Don't let the nutrients fly away!

Pitcher plants are beautiful but disturbing. Their vase-shaped pitchers are so elegant to look at, yet violate our notion of plants as passive and peaceful, because they are death traps for unwary insects and other small animals that fall in and drown in the pitcher fluid. Pitcher plants (genus Nepenthes) are one of the few carnivorous plants, who also include the Venus Fly Trap and the Bladderwort, that invert the food chain by gaining some of their nutrients from animals.

Nepenthes bicalcarata (by David Sucianto, via Wikimedia Commons)

Why would a photosynthetic organism need to trap animals? After all, they still have green leaves and chlorophyll, like any other plant. But other nutrients, especially nitrogen, are important to plant growth as well. Pitcher plants can grow in nutrient poor soil because they can supplement their intake of nitrogen and other nutrients by trapping and digesting animals, which are especially nitrogen-rich.

Not all animals will die in pitchers, however. Some insects, including the larvae of several dipteran (fly) species, can live in the pitchers and feed on the organic matter found there. The pitcher species Nepenthes bicalcarata also plays host to an ant species, Camponotus schmitzi, that is found only with N. bicalcarata. The ants are somehow able to walk on the slippery inner surface of the pitcher, and predate upon the fly larvae and other organic material, and also feeds on nectar from the plant.

It would seem at first that this is a lousy deal for the plant. The flies and ants are stealing its food right from its mouth! A new research paper published in PLoS ONE shows how the ants and pitcher plants actually derive mutual benefit.

By looking at the nitrogen isotope ratios in the plant tissue, and using isotope labeling experiments, the researchers showed that nitrogen is being transferred from the ants to the nutrients. They also observed how the ants predate upon the fly larvae that live and mature inside the pitchers. Left to their own devices, these larvae would consume the pitcher's nutrient supply, and then literally fly away with the stolen nutrients when they metamorphose into adults. For this they are (harshly) called kleptoparasites, or "thief-parasites". By capturing and eating the flies while they are still larvae or pupae, the ants put a stop to this thievery. The plant itself then recovers these nutrients in the form of the ant colony's waste products.

The ants are hence not only improving the pitcher's prey-capture efficiency, by keeping the slippery pitcher walls clean, but also prevent the nutrients from escaping with the insects. A fascinating story of symbiosis, that reveals just how dynamic and interconnected all these nutritional and behavioral relationships are in Nature.

Lynn Margulis - an appreciation

Lynn Margulis passed away recently at the age of 73 (NY Times obituary). She was responsible for one of the great ideas of modern biology -- the endosymbiotic theory for the origin of organelles. This is the idea that chloroplasts and mitochondria of eukaryotic cells originated as independent prokaryotes that became associated symbiotically with host cells, and eventually became indispensable organelles. The whole process she called "symbiogenesis". Siva blogged about this here two days ago, and suggested that I share something to.

The story of the theory itself is also quite well known. Margulis put forward the hypothesis in a paper titled "On the origin of mitosing cells" (Journal of Theoretical Biology 14: 225, under her married name L. Sagan - PubMed, ScienceDirect) in 1967, but before it was accepted for publication there, it had been rejected 15 times by other journals. It was initially controversial--to think that an essential part of our own cells are actually bacteria in disguise!--but today it is textbook knowledge. Much like the theory of plate tectonics, this is one of the great Cinderella stories of modern science.

I was fortunate enough to hear Margulis speak a few years ago when I was in college. I don't remember the details now, but I do remember a few things she said. She recalled that the last time she was at Harvard, it was at a seminar where Ernst Mayr (one of the pioneers of the Neo-Darwinian Synthesis) was in the audience, sitting right there; she pointed at the seat in front of my friend Noor and me and we got a little thrill from it. "Although he was almost a hundred years old, he was still the sharpest mind in the room!"

(She wrote a reminiscence of Mayr when he passed away in 2005, which gives some flavor of their personalities. Mayr: "You don't have to tell me what 'symbiosis' is! I studied symbiosis with Paul Buchner in Griefswald [in the 1920s]." Buchner later wrote one of the classic books on symbiosis, Endosymbiose der Tier mit pflanzlichen Mikroorganismen.)

She also showed a video of protists from termite guts, some of which have symbiotic bacteria living on their surface, which act more or less as surrogate flagella. One could tell that she was really captivated by the beauty of these organisms, and I heard later from someone that she often showed this video at her talks.

Margulis's 1967 paper is best known for its hypotheses about chloroplasts and mitochondria, which have been validated by lines of evidence, such as DNA sequencing, that were not available to her at the time. Her remaining hypothesis was that eukaryotic flagella evolved from symbiotic spirochaetes, which are corkscrew-shaped bacteria that swim helically. This idea hasn't done so well, and hasn't been supported by evidence in the way which the chloroplast and mitochondrial hypotheses have, but as her fascination with the video shows, she was still thinking about it. One of her last papers, published in 2010, was on the microscopical structure of one kind of these bacteria on a termite-gut protozoan.

On rereading her 1967 paper, a few things stood out to me. She managed to synthesize a tremendous amount of information (the paper is 49 pages long) from very different fields, including microbiology, palaeontology, geology, cytology, and evolution.

This was where she first put forward many of the concepts and themes which she would continue to think about and work on for long afterwards. For example, the scenario for eukaryote evolution that appears as a figure is re-presented in modified form in her popular book, Five Kingdoms.

The book, which she coauthored with Karlene Schwartz, was one of my favorite books as a student. The latest edition is from 1998, but it's still a good read, giving a brief overview of all the major phyla of living organisms in the classical five kingdoms: Prokaryotes, Protoctists (i.e. protists), Plants, Fungi, and Animals. It was my first introduction to the weird and wonderful world of protist and microbe diversity, which otherwise get such short shrift in introductory biology. It also shows how effective she was as an encyclopedic collator and system-builder.

In her thoroughness she also delved into the older literature. She had an interest in the history of biology, and what might be called her intellectual predecessors. She was involved in a recent project to translate a 1924 Russian book titled Symbiogenesis: A New Principle of Evolution by Boris Kozo-Polyansky. She did not shy from acknowledging these "forbears" and other early insights and ideas that were "before their time".

I think that she represented a very "classical" sort of biology, informed by visual thinking and reasoning by analogy. Looking at older books of zoology, botany, or cytology, one finds a similar frame of mind and emphasis on pattern-recognition. Modern biology is definitely still about pattern-recognition, but much of it is now impossible to "eyeball", such as searching for gene homology.

Unfortunately, reasoning by analogy can sometimes lead us down the wrong track, and an over-enthusiasm for it seems to have been responsible for a controversy that involved her in 2009. As a member of the National Academy of Science in the USA, she sponsored a paper for publication in its Proceedings, which hypothesized that "caterpillars evolved from onychophorans [velvet worms] by hybridogenesis" with insects. The paper never made it into print, but attracted a storm of protest and the imputation that she misused the submission process to push through a paper which would never have been published elsewhere.

That episode didn't help her reputation for "eccentricity", which is a word which seems to crop up in describing her, alongside "maverick" or "rebel". Nonetheless, her place in biology is secured, and I think it's important to acknowledge why. She gave us a whole new way of thinking about evolution, spurred scientific interest in endosymbiosis and early evolution, brought protists and other formerly obscure organisms to the attention of scientists and public, and defended the importance of symbiosis to the evolutionary process.

In doing so, Lynn Margulis gave us a glimpse into the biological world as it could have been at its origin, and also into the present, where we still make regular use of the concepts that she pioneered. RIP.

Björk and the Zombie Snails

No, it's not a tribute band. The quirky Icelandic musician Björk has a new album out, called Biophilia. Appropriately enough, the tracks are inspired by themes of nature and biology.

One of the songs in particular, "Virus", was written after Björk learned about "zombie snails" on YouTube. It has nothing to do with real viruses, though (Disclaimer: I haven't heard the album yet so I can't say if the music is any good). These snails are parasitized by a trematode worm called Leucochloridium paradoxum, which you can see in the photo below.

Snail infected with Leucochloridium paradoxum in its eyestalk.

Look closely at the eyestalk on the right. Yup, that's filled with worm. But it's not just one worm. It's a structure called the brood-sac, which contains hundreds of cercariae – little larval worms ("trematode life cycle" on Wikipedia. The sac is banded and green and pulsates. This attracts the attention of birds, which think that it's actually their favorite food, maggots or caterpillars. They swoop in and peck off an eyestalk with all the worms in them. The worms end up in the gut of the bird, and are carried in there to be pooped out somewhere else. Free transportation! Snails grazing along eat some bird poop with the parasites in them, and get infected, completing the cycle.

Find out more about the sneaky life cycle of this worm from this article on Wired magazine, or read the Wikipedia article, or just watch the video that inspired Björk:

Sea grape symbionts - parasites turned mutualists

The research project that I'm working on involves a symbiotic protist found in sea grapes, which are a family of sea squirts, or ascidians - sessile, filter feeding invertebrates which turn out to be close relatives of vertebrates (they're also chordates). Carl Zimmer, a science writer at the NY Times and other publications, has just blogged about a paper just published by one of my advisers, Mary Beth Saffo, and collaborators. The paper has been a long time in the works, so it's gratifying to see that it's gotten some publicity already. It's interesting how these things work, though - he found out about it because he was visiting the same marine biology station where she was doing some field work. There's plenty of serendipity in science communication, on top of the inherent general interest of the work itself.

Zombie ants in news, and musings on science reporting...

Markings on fossil leaves appear to be the 'death grip' of ants infected by the so-called zombie fungus, Ophiocordyceps. The fungus causes the infected ants to move to a position on nearby vegetation and die immobilized there, such that the sprouting fruiting body of the fungus will more efficiently spread its spores over yet more ants. This grip leaves distinctive markings on the leaves, which were recognized by a group led by David Hughes (disclosure: I have met David and heard him talk about his work).

Having this fossil evidence allows us to be able to give a minimum age for the history of this fungal life-style. Despite advances in the study of molecular evolution, fossil evidence is still the most direct way to pin a date on events in the history of life. Earlier hopes that the rate of changes in nucleotide or amino-acid sequences could provide an objective 'molecular clock' (first proposed in the 1960s by Emile Zuckerkandl and Linus Pauling - yes, that Linus Pauling) turned out to be premature, because rates of molecular evolution are not generally uniform across species and even in single lineages over time, and therefore need to be calibrated, typically against the fossil record.

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On the topic of science reporting: The Guardian newspaper article linked above is better than most newspaper science reporting, however, it still illustrates a few sticky points that nag at me when I read about science in the news.

Chief among these is the lack of citations. That is disconcerting, especially to someone in an academic setting where proper attribution is always emphasized. Science reporters are quite uneven in how they cite things: some simply omit any mention of where the research they describe is going to be published (or has been published), some state the journal name and leave it at that, and only in a few cases is a full citation (or in this article: a link to a PubMed record) given. Here, however, note that the PubMed link is to an earlier paper on a related topic, but not about the issue being directly reported. The article says that the scientific report is published in Biology Letters, but a quick search in the journal's website turned up no hits. Hence I can only conclude that it's yet to be published, and the reporter was privy to a prepublication preview.

Unfortunately, this affects blogging, too. I'm happy to highlight interesting papers and newspaper reports on biology, but without having seen the original paper, if new research is being presented, it is hard to assess the quality and reliability of the work, and whether it really is worth being blogged about. Worse yet, the reporter may have distorted the actual conclusions, or misrepresented the facts, ... the list goes on.

So the next time you see a newspaper article reporting new research, do keep an eye out - drop a comment here if you see something noteworthy that shows how caution is necessary.

On Rice, Mosquito Ferns, and Cyanobacteria...

This blog has been veering towards the theme of food in recent posts. Perhaps the most important staple food in Asia is rice, traditionally grown in irrigated paddy fields. A piece of natural history trivia that has stuck with me from my childhood fascination with ferns is how paddy farmers encourage the growth of the mosquito fern Azolla, because it has nitrogen-fixing cyanobacteria that live in symbiosis with it, thereby contributing to the nitrogen content of the soil.