How do bats in a cave know if it is dark outside yet? Guest post by Anne Marie Hodge.

As traveling is not conducive to vigorous blogging (apart from posting travelogue pictures), I have asked a couple of friends to write guest posts here. The first to step up to the plate is Anne Marie who put together her passion for bats and my passion for biological clocks and wrote this fascinating post:

Casinos on the infamous Vegas "strip" spare no expenses when it comes to extravagant decorations and architecture. You can find everything from indoor gondola rides to full-sized pirate ships that are sunk in mock-battles multiple times each day. One thing that you might notice, however, is that these massive, opulent buildings almost always lack windows in the rooms where major gambling activity takes place. The massive interior rooms echo with the bells of slot machines and the soft buzz of cards being dealt at hundreds of tables all throughout the day and night, and after several hours inside one of these caverns of opulence it is easy to forget what time of day it is supposed to be. That, of course, is the point: if you aren't able to keep track of the passing hours by subtle cues such as the angle of the sun, casino managers hope that it will keep you (and your money) around for longer periods of time.

Fortunately, whether you are a high-rolling VIP showing off your Rolex or a more budget-minded tourist playing the quarter slots with your trusty plastic Aquatech strapped to your wrist, chances are you have some way to tell time even when you are sequestered from typical environmental day length clues. Other mammals, however, don't have the luxury of mechanical time instruments. If even a few hours inside a windowless casino is enough to distort our natural perception of time, how do other mammals manage to keep regular daily rhythms?

Obviously, most mammals do not hang out in windowless casinos, and thus are able maintain circadian rhythms using external cues such as day length and temperature. Bora recently gave an excellent primer on mammalian circadian clocks, definitely check out that post for detailed information on how these rhythms are regulated.

Light cycles are crucial for proper circadian clock calibration, but some animals live in large, isolated places that lack both sunlight and slot machines. The most notable cave mammals are bats, the winged wonders of the mammal world. The idea that all bats are caves-dwellers is actually a misconception. Many bat species roost in trees, buildings, or "bat houses" put out by helpful humans in areas where natural forest roots have been destroyed. Studies have shown that day length is the most common factor regulating bats' daily activity cycles. Foraging strategies and diet specialization seem to have an impact on what time of night specific species emerge from their roosts. Insectivorous species often begin foraging a bit before true sunset, in spite of exposing themselves to increased predation risk, in order to take advantage of the peaks in insect activity at dusk (Jones and Rydell 1994). Fruit eating bats can afford to sleep in a little, because their "prey" isn't likely to go anywhere between dusk and full darkness, so it's not worth risking increased predation by diurnal or crepuscular predators. Thus, being able to detect the rising and setting of the sun is crucial for these bats to regulate their activity cycles.

While many common species of bats never even venture into caves, some species do indeed roost in large caves that are entirely devoid of light. Without being able to see when the sun rises and sets, how do these little guys maintain regular circadian rhythms?

The most extensive studies of the circadian rhythms of cave bats have focused on Hipposideros speoris, Schneider's roundleaf bat, which is native to India and Sri Lanka. Back in the 1980s, a group from Madurai Kamaraj University did some fascinating work to determine how these bats are able to tell when it is time to leave the cave for foraging each night (Marimuthu et al. 1981). Within the cave roost, bats are isolated from both light and temperature fluctuations, so the researchers sought another explanation for how they calibrate their circadian clocks. They did this by capturing some of the bats within a large colony of H. speoris, then putting them in holding cages inside the original cave, to observe their activity patterns in situ without ever letting them access a chamber of the cave that could give them external light or noise cues.

So, what did the Cave Cage experiment tell us? Surprisingly, it appears that social interactions are the key. The bats were observed to become mildly active within the cave well before the sun went down, and they spent some time grooming and flitting around within the roost chamber. Some of those bats ventured in between the roost chamber and into an outer portion of the cave, "sampling" the light. Once adequate darkness set in, all of the bats (not just the "samplers," left the cave to forage. The caged bats also increased their activity in sync with the rest of the colony, even though they were unable to "sample" the outer chambers. The researchers concluded that the bats' circadian rhythms were entrained by social cues. Bats could have been responding to the noise of the wingbeats of the first bats to leave the cage, or there could have been active vocal signaling. Pheromones could also come into play, if specific hormones are released by "samplers" as they prepare to leave for foraging, signaling the rest of the colony that it is time to leave.

One question that immediately crossed my mind was how the bats know when to start stirring around in the first place, It seems probable that the nightly emergence "sets" their clocks so that they're properly entrained to wake up slightly before sunset, using hormones such as melatonin to control the length of their sleep cycle. These are largely tropical bats, so day length does not vary much throughout the year, allowing them to have a fairly constant interval of sleep in between returning from foraging in the morning and waking up in the evening.

The group also observed activity patterns of captive bats kept inside a cave after exterminating all of the other bats that roosted there (not the most conscientious field method, but not quite as terrible as it sounds: it was a small bachelor roost and only two bats were killed). They found that bats that were isolated from conspecifics displayed "free run" activity cycles that were significantly less than 24 hours long. Thus, it appears that the bats use social cues from other colony members to time their outflight.

There is no information on whether the same individuals are "samplers" each night, although that would be a fascinating study. While social cues do appear to play a large factor in determining the circadian rhythms of H.speoris colonies, sunlight is still a factor: the "samplers" couldn't determine the time of day without sunlight available for sampling. The researchers did a follow-up study a few years later that shows that both light and conspecific communication are necessary to maintain accurate cycles. This time, they illuminated a cave around the clock (Marimuthu and Chandrashekaran 1983). Being exposed to constant light, with conspecifics resulted in free run cycles longer than 24 hours, as opposed to the shortened cycles displayed by isolated bats in constant darkness, showing that light cues facilitated by social communication appear to entrain the circadian clocks of these bats.

So, it appears that some bats depend upon social cues to help regulate their circadian clocks, with a few individuals in the colony serving as light "samplers" and alerting the other bats when it is time to emerge for nightly foraging. They still depend upon light cues for regulation, but the significant factor is that only a few actually see the light levels before emerging each evening, the rest rely upon social cues to tell them when it's dinner time and entrain their internal clocks.

1. Image credit: Phil Richardson

References:

Jones, and Rydell. 1994. Foraging strategy and predation risk as factors influencing emergence time in echolocating bats. Phil. Trans. R. Soc. Lond. B. 345: 445-455.

Marimuthu, G.S. and M.K. Chandrashekaran. 1983. Continuous light inside a cave abolishes the social synchronization of the circadian rhythm in a bat. Behavioral Ecology and Sociobiology. 12: 321-323.

Marimuthu, G., S. Rajan, and M.K. Chandrashekaran. 1981. Social entrainment of the circadian rhythm in the flight activity o fthe microchiropteran bat Hipposideros speoris. Behavioral Ecology and Sociobiology, 8: 147-150.