Crowdfunding black widow research

For the past six months, Sean and I have been spending most of our nights observing black widows in their natural habitat on Vancouver Island, BC. We did a couple of short experiments during our time in the field, but the vast majority of our work involved simply observing the spiders as they went about their business. The goal was to get a better understanding of the natural behaviour and mating dynamics of this population. This kind of basic natural history research (as opposed to experiments designed to test specific hypotheses) is not often done because it can be challenging, time consuming, and expensive, and is looked on by some as not as important as hypothesis-driven research. I think this is a shame, because there is still so much waiting to be discovered if we only take the time to look. And it is easy to overlook amazing and potentially important phenomena if we don’t take that time. It’s also easy to make incorrect conclusions about the way the world works when we rely only on experimental data and don’t already have a good understanding of the natural history of the organisms we are studying.

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Sean and I doing black widow research at Island View Beach. Drone photo: Sean Lambert (used with permission)

Let me tell a quick story. You may recall that last year our study about web reduction behaviour in black widows was published. (Here’s a plain language summary of the research). Based on observations of sexual behaviour of black widows in the laboratory, we knew that males often engage in web reduction when courting on the webs of virgin female. The male cuts up sections of the web, bundles them up, and wraps them with his own silk. We wanted to know the function of this behaviour, so we ran some carefully designed experiments in the field, and concluded that web reduction allows males to avoid competition by decreasing the attractiveness of the female’s web. We assumed that this is a common tactic used by the first male to arrive at a female’s web, in order to avoid other males from finding the female and interrupting his courtship efforts. I was looking forward to learning more about web reduction this summer as we observed black widows behaviour across the course of a mating season. Guess how many times we observed web reduction in the field? Exactly once. All our laboratory observations were of males introduced onto the webs of adult females. It turns out that in the field, males mature before females do, and most of the time they arrive at a female’s web before she is sexually mature (and before she has the attractive chemicals on her web that trigger web reduction behaviour). Our previous results were not wrong, but without this year’s fieldwork we might never have realized that by focusing on sexual interactions between males and adult females we were missing a big part of the story. How males find immature females, and their behaviour once they do, is likely much more important for avoiding competition than web reduction. There is so much we still don’t know about black widows, that’s just waiting to be discovered!

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Male western black widow (Latrodectus hesperus) engaged in web reduction behaviour on an adult female’s web. Photo: Sean McCann

I feel extremely lucky to have had the opportunity to do this fieldwork as part of my PhD research. Spending six months in the field is very expensive, and a bit of a risk scientifically, because exciting results are definitely not guaranteed. I will likely not have the opportunity to do extended natural history fieldwork like this again, because funding for basic research is increasingly hard to come by. Government funding for science is more and more focused on applied work that has clear benefits for the public. The problem with this model is that future applications and benefits of basic research are often difficult to foresee.

In my case, there are some obvious potential applications of studying chemical communication in widow spiders. Some species are invasive or considered pests in certain areas (including vineyards in BC), so a way to control them without using harmful pesticides would be very useful. Once we understand how male and female black widows respond to one another’s chemical messages, and the identity of the chemical compounds involved, we may be able to develop ways of using these naturally occurring messages to trap and remove spiders from areas where they are a problem. Partly because of this, I think, I was successful in securing an NSERC scholarship to do my PhD (thank you Canadian taxpayers!!!) but even so, I am not exactly drowning in money to support my research.

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Female black widow on her web at Island View Beach. Photo: Sean McCann

The rest of my PhD work will take advantage of the excellent understanding we now have of how black widows actually behave in nature. I will be able to design laboratory experiments that are as naturalistic in context as possible, and use what we now know based on this year’s field observations to make well-informed conclusions. However, to really understand how chemical information affects black widows over the course of their development and their mating interactions, the best place to do the work (both experimental and observational) is in their natural habitat, and this is where the title of the post comes in.

If I had my wish, next summer I would go back to the field for four months (the full mating season) to do experimental and observational studies of black widows that will improve our understanding of their chemical communication. Our lab’s funding is sufficient to pay for travel to and from the field site and for the basic equipment we’ll need to do the research*, but there’s one problem. It’s simply not safe to do the work I have planned (often at night) alone. I will need a field assistant, and that field assistant will need a salary. (Volunteer field assistantships for this kind of work do happen, but they are bad for science, and not an option we would consider.) I can and will apply for several graduate student research grants, and if I am successful these will help defray the costs of the planned fieldwork. Unfortunately, most of these explicitly do not allow the funds to be used to pay salaries. That’s where you come in!

*UPDATE: Here is a note on our campaign page where my supervisor explains the funding situation and why we’re asking for money in a bit more detail.

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The logo and hashtag for the project. Logo designed by The Vexed Muddler.

For the next 30 days, Sean McCann (who was my field assistant this year, and who will continue to collaborate on the project one way or another), my supervisor Maydianne Andrade, and I will be running a crowdfunding campaign on Experiment.com as part of their Arachnid Challenge. We hope to raise the $6000 USD (the salary of a full time field assistant for four months) that we would need to make my plans for another season of black widow fieldwork a reality. This is an opportunity for anyone to support and participate in our research. If we are successful, we will post regular updates about our plans and progress, and share stories and photographs from the field.

Please check out the campaign page for more details, and consider donating. Even $5 will make a difference, and everyone who contributes will receive our heartfelt thanks and be acknowledged in all publications and presentations resulting from the research. If you donate $15 USD (about $20 CAD) or more, we are offering various tangible tokens of our very deep appreciation, including swag with our fantastic logo (designed by the brilliant Vexed Muddler) and prints of Sean’s beautiful photographs. Even if you cannot support the project with a donation, I would be so grateful if you would consider sharing the campaign with your friends and colleagues on social media, email, or in real life. The more people we reach, the more likely we will be to reach our goal!

Thank you so very much in advance for your support – we really appreciate it!!!

Web reduction for rival obstruction!

This post is about a new paper just published online in the journal Animal Behaviour, titled Web reduction by courting male black widows renders pheromone-emitting females’ webs less attractive to rival males by Catherine Scott, Devin Kirk, Sean McCann, and Gerhard Gries! You can read the full text here (free access until 28 August, 2015).           All photos and video are copyright Sean McCann

This short video shows a male western black widow engaged in web reduction behaviour – a common element of the complex courtship rituals males perform on females’ webs. You can see him cutting some silk lines, then pulling silk out of his spinnerets with his last pair of legs, wrapping it around a bundled up section of the female’s web.

Web reduction behaviour is somewhat puzzling. This male black widow is attempting to convince a potentially cannibalistic female several times his size to mate with him. Destroying large areas of her home – which she relies on for both prey capture and protection from predators – is not the most obvious approach. So why do males do it (I know, the title of the paper probably gives this one away), and why do females let them?

Before we address the mystery of web reduction, let’s take a step back and set the scene for this story. It’s a pretty juicy one – there’s attraction, courtship, rivalry, and manipulation! Or maybe not manipulation… we’ll see!

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Black widows are sexually dimorphic: the familiar female is on the left, and the much smaller and more brightly coloured male is on the right. My study species is the western black widow, Latrodectus hesperus.

Island view beach, on the Saanich Peninsula of Vancouver Island, BC, is a beautiful place to visit. The site shown below is on the lands of the Tsawout First Nation, who have kindly allowed me to collect spiders and do field work here over the past few years.

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This coastal sand dune ecosystem supports a great diversity of organisms, but the black widows are the dominant web-building spiders. Females build their tangle-webs under the driftwood logs at a density of 2-3 webs per square metre of available habitat. There are many logs on this beach; correspondingly, there is a huge population of widow spiders.

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At our field site, black widows build their webs under driftwood logs – often several females can be found living under a single piece of wood!

Female black widows almost never leave their webs, so when it comes time to mate, they need males to come to them. The solution to this problem comes in the form of pheromones on their silk. These chemical messages are kind of like scent-based personal ads, that provide the male with information about the female’s mating status and whether or not she’s well fed (sexual cannibalism is rare in this species, but starving females will sometimes eat males!).

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If the female’s silk pheromone was actually a personal ad, it might say something like this!

Adult male black widows have only one goal in life: find a female to mate with (and become the father of as many offspring as possible). Once they mature, males stop capturing prey and abandon their webs for a more a nomadic lifestyle. If they detect an attractive female’s pheromone in the air, they follow it to her web.

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A nomadic western black widow male traverses the sand dunes in search of a mate. Note: “pheromone trail” added for dramatic effect.

Once he arrives on the female’s web, the male begins an elaborate courtship display, dancing on the web to transmit vibratory messages (including “male, not meal!”) to the female. It may take many hours of courtship before copulation finally occurs.

male_courtingSoon after he arrives, the male may start to destroy the female’s web. He cuts out sections, bundles them up, & wraps them in his own silk. Males usually reduce the area of the web by about 50%, and gather the destroyed sections up into loose silk-wrapped packages. These can be rope-like (as in the photo at the top of this page) or a tighter ball that has been wrapped extensively by the male like the one below.

silk_ball_smallNow to address our earlier question: why do the males engage in this behaviour? 

Well, black widows are not the only spiders who do web reduction. Other species in the same family (Theridiidae) and others (including Linyphiidae) have similar behaviour. Watson showed in 1986 that web reduction in the sierra dome spider makes the female less attractive to rival males. He concluded that by bundling up the female’s web, the male decreases the surface area from which the silk-borne sex pheromone is released. Some researchers have assumed that it works the same way in other species. Others have suggested that web reduction could function in communication between the male and the female, perhaps improving vibration transmission through the web, or transmitting a male silk pheromone to the female. It could have one or both of these functions in black widows, but until now, no one had ever investigated!

Neriene litigiosa

The sierra dome spider, Neriene litigiosa (family Linyphiidae).

We set out to determine whether web reduction decreases female attractiveness to male black widows in a natural setting. We were pretty sceptical that reducing the web surface area by only about 50% could limit pheromone emission. Usually you have to decrease the dose of a pheromone by an order of magnitude to see any difference in attractiveness. However, males aren’t just bundling up the female’s pheromone-laden silk – they are also adding their own. We thought maybe it could be the addition of the male’s silk (and associated pheromones) that keeps other males away. We designed an experiment to try to find out.

First, we put a bunch of female spiders in cages and allowed them to establish webs. Then we loaded up the cages and took them, and a batch of males, to our field site.

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This is what (part of) a truckload of black widows looks like. Here, my coauthor Devin is loading the cages containing females and their webs into the back of the lab pickup.

Once we got to our field site, we removed the female spiders from their cages (because we wanted to look at the attractiveness of silk only, not the females themselves) and set up four treatments: intact webs, mechanically reduced webs (with half the silk cut out), male-reduced webs (with about half the silk, on average, bundled and wrapped by the males we brought) and empty cages as controls (to confirm that captured males were actually attracted to the silk in the cages, not just wandering randomly).

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Four treatments: intact web, scissor-reduced web (50% of silk removed entirely), male-reduced web (courting males bundling up about 50% of silk on average), and no-web control.

We then turned the cages into traps that would capture any wild males attracted to the silk inside by surrounding them with sticky strips. Then we set the traps out on the beach in groups of four – one for each of the treatments.

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The experimental setup. Each of the four traps contains a different treatment, and the white sticky strips surrounding the cages trap males that are attracted to the silk inside the cage.

We set the traps out at sunset (black widows are nocturnal) and waited to see what would happen. Soon the data started strolling in. We checked the traps every three hours, collecting and preserving any captured males. The sheer number of males out on the prowl was incredible – some webs attracted more than 10 males overnight!

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Close-up of a trap containing a pheromone-laden female’s web, with a male black widow captured outside on the sticky strip.

After 24 hours, just by looking at the vials full of male spiders we had captured, the results were clear (if you want to see statistics, you can read the paper!). Male-reduced webs caught only about one third as many males as intact webs, so web reduction does in fact decrease attractiveness! As we suspected, however, removing half of the silk entirely did not significantly reduce a web’s attractiveness – we captured almost as many males outside scissor-reduced webs as intact webs. (A few spiders got trapped outside the empty control cages – they may have blundered into the sticky strips on their way toward an an attractive web.)

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Beautiful data. It’s not often that the raw data tell the whole story, but here they do!

Evidently, when a male black widow reduces a female’s web, whatever he is doing is much more effective at decreasing its attractiveness than removing half of the pheromone-laden silk entirely. And he’s not actually removing any of the female’s silk – he’s just bundling it up into a ball. There are a couple of potential explanations for how web reduction works. Perhaps the female’s pheromone is not evenly distributed on the web, and the male targets the pheromone-rich silk for web reduction. Then, by wrapping those sections up in his own silk, he creates a barrier that limits the emission of the female pheromone. Another possibility is that the male’s silk has its own pheromone on it, one which other males detect and avoid. Or it could be a combination of both these mechanisms – we’re still not sure. We did another experiment to test the second idea, but the results neither supported nor completely ruled it out (see the paper for more details!). We will try to get to the bottom of this in the future.

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Time for a cute male widow interlude! Look at him peeking out from behind that blade of grass.

For now though, let’s come back to the questions we set out to answer. Why do male black widows do web reduction? It allows them to monopolize the female, by making her web less attractive to other males. Courtship and mating last several hours, so if a male reduces the female’s web as soon as he arrives, he can decrease the likelihood of rival males arriving and interrupting. This may be very important at our field site, where competition for access to females appears to be fierce – during our second experiment, we had one intact web attract over 40 males in a single night! So web reduction is good for the male, because it helps him to avoid competition.

What about the female? Losing her web may be costly – she has to spend time and energy rebuilding it. However, we think she might actually benefit from web reduction too, and that the benefits may outweigh the costs. Sure, her web is important for prey capture and protection, but it’s also really attractive. So attractive, in fact, that even if she doesn’t add more pheromone, it will continue emitting its “come-hither” message for several days. Given number of males we saw arriving at each web during our experiment (40 in one night! even 10 is pretty extreme!), remaining attractive once she has already found a mate might not be so great. Having a choice between multiple males might be a good thing, but the female really only needs to mate once to fertilize all of her eggs. By “muting” her chemical signal though web reduction, the male might be doing her a favour: allowing her to rebuild her web without attractive pheromones (female sex pheromone production shuts off immediately after mating in black widows, but they don’t ever take down their existing webs). Rather than having to waste time and energy chasing off superfluous suitors, this may allow her to get on with the business of producing egg sacs!

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Female western black widow guarding her egg sac. These spiders are very protective mothers!

References and further reading (also linked in the text)

Baruffaldi, L., & Andrade, M. C. (2015). Contact pheromones mediate male preference in black widow spiders: avoidance of hungry sexual cannibals? Animal Behaviour, 102, 25-32.

MacLeod, E. C., & Andrade, M. C. (2014). Strong, convergent male mate choice along two preference axes in field populations of black widow spidersAnimal Behaviour, 89, 163-169.

Salomon, M., Vibert, S., & Bennett, R. G. (2010). Habitat use by western black widow spiders (Latrodectus hesperus) in coastal British Columbia: evidence of facultative group living. Canadian Journal of Zoology, 88(3), 334-346.

Stoltz, J. A., McNeil, J. N., & Andrade, M. C. (2007). Males assess chemical signals to discriminate just-mated females from virgins in redback spidersAnimal Behaviour, 74(6), 1669-1674.

Watson, P. J. (1986). Transmission of a female sex pheromone thwarted by males in the spider Linyphia litigiosa (Linyphiidae). Science, 233(4760), 219-221.

Sex pheromone on the silk of black widow females – more complicated than we thought

The first paper from my MSc has just been published online in the Journal of Chemical Ecology! This study was a collaboration with colleagues Sean McCann (bioassay designer, photography/videography master, and all-around awesome assistant), Regine Gries (analytical chemistry wizard), Grigori Khaskin (synthetic chemist extraordinaire), and my supernatural supervisor Gerhard Gries. If you don’t have access to the journal, you can read the accepted manuscript here.

Here’s the story of the paper.                                                                                             Note: all photos and the video are copyright Sean McCann.

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A female western black widow (Latrodectus hesperus) on her web. The silk is impregnated with sex pheromones that attract males and trigger courtship behaviour.

When I started my MSc, one of the goals for my research was to “find the pheromone” of the western black widow. What does that mean exactly? Well, we already knew that female black widows (spiders in the genus Latrodectus) produce sex pheromones that are somehow incorporated into the silk of their webs. These are sort of like chemical personal ads – they can provide information about things like the species, sex, age, mating history, and body condition of the individual producing them. When a male black widow matures, his only goal in life is to find a female to mate with. He abandons his web and follows his nose (not literally – we don’t really understand much about how spiders smell but their “noses” are most likely on their legs and pedipalps!) to a nearby female’s web. Given a choice among multiple available females, male black widows will go for a well-fed virgin based on the smell of her silk alone. Once he arrives at her web, he contacts the silk and “tastes” (again with receptors on his legs/pedipalps) the pheromone, which triggers courtship behaviour. We wanted to find out the chemical structure of the female’s sex pheromone.

We had a pretty good idea of what to expect, because other researchers had already identified a pheromone of the Australian redback spider (Latrodectus hasselti). It looks like this:

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N-3- Methylbutanoyl-O-(S)-2-methylbutanoyl-L-serine methyl ester. Contact pheromone of Australian redback spider (Latrodectus hasselti) females.

Male western black widows are actually attracted to the webs of redback females, implying that the structure of the pheromone is similar, if not identical, in these two species. (It’s not necessary for males to discriminate between Australian redback and North American western black widow females in nature, because they never encounter one another, so it wouldn’t be that strange if they shared the same pheromone). So we set out to analyze the silk of our western black widow females, and see if we could find a similar compound.

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We persuaded females to provide us with clean silk by allowing them to build webs on glass frames for three days. We then collected the silk and extracted it for use in behavioural experiments and chemical analysis.

Some silk collection, extraction, and analytical chemistry* ensued (I’ll leave it to you to read the paper for details if you’re interested), and just as we had hoped, our western black widow females had a compound on their silk that was very similar to the redback pheromone above:

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N-3-Methylbutanoyl-O-methylpropanoyl-L-serine methyl ester. Candidate pheromone of western black widow females (Latrodectus hesperus).

Not only is this chemical similar to the redback pheromone, it is also present in small amounts on redback females’ silk. So it seemed like an ideal candidate for the western black widow pheromone, and provided a potential explanation for the attraction between the two species. Now all we had to do was make a synthetic version* of the pheromone and test it on actual males.

Before we could determine whether the compound we had found was in fact the pheromone we were looking for, we needed to come up with a way of comparing its effects with the real thing. We knew that contact with a female’s silk triggers courtship behaviour, but black widow courtship is long and complex, and involves several different kinds of behaviour, some of which are very subtle. The male’s courtship dance sends vibrations through the web to the female, possibly providing information about his quality and identity (including that he is a potential mate, not a meal!). It also involves the production of copious amounts of silk by the male. This male silk carries its own pheromones, and is deposited all over the web and onto the female herself in the form of a “bridal veil” during courtship.

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Male black widow (L. hesperus) engaging in silk-wrapping on a female’s web during courtship. Here the male is wrapping a section of web that he has destroyed during web reduction behaviour, which I will discuss in a future post.

We designed an experimental setup to assess male responses to silk pheromones. We constructed this high-tech device out of bamboo barbeque skewers, laboratory labeling tape, and a paper cup filled with floral foam. The skewers form a “T” and at each end of the horizontal arm we slid on little envelopes made of squares of filter paper folded in half and stapled. This simple and inexpensive device was one of the big successes of the project.

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Our simple and inexpensive T-rod for testing male behavioural responses to contact silk pheromones.

The T-rod design makes it easy to compare an individual male’s response to a test stimulus on one side (for example, a female’s silk wrapped around the paper envelope) to a control (blank paper) on the other.

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Wrapping silk around a filter paper for behavioural experiments.

A male spider is introduced at the base of the “T” and climbs up to the top. Once he gets to the intersection, he can decide whether to go left or right. Males almost always began the experiment by investigating both sides of the “T”, but they spent much longer in contact with the silk-wrapped paper than the blank paper. Not only that, but they spent much of their time wrapping the female silk-wrapped paper with silk of their own – obvious courtship behaviour.

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A male black widow silk-wrapping on a filter paper with silk extract on it.

Knowing that males would respond to female silk in this way on the T-rod, we were now ready to confirm that the behaviour didn’t depend on the structure of the silk itself, and to see if males would respond to our synthetic candidate pheromone in the same way as they would respond to the real thing.

We prepared female silk extract using methanol as a solvent (this is the same idea as vanilla extract, but instead of extracting the flavour of vanilla beans into ethanol, we extracted the chemicals on the silk into methanol) and applied it to one of the filter papers on the T-rod, and methanol alone to the other.

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We tool silk from a glass frame like the one above and submerged it in methanol to extract the pheromones into the liquid, which we then used in behavioural tests.

Males responded in exactly the same way to silk extract as they did to silk itself, spending most of their time on the filter paper impregnated with extract, and wrapping it extensively with silk. Here’s a video showing what that looks like (first at full speed, and then slowed down):

This told us that a pheromone that can be extracted from the silk triggers courtship behaviour, and the structure of the silk itself is not necessary. But when we tested male responses to our candidate pheromone (dissolved in methanol, using methanol alone as a control), things were not so clear-cut. Males spent more time on the pheromone-impregnated paper than methanol alone, but they didn’t prefer it as much as they had preferred the silk extract to methanol. A few males engaged in silk-wrapping when they made contact with our compound, but not the majority, like we had seen for the extract. This means that although our “pheromone” elicited some male activity, by itself it is not enough to consistently trigger courtship behaviour. It seems to be a pheromone component – meaning that the pheromone is a mixture of one or more compounds in addition to the one we identified, and more work will need to be done to figure out what they are.

It would have been nice to be able to say we found the pheromone. But our results suggest that the chemical communication system of black widows is more complicated than we originally thought, and even more fascinating.

In the study that identified the redback pheromone, the researchers measured male activity (the amount of time they spent moving around when in contact with a filter paper impregnated with pheromone), not courtship behaviour. It could be that this pheromone too is only one component of a more complex chemical cocktail. Like our pheromone component, it may be responsible for eliciting searching behaviour, but not quite enough on its own to consistently trigger courtship behaviour by males.

If multiple compounds are involved in these spider pheromones, they might each have different functions. We don’t yet know whether the same pheromone that attracts males is responsible for triggering courtship, or if different compounds provide different kinds of information, about things like a female’s mating status and feeding history. We have learned that the scent-based sexual communication system of black widows is likely more sophisticated than we originally thought, and that there is much more to discover!

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Male and female western black widow on a female’s web.

*Neither the analytical chemistry nor the synthesis of the candidate pheromone were trivial tasks – rather they required the expertise and generous efforts of my very talented coauthors Regine and Grigori. I hope they will forgive me for glossing over the details here! 

Here’s the full citation for our paper:

Scott C, McCann S, Gries R, Khaskin G & Gries G. 2015. N-3-Methylbutanoyl-O-methylpropanoyl-L-serine Methyl Ester – Pheromone Component of Western Black Widow Females. Journal of Chemical Ecology. DOI: 10.1007/s10886-015-0582-x

 

A cunning crab spider

Sean McCann recently returned from an epic journey through the rainforest of Guyana in search of caracaras, and is busy blogging about his adventures over at Ibycter.com (so you should check it out!). To make up for not taking me along, he found and photographed lots of awesome spiders for me to blog about. Here’s the first one!

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Here we have a male crab spider (family Thomisidae) with its prey: an ant in the genus Dolichoderus*. At first glance, this may not seem particularly exciting. A small, hairy, black spider eats an insect. What’s so special about this scene?

Well, the spider appears to be Strophius nigricans, reported to be a specialist predator of ants. Most animals are not big on eating ants because they are generally distateful and well-defended by strong mandibles, stings, and defensive compounds. So specializing on ants is not particularly common, and tends to come along with some neat adaptations.

Strophius nigricans is not well studied, but I managed to find one paper about its predation behaviour. Oliveira and Sazima (1985) observed a male S. nigricans carrying an dead worker ant (Camponotus crassus) in the field in Brazil, and took it back to the laboratory to make some observations. The spider never let go of his ant carcass – this would come in handy later. In captivity, he was provided with some more C. crassus workers, and here his secrets were revealed.

The Strophius male used his ant corpse as a shield for protection against ants during predation. To eat ants, one must spend time near ants, but they don’t take kindly to intruders. The dead-ant-shield provides a clever disguise. Most ants don’t have especially good vision, and instead rely mainly on their senses of touch and smell. Whenever the Strophius male was approached by an ant, he would present his previous meal, which (obviously) feels just like another ant, and, if recently deceased, probably smells right too. As the spider pursued his prey, always attempting to sneak up from behind, he held the ant corpse aloft. Once within striking distance of an unsuspecting ant, he quickly dropped the shield and bit his new victim. Once dead, this new ant was used as a shield.

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Unlike a related crab spider species that preys on ants, Aphantochilus rogersi (a remarkable ant-mimic), Strophius doesn’t look all that much like its victims.  A. rogersi specializes on Cephalotes ants, which have relatively good vision, but its excellent mimicry is probably more important as a defense against visually hunting predators that avoid eating ants. However, a similar mode of defense is not necessarily out of the question for Strophius. The ants it preys on are black and have white hairs on the abdomen. From above, the spider carrying its ant-shield might look just enough like an ant carrying its comrade to fool a potential predator such as a bird.

As it turns out, the conclusion that Strophius nigricans are specialists on the ant species Camponotus crassus appears to be based on Oliveira and Sazima’s observations of the single male discussed above. Here we’ve seen that the spider also takes another species, and it seems that its prey capture technique should work just fine as long as the shield matches the subsequent target prey species. The visual mimicry would presumably be just as effective for any similar sized black ants. This certainly seems like a cool system that could use more investigation!

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*Thanks Alex Wild for the ID!

References:

Oliveira, P. S., & Sazima, I. (1984). The adaptive bases of ant‐mimicry in a neotropical aphantochilid spider (Araneae: Aphantochilidae). Biological Journal of the Linnean Society, 22(2), 145-155. (pdf)

Oliveira, P. S., & Sazima, I. (1985). Ant-hunting behaviour in spiders with emphasis on Strophius nigricans (Thomisidae). Bulletin of the British Arachnological Society.

Bolas spiders: masters of deception

Bolas spiders (members of the genus Mastophora, in North America) are famous for their unusual prey capture technique: rather than a web, they produce a single silk line with a super-sticky ball of glue at the end, which they fling at their prey.

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Female Mastophora cornigera hunting with her ‘bolas’. (Photo: Matt Coors)

The common name ‘bolas spider’ is not particularly accurate, though. A real bolas – two or more weights connected by cord – is swung and thrown at an animal (like a horse, in the image below) in its entirety, and works by getting tangled around the legs of the target.

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By John Miers [Public domain], via Wikimedia Commons

The spider’s ‘bolas’ differs in that it never leaves its owner’s grip, and works by getting stuck to the target, which is invariably a moth. Eberhard (1980) observed that a more appropriate name would be “sticky yo-yo spiders”. The sticky yo-yo prey capture technique is impressive enough (inspired by their speed and accuracy with the bolas, Eberhard named one species dizzydeani for Jerome “Dizzy” Dean, one of the greatest baseball pitchers of all time), but to fully appreciate the wonders of bolas spider biology, we must delve into the secret lives of these aromatic and cryptic spiders. They are masters of deception, both olfactory and visual.

Seductive scents

Hunting with a sticky yo-yo is all very fierce and exciting, but what are the chances that a moth is ever going to fly close enough for the spider to swing at? Not very high. Unless, like the bolas spider, you have a trick or two up your sleeve… er, leg… coverings. Adult female bolas spiders have the incredible ability to produce a chemical cocktail that make them smell just like female moths advertising for mates (actually, no one knows yet which part of the spider’s body is responsible for this wonderful trick). Innocent male moths following what they perceive to be a pheromone trail (whose chemical message indicates that it leads to a sexually receptive female moth) are thus duped into coming in close enough for the spider to strike. This is called “aggressive chemical mimicry”, and it is awesome.

Moth sex pheromones are typically blends of two or more chemical compounds in very specific ratios. The particular chemicals and ratios allow male moths to discriminate between females of their own and other species. If a bolas spider produced just one moth pheromone, they probably wouldn’t do very well, because their diet would be restricted to only a single moth species. It turns out that each species of bolas spider attracts several kinds of male moths, and the best studied of these is Mastophora hutchinsoni.

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Bristly cutworm moth, Lacinopolia renigera. (Photo: Andy Reago & Chrissy McClarren; licensed under CC BY 2.0)

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Smoky tetanolita, Tetanotolita mynesalis. (Photo: kestrel 360; licensed under CC BY-NC-ND 2.0)

Mastophora hutchinsoni attracts four kinds of moths, but more than 90% of their prey consists of two species in the family Noctuidae: the smoky tetanolita (Tetanolita mynesalis) and the bristly cutworm (Lacinopolia renigera). These two moth species produce entirely different sex pheromones, and they are active at different times of night. The problem for the bolas spider is that the bristly cutworm pheromone interferes with the attractiveness of the smoky tetanolita’s pheromone.

 

Here’s where the bolas spiders start to get really fancy. Let’s join an M. hutchinsoni female for a night of hunting, and learn some of her secrets.

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M. cornigera female preparing for a night of moth hunting. (Photo: Matt Coors)

She begins by building her horizontal “trapeze” line, from which she then hangs motionless, with front legs extended in hunting position (but with no bolas, yet). She is already emitting the sex pheromones (well, analogs that are close enough!) of both prey species, but so far, only the early-flying bristly cutworm is active. They aren’t put off by the smell of smoky tetanolita females mixed in with the pheromone of a female of their own species, and soon one is winging its way toward the seductive scent coming from the female spider. It passes close by, but out of reach. This moth is lucky, for now. But no matter; his fate is not our immediate concern. The spider’s outstretched legs are covered with tiny vibration-sensitive hairs (called trichobothria) that allow her to detect the sound of the moth’s wing beats nearby. Now that she knows there is prey about, she springs into action and spends the next minute or two building her sticky bolas.

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Female M. cornigera hunting with her bolas. (Photo: Matt Coors)

 

Once her weapon is complete, she returns to her prey-capture position, with the bolas hanging from one of her outstretched front legs. For her next trick, she will again rely on her ability to detect the wingbeats of flying moths with her leg hairs. She waits patiently, silent and still.

 

 

 

Soon, another hapless male moth picks up the scent and starts winging towards the bolas spider. When her sensory hairs tell her the time is just right, she takes a swing at the approaching moth and connects. Although the moth struggles, shedding scales in its effort to escape, the wet stickiness of the bolas holds it fast. The spider reels the moth in and delivers a fatal venomous bite. She waits a few moments, then wraps her prize in swathes of silk and hangs it carefully from her trapeze line to eat later. The night is young, and the moths will continue flying for some hours yet. The bristly cutworms will remain active until 22:30. Our spider builds a fresh bolas, and settles in to wait. Gradually, the smell of bristly cutworm sex pheromone coming from the spider fades. The smell never disappears entirely, but is soon faint in comparison to the scent of a female smoky tetanolita. The smoky tetanolita males will come out after 23:00, and our spider will be ready for more deadly deception.

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Female M. phrysonoma with captured moths. (Photo: Keith Simmons; licensed under CC BY-NC-SA 2.0)

So far, we’ve discovered some of the adult female bolas spider’s secrets to success, but what about juveniles and males? They don’t use a bolas, but they are no less stealthy and deceitful than their counterparts. Young bolas spiders are also employ aggressive chemical mimicry to attract prey, but they specialize on male moth flies in the family Psychodidae. Each bolas spider species is especially attractive to a particular species of moth flies. It appears to be a pleasing coincidence that small bolas spiders prey on moth flies until they graduate to real moths. Whether or not the sex pheromones of the psychodids captured by each spider are similar to those of moths they specialize on is currently a mystery.

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Moth fly (Psychodidae). (Photo: Ted C. MacRae)

Optical illusions

Mastophora females are not only masters of chemical deception, but they are also visually cryptic, and hide in plain sight from their own potential predators. They do this by mimicking bird poop.

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Excellent bird-poop mimicry by Mastophora cornigera. (Photo: Matt Coors)

The female spiders spins herself a silken mat on the surface of a leaf, and clings to it with her legs drawn in tightly around her cephalothorax.

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Another bird poop mimic, female M. phrysonoma, with visitors! (Photo: Matt Coors)

But wait, what are those tiny red things? At first glance, they could easily be mistaken for mites, but no! These are tiny males, presumably interested in mating with the comparatively massive female. Bolas spider males are usually less than 2 mm long, while females are typically 10 – 15 mm long, and sometimes as large as 2 cm!

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Another shot of the incredible bird poop mimicry and extreme sexual dimorphism of M. phrysonoma. (Photo: Matt Coors)

Because the females are so cryptic and males are so tiny, almost nothing is known about the sexual behaviour of bolas spiders. As a researcher studying sexual communication and mating behaviour in spiders, I sure would love to know how the males in the photos above found the female and what happened next! Most likely, the female bolas spiders produce attractive sex pheromones just like the moths whose chemical communication they exploit. As far as I am aware, however, no one has investigated the sex pheromones of bolas spiders. One hypothesis that might explain the evolution of their mimicry of moth pheromones is that their own chemical signals have compounds in common with those of their prey. In fact, this is a hypothesis that Andy Warren is investigating for a different group of spiders that also mimic moth pheromones – orb weavers in the genus Argiope.

If you’re not familiar with spider systematics, it might seem odd that two groups of spiders that look so different and have such different prey-capture techniques share the amazing ability to lure male moths to their doom. In fact, bolas spiders are orb-weavers (at least, they are members of the orb-weaver family Araneidae), they just don’t build webs like most of their relatives. Like orb-weavers, bolas spiders regularly eat their silken traps and recycle the silk proteins to use another day.

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Argiope aurantia female on her orb-web. (Photo: Suzanne Cadwell; licenced under CC BY-NC 2.0)

See the family resemblance?

To see a female bolas spider in action, check out this video clip from David Attenborough’s “Life in the Undergrowth” series. (The bolas spider segment starts at 3:00, but the first few minutes about the redback spider are also worth a watch!)

 

Special thanks to Matt Coors for kindly letting me feature his fantastic photographs in this post!

References:

Eberhard, W. G. (1980). The natural history and behavior of the bolas spider Mastophora dizzydeani sp. n. (Araneidae). Psyche: A Journal of Entomology87(3-4), 143-169. http://dx.doi.org/10.1155/1980/81062

Haynes, K. F., Yeargan, K. V., & Gemeno, C. (2001). Detection of prey by a spider that aggressively mimics pheromone blends. Journal of insect behavior,14(4), 535-544. http://link.springer.com/article/10.1023/A:1011128223782

Haynes, K. F., Gemeno, C., Yeargan, K. V., Millar, J. G., & Johnson, K. M. (2002). Aggressive chemical mimicry of moth pheromones by a bolas spider: how does this specialist predator attract more than one species of prey? Chemoecology, 12(2), 99-105. http://link.springer.com/article/10.1007%2Fs00049-002-8332-2?LI=true

Yeargan, K. V. (1988). Ecology of a bolas spider, Mastophora hutchinsoni: phenology, hunting tactics, and evidence for aggressive chemical mimicry. Oecologia, 74(4), 524-530. http://www.jstor.org/stable/4218505

Yeargan, K. V. (1994). Biology of bolas spiders. Annual review of entomology39 (1), 81-99. DOI: 10.1146/annurev.en.39.010194.000501 

Yeargan, K. V., & Quate, L. W. (1996). Juvenile bolas spiders attract psychodid flies. Oecologia, 106(2), 266-271. http://link.springer.com/article/10.1007/BF00328607

Yeargan, K. V., & Quate, L. W. (1997). Adult male bolas spiders retain juvenile hunting tactics. Oecologia, 112(4), 572-576. http://link.springer.com/article/10.1007/s004420050347

 

 

A comb-tailed spider

Last weekend, I joined a group of fellow arachnophiles for a day at Burns Bog. We did not achieve our goal of finding the rare ground spider Gnaphosa snohomish (a bog specialist), but instead we met a very common spider that is nonetheless not well known: a comb-tailed spider in the family Hahniidae.

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Neoantistea magna, a common yet mysterious forest-dweller (photo Sean McCann).

A distinguishing feature of spiders in the subfamily Haniinae is the arrangement of the spinnerets in a single row like the teeth of a comb – thus the common name.

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The arrangement of the spinnerets of ‘comb-tailed’ spiders in the subfamily Hahniinae.         (Photo by Tom Murray, licensed under CC BY-ND-NC 1.0)

I generally think of spiders as being one of two basic types: wanderers or web builders. The wanderers include visually hunting ground dwellers like wolf spiders, whereas web building spiders are sit-and-wait predators that rarely leave their silken snares. This is overly simplistic, of course, but asking “web or not?” is often a useful first step in  classifying spiders. The genus Neoantistea, however, gave me a first encounter with members of an intermediate group known as vagrant web builders.

The sheet webs of Neoantistea spiders are tiny – typically less than 5 cm across. They are built in moss or across shallow depressions such as those formed by the tracks left by animals walking on soft ground. The diminutive spiders (their total body length is less than 5 mm) live under their webs, retreating into crevices in the litter or moss when disturbed.

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Small sheet-web of Neoantistea magna (photo Sean McCann).

What makes these spiders unusual for web builders is that although the web can be a useful aid for catching prey, it is not necessary. Neoantistea magna have reasonably large eyes and can recognize and hunt prey just as easily off of their webs as on them (Engers & Bultman 2006).

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A portrait of a male Neoantistea magna, showing the arrangement of the relatively large eyes (photo Sean McCann).

Although it was easy to identify the spiders we found to genus – the distinctive spinnerets leave no doubt as to the family, and of the North American members of the Hahniinae, Neoantistea is the only genus of web builders – determining the species was another matter entirely. Usually spider identification relies on close examination of the genitalia.

To ID this handsome fellow, two of the key features were the tibial apophysis and the patellar spur, tiny protrusions of the pedipalps which are very difficult to see without a microscope (here’s a diagram of the segments of the pedipalps).

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The key to identifying spiders often lies in the features of their elaborate genitalia. Here the large curved outgrowth on the tibia and the hooked spur on the patella of the pedipalp are circled (photo Sean McCann).

Speaking of genitalia, although very little is known about the biology of Neoantistea magna, there is one report of mating behaviour (Gardner & Bultman 2006). During copulation, the male clasps the female with his first two pairs of legs. The robust femur and tibia (see leg segment diagram) on each of these legs are studded with a double row of tubercles, giving them a serrated look. 

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Male N. magna. Note the burly front legs, presumably modified for grasping the female (photo Sean McCann).

Although the female may attempt to disengage from her partner, he is able to maintain a firm hold with his rather spectacularly modified legs and continue copulation.

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Female N. magna, with slender front legs (photo Sean McCann).

Fun with etymology:                                                                                                             The genus name Neoantistea means “new Antistea”. Antistea comes from the Latin word antistes, which means “one who stands in front of a temple, overseer, high priest”. Why were these tiny spiders given such a grandiose name? It’s a mystery.

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References

Engers, W., & Bultman, T. (2006). Foraging Habits of Neoantistea magna (Araneae: Hahniidae).

Gardner, D., & Bultman, T. (2006). Natural History and Reproductive Biology of a Hahniid Spider in Southwestern Michigan.

Opell, B. D., & Beatty, J. A. (1976). Nearctic Hahniidae (Arachnida: Araneae)Bull Mus Comp Zool Harvard Univ.

Tetragnatha revisited: dinner and romance at sunset

This post features photographs by Sean McCann. For more beautiful photography and natural history of arthropods and other wildlife, check out his blog, Ibycter.com

As a sequel to our recent encounter with some long jawed orb-weavers in the genus Tetragnatha (the tiny and cryptic Tetragnatha caudata), this week on an evening walk at Iona Beach, Sean and I observed some neat predation and mating behaviour in another species, most likely Tetragnatha laboriosa.

We made our first observation just as the sun was beginning to set, the beginning of the most active hunting hours for Tetragnatha laboriosa. This female had just captured her first meal of the evening, a bug in the family Miridae.IMG_1953

After biting it, she began wrapping it with silk, which she pulled out of her spinnerets with her last pair of legs (you can see her caught in the act below). IMG_1956

After wrapping the bug lightly with silk, she carried it back to the hub of her orb web and settled down to dine.IMG_1962

Unfortunately for the spider, dinner was interrupted by Sean’s efforts to get a good photograph. The disturbance prompted her to drop her meal and retreat to the vegetation at the edge of her web. Isn’t she just gorgeous?!
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After a minute or so, she went back for her abandoned prey.
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She then carried it off the web to resume her meal in peace. You can see from this image how the lovely coloration of these spiders allows them to blend in with plant stems when they adopt their cryptic stick-like posture.
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Later, when the sun had all but set and we were just about to head home, Sean spotted a pair of spiders (probably the same species, T. laboriosa) mating in a female’s web.
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Mating involves a fair bit of contortion for long jawed orb-weavers. Below you can see the male’s extremely long pedipalp (one of a pair of appendages modified for transferring sperm) engaged with the female’s epigyne (genital opening). The male’s short third pair of legs is used to position his partner’s abdomen. Throughout copulation he maintains a firm grip on the female’s jaws with his own.  IMG_2106

Here is a closer look at the mating position, where if you look closely you can see one of the female’s fangs interlocking with the special tooth on the male’s corresponding chelicera.jaws_clasping

Here is a drawing by B. J. Kaston of what the cheliceral embrace looks like close-up. The male, with larger jaws, is below, and the female above.

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Fig. 876 from Kaston 1948. Interlocking jaws of Tetragnatha pallescens (which looks very similar to T. laboriosa) during mating.

The female’s fangs get locked in underneath the special large tooth that protrudes from each of the male’s chelicerae.  tooth_landscape

As if we hadn’t had enough excitement already with the chance to closely witness such an intimate encounter, moments later we spotted two additional males waiting in the periphery of the female’s web. We were in for quite a show!

Here is one of the males that was waiting in the wings, posing elegantly and displaying his long jaws and even longer pedipalps. We’ll call him bachelor #2. IMG_2120

Not long after we spotted them, one of the lurking males made his move, lunging at the mating pair with his jaws held wide.  IMG_2108

A bit of a tussle ensued, after which the mating spiders disengaged. The attacking male pursued the mated male off the web and all the way to the substrate below. The female, apparently rather perturbed by this rude interruption, also left the web. One of the two rival males, apparently dominant, soon ascended back toward the web via his dragline. IMG_2112

Just as the winner of the first brief battle returned to the web, the third male entered the ring, and a second chase ensued. This cycle repeated a couple of times, until at last only one male returned victorious to the periphery of the web.IMG_2129

Bachelor # 2 (or was it #3?) settled down to wait at the edge of the web, while the female made her way back to the hub.     IMG_2140

It turns out that female T. laboriosa only mate once as a rule, and if copulation is interrupted as we observed, it’s a toss-up whether or not she will be willing to pick up where she left off (LeSar & Unzicker 1978). We couldn’t stay to see if our champion was able to successfully mate, but we wished him the best of luck!IMG_2138

Phidippus and Salticus

Two spiders, both alike in family,

Phidippus johnsoni, the red-backed jumping spider. (Photo: Sean McCann)

Salticus scenicus, the zebra jumper. (Photo: Sean McCann)

In fair Victoria, where we lay our scene,

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Uplands park, Victoria, BC, is among the many homes of these common jumping spiders (family Salticidae). (Photo: Colin McCann)

From ancient grudge break to new animosity,

Where spider blood makes spider fangs unclean.

Notes
Jumping spiders (like all spiders) are generally predators of insects and other arthropods. Spiders are the second most common prey items of Phidippus johnsoni (27% of their diet, just after dipterans, coming in at 30% of the total count), and comprise 5% of the diet of Salticus scenicus.

References:
Jackson, R. R. 1977. Prey of the jumping spider Phidippus johnsoni (Araneae: Salticidae). J. Arachnol. 5 :145-149.
Okuyama, T. 2007. Prey of two species of jumping spiders in the field. Appl. Entomol. Zool. 42 (4): 663–668.

The zebra jumper’s stripes may serve as camouflage in many settings, but in this case they were no match for the excellent visual hunting abilities of a fellow salticid. (Photo: Sean McCann)

 

What happens when you poke, prod and pinch black widow spiders? You might be surprised…

This post originally appeared on Chris Buddle’s blog Expiscor at Scilogs.com.

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A stunning female western black widow (Photo: S. McCann)

People seem to have a particular fear mixed with fascination when it comes to venomous animals, and whenever I talk about my work with black widows I am invariably asked questions like, “have you been bitten yet?” The answer is, of course, no. Spiders almost never bite people. I’m always quick to relate that in my experience black widows are not aggressive, even when I go around poking and prodding them with my bare hands.

Replicated experimental results always carry more weight than anecdotes, however, so I am delighted to share this recent paper: Poke but dont pinch: risk assessment and venom metering in the western black widow spider, Latrodectus hesperus.

Hey look!! An actual peer-reviewed research paper about the poking, prodding, and pinching of black widows, confirming that they are reluctant to bite, even when threatened. Not only that, but the study provides some cool data suggesting that these spiders are capable of assessing risks to make decisions about how to defend themselves.

Here are the details:

David Nelson and his coauthors wanted to know if black widows change their defensive behaviour depending on the level of threat they are faced with. To find out, they used gelatin ‘fingers’ to place spiders in three different threatening situations: a ‘low threat’ attack was a single poke with one finger, a ‘medium threat’ was a series of prods simulating a more persistent attacker, and the ‘high threat’ was three a series of long pinches of the spider’s entire body between two fingers, as might be experienced if being grasped by a predator.

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Figure 1 from Nelson et al. 2014

They found that the spiders engaged in several distinct defensive behaviours during these experimental attacks: retracting the legs toward the body, moving (often retreating), ‘silk-flicking’ (drawing sticky silk out of the spinnerets with last pair of legs and flinging it toward the attacking finger), ‘playing dead’ (curling up into a ball), and biting.

During low-threat, single pokes, no bites occurred. Most spiders were completely non-confrontational, simply moving away, and only rarely flicking silk.  When the threat level escalated to persistent prodding, the spiders changed their defensive behaviour: roughly half of them flicked silk, some played dead, and only one spider (out of 43) attempted to bite the offending finger. Silk-flicking is much safer than biting for a black widow – she can maintain her distance while flinging sticky silk to subdue or slow down her attacker. Biting, on the other hand, requires getting up close and personal with the assailant in order to pierce it with her tiny fangs, making her much more vulnerable to injury.

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See the red tips of this black widow’s puny fangs? It’s a lot safer for her to keep her distance in threatening situations than get close enough to use them (Photo: S. McCann)

Only when the spiders were being pinched between two fingers (with the mouthparts already positioned right up against their ‘attackers’) did biting start to become a more common, last-resort tactic: 60% of the spiders bit the fingers as a result of being squeezed for an extended period of time, delivering on average 2.7 bites each. Pinching also resulted in silk-flicking by about half of the spiders, and a few played dead.

This is all great information, but when the spiders did bite the gelatin fingers, there was no way of knowing how much venom they injected, if any at all (sometimes venomous animals deliver ‘dry’ bites). The next question the researchers wanted to answer was, do the spiders control whether and how much venom they inject when biting? In particular, they wanted to know if the amount of venom injected would vary depending on the type of threat (in this case either pinching a leg with forceps, or grasping the abdomen with gloved fingers).

For this experiment they came up with a clever method to collect the venom: a small vial with a thin membrane over the opening was presented as a target for the spiders to bite. If a spider did bite, her fangs would pierce the membrane (the number of holes would indicate how many times) and any venom she expelled would be collected in the vial so the volume could subsequently be measured.

It turned out that more than half of all bites were dry (no venom was detected in the vials). The black widows delivered more bites per target when they were pinched on a leg than on the abdomen, but more venom was released with each bite when the abdomen was pinched. Being grasped by the body is a high-risk situation for a black widow because her abdomen is unarmored and vulnerable; a strong squeeze or puncture can be deadly. Pinching a single leg, on the other hand, represents a non-life threatening attack. Spiders can autotomize (drop) their limbs and survive without significant ill effects.

The team also found evidence that the spiders delivered more venom per bite when repeated threats were spaced 5 minutes apart than 5 seconds apart. Attacks after the longer intervals might have been interpreted as coming from new assailants, each requiring a larger dose of venom than a second or third bite to the same persistent attacker.

The results all indicate that black widows have fine control over how much venom they inject when biting. First, they can decide whether or not to use venom at all. Some spiders gave dry bites, then wet bites, as well as vice versa, demonstrating that dry bites were not simply a result of running out of venom. Furthermore, they can vary the amount of venom they inject during individual bites and in response to different kinds of threats.

Both silk and venom are metabolically expensive to manufacture, so it makes sense that spiders would be selective about when and how much of these resources to deploy in defense. This study suggests that they are able to assess risks and adjust their responses accordingly, only dipping into their reserves of silk and venom as the threat level escalates towards a life-or-death situation.

What does this all mean for humans? Grabbing and pinching spiders is generally not a good idea – they might get injured and could bite defensively. This is just good sense and didn’t require a scientific study to confirm, but the new data suggest that even if a black widow does bite, she’s not necessarily going to inject any venom. It’s also important to note that in the experiments where bites did occur, the spiders always had a ‘finger’ or target placed in direct contact with their mouthparts.

An unaggressive female black widow takes a stroll across my hand. Although I never grab spiders to pick them up, coaxing them onto my hands and letting them wander around on their own steam has never been a problem. (Photo: S. McCann)

The most exciting thing this study tells us is that spiders can make decisions about how to respond to threats (which sometimes include humans) – further evidence of their incredible sophistication. Perhaps more importantly for the arachnophobic, it suggests that black widows would much rather conserve their valuable venom for use in dispatching their next meal than waste it on a human who is of no interest as prey!

Spiders in general are amazing creatures worthy of our admiration and respect. I hope that this new information about black widows might convince some that there is more about them to be fascinated by than to fear!

References and related reading:

Nelsen, D. R., Kelln, W., & Hayes, W. K. (2014). Poke but don’t pinch: risk assessment and venom metering in the western black widow spider, Latrodectus hesperusAnimal Behaviour89, 107-114. http://dx.doi.org/10.1016/j.anbehav.2013.12.019

Vetter, R. S. (1980). Defensive behavior of the black widow spider Latrodectus hesperus (Araneae: Theridiidae). Behavioral Ecology and Sociobiology7(3), 187-193. doi:10.1007/BF00299363

W. Cranshaw (2014). Western widow fact sheet: http://www.ext.colostate.edu/pubs/insect/05605.html

Dinner or date?

A comparison of the vibrations transmitted by courting males and ensnared prey in two web-building spider species.

Today, I am excited to publish my first blog post about some of my own spider research! Our paper, “A meal or a male: the ‘whispers’ of black widow males do not trigger a predatory response in females”, has just been published in Frontiers in Zoology (freely available online).

This study is part of the PhD work of my friend and collaborator Samantha Vibert. In fact, we did some of the data collection and analysis for this paper during my very first semester in our lab, when I was working as an undergraduate research assistant. That was when I first began to really look closely at spiders and their incredible behaviour. My experience working with Sam that summer sparked my passion for the complexity and beauty of all of the various aspects of the private lives of spiders, which so often go unnoticed by humans.

Here is a plain-language summary of the paper, written with Samantha Vibert, and with photos by Sean McCann:

Spiders are fascinating but largely overlooked creatures, with sophisticated signalling systems involving chemical, vibratory, tactile, and in some species visual communication. A spider’s web is essentially an extension of her exquisitely tuned sensory system, allowing her to quickly detect and respond to vibrations produced by entangled prey. Not only is the web a highly effective prey-capture device, but it is also the dance floor on which prospective mates must demonstrate their desirability. The first moments after a male spider steps onto a female’s web may present a great risk, since spiders are often cannibalistic. We were interested in how a dancing male spider avoids a potentially deadly case of mistaken identity. One way that he might deal with this challenge is by transmitting vibratory signals that are very different from the vibrations produced by ensnared prey.

webs are good for this

Spider webs are highly effective prey-capture devices, so how does a courting male avoid the fate of flies like this one?

Our study species were the western black widow and the hobo spider, which are both found in British Columbia.

widow web

A western black widow (Latrodectus hesperus) hanging from her tangle-web under a log at Island View Beach on Vancouver Island.

Black widows are in the family Theridiidae, and build complex, three-dimensional tangle-webs, while hobo spiders (family Agelenidae) build dense sheet-webs. Female black widows are much larger than males, while hobo spider males and females are closer in size.

Hobo web

A hobo spider (Tegenaria agrestis) female on her sheet web at Iona Beach, in Richmond, BC.

The purpose of our study was to describe some of the vibratory courtship signals of males in these two species, and to determine which aspects of these vibrations might allow females to discriminate between prospective mates and their next meals.

First, we recorded the vibrations transmitted through the web by courting males in both species using a laser Doppler vibrometer. At the same time, we video-recorded the male’s courtship behaviour. This allowed us to describe and analyze the different kinds of vibrations that were transmitted through the web during specific behavioural elements of each male’s courtship display. We then recorded the vibrations produced by the struggles of two types of common prey insects (house flies and crickets), on both black widow and hobo spider webs.

We found that male and prey vibrations differed more in the black widow than in the hobo spider. Hobo spider male vibrations contrasted with prey vibrations only in terms of their duration – the courting male moves around almost continuously on the female’s sheet web, while prey struggles are generally brief and intermittent. Black widow male courtship vibrations were also longer than prey vibrations on tangle webs (for the same reason), but they were also distinctive based on their generally lower amplitude and higher dominant frequencies.

To our surprise, we also found that most courtship behaviours in both species did not generate the kind of very stereotyped, complex and distinctive “songs” that have been reported in several other spider species. These species tend to court on substrates like leaf litter and plants, which most likely transmit vibrations quite differently than webs. Some male orb-weavers also produce highly rhythmic patterns during their vibratory courtship displays. So our finding leads us to wonder to what extent web architecture and complexity might constrain the transmission of the male courtship signals, and therefore the design of these signals.

One very interesting exception to the rule turned out to be the vibrations generated by the male black widow’s abdomen tremulations (an up-and down waggle of the abdomen, performed as the male hangs upside down from the female’s web). These vibrations were always very distinct from anything produced by prey: they were long-lasting and of very low amplitude, like a constant humming.

Here’s a short video of a male western black widow vibrating his abdomen on a female’s web (Supplemental File 1 from Vibert et. al 2014):

To learn more about these particularly stereotyped, ‘whisper-like’ male signals, we built our own custom web vibrator by modifying a loudspeaker. We were then able to play recorded vibrations of a male’s abdomen tremulation or a fly’s struggles back to females and observe their responses. Black widow females were much less likely to respond aggressively to vibrations played back at the “whisper-like” low amplitude of male abdomen tremulation, but attacked when we turned up the volume to levels typical of prey vibrations. This was the case regardless of which type of vibration we played. So we speculate that the males vibrate their abdomens either to avoid triggering a female’s predatory response, or even to turn it off.

Is it possible that the females that didn’t attack low-amplitude vibrations simply couldn’t detect them? We don’t think so. First, spiders are specialists when it comes to detecting even faint vibrations, and second, some females actually responded with courtship behaviour: abdomen ‘twitches’ which are similar to the male’s abdominal movements, but more emphatic. These abdomen twitches undoubtedly transmit their own vibrations through the web, and it would be very exciting to further investigate the female’s side of the vibratory ‘conversation’ during courtship.

Abdomen vibration seems to be a relatively common type of courtship behaviour and has been described in several spider families (‘abdomen wagging’ in an orb-weaver, and what has recently been described as ‘twerking’ in jumping spiders are a couple of examples). If indeed the “whispers” caused by these vibrations are involved in lowering female aggression, this might explain why such behaviour is fairly common among spiders.

The orb-weaver Argiope keyserlingi’s courthip also involves abdomen vibration, but in this species another vibratory signal was recently implicated in reducing the risk of cannibalism. The ‘shuddering’ of a courting male delays the female’s predatory response. One of the common features of black widow abdomen tremulation and these ‘shudders’ is that they are the first courtship behaviour performed by males after they enter a female’s web.

widow pair

A male western black widow courting a large, potentially dangerous female. Abdomen vibration is performed on and off throughout the male’s courtship display, starting just after the male steps onto the web, and featuring prominently during attempts to approach and mount the female.

Very little is known about the kinds of vibratory courtship signals that male web-building spiders transmit to females through their webs, except for in orb-web weaving species. We hope that this new information about vibratory communication in tangle-web and sheet-web building spiders will contribute to better overall understanding of the function and evolution of web-borne vibratory courtship signals.

References:

Vibert, S., Scott, C., and Gries, G. (2014). A meal or a male: the ‘whispers’ of black widow males do not trigger a predatory response in females. Frontiers in Zoology, 11(4).  doi:10.1186/1742-9994-11-4

Wignall, A. E., & Herberstein, M. E. (2013). The Influence of Vibratory Courtship on Female Mating Behaviour in Orb-Web Spiders (Argiope keyserlingi, Karsch 1878). PloS one8(1), e53057. doi:10.1371/journal.pone.0053057

Wignall, A. E., & Herberstein, M. E. (2013). Male courtship vibrations delay predatory behaviour in female spiders. Scientific reports3doi:10.1038/srep03557