Monthly Archives: November 2013

The bridal veil: how spiders tie the knot

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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.

 

A VERY brief introduction to spider systematics (Part 1)

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All the information that follows is from Rainer Foelix’s excellent book Biology of Spiders. Photos used with permission from Sean McCann.

Here I will provide a brief orientation to the spiders that I hope will help place future posts that feature spiders in different suborders, orders and families. I will try to add more detailed taxonomy information as I go along. Also, I hope this post will help me to remember some basic information that I am always re-learning (never again will I look up orthognath vs. labidognath!).

There are about 40,000 more than 44,000 identified species of spiders in 110 112 families* (I hope that someday I will have posts highlighting every family!).

The order Araneae includes all the spiders. There are three suborders:

The most ‘primitive’ (phylogenetically oldest) spiders are in the suborder Mesothelae. They have segmented abdomens like other arthropods, and unlike the rest of the spiders. There is only one family in the Mesothelae, the Liphistiidae. I don’t really know anything else about them at this point (I will come back to them in the future).

The rest of the spiders are in the Opisthothelae, which contains the two other suborders, the Mygalomorphae and the Araneomorphae.

Both the Mesothelae and the mygalomorphs have orthognath chelicerae. Spider chelicerae are a large pair of mouthparts tipped with articulated fangs through which venom is injected into prey. Orthognath chelicerae work in parallel. Make ‘air quotes’ with your first two fingers – like that.

The majority of species in the Mygalomorphae are tarantulas, in the family Theraphosidae (in French, a tarantula is called a ‘mygale’, which makes this easy to remember ever since I spent some time in French Guiana).

Female Theraphosa blondi in French Guiana.

Female Theraphosa blondi (Theraphosidae) in French Guiana.

There are several other less well-known families in the Mygalomorphae that I will get to in later posts. Mygalomorphs can produce silk, but most don’t build webs; they lack the pyrifrom silk glands that that araneomorphs use to cement their silk threads together or to a substrate.

Araneomorphs have labidognath (opposing) chelicerae. Touch your thumb and forefinger together repeatedly in pincer-like fashion, so. The Aranaeomorphae includes all the ‘usual’ non-tarantula spiders you might run into, including families such as the

Araneae (orb-web spiders),

araneus

A common European Garden Spider, Araneus diadematus (Araneidae), on her orb-web.

Salticidae (jumping spiders),

jumper

A gorgeous Salticid. Check out those brightly coloured labidognath chelicerae! The red bits are the opposing articulating fangs.

Thomisidae (crab spiders),

A goldenrod crab spider, Misumena vatia (Thomisidae) doing her thing.

Lycosidae (wolf spiders),

wolf

A female Lycosid carrying her spiderlings on her abdomen. Some spiders have highly developed brood care!

Pholcidae (cellar spiders),

pholcid

A female cellar spider, Pholcus phalangiodes (Pholcidae) carrying her egg sac. I grew up calling these spiders daddy long legs, but that name is also sometimes used to refer to harvestmen (order Opiliones), which are non-spider arachnids.

Theridiidae (the combfooted spiders, also known as cobweb or tangle-web weavers),

widow

Female western black widow, Latrodectus hesperus (Theridiidae), on her tangle-web.

Agelenidae (funnel-web weavers),

hobo

Female hobo spider, Tegenaria agrestis (Agelenidae). Her close relatives T. domestica and T. duellica are often found in homes.

and lots of other less common/well-known ones that I intend to make posts about in due time. Although some of them don’t build webs at all, they all produce silk draglines that can be anchored to a substrate (often useful as a sort of ‘safety line’).

To sum up, the relationships and basic differences between the three suborders look like this:

phylogeny

For more about the phylogenetic relationships among the Araneae see the tree of life page.

UPDATE: I learned this morning that the in the latest phylogenies Opisthothelae is considered a suborder, with Mygalomorphae and Araneomorphae as infraorders.

*UPDATE 2: Thanks to Chris Buddle for pointing me to the latest information at the World Spider Catalog!

What do spiders and velcro have in common?

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Note: all photographs (unless otherwise indicated) are used with permission from Sean McCann.

This post was inspidered by a tweet from Chris Buddle:

Acoustic communication is common in spiders, but the vibrations are usually transmitted through a substrate, like the ground, leaves, or webs. Spiders detect substrate-borne vibrations with highly sensitive receptors on their legs. In other words, spiders don’t have ‘ears’ or hear in the way that humans do, while we are generally deaf to the sorts of acoustic communication signals they are sensitive to. As a new tweeter, I was excited that I could answer this question, having recently read a book chapter by Gabriele Uhl and Damian Elias on spider communication. They mentioned a tarantula called Theraphosa blondi, or, commonly, the Goliath Birdeating Spider (don’t worry, more about this intriguing name later) producing a defensive hissing sound like a snake. Importantly, this audible (to humans) sound occurs during communication with vertebrate predators, rather than other spiders. Recently, I read the original paper by Marshall et al. (1995) describing the mechanism of sound production by Theraphosa blondi, which will be the topic of this post.

First off, a little background on the ‘Goliath Birdeaters’. There are two species: Theraphosa blondi (or leblondi, depending where you look) and Theraphosa apophysis. I had the pleasure of meeting large females of both these species while in French Guiana doing some field work on army ants with Sean last winter.

Female Theraphosa blondi in French Guiana.

Female Theraphosa blondi in French Guiana. A quick spider anatomy lesson: spiders have two body segments – the front one with the legs is the cephalothorax (sometimes called the prosoma) and the rear one is the abdomen (or opisthosoma). In addition to 4 pairs of legs, the front-most pair of appendages are modified legs called pedipalps (sometimes just palps). Notice the hairs on the rear of the abdomen – these are the defensive urticating hairs mentioned later.

The Goliath Birdeaters live in burrows. Tarantulas (members of the family Theraphosidae) generally don't make much use of silk, but here you can see the 'doormat' that extends from the silk lining of this T. blondi's burrow. We were able to lure her out by twisting a twig around on the silk at the burrow entrance. The spider detected the vibrations from the movement, and, most likely mistaking our stick for prey, rushed out of the burrow to attack.

The Goliath Birdeaters live in burrows. Tarantulas (members of the family Theraphosidae) don’t build webs, but here you can see the silken ‘doormat’ that extends from the silk-lined burrow of this T. blondi female. We tried to lure her out by twisting a twig around on the silk mat at the burrow entrance.

The spider detected the vibrations from the movement of our stick through her legs, which are always in contact with the silk lines. Presumably we did a passable job of imitating a prey item, as she soon rushed out of the burrow to attack, biting the stick. Her fangs were impressive (about 2 cm long) but the venom of these spiders is not that potent – a bite is apparently not much worse than a wasp sting.

Female THeraphosa ___ just outside her burrow.

Female Theraphosa apophysis outside her burrow. This spider has evidently seen some rough times, having lost her last two legs on her left side.

The ‘goliath’ part of the name is appropriate: they are extremely large.

A Theraphosa blondi female next to a woman's hand for scale.

A Theraphosa blondi female next to a woman’s hand for scale.

As for ‘birdeater’, like most spiders, they mainly prey on insects and other arthropods. They have also been reported to take juvenile toads, skinks, snakes, mice and earthworms, but rarely birds*.

Spiders have predators themselves, which is where defense mechanisms come in handy. Tarantulas in the New World employ urticating hairs in defense against predators such as small mammals. These barbed bristles on the spider’s abdomen are brushed off with the last pair of legs in the direction of an attacker and can result in severe irritation of the skin and mucosa. Coatis (members of the raccoon family) prey on tarantulas and apparently use tactics that allow them to avoid being injured by their prey’s urticating hairs.

White-nosed coati (a relative of raccoons in the family Procyonidae). These guys like to eat tarantulas.

White-nosed coati (a relative of raccoons in the family Procyonidae). These guys like to eat tarantulas. (Photo courtesy Adam Blake)

Coatis have a severe reaction to the hairs of Theraphosa blondi, however, and seem to recognize and avoid them. The authors of the paper suggest that the hissing sound the spiders produce is an acoustic aposematic (warning) signal that works in combination with the urticating hairs to provide an effective defense against vertebrate predators. The point of their study was to figure out exactly how these giant spiders hiss.

When the researchers looked closely**, they found that the spiders have many plumose setae (tiny hooked hairs) on the femora of their pedipalps and first two pairs of legs. When threatened, Goliath Birdeaters rear up and rub these leg and pedipalp segments together.

Theraphosa ____. The arrow indicates the femur of the right first leg. THe plumose setae referred to in the paper are on this leg segment in and the femora of the pedipalps and second pair of legs as well.

Theraphosa apophysis. The arrow indicates the femur of the right first leg. The plumose setae referred to in the paper are on this leg segment as well as on the femora of the pedipalps and second pair of legs.

Experimentally removing the setae completely silenced the spiders during their threat displays. Sequentially removing more and more of the hairs caused the amplitude of the hissing sound to decrease incrementally, but the frequency remained the same. Using dead or anaesthetized spiders, it was possible to produce pretty much the same sound by rubbing the legs together the way the spider would. The authors concluded:

“The mechanism of sound production is apparently the entanglement of the terminal hooks of one seta with the filaments of the plumose setae on the opposing leg surface. This produces sound in a similar way (and with similar effect) that hook-and-loop fabric closures (marketed as ‎Velcro) do during opening.”

So basically, although Goliath Birdeaters don’t really eat all that many birds, they have a nifty trick for avoiding being eaten themselves. They use a velcro-like technology to make a hissing sound that warns potential predators that they are dangerous and painful to attack. Pretty awesome.

 

*I haven’t been able to track down any references for this, but I have read in a few places that the original species description for Theraphosa leblondi included a record of the spider having taken a hummingbird.

**The figures in the original article Marshall et al. 1995 (paywalled) include close-up images of theses structures. For (non-paywalled) images of stridulatory setae in another Theraphosid see Pérez-Miles et al. 2005.