Category Archives: Mind & Brain

Sharks have rhythm, too

Sharks are not known for being good at running in running wheels. Or hopping from one perch to the other in a birdcage. Which is why, unlike hamsters or sparrows, sharks were never a very popular laboratory model for circadian research.

The study of fish came late into the field of chronobiology due to technical difficulties of monitoring rhythms, at the time when comparative tradition was starting to make way to the more focused approach on choice model organisms – in this case, the zebrafish.

But the comparative tradition was always very strong in the field. Reading the old papers (especially review papers and loooong theoretical papers) by the pioneers like Jurgen Asschoff and Colin Pittendrigh, it seems like researchers at the time were just going around and saying “let me try this species…and this one…and this one…”. And there were good reasons for this early approach. At the time, it was not yet known how widespread circadian rhythms were – it is this early research that showed they are ubiqutous in all organisms that live at or close to the surface of the earth or ocean.

Another reason for such broad approach to testing many species was to find generalities – the empirical generalizations (e.g,. the Aschoff’s Rules) that allowed the field to get established, and that provided a template for the entire research program, including refining the proper experimental designs.

Finally, this was also a fishing expedition (no pun intended…oh, well, OK, intended) for the best model organisms on which to focus more energies – organisms that can be studied in great detail in both field and lab, that are easy to find, breed, care for, house and handle, and organisms in which circadian rhythms are clear, robust, and are easy to monitor with relatively cheap and simple equipment. Thus hamsters, cockroaches, and sparrows, green anoles and Japanese quail. Later, with molecular discoveries, organisms with better tools for genetic manipulation, even though perhaps not as good as circadian models, took precedence – the fruit fly, mouse, zebrafish and the like.

But it’s not that sharks were never looked at before. They may not run in wheels, but researchers can be creative and monitor the rhythms nonetheless.

Horn Shark and Swell Shark

The Nelson and Johnson 1970 paper appears to be the very first systematic study of daily rhythms in sharks. They cite a number of previous non-systematic observations in the field, all suggesting that many shark species are nocturnal (night-active). They combined field and lab studies in two species (horn shark Heterodontus francisci and the swell shark Cephaloscyllium ventriosum).

Pattern of activity of bottom-dwelling sharks in the field. From Nelson and Johnson 1970.

In the field, they dove at different times of day and night, counted and observed the sharks, and rated their activity levels. Both species were exclusively nocturnal, barely making any movements at all throughout the day, while actively swimming at night.

In the lab, they placed sharks in small pools, each pool in a light-tight enclosure. They controlled lighting regimes (e.g., constant dark, constant light, or various light-dark cycles) and they monitored the activity with a nifty sensor – a set of six steel rods in each pool, each rod hanging from above all the way to the bottom of the water. Whenever a fish pushed one of the rods (and they did not observe any avoidance), the rod would move and momentarily close an electrical circuit. This would be recorded as a dash line on long paper rolls by an Esterline-Angus recorder.

Afterward, they would take those paper rolls out, cut them (by hand) into strips, glue the strips (by hand) onto large pieces of cardboard, do the measurements and calculations (by hand, using rulers and compasses), and photograph the best records for publication. Yes, very manual work! In this day of computers, it’s pretty easy to just click. Our PI used to sometimes take us grad students to a back room to show us the old equipment and to describe the process, just so we would appreciate how easy we have it now.

Actograph of the Swell shark in different light conditions. From Nelson and Johnson 1970.

What they found is that the two species are quite different. The Horn shark readily entrained to the light-dark cycles (both 24-hour and 25-hour cycles), starting activity as soon as the lights go off, and ceasing activity the moment the light come back on. They kept swimming all the time both in constant darkness and in constant light. This suggests that their behavior is triggered directly by environmental light and not driven by an internal clock.

On the other hand, the Swell sharks showed circadian rhythms – they alternated between active and inactive periods in constant light and in constant darkness. In light-dark cycles of both durations, they showed a little bit of anticipation, starting their activity a few minutes before lights-off. This suggests that the daily alteration of behavior is driven by an internal circadian clock.

In a later study (Finstad and Nelson 1975), they changed the intensity of light of the experiment, and this time Horn sharks also exhibited internally generated circadian rhythms.

Dogfish Shark

Daily rhythm in the dogfish shark. From Casterlin and Reynolds 1979.

In 1979, Casterlin and Reynolds tried a different experimental setup and a different species – smooth dogfish shark, Mustelus canis. In their setup, as sharks swim through a series of chambers they break photocell-monitored light beams. Instead of simple light-dark cycles, they used light-dusk-dark-dawn cycles in which dawn and dusk light was dim, while daytime light was bright. Again, most of the activity was observed during the night:

Lemon Shark

In 1988, Nixon and Gruber took a bunch of Lemon sharks (Negaprion brevirostris) and placed them in a complex setup in order to simultaneously monitor both locomotor activity (that is: swimming around and around in circles) and the metabolic rate (oxygen consumption):

The lemon shark setup. From Nixon and Gruber 1988.

Daily rhythms of activity (top) and metabolic rate (bottom) in the Lemon shark. From Nixon and Gruber 1988.

The sharks were only tested in light-dark cycles, which is not a proper test for the existence of the circadian clock, but the data were strikingly “clean”. While behavior can be strongly affected by direct influence from the environment (e.g., sudden lights-on), it is harder to explain changes in metabolic rate purely behaviorally, suggesting that an internal clock is likely driving the day-night differences in metabolism.

Megamouth Shark

Megamouth shark daily dives. From Nelson et al. 1997.

This big guy is hard to find. The subject of this paper was only the sixth individual known to science. It was caught, they scrambled for about a day to get all the gear in place, attached satellite telemetry radiotransmitters, and let the animal lose to swim. What they saw was a distinct pattern of diving deeper before the sunrise, and rising up closer to the surface before sundown. While nothing can be said about circadian regulation, as the pattern could just be the animal following light clues or vertical migration of its plankton food, it is nonetheless a very cool study.

Hammerhead Shark

It is interesting that a number of senior researchers, as they come close to retirement and are not in the rat-race for grant funding any more, abandon the standard lab models and go back to the old comparative tradition, picking unlikely species (from chipmunks to Monarch butterflies) and moving out of the lab back into the field. It’s definitely more fun to do!

One of them decided to shift his focus to juvenile hammerhead sharks. Unfortunately, Milton H. Stetson suddenly died in 2002, and I could only find one publication from that work (Okimoto and Stetson 1995), which I cannot read as it was published in a conference proceedings (if anyone can scan a copy and send me, I’ll be grateful):

Nonetheless, this paper was cited in several other places, and if they cited it correctly, what Okimoto and Stetson found was that the pineal glands of these sharks (and later the same also found in dogfish shark Squalus acanthias) does not show cycles of melatonin synthesis and release in constant light conditions (it does in light-dark cycles). This does not necessarily mean that there is no clock in the pineal, or that there is not rhythmic production of melatonin, as later work in our lab showed that culture medium can have a dramatic effect.

Whale Shark

Combined 206 daily records of a whale shark dives. Graham, Roberts and Smith 2006

Combined 206 daily records of a whale shark dives. From Graham, Roberts and Smith 2006

In Graham, Roberts and Smith 2006, nine whale sharks were tagged with archival satellite tags which provided data on water temperature, illumination and depth. What they found are three distinct types of rhythms: ultradian (short), circadian (about a day) and infradian (long) cycles.

The short cycle was about 45 minutes long, essentially the sharks swimming up an down underneath the surface, not really diving very deep.

One day record of a whale shark diving activity. From Graham, Roberts and Smith 2006

One day record of a whale shark diving activity. From Graham, Roberts and Smith 2006

The long cycle was a 29-day cycle, likely not generated from within the nervous system of the shark, but rather the animals following the snapper spawning events which are modulated by the moon phases.

The daily cycle was that of deep dives. The sharks made very deep dives – sometimes over a kilometer down – only during the day. Again, nothing in this experimental protocol can distinguish between internally generated rhythms and behaviors directly induced by the environment, e.g., light intensity, vertical migrations of prey, etc.

And yes, this is it, that’s all. Not much work on sharks done, for obvious reasons – they don’t do well in running wheels.


Casterlin, Martha E., and William W. Reynolds. Diel activity patterns of the smooth dogfish shark, Mustelus canis. Bulletin of Marine Science 29.3 (1979): 440-442.

Finstad WO, Nelson DR. Circadian activity rhythm in the horn shark, Heterodontus francisci: effect of light intensity. Bull. S. Calif. Acad. Sci, 1975

Graham, Rachel T., Callum M. Roberts, and James CR Smart. Diving behaviour of whale sharks in relation to a predictable food pulse. Journal of the Royal Society Interface 3.6 (2006): 109-116.

Nelson, Donald R., and Richard H. Johnson. Diel activity rhythms in the nocturnal, bottom-dwelling sharks, Heterodontus francisci and Cephaloscyllium ventriosum. Copeia (1970): 732-739.

Nelson, Donald R., et al. An acoustic tracking of a megamouth shark, Megachasma pelagios: a crepuscular vertical migrator. Environmental Biology of Fishes 49.4 (1997): 389-399.

Nixon, Asa J., and Samuel H. Gruber. Diel metabolic and activity patterns of the lemon shark (Negaprion brevirostris). Journal of experimental Zoology 248.1 (1988): 1-6.

Okimoto, D. K., and M. H. Stetson. Effect of light on melatonin secretion in vitro from the pineal of the hammerhead shark, Sphyrna lewini. Proceedings of the Fifth International Symposium on Reproductive Physiology of Fish, The University of Texas at Austin. 1995.

Images: Shark in the running wheel: shark from ClipArt Supply, wheel from Shaping Youth, photoshop by Tobias Gilk. Shark clock – ToadAndLily on Etsy (where you can actually buy the clock). Other images are figures from papers, according to the Fair Use principle.

Good Night, Moon! Now go away so I can sleep.

Mars has two moons - Phobos and Deimos. Here we see Phobos passing in front of the sun, as seen from the surface of Mars. How would having two moons with different phases affect behavior of Martians?

Mars has two moons - Phobos and Deimos. Here we see Phobos passing in front of the sun, as seen from the surface of Mars. How would having two moons with different phases affect behavior of Martians?

Scientific papers usually don’t faithfully convey exactly how the researchers came up with the idea, or the chronological order in which the investigation proceeded. And there is a good reason for that – papers need to be standardized so other scientists can easily read them, understand them, replicate them and use them to perform further research.

But sometimes, a paper is honest about the process. It is wonderful – and shows that scientists are human, with a great sense of humor – when #OverlyHonestMethods sneak into the text of a scientific paper, surprising and rewarding the careful reader with an ‘easter egg’.

One such paper – on the effects of moon phase of sleep quality – just came out in Current Biology.

The first thing I noticed was that the data were collected in 2000-2003. Why did it take a decade to publish? Was it just sitting on a back burner of a PI for years after the student left the lab? Did it have to go through many rounds of peer review in several journals until it finally managed to get published? None of those reasons, actually! See for yourself:

We just thought of it after a drink in a local bar one evening at full moon, years after the study was completed.

And that is where we encounter yet another effect of the full moon (in synergy with ethanol) on human behavior, at least on WEIRD populations, such as scientists!

But jokes aside, this is also a great example of a paper that usefully re-visits and re-analyzes old data sets. Of course, the authors emphasize the positives of this post hoc approach – nobody at the time of the study could possibly know that the data would be analyzed in this way, so there were no possible subconscious psychological effects – it was a truly triple-blind study:

Thus, the aim of exploring the influence of different lunar phases on sleep regulation was never a priori hypothesized, nor was it mentioned to the participants, technicians, and other people involved in the study.

On the other hand, a study specifically designed to test for moon-phase effects on sleep quality would have been designed differently to ensure it has just the right controls and that maximum information can be derived from the data.

Research in chronobiology is frustratingly slow. In circadian research, each day is just one data point, so each study has to keep subjects in isolation for many days. In the study of lunar rhythms, each month is a data point and the subjects need to be kept in isolation for many months.

To determine if a rhythm is generated by an internal timer (daily or monthly) as opposed to being a direct behavioral response to environmental cycles requires a whole battery of tests, which are hard and time-consuming enough in circadian research, and twenty eight times more so in circalunar rhythm research

Back in the 1960s, it was possible to keep (well compensated) human subjects in isolation rooms for long periods of time (see pioneering research by Wever and Aschoff in the underground bunker in Andechs, Germany). Likewise, animal subjects can be kept and monitored in isolation chambers for long periods of time.

As lunar rhythms are more “messy” than daily rhythms, more data over more time are necessary for the robust statistical analysis. And, due to ethics creep, it is not certain that either animal or human studies of such scope can be approved and performed any more. So, one has to be creative and get quality information out of imperfect experimental protocols (just like we cannot wait to observe multiple cycles of 17-year cicadas, but have to invent creative, short-term approaches instead).

But this time, the researchers were just lucky! Their data-set came from an old experiment which was designed well enough for this new purpose. The key is they had LOTS of data. Their subjects came in to the sleep lab many times and a number of different parameters were measured. Ideally, each subject would stay in the lab for a few months instead of just four days at a time. But having such a huge data set allowed them to weave together a patchwork of fragmented data into a large, trustworthy whole. Each first night of the test was eliminated from the data due to potential influence of the previous day (and the so-called “weekend effect”, as people tend to change sleep times on their days off). Each phase of the moon was covered by multiple subjects multiple times. So they could employ powerful statistics to tease out the effects of the moon phase on various parameters of sleep quality.

And they found some interesting stuff! My colleague Dina Fine Maron has covered the paper in greater detail here. In short, human subjects with no access to information about moon phase, or any ability to perceive the moon itself or its light intensity, nonetheless slept about 20 minutes shorter on the nights of full moon, mostly due to taking roughly 5 minutes longer to fall asleep in the evening than on a night of the new moon. Levels of melatonin, hormone released by the pineal gland during the night, were lower during full moon nights as well. Some of the age and sex differences cannot be explained at this time due to imperfect experimental design – and that is OK. I’d rather see new interesting information coming out of an old data set, than never seeing it at all just because it cannot be “just perfect”.

There are many claims around about lunar periodicities in all sorts of human behavior. For some of those, there is no evidence the claims are true. For others, there is strong evidence the claims are not true. But a few subtle effects have been documented. This paper adds another set with persuasive statistics.

Is this a demonstration that there is a working circalunar clock in humans, operating endogenously, and independently from the actual moon? It’s not possible to tell yet. Those kinds of demonstrations (just like for circadian clocks) require a battery of tests, starting with documenting multiple cycles (I’d say at least three complete monthly cycles) in complete isolation, ability of artificial moonlight to phase-shift the phase of the rhythm in a predictable manner (consistent with a Phase-Response Curve), and hopefully identification of body structures or cellular components which are devoted to generation of the rhythms, with at least some hint of the mechanism how they do it.

We are far from it yet even in animals we can manipulate in lab and field studies. Much work has been done over the decades in the study of lunar and circalunar rhythms in various animals, mostly aquatic and intertidal ones. There are documented lunar cycles (but not necessarily internal lunar clocks) in a variety of organisms, including sponges, cnidaria, polychaetes, aquatic insects, and many different crustaceans including crayfish.

In the terrestrial realm, antlions possess internal lunar clocks, but many other species show modifications of behavior during different phases of the moon, including honeybees, rattlesnakes, ratsnakes, some rodents, some lizards, and lions.

The gravitational force of the moon is so weak that it can affect only very large bodies of water on the Earth’s surface. It cannot even affect smaller lakes and rivers. There is no theoretical mechanism by which any molecule or cellular structure in a human body can be so sensitive as to detect the gravity of the moon. So that hypothesis is out.

In field studies, animals can see and synchronize to the changing night-time intensity as the moon goes through its phases. But in the lab, as in the case of this study, there are no visual clues to the moon phase for the subjects, and, since they had no idea the data would be analyzed for moon phases, they probably did not pay attention to that before they entered the light-isolation lab.

With both gravity and light eliminated as potential clues, the internal clock remains the strongest hypothesis. But it’s still a hypothesis that needs to be tested before one can state with any certainty that it is the case.

As for evolutionary explanations for the existence of a putative lunar rhythm of humans? I would be very careful about this. Demonstrating that any trait is actually an adaptation (and not an exaptation or side-effect of development, or something else) is an incredibly difficult task. Just because something seems “obviously useful” does not make it an adaptation. It is an error of hyperadaptationism to pronounce a trait an adaptation just because it exists, and then to tack on a semi-plausible scenario as to how it may have been selected for. Evolutionary biology is much more rigorous than that kind of lazy armchair speculation.

Sure, if our ancestors actually had lunar clocks as adaptations, it is possible that the mechanism for it may still remain, even if in a weak state, in at least some of today’s humans. But maybe not. And like a rudimentary organ, it does not seem to have any obviously useful function for humans living in the modern society. Twenty minutes of less sleep, that’s all. But it’s good to know. So we can find good use to those extra twenty minutes, perhaps come up with new scientific hypotheses over a pint with colleagues at a local pub.

Reference: Cajochen et al., Evidence that the Lunar Cycle Influences Human Sleep, Current Biology 23, 1–4, August 5, 2013,

Images: top: by NASA, bottom: from the paper.

Let’s Not Spring Forward.

Cross-posted from Zocalo Public Square.

Even cows don’t like Daylight Saving Time. Come Sunday morning, when the milking machines get attached to their udders a whole hour too early, the otherwise placid bovines on dairy farms around the United States will snort in surprise and dismay. They may give less milk than usual. They could take days or weeks to get used to the new milking schedules.

We are no different. While most of us won’t be hooking ourselves up to udder pumps, our bodies next week will experience a disturbance very much like the cows’ – one that can affect our mental and physical health. The reason lies in the clash between sensitive, eons-old biology deep within our cells, and human-imposed time-keeping traditions that are barely a century old. Twice every year, when we “spring forward” and “fall back,” our bodies must do battle between “sun time” and “social time.”

Before the mid-19th century, time was more flexible. Each town and village maintained the local church clock more-or-less in sync with the natural light-dark cycles of the sun. The spread of railroads changed all that. The need to keep trains moving in and out of stations at predictable times forced the adoption of a standardized time. That, in turn, led to the formation of time zones.

Daylight Saving Time (DST)—the resetting of all clocks twice a year—was first proposed by New Zealand entomologist George Vernon Hudson in 1895, for quite selfish purposes. He was studying daily cycles in insects and wanted to be able to do more of it during daylight hours. But his idea of maximizing daylight soon spread. The first country to adopt DST was Germany in 1912. Most other countries soon followed, including the United States, which instituted DST in 1918.

The leading argument in favor of DST has always been that it saves energy. Back in the early 20th century, most energy was used for lighting. So, the argument went, placing work and school schedules within daylight hours would save electricity. People wouldn’t need to use light bulbs to navigate around their homes, offices, factories, and fields in the dark, and they would have more time in the evening to indulge in commerce and entertainment.

Today, the situation is very different. The proportion of total energy that is used for lighting is miniscule compared to other, time-independent uses like factories, computers, nuclear plants, airport radars, and other facilities that run 24/7. Energy companies themselves have measured the effect, and have concluded that DST does not save energy.

With this knowledge, some nations have started re-thinking the concept. Russia, for example, abandoned the clock change in 2011, keeping one time all year round. Iceland and Belarus did the same. On the other hand, in 2007, U.S. Congress, clinging to the notion that DST saves energy, moved the onset of DST three weeks earlier than before. That change, I think, makes a difficult transition even more stressful.

Although Congress can impose these changes, it’s a bit unclear who exactly has the right to determine whether DST is implemented. Until very recently, a large number of individual counties in the state of Indiana refused to go through the clock-changing ritual. Arizona doesn’t change its clocks at all—the only state in the union (apart from Hawaii) to defy DST altogether. This lack of clarity about who is in charge may be one of the reasons why a more sustained effort to abolish DST has been unsuccessful nationwide.

Whether or not DST saves energy is the least of the reasons why it’s a bad idea. Much more important are the health effects of sudden, hour-long shifts on our bodies and minds. Chronobiologists who study circadian rhythms know that for several days after the spring-forward clock resetting – and especially that first Monday – traffic accidents increase, workplace injuries go up and, perhaps most telling, incidences of heart attacks rise sharply. Cases of depression also go up. As the faint light of dawn starts preparing our bodies for waking up (mainly through the rise of cortisol secretion), our various organs, including the heart, also start preparing for increased function. If the alarm clock suddenly rings an hour earlier than usual, a weak heart can suffer an infarct.

The reason for negative health effects of DST is that, in essence, the entire world is jet-lagged for a few days. Unlike some animals, like honeybees and reindeer, humans have a very robust circadian clock system that resists abrupt shifts.

Every cell in our bodies contains a biological clock which coordinates the events in those cells—for example, when gene transcription turns on and off, or when specific proteins are made. When we are exposed to a light-dark cycle that is different from what we experienced the previous days, some types of cells synchronize to the new environmental cycle faster than the others. Cells in our eyes, for example, may adjust in about a day, while cells in our brains take a couple of days. Cells in the digestive system and liver may take weeks. So, for weeks after the DST clock change, our bodies are like a clock shop in which each timepiece cuckoos at a different time of day—a cacophony of confusing signals.

Our bodies are constantly being pulled apart by conflicting demands of the natural ‘sun time‘ and culturally imposed ‘social time‘. People living in urban areas may be better shielded from the sun time than their rural counterparts, because of artificial lighting and the skyglow it produces, but nobody is completely isolated from its influence. Twelve noon according to the clock is not twelve noon according to the planet. Citizens of Barcelona and Bucarest are almost two hours apart in their perception of sun time, yet live in the same social time—the same time zone that encompasses most of Europe.

Even those of us who are lucky enough to work from home and can generally set our own work schedules are not completely immune to the effects of DST. I still have to drive my daughter to school at the time prescribed by the local clock, not by local sunlight. My colleagues have expectations about when I will pick up the phone for a teleconference or respond to their emails. I am supposed to show up for my dental appointment at 7am, not “two hours after dawn”.

But if I ever buy a cow—and that is not as crazy as it sounds since I live next door to a dairy farm—I have a plan. Of course I’ll ignore the bi-annual clock changes, which I hear many smart dairy farmers already do. But I’ll go a step further and ignore social time altogether, milking her at the sun time her nervous system can understand, probably the crack of dawn. Whatever I do, I will never make her suffer through the sudden shift of DST. And none of us human animals should suffer it, either.

Image: Dirk Hanson

No rats in Ryder Alley

Last week, in the wake of superstorm Sandy, I saw a number of people asking questions on social media (and some traditional media picking up on it) about a potential for ratpocalypse, i.e,. the possibility that hordes of rats will come out of the sewers and subway tunnels and flood the streets of New York City in a Pied Piper style. So I wrote a blog post debunking this and explaining why this will not happen, which made me a temporary expert on behavior of rats in storms, so I got interviewed in various places, etc.

As I noted at the very end of the post, my main source of information, at least initially, was a book, Rats: Observations on the History and Habitat of the City’s Most Unwanted Inhabitants by Robert Sullivan. I read it several years ago, when it first came out, and loved it. Reading it provoked me to read more on the topic, so when these questions came up, I already knew most of the answers, and knew where to look for additional information.

The book describes a year in Sullivan’s life, spent observing rats by night, and researching them by day. He went every night downtown to Fullton Street, and just stood there in the middle of two L-shaped alleys: Edens Alley and Ryder Alley. He watched rats come out at night, eat the food discarded by the two restuarants edging the alleys one on each side, fight, hide, and whatever else rats do when they are up on the surface.

The first opportunity I had to go up to New York City after reading the book was in 2007. I just could not resist! The book has no photos of the alleys, so I just HAD to go and see them myself.

My wife and I hailed a cab. Told the driver: Edens Alley. Driver: Hmmm, this is my first day on the job, do you know how to get there?

This was before I had iPhone, GPS, Google Maps…. I pulled out an old-style map, printed on paper, and gave the driver turn-by-turn directions. Once we got there (after making several circles around the area), the driver refused to take any money. I forced him to take double the amount of the fare. He did well for the first day as a NYC taxi driver. This place was hard to find. And off the mid/up-town grid.

Of course, this was in the middle of the day. I did not expect to see any rats there at that time. If I did, that would be an indication that the underground population is astoundingly large, forcing some of the sub-dominant individuals to forage during the day. But I was looking for traces of rats, and for holes and crevices from which they emerge at night, for bags of garbage full of Chinese food, and I took the pictures. I had the pictures stashed away in my Dropbox for more than five years. This is the first time they see the light of day. See for yourselves:

Did NYC rats survive hurricane Sandy?

Floodwaters enter Hugh L. Carey Tunnel. MTA photo

Floodwaters enter Hugh L. Carey Tunnel. MTA photo

How many of the NYC rats survived hurricane Sandy? This question has been asked in the wake of Sandy’s flooding of lower and east Manhattan. See, for example, articles in Huffington Post Green, Forbes, National Geographic, Business Insider, Mother Nature Network and NYMag.

The short answer is: some rats drowned, some survived.

The complicated question, how many drowned and how many survived, is probably impossible to answer. But we can speculate using the information and knowledge we have in our possession. But things we really need to know, we don’t – information is just not available (and some of it never will be).

How many rats are in NYC?

Nobody knows. Nobody seems to even be attempting to estimate.

Beware of the myth that there is one rat per person. That is a very old myth. It started in 1909 when W.R.Boelter published a study of rats in England. He asked farmers (but never bothered to look in the cities) to estimate how many rats they have in their fields. From that informal survey, Boelter came up with an average of one rat per acre (yes, of agricultural land). At that time, there were 40 million cultivated acres in England. From that, he estimated the total population of rats on agricultural land to be about 40 million. Completely coincidentally, England in 1909 also had a population of 40 million people. So, the 1:1 ratio stuck. And it has been repeated for more than a century, by media, by scientists, by United Nations, by pest control companies, by health departments, and apparently everyone else.

In 1949, Dave Davis did a systematic study of rats, by trapping and capturing them, and estimated that rat population in New York City was only about 250,000. Not even close to 8 million.

An aside – I have an indirect personal connection to Davis. For a while he was a professor in the Department of Zoology at NCSU, that is, in my own department. At the time he was ready to retire, in the 1970s, he was actively working on daily and seasonal rhythms in various animals. He used to work with Curt Richter before, at Johns Hopkins, and Curt is one of the pioneers of chronobiology. David sent some woodchucks on a ship from Philadelphia to Australia. While on the ship, rats kept EST time, but quickly re-entrained to the Australian local time once they arrived there and were exposed to ambient light. Although the field was still very young, Davis’ work made the rest of the department aware of it (they did not think it was Biorrhythms silliness, as many assumed at the time), so they were interested in hiring a replacement who was doing something similar. So they hired this bright, young lad from Texas in his spot – two Science papers already published and he took only 3.5 years to get both MS and PhD. The new faculty’s name was Herbert Underwood. Two decades later I joined the Underwood lab. The rest is history.

Anyway, back to rat population. Estimates vary wildly, to as high as 32 million. Nobody really knows.

New York City is old. It was built and rebuilt. New buildings were built on top of the old ones. There are old, buried tunnels, rooms, chambers, now not accessible to humans but perfectly accessible to rats. Gradually, the city dug out more and more sewers, more and more various pipes, more subways and other tunnels. Thus more places for rats to nest. We gradually built comfortable homes for more and more rats.

The rat population is not evenly distributed either. They tend to be where poor people live, and where the restaurants are. That’s where there is food.

And not all rats go to the surface. Rats are pretty loyal to the place of birth, and rarely venture more than about 60 feet from it, throughout their lives. If displaced, they can find their way home from as far as 4 miles, but for a foot-long animal, that is an extremely long distance.

If they can get food down under, e.g., from subway passengers throwing out uneaten food onto the tracks (which they do), rats never need to go up to the surface. They never get captured and counted in surface surveys.

Can rats swim?

Yes, rats are strong swimmers. They can even dive for a little while – see this video: if a domesticated rat can be trained to dive (and enjoy it), I assume that a wild rat can do it when its life is threatened:

The thing is, swimming in a water maze in the lab, or on the surface of a body of water is one thing. Swimming upward, against the powerful stream of water streaming downward is a completely different thing. They may be strong swimmers, but they are not Johnny Weissmullers.

Photo: Hiroko Masuike, NYTimes

MTA workers pumping out water from subway tracks at South Ferry subway station in New York, Tuesday, October 30, 2012. Photo: Hiroko Masuike, NYTimes

There are many ways up to the surface, but they all go up. And if the water was mainly gushing into the tunnels from above, from the streets as Sandy was flooding, they would have had to swim or dive up narrow pipes, essentially vertically up against the water. No way. Those guys drowned.

To go up to the surface, rats need to know the way to the surface. Rats know their own territory very well. But rats that never go to the surface do not know how to get there. They may still want to instinctually go up, but they don’t know the way so would have to get lucky to actually find the stairs and then fight their way up against the gushing water.

Rats already on the surface would probably be fine. The water and wind from Battery would carry them north until they reach the dry ground. They can certainly stay on the surface. Salty water is denser than fresh water, so they would find it even easier to stay on the surface, though their eyes may not like all of the salt.

What was flooded, when and how?

Right now, we do not know exactly where, when and how the water entered the subway tunnels, sewers, etc. MTA site does not provide much information. New York Times does not either – they are concerned with information useful to people, e.g., when will the subway open again, not where, when and how the subway initially flooded. Most likely the water came from above, from the flooded streets after sea water rose high at the Battery and the East side. This is important. It is easier for rats to float on the surface of water rising from below, than to fight against the water falling from above.

Also, most of Manhattan (and rest of NYC) did not flood at all. Most of the rats probably survived just fine where they were.

Who lived, who died?

NYC subways system flooding. New York Times (see link in the main text). So, from above, we can speculate that many rats survived. Some were never affected by flooding. Some were on the surface already and managed to run or swim to the higher ground. Some knew their way out to the surface and made it there. Rats are smart and crafty – if they can find a way to hide or go out, they will.

But some rats certainly drowned. Those are the rats that live deep inside holes we never know about, let alone visit. Rats that never go up to the surface. Rats that had the misfortune to have to try to escape essentially vertically up against strong gushing water.

There is a rule of thumb – if you see a rat on the surface during the daylight time, this means that the underground population is enormous. And I see them every month I go up to New York. When the rats are crowded, dominant rats take the best spots. If the population forages on the surface, dominant rats forage during the night. Subdominant (or submissive) rats are temporally displaced to the daytime shift.

This is important. If Sandy started to flood the tunnels during the day (and nobody knows, or makes public, this information as the subway was already closed to people by then), it will be the non-dominant rats who are on the surface, and thus more likely to survive. If the flooding started at night, it will be dominant rats on the surface, floating away into safety. Dominant rats are more likely to be able to relocate and survive in other places where they have to compete with locals. Non-dominant rats would have a much harder time finding a new home.

So, my guess is that most of the rats survived. But quite a large number of rats drowned – depending on exact location, depth, how much they know how to get to the surface at all, their exact route to the surface, and their status in the social hierarchy.

You can learn much more about New York City rats from Rats: Observations on the History and Habitat of the City’s Most Unwanted Inhabitants by Robert Sullivan, one of the most wonderful popular science books I have read over the past decade.

I will also be doing a HuffPoLive segment about this at 1pm EDT, will post the link in the comments once I have it.

Update: More from The Urban Scientist, Jezebel, Tha Daily Beast, Live Science, Forbes.

Charlotte’s Web: what was she smoking?

“Don’t touch those webs!”

Me and an enormous spider, at the Natural History Museum in Berlin, 2008.

A couple of decades ago, my wife and I worked on a horse farm where everyone was explicitly instructed not to ever clean the cobwebs inside the barn. Sure, the owners themselves would occasionally, very carefully, almost surgically, remove a few targeted old cobwebs here and there, but the majority of the webs remained up at all times. Explanation? Spiders don’t bother anyone, while flies and mosquitoes bother both horses and humans.

On the other hand, for balance, there is an old Serbian proverb that goes like this: “If there were no wind, spiderwebs would cover the sky”

I assume this is said every time someone complains about the strong eastern wind, Koshava, that sweeps through the country in autumn.

And this situation – spiderwebs covering the sky – is something that happens in Mark Twain’s story Some Learned Fables, For Good Old Boys And Girls, featuring Herr Spider as one of its key characters. I read Twain’s short stories over and over again as a kid. Still love them.

Why are we so enchanted by spiders, in real life, in mythology, and in popular culture? I certainly am, always was.

There were Little Miss Moffet, and Itsy Bitsy Spider.

As a little kid, I watched, and was greatly impressed by the old film Tarantula. Later I could not help myself – just had to watch Eight Legged Freaks and Arachnophobia. And yes, Spiderman, despite its scientific…er, bloopers.

Of course I knew about Arachne and the beautiful myth of the origins of the callipygous Shenora Spider (does such a species even exist in reality?).

And then there are spiders in literature. I was scared by the Spider-Man in John Wyndham’s The Chrysalids. I fought the giant spiders of Mirkwood when I played The Hobbit computer game on Sinclair ZX Spectrum back in 1981 or so, after I have already read the book both in Serbian language and the original English. There was Shelob in Lord of the Rings, and Aragog in Harry Potter.

And of course, the best spider in all of history – Charlotte!

Charlotte. She could write.

Today is the 60th anniversary of the first publication of Charlotte’s Web, the beautiful, haunting story of a talking pig and a writing spider.

Interestingly, growing up in Yugoslavia the first 25 years of my life, I have not heard of Charlotte’s Web until I came to the States. But then I had kids. And kids loved to watch the movie over and over again. So I read the book.

And to this day, occasionally, spontaneously, I start singing “Isn’t it great that I articulate!” An important and heart-felt sentiment for a writer for whom words are toys.

Then I received in the mail (but am yet to read it, I promise I will), Michael Sims‘ book The Story of Charlotte’s Web, a biography of E.B.White and the story of the making of the book.

But not everything is fiction and myth. I am a scientist at heart. Each one of those invented characters always made me want to learn more about the real creatures.

Orb weaver (Argiope sp.) Members of this genus are found all around the world and spin large webs that often contain striking designs. Charlotte’s Web author E.B. White, who consulted with a Museum curator while writing the classic children’s book, named the main character Charlotte A. Cavatica after a common orb weaver, Araneus cavaticus. © AMNHR. Mickens

Orb weaver (Argiope sp.) Members of this genus are found all around the world and spin large webs that often contain striking designs. Charlotte’s Web author E.B. White, who consulted with a Museum curator while writing the classic children’s book, named the main character Charlotte A. Cavatica after a common orb weaver, Araneus cavaticus. © AMNHR. Mickens

A couple of months ago, I went to the American Museum of Natural History in New York City (thanks for the tickets, you know who!) to see their new exhibitSpiders Live. Yes, “Live” is a good description – there are plenty of living specimens in there, many quite fascinating.

As usually happens in museum exhibits, there was plenty to learn about what we know. Anatomy, physiology, ecology, evolution, geography, behavior. Sure, there were a couple of non-spiders there, like scorpions, but it was clearly explained exactly why they are not spiders and how they are related.

One could see a short video showing how Gladiator spider catches its prey by throwing a carefully counstructed web trap on it, like this:

And they mentioned the Bolas spider which catches its prey by lassoing it in with its bolas-like ball of silk:

Interesting – to me at least, as a chronobiologist – is that the Bolas spider uses its circadian clock for an interesting function – it produces different blends of chemicals in its pheromone at different times of night (pdf) to coincide with different times when two different species of moths are flying around, each species attracted to a specific mix of aromatic chemicals.

But beyond learning facts, I was also looking at the ways the exhibit tries to include the scientific process – how we know what we know about spiders? I was looking for, perhaps, descriptions of ingenious experiments on the courtship signaling in wolf spiders, or the research on unique social, colonial spiders. Nope.

There was a part, at the end, which described how scientists collect spiders in the field, how they catch them, preserve them and label them.

And then I saw what I was really looking for. Yes! They did it! The exhibit had a really nice description of my favorite spider research ever! And there it was, The Charlotte’s Web connection, and my own personal connection! I talked about it at the last #TriSciTweetup at the NC Museum of Natural Science in Raleigh NC, for the inaugural Lightning Talks with Brian Malow on Thursdays at the Daily Planet Cafe:

Back in 1948., zoologist H. M. Peters was studying how spiders spin webs. He was getting tired as he had to do all of his research late at night, when spiders spin their webs. So, he asked his friend Peter Witt, a pharmacologist, if there is anything that he could give to spiders that would make them spin during the day. Peter suggested amphetamines. It did not work. Spiders kept weaving at night. But, oh my, their webs looked crazy! They were like impressionist art!

Argiope spider web This real argiope spider web has been colored and preserved. Its most striking feature, an ‘X’ running through it, is something of a mystery. Many spiders embellish their webs with these designs, called stabilimenta, but the reason is unknown. Scientists think stabilimenta may attract insects by reflecting light, warn birds away, or camouflage the spider from predators. © AMNHD. Finnin

Argiope spider web. This real argiope spider web has been colored and preserved. Its most striking feature, an ‘X’ running through it, is something of a mystery. Many spiders embellish their webs with these designs, called stabilimenta, but the reason is unknown. Scientists think stabilimenta may attract insects by reflecting light, warn birds away, or camouflage the spider from predators. © AMNHD. Finnin

Peter Witt was an amazing person, a wonderful man. I had the fortune to meet him once, in 1998, just a couple of weeks before he died. He was the Head of the institute for brain and behavior at Dorothea Dix hospital in Raleigh, now unfortunately closed.

Intrigued by the results his friend Peters got when giving spiders amphetamines, he turned his own research into that direction, using spider webs as windows into the way different chemicals affected the nervous system. Some of those were pharmaceuticals of the day. Others were drugs found relatively easily on street corners back in the 1950s and 1960s. Both were of interest to science, of course, for different reasons.

Different drugs had different effects on the shapes of the web. In high doses, almost every drug resulted in highly irregular webs. But at carefully chosen lower doses, there were some interesting differences. For example, under the influence of caffeine, the webs were vertically shorter but horizontally wider, as spiders made larger angles between the radial spokes of the web.

The most striking was the effect of LSD-25. Yes, LSD. This is the only drug which resulted in webs being more carefully weaved and more perfect than the controls.

Charlotte? Is that you?

Many years later, I was teaching a lab at NCSU in animal physiology. Part of the lab was a project, done by students under my supervision. Some students did projects on humans – each other. But the other half used animals. Invertebrates, as there was no time to get an IACUC (institutional animal care and use committee) approval for use of vertebrates (that is a long and difficult process).

A spider web on pervitine

A spider web on pervitine

One of my students decided to use Peter Witt’s experimental protocol, applying a chemical that he never used way back then – serotonin. Result? Spiders made decent webs, but they took about twice as much time to make them. They went slow about it. They made perhaps half of the twists of the spiral before deciding that was the end, leaving about twice as much space between the loops of the spiral.

Spider brains are large and complicated. They are so large they can’t even fill just the head, a part of them fills the thorax. Of course, spider brains are difficult to study. Not to mention that we do not have a spider genome sequenced yet so we do not have the tools to monitor what is happening in a spider brain. Thus, this line of research has been largely abandoned.

But it was not all in vain. Apart from being able to categorize substances along the lines of their effects on spider webs (often corresponding to their effects on human brains), this method now has a place in agriculture. Placing a few spiders in a field or orchard overnight and taking a look at the webs in the morning can tell the researcher if there are pesticides there, and perhaps which class of pesticide if not the exact kind.

Perhaps there is something in the air that can induce a spider to write “Terrific” and I’d love to know how it does that.

Stumped by bed nets, mosquitoes turn midnight snack into breakfast

Anopheles mosquito (unknown source)

Anopheles mosquito (unknown source)

One of the most effective methods for the control of spread of malaria is the use of bed nets infused with insecticides. Most species of mosquitoes (the Anopheles genus) that carry the malarial parasite (Plasmodium falciparum) are considered to be strictly nocturnal – they are active only during the night.

Thus, sleeping under the net provides protection against getting bitten by the insect vectors of the disease. The net does it in two ways – by providing a mechanical barrier between the mosquito and the human, and by killing mosquitoes that get in contact with the infused insecticide.

As we have learned many times, often the hard way, evolution tends to find a way around such tricks. A number of Anopheles species or local populations have evolved resistance to pyrethroid insecticides usually used in the nets. Yet, the mechanical protection of the net should still be effective, right?

Not so fast! A new study published in September 21 in the Journal of Infectious Diseases documents a behavioral change in a local mosquito population that effectively works around the safety protection of bed nets. What do they do that’s new? They changed the time of day when they bite!

Malaria-carrying mosquitoes are thought to all be strictly nocturnal. Recently, this dogma has started to be questioned, mainly because the rates of malaria did not significantly diminish in areas where bed nets have been implemented. Perhaps they fly and bite during the day, yet nobody bothered to test that hypothesis yet? A previous study noticed a shift in timing of activity and biting from middle of the night into early night. This study was quite systematic – repeating the experiment in two locations in Benin at three time-points: before, during and after the full implementation of bed nets in both locations.

Chronogram of the experiment. Translation for humans: 'chronogram' is an "aren't we sophisticated in our clever use of silly, opaque, uneccessary jargon" version of 'timeline'.

Chronogram of the experiment. Translation for humans: 'chronogram' is an "aren't we sophisticated in our clever use of silly, opaque, uneccessary jargon" version of 'timeline'.

What did they do? They collected mosquitoes in large numbers and recorded the time of day they caught mosquitos. In addition, they used morphology to identify the genus, and PCR to identify the species. Every single mosquito was Anopheles funestus. They tested the caught mosquitoes for pyrethrin resistance and did not detect any – every single mosquito died. Thus all the changes were strictly behavioral.

How did they collect them? They placed humans in strategic places as living targets. It looks pretty much like this video, except they actually captured the insects into vials, then transferred them into small bags:

During the period of just a few years as the bed nets got implemented in the two villages, local mosquitoes dramatically shifted the timing of activity. Instead of 2 or 3am, they now predominantly bit humans around 5am:

Shift in timing in mosquito activity in two locations over three sampling periods.

Shift in timing in mosquito activity in two locations over three sampling periods.

What does that mean?

First, we don’t know yet if this was an evolutionary (i.e., genetic) change or a purely behavioral change. It is possible that there was quite a lot of genetic variation in timing of activity in the population a few years ago and that the bed nets provided a selective regimen that skewed the population to consist mainly of late night and dawn-active individuals. It is also possible that there is sufficient behavioral plasticity in the mosquito allowing it to learn the new best time of day to go out foraging. I’d love to see the mosquitoes placed in isolation chambers to monitor purely genetic patterns of circadian rhythms of activity.

But let’s think more in ecological terms. There are several players here: the Plasmodium parasite, the Anopheles vector, the human host, and predators that eat mosquitoes, notably bats. I have written at length about this a few years ago. Here’s a simple schematic of how the system works when undisturbed:

A crude schematic of possible timing of activity in this ecological system

A crude schematic of possible timing of activity in this ecological system

If the mosquito shifts to almost dawn, what happens?

First, the humans are up and about, outside of nets, readily available to bite. If the humans are healthy but mosquitos are carriers, this is a good way to transmit malaria to them.

But the humans who are sick, the sources of malaria, are still not available. At the times when they undergo “quaternary fevers”, which are the times when malarial parasites are present in their blood (I explained this in great detail before), they are safely hidden by the nets in the middle of the night and they are not bitten by late-biting mosquitos.

Second, a mosquito that bites a human around dawn is much more likely to get detected by that human and be swiftly turned into a small, bloody mush.

Third, while a mosquito that flies around dawn may be able to avoid some of the bats (though not all of them – many bats hunt until the break of dawn), they are now increasingly vulnerable to other predators – frogs, lizards and birds – that tend to hunt at dawn.

As it often happens, there are pros and cons when it comes to evolving new adaptations. The bed nets are now selecting for new adaptations in mosquitoes. It is hard to predict what will be the pros and cons of those adaptations for human health, or the pros and cons of those adaptations for mosquitoes and their survival, or pros and cons of these adaptations to insects’ predators. Future research on this will be both very interesting to watch and very useful for control of malaria.


Nicolas Moiroux, Marinely B. Gomez, Cédric Pennetier, Emmanuel Elanga, Armel Djènontin, Fabrice Chandre, Innocent Djègbé, Hélène Guis and Vincent Corbel, Changes in Anopheles funestus Biting Behavior Following Universal Coverage of Long-Lasting Insecticidal Nets in Benin, J Infect Dis.(2012) doi: 10.1093/infdis/jis565