They mostly come at night… mostly.

Posted on March 12, 2023 by cataranea

This post is not about aliens, but it is about the night-time marauding behaviour of fierce, many-limbed* predators: candy-striped spiders!

I am very excited to share this new paper that was a collaboration with my partner in life and science, Sean McCann! It’s the shortest paper I’ve ever written, and also my favourite scientific contribution so far. Written in a style that I hope is engaging and accessible, it documents some of the fascinating natural history of candy-striped spiders in North America. It is very short, so I encourage you to go read it in its entirety! Here I will present some back story and behind-the-scenes photos of what went into this study about the foraging behaviour of these intrepid spiders.

It all started with Sean’s penchant for getting up before dawn to take pictures of sleeping insects like these cuckoo leaf-cutter bees:

A pair of sleeping *Coelioxys* against the sunrise.

While we were doing fieldwork as part of my PhD research on black widow spiders on the lands of the Tsawout First Nation on the Pacific Coast, we had a mostly nocturnal lifestyle, but occasionally we would head out to our coastal dune field site early in the morning for some recreational spider and insect observations and photography. While searching for sleeping insects for Sean to shoot, we started to notice that wasps and bees would often be perched on dead vegetation in large aggregations like the one below.

A group of sand wasps (*Ammophila* sp.) sleeping together on a communal perch. Photo: Sean McCann.

Sometimes multiple species of wasps and bees would be sleeping together on the same dead plant. The stems used for perches were typically isolated from other vegetation, and we started to wonder about the sleeping habits of these insects. Does perching together in large groups reduce the risk of being taken by predators? Do the same bees and wasps come back to sleep together at the same perch night after night?

Cuckoo leaf-cutter bees (*Coelioxys*), sand wasps (*Ammophila*) and a lone thread-waisted wasp (*Prionyx*) all perched together before dawn.

We decided we would do a little project to try to find some answers. We located a few communal perches within our widow spider study area that we could visit each night during our regular surveys. Then we painted all the insects sleeping on the same perch with a dot of the same colour of paint, so we would recognize them if they returned.

Then over the next few nights, we returned to the perches to count the number of painted insects and new arrivals.

Soon, our ideas about safety in numbers were put to the test. We started to find our bees and wasps being picked off by spiders! In one case (shown below) a single sleeper of a group of 5 was captured and killed by a spider in the night.

A candy-striped spider feeding on an unlucky sand wasp while its perch mates sleep on, apparently blissfully unaware of the horror below.

In other cases however, we came upon perches whose whole cohort of sleepers had been massacred by a single spider! Now our curiosity turned to the behaviour of the spiders, who we suspected were able to subdue these large, otherwise well-defended (with venomous stings) prey by sneaking up on them while they were sleeping and too cold to defend themselves.

A death scene at dawn: the results of nocturnal marauding by a candy-striped spider (*Enoplognata* sp.). Photo: Sean McCann (Figure 1 from Scott & McCann 2023)

We now wanted to know who these spiders were, and what was known about their predation behaviour. The details are all in the paper, but the short version follows.

Candy-striped spiders (*Enoplognatha ovata* and *E. latimana*) come in three colour forms.

Candy-striped spiders are introduced to North America from Europe, and they can be extremely abundant in many habitats. They come in three colour varieties, and while the genetics of this polymorphism has been worked out, not much attention has been paid to their behaviour. Most of what we know about their predation is based on the observations of William Bristowe, an English naturalist who studied about these spiders almost 100 years ago. He described the following foraging tactics:

Web-based ambush. Like other members of the family Theridiidae, candy-striped spiders build messy tangle webs, often under flowers. When day-flying insects land on the flowers to feed on nectar and make contact with her silk threads, the lurking spider will rush out to wrap the prey with strong, sticky silk.

A candy-striped spider with a sparse tangle-web under yarrow has captured a wasp that landed on the flowers to feed on their nectar.

Web invasion for kleptoparasitism (stealing prey) and araneophagy (spider-eating). Sometimes, candy-striped spiders connect their webs to those of neighbouring spiders to eavesdrop on the vibrations produced by prey insects. At our field site, they would often have lines connecting their webs to those of black widows, and creep onto the web to try to steal prey from their much larger relatives (black widows are in the same family of tangle-web weavers: Theridiidae). They also sometimes eat the spiders themselves!

A very bold candy-striped spider whose web connects with that of her neighbour, a black widow, attempts to prey on both the web owner while she is in the process of wrapping a large spider (a male foldingdoor spider, *Antrodiaetus pacificus*) recently caught in her web. This attempt was ultimately unsuccessful.

Here a candy-striped spider preys on black widow spiderlings before they have a chance to disperse from their mother’s web.

More recently, candy-stiped spiders have been reported actively foraging without the aid of a capture web. A very cool study found that the spiders eavesdrop on the vibrations produced by sexually signalling leafhoppers and use these to locate these insects as they move around in grasses and shrubs.

A candy-striped spider with a pair of froghoppers taken without a web. Perhaps she located these individuals based on listening in on their vibratory duet as she prowled around on the leaves.

Launching sneak-attacks on sleeping insects, however, appears not to have been previously reported. You can find a whole gallery of images and videos of the behaviours we observed here, including some attacks on sleeping bees and wasps that we just happened to witness, and some that we set up.

Here’s an action shot of a candy-striped spider in the process of trapping a pair of still-sleepy sand wasps.

There’s much more in the paper about the diet of these spiders, and the details of how we studied them, and I hope you’ll go check it out! As for conclusions, this research resulted in a lot more questions than answers. What prompts the decision by these spiders to leave their webs and go marauding? (Presumably it is risky to leave the protection of the tangle web.) Do they all do it, or is this a new or learned behaviour in an environment where sleeping insects are particularly abundant? Do the spiders just search randomly for sleeping prey, or are they able to detect them from a distance (perhaps using chemical cues)? And what is the impact of all this predation on insect communities, particularly in threatened ecosystems like the sand dunes where we worked? These spiders take a lot of pollinators, but they also take all kinds of other bugs—are they impacting pollinator populations, helping to control insect pests in agricultural ecosystems, or both? The list goes on, and we have years of work ahead of us to find out!

Candy-striped spider wrapping a *Coelioxys.*

Speaking of which, if you’re in North America, YOU can help us with our ongoing work on candy-striped spiders! Please keep your eye out for these spiders, wherever you are, and contribute observations to our iNaturalist project. More information about this participatory research here.

*As far as I can tell, the “queen” alien from the movie has 6 limbs, but apparently James Cameron drew some inspiration from black widows in coming up with her morphology!

The global spread of misinformation on spiders

Posted on August 23, 2022 by cataranea

This post is a summary of a recently-published paper (and related open-access dataset) that was a very fun collaboration led by Stefano Mammola, Angela Chuang, Jagoba Malumbres-Olarte and 61 other arachnologist colleagues* from around the world.

Illustration of a person holding a medaphone and a newspaper with the headline "panic!!" He is standing on top of a map of the world, and a woman with an afro, wearing a white lab coat, and holding a spider biology textbook is correcting a misleading image on the newspaper with a red pen. White figures around the works are reading the news. — Summary illustration of the paper by coauthor Jagoba Malumbres-Olarte.

This study was largely motivated by our collective frustration at the often inaccurate and sensational way that spiders are portrayed in the media. But just how bad is the quality of reporting on spiders, and why is it so pervasive?

To answer these questions and understand how misinformation about spiders flows at the global scale, we amassed a team of experts from all over the world to analyze 10 years of online news stories about human-spider encounters. We first searched Google News (using variations on the search term “spider AND bite”) to find more than 5000 news articles from 81 countries published in 40 languages. We then read each paper to collect data including the date and location of each reported event, whether the story described a human-spider encounter (but not a biting event) or a “bite” or “deadly bite” (spoiler: articles rarely included evidence of an actual spider bite), and checked each news item for errors (e.g., misidentified spiders in photos, incorrect information about spider biology or venom) and sensationalism (somewhat subjective**, but often based on the inclusion of words like “horror”, “terrifying”, and “deadly” ). We also recorded whether the article quoted an expert, and whether they were a medical professional, a spider expert (usually an arachnologist or entomologist), or “other” (e.g., a pest management professional). All of this data, detailed methods, and a summary of what we found broken down by continent is freely available online here.

A large spider clings to a tree above floodwaters. Caption: The massive spider rescued from the Queensland flood seemed too horrifying to be real. Additional text below photo reads: news.com.au. It really does sound like something from a horror movie: a giant spider larger than a man's hand, which makes loud hissing sounds and has powerful long venomous fangs. — An example of sensationalist reporting on a human-spider encounter in Australia.

Overall, the quality of the reporting was poor: 47% of all articles contained one or more errors and 43% were sensationalist. Stories with photos of spiders or alleged bites were more likely to be sensationalized, as were stories that contained errors. Whereas quotes from medical or other experts were unrelated to sensationalism, stories that contained quotes from spider experts were much LESS likely to be sensationalized.

Drivers of sensationalism in media articles about spiders. Odds ratios to the left (right) of the dotted line indicate a decrease (increase) in the likelihood of sensationalism. Figure from Mammola et al. 2022.

One of our plans for the future is to create a global database of arachnological experts to make it easier for journalists to identify and contact arachnologists in their region who are willing to be interviewed and provide factual information about spiders. We are also already working on a paper outlining guidelines for journalists covering spider news stories, which we hope will help to prevent some of the most common errors we saw and improve the overall quality of reporting.

We next conducted an analysis to describe the flow of spider news stories around the world and to get at what may be driving the spread of (mis)information about spiders online. Unsurprisingly, countries with shared languages and with higher proportions of internet users were more likely to be connected in the global network. The number of medically important spider species present (i.e., those capable of harming and potentially killing humans) also increased the connectedness of individual countries within the network. Most notably, we identified sensationalism as a key factor underlying the spread of (mis)information.

Global distribution of news articles about on human-spider encounters showing links between countries (pies; n = 79) with each spider-related event reported by the press (dots, n = 2,644). The size of each pie chart represents the number of news articles published in the country between 2010 and 2020. Figure from Mammola et al. 2022

This study provides insight into what drives the global flow of information about spiders in particular, but can also teach us some more general lessons. Our results make us optimistic because they suggest a way to improve reporting on spiders, and in turn, to shift the quality and spread of online information more broadly. News stories are less sensationalized when they consult appropriate experts, and reducing sensationalism can help decrease spread of misinformation. We found that even local-scale events published by regional news outlets can quickly become broadcast internationally, which means improving news quality at the local scale can have positive effects that travel through the global network.

*Full author list: Stefano Mammola, Jagoba Malumbres-Olarte, Ingi Agnarsson, Valeria Arabesky, Diego Alejandro Barrales-Alcalá, Aimee Lynn Barrion-Dupo, Marco Antonio Benamú, Tharina Bird, Maria Bogolomova, Pedro Cardoso, Maria Chatzaki, Ren-Chung Cheng, Tien-Ai Chu, Naufal Urfi Dhiya’ulhaq, André-Philippe Drapeau Picard, Hisham K. El-Hennawy, Mert Elverici, Caroline S. Fukushima, Zeana Ganem, Efrat Gavish-Regev, Naledi Gonnye, Axel Hacala, Charles Haddad, Thomas Hesselberg, Tammy Ai Tian Ho, Thanakorn Into, Marco Isaia, Dharmaraj Jayaraman, Nanguei Karuaera, Rajashree Khalap, Kiran Khalap, Dongyoung Kim, Tuuli Korhonen, Simona Kralj-Fišer, Heidi Land, Shou-Wang Li, Sarah Loboda, Elizabeth Lowe, Yael Lubin, Marija Miličić, Alejandro Martínez, Zingisile Mbo, Grace Mwende Kioko, Veronica Nanni, Daniel Nwankwo, Yusoff Norma-Rashid, Christina Painting, Aleck Pang, Paolo Pantini, Martina Pavlek, Richard Pearce, Booppa Petcharad, Julien Pétillon, Onjaherizo Christian Raberahona, Joni A. Saarinen, Laura Segura-Hernández, Lenka Sentenská, Gabriele Uhl, Leilani Walker, Charles M. Warui, Konrad Wiśniewski, Alireza Zamani, Angela Chuang, Catherine Scott.

**For the news in English, Spanish, French, and Italian we checked to see how closely scores aligned for different collaborators assessing the same article, and we were pretty consistent.

Risky business: brown widow males choose cannibalistic adults over safer subadult females

Posted on April 26, 2022 by cataranea

I am very happy to share the publication of a new paper reporting research led by my fantastic colleague Lenka Sentenska and coauthored by Pierick Mouginot and Maydianne Andrade, in the journal Behavioral Ecology.

Brown widow spiders (Latrodectus geometricus), like their relatives the Australian redbacks (L. hasselti), are sexually cannibalistic. This is not the situation most people imagine when they hear “black widow,” however, in which the female devours the male after mating. In redbacks and brown widows, sexual cannibalism is better thought of as male self-sacrifice. The diminutive male somersaults during copulation and puts his abdomen in front of the female’s mouthparts, literally offering himself to her and continuing to transfer sperm as she begins to feed on him.

A copulating Australian redback spider pair. The much smaller male has somersaulted, presenting his abdomen to the female so that she can begin feeding on him. Photo: Sean McCann.

At first glance, this doesn’t seem like a particularly good outcome for the male. Although he is able to pass on his genetic material before his death (win!), he will be unable to mate with additional females and increase the total number of offspring he fathers. Recently, a group of colleagues discovered that male redbacks and brown widows can take a shortcut that allows them to survive mating. It turns out that just before their moult to maturity, immature females have fully developed reproductive organs ready to go under the cuticle that they are preparing to shed. This means that a male can bite through the cuticle and successfully copulate with a subadult female, and she will retain the sperm through her moult, and then go on to lay fertilized eggs once she is an adult.

This immature mating tactic has several major benefits for the male: he barely has to spend any time or energy courting the female (usually males court adult females for hours), males mating with subadults are more likely to copulate twice (thus depositing sperm in both of the female’s paired sperm storage organs), and subadult matings do not end in ritual cannibalism! On top of all that, females mated as subadults produce just as many offspring as those mated as adults. Given all this, you might expect that a male brown widow with a choice between an adult and a subadult female mating partner would choose the safer option: the subadult.

Previous studies (including this one by my colleague Dr. Sentenska) have tested this idea and found that when given a choice, brown widow males preferentially approach adults over subadults. This could just be because subadults are more difficult to detect from a distance; once they mature, adult female widow spiders produce a silk-bound sex pheromone that advertises their location and receptivity to males, and as far as we know, subadults do not produce such airborne signals. In this study, we wanted to see if males would make the same choices based on direct contact with silk (which may contain chemical information that allows males to discriminate between subadults and adults). We also wanted to find out what is driving the reduced courtship and copulatory cannibalism when males mate with subadult females—are courtship behaviours triggered by the sex pheromones on adult females’ webs, or do males adjust their behaviours depending on the kind of female they are attempting to mate, regardless of chemical cues on her web?

To answer these questions, we ran two experiments. First, we asked males if they preferred silk produced by adult or subadult female’s in a two-choice Y-maze. When the male entered the maze (via the common arm in the figure below) he would be walking on both kinds of silk, and then at the intersection of the Y he could choose to follow the adult or subadult silk trail. Once he got to the end of that arm, he could turn around and go investigate the other option, or continue searching on the first arm he chose. We found that initially, males were equally likely to choose each of the two arms of the Y-maze (not displaying a preference for either kind of silk), but that they spent more time on the adult silk. This reinforces the idea that males prefer adult females to subadult females based on silk-bound chemical cues (which spiders detect with hairs on their legs and mouthparts).

The y-maze setup for testing male brown widows’ responses to contact with dragline silk produced by adult or subadult females.

Next, we ran a web-swap experiment where we placed adult and subadult females on webs built by different individuals who were either the same stage or opposite stage, resulting in four combinations: subadults on subadult webs, subadults on adult webs, adults on subadult webs, and adults on adult webs. We then introduced a male onto each web and recorded his courtship behaviour, whether he successfully copulated, and whether he engaged in self-sacrifice behaviour (somersaulting and presenting his abdomen to the female).

This experiment revealed that the kind of web was the main driver of an important male courtship behaviour, silk laying (part of web reduction) and of the total time the male spent courting on the web at a distance from the female. The majority of males engaged in silk laying on adult webs, and almost no males engaged in this behaviour on subadult webs, regardless of whether the female on the web was an adult or a subadult. Males also approached females much more rapidly when they were courting on subadult webs, no matter the actual status of the female on the web. These results are consistent with the idea that males invest more time into courting adult females, and that energetically costly courtship behaviours like silk laying are triggered by the sex pheromone on silk produced by adult females.

The stage of the female herself, however, determined whether males successfully mounted and copulated with females, and how long it took them to progress from one stage of mating to the next. Males were much more likely to mount adult females than subadults, and were able to mount them more quickly. Similarly, males were more likely to copulate with adults than subadults, but the time they spent engaged in courtship on the female’s body prior to copulation was much longer for adult females. This is related to the result that males much more rarely engaged in mate-binding behaviour (wrapping the female’s body with silk) when courting subadult females compared to adult females. Intriguingly, we also found that males who bound females were more likely to successfully mount, particularly when the female was a subadult. This supports the idea that mate binding functions to increase female receptivity, perhaps via a pheromone on the male’s silk.

The tiny brown widow male in this photo has reduced much of the larger female’s web, leaving a thick rope of silk that she is hanging from. Here he is laying silk on her front legs, part of the “bridal veil” or mate-binding behaviour. Photo: Sean McCann.

Finally, we found that males nearly always somersaulted during copulation with adult females, but almost never offered themselves to subadults. This indicates that the lack of sexual cannibalism during subadult mating is a result of males choosing not to engage in self-sacrifice, rather than adult females being more cannibalistic than subadults, which suggests that perhaps we should change our thinking about subadult females being the “safer” option for males.

Here the male is withdrawing his coiled embolus (one of his paired sperm-transfer organs) from the female’s genitalia. The drop of fluid on his abdomen indicates that the female bit him after he somersaulted during the first copulation. He can now copulate a second time, and again offer himself to the female so that she can complete her meal. Photo: Sean McCann

Taken together, our results confirm that male brown widows prefer to approach and attempt to mate with adults than subadults, despite the apparent advantages of subadult mating. The shortened time to mating and the lack of cannibalism, however, may be better thought of as males investing less into mating with subadults than as benefits of this tactic. This makes sense when we consider that adult females seem to be more receptive to male mating attempts than subadults, and that they are ready to produce an egg sac shortly after copulation, whereas subadults must first moult to maturity. Moulting spiders are extremely vulnerable to predators, and all the advantages of mating with a subadult disappear if she dies before producing any offspring. We conclude that mating with adults, despite resulting in a male’s death, may actually be the safer option in terms of the return (offspring) on his investment into a given female.

References & related reading:

Sentenská, L., Neumann, A., Lubin, Y., & Uhl, G. (2021) Functional morphology of immature mating in a widow spider. Frontiers in Zoology 18: 1-18.

Sentenská, L., Uhl, G., & Lubin, Y. (2020) Alternative mating tactics in a cannibalistic widow spider: do males prefer the safer option?Animal Behaviour 160: 53-59.

Biaggio, M. D., Sandomirsky, I., Lubin, Y., Harari, A. R., & Andrade, M.C.B. (2016) Copulation with immature females increases male fitness in cannibalistic widow spiders. Biology Letters 12: 20160516.

The great black widow race: how males use the silk road to find females faster

Posted on July 31, 2019 by cataranea

I am very excited to share the publication of a new paper coauthored with Sean McCann and my supervisor Maydianne Andrade in the journal Proceedings of the Royal Society B. The full paper can be found here (please email me or contact me on twitter if you don’t have access and would like a pdf copy). Before I summarize the study below, I would like to first thank the Tsawout First Nation for allowing me and my collaborators to study black widows on their beautiful lands for the last several years. We also offer heartfelt thanks to the many generous contributors* to our #TeamBlackWidow crowdfunding campaign, without whom this research would not have possible. Finally, we are also very grateful to the Toronto Entomologists’ Association for funding part of the fieldwork with the Eberlie Grant, and to NSERC for funding our lab’s research and my PhD program.

Female (left) and male (right) western black widow spiders (Latrodectus hesperus). Photo: Sean McCann

For solitary animals that reproduce sexually, finding a partner is a critical first step in the sequence of events that lead to mating. We know a lot about the traits that help males win fights over females (like horns and other weapons), as well how female preferences can lead to the evolution of extravagant ornaments and displays like the tails of male peacocks (or peacock spiders). But these two mechanisms of sexual selection (male competition and female choice) can often only operate on males that actually find females to compete over. In a lot of animals, including many terrestrial arthropods like insects and spiders, a race to find females determines which males get the opportunity to pass on their genes. The kinds of traits that help males to win this race are less well understood than male ornaments and weapons, in part because it can be tricky to track mate searching males in nature.

Our field site on the sand dunes of southern Vancouver Island, British Columbia. At this site, driftwood logs provide shelters for western black widows. Photo: Sean McCann

In this study, my coauthors and I used experiments and observations of the natural movements made by black widow males to learn more about what gives them an edge when it comes to finding females. First, we spent about six months in the field tracking hundreds of male black widows in their natural habitat. We marked all of the females (who generally stay put on their capture webs, which makes them relatively easy to keep track of) and males (who actively search for females) that we encountered during the season. This allowed us to estimate how many males survive the trip to find females (only about 12%!) and how far they move when they do survive (in most cases, less than 60 metres, but sometimes more than 200, which is pretty impressive for spiders with a body length of less than 1 cm!). We were also able to determine that males outnumber receptive females by more than 10 to 1 during the height of the mating season, which means that competition over mates is fierce, making traits and tactics that confer an advantage to searching males all the more important.

We spent a lot of nights on the beach checking the webs of marked females, marking and recording any males who visited them. Photo: Sean McCann

Before we get to those tactics, however, let me back up for a minute and summarize some important features of black widow sexual communication and behaviour that are relevant to this story. First, female black widows produce a sex pheromone that functions as a chemical personal ad. This chemical message is released from the silk of a female’s web, and it provides males with information about her location and sexual receptivity. Before this study, we didn’t know the range of this message, just that it operates over some distance, allowing males to locate females who are ready to mate. Male black widows detect the female’s pheromone using sensory hairs on their legs. Once a male finds a female, he engages in a courtship dance that transmits vibrations through her web, providing her with information about his identity and quality as a mate. After several hours of dancing and laying down silk all over the web and the female’s body (this silk may contain chemical messages just like the female’s), and assuming he is not interrupted by a rival or eaten by the female (it happens, particularly if she’s hungry and therefore more interested in a meal than mating!), the male eventually mates with her. Spiders do this in a strange and unique way, transferring sperm with paired copulatory organs called pedipalps. The first male to mate can break off the tips of his copulatory organs inside the female, effectively blocking rival males from inseminating her, and thus ensuring his paternity.

A female (yellow 567, whose number corresponds to the location of the paint marks on her legs) consumes an unlucky male. Photo: Sean McCann.

Ok, now back to the research! The experimental part of our study involved setting up a series of actual races for male black widows—first longer-distance contests in the field, and then shorter sprints in the laboratory. For the great black widow races of 2016 and 2017, we set up a 60-metre course on the sand dunes at our field site. The finish line was made up of a series of mesh cages containing females and their silk.

The finish line of the 2016 great black widow race. Each cage contains a female black widow on her pheromone-emitting web. Photo: Sean McCann

Before the race, we weighed in each male on a tiny scale**, measured the length of his legs, and painted him with unique racing stripes so we would be able to track whether he completed the race and calculate his average speed. At sunset (black widows are nocturnal, so males search for females at night) we released groups of about 20 males at 10 metre intervals from the finish line, so that the closest group only had to travel 10 metres and the farthest group had to travel 60 metres. The course was set up so that males would be downwind of the line of pheromone-emitting females (assuming that the forecast was correct), and once all of the males were released, we waited at the finish line for them to start arriving outside of females’ cages.

A green-marked male crosses the finish line! Photo: Sean McCann

In 2016, when the wind was strong and came fairly consistently from the forecasted direction, males released at all distances up to 60 metres were equally likely to find females, which suggests that they are very sensitive to the smell of females. In 2017, however, when the wind ended up being weak and highly variable in direction, males released farther than 40 m from females were never able to locate them. Clearly, wind speed and direction will strongly affect the ability of a male to detect and find a female using only their sense of smell. But these experiments also revealed something surprising. In 2016, we found that the males that started out farthest from females achieved the fastest average speeds during searching—up to almost 1.5 metres (or more that 150 body lengths for spiders that are typically less than 1 cm long) per minute! And in 2017 we found that not only were males able to reach the finish line even after the wind shifted so much that smelling females on the racecourse was likely impossible, but also that the vast majority of males ended up outside of the cage of the single female who was in line with the direction of the wind during the first couple hours of the experiment.

A yellow-marked male makes his way down the race course. Photo: Sean McCann

Spending time watching what these spiders actually do when they search for females helped us make sense of these results. Male black widows have very poor vision, so they are guided toward females by their sense of smell. To get their bearings, they climb up vegetation, and wave first pair of legs (which you’ll recall are covered with sensory hairs), apparently ‘tasting’ the wind. After a while, they will climb back town to the ground and continue to move toward their target. Like all spiders, male black widows trail silk draglines behind them as they move through their environment. They anchor these safety lines to the vegetation periodically, such that they leave a silk path wherever they go. We noticed that when a searching male encounters one of these trails, he runs along it, using it like a silk highway. We realized that if males recognize the silk of rival males, they may use their trails to find females, even if wind conditions make it difficult to smell a female directly. And since these spiders are much more adept at walking on silk than on the ground, this might explain why the males in our experiments who traveled farthest also traveled fastest. The males released at 60 metres would have been most likely to encounter the silk trails left behind by all those who were released closer to the females.

A white-marked male has climbed up some grass and is extending his forelegs to taste the air for female pheromones. Photo: Sean McCann

To test this idea directly, we next ran a series of experiments that we called the X-races, the first of which was carried out by students in the behavioural ecology class Sean and I taught together at UTSC in 2017. The race course in this experiment is an X-shaped maze made out of string, with a female set up at one end with a fan behind her to blow her pheromone toward the male, who is released on one of the short arms of the X at the end opposite the female.

The X-race, an experimental setup for testing whether males follow or avoid the silk of rival males.

After being placed on the string, he moves upwind and when he reaches the centre of the X, he can choose to follow either arm—both lead to the female, and either way, he leaves a trail of silk behind him. Next, we introduce a second male to the end of the maze farthest from the female, but on the opposite arm from the first male. When this male gets to the intersection of the X, he now has a choice to follow or avoid the silk of the rival male. We used this experimental set up to confirm that males follow the silk of rivals when given the choice, and that they travel faster when they do. Using a modified version of the X-race, we also found that males only follow the silk of other black widows (and not that of closely related false widow males, who also occur at our field site), which means that the information on the silk is species-specific.

Sean (foreground) and our 4th year behavioural ecology students set up an X-race in the lab. The trays of water below prevent the spiders from leaving the maze if they drop down on a dragline.

When we put all this together, it tells us that male black widows use the somewhat surprising tactic of following their rivals to find females faster, and that exploiting the silk trails produced by earlier searchers allows them to locate females efficiently even when conditions make it difficult to directly detect their chemical messages. It might not seem like a great idea to follow another male to a female’s web, because this guarantees a competition over the opportunity to mate with that female. We would expect male animals to use cues about the presence of rival males to avoid competition, when given the choice (and in at least one other spider species, they do). But our time following this population in the field revealed that these males are unlikely to ever have that choice. There are so few sexually receptive females signaling on any given night that competition is inevitable. In this situation, the best tactic for males may be to arrive at a female’s web as fast as possible, even if other males are already there. Although being the first male to mate is important for black widows, being first to arrive is not critical, because courtship may last several hours. It’s at this point, at the female’s web, that competition and female choice can finally kick in.

Two males who have arrived at the same female’s web one after the other. Photo: Sean McCann

We are excited about these results, which reveal a surprising means of using indirect information to gain a competitive edge in the race to find females. We are also hope that our experimental race designs can allow us and other researchers to learn about spider mate searching behaviour and chemical communication in the future. Setting up races over different kinds of terrain to look at the effects of physical barriers on male performance, or doing races over several days and longer distances could yield more insights into what traits are important for searching males. Longer distance ultramarathons for spiders might be more appropriate in environments where females are more widely dispersed than at the site we studied. And the X-race is a convenient way to test male decision-making under controlled laboratory conditions while using a setup that reasonably reflects how male spiders actually move in the field.

This is only the first chapter of black widow behaviour research brought to you by the support of #TeamBlackWidow, and we look forward to sharing the next instalment soon!

*^ Thank you SO MUCH to Catherine & Doug Antone, Joe Lapp, Robb Bennett, Roy Dunn, Sean Lambert, Betty Kipp, Dora Sardas, Kristen Cain, Christy Peterson, Christy Peterson, Raphael Royaute, Dawn Bazely, Woodrow Setzer, Pierre Robillard, John Barthelme, Nemo de Jong, Mike Boers & Tanya Stemberger, Sina Rastegar, Sarah Langer, Sidnee & John Scott, Stephen & Linda Lambert, Staffan Lindgren, Amanda Yee, Rob Higgins, Tonia Harris, Tanya Jones, Joe O’Franklin, Dezene Huber, Tracey Birch, Peggy Muddles, Regine & Gerhard Gries, Gwylim Blackburn & Samantha Vibert, Alex & Karla Antone, Gil Wizen, Gwen Pearson, Joan Andrade, Kate Compton, Peggy McCann, Peter Andrade, Rick Redus, Robyn Raban, Shelley Barkley, Stewart, Geoff Bennett, Kyle Cassidy, Colin & Heather McCann, Jonathan Meiburg, Lori Weidenhammer, Diana Davis, Ray Scanlon, Ashley Bradford, Ed Morris, Robert Cruickshank, Marc Rashinski, James Petruzzi, Joseph Peter McNamara, Ariel Ng, Robert Neylon, Auriel Fournier, Victoria Nations, Leah Ramsay, Tom Pearce, Chloe Gerak, Scott Severs, Angie Macias, Nick Spencer, Thomas Astle, Luna Nicolas Bradford Ley, Peter Midford, Laurel Ramseyer, Morgan Vis, Tom Pardue, Scott Schrage, Kelly Brenner, Karen Yukich, Charmaine Condy, Amy Parachnowitsch, Catherine Scott, Christine Rock, Jason Parker-Burlingham, Jonathan Kade, Joseph Peter McNamara, Joshua Erikson, Juniper English, Nick Spencer, Robert Cruickshank, Sabrina Caine, Suran TheStorm, Richard Dashnau, Stephen Heard, Holly Fraser, Lynne Kelly, Roberta Chan, Kat Cruickshank, Meera Lee Sethi, Mike Hrabar, Tiffany Jacobs, Connie Larochelle, Willow English, David Steen, Michelle Reeve, Tone Killick, David Esopi, Antonia Guidotti, Elaine Wong, Lisa Wrede, Naomi Gonzales, Don Campbell, Matt Masterson, Paul Manning, Casey Peter, Dave Rich, Jessical Olin, Kate Rey, Katie Russell, Shari McDowell, Suzanne Spinelli, Christina Tran, Cindy Wu, Aaron Soley, Chris Garbutt, Greg Randolph, Lila Robinwood, Eric Damon Walters, The Spider Chick, & Steve Waycott!!!

** ^Thanks very much to Jay Cullen at UVic for kindly allowing us and our spiders access to his lab and microbalance!

Spider sex and silk: From mating threads and bridal veils to nuptial gifts and silk-lined chambers

Posted on July 13, 2018 by cataranea

I am very pleased to announce the publication of a review paper in the Journal of Arachnology (check out the full pdf here) about the fascinating uses of silk during spider sexual interactions coauthored with Alissa Anderson and my supervisor Maydianne Andrade. This paper has been several years in the making, and some of my very first blog posts were based on the research I did when I first started writing it back in 2013 as part of a reading course for my MSc degree.

Pisaurina mira (a nursery web spider in the family Pisauridae), one of the many diverse species featured in our paper, and the focus of my coauthor Alissa’s PhD research (photo: Sean McCann).

Overview

In this paper we describe the many weird and wonderful ways that male spiders use silk during courtship and mating. Little experimental work has been done to determine the function male silk in sexual interactions, but the available research suggests that in general silk use improves the male’s chances of mating with a particular female or reducing the risk that she will mate with other males. There is also mounting evidence that silk-bound sex pheromones are commonly produced by male spiders (though much less well studied than female silk pheromones), which may help to explain the importance of silk production during sexual interactions in many species. In the paper, we divide male silk use into three categories, briefly summarized below.

Silk deposition on the female’s web or other silk structures

Figure 2 from the paper. Examples of silk deposition onto females’ webs during courtship. (a) Araneus diadematus (Araneidae) male and female hanging from the male’s mating thread, attached to the periphery of the female’s web (photo: Maria Hiles). (b) Web reduction with silk addition by a Latrodectus hesperus (Theridiidae) male. The male has dismantled part of the capture web (which would have filled the lower half of the photograph before he began web reduction behavior) and is wrapping it with his own silk (photo: Sean McCann).

The most common and widespread form of silk use during sexual interactions across spiders is simply the deposition of silk on the female’s web or the silk surrounding her burrow entrance. More elaborate use of silk includes the installation of silk mating threads or webs on which courtship and copulation take place and web reduction, which can result in extreme modification of web architecture. The few experimental studies of this kind of silk use indicate that it is involved with preventing females from mating with other males, as in black widows. However, it is likely that mating threads and webs generally function to improve male mating success by improving transmission of their vibratory courtship signals and/or to reduce the likelihood of sexual cannibalism.

Silk bondage: the bridal veil

Figure 3 from the paper. Examples of silk ‘bridal veils’ applied to females’ legs and bodies during courtship. (a) Nephila pilipes (Araneidae) male depositing silk onto the female’s carapace, legs, and abdomen (photo: Shichang Zhang). (b) Xysticus cristatus (Thomisidae) female with silk on her forelegs and abdomen as she feeds on a prey item—note that the male is underneath her abdomen (photo: Ed Niewenhuys). (c) Latrodectus hesperus (‘‘texanus’’ morph, formerly Latrodectus mactans texanus; Theridiidae) male depositing silk onto the female’s legs (photo: Sean McCann). (d) Pisaurina mira (Pisauridae) male wrapping a female’s legs with silk prior to sperm transfer (Photo: Alissa Anderson).

The “bridal veil” (which I’ve previously written about in detail here) describes the silk some male spiders wrap around females prior to copulation. Arachnologists have debated the function of this behaviour for many years but it has been generally assumed to prevent sexual cannibalism. In some species like the nursery web spider Pisaurina mira, the silk wrapping physically restrains the female, giving the male time to escape while she struggles free of her bonds. In the orb-weaver Nephila pilipes, on the other hand, tactile cues and chemicals on the silk have been implicated in reducing the female’s aggressive tendencies. In both species, males that wrap females with silk are able to transfer more sperm to females, improving their mating success. Bridal veils are used by males from at least 13 families of spiders, including both web builders and wanderers, and there is still much to learn about the function of this fascinating behaviour across the diverse species that use it. In one species of wolf spider, the female even eats the silk of the veil after mating, which brings us to the third category of male silk use.

Silk wrapped nuptial gifts, or the gift of silk itself

Figure 4 from the paper. Examples of silk-wrapped nuptial gifts. (a) Female (right) Pisaura mirabilis (Pisauridae) accepts a silk-wrapped gift from a male (photo: Alan Lau). (b) A male (right) Metellina segmentata (Tetragnathidae) has wrapped a rival male in silk as a nuptial gift for the female (photo: Conall McCaughey).

In two families of spider, the nursery web spiders (Pisauridae) and their close relatives the longlegged water spiders (Trechaleidae) males present females with silk wrapped prey items called nuptial gifts (which I previously wrote about here). Sometimes, though, the silk package actually contains non-food items like rocks or plant material. The silk itself seems to be the important thing for getting the female to accept the gift and grasp it in her jaws, keeping her busy (and the male safe) during copulation. Both visual signals associated with the colour of the silk and chemicals on the silk may be important ways that gift-giving males communicate their quality and persuade females to mate with them, not to mention potentially deceiving them into accepting worthless gifts.

In other spiders gift-giving is less ritualized or happens only some of the time, like in the longjawed orbweaver Metellina segmentata. Males of this species often compete on the female’s web, and sometimes one of them will kill his rival, wrap him up with silk, and present him to the female. As with the habitual gift-givers discussed above, mating with the female while she is busy feeding on her erstwhile suitor likely decreases the male’s chance of becoming dinner. In still other spiders, the silk itself constitutes the gift, rather than the wrapping. In the ray spider Theridiosoma gemmosum, the male feeds the female silk directly from his spinnerets during courtship and copulation. This silk gift provides the female with nutrients (these spiders can recycle silk proteins). Finally, silk-lined burrows are considered gifts in the sex-role reversed wolf spiders Allocosa senex and A. alticeps. In these species, males dig deep silk-lined burrows to which they attract females with a pheromone. Mating takes place inside the burrow, and afterward the male helps the female to seal herself inside the burrow where she lays and broods her egg sac. The energy and silk that go into producing the burrow are a considerable investment for the male, and directly benefit the female and his offspring by providing a safe refuge.

The big picture

Silk use during courtship occurs in diverse species all across the spider tree of life, and provides myriad opportunities for future research. In the figure below, many families are not highlighted, but this is as likely to represent lack of knowledge about their courtship behaviour (or even anything about their natural history) as lack of silk use, and I hope that this paper will inspire other arachnologists to investigate mating behaviour, silk use, and the potential for male pheromone production in some of these little studied spiders. There are undoubtedly many exciting new discoveries to be made and I look forward to reading about them and perhaps making some myself in the future.

Figure 1.—Cladograms illustrating relationships between araneomorph spider families (based on Wheeler et al. 2016) and the occurrence of male silk and pheromone use. Note that in the Mygalomorphae (families not shown on the figure) there are records of male silk deposition on the female’s web or silk for species in the following three families: Dipluridae, Porrhothelidae, and Theraphosidae.

Full citation of the paper:

Scott CE, Anderson AG & Andrade MCB. 2018. A review of the mechanisms and functional roles of male silk use in spider courtship and mating. Journal of Arachnology 46(2): 173-206. Open access here

Crowdfunding black widow research

Posted on October 5, 2016 by cataranea

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.

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!

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.

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.

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!

Posted on July 9, 2015 by cataranea

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!

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.

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.

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!).

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.

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.

Soon 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.

Now 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!

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.

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).

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.

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!

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.)

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.

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!

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 spiders. Animal 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 spiders. Animal 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

Posted on May 8, 2015 by cataranea

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.

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:

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.

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:

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.

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.

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.

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.

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.

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!

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

Dinner or date?

Posted on January 17, 2014 by cataranea

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.

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.

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.

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.

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 one, 8(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 reports, 3. doi:10.1038/srep03557

Red-throated Caracaras: awesome birds that eat wasps

Posted on December 26, 2013 by cataranea

This post is not about spiders (sorry for any disappointment this may cause). Instead, it’s about some amazing (crazy?) neotropical raptors that specialize in preying on the brood of social wasps!

Red-throated Caracaras (Ibycter americanus) in French Guiana. These birds are members of the family Falconidae, and they are specialist predators of social wasps. (photo: Sean McCann)

Getting close enough to a wasp nest to eat its contents is no mean feat–as anyone who has ever been stung by a worker wasp defending its nest can probably attest. I was privileged to be involved in a study of these birds in French Guiana, led by Sean McCann.

Today, Sean and I and all our co-authors got a belated Christmas present with the publication of our paper in PLOS ONE.

Here’s a quick video summary of our research, narrated by me and Sean:

For more information, videos, and photographs, head over to Sean’s blog, Ibycter.

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