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

Pseudoscorpions! Small, strange arachnids

Posted on May 25, 2015 by cataranea

Yes, this is a blog about spiders, and no, pseudoscorpions are not spiders. But they are members of the class Arachnida, like spiders, and fascinating, like spiders! I encountered them for the first time on a recent trip to the Okanagan with Sean, so here’s a post about some of their natural history.

Two tiny pseudoscorpions Sean and I found while doing some rock flipping on a hillside near Vaseux Lake, BC. Photo: Sean McCann

Pseudoscorpions are really weird, and really awesome, creatures. Their name means “false scorpion” (which is also a common name for this order of arachnids), because superficially they look a lot like scorpions (members of another arachnid order), minus the “tail” with its stinger on the end.

Drawings of a pseudoscorpion and a scorpion from JH Comstock’s book. The illustrations are most likely by Anna C. Stryke, but possibly by Mrs. Comstock. Note that the scale is different for each drawing.

Pseudoscorpions are tiny. The one below (photographed under a microscope) is only about 1 mm long! The largest pseudoscorpions can get as long as 10 mm. Their small size means they can live in tight spaces, like between floorboards, under tree bark, or even under the elytra (hardened forewings) of beetles – but more on this later.

Pseudoscorpion found in Vero Beach, FL. Photo: Sean McCann

Pseudoscorpion morphology is strange. Like other arachnids, pseudoscorpions have two main body segments: a cephalothorax (the front part, a combined head-and-thorax bearing all of their appendages), and an abdomen. They may have one or two pairs of simple eyes on the sides of the cephalothorax (or none at all) and their vision is generally poor. As well as four pairs of legs, they have enormous chelate (pincer-like) pedipalps that they use for capturing prey and sensing their environment.

A neobisiid pseudoscorpion nicely displaying its chelate jaws and pedipalps. Photo: Marshal Hedin, licensed under CC BY-NC 2.0.

Pincer-like chelicera (singular of chelicerae) of a pseudoscorpion, bearing spinnerets on the movable finger. From Comstock’s book.

Their jaws (called chelicerae) are also like miniature pincers. Like spiders, pseudoscorpions can produce silk. Unlike spiders, who have abdominal silk glands and spinnerets, pseudoscorpions’ silk glands are in their cephalothoraxes, and their spinnerets are on the tips of their chelicerae! (The spitting spiders in the family Scytotidae are exceptional among spiders in also having silk glands in their cephalothoraxes, and “spitting” the silk out of their fangs along with venom.)

Pseudoscorpions use silk to build retreats* or cocoons for moulting, overwintering, and sometimes brooding their young.

Also like spiders, many pseudoscorpions use venom to subdue their prey, which includes mites and other tiny arthropods. The venomous pseudoscorpions are in suborder Iocheirata, which means “poison hands”. Their venom glands are in their modified pedipalps, with openings in the tips of one or both of the fingers of their claws.

To me, pseudoscorpion anatomy is all topsy-turvy (at least compared to spiders): their silk comes out the wrong end and their venom comes out of clawed “hands” instead of fangs.

Pseudoscorpion – modified from the illustration in Comstock’s book.

Pseudoscorpions also have pretty strange reproduction. Males deposit a spermatophore (a package of sperm) on the ground, which a female must then pick up and insert into her reproductive opening. Males of different kinds of pseudoscorpions have various methods of ensuring that a female finds and uses their sperm. Some are carefree: the male deposits the spermatophore, walks away and (figuratively) crosses his fingers and hopes that a female will encounter it by chance. Other tactics are rather more direct and reliable: the male engages the female in an elaborate “mating dance” and eventually pulls her over his spermatophore to ensure that she picks it up. In one species, Serianus carolinensis, males only produce spermatophores when a female is nearby, then they spin special silk webs that direct her to the package.

Once a female’s eggs are fertilized, she keeps them in a brood pouch under her abdomen (or sometimes next to her in a silken brooding chamber). This brood-sac contains food for the developing pseudoscorpion embryos, which grow and moult into protonymphs (juveniles that look just like adults, but smaller) before emerging.

A female Arctic pseudoscorpion, Wyochernes asiaticus, with her brood pouch. Photo: Crystal Ernst (used with permission)

Pseudoscorpions love books! Although I would like to think the little pseudoscorpion in the photograph below enjoys reading, what they really like about books is the booklice that sometimes live in them. Because pseudoscorpions can sometimes be found living between the pages of books and feeding on booklice, one common name for them is “book scorpions”.

“Book scorpion” enjoying some literature while waiting for booklice. Photo: Sean McCann

Finally, pseudoscorpions are hitchhikers! Because they are so small and don’t fly, pseudoscorpions can’t get very far on their own. To overcome this obstacle, they hitch lifts on other organisms – usually larger arthropods like beetles and flies. This particular kind of symbiosis – in which the individual doing the carrying is apparently unharmed – is called phoresis.

A longhorn beetle, Xylotrechus sagittatus, with phoretic pseudoscorpions hitching a ride on its leg. Photo: Sean McCann

Phoresis is a fantastic word that comes from Greek: phor means “carry, bear; movement” but it can also mean “thief”. Phoretic pseudoscorpions latch onto the bodies of their transportation with their pincers to steal a free ride. Some pseudoscorpions are stowaways under the elytra of comparatively gigantic harlequin beetles, and feed on phoretic mites and find mates while they travel. Piotr Naskreki has a wonderful blog post with pictures of these tiny ecosystems on a beetle’s back.

A closer view of the cluster of tiny travelers. Photo: Sean McCann

Want to find out more about pseudoscorpions? Of course you do! Here are some references and further reading from around the web:

10 Facts about Pseudoscorpions. Fantastic blog post by arachnologist Chris Buddle, who also created this great photographic key to the pseudoscorpions of Canada.

Comstock JH (1912). THE SPIDER BOOK: a manual for the study of the spiders and their near relatives, the scorpions, pseudoscorpions, whip-scorpions, harvestmen, and other members of the class Arachnida, found in America north of Mexico, with analytical keys for their classification and popular accounts of their habits. Doubleday, Page & Company. (Available from the Biodiversity Heritage Library, with wonderful illustrations)

Harvey MS (2013). Pseudoscorpions of the World, version 3.0. Western Australian Museum, Perth.

Pseudoscorpions page on the Massey University Guide to New Zealand Soil Invertebrates website. *Includes photos of pseudoscorpions’ silk retreats!

Pseudoscorpions page on the Encyclopedia of Life.

The order of the Pseudoscorpiones. Nice summary of pseudoscorpion biology by F. Schramm, with lots of photos and scholarly references.

Zeh DW & Zeh JA (1992). On the function of harlequin beetle-riding in the pseudoscorpion, Cordylochernes scorpioides (Pseudoscorpionida: Chernetidae). Journal of Arachnology, 47-51.

Tetragnatha revisited: dinner and romance at sunset

Posted on July 4, 2014 by cataranea

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.

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).

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

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?!

After a minute or so, she went back for her abandoned prey.

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.

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.

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.

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.

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.

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.

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.

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

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.

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.

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.

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!

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

Silk-wrapped prey items are a girl’s best friend

Posted on December 6, 2013 by cataranea

Following from last week’s story about silk bridal veils, this post focuses on another rare use of silk in spider courtship behaviour: the giving of silk-wrapped ‘nuptial gifts’.

This phenomenon has been most well studied in two spider species in closely related families: Pisaura mirabilis (Pisauridae)

Pisaura mirabilis male carrying a silk-wrapped nuptial gift. (Photo by Ferran Turmo Gort, licensed under CC BY 2.0)

and Paratrechalea ornata (Trechaleidae).

Male of genus Paratrechalea. (Photo by Gonzalo G. Useta, licensed under CC BY 2.0)

These spiders can teach us three valuable lessons about gift-giving in advance of the holiday season*.

1. Gift-giving can improve mating success.

In both families, nuptial gift giving behaviour is essentially the same. Before mating, the male obtains a prey item, (usually) wraps it up with silk, and offers it to the female during his courtship display. If she’s in the mood, she’ll grasp the package in her chelicerae, and while she’s busy consuming the prey inside, the male will copulate. It’s possible to mate without providing a gift, but in both Pisaura mirabilis and Paratrechalea ornata, males that give gifts have higher mating success: they have longer copulation durations and fertilize more of the female’s eggs.

2. Failure to wrap delicious gifts may result in their consumption, but no sex.

Females willingly accept unwrapped prey items, but may run off with them before mating can occur. This happens much less frequently with wrapped gifts, which are easier to hang on to. In Pisaura mirabilis, if the female tries to abscond with a gift that he still has in his grasp, the male goes limp (called thanatosis, or death-feigning) and allows himself to be dragged along with the gift. Once the female settles down to eat it, the male springs back into action and copulates.

3. Attractive silk gift-wrap will effectively disguise useless items, but only for a limited time.

Visual appeal may play some role in whether females accept nuptial gifts, but in Paratrechalea ornata, there are chemical cues specific to the male’s gift-wrapping silk that elicit female grasping behaviour. One of the advantages of this is that males can get away with giving females worthless items such as seeds, plant material, or prey that they’ve already fed on. Provided it’s wrapped up in attractively scented (or tasty) silk, the female will accept the gift and the male can copulate. As soon as the female realizes there’s no food inside the package, however, she’ll cut the mating short.

So there we have it. Pick the perfect prey item, wrap it up in silk, and hang on tight!

*Lessons may have limited application to non-spider interactions

REFERENCES (also linked in the text)

Albo, María J., & Costa, F. G. (2010). Nuptial gift-giving behaviour and male mating effort in the Neotropical spider Paratrechalea ornata (Trechaleidae). Animal Behaviour, 79(5), 1031–1036. doi:10.1016/j.anbehav.2010.01.018

Albo, Maria J, Winther, G., Tuni, C., Toft, S., & Bilde, T. (2011). Worthless donations: male deception and female counter play in a nuptial gift-giving spider. BMC evolutionary biology, 11(1), 329. doi:10.1186/1471-2148-11-329

Andersen, T., Bollerup, K., Toft, S., & Bilde, T. (2008). Why Do Males of the Spider Pisaura mirabilis Wrap Their Nuptial Gifts in Silk: Female Preference or Male Control? Ethology, 114(8), 775–781. doi:10.1111/j.1439-0310.2008.01529.x

Brum, P. E. D., Costa-Schmidt, L. E., & de Araujo, A. M. (2011). It is a matter of taste: chemical signals mediate nuptial gift acceptance in a neotropical spider. Behavioral Ecology, 23(2), 442–447. doi:10.1093/beheco/arr209

The bridal veil: how spiders tie the knot

Posted on November 29, 2013 by cataranea

I’m currently sifting through mountains of literature on spider biology searching for references to silk use in courtship and sexual communication. One of the particular topics I’m interested in is the rarely reported ‘bridal veil’. So far I’ve found records of bridal veils in 12 families, all in the Araneomorphae. I’ve included photos of most of the species in question (or a species in the same genus) to highlight the morphological diversity of the spiders that share this weird and wonderful behaviour!

Safe sex

Courting a female can be a risky business. Spiders are predators (with some exceptions), and sometimes highly aggressive females would rather treat a male as dinner than a date. Male spiders have diverse, complex repertoires of courtship behaviours, some of which most likely function to inhibit the predatory tendencies of females.

The paired pedipalps of male spiders are modified for transferring sperm. This means that, usually, the male needs to copulate twice in order to secure paternity of as many offspring as possible. The mechanics of copulation are often complex, and the male can’t afford any untimely interruptions. Possibly, the bridal veil has a role to play…

Getting tied down

Bristowe coined the term ‘bridal veil’ in his 1958 paper describing the mating behaviour of the crab spider Xysticus cristatus and Xysticus krakatuensis (Thomisidae).

Xysticus cristatus female (photo credit: Arlo Pelegrin)

Part of the male’s courtship behaviour includes anchoring the female’s legs and cephalothorax (front body segment) to the substrate with a ‘veil’ of silk threads. After mating, the female apparently has no trouble freeing herself from her silken bonds.

The centimetres high club

The nursery web spider Pisaurina mira (Pisauridae) puts a spin on the bridal veil idea.

Pisaurina mira (photo credit: Keith Bradley)

In this species, courtship and mating take place as the spiders hang in midair, suspended by their draglines below a leaf. Before copulation, the male ties up the female’s first two pairs of legs in front of her cephalothorax, by spinning silk as he twirls the female around on her thread. Bruce and Carico (1988) suggested that the split-second that it took for the potentially cannibalistic female to struggle free from the veil gave the male just enough time to climb up out of harm’s way.

Oxyopes schenkeli (Oxiopidae) males have very similar bridal veiling behaviour, which results in the binding of the female’s first three pairs of legs with silk.

Oxyopes elegans (Oxiopidae) (photo by Robert Whyte, licensed under CC BY 2.0)

The context of courtship in these spiders is also up in the air, suspended by silk draglines from a leaf (60-90 cm above the ground). After observing at least one male getting cannibalised despite spinning a bridal veil, Preston-Mafham 1999 proposed that the main function of the bridal veil is to stimulate the female to mate, possibly via pheromones (chemical signaling molecules) on the silk.

A touch of silk

The courtship of Dictyna volucripes (Dictynidae), takes place on the female’s web.

Dictyna species (photo by Farran Turmo Gort, licensed under CC BY 2.0)

The male begins by depositing silk on the web, at a distance from the female, before approaching and applying a light silk wrapping to her body. Starr (1988) concluded that males of this species are not in any real danger from females – although females occasionally rushed towards males, males were able to easily avoid them.

Meta segmentata is a long-jawed orb-weaver (Tetragnathidae).

Meta segmentata female (photo by Brandobras, licensed under CC BY 2.0)

The veiling behaviour in this species was described as “partial wrapping of the female as though she were prey”. Lopez (1986) suggested that the silk of the bridal veil might inhibit female aggression through physical contact with sensory hairs on her body.

Throughout copulation, Schizocosa malitiosa (Lycosidae) males release dragline silk over the upper surface of the female’s front legs.

Penultimate (one molt away from maturity) Schizocosa male (photo by Marshall Hedin, licensed under CC BY 2.0)

A fairly sparse bridal veil is a common element of courtship in the genus Latrodectus (Theridiidae). Since I study western black widows (L. hesperus), I’ve included a video of one of ‘my guys’ doing his thing (video taken by Samantha Vibert)

Ross and Smith (1979), studying L. hesperus, and Aisenberg et al. (2008), studying S. malitiosa, suggested that the bridal veil silk is impregnated with a pheromone that induces female catalepsy. Placing the pheromone-laden silk directly on the female’s body might be the best way to ensure that she receives the chemical message and remains passive throughout copulation.

Putting a ring on it

A version of the bridal veil has been described for both species in the very small family Homalonychidae: Homalonychus theologus (Dominguez and Jiminez 2005) and Homalonychus selenopoides (Alvarado-Castro and Jiménez 2011).

Homalonychus theolougus penultimate male (photo by Marshall Hedin, licensed under CC BY 2.0)

These are wandering spiders, and mating takes place on the ground. With the female’s legs all drawn up close to her cephalothorax, the male circles around her, binding her legs together tightly with a ring of silk. After the first copulation, he’ll add some more silk, reinforcing the ring, then mate a second time. As soon as the second copulation is completed, the male beats a hasty retreat. A second later the female breaks free from the silk ring, and spends some time grooming, trying to remove all the silk from her legs.

Thalassius spinosissimus (Pisauridae) females build a special mating web and hang from it in ‘mating posture’ with all the legs drawn in tightly as described above for the homalonychids. Males in this species also ring the female’s legs with silk (Sierwald 1988).

Thalassius albocinctus (photo by Vijay Anand Ismavel, licensed under CC BY 2.0)

Ancylometes bogotensis (Ctenidae) takes the ring thing to the next level.

Ancylometes bogotensis (Ctenidae) (photo credit: Sean McCann)

The male starts by spinning an ‘outer’ ring of silk around the female’s tibiae, then he adds a second, ‘inner’ ring around the patellae (see diagram with names of leg segments here). His handiwork complete, he tips the trussed-up female over onto her side and mates with her (Merrett 1988).

Cupiennius coccineus (Ctenidae) males, in staged encounters with heterospecific (Cupiennius salei) females, sometimes engaged in bridal veil spinning behaviour.

Cupiennius salei (photo by Ian Morton, licensed under CC BY 2.0)

Here’s where it starts to get interesting. Normally, when mating with females from their own species, Cupiennius males don’t go in for the bridal veil thing. However, when researchers paired C. coccineus males with C. salei females (who are on average a bit bigger than the C. coccineus females), some males circled the female, depositing silk on her legs. Two of the three males that spun bridal veils were able to mate with the heterospecific females, while the third became lunch. As Schmitt (1992) noted in reference to this unfortunate male’s demise, “Obviously, the male silk did not seriously affect the female’s mobility.”

One explanation is that the ‘veil’ in this situation is a result of some confusion over whether to treat the too-large female as a potential mate, or prey (these guys can take down prey larger than themselves and normally use silk in this context). Another option is that this is a part of the courtship repertoire of Cupiennius males, but it’s reserved for especially large, potentially dangerous, females and was never seen before because usually similarly sized individuals were paired for laboratory mating observations (Schmitt 1992).

Courtship in both Argiope aemula (Araneidae),

Argiope aemula female (photo by falilin, licensed under CC BY 2.0)

and Nephila pilipes (Nephilidae),

Nephila pilipes female CC from drriss http://www.flickr.com/photos/drriss/10946835995/

Nephila pilipes female (photo by drriss, licensed under CC BY 2.0)

takes place on the female’s orb-web. The tiny male does a variation on the ring-type bridal veil, doing his silk spinning on the top of the female’s cephalothorax and abdomen (he’s so small he has room to walk around on there). He attaches silk at the bases of the female’s legs, building up a complex network of silk (Robinson and Robinson1980).

Lifting the veil

Recently, Zhang et al. (2011) published the first experimental study of the function of a bridal veil. The authors wanted to figure out if the bridal veil in Nephila pilipes has any role in reducing female aggressiveness, and if so, whether chemical and/or tactile cues were responsible.

In the lab, males never spun bridal veils prior to their first copulation. When female movement interrupted the first copulation, males that deposited silk inevitably copulated a second time, while most males that tried to mate again without spinning a bridal veil were cannibalized.

The researchers then compared the success of normal, silk-slinging males with males that had their spinnerets covered with super-glue*. It turned out that these males did just as well as normal males by going through the motions of bridal veiling behaviour even though they were prevented from spinning silk. Further experiments preventing females from detecting potential chemical and/or tactile cues associated with bridal veil spinning behaviour suggested that both touch and smell are likely involved.

Tying it up

Are bridal veils physical restraints or stimulating strands? Is silk a substrate for sexy scents or catalepsy-inducing compounds? It’s really not clear. Given that female spiders commonly produce silk-bound pheromones, I suspect that male silk pheromones are probably important. However, it’s becoming increasingly apparent that spider communication systems are highly sophisticated, and messages may be simultaneously transmitted between individuals via multiple modalities. Spiders use vibratory, chemical, tactile, and (sometimes) visual signals and senses in a variety of combinations, and untangling this mystery will take a lot more investigation!

*In case you’re concerned that super-gluing spiders is not a nice thing to do, I can assure you that cyanoacrylate is recommended for use on spiders in the book Invertebrate Medicine. I’ve looked into it because I’ve done some spider gluing myself.

References without direct links in the text:

Bristowe, W.S. 1958. The World of Spiders. Collins, London.

Lopez, A. 1986. Glandular aspects of sexual biology. In: Ecophysiology of Spiders (Nentwig, N., ed.). Springer Verlag, Berlin, pp. 121—131.

Merrett, P. 1988. Notes on the biology of the neotropical pisaurid, Ancylometes bogotensis (Keyserling) (Araneae: Pisauridae). Bulletin of the British Arachnological Society. 7: 197-201.

Preston-Mafham, K.G. 1999. Notes on bridal veil construction in Oxyopes schenkeli Lessert, 1927 (Araneae: Oxyopidae) in Uganda. Bulletin of the British Arachnological Society. 11(4): 150-152

Schmitt, A. 1992. Conjectures on the origins and functions of a bridal veil spun by the males of Cupiennius coccineus(Araneae, Ctenidae). Journal of Arachnology 20:67–68.

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