A comb-tailed spider

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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References

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

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

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

Tetragnatha revisited: dinner and romance at sunset

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

Dinner or date?

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

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

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

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

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

webs are good for this

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

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

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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.

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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.

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

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

References:

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

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

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

Meet the Mygalomorphae!

Mating behaviour and silk use in (some) mygalomorphs

So in my ‘intro to spider systematics’ post, I wrote that most of the Mygalomorphae are tarantulas. This is not actually true when you consider total numbers of species. Of the 2775 mygalomorph species (in 16 families), 950 species are in the family Theraphosidae (tarantulas), so that’s actually only about 34%. I probably should have said that the tarantulas are the most common mygalomorphs (and the ones people are generally most familiar with). Theraphosidae definitely wins the prize for the largest mygalomorph family, though. The next most speciose family is Nemesiidae, with 364 species.

I also implied that the Mygalomorphae aren’t all that sophisticated when it comes to silk use. Whereas the Araneomorphae have the ability to spin several different kinds silk specialized for particular functions, the Mygalomorphae produce only one general purpose silk. This is not to say, however, that they have not come up with some marvellous silk-based innovations!

turret M Hedin http://www.flickr.com/photos/23660854@N07/4485414016/sizes/z/in/photolist-7QmVjq-hBLdXo-7L4ijK-7L8h9G-bsNAPc-bsNArZ-bsNBLK/

In the centre of the vegetation in the foreground, you may spy the mouth of a well camouflaged silk-lined ‘turret’ built by a mygalomorph in the family Antrodiaetidae. (Photo by M. Hedin, licensed under CC BY 2.0)

Mygalomorphs have poor vision, so they must rely on chemical (smell or taste), vibratory, and tactile senses. It was traditionally thought that these relatively ‘primitive’ spiders had simple sexual communication systems. However, in their recent review in the Journal of Arachnology, Ferretti and coauthors argue that the sexual behaviour of mygalomorphs actually involves some quite elaborate courtship displays and complex mechanisms of communication. This post will highlight the 6 mygalomorph families described in the paper, most of which use silk in various ways for both prey capture and sexual communication.

Now, as a general rule, spiders are predatory, and mygalomorphs are no exception. They’re pretty keen to snap up anything that blunders into their field of vibratory perception, even if it’s another spider. The main functions of courtship behaviour in mygalomoprhs are mate recognition, orientation and synchronization of sexual behaviour, and suppression of non-sexual responses. Females must advertise their location and receptivity, and males must somehow signal “male, not meal!” to their potential partner. This can be tricky when the stage on which the male must show off his desirability as a mate is the same one that the female uses to detect prey. We’ll see what kinds of things these spiders get up to in order to make it to the finish!

Antrodiaetidae: turret mygalomorphs

Antrodiaetids live underground in silk-lined burrows. The burrow entrance is extended with a turret made from silk, soil, and plant material that blends in beautifully with the surrounding substrate. The spider waits for prey just out of sight inside the tube, where she can detect and quickly respond to vibrations produced by insects brushing against the litter encasing the turret. Males detect the female’s location using pheromones – chemicals acting as olfactory personal ads – on the silk that lines her home.

Antrodiaetus riversi (Antrodiaetidae) in feeding position in turret (Photo by M. Hedin, licensed under CC BY 2.0)

Dipluridae: funnel-web mygalomorphs

The diplurid funnel-web is a horizontal silk sheet leading to a tubular retreat in a crevice or perhaps under a stone or log. From this silken hideout, the spider detects vibrations produced by prey passing over her sheet web. The female’s funnel-web also forms the dance-floor for the male’s vibratory courtship display. The male’s courtship signals are transmitted to the female through the silk sheet. Typically, she does not respond, which is great news for the male! Presumably his pedipalp drumming and many legged tap-dancing is quite distinct from prey vibrations, inhibiting the predatory tendencies of the female.

Ischnothele caudata (Dipluridae) female in her funnel web. Note the elongated spinnerets characteristic of this family. (Photo by M. Hedin, licensed under CC BY 2.0)

Mecicobothridae: sheet-web mygalomorphs

Mecicobothriidae is a family containing nine species of small spiders that build sheet-webs on the soil. In Mecicobothrium thorelli, chemical and/or tactile signals on the female’s silk trigger the male’s courtship display. Like in the diplurids, the male’s dance moves transmit vibrations through the silk to the female, who sits passively in judgment. The receptive female apparently enters a cataleptic state, allowing the male to haul her around the web and manoeuvre her into just the right position. It’s not quite as easy as all that for the male, though. In order for a successful copulation to occur, the chelicerae of the spiders must interlock in a very specific way. If the couple is disturbed while in copula, or there are any difficulties disengaging from this toothy embrace, it’s game over for the male, and dinner time for the female. Once the deed is done, a successful male will stick around on the female’s web, attacking any other males attempting to try their luck with the female. This ‘mate guarding’ behaviour is very unusual among mygalomorphs.

Female Mecicobothrium thorelli (Mechicobothriidae) on her sheet-web. (Photo credit: Gabriel Pompozzi)

Theraphosidae: tarantulas

Theraphosids often live in silk-lined underground burrows, or silken retreats under rocks and vegetation. Sometimes they even build their tube-like homes in trees. Pheromones on the silk allow males to find and recognize females, and also trigger courtship behaviour. Males transmit species-specific vibratory courtship signals through the ground, to the female listening in her burrow. These seismic love songs can be detected by females at a distance of more than one metre. In Avicularia avicularia, the female actively responds, tapping her first pair of legs and pedipalps on the substrate. These good vibrations tell the male she is receptive to his advances, and may also help the male orient toward her.

Immature Avicularia avicularia (pinktoe tarantula) (Photo credit: Sean McCann)

Nemesiidae: tube-trapdoor mygalomorphs

Nemesiids generally live in silk-lined burrows, sometimes finished with hinged, camouflaged trap-doors. Male courtship includes scratching and tapping with the legs on the ground, often at a distance from the female’s burrow entrance, suggesting that this is another form of long-distance seismic communication. While most female mygalomorphs remain relatively passive throughout courthship and copulation, Acanthogonatus centralis females jerk violently, twitching all their legs and pedipalps. This enthusiastic behaviour may stimulate the male to begin copulation.

Nemesiidae (M Hedin)

Calisoga longitarsis (Nemesiidae) at burrow entrance (Photo by M. Hedin, licensed under CC BY 2.0)

Microstigmatidae

The family Microstigmatidae contains 16 species of tiny spiders (males are only 1-3 mm long!). This is one family that apparently makes minimal use of silk. Xenonemesia platensis males only begin courtship after making direct contact with the female’s body. The male’s courtship behaviour includes quivering with the first two pairs of legs. The female, if she is receptive, responds by moving into a mating posture with her genital area exposed, allowing the male to clasp her pedipalps and chelicerae with his first legs.

This clasping of the female’s chelicerae by the male is common in mygalomorphs; in many species males have specialized structures on their legs that facilitate the embrace. Some researchers think it may be a way of restraining a potentially lethal female, keeping her fangs at leg’s reach. However, the fact that female catalepsy during copulation is also widespread sheds some doubt on this interpretation. Alternatively, it may be a more ‘symbolic’ form of bondage akin to the bridal veil in some araneomorphs. The tactile stimulation associated with the male’s clasping may in fact cause the female to become quiescent.

Throughout copulation, the Xenonemesia platensis male continues his tactile courtship, tapping and scraping his second pair of legs against the female. It’s possible that this copulatory courtship persuades the female to use his sperm over that of competitors, but more work needs to be done to test this hypothesis.

Mating Xenonemesia platensis (Microstigmatidae). The male has the female’s pedipalps and chelicerae clasped in his first pair of legs, while he uses his second pair of legs to beat and scrape the female’s coxae (leg segments closest to the body) (Photo credit: Gabriel Pompozzi)

The mygalomorphs may all look fairly similar, but they have surprisingly diverse habits, and use their multi-purpose silk in clever ways. Their sexual communication is most certainly not simple, incorporating multiple signaling modalities. Just as with most araneomorphs, good vibrations and sexy scents are the key!

Growing evidence suggests that contact sex pheromones associated with female silk are common in mygalomorphs (as they are in araneomorphs). Sex pheromones have also been implicated in the sexual communication systems of some spiders in the Mesothelae, suggesting that chemical communication was acquired early in the evolutionary history of spiders.

This story of mygalomorph mating also highlights the fact that female spiders in general are not simply passively waiting for marauding males to stumble across their doorsteps. On the contrary, they actively advertise for a mate, sometimes participating in a vibratory signaling ‘conversation’ with courting males, and likely judge a suitor’s quality both before and during copulation.

The private lives of spiders never cease to fascinate!

References, resources, and acknowledgements:

For a wonderful read about the evolution of spiders and their silk, including lots more information that I didn’t include about the fascinating habits of mygalomorphs, I highly recommend Leslie Brunetta and Catherine Craig’s book Spider silk: Evolution and 400 Million Years of Spinning, Waiting, Snagging, and Mating (an excellent gift idea!).

Ferretti, N., Pompozzi, G., Copperi, S., Gonzalez, A., & Pérez-Miles, F. (2013). Sexual behaviour of mygalomorph spiders: when simplicity becomes complex; an update of the last 21 years. Journal of Arachnology, 16(3), 85–93.

Ferretti, N., Pompozzi, G., Copperi, S., Pérez-miles, F., González, A., & Pe, F. (2012). Copulatory behavior of Microstigmatidae (Araneae: Mygalomorphae): a study with Xenonemesia platensis from Argentina. Journal of Arachnology, 40(2), 252–255.

Costa, F. G., & Perez-Miles, F. (1998). Behavior, life cycle, and webs of Mecicobothrium thorelli (Araneae, Mygalomorphae, Mecicobothridae)Journal of Arachnology26, 317–329.

Special thanks to Gabriel Pompozzi for allowing me to use his photographs of Xenonemesia platensis and Mecicobothrium thorelli. Check out more of his fantastic images of mygalomorphs here.

I am also very grateful to Marshal Hedin for generously making his photographs available under creative commons licenses. He has some really wonderful sets of shots of several mygalomorph families on flickr.

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

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

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 sp CC ivijayandan

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.