Budapest slug mating

It's the last day of October: damp, windy and mild. As I go out into the garden, pondering upon the impending winter lockdown, I find two Budapest slugs circling on a cherry leaf on the ground. Budapest slugs remind me of hedgehog poo, dark and shiny and all the right shape. If they had been on the path pebbles I would have easily missed them. I watch them for a few minutes. They keep slowly circling, head-to-tail for a while as they follow each other's mucus trails. This is slug courtship and it happens at slug pace. It's 10:40 and it doesn't look like much is happening any time soon. I regularly go out to check on them for the rest of morning and afternoon. As I'm typing this, I grab a torch and decide to check on them again. They are still there, exactly in the same position as 3 hours ago. 

10:42

11:06. The pair have moved onto the path pebbles now, the circling has stopped. They are now finding each others genital openings at the right side of their heads.

11:20. Copulation proper appears to start.

12:20

14:31

17:20. Very little change in the last few hours. The slugs are now entwined and practically immobile.

I pick the Slugs of Britain and Ireland and check the species account for info on their mating behaviour. Of note is that they are mainly subterranean and active year round.

This quote is fitting: 

"in winter adults are often found almost motionless, mating. Mating lasts many hours and involves the production of elaborate spermatophores"

I wonder if they'll be there tomorrow.

More information

Rowson, Ben, James Turner, Roy Andreson and Bill Symondson Slugs of Britain and Ireland. 2014. FSC Publications. AIDGAP.

Migrant hawkers scramble competition

I'm used to watching migrant hawkers foraging over gardens, leafy streets and sheltered woodland rides, some times in groups. They are immature individuals, gathering energy away from water. Migrant Hawkers, unlike other hawkers, mature slowly, and will move to suitable breeding sites after their long immature period. During this past week I've watched them in their breeding sites in lakes and drains, where mating and egg-laying takes place.

A mature male rests briefly between bouts of searching (Pickering Park, 27th August) 

Males at the breeding site 
At one of my local parks (Pickering Park) last week, dozens of Migrant Hawkers sat or patrolled alongside marginal vegetation around the lake. The males, now fully mature and showing their bright blue spots and eyes and side yellow-green stripes often hovered in a spot, or explored the vegetation, flying well into it, searching for females.

A typical hovering male in a clearing at the marginal vegetation (Pickering Park, 27th August), offering them good views.

Mating
I saw no females, until one was captured by a male: no preliminary or courtship, the male just tackled her and positioned himself to grab her by the head. The female is then able to curve her abdomen and mate, retrieving sperm from the male's secondary genitalia at the base of the abdomen, forming the 'wheel position'. They may fly in wheel position very fast, zigzagging alongside the marginal vegetation edge or briefly rising into the air, before settling on vegetation (above).

Ovipositing female (Foredyke Stream, 1st September)

The moment when the male passes by, and sees the female.

The pair, mating.

Oviposition
A couple of days ago I watched a patrolling male on a ditch doing its usual patrolling routine, rising to inspect any passing individual, even paying attention - briefly rising - to birds flying over. A mated female arrived, unnoticed, and started laying eggs on live leaves well above the water line, I'd say over one metre over the water. She checked leaves and unsheathing her ovipositor, started laying into them (the eggs will overwinter inside the plant leaves, where they are protected from predation). After a couple of minutes, the male noticed her, tackled her and mating ensued. This time the pair settled briefly on plants, which allowed me to take a shot (above). Mating in Migrant Hawkers is longer than in other territorial relatives.

Two males resting near each other (Pickering Park, 27th August)

Nonterritorial males
This species is notoriously non-aggressive, even at the breeding sites. Males will even rest within view from each other (above). A patrolling male will swiftly rise to check a passing one, but the interaction is suggestive of them 'checking' that they are not a female, and letting the other individual go their way if it's a male. There is no defended territory, just males congregating on suitable ovipositing sites and searching for females, a type of mating tactic called 'scramble competition'. This appears to be the reason behind the long copulation. A territorial male mating for a long time may lose the territory to an invader, or miss extra mating opportunities. A nonterritorial male has less to lose, and therefore makes sure that he fertilises as many as possible of the females' eggs, possibly by taking time to remove any previous sperm before transferring his transfer. These patterns have been shown to stand when the copulation duration of territorial and nonterritorial drogonfly species were compared, but I haven't found specific data on the Migrant Hawker. To illustrate the pattern, the Emperor, a territorial species, copulates for an average of 10 min, while the Common Hawker, a non-territorial one, copulates for an average of 67 min. Of course, this lengthy copulation is not necessarily to the benefit of the female, who may be already mated, as the female already laying eggs, and therefore this sets the stage for the evolution of female counter-tactics, such as visiting the water as little as possible and avoiding males if they can, something I have covered before at Bugblog.

More information
Córdoba-Aguilar, A., Serrano-Meneses, M. A. and Cordero-Rivera, A. Copulation Duration in Nonterritorial Odonate Species Lasts Longer than in Territorial Species. Ann. Entomol. Soc. Am. 102, 694–701 (2009).

How do female dragonflies avoid male harassment?

After egg laying, female damselflies and dragonflies can be exposed to males trying to mate. Females will then be unreceptive and in order to avoid a lengthly and potentially costly copulation, they have evolved different strategies to avoid male harassment. These are only some of these strategies:

1) Avoiding water. This strategy appears to be quite general in the group. Males will return to the breeding ponds first after they mature and will be very obvious as they spend a lot of time patrolling the pond or sat on prominent perches, lake or river or hanging around near the water. In contrast, females often stay well away from the water, only returning to the breeding site to mate and oviposit. Staying away from the water allows females some control about when to mate.

2) Sneaking in. Females can be quite secretive when approaching an oviposition site, or they may lay during cloudy or cold weather - especially the larger species which can generate heat by whirring their flight muscles. Males are more likely to be roosting during dull weather or early in the morning, so females might be able to oviposit uninterrupted if they time their visit to the pond well.

3) Adopting an oviposition posture. If a male flies overhead, a female may try and repel him curving her abdomen down, like she was ovipositing. A great photo showing this behaviour in an Emperor female is here.

4) Looping the loop. Female dragonflies can fly faster than a chasing male, or do a loop the loop or even dive under water to avoid harassing males!

5) Androchromes. In many damselflies, such as the Blue-tailed and the Common Blue damselflies there is genetic variation in female colour with some of the colour forms strongly resembling males. I have covered this topic recently in Blue-tailed Damselflies.

A female Emperor with a very blue abdomen (16/07/2018). 

6) Age-related male mimicry? Females have an ability to store sperm and the sperm from a single mating should be enough to fertilise all her eggs for two weeks. In some species of dragonflies, females change as they age to resemble males (e.g. Emperor, Common Darter). The abdomen of mature female emperors is green, but it may turn blue - like a male's- when they are about 2 weeks old (it is unclear, however, it this is a purely age effect or a temperature response to warmer weather as the season progresses). If this was age-related, then male mimicry might reflect a different evolutionary response to the same selective factor than the genetic androchromes. When the female is young it is in her interest to attract males and mate, but as she ages she is likely to have already mated and the colour change might make it easier to avoid male attention. More research is definitely needed!

7) Playing dead. One of the most striking strategy of male avoidance is that of the Common (or Moorland) Hawker Aeshna cyanea (top shot). Ovipositing females often chose sheltered spots with denser vegetation in ponds to avoid male detection. As females leave ponds after ovipositing, males chase them. Rassim Kheliffa carefully documented that in such occasions, females dived into the tall grass surrounding the pond, staying motionless, often upside down, and so avoiding being grabbed by the males. The females were alert and responsive, and 87% (out of 31 attempts) where able to successfully avoid being picked by Rassim. He hypothesised that death feigning has evolved by females co-opting a pre-existing antipredator behaviour into a male avoidance strategy to avoid undesired mating attempts

More information
Corbet, P. S. The Life-History of the Emperor Dragonfly Anax imperator Leach (Odonata: Aeshnidae). J. Anim. Ecol. 26, 1–69 (1957).
Khelifa, R. Faking death to avoid male coercion: extreme sexual conflict resolution in a dragonfly. Ecology 98, 1724–1726 (2017).

Credit: Top photo of Common Hawker by Robert, used with permission.

Female polymorphism in blue-tailed Damselflies

It's 30 days wild! I am joining again this June, trying to see, record and find out about as much wildlife as I can - and reviving BugBlog, which has been dormant far too long. I will make a especial effort with dragonflies and damselflies, writing a post on each species I see, but I will also be blogging in my other blogs Wild about Hull and The Rattling Crow.
 Adult dragonflies and damselflies tend to be active in warm weather. Today it was a warm, but cloudy and humid day with a few brief sunny spells. I went to Oak Road Lake to try and see some. This site is well known by odonatologists (yes, that is the name for people who study damselflies and dragonflies, which are a group called Odonata) in Yorkshire as the northernmost site for the Small Red-eye Damselfly in 2006. Thirteen species have been recorded at the site.
 I walked around the lake and there was not much activity, probably due to the weather. On the northern site I found a few Blue-tailed Damselflies, a common and widespread species that is often active in this kind of weather. This species is interesting as the females come in a wide array of colour morphs, one of the morphs has the looks of a male: blue and black. The colour pattern changes also markedly by age, but adult females can be either looking like a male or more brownish green, although in the process they can look pink or purple. Why would females look like males? won't males get confused? This actually appears to be the reason behind the females attire: male mimicry to deceive males! Males actually were more attracted to the brown females than to the blue ones. Females look like males because they are more likely to be left alone, and not harassed by males into further matings. Mating is very long in the species, usually 3-4, but up to 8 hours (which is why it is relatively easy to observe). In addition, females only need to mate once to fertilise all their eggs. Therefore, females could benefit from avoiding unnecessary long matings as they could use that time feeding to produce more eggs, and possibly being less exposed to predation when mating as well. Experiments showed that androchrome females were often found alone, while the other female morphs were more frequently found mating. Further, androchrome females had less sperm in their storage organs and some ended up not mating at all. Another hypothesis, which might not be exclusive, is that when males are very common in comparison to females it pays to look like a male to avoid frequent mating attempts, while when the sex ratio is more even then the androchromes may not benefit as much as they might not be able to mate at all.

 Androchromes trick me as well, but you can see in the top shot that when you find a pair mating the male and the female look the same (top shot, 21/07/2012 at Tophill Low). I only found a mating pair today, on the grass, and the female was brownish/green (below).

The following photos show some of the various colour morphs of Blue-tailed Damselflies

This is female form violacea, which matures into an androchrome. 

This is female form rufescens, which matures into a pale brown form 

This is the olive green form infuscans.

A male or a female androchrome?

More information

Cordero, A., Carbone, S. & Utzeri, C. Mating opportunities and mating costs are reduced in androchrome female damselflies, Ischnura elegans (Odonata). Anim. Behav. 55, 185–197 (1998).

Why do male Wool-carder bees defend a flower patch?

I found the first male Wool Carder Bee, Anthidium manicatum of the year in the garden today, patrolling and basking on the large sage patch that is a favourite if many species of bee. If you have a flower-rich garden with a sunny aspect, chances are that in warm, sunny summer days you will see this chunky bee attacking other flower visitors, including large bumblebees. Male bees from most bee species often just hang around nests where they can mate as females emerge, or patrol flowers favoured by females. Occasionally they 'jump' onto or chase other bees or insects, possibly checking if they are females. For example, Male Hairy-footed flower bees, Anthophora plumipes, who emerge a week or so before females, will jump onto bluebottles, the only insect that roughly resemble the black females of his species. No other male bee is as aggressive actively defending a patch of flowers as Wool carder bees. They even have sharp spines at the end of their abdomen with they can use to harm, or even kill, other bees, so they rapidly become the only bees using the flowers

The abdominal spines of male Wool carder bees

 Most female bees mate once shortly after emergence, so males only had a chance of mating successfully early in the season. Females store the sperm of this early mating and use it to fertilise their eggs throughout the nesting season. Females will repel or avoid courting males vigorously once they've been mated. In contrast, Wool-carder bees are unusual in that females both mate multiple times and accept matings throughout their flight season. Witnessing solitary bees mating is quite rare, but with Wool carder bees, matings are quite frequent. Many females visiting a defended flower patch will mate with the resident male. The male defending a good flower patch will likely gain many matings with several visiting females, but, given what we know about sperm usage in solitary bees, will he benefit from fathering the female's offspring?

Mating Wool carder bees

 In a recent study, Kathrin Lampert and colleagues from Ruhr-University Bochum carried out some experiments to investigate why Wool Carder bee mating behaviour is so different from other bees. They in particular were interested in testing the hypothesis that Wool-carder bees might show what is known as 'late male sperm preference' in which the last male mating with a female has a disproportionally higher chance of fathering the females offspring.
 To find out 'who is the daddy' they used genetic testing in a similar way to how paternity is tested in humans, using genetic markers that have many variants, and therefore are likely to be different between individuals. In order to be able to capture the likely mothers and fathers of particular nests they constructed large flight cages containing Betony plants (for pollen and nectar) and Stachys byzantina (for plant wool, which the females collect to line their nest cells). Wool carder bees nest readily in sections of bamboo sticks, and they fixed artificial nesting sites inside the flight cages. Offspring of a female are found in a linear nest in consecutive order, the deeper cells in the bamboo stick contain the earlier laid eggs, while the cells closer to the entrance contain the later brood, which is likely to be male offspring. They carried out three experiments, in the first one, to test the feasibility of these experiments wild males and females (likely to have mated before) were captured, individually labelled with a dot of paint in the thorax, and released in the flight cage. In the second experiment, males in the cage were swapped to test if males with later access to females would father offspring. In the third experiment males were removed after a few days and females left to nest with no males, to investigate if females are able to store sperm. After the females had completed their nests in all the experiments, DNA samples were taken from the males and females, and them and the offspring found in the artificial nests screened for genetic paternity analyses.
A problem with their experiment were cleptoparasitic wasps, which destroyed the bee larvae and prevented genotyping. Another problem, which stems from bee's sex determination system, is that only female offspring have a dad: males develop from unfertilised eggs, so they only have a mum. They could only find out if offspring were male or female after genetic screening. Despite this, they obtained a number of female offspring from many females.
 The results revealed that the males flying with females at the time the females were provisioning a cell, where they are close to laying the egg, were the most likely fathers of the offspring (84% of the time), whereas most of the remaining fathers were males present in the cage in previous days, supporting the hypothesis of late male sperm preference. Males that were dominant, that is, chased away other males from flowers, tended to father more offspring, as most matings happened on flowers.
 The male removal experiment showed that females were able to store sperm for at least 11 days, and possibly much longer.
 This research suggests that a predisposition for late male sperm precedence in the ancestors of wool carder bees might have been what favoured the aggressive territorial behaviour seen in males, as they can benefit from monopolising floral resources visited by females.

More information
Lampert, K. P., Pasternak, V., Brand, P., Tollrian, R., Leese, F., & Eltz, T. (2014). ‘Late’male sperm precedence in polyandrous wool-carder bees and the evolution of male resource defence in Hymenoptera. Animal Behaviour, 90, 211-217.

Tetragnathidae: stretch spiders or long-jawed orb weavers

This is a large world family, with only 14 British species. Most build orb webs and sit in the middle, instead of having a signal thread and a retreat as in typical orb weavers (Araneae). Tetragnatha are very elongated spiders with slender bodies and long legs, except the third pair, which is short and often hold the spider to stems and grasses while the remaining pairs are stretched forward and back. When disturbed, they run out of their web and stretch themselves along leaves or stems. Some species have a preference for damp places and one of them Meta menardi, lives in caves and other dark places. One of the genera, Pachygnatha, does not build webs when adults.

The locking of the jaws

Males and females have extremely long chelicers furnished with internal spines. Males have two pair of additional large and spines protruding from the inside and outside of his chelicers. These spines lock the female's chelicers open during mating. The male's palps are also very long. For a video of a mating pair of Tetragnatha click here and for a fantastic post by Catherine Scott with observations of mating and male competition click here.

Tetragnatha extensa on resting posture on a leaf over the pond water.

Tetragnatha extensa turning on a leaf allowing to see her chelicers.

Tetragnatha extensa on her web over a pond

Female Metellina sp. on her web. Metellina females are quite plump and don't have particularly long legs.

Male Metellina guarding a female's web. Unlike the female, he is slender and looks more similar to Tetragnatha. He will wait until a female catches an insect to mate. For more information on this species mating strategy see this post at Bugblog.

Pisauridae: Nursery web spiders

This is one of my favourite spider families, which displays a treasure trove of fascinating natural history. The family has just three medium size or large species in the UK, a terrestrial wandering hunter, Pisaura mirabilis, commonly known as the nursery web spider, and two semiaquatic species, the fishing spiders or raft spiders of the genus Dolomedes, able to run on water and dive to escape danger. I am yet to see a Dolomedes, but you can watch a video of the raft spider Dolomedes fimbriatus, a rare, protected species in the UK, with footage of courtship, egg sac building and maternal behaviour. Adult nursery web spiders do not make webs for hunting, but they build nursery webs for their young. The young (and some non UK species) do hunt with webs. These spiders have long, stout legs and they often hold the first and second pairs of legs extended together, like in the photo below.
Nursery web spiders are easy to recognise, they often have a pale line on their cephalothorax and parallel lines along the body. They are quite variable in the tone and colour of the lines, as you can gather from the individuals shown here.

Pisaura mirabilis basking in typical posture

Food for sex and feigning death

The reproductive behaviour of Pisaura mirabilis has attracted the attention of many researchers. When adult, males will catch an insect, wrap it in silk and search for females. It is thought this behaviour is elicited by the male coming across female silk drag lines, possibly impregnated with pheromones. When they find a female they present her the gift in their chelicerae while raising his body and front legs and palps (watch this video of the approach). If the female accepts the gift they will mate. Males without a gift have reduced chances of mating with females, but sometimes males 'deceive' females by wrapping some insect carcass or a piece of debris to offer the female. Presenting a silk wrapped gift increases the chances that mating will be completed before the females grab the parcel and run away. If the female shows aggression, the male can immediately become immobile (death feigning), while still holding his present. When the female renews her interest in the parcel the male comes back to life and resume mating.  

Male Pisaura mirabilis in another typical resting position. Note its swollen palps.

This male has captured a greenbottle fly.

Maternal behaviour
During the summer, in the lower level of meadows and other open, sheltered places, amongst grass and wildflowers, you might be lucky to come across a female Pisaura mirabilis carrying her large, white egg sac. She holds the egg sac on her chelicerae and palps until the spiderlings are ready to hatch, and despite her long legs, she looks like is walking on tiptoes with her cumbersome load. Once the young start to hatch, she loosens the egg sac and attaches it to a blade of grass. She then builds her nursery tent around the egg sac, where the spiderlings will reside for a while.

Female Pisaura mirabilis with fresh egg sac. Compare with the texture of the older egg sac on the top shot, note that the female on the top shot has a piece of egg sac covering between her chelicerae, so she might well have already loosen up the covering of the sac in preparation for building her nursery.

Nursery web with spiderlings. The spiderlings will form balls like in Araneus diadematus, and the balls also 'explode', with the spiderlings running away from each other when disturbed.

A female standing guard by her nursery web. The spiderlings will disperse after their second moult. Later in the summer, she may lay another batch of eggs.

Araneidae: typical orb weavers

It's #arachtober, a whole month dedicated to the celebration of spider awesomeness and diversity! For this reason, I will be writing a daily post on the natural history of a British spider family.

For the first post, I have chosen Araneidae, the typical orb weavers. This is one of the largest spider families and include many familiar species, such as the garden spider (Araneus diadematus), the window frame spider, Zygiella X-notata, the wasp spider Argiope bruennichi, and the small cucumber spider Araniella sp. There are 33 species in the UK.  The drawing on the left shows the eye arrangement in the family (based on a photograph by Kiron Basu)

In foggy weather, orb webs become very visible, heavy with dew. The spider is sitting in the central hub.

A. diadematus spinning its web.

The spider's web
The most characteristic feature of araneids is that they spin flat, rounded webs with radial threads connected by a spiral net-like pattern of threads, which they attach to vegetation or other structures  The threads are sticky, and able to trap flying insects. The spider either sits in the middle of the web (often at night) or hides in a retreat on a corner of the web, with one of their legs touching a signal thread connected to the hub of the web, which allows them to detect the vibrations produced by any struggling insects. Orb spiders often eat their web at the end of the day, and build a new one in the morning. As they adopt a sit and wait strategy to catch prey it is easy to find particular individuals in the same spot every day.

Dangerously close. The male (on the left) was dispatched before he had the chance to mate, after a lengthy and careful approach.

Mating and cannibalism
Adult females are readily distinguished by their larger size and swollen abdomen. Females often cannibalise males (often right during mating), and males might die after mating a couple of times so at the end of the season, only mature females might remain.

Female Araneus diadematus with its fresh egg sac.  Once their egg sac is finished, the female sits on it and will die in a few days.

Egg sacs and spiderlings
Females lay their eggs, often over a thousand of them, and spin an egg sac around them. Females might die shortly after egg laying. The spiderlings hatch, moult inside the egg sac and then they emerge. In some species, like the garden spider, they spin a communal web and cluster together in it until they are ready to disperse.

A spiderling ball, newly born A. diadematus

At the end of the summer, full size Araneus diadematus can subdue quite large insects such as droneflies, butterflies and wasps.

A. diadematus are very variable in background colour with a range from sandy to chocolate brown, although the white markings on the abdomen tend to be more uniform.