in it all!


Our nights were filled with work, but the daytime was spent waiting for Alvin to return from the bottom. We often peered overboard trying to spot marine life. Often floating debris from islands or continents far away would pass beside the ship with several colorful fish hidden underneath seeking its protection. One day a coconut floated by. I don't know whose brilliant idea it was, but one of the biologists netted it for fun I suppose. As it turned out this coconut was full of wonderful surprises!

All the images, except the picture of myself in Alvin, were taken by my friend and colleague, crustacean biologist T.A. Haney. Unfortunately, I cannot tell you what any of these are, none of the specimens were in my possession since the end of that cruise. I presume they ended up deposited in the Field Museum along with everything else. The barnacle appears similar to species in the genus Poecilasma, but has lateral plates, which I haven't seen in Poecilasma. The clam has a massive siphon! But I think the polychaete steals the show. I can try to ID the family and maybe genus, using Fauchald's 1977 key to polychaetes tomorrow when I'm in the lab.

I just wanted to share these photos for a couple reasons. One is that they have fascinated me since I saw them. All of their coloring is reminiscent of a coconut. Its almost as if they intended to live inside of a coconut hull and have all independently evolved "cocomaflage". It is rather uncanny. I think the currents at 8-13 north run east to west. I'm not sure where the equatorial counter current was at that time and that year, but we were probably above it. Therefore this microcommunity had to have come from Mexico or Central America or an island offshore. We were about 400km from the coast, so it had to travel quite far and all the inhabitants seemed healthy and were responsive. What did they eat in there? Did the species interact? They all appeared to be adult forms.

Observations like this open so many questions for me about connectivity in the ocean. If I end up staying in research after I finish my degree, I will be putting proposals in to study floating microcommunities such as this one. Just think of trolling the open seas in transects and picking up anything you can spot and seeing what lives there. There can be higher and more rigorous scientific questions posed too, other than mere fascination with discovery and natural history. For instance, how do floating communities affect genetic structure of animal species? We can take an island biogeographic model and throw in information about the frequency of immigration events such as these into the mix and see if communities can be sustained or recolonized after local extinction. The role of floating debris, whether natural or man-made, is an underappreciated question in marine ecology, in part of the ephemeral nature of the debris. Anyone want to write a grant proposal? Or give me a job at a non-profit, or a post-doc, or... to investigate cool stuff like this? (big cheesy smile)

Toadally Tangled #96

Martin Rundkvist has the 96th edition of the Tangled Bank up at Aardvarcheology. Lots of great links to lots of great science writing, including my barnacle evolution post. Go there and read away, its toadally awesome!

Coloring Books for Grad Students

Today is my son's birthday and one of his presents (found through Kevin's comic book posting - Johann says "Thanks Kevin!") is The Marine Biology Coloring Book by Tom Niesen. I hadn't seen this one before, and it is definitely not a run of the mill coloring book!

The illustrations are far more anatomically correct with wonderful details such as the reproductive cycle of sacculinid barnacle. The text that accompanies it is both explanatory and accessible. It is very specific and aimed generally at students or very serious beachcombers. While accessible to advanced middle school, high school, or early college students, some professors use the book as a quick orientation to marine biology for students coming to the marine biology graduate program from other fields.

The book starts with a general overview of oceanographic currents, weather, tides and proceeds into 14 page spreads covering major habitats including zonation concepts, the photic zone and a page spread each covering deep sea and hydrothermal vent habitats. Spreads on biological diversity and reproduction are organized taxonomically. Special topic pages follow on migrations, symbiosis, competition, defense, feeding strategies and oceanographic technology.

The book does a very good job covering the balance of verts to inverts despite the cover focus. After taking out the 17 page spreads on physical oceanography and habitats, there are 4 page spreads on plants and algae. Invertebrates are represented by 54 page spreads while fish, reptiles, birds and mammals by total 37 spreads. Some of those are overlap such as the spread "Symbiosis: Parasitism" which highlights three parasitic relationships: copepods parasitizing fish, fish parasitizing sea cucumbers and barnacles parasitizing crabs.

A Highly recommended book for junior marine biologists, or maybe for all the family members.

(edit 5/22 - added author information (doh!) after noticing I forgot it after three of his former students - including authors of the Brine Queen and Echinoblog - checked in with wonderful comments.)

Molluscan Zodiac

A new site has sprung up... The Molluscan Zodiac run by Keith Bradnam.

Hmmmm... looking at his definitions of the cast of characters I see potential trouble here...

From his description of the character traits of the Snail:

Slow in both body and mind; snails are loyal yet stupid, giving yet selfish. Snails do not get on with barnacles, limpets, clams, or squids, and at best, only ever tolerate slugs.

For a sample horoscope, how about the Limpet for this week...

The Limpet
March 10th - May 1st

Big developments will occur in the bedroom this week. Make sure your sheets are clean. Take a second look at what you are wearing. Your friends think that it is time that you burn your wardrobe. Maybe they are right?

Hmmm. so acordin to this zodiak I'm a Barnacle... hmmmm... yeah, not going to touch that one.

So what's Your sign?