Pirate spider eyespots?

Wolf Pirate Spiders (likely Pirata piraticus, but there is a similar species, P. tenuitarsis) are one of my favourite spiders, their existence in the boundary of water and land, and their ability to walk and run on water makes them fascinating. A few days ago at the wildlife garden, I discovered a curious fact about them while looking at a photo of a female carrying an egg sac. The female was lodged at an angle on some leaves and I did a double take: it gave me the impression that the abdomen of the spider was in fact, its face. This impression was due to two paired white spots on the female's abdomen looking like eyes. Instead of a spider facing away with her egg sac attached to its abdomen, it looked like a spider looking forward, while carrying its egg sac on its jaws, in the way of nursery web spiders. Pirate spider eyespots? Wolf pirate spiders have paired line of white spots on their abdomen, so I wondered if it was just this particular individual that casually had the spots in the shape and area to give this impression. I checked my photos of this spider and found at least two others with the same spots, one also carrying an egg sac. I also found other photos on the web of this species with the same abdominal spots.

Another Pirata sp with egg sac and 'eyespots' 22/07/2014, same habitat

For comparison, a female nursery web spider carrying her egg sac with her chelicerae.

 Only photos taken in a particular angle, of the spider facing away show this, and I guess everybody prefers a front shot of a spider, so I think this pattern is probably found in the species at least regularly, and not only in the females, this side view of the spider allows to see the larger spot towards the end of the line of spots in a male

24/05/2014

A frontal view of the same male showing his enlarge palps:

Have these spots evolved due to them giving an impression of eyes to visual predators, as the eyespots found in some caterpillars and butterflies? In some cases eyespots function to startle a predator giving the impression of a different, larger animal (like the elephant moth caterpillar, the peacock butterfly or this amazing tropical caterpillar), instead, in the wolf pirate spider the eyespots would work like those found at the rear end of some fishes and butterflies, whose function might be to trick or confuse a predator as to where the head of the animal actually is. In fact, eyespots are not unheard of in spiders.

 Why would this be beneficial to this spider? What follows is only speculation, but apparently, wolf pirate spiders live in retreats in moss at the shore of ponds, and females carrying egg sacs often expose the egg sac to the sun at the retreat entrance, while the female remains inside. This could put the female in danger of predation, as she would be less able to detect danger, so the eyespots could afford some protection to the mother and its offspring to be, but I am not aware of any research into the evolution of these eyespots.

With thanks to Catherine Scott (@cataranea) for discussing this on twitter before I wrote the post.

Losing old legs and growing new ones

I see lots of Philodromus spiders with missing legs, some of them with up four legs missing. They are - incredibly - able to walk, and presumably find enough food to stay alive. Many spider species have weak points in their legs, when in danger of being predated or otherwise attacked, they shed them, a phenomenom called autotomy. Spider autotomy has actually been shown to be a voluntary act, as anesthetised spiders would not shed their legs. For a spider, it is costly to lose a leg, as it might impair reproductive or fighting ability, or success at hunting, but it is a small price to pay when the alternative is to be eaten. And the best thing is that sometimes legs are not lost forever, as immature spiders maintain the ability to regenerate lost limbs in the next moult  (although long lived spiders that moult when adult, like tarantulas, do keep that ability for life). The spider on the top shot, enjoying a juicy aphid a few days ago, has regenerated the middle pair of legs on the foreground: notice that they are thinner and shorter than the rest, and lack the colour pattern seen on the equivalent legs on the other side. Even in the Philodromus below, which has lost four legs and a palp, the apparent stumps of the missing legs are actually the miniature folded regenerated legs.

Chirping lily beetles

The sun shone in all its glory to end this most rainy April. Many insects came out of their temporary hiding places to dry out and enjoy the warmth. Some of these were Scarlet Lily Beetles. I wasn't sure if I had an infestation, as I had collected just a couple of adults in the last few weeks, but today I found 12, the first ones were a mating couple. As I found them I placed them in a plastic pot, and while I was carrying it I noticed a faint chirping call. I thought that there must be a nest nearby with calling chicks, but then I realized that the sound was actually coming from the pot: the disturbed Lily beetles were stridulating! when I touched them, they chirped repeatedly. You can watch this short clip of them in the pot, as I push them inside the pot, they chirp - I was trying to place the camera on the pot opening to improve the sound recording, but they kept climbing up the pot.



The first description of the stridulation of this beetle was written by the early entomologist René Antoine Ferchault de Réaumur in 1737:

when one holds it, it lets a little cry be heard, produced by the friction of its last abdominal segments against the elytra, the more one presses the elytra against the body, the louder it cries

More recent studies have confirmed this description, and also shown that stridulation is common in the Lily Beetle subfamily (Criocerinae). The stridulatory apparatus consists on a file on the last tergite - the dorsal end of the abdomen - made of microscopic parallel ribs, which are scraped by files of sharp denticles in the underside margins of the elytra. The sound is produced while the abdomen contracts, and these contractions can be amazingly rapid, up to 200 times per minute and is loud enough to be heard if the beetles are less than 30 cm from your ear. The high variability of the chirps and the situations in which they are produced suggest that this behaviour is a defence mechanism: the beetle will chirp if captured and the sound can startle the potential predator to release the beetle before swallowing it. In other beetle species chirping is used in intraspecific communication, with the lily beetle, is is yet another way of avoiding being eaten.

More information
Michael Schmitt & Dieter Traue. 1990. Morphological and Bioacoustic Aspects oî Stridulation in Criocerinae (Coleóptera, Chrysomelidae). Zool. Anz, 1990, 225: 225-240.

Why are some hoverflies poor mimics?

Merodon equestris, the Narcissus fly, a bumblebee mimic

Eristalis tenax, a dronefly (top left) and honeybee

Volucella zonaria, a large and colourful hoverfly that is an excellent mimic of the european hornet Vespa crabro

Helophilus, a wasp mimic 

 Sericomia silentis, a wasp mimic

The photos above illustrate that hoverflies are amongst the best examples of mimicry. Although harmless, their colours, patterns, level of hairiness, and detailed morphological and behavioural features often matches species of bees, bumblebees and wasps, making them such wonderful impostors that they fool people into thinking they really are stinging bees or wasps. At close range, anybody can learn to tell mimics and models apart (the shape and size of the antenna is a giveaway). But the fantastic mimicry of hoverflies is shown by the repeated identification failures of natural history photographers, and even specialised editors (a book cover on bees featuring a hoverfly). These are evident when you have a look at many natural history photography websites. As an example I googled "wasp flower" and the first hit was a hoverfly.

The selective pressure for mimicry is predation. Many birds are consummate fly predators, but they will avoid bees and wasps. Although birds could benefit nutritionally from preying upon these succulent, soft flies there is a heavy cost to pay if they get it wrong: a painful and possibly debilitating sting. Given this, shouldn’t natural selection perfect mimicry? Why are there some hoverflies that only have a vague resemblance to bees and wasps?
 Here is an example:

Syritta pipiens, an example of a poor mimic

 There had been many hypotheses put forward to explain why there are poor mimics:

1. 'Eye of the beholder': Imperfect mimics are only imperfect to the human eye, they are really much better mimics to bird eyes. The poor resemblance would be a reflection of our own perception bias.
2. 'Multimodel' Maybe mimics could be safer when imitating roughly several models.
3. 'Kin selection' Flies that are abundant might be surrounded by relatives, and kin selection might have selected for these imperfect mimics.
4. 'Trade offs' mimetic perfection cound be trading off with camouflage ability, or thermoregulation.
5. 'Constraints' mimicry could be limited by developmental or phylogenetic constraints.
6. 'Relaxed selection': small hoverflies – which are less profitable to eat – could have lower predation even if they are poor mimics, which will mean that natural selection for improved mimicry will be weaker.

Heather Penney and co-authors tested these hypotheses using a large set of European hoverfly species. They obtained morphological data and human volunteer rankings of mimicry fidelity to bee, bumblebee and wasp models and phylogenetic data to test these hypotheses.

First, they carried out a detailed morphological analysis on a large set of hoverlfy species which shows that human perception of mimicry fidelity indeed corresponds to objective assessments of similarity between mimic and model based on their morphological analysis. This rules out the 'eye of the beholder hypothesis" and also the 'multimodel' as poor mimics did not fall in between different potential models.

They also performed a meta-analysis showing that poor mimics were not more abundant than accurate mimics and therefore rules out the importance of kin selection in the evolution of imperfect mimicry.

The constraints hypothesis, they did not explicitly test even when they had phylogenetic data to evaluate the importance of phylogeny as a constraint.

The core result of the paper was that the degree of fidelity to the model is strongly correlated with hoverfly body size even when correcting for phylogenetic relationships, as shown in their figure:

Relationship between an estimate of body size and human ratings of mimetic fidelity (fHR). Lines 

show the fitted linear regressions. Filled triangles, wasp mimics; open triangles, bee mimics; filled circle, the non-mimetic syrphid Cheilosia vernalis (from Penney et al 2012)

As the benefit of predating a hoverfly (a meal for the bird) is directly related to the size of the fly, while the cost of error should be constant, the higher risk of predation when the hoverfly is large imposes a higher selective pressure to be a good mimic. Therefore, a hoverfly doesn’t need to be a good mimic if it is small, as the benefit of eating a small fly for a bird is too insignificant to risk the potential cost, therefore resulting in a lower predation pressure for small hoverflies. Birds will err on the side of caution and avoid even the poor mimics when they are small. The other way round: Large hoverflies provide a bigger benefit, so the predator might risk being stung and therefore they have been selected for more precise mimicry. 

Although the results are solid and the hypothesis makes intuitive sense, I found two problems with their design: (1) the limited choice of models and (2) the geographically biased choice of some models, both of them resulting in an underestimation of the degree of mimicry of some hoverflies.

First, not all potential models or even model types were available and this will create an alternative explanation for the evolution of "poor" mimicry, if you can't compare the mimic with its model, they it will by necessity result in a poor mimic. There are hundreds of European species of bees, wasps and bumblebees with a broad range of colours and patterns, but they only used ten. Syritta pipiens, the little hoverfly shown above was rated as a poor mimic in their study, but who says it doesn't mimic a small solitary wasp or bee not included as a model?
In addition, of the three bumblebee species they included two were American bumblebees (B. affinis and B. impatiens), which seemed strange given that their hoverfly sample was European. A single European bumblebee, B. lucorum was included. Given that bumblebees differ extensively in coat colour, this might create biases in the evaluation of mimicry fidelity in bumblebee mimics: they cannot be regarded as excellent mimics if their models are not available for comparison. This is likely to have caused a bias in the evaluation of, for example, the bumblebee mimic Merodon equestris, the Narcissus fly, also illustrated above, which is highly polymorphic for coat colour pattern and mimicks different bumblebee species. They included just a single colour form of this hoverfly, which imitates the all-brown Carder Bee B. pascuorum, but not a single all-brown bumblebee was used as a model. This predictably resulted in (1) the misclassification of M. equestris as a honeybee mimic and (2) his rating as a poor mimic, when this species is in fact a fantastic bumblebee mimic which has tricked me in more than one occasion.
   I wonder up to what point the narrow selection of hymenoptera could result in the assessment of many hoverflies as poorer mimics than they really are. We might not really know some hoverfly species are really imitating because the models they mimic might not relevant to us such as large bees and wasps are.
 Although I think they are valid concerns, I don't think the conclusions of this paper would be affected, but they might have ever got stronger results if their model choice had been wider.

More information

Penney, H., Hassall, C., Skevington, J., Abbott, K., & Sherratt, T. (2012). A comparative analysis of the evolution of imperfect mimicry Nature, 483 (7390), 461-464 DOI: 10.1038/nature10961

Do spiders find ladybirds distasteful?

 I witnessed a curious interaction today. A 7 spot ladybird was walking up a wall, when a sudden movement caught my eye. It was a large spider, a female Amaurobius similis that had dashed out of her burrow in a hole in the wall, probably alerted by the pull of one of the silk threads that radiate from her burrow. She had caught the ladybird by one leg. The ladybird struggled to free itself, but she need not fight much. After a few moments, the spider released her grip, turned round and retreated into her burrow. The spider obviously had assessed the ladybird and regarded it not suitable for a meal. I doubt it was due to the ladybird size or strength, as Amaurobius are powerful spiders, able to subdue large flying insects such as droneflies and honeybees. The other possibility is that the spider has tasted the alkaloid rich liquid that constitutes ladybirds chemical defence mechanism and that is released from their leg joints when alarmed (the 'blood reflex'). I have previously seen dead ladybirds wrapped on silk caught on the webs of two spider species (garden spiders Araneus diadematus and the false widow Steatoda bipunctata). Indeed, field surveys and experiments carried out by John Sloggett showed that A. diadematus does trap and consume ladybirds, and is apparently immune to the toxic effects of ladybird's chemical defences. In contrast, other spider species do seem to find ladybirds distasteful, so this is a strong possibility for Amaurobius.

Another view of the interaction, not as sharp, but it shows clearly how the spider's chelicerae are pulling and lifting the ladybird's front right leg.

For other spiders, however, ladybirds are not even considered a food item. Take this little wolf spider, enjoying the company of the 7 spot ladybird a few days ago. Both individuals were sunbathing next to each other most of the morning. The spider popped in and out, paying no attention whatsoever to the ladybird.

More information

Sloggett, J. (2010). Predation of ladybird beetles by the orb-web spider Araneus diadematus BioControl, 55 (5), 631-638 DOI: 10.1007/s10526-010-9291-0

Dropping aphids and their alarm pheromones

Fortunately for the organic gardener, aphids have many predators: hoverfly larvae, lacewings, ladybirds, shield bugs and spiders eat them in numbers. Although aphids appear defenceless against their predators, they have evolved a suite of antipredator responses. Some aphids have warning coloration and sequester chemicals from their feeding plants that are distasteful or toxic to their predators, other release toxic chemicals or waxes and a few have a hard-skinned soldier caste to defend the colony, yet others maintain an army of ants that defend them. The most common form of defence - both against predators or parasitoids - is however, behavioural: the aphids move away or drop from the leaf they are feeding on when they sense an approaching predator.
 Dropping is very effective in reducing immediate risk: aphids fall away from the approaching danger onto the ground. Once there other costs become apparent: the aphid may be far from the host plant and is exposed to ground predators or to desiccation.
 The orange tree in my conservatory is infested with aphids. I took advantage of the abundance of 7 spot ladybirds in the garden and brought a few onto the tree, placing them on particularly infested branches. I was pleasantly surprised by the eagerness with which the ladybirds took to the intended job. They started munching aphids straight away, clearing whole shoots in a few minutes. After a little observation, however, it became apparent that it was the aphid's behaviour which was mostly responsible for the shoots being cleared. The undisturbed aphids sat motionless, on a living carpet feeding on the tender leaf sap nearby. In contrast, as soon as a ladybird attacked, the aphids on the same leaf came alive and some started to move away, going into another leaf, while many aphids dropped to the ground as the ladybird fed on their unfortunate siblings. The following two photos illustrate this. They were taken about 27 seconds apart. In the first one, notice the three aphids on the tip of the leaf. In the second photo, these aphids have dropped to the ground, leaving just a couple of aphid molts stuck to the leaf tip, while the ladybird is still feeding on an aphid, motionless.

 Ladybirds are very effective at eliciting the drop response from aphids, especially when compared to smaller, less energetic feeders, as demonstrated in experiments by John Losey and Robert Denno on pea aphids feeding on alfalfa exposed to a predator insect.

This means that on average 60% of aphids feeding on a plant stem dropped to the ground when a 7 spot ladybird (Coccinella septempunctata) was introduced, in sharp contrast to the lower dropping response to the bugs and the control. Given the higher mortality of aphids on the ground, it follows that ladybirds would be very effective clearing aphid infestations through direct predation, and their indirect effect on aphids dropping from the plant.
 What mechanisms are responsible for this dropping behaviour? or, put differently, how do aphids sense that a predator is approaching? Dropping behaviour happens in response to predator contact, vibrations generated by the predator, or in response to an alarm pheromone secreted by individual aphids when attacked. This chemical signal, (E)-ß-farnesene (EBF), is secreted in dropplets by the cornicles, little tubes at the rear of the aphid, and they may impregnate the predator, which in its next move will elicit the dropping response before actually attacking another aphid.
 The release of an alarm pheromone by an individual that is likely to be eaten by a predator seems paradoxical. What benefit can this individual gain from its production? An alarm pheromone can be adaptive when the benefit is shared by relatives. This is indeed the case in aphids: groups of aphids feeding in close contact are likely to be members of the same clone, that is, they are genetically identical, as aphids often reproduce parthenogenetically. The alarm pheromone also has longer lasting effects benefiting the individual relatives, as the aphids that have been exposed to the chemical tend to produce winged offspring, which will likely disperse away from predators, in the case of the ladybird attacker, they will be likely to avoid the following generation of ladybird larvae.

References
LOSEY, J., & DENNO, R. (1998). The escape response of pea aphids to foliar-foraging predators: factors affecting dropping behaviour. Ecological Entomology, 23 (1), 53-61 DOI: 10.1046/j.1365-2311.1998.00102.x
Schwartzberg, E., Kunert, G., Stephan, C., David, A., Röse, U., Gershenzon, J., Boland, W. & Weisser, W. (2007). Real-Time Analysis of Alarm Pheromone Emission by the Pea Aphid (Acyrthosiphon pisum) Under Predation. Journal of Chemical Ecology, 34 (1), 76-81 DOI: 10.1007/s10886-007-9397-8

Scary peacock butterflies

Butterflies have high predation rates by birds. I am sure most of you have come across a butterfly with damaged wings suggestive of a beak 'bite' mark. Long-lived butterfly species often rely on camouflage (crypsis) to avoid being attacked in the first place. The Comma, the Small Tortoiseshell and the Peacock are some of these, mimicking shriveled leaves. They remain immobile if resting, with their wings closed. The Peacock (Inachis io) has a second defense mechanism. If discovered, they suddenly flash their wings open, exposing four large eyespots they also may flick their wings repeatedly and at the same time they make a hissing noise and a series of inaudible clicks by rubbing two wing veins together, during this display, they continually adjust the tilt of their bodies to face the potential attacker.

This Peacock was feeding upside down on a Buddleia showing its eyespots

 This intimidating display was described over a century ago and its effect on predators noted, but experimental support for its effects on the survival of the butterflies themselves was lacking until very recently. Adrian Vallin and collaborators tested the effect of eyespots, stridulation and both combined by modifying captive-reared peacock butterflies experimentally. They removed the eyespots by painting over them with a black marker pen and removed the stridulation ability of the butterflies by cutting out the veins responsible for making the hissing noise. They also tested the effect of the combined factors, that is removing both the eyespots and the noise-making wing veins. Unmodified controls, and controls in which a similar area of wing was painted black without touching the eyespots or cut without affecting the ability to make noise were also tested (bottom row below).

The researchers recorded the effect these various treatments had on survival of peacocks upon exposure to a potential predator, blue tits (Cyanistes caeruleus), a small insectivorous bird. The results show conclusively that butterflies without eyespots are more likely to be predated by the blue tits. All except one butterfly with intact eyespots survived by scaring the blue tit away, showing how effective the eyespots are in intimidating the bird. The effects of the sound or the combined effect were not significant. The predated butterflies were readily eaten by the birds, indicating that the Peacock is not distasteful and supporting the view that, in the words of the researchers, 'a harmless prey can increase its fitness by survival through the adoption of intimidation by bluffing'.
References: 
Vallin, A., S. Jakobsson, J. Lind & C. Wiklund (2005) Prey survival by predator intimidation: an experimental study of peacock butterfly defence against blue tits. Proc. R. Soc. B. 272:1203-1207.

Ruxton G.D. (2005) Intimidating butterflies. Trends in Ecology and Evolution 20: 276-278.