One day, earlier in the summer (on 28th June 19), I came across huge numbers of common blue damselflies (Enallagma cyathigerum) which had emerged from a lake – Felmersham gravel pits – and were basking in the sunshine on vegetation round about. Many of them were mating, and I took a series of photographs of a couple of mating pairs. The males are bright blue (below) whilst the females are variable in colour. Some females look like the males – a cunning ploy to avoid getting too hassled by the males! – whilst others are distinct, being brown or green (as here).
The club, or mushroom-shaped black mark on the dorsal (upper) surface of the second abdominal segment (S2) is, I understand, diagnostic of this species (see below, white arrow).
The male usually initiates copulation, after seizing a female, but he cannot force her to mate if she does not want to. Even if the female is willing, she initially makes no attempt to copulate, remaining clasped by the male (in tandem), but with her abdomen hanging down. Male damselflies must transfer sperm from their primary genitalia (which are located towards the end of their abdomens) to their secondary, or accessory genitalia (which are near the front of the abdomen). Incredibly, they can do this whilst still clasping the female with the end of their abdomen. Here is a photograph of this so-called, intra-male sperm translocation behaviour, in another damselfly: Hemiphlebia mirabilis (from Cordero-Rivera, 2016).
The female is clearly aware of the sperm being transferred just above her head (!) and will not bend her abdomen around and ‘mate’ with the male’s secondary genitalia, until this transfer has occurred.
Coenagrionid damselflies, like the common blue, are rather unusual – although this behaviour is also known to occur in butterflies! – in that the males have a specially shaped penis which allows them to remove (or at least shove out of the way!) any sperm deposited in the storage organs of the female, by previous males! It took me a while to work out that the penis, and temporary sperm storage sac, are located in the male’s second abdominal segment. An amazing photograph of a male damselfly’s penis, or aedeagus, is shown here. There are two hook-like extensions – like elaborately curved spoons! – for scooping out rival’s sperm.
At first, the mating pair were watched closely by another male (below). Perhaps he had previously mated with this female (?) and knew that his sperm was being succeeded! Probably not, but he was clearly taking a close interest in the proceedings.
After a short while, about a minute, the watching male departed, leaving the pair in peace (apart from a gawking photographer!) to form a mating wheel (below).
The removal of sperm, which gives a male precedence over previous suitors, occurs during a fairly protracted (initial) stage of the mating, prior to inseminating the female with his own sperm. The males carry out a number of rhythmic movements during this first stage, and the long copulation time of Enallagma cyathigerum (ca. 20 min or more) is thought to be because of this sperm removal, or sperm precedence, activity (Miller & Miller, 1981; Miller, 1982). The action takes place in those parts of the abdomen which come together during copulation: i.e. the male’s second segment and the female’s 8th and 9th segments, I think (counting them!).
Not surprisingly, copulation times with females who have already mated are much longer than with virgin females, either because of this subtle form of sperm competition, or because they are trying to get the female to use their sperm and not that of her previous lover! In other words, the females also have some control over whom they wish to have as the father of their offspring! Something called ‘cryptic female choice’. In other words, there is a lot going on, unseen, in this union!
During these processes, the male clasps the female via the back of her thorax (the pronotum). At first glance, it looks as though he has hold of her by the neck, but in fact, there are small grooves – supposedly unique in shape and form to each species – into which the male claspers fit. The following photograph is a bit grainy, but clearly shows the male gripping the ‘back’ of the female.
I also photographed a second pair, who had formed a nice heart-shaped wheel (below).
Closer inspection of these photos, shows that the male was carrying a small cluster of mites at the top of the thorax (below), and possibly one larger one under his 3rd abdominal segment. These are water mites (Arrenurus spp. I think). They hitch a lift when the damselfly emerges from the water, and apparently feed on body fluids, i.e. haemolymph, so they are parasites.
The mites detach themselves when they are fully grown, and reenter the water. They tend to jump off when the damselfly host drops down over a new pond or wetland. Damselflies are reportedly, not much affected by these parasitic mites; they do not reduce their survivorship, but they can reduce male mating success in some circumstances (Andres & Cordero, 1998).
There was also a solitary mite on this male (below).
N.B. some of these photographs are a bit grainy, when heavily cropped, as I was pushing the depth of field (to f/16) as well as maintaining a fast shutter speed (so the ISO reading goes up).
Andres, J. A., & Cordero, A. (1998). Effects of water mites on the damselfly Ceriagrion tenellum. Ecological Entomology, 23(2), 103-109.
Doerksen, G. P. (1980). Notes on the reproductive behaviour of Enallagma cyathigerum (Charpentier)(Zygoptera: Coenagrionidae). Odonatologica, 9(4), 293-296.
Hassall, C., Lowe, C. D., Harvey, I. F., Watts, P. C., & Thompson, D. J. (2010). Phenology determines seasonal variation in ectoparasite loads in a natural insect population. Ecological Entomology, 35(4), 514-522.
Miller, P. L. (1982). The occurrence and activity of sperm in mature female Enallagma cyathigerum (Charpentier)(Zygoptera: Coenagrionidae). Odonatologica, 11(2), 159-161.
Miller, P. L., & Miller, C. A. (1981). Field observations on copulatory behaviour in Zygoptera, with an examination of the structure and activity of the male genitalia. Odonatologica, 10(3), 201-218.
Perry, S. J., & Miller, P. L. (1991). The duration of the stages of copulation in Enallagma cyathigerum (Charpentier)(Zygoptera: Coenagrionidae). Odonatologica, 20(3), 349-355.
Cordero-Rivera, A. (2016). Sperm removal during copulation confirmed in the oldest extant damselfly, Hemiphlebia mirabilis. PeerJ, 4, e2077.
Uhía, E., & Rivera, A. C. (2005). Male damselflies detect female mating status: importance for postcopulatory sexual selection. Animal Behaviour, 69(4), 797-804.
Waage, J. K. (1986). Evidence for widespread sperm displacement ability among Zygoptera (Odonata) and the means for predicting its presence. Biological Journal of the Linnean Society, 28(3), 285-300.