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Swarms of tasty cicadas don’t help the birds — what gives?

Every thirteen years they come. After over a decade underground, they build burrows to the earth’s surface and emerge in synchrony, clawing and crawling up through the soil, rip their skins down the back and are reborn as adults. And after a month, they will be dead, whether consumed by the animals awaiting their arrival or as a part of their lifecycle, with the females having laid eggs in the soil to develop for another thirteen years.

A cicada emerging on April 26, 2011 in Harmony, NC. Flickr user Janet Tarbox in the 2011 Brood XIX album

Some cicadas emerge every single year — annual or “dog days” cicadas — but two broods are on much lengthier cycles. This year, 2011, Brood XIX cicadas have already begun emerging throughout the southern United States. In 2004, I was lucky enough to experience the emergence of Brood X and won’t have the honor again for yet another decade, after a total of 17 years in 2021.

Their peak in 2004 coincided with Princeton University’s alumni weekend — which I attended as a bored high schooler —  and what poor timing for that event! The endless drone of the insects forced us to yell just to make conversation; the air was so dense with their swarms that they would fly into unsuspecting Princeton grads with a size and velocity that was actually painful; sidewalks and windshields were splotched with the pale green stains of the squished deceased.

Besides providing a weekend of entertainment for high school hooligans witnessing the torture of exasperated ivy-league graduates, the emergence of millions upon millions of cicadas for just a single month provides an ephemeral pulse of resources. Once dead, their decaying bodies add nutrients to the soil (1) and streams (2), increasing soil microbes (3) and detritivorous insects (4), while their predation on roots as nymphs and plants, young ones in particular, as adults can decrease tree (5, 6) and plant (7) growth in the cicadas’ emergence year.

This deluge of huge, nutritious bugs should be a boon for their predators as an undepletable food source. While one study (8) found no change in a population of white-footed mice after Brood X emerged, the same study saw the number of short-tailed shrews increase four-fold — now that’s a lot of shrews!

An Eastern Kingbird going after a cicada. From Flickr user Michaela Sagatova

So you’d probably expect a similar reaction from insect-eating birds — that some would have no change, but some would benefit greatly from the cicada surge, especially since their migratory nature would allow them to gather by the cicadas during emergence years. But when ornithologist Walter Koenig and entomologist Andrew Liebhold compared populations of 24 bird populations over the course of 37 years from the Breeding Bird Survey data set with periodic cicada pulses (9), they found only two species that showed up just for the cicadas — both North American cuckoo species. Out of the other 22 species, only 6 populations increased; the remaining 16 declined, and 5 of them with statistical significance.

What gives?

They had three hypotheses to explain why so many bird populations were decreasing, according to a large observation-based bird survey, even when the birds were practically drowning in ample food resources. The overwhelmingly loud noise of cicada calling could drown out bird calls for the birdwatchers, creating an observer bias artificially lowering the reported number of birds in the area — the detectability hypothesis. Alternatively, all the racket could keep the birds from hearing one another, disrupting their communication and driving them to quieter areas with fewer cicadas — the repel hypothesis. Or the birds populations could be declining for another reason, affecting them beyond the ranges of the cicadas — the true decline hypothesis.

Brood XIX cicada on May 3, 2011. Flickr user Patrick Coin

Koenig and Liebhold just published a reanalysis (10) in March 2011 in Ecology to test their ideas about why these bird populations are dropping. Again, they used the Breeding Bird Survey data for the 12 species showing the greatest decline from their previous paper, but also compared populations to the counts from the previous winter (Christmas Bird Counts) and incorporated notes about cicada prevalence from the counts where they could.

Their results supported the true decline hypothesis — that the birds’ population declines are not related to the emergences at all. They suggest that the drop in population numbers could be an indirect effect of the cicada emergences, however. The voracious plant consumption of the cicadas could be negatively affecting other insect prey sources or otherwise adversely impacting the immediate habitat. Additionally, while North American cuckoos are not typically nest parasites, this behavior — laying their eggs in the nests of other birds — has been observed when cuckoos are under intense competition with one another, as in this situation.

Is that cat hungry or just looking to cuddle? By Flickr user Allan Janus, 2004

Some scientists (11) suggest that cicadas emerge on such odd timescales — 13 and 17 years, I mean, c’mon! — specifically to mess with their predators. If they emerged too frequently, their tactic of completely overwhelming the area with their presence, basically guaranteeing that many of them will successfully reproduce no matter how many housecats and cuckoos are fed — predator satiation — wouldn’t work. If they emerged more frequently, the gains of their predators from the cicadas’ previous emergence may still be lingering, effectively increasing their predators’ numbers each year until the cicadas themselves were overrun. (A hard scenario to imagine, I know — that would take even more shrews!)

But could the cicadas have evolved to take advantage of such a long-term concept? That they would have to effectively “wait” for their predators to be on the decline before they emerge again? Some biologists have even hypothesized that the latency periods of 13 and 17 years are significant because they are prime numbers! Take it away, Dr. Nicolas Lehmann-Ziebart:

[A]ssume that cicada predators consist of species having cyclic or ‘‘quasi-cyclic’’ dynamics with either two- or three-year periods. This leads to high predator abundances, and high predation rates, in years divisible by either two or three. Because primes are the only numbers between 10 and 18 that are not divisible by 2 or 3, broods of prime-period cicadas frequently escape high predation levels and hence tend to dominate hypothetical cicadas with nonprime periods. This mechanism for generating prime numbers relies on either externally driven two- and three-year cycles of predators, or predators that have strict fecundity schedules creating dynamics that tend to show two- or three-year oscillations.

Lehmann-Ziebart and his undergrads suspect that the cicadas emerge in these odd patterns as a balance between predator satiation and competition within the cicadas themselves. They, unfortunately, couldn’t find an obvious explanation for the prime numbers, though suggest it could have to do with a genetic counting mechanism.

Another explanation for this odd pattern of bird decreases coinciding with great cicada food sources is shoddy data. The Bird Breeding Survey is performed by mere citizens after all — can’t trust them! JUST KIDDING! There have been criticisms of the survey, including new observer bias (a n00b bird counter gets better each year, so the early years are unreliable and this bias is not accounted for), its road-based sites and transects for the counter’s ease could cause bias due to car traffic, and variation in the number of counters year-to-year. Nonetheless, the survey covers an incredible amount of ground — with each route covering nearly 25 miles — and over 400 bird species and has been ongoing since 1966. Pretty good for any large-scale data set which will always have caveats.

It looks like the jury’s still out on why bird populations decline during cicada emergences, though I suspect it’s a combination of many factors — bird communication problems, detectability bias, ecosystem changes induced by the cicadas and the overall variability in bird populations and routes.

This post was chosen as an Editor's Selection for Wheeler, G., Williams, K., & Smith, K. (1992). Role of periodical cicadas (Homoptera: Cicadidae: Magicicada) in forest nutrient cycles Forest Ecology and Management, 51 (4), 339-346 DOI: 10.1016/0378-1127(92)90333-5

(2) Pray, C., Nowlin, W., & Vanni, M. (2009). Deposition and decomposition of periodical cicadas (Homoptera: Cicadidae: Magicicada) in woodland aquatic ecosystems Journal of the North American Benthological Society, 28 (1), 181-195 DOI: 10.1899/08-038.1

(3) Yang, L. (2004). Periodical Cicadas as Resource Pulses in North American Forests Science, 306 (5701), 1565-1567 DOI: 10.1126/science.1103114

(4) Yang, L. (2005). Interactions between a detrital resource pulse and a detritivore community Oecologia, 147 (3), 522-532 DOI: 10.1007/s00442-005-0276-0

(5) Speer, J., Clay, K., Bishop, G., & Creech, M. (2010). The Effect of Periodical Cicadas on Growth of Five Tree Species in Midwestern Deciduous Forests The American Midland Naturalist, 164 (2), 173-186 DOI: 10.1674/0003-0031-164.2.173

(6) Koenig, W., & Liebhold, A. (2003). Regional impacts of periodical cicadas on oak radial increment Canadian Journal of Forest Research, 33 (6), 1084-1089 DOI: 10.1139/X03-037

(7) Yang, L. (2008). PULSES OF DEAD PERIODICAL CICADAS INCREASE HERBIVORY OF AMERICAN BELLFLOWERS Ecology, 89 (6), 1497-1502 DOI: 10.1890/07-1853.1

(8) Krohne, D., Couillard, T., & Riddle, J. (1991). Population Responses of Peromyscus leucopus and Blarina brevicauda to Emergence of Periodical Cicadas American Midland Naturalist, 126 (2) DOI: 10.2307/2426107

(9) Koenig, W., & Liebhold, A. (2005). EFFECTS OF PERIODICAL CICADA EMERGENCES ON ABUNDANCE AND SYNCHRONY OF AVIAN POPULATIONS Ecology, 86 (7), 1873-1882 DOI: 10.1890/04-1175

(10) Koenig, W., Ries, L., Olsen, V., & Liebhold, A. (2011). Avian predators are less abundant during periodical cicada emergences, but why? Ecology, 92 (3), 784-790 DOI: 10.1890/10-1583.1

(11) Lehmann-Ziebarth, N., Heideman, P., Shapiro, R., Stoddart, S., Hsiao, C., Stephenson, G., Milewski, P., & Ives, A. (2005). EVOLUTION OF PERIODICITY IN PERIODICAL CICADAS Ecology, 86 (12), 3200-3211 DOI: 10.1890/04-1615

Written by Hanner

May 4, 2011 at 11:15 pm

Natural history collections in ecological research

Once I dreamed a dream of being an evolutionary biologist.  As I imagined it, I would hang out in a natural history museum, comparing fossils to one another, taking notes on the minute differences, and piecing together the history of life. It wasn’t until a job fair years ago, when I babbled to an evolutionary biologist about morphologies, collecting specimens, and, pretty much word for word, “working in a dusty basement full of drawers of fossils,” that I realized it was an unlikely future.  The scientist looked at me like I was nuts: “Um… that’s not really what I do.  I work with DNA and genomes.”  I pushed him further, but his answer was clear: The job I described did not exist anymore.

Why can't I just hang out and compare the varying shapes of animals in a basement lair? Image: Wikimedia Commons: Haeckel, Kunstformen der Natur (1904), plate 44: Ammonitida

But while the job does not exist (or is a rare find at best), the specimens do. There are still huge archives at museums stuffed with bones, skins, ad infinitum. I am fortunate to have a friend who works at the American Museum of Natural History in New York in the mammals department. When I visited Catherine back in October, she was spending most of her time with the bat specimens, ensuring that they were in proper order and condition.

She gave me a tour of the place and I was blown away: I had always dreamed of walking into a room, stacked ceiling to floor with hippo skulls, and there I was! Catherine showed me the cleaning rooms, where fresh skeletons are picked clean by flesh-eating beetles; slid open a case in which hung tiger skins, as if it were her coat closet; and, by far my favorite, the marine mammal room, with massive whale vertebrae lined up on shelves. It’s funny to imagine a whale complaining of back pain, but there was even a pair of calcified vertebrae among the bunch.

After walking through the maze of rooms and seeing this vast collection with my own eyes, I couldn’t help but wonder: What are these even used for anymore? Certainly, education, but the museum was already packed with skeletons and stuffed animals without this backup. Catherine told me that sometimes researchers try to extract DNA from specimens, but that purpose alone doesn’t seem to make the best use of this huge collection. If taxonomy is now prescribed by genomics, are these collections, compiled and curated over centuries, going to waste?

In the past couple months, I stumbled upon three papers describing three different ways that these collections can be used to study ECOLOGY! (O, be still, my heart!)  The first, in Marine Ecology, online on Feburary 16, 2011, argues for the use of natural history collections to inform us about past species assemblages of areas that haven’t been heavily studied — baseline data. The researchers used Saba Bank, a reef in the Caribbean Netherlands, as a case study, studying coral specimens collected by divers in 1972. In this older collection, there were five species of corals collected that are no longer found in Saba Bank, suggesting that this understudied reef may need greater protection.

This may seem like an obvious use – but the authors note that it’s relatively unexploited. This may be because of poor record keeping, or the difficulty of locating collections from a specific area that have been shipped off to another museum. Another problem is that, if earlier sampling methods weren’t written down, it’s hard to know how representative a collection is of the area. Divers, not scientists, collected the Saba Bank specimens, so they may not have been trying to take note of all the species there at the time. But finding five species that survived there previously but don’t now is very useful information, no matter the completeness of the collection.

Certain organisms can provide information about their growth through growth rings, which makes their presence in natural history collections useful for learning about environmental conditions. Robert Scott is remembered for failing to reach the South Pole before Roald Amundsen – and part of the reason he was so slow is that he was so busy collecting specimens and taking measurements for SCIENCE. During his 1901 and 1913 expeditions, Scott collected Cellarinella nutti, a bryozoan that develops growth rings. Because this species was collected throughout the twentieth century, scientists were able to date the rings based on collection date, and create a timeline of relative growth: did the bryozoans grow significantly more in one decade than another?

The scientists found no change in growth between 1890 and 1970, but a sharp increase since the 1990s, as they published in Current Biology on February 22, 2011. Based on studies in related species, they think that this growth acceleration is either related to (a) greater production of phytoplankton, the food chain base or (b) a switch in the dominant species of phytoplankton, which could alternatively be more nutritious, speeding their growth. If they’re correct, it means that these museum specimens provide evidence for a recent increase in carbon storage on the seafloor in the Antarctic.

A chicken infected with avian pox with lesions around its beak and eyes. Image: Wikimedia Commons: Roman Halouzka

Natural history specimens can also be useful for tracking the development of disease in an animal population. Avian pox is caused by a DNA virus (the aptly named Avipoxvirus) that causes lesions either externally, on feather-free areas, or internally, in the mouth, windpipe and lungs. Beyond the metabolically draining effects of the virus, the pox symptoms can cause trouble feeding, cleaning and breathing. The virus is carried by mosquitoes and has been linked to the extinction of Hawaiian bird species.

Avian pox has been identified recently in the Galapagos islands, affecting mockingbird, warbler, and finch species that are only found there. To figure out when the virus arrived to help trace the progression of the infection, scientists used natural history specimens. Digging through past collections, the researchers selected birds with lesions like those found on avian pox victims, and looked for viral DNA to confirm that these lesions were caused by the virus. Their research, published on January 13, 2011 in PLoS ONE, reports the earliest specimen with avian pox they found was infected in 1898, and that the infections generally followed the pattern of human colonization. This suggests that the virus has been spread not by mosquitoes moving between islands, but by chickens and other pox-carrying fowl brought by settlers.

These perhaps unexpected uses for natural history collections — to reconstruct species assemblages, extrapolate climatic or ecological variability reflecting growth, or trace a disease through a population — should force scientists to rethink their collection methods. Historically, these collections were created to answer a simple question: What species are out there? As a December 2010 paper in the American Journal of Botany notes (hat tip to Colin Schultz), this mindset often leads to (a) oversampling of rare species, as just one or two specimens can misrepresent their abundance proportionally and (b) undersampling of common species, since just a couple specimens will do.

But gathering fully representational collections is easier said than done. These are real people out in the field, digging in the dirt or seafloor and may not have the space or energy to haul back many examples of a single species. Plus, you can go too far in the other direction; there is also no need to destroy the ecosystem for the sake of fair sampling!

But it does make clear that the age of DNA and genomics does not exclude the need for sampling. To ensure that past collections remain useful as ecological tools, scientists need to keep sampling for the sake of future science.

Edit: Fabulous commenters leave links to relevant articles! They each get a gold star sticker

  • Tracing the history of the parasite Wolbachia in butterflies using museum collections
  • Utilizing museum specimens to map deep sea creatures
  • Using bivalve fossils to study the latitudinal diversity gradient extending from the equator

This post was chosen as an Editor's Selection for>Barnes, D., Kuklinski, P., Jackson, J., Keel, G., Morley, S., & Winston, J. (2011). Scott’s collections help reveal accelerating marine life growth in Antarctica Current Biology, 21 (4) DOI: 10.1016/j.cub.2011.01.033

Hoeksema, B., van der Land, J., van der Meij, S., van Ofwegen, L., Reijnen, B., van Soest, R., & de Voogd, N. (2011). Unforeseen importance of historical collections as baselines to determine biotic change of coral reefs: the Saba Bank case Marine Ecology DOI: 10.1111/j.1439-0485.2011.00434.x

Parker, P., Buckles, E., Farrington, H., Petren, K., Whiteman, N., Ricklefs, R., Bollmer, J., & Jiménez-Uzcátegui, G. (2011). 110 Years of Avipoxvirus in the Galapagos Islands PLoS ONE, 6 (1) DOI: 10.1371/journal.pone.0015989

Steege, H., Haripersaud, P., Banki, O., & Schieving, F. (2010). A model of botanical collectors’ behavior in the field: Never the same species twice American Journal of Botany, 98 (1), 31-37 DOI: 10.3732/ajb.1000215

Written by Hanner

March 2, 2011 at 12:41 am

The many relationships of leaf-cutter ants

Are those little leaf scraps on the ground? Or is it a line of leaf cutter ants (Atta cephalotes)? Photo taken at La Selva Biological Station, December 2008 by Hannah Waters

Trying to capture the movement of a colony of leaf-cutter ants in a single photo is nearly impossible in my (amateur) experience.  The queues of ants follow a worn-down trail in the ground that they themselves made with the impact of their little ant feet.  There are ants moving in both directions, between the food source and their nest, but you rarely see them run into each other.  (Though small ants, minima, will hitch rides on another ant’s leaf.)  It’s an organized flow of ants and materials – but a photo can only capture the single frame, as if it’s just bits of leaf littering the ground.  The sense of movement is lost.

But that’s only the the frustration if this is the aspect of ant symbiosis you’re trying to capture: the leaf cutter ants collecting foliage to feed to their cultivated fungus. What if it’s a different symbiotic relationship you’re interested in?

BOOM! Image by mass spectrometer to measure the amount of an antibiotic, valinomycin, on a leaf cutter ant, Acromyrmex. by Schoenian et al. 2011.

Leaf cutter ants, of the genera Atta and Acromyrmex, live in huge colonies and can form nests more than 30 meters in diameter.  They’re most noted for their agricultural behavior: they harvest leaves (and can defoliate entire trees in the process) which they bring back to their nests to feed their mutualistic fungus (of the family Lepiotaceae), which acts as a food source for the ants in exchange for the food.

Imagine being in that nest, inside a cavern full of warm, wet fungus.  Most organisms would be looking forward to gorging on this food source, or to growing there themselves.  The ants meticulously clean their fungus gardens and even secrete an antimicrobial acid to keep themselves from bringing in outside visitors, but is that enough to fend off the various microbial and fungal intruders?

In 1999, Cameron Currie (whose ant colony has a twitter account) identified a microbe (Streptomyces) living on the ants’ bodies that produces an antibiotic chemical.  He found this same microbe living not just on one, but many leaf-cutter ant species, including two genera of fungus-growing ants that evolved earlier than the leaf-cutters Atta and Acromyrmex we know and love.  This microbe produced an antibiotic that was very potent against a common garden-invading fungus, Escovopsis.  So it seemed that this was a 3 way mutualism: the ant, the fungus it feeds on, and the microbe that helps protect the garden.

Is anything in biology ever so simple?  The hunt began to find more bacterial antibiotic-producing symbionts.  Scientists have found many more symbionts and garden parasites, revealing the complexity of this ecosystem.  But the microbial symbionts aren’t always masked superheroes protecting the fungal garden: their antibiotics can also do harm to the farmed fungus itself.  Additionally, if there are many species of microbes around, an evolutionary arms race can emerge in which the microbes try to outcompete one another, creating stronger and stronger antibiotics which could be harmful.

Instead of simply listing off the species of microbes they discover on ants, Dieter Spiteller and his lab have been working to identify the antibiotics they produce.  This approach allows them to more easily identify what antibiotic types work on what pathogens and parasites and see what combinations of antibiotics show up together.  After all, the ants don’t care much about what species of microbe lives on them: only the benefit of the antibiotics.

Many of these microbial symbionts are not well-studied, if at all, so figuring out what type of antibiotic they are producing is a bit of a trick.  In their recent paper, the researchers used the evolutionary relationships of the symbionts – constructed using 16S rDNA sequences, which are commonly used to measure the “closeness” of two species – to find their closest relative that had already had its antibiotic identified by scientists.  This allowed them to narrow down their screen to look for the antibiotics that were most likely being produced by each bacterial species instead of having to screen for ALL of them.

They identified many types of antibiotics that fell into three main categories:  antimycins, valinomycins, and actinomycins, the latter so toxic that they aren’t used as antibiotics in humans due to damage to surrounding cells.  Then they tested the effectiveness of each antibiotic against a variety of pathogens and parasites that could endanger the nest: fungal pathogens of the gardens and insects, the common soil bateria Bactillus subtilis, microbial isolates taken from the ants and garden, and even the mutualistic fungus itself, Leucoagaricus gongylophorus.

The antibiotics varied in their strength and specificity.  Unsurprisingly, the most potent was the combination of the three – thus biochemical and microbial diversity is quite important to the success of these ants.  However, the antibiotics can have detrimental effects on other microbes living on the same ant (in particular actinomycin).  But this competition encourages the selection of stronger antibiotics in other species, which is beneficial to the ant and thus the symbiosis overall.

And that brings us back to that second image above: a visualization of the valinomycin distribution on a single ant.  As you can see, it’s pretty widespread – and is found more regularly in a high concentration than in the fungus gardens.  This makes logical sense: an ant would want to kill as many pathogens as possible BEFORE it brought the leaf into the nest.  But it also keeps the antibiotics from killing off too much of the ants’ fungus food.

To sum up: I just wrote a post about antibiotics produced by bacteria, which are competing for space on the back of an ant.  This ant climbs trees, cuts down leaf pieces, and carries them back to its nest to feed to a fungus which it then eats.  The antibiotics produced by the bacteria on its back keep pathogens at bay – protecting the fungus garden, thus the ant, and thus the bacteria. Phew! Currie, C., Scott, J., Summerbell, R., & Malloch, D. (1999). Fungus-growing ants use antibiotic-producing bacteria to control garden parasites Nature, 398 (6729), 701-704 DOI: 10.1038/19519

Schoenian, I., Spiteller, M., Ghaste, M., Wirth, R., Herz, H., & Spiteller, D. (2011). Chemical basis of the synergism and antagonism in microbial communities in the nests of leaf-cutting ants Proceedings of the National Academy of Sciences, 108 (5), 1955-1960 DOI: 10.1073/pnas.1008441108

Written by Hanner

February 8, 2011 at 10:20 pm

When adaptation doesn’t happen

“Evolutionary biology has been enriched by considering not only how adaptation happens, but also why it often does not happen,
or at least does not happen as we might naively expect.”

Douglas Futuyma (2010)

In 2005, a group of scientists from La Trobe University in Australia investigated how species will adapt to global warming by studying a species of rainforest fly, Drosophila birchii (later published in Science).  Increased temperatures may lead to drier conditions in rainforests, so the authors wanted to see how quickly this fly could adapt and develop resistance to desiccation.

As in many directed evolution experiments, they took the flies to a lab and exposed them to dry conditions, with most of the flies unable to survive the dryness.  The survivors were then bred to one another.  Thus generation after generation, only the most desiccation resistant flies would survive, resulting in a population that could survive dry conditions potentially induced by global warming.  Right?

Well, that was the idea at least.  At first, their population of flies did show a bit of increased resistance.  However, in the proceeding 28 generations of selection, there was no increased resistance to desiccation, despite that previous papers had found increased resistance in 3 other Drosophila species.  Drosophila birchii was unable to adapt to these conditions.  What went wrong?

The assumptions of natural selection

Natural selection itself is based on three assumptions in a population.  The first is that there will be variation in traits, such as multiple colors of eyes or hair.  The second is that these traits be heritable through the generations, that children will inherit the traits of their parents.  The third is that these variable traits have differential fitness, or that some versions of a trait might help you survive better than another.  Thus certain trait variants will help its carrier organism survive better, passing that trait to its offspring which will in turn bear this trait.

In order for populations to adapt by natural selection, these three requirements must be fulfilled.  When a biologist sees any population, he or she typically assumes that these they are met, and I can’t really blame them.  All cellular life we know of on this planet has a hereditary mechanism, the gene, which has differential fitness depending on the variation, thus meeting requirements two and three.

But what about requirement one, genetic variation in a population?  It has frequently been assumed to also exist in all populations.  In his 2010 review, Douglas Futuyma quotes the famous geneticist Richard Lewontin, who concluded in his 1974 book that “genetic variation relevant to all aspects of the organism’s development and physiology exists in natural populations,” for “[t]here appears to be no character—morphogenetic, behavioral, physiological or cytological—that cannot be selected in Drosophila.”

The idea here is that at any point in a healthy population, there will be many variants of genes in the population, which are replenished infrequently by new mutations.  Thus, when selective pressures come around, there is a full stock of variants to differentially survive and lead to new adaptations.  This is why small populations and inbreeding are considered such problems: the small gene pool means fewer gene variants and an increased inability to adapt to new conditions.

But why should this have to be true?  Is a lab-bred stock of Drosophila really enough to show that there is variation in natural populations, when the lab has a completely different set of selective pressures?

Selection bias in evolutionary studies

When the researchers studying the rainforest Drosophila birchii analyzed the genetic diversity of their collected populations, they found very low variation in the desiccation gene group compared to other genes in the population such as wing size.  This lack of variation prevented the flies from adapting to new conditions – though the researchers weren’t sure why.  Perhaps these dessication genes had (relatively) recently been under selective pressure, and had not had time to reconstitute the genetic diversity in the population.

Unfortunately, there are very few studies of this kind so it’s hard to draw any conclusions.  After all, people studying evolution usually want to study EVOLUTION IN ACTION and not evolution when it doesn’t happen.  I suspect that past experiments that have found low genetic diversity have been tossed simply because it seems less interesting evolutionarily – when maybe it is in fact more interesting.

This would be a form of selection bias: the choice of study populations or species unconsciously (or consciously) swayed by the desired outcome of EVOLUTION IN ACTION.  In his 1991 Croonian Lecture at the at the Royal Society, Anthony Bradshaw gave a compelling example of this sort of selection bias in evolutionary studies (published here).

In Prescot, Merseyside, a copper refinery opened up next to a meadow that had many species of grasses and wildflowers.  Over time, the soil was contaminated by copper, killing off many of the plants.  However, after 70 years, there were 5 species that were still able to thrive in these meadows!  They had adapted and developed a resistance to copper.

Even now I’m thinking to myself, “oh! cool!  How did they adapt that way?  How did that mechanism work?  How quickly did the resistance gene spread?” etc.  But what I’m forgetting is that, while five species did adapt, twenty-one species failed to adapt.  If there really was massive diversity at all genes in each population, you would think that at least one would confer some benefit to survive the copper.  But this did not happen: twenty-one species went locally extinct.

Just as interesting a question as “How did these 5 adapt?” is “Why did these 21 fail to adapt?”  But it’s a question that’s only begun to be reconsidered.  Death and extinction are far more powerful forces in shaping the whole of biodiversity on our planet than successful adaptation, but these evolutionary failures that occur all around us are little studied.  Especially as we anticipate global climate change causing unknown impacts on species worldwide, we should be studying non-evolution to get a better sense of what natural genetic variation actually looks like and what we may be facing in the future.

Literature Cited

Bradshaw, A. (1991). The Croonian Lecture, 1991: Genostasis and the Limits to Evolution Philosophical Transactions of the Royal Society B: Biological Sciences, 333 (1267), 289-305 DOI: 10.1098/rstb.1991.0079

Futuyma, D. (2010). EVOLUTIONARY CONSTRAINT AND ECOLOGICAL CONSEQUENCES Evolution, 64 (7), 1865-1884 DOI: 10.1111/j.1558-5646.2010.00960.x

Hoffmann, A. (2003). Low Potential for Climatic Stress Adaptation in a Rainforest Drosophila Species Science, 301 (5629), 100-102 DOI: 10.1126/science.1084296

Written by Hanner

January 5, 2011 at 10:58 am

Tiny tunicate throws structure to the wind

Today I bring you something extra special: A guest post from Lucas Brouwers of the world-famous blog Thoughtomics.  He loves genomes, I love plankton, and you get a great story involving spaceships, genomic party crashers, and, of course, a planktonic sea squirt.  Enjoy! Just below the surface of the sea, little animals are floating through a universe where the stars are made of plankton. They travel in what can best be described as gelatinous spaceships, which provide both shelter and food. They are Oikopleura dioica (Oikos is ancient Greek for house or household).

Their spaceships are ingenious constructions, made in such a way that every beat of Oikopleura‘s tail brings in a new flow water. The water and all the plankton it contains, is led through different tubings and chambers of the ship, until it reaches the waiting mouths of Oikopleura. The spaceships are not of a durable design and last for only a couple of hours before they are broken down again. Oikopleura spend the largest part of their short lives (5-10 days) repeating a cycle of building, feeding and destruction.

Oikopleura in its gelatinous house.

As small and short-lived as they may be, their genomes are evolving at at an extraordinary speed. A large team of scientists sequenced the full genome of Oikopleura recently, and found that its genome has been reorganized and trimmed down on an unprecedented scale.

One of the first things they noticed was the rapid evolution of introns in the genes of Oikopleura. Introns are the genetic equivalent of party crashers who show up at parties uninvited. They hang around inside genes, without coding for anything. Our cell have to force the introns out of messenger RNAs before they can properly be translated into proteins. Despite their apparent lack of use, many genes of distantly related animals have introns in exactly the same places. These introns have been conserved for millions of years, leading some to believe that they provide an evolutionary advantage somehow.

Oikopleura doesn’t care about these million year old traditions though. A staggering 76,2% (or 4.260) of its introns are unique to Oikopleura. Conversely, 3.917 of introns that are present in other animals (including close relatives) have been lost in Oikopleura. Not only do the newer introns outnumber their older peers, they are also good deal shorter than the few introns that have been retained.

But the extensive remodeling of the genome didn’t stop with introns. Normally, genes tend to hang out in similar neighborhoods in different species. There’s a good chance that two genes that are close to one another in mouse, are also close together in the human genome for example. Just like introns, many of these neighborhood relationships have persisted in species that are as far apart as humans and sponges.

Not so in Oikopleura. Its genes have been shuffled and switched around until the point that conventional gene orders are no longer recognizable. For small sets of genes the gene order in Oikopleura is closer to random than the gene order in other species.

The authors subtly hint at a potential cause for all this genetic upheaval: Oikopleura‘s genome lacks a full set of DNA repair genes. DNA is a robust molecule, but it can still be damaged. One of the nastier things that can happen is that both DNA strands of a single chromosome break. Cells can repair this type of damage in two different ways. The first way of repair works by taking a close look at the sister chromosome, and see how the damaged strands should be repaired, as shown in the video below. Another way is to directly seal the broken ends.

Oikopleura is lacking the genes for this last type of repair work. This means that every double strand break in Oikopleura‘s DNA can only be repaired via a sister chromosome, increasing the recombination rates (the exchange of genetic material between chromosomes) for Oikopleura. The causal link between the missing DNA repair genes and the accelerated evolution of Oikopleura‘s genome remains to be proven, but it isn’t hard to imagine how their absence could have played a large role in the overhaul of genomic architecture.

In addition to having a fast evolving genome, Oikopleura also has one of the smallest animal genomes (70 MB, compared to 3,174 MB for humans), which still contains some 18,000 genes (compared to ~21,000 in humans). Clearly, we don’t need that extra 3,100 MB for only a couple of thousand genes more. Compared to Oikopleura, our genomes are like attics crammed full of boxes and old furniture. Some scientists think that many features of our genomes (such as introns) are quite unnecessary, while others disagree. The debate boils down to this: are we keeping all the stuff because it is worth a lot, or because we never got around to throwing all the junk away?

Since Oikopleura was successful in redecorating and cleaning out its entire genome, our conserved genomic architecture might be nothing more than a product of historical contingency. In the small and slowly reproducing human population, natural selection might not be strong enough to remove all the unnecessary junk.

Despite the large genomic changes, Oikopleura has remained an animal in every way. While it might not be immediately obvious, they are very closely related to us vertebrates (animals that carry a backbone such as fish, reptiles, birds and mammals). They don’t have a spine, but they do have a lining of tough cells (a notochord) and a neural tube running through their entire bodies.

A juvenile Oikopleura Dioica. Notice the vertebrate-like appearance, Oikopleura has a notochord, nerve cord, separate head and tail.

Oikopleura belongs to a group of animals known as tunicates, or sea squirts. Most sea squirts live a sedentary life on the ocean floor where they filter plankton from seawater. They are basically hollow bags with two siphons – one for drawing seawater in, and the other to expel waste and water. But the solitary and free swimming Oikopleura don’t look anything like these stationary creatures, so what are these familial ties based on?

A different life stage holds the answer: every sea squirt starts its life as a larvae, looking very much like Oikopleura. After swimming around for a couple of days the larvae attach themselves to a comfortable looking outcropping and morph into the sedentary sea squirts. By retaining its larval features and delaying its further development, the ancestor of Oikopleura has permanently avoided the fate of settling down (these processes are known as neoteny and progenesis).

The similarity between vertebrates and sea squirt larvae implies that our own vertebrate ancestor once looked very much like larvaceans such as Oikopleura. Like Oikopleura, we are basically sea squirts that have never grown up. But unlike them, we still carry the baggage of 600 million years of animal evolution. I think there is much that we can still learn from the Peter Pans of the oceans.

Source for picture 1 and 2.

Denoeud F, Henriet S, Mungpakdee S, Aury JM, Da Silva C, Brinkmann H, Mikhaleva J, Olsen LC, Jubin C, Cañestro C, Bouquet JM, Danks G, Poulain J, Campsteijn C, Adamski M, Cross I, Yadetie F, Muffato M, Louis A, Butcher S, Tsagkogeorga G, Konrad A, Singh S, Jensen MF, Cong EH, Eikeseth-Otteraa H, Noel B, Anthouard V, Porcel BM, Kachouri-Lafond R, Nishino A, Ugolini M, Chourrout P, Nishida H, Aasland R, Huzurbazar S, Westhof E, Delsuc F, Lehrach H, Reinhardt R, Weissenbach J, Roy SW, Artiguenave F, Postlethwait JH, Manak JR, Thompson EM, Jaillon O, Du Pasquier L, Boudinot P, Liberles DA, Volff JN, Philippe H, Lenhard B, Crollius HR, Wincker P, & Chourrout D (2010). Plasticity of Animal Genome Architecture Unmasked by Rapid Evolution of a Pelagic Tunicate. Science (New York, N.Y.) PMID: 21097902

Written by Hanner

December 1, 2010 at 3:18 pm

If you feed them, they will come: the effects of nitrogen fertilization on community composition in a salt marsh

This post was chosen as an Editor's Selection for Eutrophication has gained a pretty bad reputation considering that it is a natural process.  The word itself comes from the Greek “eutrophia” which means “healthy” and simply means the addition of nutrients into an ecosystem encouraging plant growth.  Of course, there’s good reason why eutrophication has such negative connotations these days.  Since the industrial revolution, the amount of fertilizing nutrients, particularly nitrogen and phosphorus, entering ecosystems from runoff has doubled.  Just like your mother told you, too much of a good thing can be bad: too much nitrogen cause unlimited plant, algal, or phytoplanktonic growth.  When these organisms die, their decomposition uses up an incredible amount of oxygen, creating areas where these is little (hypoxic) or no (anoxic) oxygen.  One of the most famous areas for this overgrowth leading to hypoxia from eutrophication is the Gulf of Mexico dead zone, which is 6000-7000 square miles!

Satellite image of the northern Gulf of Mexico/Mississippi Delta showing hypoxic coastal water (light blue). This color change is due to excessive nutrients being washed into the sea. Source: Jacques Descloitres, MODIS Land Rapid Response Team, NASA/GSFC, January 2003.

But this is not necessarily how the story always ends.  A little bit of fertilizer runoff can actually fertilize natural ecosystems.  This typically increases the growth of plants or other photosynthetic organisms, whose growth is normally limited by the scarcity of nitrogen and phosphorus.  When there are more plants, there is more energy available to herbivores and, in turn, omnivores and carnivores, altering the food web.

So – as you can guess – we are very interested in studying how these food webs are changed, and how the fertilizer runoff from human activities alters the structure of communities.  One effect frequently seen is that the increase in nutrients allows rarer plant species the opportunity to grow.  This increase in plant diversity leads to a greater diversity of herbivores, since herbivores that only feed on one type of plant are drawn in.  Thus this increase in diversity of species can ripple throughout the system.

One question that ecologists have been asking is how a pure plant biomass increase would effect the diversity of herbivores, omnivores and carnivores in an ecosystem.  That is – not an increase in plant diversity, but a simple increase in the amount of food available.  This is a harder question to study than you might think.  Most ecosystems are diverse to start, and the rarer species with greater nutrient requirements are always looking for a way to wiggle their way in to grow and reproduce.

Spartina alterniflora-dominated salt marsh at College Creek in James City County (Colonial National Historical Park). Photo: Irvine Wilson / © DCR Natural Heritage.

A recent study in Ecology features some beautiful experiments that do a great job addressing this question.  Gina Wimp and her crew studied a salt marsh on the coast of Tuckerton, NJ.  Salt marshes are usually a monoculture: they only have one species of plant growing, a grass called Spartina alterniflora.  Not only is it a monoculture, but just one plant!  This grass species has a rhizomal root system, which can spread its roots underneath the soil and shoot up new stalks where it can find the resources and space.  So in miles of salt marsh, you will often find a single organism.  Pretty amazing!

The researchers used this monoculture to their advantage to see whether the species composition of the community changed when there was simply MORE Spartina available as a food source.  The researchers marked off three types of plots in the salt marsh.  One was an unaltered control plot, and the other two had “low” and “high” nitrogen additions 5 times throughout the 2-month growing period.  The “high” level was the maximum amount of nitrogen you could add without killing the Spartina.  They samples the insect communities 4 times during the season, and also took measurements of the changes in plant biomass and grass height when they sampled these insects with a D-vac suction sampler.  (Yes, a vacuum for bugs.)

What did they find?  Well, to start off, they did find significantly greater growth of Spartina in the fertilized plots, and it remained a monoculture, confirming what we already thought we knew.  (Phew!)  In the fertilized plots, they found not only more insects living on the grass, but a greater diversity of species, as you can see in the figure below.  The asterisks above the sampling date show that there was a significant difference between each nitrogen treatment – that is, the different in number of insects was large and consistent enough that it was not due to chance.  AND! On top of that, the actual communities of insects were also significantly different.


Arthropod species diversity and abundance in plots of Spartina alternifora grown under 3 different nitrogen fertilization conditions (control, low and high). Both diversity and richness increased with greater fertilization. From Wimp et al. 2010 (Ecology)

In summary: the increase in the amount of plant biomass alone (through fertilization) not only increased the number of insects and the number of different species sequentially, but also the relative abundances of each of those species to one another.  WHOAA!

What does this mean really?  Most of the focus on overfertilization from runoff has been on these dead zones and areas of hypereutrophication that I discussed earlier.  But this study shows that, even when plant diversity is unaffected, the addition of nitrogen and phosphorus affects not only plant growth, but what species are living in an area and how many of each are around.  That is: we are changing entire ecological communities.

On one hand, this seems like a good thing.  When a little bit of fertilizer reaches ecosystems, there is an increase in production and an overall increase in biodiversity, which we generally agree is a good thing.  But the problem with changing the structure of a community and even altering its food web is the potentially for causing a fundamental change in an ecosystem itself.  Seems like a strange concept – but what if the increase in growth brings in an organisms that somehow disrupts the growth of Spartina in the first place?  Then, while we temporarily have a buzzing, diverse community of organisms, the initial community could be lost, decreasing overall biodiversity.

I’m not trying to scare you or be a fearmongerer: but these are the extreme questions we have to ask when contemplating how our actions are influencing the typically balanced communities of organisms that surround us.  This truly beautifully-designed study gives us the information that communities can change just from more food resources being available.  And we can use this information to help regulate agriculture and prevent vast ecological changes from occurring that could be detrimental to the organisms, and us, in the end.

Wimp, G., Murphy, S., Finke, D., Huberty, A., & Denno, R. (2010). Increased primary production shifts the structure and composition of a terrestrial arthropod community Ecology, 91 (11), 3303-3311 DOI: 10.1890/09-1291.1

Written by Hanner

November 5, 2010 at 10:50 am

The Allee effect in action: why endangered Vancouver Island marmots are struggling to recover There are under 200 California condors alive in the wild.  There are under 600 wild Ethiopian wolves.  There are around 3500 wild tigers and under 5500 African wild dogs outside of zoos.

It has been ingrained in all of us that these are fearsome facts, that the very low population of a species means they are close to extinction (and with good reason).  But when you think about what this means – that a smaller population is less able to recover and grow in size – it doesn’t make perfect sense at first.  A small population should have more resources available for each individual because there is less competition within the species.  Additionally, there should be overall less predation on a lower population because, in a simplified model, this population will support fewer predators, and the predators are less likely to preferentially seek out a scarce animal in favor of other prey.  (For a primer on population ecology, check out this one I wrote up here.)  Why shouldn’t the animals be able to reproduce and increase the size of their population?

Despite these caveats, we see the pattern repeat itself: when a population of a species gets small enough, it seems to get stuck there, unable to recover its numbers.  Instead, it continues to shrink.

What is the cause of this?  In the 1930s to 1950s, an ecologist named Warder Cylde Allee described what was known afterwards as the Allee effect, this pattern of a decrease in the per capita reproductive rate in a species when the population gets to be too small.  Of course, “too small” is a variable number depending on the species and its life history traits, such as feeding preferences, natural range, and social behavior.

This is a notably difficult theory to study because it requires a foresight that we lack.  Identifying a species that is already at a critically low population isn’t enough.  To provide evidence for the Allee effect, scientists need to identify a threatened population before it becomes threatened in order to collect data on its range, foraging behavior, and social activity, and compare these data to similar traits when the population has gotten “too small.”  But if we had this sort of foresight, we hopefully would put in enough effort to prevent the population from dropping in the first place.

Vancouver Island Marmot

I am sorry to report that such a species has been identified, one that is on the brink of extinction: the Vancouver Island Marmot.  This large rodent (5-7 kg! 70 cm long!) is geographically restricted to Vancouver Island, and evolved rapidly after its arrival after glacial retreat 10,000 years ago.  It is an herbivore and lives in large burrowing colonies.  The cause of their population drop (from 300 animals in the 1980s to 25 (25!) in 2001) is not entirely clear, but is thought to be associated with increased logging.  A possible cause is that the clearcut forest from logging looked like prime meadow for setting up colonies, but the quick regrowth of these forests uprooted the colonies, scattering the animals.

A clear Allee effect in this population is shown in the figure below, from a study by Justin Brashares (UC Berkeley), Jeffery Werner (UBC) and A. Sinclair (UBC) in the September 2010 issue of the Journal of Animal Ecology. At the right side of the curve, decreases in Vancouver Island marmot population size resulted in a higher per capita reproductive rate.  But at a certain threshold (around 200 marmots), the curve turns downward, with a decreasing reproductive rate with decreasing population size.  This Allee effect is so evident from these data that I may as well have copied this figure from a population ecology textbook.

As the population size of Vancouver Island marmots decreases, so after a certain point, so does their reproductive rate, demonstrating an Allee effect. Figure from Brashares et al. 2010 (Journal of Animal Ecology)

The authors wanted to explore what changes in the marmots’ behavior caused this decrease in reproductive rate.  What exactly prevents these animals from reproducing effectively and recovering their population?  They collected data on the marmots’ activity budgets (where they spent their time) for comparison with a similar set of data from the 1970s.  They also used similar marmot species for comparison, as they only diversified 10,000 years ago.

They first looked at the modern home ranges of the marmots compared to other closely related species.  As they are colonial animals, marmots don’t frequently leave their burrow, and do so on a daily basis only to forage.  Males will leave to seek mates at other burrows, but historically burrows have been very dense and thus the males would not have to travel far.  As shown in the figure below, the Vancouver Island marmots have a modern range ten times larger than any other social marmot species.  This increase in travel and distance from their colony increases their exposure to predators, as they no longer have the alarm calls and protection of their colony.  The authors hypothesize that the marmots have increased their range due to a lack of mates nearby.  Thus the very process of increasing their reproductive rate is hindered because they cannot find mates, and when they go looking, are more likely to be killed by predators or get lost in unfamiliar territory.

Vancouver Island marmots have a home range ten times larger than any of the closely related social marmot species in order to search for scarce mates. Figure from Brashares et al. 2010 (Journal of Animal Ecology)

The authors also observed drastic changes in their social behavior.  Compared to historical Vancouver Island marmot behavior and that of other related species, the modern population spends far more time on watch for predators (nearly two-thirds of their above-ground time!), as predator populations have increased since the 1970s.  But despite these efforts, far fewer alarm calls were heard per animal, indicating that there are still not enough animals to properly stand watch for the colony.  By spending so much time on watch, they lose time for feeding, risking starvation, and forcing them to go into hibernation later, risking freezing to death.  Time in the burrow also increased, perhaps in an attempt to hide from predators and rest from the constant vigilance and lack of energy from decreasing foraging.

It’s a sad picture these authors have shown us.  These social rodents are travelling far distances alone in search of a mate, and spend most of their active time watching for predators instead of foraging for themselves and their offspring.  So hungry!  So cold!  And despite all this effort, their reproductive rate continues to drop!  Is there any hope?

The hope we have is in reintroduction programs.  The idea is that if we are able to successfully breed large numbers of marmots in captivity and raise them so that they can be reintroduced properly, we can increase the population to a suitable level that these animals are able to find mates and start reproducing again.  The Vancouver Island Marmot Foundation has a recovery plan and has been working to reintroduce the animals, which it has been able to do successfully.  (You can see their recovery plan on their website.)

I have long been a critic of zoos because I didn’t see how their conservation benefits outweighed the impacts of captivity on the animals kept there.  But this is why they are important.  The key is to keep a certain wildness in the animals so that, if their population does drop low enough to show an Allee effect, we have some hope for adding more animals to the population to help save the endangered species.

Brashares, J., Werner, J., & Sinclair, A. (2010). Social ‘meltdown’ in the demise of an island endemic: Allee effects and the Vancouver Island marmot Journal of Animal Ecology, 79 (5), 965-973 DOI: 10.1111/j.1365-2656.2010.01711.x

Written by Hanner

October 20, 2010 at 1:32 pm

The evolution of the eukaryotes and our human story

“Taxonomy and classification are funny,” my father joked recently, “because the organisms being classified really don’t care what they are. We’re the only ones who care!”

Well, at least I thought it was a good joke.  And it speaks to a certain truth: humans generally are obsessed with organizing and putting things into categories.  It is evident in the way we divide our music into genres (“Is this chillwave or witch house?”) or put our pants in a different drawer than our shirts. This may seem silly, but, with our consciousness and perception, we need to categorize in order to make sense of our world, to generalize, and, well, to help us find things.

We no longer have unicorns in our taxonomical literature. From the Ashmole Bestiary, 1504. Via BibliOdyssey.

Long before any ideas of natural selection and evolution as we know them now, people were trying to organize the natural world around them.  In 350 BCE, Aristotle published his History of Animals, which attempted to categorize the various “natures” of animals based on their characteristics.  For example, he identified what we now know as arthropods as animals that do not have blood and, “if they have feet, have many” (French 1994).  Some of his categorizations were not so on-par; for example, he placed foxes and snakes in the same category because they both burrow underground and thus have “sympathetic natures.”  Accurate or not, the effort is there: making sense of the world through categorization.

Although we’ve been at it for a long time, we are not close to being finished identifying all extant species, much less cataloging them.  Just this week it was announced that, due to double-counts, the estimate of the number of flowering plant species will be cut by 600,000.  600,000!  And those are just the plants that are living today, excluding all the known and unknown species that have gone extinct.

It would be easy to say, “whatever, who cares about the extinct ones?  If I’m categorizing to make sense of the world, I want to pay attention to the world I’m living in.  Leave the past in the past, man!”  But if people view the world as stories as I believe we do, we need this history of organisms to construct our narrative1.

A basic illustration of the 3 domain system of taxonomy. The yellowish circles indicate the 3 nodes and the 3 domains of the Bacteria, Eukarya and Archaea. The Eukarya and Archaea share a common ancestor but evolved separately from there. Not to scale in terms of time or breadth. Drawn by Hannah Waters.

And, in particular, we need to know the history of our own species: where do we fit into the puzzle?  How far back can we trace our own ancestors?  When I was 14, I was taught that we are part of the Animal Kingdom, one of the five kingdoms of life.  When I was 17, I was instead taught the three domain system: the Bacteria, the Archaea, and the Eukarya, a classification developed by the microbiologist Carl Woese in the late 1970s.  This new system organized the world based on cell type, in particular dividing the Monera, which previously described all single-celled life, into the Bacteria and the Archaea, which are each single-celled but have many differences in structure.  (See this great post by Labrat for more information on their distinction.)  No longer were we humans described as “animals” as in ancient times, but rather based on an ancient ancestor, the first to embody the type of cell that makes up our bodies.

In the three-domain system, we eukaryotes are more closely related to the archaea, but evolved separately from a common ancestor (sister lineages).  We evolved a unique nucleus composed of specific proteins, and later acquired mitochondria or plastids from bacteria through endosymbiosis.  However, a different hypothesis has arisen in the past couple of decades: the 2-domain system.  In this system, the Eukarya are even more closely related to the Archaea.  In fact, we are a subgroup, having evolved from a singular lineage within the Archaea.  A mere secondary domain, replacing Eukarya as a “primary domain” or sister lineage as put forth in the 3-domain system.

A basic illustration of the 2 domain system of taxonomy. The yellowish circles indicate the 2 nodes and the 2 domains of the Bacteria and Archaea. Of note is that the Eukarya evolved from the Archaean domain. Not to scale in terms of time or breadth. Drawn by Hannah Waters.

Why is the 2-domain system being considered at all?  The Archaea and Eukarya share many of the same components of their genetic information systems, such as over 30 ribosomal proteins, RNA polymerases, transciption factors, promoters to initiate transcription of the genome, and replication enzymes (Gribaldo et al. 2010).  A general tenet of constructing phylogenies, evolutionary trees through time, is that the simpler answer is usually better.  Proponents of the 2-domain system argue that it is simpler for these genetic pathways to have evolved once in the older domain, the Archaea, and been retained in the newer subdomain, the Eukarya.  Proponents of the 3-domain system hold that these systems evolved earlier before the lineages split and were preserved in both the groups over time.

Eukaryotes also share many genes with the Bacteria, even more than with the Archaea.  Do these genes “even out the score” and support the 3-domain system, or were they acquired as a remnant of bacterial endosymbiosis?  An early edition PNAS paper (2010) by James Cotton and James McInerney of the National University of Ireland argues its title: “Eukaryotic genes of archaebacterial origin are more important than the more numerous eubacterial genes, irrespective of function.”

The authors compared every gene in the yeast genome to bacterial and archaeal genomes, finding that 952 genes have bacterial homologues, while 216 show homology to archaeal genes.  Using these genes, they performed two main tests.  First, they examined how frequently each of these genes killed the cell when deleted from the genome – a test to see just how imperative each is to the cell’s survival.  They found that lethal genes are twice as likely to be of archaeal origin than bacterial origin, giving the Archaea one “important point” in their book.  Second, they looked at how frequently these genes were actually transcribed, or copied into a form from which they can be made into proteins.  Using RNAseq, they found that there was significantly more expression of genes with archaeal homologues than bacterial.  Another “important point” for Archaea.

This study seems to support the 2-domain hypothesis: the genes that come from Archaea are used more frequently and are more necessary for cell survival, despite being fewer in number than Bacterial genes.  But remember: both systems of taxonomy support the idea that Eukarya are more closely related to Archaea.  Importance is merely a factor of correlation, not evolutionary causation.  It provides evidence that the two domains are related, but not the direct evolution of Eukarya from the line of Archaea.

These lineages have been diverging from one another for at least 2.5 billion years – it seems like a bit of a stretch to be doing genomic studies at all!  Think of all the mutations and changes that have been made in the DNA over those 2.5 billion years, obscuring the true relationships and further separating these domains morphologically.  A review coming out next month in Nature Reviews Microbiology goes through a number of studies that attempted to analyze eukaryotic evolution and found that none drew a strong conclusion, or even found conflicting results, “despite analyzing largely overlapping data sets of universal genes.”  They conclude that “it is premature to label any one of these analyses as definitive” and that these large-scale genomic studies have “not yet yielded a resolution to this debate and ha[ve], if anything, intensified it.”

Even if we did know the truth, what would this mean for the “story of human evolution” I was babbling on about earlier?  Well, it means that we’re Archaea deep down!  Those badasses who live in hot springs and sulfur!  We had the potential to be hardy, tough organisms, but instead we’re frail and get cold really easily and get hunger pangs after just a few hours…

More than anything, the fact that this debate exists in the first place gives us a great perspective on our story.  Under 2500 years ago, Aristotle categorized foxes and snakes together.  Now, we’re splitting hairs over the type of ancient cell that foxes, snakes, and ourselves evolved from over 2.5 billion years ago.  It provides the history of our progress.  And look how far we’ve come!

1 Of course there are many applications for studying evolution beyond a desire to learn about our own history.  This 2005 interview with Massimo Pigliucci, an evolutionary biologist at SUNY Stony Brook, and the 1998 collective paper “Evolution, Science and Society: Evolutionary Biology and the National Research Agenda” are good places to start.

NOTE: Molecular evolution is incredibly hard to explain (in my opinion), and I did my best to do so in English.  If you have any questions or think some parts need clarification, please let me know in the comments or write me at hannah.waters [at]  I’d really appreciate it! Thanks!

Cotton, J., & McInerney, J. (2010). Eukaryotic genes of archaebacterial origin are more important than the more numerous eubacterial genes, irrespective of function Proceedings of the National Academy of Sciences DOI: 10.1073/pnas.1000265107

French, Roger.  Ancient Natural History.  New York: Routledge, 1994.

Gribaldo S, Poole AM, Daubin V, Forterre P, & Brochier-Armanet C (2010). The origin of eukaryotes and their relationship with the Archaea: are we at a phylogenomic impasse? Nature reviews. Microbiology, 8 (10), 743-52 PMID: 20844558

Written by Hanner

September 29, 2010 at 7:52 am

Can seabirds overfish a resource? The case of cormorants in Estonia

This post was chosen as an Editor's Selection for

Published in Open Lab 2010, a print compilation of the best science blog posts of the year.

“Overfishing” is a term associated with resource depletion, extinction, and human greed.  While the definition of overfishing is technically a subjective measure (How much fishing is too much?), it has been widely accepted to mean catching more of an aquatic resource than can be replenished naturally by the system.  The idea of depleting a marine resource is ubiquitous and familiar these days, with the bluefin tuna even featured as the cover article of the New York Times Magazine this past June.

That’s a lot of mackerel for one net! Image: NOAA

The idea may be commonplace now, but this was not always so.  A 2003 paper by Nicholas Dulvy and others enumerates the reasons why it was long believed that marine populations were more resilient than terrestrial species, and less likely to go extinct due to overfishing, habitat loss, invasive species, disease, and other causes.  Jean Baptiste de Lamark himself was a proponent of the “paradigm of ocean inexhaustibility” due to the high fecundity of fish.  He (and others) argued that because fish lay so many eggs and have excessive offspring (with little care put into each), we could never actually catch enough of a population to cause any damage.  One problem with this argument is that fecundity often increases with size of an individual.  Since we selectively catch larger fish, we’re catching the most reproductively able of a population and causing a large impact per fish caught.  Other arguments about the impossibility of aquatic extinction include broad geographic range and dispersal, and that economic extinction of a fishery would precede biological extinction of a species (all of which have counter-arguments).

In all the discussion of overfishing, it is always humans that are doing the fishing to the detriment of non-human species, either through depletion of a fished species itself, or by reducing resources for other species that rely on it for prey.  It is we humans who must reduce our impacts and allot resources for other species on our fair planet.

Last month (August 2010), an article from ICES Journal of Marine Science asks whether humans are the only species capable of overfishing.  More interesting than the research itself is the questions it raises about our own relationship with “nature.”

The story of cormorants in the Baltic Sea


The Great Cormorant (Phalacrocorax carbo) is a seabird that lives in the Baltic Sea, along with many other locales.  According to the Helsinki Commission, in the 1950s and 1960s the bird was overhunted to near-extinction locally, at which point they were put under government protection.  Over the rest of the 20th century, the bird population improved dramatically, recolonizing old haunts with great success.  They were so successful that they began expanding their original range, initially colonizing Estonia in 1983.  In 2005, there were 20 great cormorant colonies in Estonia with an estimated 10,000 nesting pairs.

Over the course of this period, fishing decreased in Estonia waters, in part to conserve the estuarine wetlands that are important for bird migration and fish spawning.  Despite this, many commercially valuable fish stocks plummeted.  Though working with a limited data set (fish were sampled only in 1995 and 2005), in the ICES paper, the scientists satisfactorily concluded that this loss of fish species was due to overexploitation, not by humans, but by these great cormorant colonies.  The cormorants were fishing 10-20 times more than the commercial catch of fish species such as perch Perca fluviatilis and roach Rutilus rutilus, decreasing the fishes’ ability to recover year after year.

Population development of the Cormorant in the eastern and northern Baltic (Estonia and Finland). Data from SYKE (2008, 2009), Lilleleht (2008), and Evironmental Board of Estonia (2009, pers. com). From the Helsinki Commission

How this questions our typical relationship with “nature”

This is an interesting story for several reasons.  The birds were able to spread their range as far as they did and, in the end, compete with humans for food resources because we were trying to protect them.  Their near-extinction in the 1950s probably led the government to be hesitant to lift protection because the birds were no longer birds, but a symbol of species recovery.  After such a great success, how could we take their resources away and potentially lead them to extinction once more?

The fact alone that they are seabirds also makes their presence hard to define.  Some cases of “invasive species” are very clear cut.  For example, brown tree snakes are not from Guam, but were brought there and are now wreaking havoc on native animal populations.  But seabirds toe the line.  They are able to fly anywhere, and simply live on colonies at sea.  Who are we to determine where geographically those colonies exist?  The authors of the paper do not even use the word “invasive” to describe the expansion of great cormorants into Estonia until the end of the paper.

Are these birds invasive?  It depends on your definition of the term.  Some would argue that, yes, they did not live there before but do now, and are affecting the ecosystem to the detriment of other species.  But it’s all relative: invasive species are defined by an anthropocentric view of the world, in which what is “natural” is the distribution of organisms we initially encountered and recorded.  But who are we to decide that a species belongs or does not belong in a certain place?  Who are we to tell the cormorants that they cannot live on that rock near an ample food supply?  We’re the only species that sets these sorts of boundaries; all the other species are just trying to utilize resources and survive.

The idea that humans are the only species able to overexploit a resource is also anthropocentric.  It makes Homo sapiens the center of the world, the ones who determine the fate of all other organisms, who can harvest them for ourselves or choose to spare them.  This case of the cormorants places us back in our role as a competitive species: we have to decide whether or not we are willing to take back our resource, even if it means losing some of these big, aesthetically-valuable cormorants.  We are no longer the masters of nature, but rather are inserted back into it.

I hope I manage to keep up with this case and find out what happens in Estonia.  At this point, “taking back our resource” would not mean going in and competing by fishing; there are too many cormorants, so we would simply deplete the resources further.  Instead, the Estonian government would have to enter the colonies and manage the population through oiling or pricking eggs to kill the developing birds (the Helsinki Commission estimates that this is done to 18% of nests in Denmark).  Already 10,000-20,000 birds are shot in the Baltic Sea area each year, but public protests limit the amount of population control that is performed.

We may have simply lost control of the situation at this point.  There may just be too many cormorants to keep them from overfishing, for our own sake or to preserve the fish as an ecosystem resource.

Dulvy, N., Sadovy, Y., & Reynolds, J. (2003). Extinction vulnerability in marine populations Fish and Fisheries, 4 (1), 25-64 DOI: 10.1046/j.1467-2979.2003.00105.x

Vetemaa, M., Eschbaum, R., Albert, A., Saks, L., Verliin, A., Jurgens, K., Kesler, M., Hubel, K., Hannesson, R., & Saat, T. (2010). Changes in fish stocks in an Estonian estuary: overfishing by cormorants? ICES Journal of Marine Science DOI: 10.1093/icesjms/fsq113

Written by Hanner

September 17, 2010 at 9:33 am

Marine Snow: dead organisms and poop as manna in the ocean

Edit: Republished at the American Society for Microbiology blog, Small Things Considered

“When I think of the floor of the deep sea…I see always the steady, unremitting, downward drift of materials from above, flake upon flake, layer upon layer…the most stupendous “snowfall” the earth has ever seen.”
-Rachel Carson, The Sea Around Us (1951)

This post was chosen as an Editor's Selection for Marine snow: does the phrase make you think of fish wearing ice skates, seahorses in knit caps, and crabs building snow-fish? If so, I can’t entirely blame you: the stuff looks like snow, hence its name. But marine snow is not composed of frozen water, each flake unique and beautiful. It is, in fact, made up entirely of dead organisms, poop, and random junk floating in the ocean. (Still fancy a marine snowball fight?)

To undergo photosynthesis, marine phytoplankton (the “wandering plants” in Greek) can only live in the sunlit areas (the photic zone) of the ocean, which rarely reaches a depth greater than 200 meters. The phytoplankton do their thing, you know, generate nearly half of the planet’s primary production (no big deal?!), until they are either eaten or die. And when you’re living at the top of a miles-deep ocean, the only way to go is down. And thus we have marine snow.

Marine snow is complicated stuff.  While initially it is mostly composed of dead material, slowly drifting downward, overtime it is affected by many processes that create an indescribable mass of fluff and particles and organisms stuck together.  But along the way, it continues to sink, until eventually it reaches the seafloor, often miles down.  And it needs to reach that destination, as it is a primary source of carbon for deep sea organisms who have no light by which to photosynthesize.

Rattail swimming out of a cloud of marine snow near the bottom of the northern trench of the Charlie-Gibbs Fracture Zone (4400 m, June 2003) - Taken as part of MAR-ECO project through CFML

A floater or a sinker?

But how does a clump of algae or cells manage to sink for miles?  By straight physics alone, a particle in still seawater would take years to reach the seafloor.  Add to that waves, currents, water stratification, and you have some particles that aren’t going anywhere.  Many studies have provided evidence that most movement takes place when the phytoplankton have been ingested and egested as fecal pellets (i.e. poop).

An environmentally sobering study done in 1987 and published in Nature presents strong evidence for the increased sinking rates of fecal pellets.  After the Chernobyl Disaster in 1986, when a nuclear power plant blew out and released radioactive fallout, scientists studying vertical transport in the ocean decided to make the best of the tragedy.  Several days after the disaster on April 26, 1986, rain fell on the ocean, delivering the radioactivity to the surface of the water.  The scientists had already set up particle traps at 200 meters depth and, upon review, found that radioactivity was found in the traps just 7 days after the rainfall, with an average sinking rate of 29 m/day.  Physics predicted that radioactive particles would take years to reach this depth!  To explain this discrepancy, the authors identified the particles as fecal pellets and – lo and behold! – the high sinking rate was explained by the repackaging of these radioactive particles through ingestion and then egestion by zooplankton.  The fecal pellets were larger in size and more dense, and thus able to sink more rapidly through the water column.

But not all fecal pellets are created equal; many factors contribute to their size and density, which in turn determines how fast they will sink and quickly they will deliver carbon and nutrients to deeper waters.  Different “types” of feeders, for example, have different efficiencies of repackaging as particles.  Carnivores tend to eat larger food and make it smaller, while grazers such as filter feeding mollusks or some zooplankton species collect tiny, slow-sinking particles and collect them into a larger fecal pellet, greatly increasing the sinking rate of those particular particles.

In the below figure, from a 2001 Bioscience paper entitled “Feces in Aquatic Ecosystems,” data on sinking rates of various taxa are shown.  However, these data need to be taken with a grain of salt.  These are sinking rates from individual studies taken in different years in different parts of the ocean.  Fecal pellet sinking rate is determined not only by repackaging efficiency by species, but also by the organisms’ diets, water turbulence at the surface, water stratification, season, and even time of day.  But what it does show is how variable sinking rates are, even for something as simple as a little speck of poop.

Sinking rates of fecal pellets of different taxa. Image from Wotton et al. (2001). Numbers at the end of taxa names refer to the paper data originates, which is detailed at the end of this post.

But the wild trip isn’t over for organic carbon bound up in fecal pellets.  As they sink, they get stuck in larger pieces of marine snow.  They start to degrade from friction alone, but also from grazing organisms or microbes that are living on them*, creating more drag and slowing their sinking rate.  And then, inevitably, a fish or a zooplankter comes along and eats them, transporting the carbon back up to the surface or down deeper until they are re-released as a fresh pellet, and the cycle begins again.

Salps, a zooplankton species, can form huge schools (275 individuals per cubic meter!), and are well known for their voracious feeding on phytoplankton. They are incredibly efficient repackagers. Their fecal pellets sink rapidly, and the bodies of the dead salps themselves provide a large amount of carbon to the seafloor. (See Iseki 1981, citation at bottom)

It seems like such a long and hard way to travel: passively drifting for miles, eaten and pooped out over and over again.  How does marine snow ever make it to the seafloor?  We had photographs of marine snow at the seafloor, but its existence did not seem to make sense.  Paper after paper reported that marine snow in the water column decreases with depth due to much grazing in the euphotic and mesopegalic (where light reaches, but not enough for photosynthesis) zones.  Most papers rely on sediment traps: essentially a huge funnel to collect small particles.  A 1993 Nature paper evaluated this method itself, and suggested that it severely underestimates the volume of marine snow in the water column.  But there had been no detailed studies yet quantifying marine snow volume in multiple locations and depths.

That is… until this May (PNAS, 2010), when the marine snow veterans Alexander Bochdansky, Hendrik van Aken, and Gerhard Herndl decided to try a new method: quantification through photographic analysis and optical backscatter.

On a research vessel, the team traversed a 4000 km horizontal transect across the Atlantic, including area over the Romanche Fracture Zone, which at 6000 meters is the deepest section of the mid-Atlantic Ridge.  The researchers threw lights at sections of water at particular angles, and the light reflected back by particles was visible in photographs (>500 um).  They additionally used a Seapoint Turbidity Meter, which quantifies light reflected off of very small particles in the water through voltage.  By running these tests at 17 points along their transects, and at these points, from the surface to the ocean floor, the researchers were able to visualize a bigger picture for particulate and marine snow suspension in the ocean.

This figure shows the number of particles per frame (colored bar on right, blues indicating few pellets and warmer reds indicated high pellet number) along their 4000 km transect (x-axis) by depth (y-axis). From Bochdansky et al. 2010 (PNAS).

The figure above shows this picture.  In the upper 2000 meters of the ocean, marine snow abundance is high, gradually decreasing with depth, with microscopic particles more abundant than macroscopic ones.  But below 2000 meters, there is an increase in marine snow overall, and there are greater numbers of macroscopic particles than microscopic.  The researchers also looked at oxygen rates in each frame they selected, and found a significant negative cross-correlation between oxygen values and particle volume, or more particles meant less oxygen.  This suggests that there is greater oxygen consumption at particles, indicating microbial respiration.

The authors suggest that, at greater depths, the marine snow particles and fecal pellets form larger aggregates, which slows their sinking rate due to increased drag and decreased density.  These are larger particles that are sinking very slowly or are neutrally buoyant, and are thus not caught in sediment traps.  The particles that are able to escape the highly grazed areas of the mesopelagic clump together in the deep, but are less rapidly consumed because there are simply fewer organisms around to consume them.  Slowly but surely they sink down, providing carbon to the depths and forming “hotspots of biological activity.”

In light of recent research: ecosystem effects of decreased phytoplankton

Marine phytoplankton have been hot in the news lately: Daniel Boyce and Boris Worm published a study in Nature (covered well by others) reporting that over the last century, marine phytoplankton biomass has decreased by 1% per year.  You read right: the organisms that produce nearly half of our oxygen and absorb a significant amount of carbon dioxide are disappearing at an alarming rate.

Much of the coverage has focused on the climate change aspect of this study.  Phytoplankton are a huge carbon sink, and it was assumed that increased temperatures through climate change would actually increase their growth.  But – alas! – the decrease in phytoplankton biomass actually correlated with increased sea surface temperatures.  So the exact opposite of what we predicted would happen is occurring, according to this study.

But I’m an ecologist: what does this decrease in phytoplankton mean for the marine ecosystem?  As I’ve explained throughout this post, phytoplankton are the primary energy source for the ocean.  They themselves convert sunlight to energy, are eaten by other organisms, and then this poop slowly sinks to the deep-sea to provide food for organisms living on the seafloor.  In his 2002 review, Jefferson Turner argues that seasonal mass sinks of phytoplankton and algae biomass are vital for survival for deep-sea organisms.

While we probably haven’t lost enough phytoplankton to cause great loss in the deep, it’s something we should be thinking about.  A tenet of ecology is that a change in the abundance of one organism can have cascading effects through an ecosystem, in turn affecting the abundances of many others.  The thought of losing a primary carbon sink is unsettling; but the thought of removing a crucial food source for most of the ocean is far more horrifying.  It seems unlikely enough that a fecal pellet would reach the deep on its own even with the relative abundance of phytoplankton that exists now.  Losing a significant amount of phytoplankton could have grave impacts through the entire ocean ecosystem.  I don’t think we want to know the end of that story.

* Fecal pellets as microhabitats or even islands is a fascinating subject.   A 1978 Science paper found that there is greater taxonomic diversity on pellets than in the open water, and that the species living in and on pellets is significantly different that those in the water.  Also, organisms that survive gut passage (microbes and invertebrates) are often released, live, in fecal pellets.  For more on this, see this recent paper on applying island biogeography to fecal pellets.

Fecal pellet sinking rates figure:

(1) Turner JT. 1977. Sinking rates of fecal pellets from the marine copepod Potella meadii. Marine Biology 40: 249–259.
(2) Alldredge AL, Gotschalk CC, MacIntyre S. 1987. Evidence for sustained residence of macrocrustacean fecal pellets in surface waters off Southern California. Deep-Sea Research Part A: Oceanographic Research Papers 34: 1641–1652.
(3) Smayda TJ. 1969. Some measurements of the sinking rate of fecal pellets. Limnology and Oceanography 14: 621–625.
(4) Deibel D. 1990. Still-water sinking velocity of fecal material from the pelagic tunicate Dolioletta gegenbauri. Marine Ecology Progress Series 62: 55–60.
(5) Ladle M, Welton JS, Bell MC.1987. Sinking rates and physical properties of faecal pellets of freshwater invertebrates of the genera Simulium and Gammarus. Archiv für Hydrobiologie 108: 411–424.
(6) Fowler SW, Small LF. 1972.Sinking rates of euphausiid fecal pellets. Limnology and Oceanography 17: 293–296.
(7) Ladle M, Welton JS, Bell MC.1987. Sinking rates and physical properties of faecal pellets of freshwater invertebrates of the genera Simulium and Gammarus. Archiv für Hydrobiologie 108: 411–424.
(8) Yoon WD, Marty JC, Sylvain D, Nival P. 1996.Degradation of faecal pellets in Pegea confoederata (Salpidae,Thaliacea) and its implications in the vertical flux of organic matter. Journal of Experimental Marine Biology and Ecology 203: 147–177.
(9) Taghon GL, Nowell ARM, Jumars PA. 1984. Transport and breakdown of fe- cal pellets: Biological and sedimentological consequences. Limnology and Oceanography 29: 64–72.

Bochdansky, A., van Aken, H., & Herndl, G. (2010). Role of macroscopic particles in deep-sea oxygen consumption Proceedings of the National Academy of Sciences, 107 (18), 8287-8291 DOI: 10.1073/pnas.0913744107

Boyce, D., Lewis, M., & Worm, B. (2010). Global phytoplankton decline over the past century Nature, 466 (7306), 591-596 DOI: 10.1038/nature09268

Fowler, S., Buat-Menard, P., Yokoyama, Y., Ballestra, S., Holm, E., & Nguyen, H. (1987). Rapid removal of Chernobyl fallout from Mediterranean surface waters by biological activity Nature, 329 (6134), 56-58 DOI: 10.1038/329056a0

Goldthwait, S., Carlson, C., Henderson, G., & Alldredge, A. (2005). Effects of physical fragmentation on remineralization of marine snow Marine Ecology Progress Series, 305, 59-65 DOI: 10.3354/meps305059

Iseki, K. (1981). Particulate Organic Matter Transport to the Deep Sea by Salp Fecal Pellets Marine Ecology Progress Series, 5, 55-60 DOI: 10.3354/meps005055

Lampitt, R., Hillier, W., & Challenor, P. (1993). Seasonal and diel variation in the open ocean concentration of marine snow aggregates Nature, 362 (6422), 737-739 DOI: 10.1038/362737a0

SILVER, M., SHANKS, A., & TRENT, J. (1978). Marine Snow: Microplankton Habitat and Source of Small-Scale Patchiness in Pelagic Populations Science, 201 (4353), 371-373 DOI: 10.1126/science.201.4353.371

Turner, J. (2002). Zooplankton fecal pellets, marine snow and sinking phytoplankton blooms Aquatic Microbial Ecology, 27, 57-102 DOI: 10.3354/ame027057

WOTTON, R., & MALMQVIST, B. (2001). Feces in Aquatic Ecosystems BioScience, 51 (7) DOI: 10.1641/0006-3568(2001)051[0537:FIAE]2.0.CO;2

Written by Hanner

August 19, 2010 at 11:33 am

Posted in Journal Article