Slithering through history: Snakes have been primates’ predators, prey and competition


ResearchBlogging.orgIn pre-colonial Mexico, the winged serpent Quetzacoatl was worshipped as a god. In modern-day Texas, rattlers are regularly fried and eaten. And in Pennsylvania, the snakes at the Philadelphia Zoo’s reptile house have quietly gone about their business while my girlfriend stood in the corner, eyes squeezed shut, shaking with fear.

People’s feelings toward, and relationship with, snakes have varied greatly depending on the time period, location and culture. Today in the U.S., if fear isn’t the most common reaction (it was our #1 fear 10 years ago), then it’s at least very high profile…


You might assume it’s an old fear, too. Certainly our ancestors, whether two hundred or two million years ago, encountered snakes more often than most of us do. In a new study published this week in Proceedings of the National Academy of Sciences, anthropologist Thomas N. Headland and ecologist Harry W. Greene suggests that pre-modern humans and the lower primates have indeed had a long shared history with snakes, and its more complex than we had thought. Because constrictors usually swallow their prey whole and intact and venomous snakes attack soft tissue, there’s almost nothing in the fossil record to tell us anything about snakes attacking and/or eating humans and other primates. To figure out the relationship extinct hominins and pre-modern humans might have had with snakes, examining bones wouldn’t cut it, so the Headland and Greene had step back in time, in a way.

In 1962, three weeks after their wedding, Headland and his wife left Minnesota for the Philippines. For the next 24 years they lived among the Agta Negritos, the indigenous people of Luzon, the country’s largest island. By the time the Headlands arrived, the Agta couldn’t fairly be called primitive, but their lifestyle and size made them both similar to our prehistoric hominin ancestors and susceptible to attacks from large snakes. They were only recently hunter-gatherers and nomads, living in temporary shelters in family-based groups and subsisting on foraged plants and wild meat from the rainforest. Adult male Agta are, on average, a little under five feet tall and tip the scales at 97 pounds, while the reticulated pythons (Python reticulatus) that share the rainforest with them grow as long as 23 feet and weigh in at 165 pounds. An Agta male walking through brush is not only open to an attack from a big python, but also just the right size to be considered a decent meal for a snake, which has been known to eat pigs as big as 130 pounds.

Sure enough, when Headland started interviewing the Agta in the mid-1970s about their experiences with pythons, 15 of 58 men and 1 of 62 women said a python had attacked them. Of the men, two had been attacked twice and 11 still had scars from their attack. The interviewees could also collectively remember six people who were killed by pythons in the previous 40 years, including a man who’s son found the snake, cut it open and retrieved his body for burial.

The hunters also became the hunted sometimes. Every Agta man interviewed said they had killed at least one small python (up to six feet) during their lives, and some had killed larger ones. While Headland was living with them, an Agta hunter shot a 22-foot-long python and butchered it for some 55 pounds of meat.

The 22.6-foot reticulated python, shot by Kekek Aduanan (right) on June 9, 1970

The skin of the same python, post-butchering.

When the Agta and the pythons were not stalking each other, it turns out they were often hunting the same game. Until the 1970s, the Agta routinely hunted and ate Philippine deer, Philippine warty pigs and long-tailed macaques, three species that they often found in the bellies of the snakes they butchered.

The Agta and the pythons, the interviews make clear, have had a complex relationship, acting as each other’s predator and prey, and even directly competing for resources. Headland wanted to see if these same relationships showed up elsewhere in our family tree, so he turned to Cornell ecologist Harry Greene, who searched the natural history literature for primate-snake encounters and found a batch of stories that make the serpent in the Garden of Eden look like nothing. While no living serpent feeds exclusively on primates, Greene found anecdotal evidence that several constrictors prey on them regularly, and that venomous and constricting snakes have attacked at least 26 species of non-human primates, including lemurs, lorises, tarsiers, eight species of New World monkey and ten species of Old World monkey.

Green found that, like the Agta, nonhuman primates have stood up to snakes and attacked them. He found stories of capuchins using branches to kill a terciopelo, and lemurs ganging up on Madagascan ground boas. In some of these battles, the primates were probably defending themselves, but snakes are also potentially great prey choices for a primate, since their flesh isn’t toxic and they stay and confront attackers instead of fleeing.

Scientists have found in other animals, and even plants, that the shadow of an enemy looms long. Could it be that modern humans’ ophidiophobia is the relic of our long shared history with snakes? Is my girlfriend’s uneasiness an ancient, hard-wired instinct kicking in? Well, that’s tricky. Previous research has shown that very young children can detect snakes quicker than other objects, with the researchers suggesting that this is because they’re evolutionarily relevant threats. Subsequent research found that even with this quick detection, kids don’t associate fear, or any other emotion, with snakes until they learn to do so from adults. They only make the connection after seeing the reactions of people around them. If you see a snake, and your mom freaks out, you’ll learn to fear them, too, pretty quickly. Carnegie Mellon psychologist David Rakison, who did the research, points to the late crocodile hunter Steve Irwin’s kids, as examples of the opposite reaction. Irwin worked with dangerous animals very closely without any outward signs of fear, and his kids learned from that (sometimes very up close). Now, both kids are following in their dad’s footsteps.

Even though he and Headland don’t draw any conclusions about the question in their study, Greene told Cosmos magazine that he could “easily entertain as logical the hypothesis” that our fear of snakes is genetic and may formally investigate this in the future. Until we get a better idea of why fear of snakes is so seemingly widespread, it’s fascinating and sort of comforting for now to know that almost all members of our primate family. Since we came down from the trees, and maybe even while we were still in them, we’ve been listening carefully for a rustle in the leaves and a soft, low hiss.

References: 

de Lange, Catherine, (2011). “Fear of snakes? This could be why.Cosmos.

Headland TN, & Greene HW (2011). Hunter-gatherers and other primates as prey, predators, and competitors of snakes. Proceedings of the National Academy of Sciences of the United States of America PMID: 22160702

Yong, Ed. (2011). “Meet the Agta, a tribe where a quarter of men have been attacked by giant snakes.“ Not Exactly Rocket Science. 

Images: Beauty comes in all sizes and shapes :)” by spisharam; Python and Agta photos courtesy of Thomas N. Headland


 

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Night of the Bargain Hunter: some bats pick prey based on the cost of the hunt

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While they’re less likely to Wall Street than a barn upstate, bats are as concerned as we are about the economy. Their economy revolves around energy instead of money, though, and a problem on the balance sheet can be a matter of life and death. If they spend more energy catching a meal than that meal provides, they’ve created an energy deficit that impacts their health, growth and survival.

There’s no need to worry about bats during a recession, though. New research from biologists in Germany suggests that bats are actually pretty savvy shoppers and are able to use echolocation to make economic decisions while hunting and stay in the black, calorically speaking.

Bats gather information about their environment and prey by making clicking calls and then analyzing the echo patterns that bounce back at them. The conventional wisdom, backed by research, was that bats selected their prey based on biased information. That is, some prey had more conspicuous echo patterns because they were bigger or moved more and were over-represented in a bat’s perception. In the last few decades, though, that way of thinking has started to change, thanks to guano. Biologists began noting here and there that, in some colonies’ guano, there were more large insects than could be expected by chance and biased selection. In 2006, biologists from Frostburg State University in Maryland found that the proportion of beetles in the guano of one colony they were studying was greater than it should have been relative to the beetles’ abundance in the area. This all suggested to biologists that bats might be able to actively select their prey instead of just grabbing the most obvious things flitting about.

Since then, biologists have learned that some bats are indeed very sophisticated hunters. Greater horseshoe bats (Rhinolophus ferrumequinum) are known to be able to accurately discriminate between different types of insects based on information in the echoes of their fluttering wings (what’s more, they can change the frequencies of their echo calls to compensate for the of their own flight speed). More recently, Klemen KoseljHans-Ulrich Schnitzler and Björn M. Siemers from the University of Tubingen and the Max Planck Institute for Ornithology in Germany suggested that horseshoe bats are not only picking their prey selectively, but making those decisions based on energy economics.

Thinking about those piles of guano, Koselj wondered if the prey discrepancies other researchers had found could be explained by the bats hunting prey that optimize their energy profitability: They picked the certain insects not because they were obvious or especially tasty, but because they knew that some bugs gave them a better meal for their effort.

To find out, he’d need to watch them while they hunted, instead of just going through their waste. Koselj and his team captured half a dozen greater horseshoe bats and let them loose in a lab to hunt. To fully control the echo information the bats got, Koselj had them prey not on bugs, but computer-controlled propellers. The faux bugs came in different sizes and rotated at different speeds to produce echoes that resembled natural insects, some bigger and more energetically profitable than others. For a successful attack on a small propeller, the bats were rewarded with the wing of a mealworm and attacks on big ones netted them large, whole mealworms.

As the bats hunted, Koselj varied the conditions of the bug market, changing the frequency of small and big bugs and the amount of time between bug appearances to simulate different conditions of bug density and abundance. Throughout the hunts, Koselj paid close attention to the bat’s prey-selection decisions – catch or skip – in the context of abundance. Then, he then compared the results with standard models of prey choice to figure out if the bats were choosing prey based on energy costs and benefits. If they were, Koselj figured, they’d take the bigger, more profitable prey when they could get it and ignore the small ones, and be less picky when big bugs were scarce.

All six bats adjusted their prey selection to the different wait times between appearances of the large bugs, attacking both large and small bugs when the big ones didn’t show up as often and rejecting small ones and taking more of the big ones when they were more frequently available. One even rejected the small prey outright and took only the large prey when it showed up frequently enough. This selectivity didn’t appear to be just a matter of sensory bias, either. Often, when the small propeller started rotating, the bats would turn toward it, jerk their wings and get ready to take off, but then stand their ground, suggesting that they noticed the small prey and decided to skip it and wait for something worth the flight.

The bats, it seems, are savvy consumers, choosing their prey based on specific echo information associated with energy profitability and on that prey’s availability, estimated from how frequently they encounter it. This gives them a leg up on many other animals that also eat insects. Experiments with fish, amphibians, and birds have shown that these animals often reject the most profitable prey, an uneconomic decision that suggest they’re picking meals based on happenstance. As for other bats, which represent about a quarter of all mammals on earth, Koselj thinks that more species might be able to match the horseshoe’s decision-making, but that there might be a performance gap between bats that use short frequency-modulated (FM) calls those like the horseshoe that use long continuous frequency ones.

Meanwhile, another German team has discovered that tropical bats balance their energy costs and gains with slower metabolisms.

Image: “Greater horseshoe bat, Rhinolophus ferrumequinum Schreb. 4/5 natural size,” by Friedrich Specht, via Wikimedia Commons.

References: Koselj K, Schnitzler HU, & Siemers BM (2011). Horseshoe bats make adaptive prey-selection decisions, informed by echo cues. Proceedings. Biological sciences / The Royal Society, 278 (1721), 3034-41 PMID: 21367788

Jones, G. (1990). Prey Selection by the Greater Horseshoe Bat (Rhinolophus ferrumequinum): Optimal Foraging by Echolocation? The Journal of Animal Ecology, 59 (2) DOI: 10.2307/4882

Salvatore J. Agosta, David Morton, & Kellie M. Kuhn (2003). Feeding ecology of the bat Eptesicus fuscus: ‘preferred’ prey abundance as one factor influencing prey selection and diet breadth
Journal of Zoology , 260 (2), 169-177 : 10.1017/S0952836903003601

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Good Webkeeping: Spiders use Decorations as Defense

ResearchBlogging.org
Orb-weaving spiders are those spiders that build the spiral wheel-shaped webs that we often tend to think of as the Platonic ideal of spider webs. The ones you find draped between two dewy branches in a sun-dappled meadow, spider sitting in the dead center lying in wait for hapless flys and other insects to collide with the nearly invisible, impossibly sticky threads and get trapped. Dinner is served.

While this technique keeps the spiders’ bellies full, it’s not without its problems. Those of us who’ve walked through a doorway or between two tree branches, only to come away covered in thin, sticky web threads know that it’s not pleasant (for me, it is the stuff of nightmares). For the spider, it’s absolutely disastrous. Severe damage to the web by humans and other animals that the spider has no intention, or hope, of devouring costs them the production of more silk for a new web, exposure to predators, lost hunting opportunities and missed meals, and ultimately plays with the odds of their survival.

What’s a spider to do, then, when getting through the day requires a web that’s inconspicuous enough that prey don’t notice it, but has enough presence to warn animals that would just wreck it?

The species of the genus Argiope pull off a contradictory, but seemingly necessary, signaling paradox by constructing “decorations” of zigzagging bands silk on their webs. They make the web very conspicuous to the naked eye, even from a distance, but don’t seem to tip off prey insects that they’re about to stumble into a trap.

Previous studies showed that decorated webs are damaged and destroyed less frequently than undecorated ones, and André Walter and Mark A. Elgar from the University of Melbourne wondered if this protective function was what motivated the spiders to build the decorations. It is, after all, one of three explanations that entomologists have for the decorations, the others are that the decorations provide a signal for prey attraction or conceal the spiders’ outlines and camouflage them from predators.

Walter and Elgar collected females of the species A. keyserlingi (above, also known as the St. Andrew’s Cross spider because the decoration they build at the center of their web resembles the X-shaped cross the Christian St. Andrew was crucified on) near their lab at the University of Melbourne and left them to build their webs in a group of plastic frames set up in the lab.

Once the webs were built, Walter and Elgar rained destruction down upon them. He divided the spiders into three groups, left one group’s webs alone, “lightly damaged” another group’s by cutting web threads to simulate damage caused by prey impact and “heavily damaged” the third group’s cutting ¼ of the web threads plus cutting two diagonally opposite anchor threads to collapse the web. When the webs were rebuilt, he cut them down again and again for what might have been the most stressful 14 days of these spiders’ lives.

Throughout their reign of terror, Walter and Elgar kept tabs on two key characteristics of the webs: the size of the web’s “capture area” (the central sticky part where insects get stuck), and the pattern and the size of web decoration bands.

Capture area size didn’t change in the webs that experienced no damage or mild damage, but shrank by about 13% over the course of the experiment in the webs that experienced heavy damage. In all three groups, the proportion of spiders that built web decorations increased. At the start of the experiment, about a quarter of the spiders in the no damage group decorated their webs. At the end, a little more than half of them were building decorations. The decoration increase in the mild damage group wasn’t much greater than that in the no damage control, but the heavy damage spiders really got in touch with their inner Martha Stewarts and the proportion of decorators shot up from 28% to 81%.

The post-damage decorating craze led Walter and Elgar to think that the spiders are using the decorations tactically to make their webs more obvious to passing animals that might unintentionally hit them and tear them down.

But why the increase in decorating among spiders that didn’t get their webs wrecked too badly or even touched at all? Walter and Elgar think that the slight uptick there was because the captive spiders were well fed and could afford to invest a little more in their webs, whether their homes needed sprucing up or not.

Reference: André Walter, & Mark A. Elgar (2011). Signals for damage control: web decorations in Argiope keyserlingi (Araneae: Araneidae) BEHAVIORAL ECOLOGY AND SOCIOBIOLOGY : 10.1007/s00265-011-1200-8

Image: “Argiope aetherea - St Andrew’s Cross spider” by Amos T Fairchild. Used under a Creative Commons License

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Cannibal Crickets Can Control a Crowd: How Eating Your Friends Aids Collective Motion

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On the wide, open plains of the American West, it’s more than the buffalo and the antelope that roam. Mormon crickets (Anabrus simplex) also sweep across the land in huge migratory swarms that can stretch six miles long and three miles wide. The crickets (a misnomer, they’re actually flightless katydids) can march up to a mile and a quarter a day in these groups, devouring every scrap of vegetation in their path and devastating agriculture in areas they pass through.

It sounds like a Biblical plague*, but consider the poor crickets. While the swarming behavior isn’t completely understood, entomologists think that it’s partly a strategy to avoid being eaten. Observations and experiments have shown that crickets that become separated from the group are easy prey and a big, cohesive group minimizes the risk of predation for any individual cricket.

Not that life in the swarm is any easier. In addition to consuming any and all plants they come across, the crickets often eat each other. One reason for this should be obvious, says a new study, “huge, concentrated numbers of crickets require huge, concentrated amounts of food. If the landscape doesn’t provide it, a fellow cricket will.”

A not so obvious side effect of this crickety cannibalism is that it might be helpful, even necessary, in keeping the swarm moving as a unit. A swarm of insects is simply the sum of its parts. The group’s movement, coordination, cohesiveness and persistence are the simple decisions and interactions of millions of individuals scaled up to the population level, and some of those decisions and interactions happen to involve one insect eating another. Another swarming insect, the desert locust (Schistocerca gregaria), tends to cannibalize traveling companions that have stopped moving or can’t keep pace with the group, and the threat of cannibalism influences their marching behavior. Individuals keep moving and maintain proper direction and pace to keep from becoming lunch for the guy behind them, and this helps maintain coherent swarm motion.

Snacks for the Road

Sepideh Bazazi and colleagues from the U.S. and Australia thought that the same would be true of Mormon crickets. To test their hypothesis, they used a unique natural “laboratory:” two sites in Daggett County, Utah where lingering swarms of crickets provided a continuous stream of test subjects.

They captured four crickets, hot-glued them to pieces of pieces of wood and placed them, facing in four different directions, in a row in the path of the approaching swarms. As the swarm approached the sacrificial lambs, the researchers filmed things from above. They then repeated the catch-glue-set out-film process with different crickets for a total of 24 times.

After reviewing the films, Bazazi and his co-authors tallied the number of times an approaching cricket from the swarm stopped within one antenna-length of a glued cricket. They also categorized and counted the outcomes of these encounters, whether it was the approaching cricket moving away, making a successful attack and biting the trapped cricket or making an unsuccessful attack and getting kicked away by the bait.

They counted 2,056 total encounters over 24 trials, an average of 4.3 encounters per minute per immobilized cricket. Fifty-nine percent (1,258) of the encounters resulted in attacks, and 58% (734) of those were successful.

Blood on the Sand

The biologists came away with three observations. First, female Mormon crickets are more likely than males to engage another cricket that isn’t moving, even when there’s an even sex ratio in the swarm, but aren’t more likely to be successful if they attack (on the other hand, the sex of the immobilized crickets had no effect on the number of crickets that approached or attacked them). The researchers hypothesize that females engage potential victims more often because they have more demanding nutritional requirements.

They also noted that crickets whose bodies were perpendicular to the direction of swarm movement were most vulnerable to encounters, since a side-facing cricket exposes a larger surface area. The right and left sides of the immobilized crickets were more likely to be approached than the head and back end, but all body areas were equally likely to be attacked and attacked successfully. Crickets who don’t want to become dinner minimize their risk of being bothered by protecting their flanks, which means moving along with the swarm. Like with the locusts, the threat of cannibalism aids the smooth flow of traffic.

Lastly, they found that the duration of a moving cricket’s encounter with an unmoving cricket and the likelihood of that cricket successfully attacking and cannibalizing another are strongly affected by the behavior of the other crickets around it. The number of moving crickets already in contact with an immobilized one increased the probability that an approaching cricket would also attack the victim and that that attack would be successful. While moving crickets were already highly likely to approach and attack even in the absence of others, that likelihood almost doubled once there were nine or more other crickets already on the attack. The more crickets attacking a victim, the longer each new approaching cricket stuck around, too.

Bazazi suggests that this happens because of “social facilitation,” an increase in the frequency of a behavior in response to others engaged in that same behavior. This could work in two ways with the crickets. First, the crickets already interacting with and cannibalizing a stationary cricket could provide approaching crickets with social information about the location of food. Second, cues from the wounded cricket could create a “blood in the water” effect, spurring approaching crickets to attack and feed.

Either way, the result is that crickets move towards others in the swarm, ultimately helping to maintain cohesive movement and momentum for the group, making both the threat of cannibalism and the desire to grab a meal on the go driving factors of swarm movement.

*The insect’s name actually comes from a mutually destructive encounter with a religious group. The wheat crop at first Mormon settlement in Utah was supposedly set upon by the bugs and rescued by the miraculous appearance of a flock of California gulls, which devoured the entire swarm.

References: Bazazi S, Ioannou CC, Simpson SJ, Sword GA, Torney CJ, Lorch PD, & Couzin ID (2010). The social context of cannibalism in migratory bands of the Mormon cricket. PloS one, 5 (12) PMID: 21179402

Bazazi S, Buhl J, Hale JJ, Anstey ML, Sword GA, Simpson SJ, & Couzin ID (2008). Collective motion and cannibalism in locust migratory bands. Current biology : CB, 18 (10), 735-9 PMID: 18472424

Sword GA, Lorch PD, & Gwynne DT (2005). Insect behaviour: migratory bands give crickets protection. Nature, 433 (7027) PMID: 15716941

Images: Cricket photo Whitney Cranshaw, Colorado State University; cricket swarm photo Steve Jurvetson cricket drawing by Art Cushman, USDA, Property of the Smithsonian Institution Department of Entomology. Both via Bugwood.org and used under a Creative Commons License

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Man of Steel: Armor, not weapons, protects harvestmen from certain doom


ResearchBlogging.org

A lot of people mistake harvestmen for spiders, but there are two big differences between the two orders of arachnids. One, harvestmen do not scare the living shit out of me and I do not need to my girlfriend to kill any that wander into our house. Two, the eight-legged freaks commonly called daddy longlegs are awesome beyond your wildest imagination, whereas spiders are demons from Hell and are not awesome.

Among the 6,400 known species of havestmen, there are females who can give birth without the need for a male to fertilize thier eggs. There are males who mate with multiple females and then guard all the eggs, sometimes from egg-eating females they’ve recently mated with. There are harvestmen who enjoy each other’s company so much that they live together in groups of 70,000+ individuals. Then, there’s the granddaddy of wieners, willies, dongs and johnsons, the 400-million-year-old fossilized harvestman that possesses the world’s first known penis.*

Harvestmen are unique – and, again, awesome – among arachnids in that they have a pair of exocrine glands that secrete a variety of compounds like quinones, ketones and phenols that they use for communication, defense and even as antibacterial agents. Producing these chemicals is costly, though, and can deplete a harvestman’s energy reserves and affect their adult size, fitness and reproductive success.

For animals that produce chemical defenses, but also employ alternative defenses that are less costly, it makes sense use the cheaper options first and reserve the chemical weapons until they’re absolutely necessary. Harvestmen have a number of defensive options besides their chemical secretions, like running away, playing dead, pinching attackers with their mouthparts or leg spines and shedding legs as a distraction. They also have a hard exoskeleton that can protect them from injury in an attack.

If it can take a bit of punishment and keep a harvestman alive long enough for a predator to get frustrated and give up, relying on the exoskeleton would be the cheapest and best defense option. However, harvestmen are not a group that’s gotten a lot of attention from scientists (about one third of today’s known species were described by one guy, Carl Friedrich Roewer), so no one knew if this was actually the case. To find out, Elene da Silva Souza and Rodrigo H. Willemart, from the University of Sao Paulo, arranged a five-round arachnid vs. arachnid cage match to look at the aggressive and defensive behaviors of the harvestman Discocyrtus invalidus and the spider Enoploctenus cyclothorax.

E. cyclothorax is a large ambush hunter. Prior to this study, no one knew if it preyed on D. invalidus, but the spider’s penchant for dining on large roaches, crickets, other spiders and other species of harvestmen made it a sensible choice to play the role of predator. The first experiment tested whether or not the spider was actually up for the task and would go after the harvestman. Thirty-two spiders were collected from the wild and starved for one month to ensure they were hungry. Sixteen spiders were each paired with one harvestman and left together in the same tank for five days, while the other 16 spiders were each left in a tank with some crickets for the same amount of time.

The tanks were monitored once a day and inspected at the end of the five days. Thirty percent of the crickets were preyed upon within an hour of being placed in the tank and at the end of the experiment, less than a quarter of them were still alive. On the other hand, every last one of the harvestmen was still alive at the end of the fifth day and no injuries were noted on any of them.

Previous research by Willemart focused on starving E. cyclothorax and isolating it with another harvestman species, M. cuspidatus. In that study, only two out of nine spiders attacked and fed on the harvestman. Each of these spiders waited a full week in the tank before feeding and each fed on only one harvestman. The remaining seven spiders did not feed on the harvestmen even after 68.6 days in the tank and 21.8 days of starvation before even being placed in there. Every one of those spiders starved to death. Some of these spiders did attack, bite or touch the harvestmen, though, and strictly avoided them after that, suggesting that in close contact they recognized undesirable or dangerous prey through chemical signals.

The second experiment focused on the details of the spiders’ and harvestmen’s interactions. Thirty-two spiders were starved and then each exposed to either a harvestman or a cricket and individually monitored the whole time. Eighty-one percent of the spiders attacked the harvestmen, but did not consume them, and ignored or avoided them after the first attack. Of the 13 harvestmen that were attacked, seven walked away from the spiders, five remained stationary and one was consumed. None of them attempted to defend themselves by pinching or biting the spiders, playing dead or releasing an amount of chemical defenses that the researchers could see or smell.

Silva Souza and Willemart wondered if the harvestmen were indeed releasing defensive secretions, but in very small doses undetectable by the human eye and nose, a subtle chemical shield that could explain their lack of concern with being eaten. For the third experiment, forty-eight spiders were each isolated with either a harvestmen that had its glands obstructed with glue, a harvestmen with glue on its back, crickets with glue on their back or crickets with no glue. The unclogged harvestmen were attacked as often as the clogged ones (both types of cricket were attacked and eaten almost equally, so the glue seems to have had no effect on the spiders), suggesting that the harvestmen secreted no chemicals even when they were able to. Again, no other defensive behaviors were seen and 75% of the harvestmen simply walked away from the attacking spiders, 21% just stood there during the attack and one was eaten.

The harvestmen weren’t using a chemical defense, but if they did, would it even do any good? The researchers collected the chemical content and secretions of ten harvestmen’s scent glands for a fourth experiment. Several spiders were offered crickets, and as soon as the spiders captured their meal, the researchers applied the harvestman secretions to the some of spiders’ mouths and applied water to some of the others. None of the spiders released their crickets. While E. cyclothorax released captured crickets in other studies after a dose of secretions from the harvestman Acutisoma longipes, the chemicals from D. invalidus didn’t ruin its meal here.

Four rounds into things, the harvestmen had put up no mechanical or chemical resistance to attack. They hadn’t fought back, they hadn’t run and they hadn’t used their chemical defenses, which, it turns out, didn’t seem to bother the spiders anyway. The spiders kept giving up, though, and mostly steered clear of the harvestmen after a single attack or encounter. The harvestmen only had one more trick up their sleeves…

I am Harvestman!

The harvestman’s exoskeleton had to be the trick to fending off the spiders. To test the exoskeleton’s mettle, Silva Souza and Willemart took ten spiders and held harvestmen up to their mouths to be bitten. The bites were recorded on video, and later viewing revealed that only one of the spiders pierced the body of the harvestmen.

Photographing a harvestman with a scanning electron microscope revealed the chinks in the armor that allowed that single bite. The harvestman’s exterior is hardened on its back, bottom, sides and legs. The only soft, unprotected spots on D. invalidus are its mouth, the articulations of its appendages and the tips of the legs. There’s such extensive protection that the spiders, despite being much larger and stronger, rarely managed to find a spot their teeth could sink into. The harvestmen make the most of their armor with the way they walk keeping their body close to the ground and forming a “fence” around their body with their legs.

These experiments don’t rule out the use of defensive secretions by D. invalidus at all times and places, and its defensive chemicals might be its best bet against other predators. When staring down E. cyclothorax, though, a harvestman in shining armor is efficient and effective enough.

*There is one awesome harvestman fact that’s only a myth, though. Urban legend has it that the harvestman is the most venomous animals in the world, but possesses fangs too short or a mouth small to bite a human. However, no known species of harvestman has venom glands or fangs.

Reference: Souza, E., & Willemart, R. (2011). Harvest-ironman: heavy armature, and not its defensive secretions, protects a harvestman against a spider Animal Behaviour, 81 (1), 127-133 DOI: 10.1016/j.anbehav.2010.09.023

Willemart, R., & Pellegatti-Franco, F. (2006). The Spider Enoploctenus Cyclothorax Avoids Preying On the Harvestman Mischonyx Cuspidatus. Journal of Arachnology, 34 (3), 649-652 DOI: 10.1636/S05-70.1

Image: “Macro shot of Opiliones Harvestmen” by Mehran Moghtadai, used under a Creative Commons license

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Context is King: Squirrels’ bodies react differently to warnings about different predators

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One if by land, and two if by sea/And I on the opposite shore will be/Ready to ride and spread the alarm/Through every Middlesex village and farm/For the country folk to be up and to arm.

On April 18, 1775, Paul Revere told three Boston patriots to hang two lanterns in the steeple of the city’s Old North Church. A militia waiting across the Charles River in Charlestown kept an eye out for these signal lanterns and were prepared act appropriately as soon as they saw one or both of the lights stab out at the darkness. The meaning of the two lanterns has been memorized by countless American schoolchildren in the century and a half since Longfellow published “Paul Revere’s Ride.” One lantern told the militia that the British Army would march over Boston Neck and the Great Bridge, and two meant that that the Redcoats would take boats across the river to land near Phips farm.

Many, if not most, birds and mammals that live in groups have their own signals and alarms that alert members of the group to predators and other dangers. An alarm call can mean the difference between life and death for animals who didn’t detect the threat on their own and younger animals who are especially vulnerable to predation. Belding’s ground squirrels take a cue from Revere and use two different alarm calls to warn of two types of danger. Whistle alarm calls signal aerial predators and trill alarm calls signal terrestrial ones. A squirrel needs to react differently to each type of call and to each type of predator. Listeners respond to whistles by entering a burrow or another hiding spot, and adopt a “posting” stance on their hind legs in response to trills.

When young Belding’s squirrels first emerge from their burrows when they’re a month old, they don’t respond appropriately to the two different calls and if they respond at all, they typically just freeze. They pick up on the appropriate behavioral responses very quickly, though, often within five days of coming above ground. Watching the responses of mom, dad and the other squirrels could teach a youngster what they need to know pretty quickly, but Jill Mateo, from the Department of Comparative Human Development at the University of Chicago, wondered if there was also a physiological factor. For many species, the sight, sound or even odor of a predator spurs physiological changes that make individuals better prepared to track predators and the responses of other animals, hide and be still, defend itself or run/fly/swim like hell. Maybe the body itself reacts differently to a whistle than it does to a trill – to two lanterns than it does to one, if you will – and helps prime a squirrel for one response or another.

For the first five days after they come aboveground, juvenile ground squirrels show a higher level of cortisol (a steroid hormone released in response to stress) than during the days before emergence or the weeks after. To see if the hormone had some role in ground squirrels learning appropriate anti-predator behavior, Mateo tested how the levels of the hormone changed in response to different alarm and non-alarm calls. She caught pregnant female squirrels at a few sites near the Sierra Nevada Aquatic Research Laboratory (SNARL) at Mammoth Lakes, CA and brought them back to the lab so they could give birth and rear their young. Around the time the babies would normally leave the burrow, Mateo placed them, in pairs, in a large, dark wooden box once per day and played either a recording of ground squirrel whistles alarm, trill alarm calls, squeals young squirrels use during play or a silent control.

Every time a squirrel heard a recording, Mateo took a blood sample from it. These tests continued until she had one blood sample for each of the four recordings from a squirrel or until the squirrel turned 35 days old (in some cases, she was not able to get complete samples from a squirrel before it reached the age limit or did not have a large enough sample to analyze). After two rounds of tests in 2006 and 2008, Mateo had partial samples from 32 squirrels and complete samples from 17 of those.

Mateo analyzed the samples and, using a squirrel’s cortisol concentration following the silent stimulus as its baseline, looked at the hormone’s percent change in response to the alarm calls and play noises. Because multiple squirrels from several different litters were tested, Mateo averaged the cortisol responses to each recording for each litter.

For all litters, cortisol concentrations were higher following playback of trill alarm calls than after the other recordings (see graph above). The change in cortisol levels compared to the baseline was only significant in response to the playback of the trill alarm calls (graph below). The whistle alarms did not increase cortisol concentrations, but earlier research by Mateo showed that they do elicit bradycardia, a slower than normal heart rate.

So the squirrels do have different physiological responses to the two alarm calls. What relationship do these changes inside the body have with behavior, though, and what do they have to do with aerial versus ground attacks? Mateo hypothesizes that cortisol might not increase in response to whistles because attacks by avian predators often only last a few seconds and most birds don’t make repeated attacks if their first one is unsuccessful; the attack would be over before circulating cortisol increased. Bradycardia is associated in young squirrels with decreased motor activity and enhanced information processing. If the heart slows in response to whistles, the squirrels can stay still and pay attention in case it needs to make a break for another hiding spot.

The terrestrial predators that squirrels respond to with trills, on the other hand, usually spend a significant amount of time (up to 30 minutes) either moving around squirrel burrows or waiting near one to attempt an ambush. Increased cortisol makes glucose available as fuel, allowing for sustained vigilance in posting stances and, if needed, for multiple escape attempts.

Both of these physiological reactions increase arousal and attention in a variety of species, so both might simply aid young squirrels in noticing and paying attention to the responses that nearby adults have to the alarm calls, making for a faster association between the alarms and their appropriate responses.

References: Mateo JM (2010). Alarm calls elicit predator-specific physiological responses. Biology letters, 6 (5), 623-5 PMID: 20236965

Mateo JM (1996). Early auditory experience and the ontogeny of alarm-call discrimination in Belding’s ground squirrels (Spermophilus beldingi). Journal of comparative psychology (Washington, D.C. : 1983), 110 (2), 115-24 PMID: 8681525

Image: “Belding’s Ground Squirrel in the Sierra Nevada Mountains, California, USA” by Justin.Johnsen via Wikimedia Commons. Used under a Creative Commons Attribution 3.0 license.

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Deathstalker v. Nightstalker: Bats take down highly venomous prey without a care in the world

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There are some 1,400 described species of scorpion in the world, and while only 25 of those have proven they can take down a human being with their venom, many more of them can easily injure and kill smaller creatures. Given that, you’d expect scorpions to be important predators in desert food webs, but you might not expect them to be equally important as prey.

Otonycteris hemprichii

Yes, despite the pincers and the stinger and the venom, plenty of animals – among them, centipedes, tarantulas, lizards, owls,shrews and bats – regularly chow down on scorpions. Hemprich’s long-eared bat (Otonycteris hemprichii, at right), found in deserts in northern Africa, the Middle East and south-central Asia, considers scorpions a major food group, along with beetles, centipedes and spiders. In Israel’s Negev Desert, the proportions of these groups in the bat’s diet changes throughout the year, with scorpion fragments found in only 10% of bat droppings in the early spring and in a whopping 70% in the late summer.

That’s a whole lot of scorpions they’re eating, and while some of those are certainly weakly toxic Large-clawed Scorpions, the bats also prey on the Palestine yellow scorpion (Leiurus quinquestriatus, below). Everything you need to know about L. quinquestriatus can be summed up in its nickname, the deathstalker. These scorpions are considered some of the most dangerous in the world and possess a highly toxic venom that contains a grab bag of neurotoxins. Their sting can cause extreme pain, fever, convulsions, paralysis and death (via heart or respiratory failure), even in humans. These scorpions are also “sit-and-wait predators” that hunt by remaining quiet and still and lashing out at unsuspecting prey that wanders too close.

They certainly sound appetizing, but how do the bats deal with prey that present such a challenge to both detecting and disabling them? Carmi Korine, of Ben-Gurion University of the Negev in Midreshet Ben-Gurion, Israel, and colleagues found that Hemprich’s long-eared bat is what’s known as a gleaner, which means it takes prey from surfaces and not right out of the air, as many bats do. Korine and his team hypothesized that, like gleaning Pallid bats that prey on scorpions in North America, Hemprich’s bat might rely on passive gleaning to find its meals, simply listening for the prey to make noise instead of actively using echolocation to detect it based on its echo signature. The researchers figured that, if that was the way the bats hunted, then they would select prey based on 1) body size (bigger scorpions being easier to detect), and 2) toxicity (less venomous scorpions posing less risk of injury).

The team captured eight O. hemprichii individuals, set them up in a room with a scorpion buffet that included both living and dead Large-clawed Scorpions (Scorpio maurus palmatus), Israeli common scorpions (Buthus occitanus israelis) and, of course, deathstalkers.

When the bats took off to search for food, they spent a few minutes circling the room and dropped down directly onto a scorpion once they noticed it. They only went after the live scorpions, ignoring the dead ones and even walking right over motionless live ones if they missed on their initial divebomb, confirming that they glean passively and rely on prey noises.

Once they landed on a scorpion, the bats immediately started biting the scorpions’ heads. The scorpions did not take this lying down and fought back, stinging the bats on the head and face and, in one case, under the eyelid. The bats made no observable attempts to either avoid or disable the stingers and once they had killed the scorpions they often ate the whole thing, including the stinger and poison gland.

This is how the bats hunted all the scorpions. Contrary to the researchers’ predictions, the bats showed no preference among scorpion species based on either on size or toxicity, diving on their prey immediately after detection without any further inspection and going only on limited acoustic information. In 49% of the test sessions the bats actually went after the more poisonous of the available species (and in 24 direct comparisons, the deathstalker was chosen 50% of the time).

The researchers did not have an explanation for the bats’ indifference to the danger their meals pose, but speculated that either scorpions aren’t able to pierce the bat’s skin, or that the bats have at least a partial tolerance to the venom. Given that the bats regularly ate the stingers and venom glands, it seems more likely that their just tough enough to handle what the deathstalkers can dish out.

For other takes on this study, see Michael Marshall’s post at Zoologger and Zen Faulke’s post at Neuro Dojo .

Reference: Holderied M, Korine C, & Moritz T (2010). Hemprich’s long-eared bat (Otonycteris hemprichii) as a predator of scorpions: whispering echolocation, passive gleaning and prey selection. Journal of comparative physiology. A, Neuroethology, sensory, neural, and behavioral physiology PMID: 21086132

Images: “Otonycteris hemprichii” by Wikimedia Commons user Charlotte Roemer, used under a Creative Commons license.

“Deathstalker near Tzehelim, Israel” by Wikimedia Commons user Yair Goldstof, used under a Creative Commons license

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