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

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.

  1. 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.

  1. 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.

  1. 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 matingJournal of Arachnology 46(2): 173-206. Open access here

Rhomphaea: ridiculously long theridiids

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Male Rhomphaea fictilium – a theridiid with a ridiculously long abdomen and pedipalps! Photo: Al Denesbeck (used with permission).

I’ve written about long spiders before: the “stretch spiders” in the family Tetragnathidae (long-jawed orb-weavers) are notable for their elongated bodies as well as their long jaws. When I first spotted Rhomphaea, I thought it might be a tetragnathid, before taking a closer look and realizing it must be something else entirely. As it turns out, Rhomphaea is a very odd-looking member of the family Theridiidae, or comb-footed spiders, which includes the black widows!

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Rhomphaea fictilium from my field site at Island View Beach on Vancouver Island, BC. This spider does not show much resemblance to its relatives the black widows, who are found nearby! Photo: Sean McCann (used with permission).

Rhomphaea is a Latin word of Thracian origin that literally means long spear or javelin. The long, straight abdomen of the male in the photo below helps explain the name.

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Male Rhomphaea fictilium with long, “spear-like” abdomen and extremely long pedipalps. Photo: Kyron Basu, licensed under CC BY-ND-NC 1.0.

Below is a female Rhomphaea projiciens with her egg sac. Note that the spider has a tiny spine on the end of her abdomen, making it more literally spear-like!

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Rhomphaea prociciens female with egg sac. Photo: Jon Hart (used with permission).

My first encounter with this genus was observing Rhomphaea fictilium. Fictilis means “clay” in Latin, and the Latin-derived English adjective fictile “means capable of being molded.” The abdomens of Rhomphaea fictilium are worm-like and flexible, allowing the spider to change its shape. This ability may help Rhomphaea to camouflage itself in different contexts – the shortened abdomen of the little one in the photo above helps it to blend in with the seed heads it rests on. When their abdomens are held out long and straight, these spiders can look like very convincing sticks. The incredible photo below shows an individual that looks like it has the tail of a (very tiny) dragon!

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Rhomphaea fictilium with extended abdomen (dragon’s tail?). Photo: Gergin Blagoev, licensed under CC BY 3.0.

As well as having wonderfully strange morphology, Rhomphaea have rather unusual habits. Most spiders are generalist predators, and spiders in the family Theridiidae typically build tangle webs that they use to catch crawling insects and other arthropods, including other spiders. Rhomphaea, unlike most of their relatives, specialize on hunting other spiders. They do sometimes build their own rudimentary webs from just a few silk lines, but they also enter the webs of other spiders and use aggressive mimicry to hunt their owners. Rhomphaea will pluck the web and produce vibrations that lure the resident spider out to investigate what they perceive to be prey caught in the web. The web-building hunter then becomes the hunted, tricked into the approaching the dangerous intruder. Rhomphaea fictilium have been reported to prey on other theridiids, orb-weavers (araneids), sheet-weavers (linyphiids) and others.

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Rhomphaea fictilium with its unfortunate prey. Note that the spider is covered with silk – theridiids comb sticky silk out of their spinnerets with their fourth legs and throw it over their victims to subdue then before biting. Photo: Al Denesdbeck (used with permission).

These tiny, cryptic spiders are rare and difficult to spot, but keep your eyes out for them in low tree branches, grasses, and bushes – or in the webs of other spiders!

References & further reading

Bradley, R. A. (2012). Common Spiders of North America. Univ of California Press.

Exline, H., & Levi, H. W. (1962). American spiders of the genus Argyrodes (Araneae, Theridiidae). Arañas americanas del género Argyrodes (Araneae, Theridiidae). Bulletin of the Museum of Comparative Zoology., 127(2), 75-202. Full text at BHL

Paquin, P., & Dupérré, N. (2001). On the distribution and phenology of Argyrodes fictilium (Araneae, Theridiidae) at its northern limit of North America. Journal of Arachnology, 29(2), 238-243. PDF

 

Spiders of Lost Lagoon

This weekend, I was lucky to spend a rare rain-free November morning in Vancouver’s famous Stanley Park with Sean McCann, who kindly provided all the photos for this post. Despite the late season and cool weather, it turned out to be a very spidrous (a term coined by Sean) day indeed! We must remember that the end of Arachtober does not necessarily mean the end of spider season, as Eric Eaton pointed out in a recent Spider Sunday post.

Our first spider-observation stop was outside the Lost Lagoon Nature House. What at first glance looked like a dirty and unremarkable garage door turned out, upon closer inspection, to be a veritable spider heaven!

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Here I am making notes on an impressive aggregation of spiders.

Although not quite on the massive scale of the aggregation of thousands of orbweavers inside a wastewater treatment plant that Gwen Pearson wrote about recently, I estimate that the area around this single garage door is home to several hundred spiders all living in extremely close proximity. In this case, the aggregated webs are just a couple metres away from the edge of Lost Lagoon, a freshwater habitat that produces large numbers of chironomid midges as well as larger aquatic insects. Lights attract these insects, making this the perfect hunting ground at night, when the spiders are most active.

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It’s hard to see individual spiders at this scale, but looking closer, they are everywhere!

Here’s a closer look  at one small area of the door (zooming in on the upper right corner of the photo above). Two large females rest in the open while a third hides away in a silken retreat next to a cluster of 3 egg sacs.

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Almost all the spiders in this aggregation were members of a single species, the bridge orbweaver Larinioides sclopetarius (family Araneidae). Here are some closer shots of a male and female:

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Male Lariniodes sclopetarius against the blue backdrop of the building.

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Female Lariniodes sclopetarius posing on some nearby vegetation.

We did find a few spiders other than bridge orbweavers on the building. A female L. sclopetarius and what’s most likely a juvenile Eratigena (formerly Tegenaria) appeared to be sharing the same retreat in a cement pillar.

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Moments before this photo was taken, these two were hunkered down close together in the pit in the cement, apparently  oblivious to one another.

Right on the other side of the same pillar, this male longjawed orbweaver Tetragnatha elongata was hanging out.

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It turns out that Lariniodes and Tetrgnatha are the usual suspects when it comes to communal living and megawebs. Spiders in both genera like to live near water as was the case here next to the lagoon. Lariniodes sclopetarius often build their webs on human-made structures, and especially prefer to be next to lights (Greene et al. 2010 and references therein). This preference was very evident at the Nature House – of the four identical  garage door sections of the side of the building facing the lagoon, the spiders were almost exclusively living on the only one with a light.

Although our first stop provided plenty of arachnological excitement for one day, we eventually moved on and explored the rest of the lagoon.

We found this male Pimoa altioculata and several others of the same species on webbing underneath the railing of a small footbridge.

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Spiders in the family Pimoidae are related to the linyphiids, and also build sheet-webs.

When Sean removed the spider from his web to try to get some better shots, he immediately went into “play dead” mode, tucking all his legs up tightly around his body for defense.

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Several more longjawed orbweavers were hanging out under the railings of the same bridge.

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Another Tetragnatha sp. These spiders are typically found near water.

We also found this beautiful example of a hammock-shaped sheet web built by a small linyphiid.

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In this shot you can see the silhouette of the spider at the upper left hand side of the “hammock.”

We admired the web for some minutes before noticing the resident spider, who eventually came out onto the web for the lovely shot below:

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You can tell from the bulbous pedipalps that this is a subadult male. I am pretty sure the species is Neriene digna.

All in all it was a wonderful day at the park. I hope your November is just as spidrous as ours has been so far here on the wet coast!

Reference:

Greene, A., Coddington, J. A., Breisch, N. L., De Roche, D. M., & Pagac, B. B. (2010). An Immense Concentration of Orb-Weaving Spiders With Communal Webbing in a Man-Made Structural Habitat (Arachnida: Araneae: Tetragnathidae, Araneidae). American Entomologist, 56(3), 146-156.

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

Long, cryptic spiders

Iona beach, near the Vancouver International Airport in Richmond, BC, is fantastic place to go looking for spiders and other arthropods, and there always seems to be something new to discover on the dunes. So it was an unusual situation when last Friday evening, just before the park gates were about to close, Sean was lamenting not having found anything very interesting to photograph. We decided to spend our last minutes on the beach in an effort to turn up some sleeping hymenopterans in the vegetation bordering a walking path. After closely inspecting a couple of plants, instead of a sleeping bee or wasp, I found what at first glance looked like a tiny twig hanging in the middle of a spider’s orb web. Meet Tetragnatha caudata, the longest, most cryptic orb-weaver I have ever met!

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This slender female was not easy to spot among the grasses, even though she was hanging right in the middle of her web. Her body is only about 1cm long from tip to tail.

Tetragnathidae is the family of the longjawed orb-weavers. You can see where the name comes from in the photo of a male below. During mating, the male and female interlock their large chelicerae in toothy embrace. This is where the male’s exceptionally long pedipalps come in handy, allowing him to reach the female’s epigynum while maintaining his hold on his partner’s fangs.

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You can see this male’s large, powerful jaws sticking out to the sides underneath his very long, slender pedipalps.

Spiders in the genus Tetragnatha are sometimes called ‘stretch spiders’ because of their elongated bodies. They often rest with their first two pairs of legs stretched out in front. They can be very cryptic in this posture, especially if they cling to twigs or stems that are similar in colour to their bodies. Although they normally use their webs for hunting, sometime Tetragnatha will also snap up unsuspecting prey when lying low like this on vegetation.

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A male Tetragnatha in camouflage mode. This works better on dry grasses or twigs, I would think. But still pretty stealthy here.

Most species in the genus Tetragnatha are difficult to tell apart, but I got lucky with this one (it keys out in the second couplet of the key to the Canadian species in this genus). Tetragnatha caudata is so named because of its strange looking abdomen (caudata means ‘tailed’ in Latin). While I would expect the spinnerets to sit at the tip of a spider’s abdomen, in this species there is a slight kink where the spinnerets sit on the underside of the abdomen, and a pointy tail sticks out behind them.

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If you look closely you can see a strand of silk coming out of this female’s spinnerets, located on the underside of her abdomen just before it bends into a pointy tail.

The orb webs of Tetragnatha are usually horizontal or angled (unlike the vertical webs of spiders in the more familiar orbweaver family Araneidae) and have a hole in the centre where the spider sits waiting for prey.

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We found several of these tiny Tetragnatha caudata among tall grasses, but larger members of the genus typically build their horizontal orbwebs over water, allowing them to capture insects such as mosquitoes as they emerge.

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So let this be a lesson: next time you’re out looking for wildlife, stop and take a careful look in some seemingly boring vegetation! You never know what wonders you might turn up.

Thanks to Sean, as usual, for the great photos!

References:
Adams, R.J. (2014) Field Guide to the Spiders of California and the Pacific Coast States. University of California Press, Berkeley and Los Angeles.

Bradley, R. (2013) Common Spiders of North America. University of California Press, University of California Press, Berkeley and Los Angeles.

Dondale, C. D., Redner, J. H., Paquin, P., & Levi, H. W. (2003). The Insects and Arachnids of Canada. Part 23. The Orb-weaving Spiders of Canada and Alaska (Araneae: Uloboridae, Tetragnathidae, Araneidae, Theridiosomatidae)Ottawa, NRC Research Press.