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.
'Look, a slug standing up' called my 7 year old daughter. I went over by her and watched. Indeed, a Spanish Slug, Arion vulgaris, reared up as high as it could go in between some pots. It waved its body from side to side, and after some time it bent over itself turning round, touching its mucus pore with its head. I had seen this behaviour previously described in Rowson and colleagues' FSC guide 'Slugs of Britain and Ireland':
'Arionids are sometimes seen rearing up off the ground, as if sniffing the air'
It is a curious behaviour of unclear function, are they really 'sniffing' the air? could they be sensing humidity in the air, assessing when to retreat to a refuge, or looking/smelling for food? Although slugs have very simple eyes, this rearing and moving side to side could allow them to assess where shadows are indicating plants to climb. Alternatively, they could be detecting or emitting pheromones to find or attract potential mates.
As predicted, it rained all night and most of the morning. In the afternoon, the rain turned to drizzle and eventually stopped. This was an ideal day slugs, so my youngest daughter and I went to the wildlife garden to try and see some. Slugs don't have many fans. Many gardeners detest them and fight the slug wars with any means available. Out of the 40+ British species, many of them introduced, some are indeed serious agricultural pests specialising on feeding on living plant tissue. Slugs as a group, however, are ecologically very diverse and most species cause little or no damage feeding on algae, decaying plants, lichens, carrion, or fungi. A few species are earthworm predators. Slugs are not a natural group, they are a mixed bag of snails which have lost their shells: British slugs are the result of four different evolutionary shell loses, each group being more closely related to a different snail family, but more on that on a future post.
Slugs were plentiful in the garden today and gave a good idea of the diversity of the British fauna. A nice feature of slugs is that they can be easily collected by hand - provided you don't mind getting covered in their mucus - and they are best identified live, so no collecting is necessary (except for some species where dissection is necessary for identification). I tried to get photos of the right side of the slug, with shows the breathing pore and other diagnostic characters, and used the Slugs of Britain and Ireland FSC guide by Ben Rowson and colleagues to identify them. I am no expert, and if you see any misidentification, I will be grateful if you let me know.
We first came across some large Arion slugs (above photo). These are often active and out and about during the day. The one on the top shot was feeding quite high up on an angelica plant. When disturbed (e.g. poked with a finger), these slugs make a semispherical hump. The first one we came across, a very dark one, started rocking from side to side, a dancing slug was a good start! Only a couple of very variable species, Arion ater and Arion rufus will show this rocking response. Despite its dark colour, this one appears to fits better with Arion rufus, which has a bright orange foot fringe, but Arion often hybridise and species identification is tricky, especially in disturbed habitats.
This was another large Arion, which wasn't as keen to dance:
An Arion adopting its humped defence position.
We found the next slug, the Iberian Threeband Slug, Ambigolimax valentinus, inside an upturned plastic pot, which is fitting as this species is thought to have been introduced initially to greenhouses, but now it is readily found outdoors.
Ambigolimax valentinus
And now to our 'kitchen slug': the Green Cellar Slug, Limacus maculatus. A large, strictly nocturnal species able to squeeze through the tiniest cracks. If you go out into your garden at night, you are likely to see this slug in large numbers. They will often feed on other dead slugs or snails that had the misfortune of being squished on paths during the day. The ones inside our house will feed on cat food if there is any left. This was found together with others under an upturned large plastic tray.
Limacus maculatus
We lifted a few logs and there I found one of my favourite slugs, the Worm Slug, Boettgerilla pallens. I've never seen it in my garden, but it is common in the Wildlife Garden. It is an introduced species first detected in the UK in 1972, when it was already widespread. It was first described from mountain forests in the Caucasus and since then it has spread to western Europe. It is a mainly detritivorous slug, long and thin when moving, reminiscent of a worm. It lives underground, down to 60 cm deep, and moves through earthworm burrows.
The Worm Slug on the log where we found it.
Worm slug on the white bowl.
I got to Deroceras invadens/panormitanum for the next two slugs. Although they look quite different, they look like they have a hump and a truncated tail.
The last one is also a Deroceras, but the tail end is not as truncated, so I got to Deroceras reticulatum.
I was amazed walking into the kitchen a few minutes ago when I came across this massive slug, stretched to over 10 cm long on the floor. A Limacus maculatus, it was covered on tiny mites, clustered near the bottom of the slug's body (click the photo to enlarge). Slugs and snails often carry mites of the genus Riccardoella but I have never noticed so many in a slug.
UPDATE. Thank you to Richard Comont and Ryan Clark for pointing me to the right species of mites. I have now amended the post.
After the very rainy April we are having a teasel growing in the garden is looking very luscious. It has grown a large rosette of leaves, and developed two large leaf-cups which are filled with water to the rim. If you want an account on this fascinating carnivorous plant, check here. I had a peek a couple of days ago to check if any drowned invertebrates were visible. And there were indeed! On the bottom cup (above) a 7 spot floated on a very cloudy liquid, while on the top one, a drowned slug was visible at the bottom of the clearer water, and a few small unidentified insects. What a catch!
The current dry weather means I am not coming across as many terrestrial molluscs as usual. While moving some pots I came across these two beauties, the Yellow slug (Limacus flavus, top) and the Irish Yellow Slug (Limax maculatus). After a while they relaxed on a wet white bowl and let me take their portraits before being returned to the plastic pot pile. Until recently, they were considered the same species, but these two look very different, not only in coloration, but in body shape, despite being a similar length. Both are very common out and inside my house, and are active at night.
I found this useful slug key in the field studies website.
As their snail relatives, slugs are hermaphrodites, each individual producing eggs and sperm. Although some species regularly self-fertilise, in many others, individuals - given the chance - will trade sperm with other individuals they encounter. I came across this pair of courting slugs under a fallen apple an evening last week. They are Deroceras panormitanum (thanks to Fauna, from WAB for the ID). At the right time of the year, and when meeting a potential partner, these slugs crawl in circles, producing and eating chemicals mixed in their respective mucus trails, before mating happens. The outcomes of courtship and mating are diverse: the slugs are able to mate repeatedly and use sperm from several donors to fertilise their eggs, or they might decide not to give sperm to its partner, or digest the sperm obtained and self-fertilise. This means that, despite being hermaphrodite, a slug can decide if to act only as male (digesting the partners sperm but providing its own), as female (refusing to give sperm, maybe preferring to save it for a better partner) or as both. This can create conflict between the partners - each with their own interests - and has been hypothesized to spur an "arms race" - or "genitals race" if you wish, and has led to the evolution of a range of bizarre copulatory structures and complex mating courtships.
Heike Reise has reviewed and described the behaviour of these diverse genus of slugs and summarized courtship and mating as follows:
(i) Precourtship phase: the partners encounter and investigate each other.
(ii) Courtship phase: both partners have their sarcobelum protruded from the genital opening and assume a position with their genital pores facing each other, forming a circle or yin-yang configuration.
(iii) Copulation phase: the slugs evert their penes, entwine them, and mutually transfer the ejaculates from penis to penis (there is no intromission).
(iv) Withdrawal phase: the penes are retracted together with the attached sperm masses.
After coming across a potential partner or trail, some behaviour follows. This species has a flattened tail, which is enlarged during courtship and waved from side to side. These movements increase the chances of contact with the partner's tentacles. If the leading individual is ready to mate, it eventually turns round and starts following the second individual, forming a circle. Both individuals then evert their sarcobellums - as seen in the top shot - a solid, mobile structure in the genitalia which produces chemicals, that are exchanged during their circling behaviour. The sarcobelum is very active during the courtship, tracking closely the partner tail end and stroking it, at the same time that smears the partner with chemical secretions. In this species, courtship can last over an hour, followed by a relatively quick copulation (a few minutes), in which the slugs genital openings become very close, actual penises - bluish, transparent masses - are everted and entwined with the partners and sperm are exchanged externally. These slugs also have a penial, multifingered gland, that they also evert after insemination and lay over their partner's back, transferring some secretions. The function of this gland has been suggested to be equivalent to the snails' dart, the smeared chemicals on the partner might increase the chances of paternity. The slugs above were in the courtship stage, but unfortunately, by the time I went out again to check on them, they had disappeared.
References Heike Reise (2007). A review of mating behavior in slugs of the genus Deroceras (Pulmonata: Agriolimacidae) American Malacological Bulletin, 23, 137-156 Benke M, Reise H, Montagne-Wajer K, & Koene JM (2010). Cutaneous application of an accessory-gland secretion after sperm exchange in a terrestrial slug (Mollusca: Pulmonata). Zoology (Jena, Germany), 113 (2), 118-24 PMID: 20202803
A showery day, I come across this enormous Arion slug crossing the garden path. It must be close to 15 cm. Identification to species level is difficult to impossible as they are distinguishable by examination of internal genitalia characters - or molecular genetic analysis, and hybrids are common. British large Arion slugs are made of several species complexes, Arion ater/rufusA. lusitanicus and A. flagellus. Both groups are very polymorphic slugs, from almost white to black, including all shades of brown yellow red and orange. I have never found the the black morph in the garden, but a good representation of the others abound. The polymorphism of these slugs in the U.K., not only in colour, but also in genital characters, might stem from common hybridisation between several subspecies that colonised the British Isles from Europe, postglacially but also in more recent human introductions. Distribution changes might also come about due to expansions as a result of climate change. In addition, the slugs - except for A. flagellus - are able to self-fertilise and form relatively homogeneous populations, which might give the impression of being a separate species.
Arion slugs had deep tubercles on their backs, and no keel. At the end tip is the mucus gland, producing an extremely sticky mucus. Unlike the yellow slug, which is strictly nocturnal, Arion slugs are active all around the day, provided that it is damp. When disturbed they show a characteristic behaviour: they contract their bodies into an almost round shape and retract their tentacles inside their mantle. Inspired by a post in Myrmecos, I set the photo vertically. I had to use a white plate - instead of bowl - and allow the slug to relax and start to crawl out.
A very yellow specimen
A disturbed Arion
A selection of colours found in the garden
The black morph of Arion sp.
References
Noble, L. R. Jones, C. S. (1996). A molecular and ecological investigation of the large arionid slugs of North-West Europe: the potential for new pests The ecology of agricultural pests: biochemical approaches Ed. William O. C. Symondson, Systematics Association, special volume. Clarendon Press., 53, 93-132 Evans, N. (1986). An investigation of the status of the terrestrial slugs Arion ater ater (L.) and Arion aterrufus (L.) (Mollusca, Gastropoda, Pulmonata) in Britain Zoologica Scripta, 15 (4), 313-322 DOI: 10.1111/j.1463-6409.1986.tb00232.x
UPDATE 30/08/11: reference added and Arion ater in a photo caption changed to Arion sp.
Late last night I went to the kitchen and found a couple of large yellow slugs entwined on the kitchen floor. I dashed back to the front of the house to grab the camera but in the few seconds that took me do do it - it is a well rehearsed sprint of mine - they had started going their separate ways. The sudden flash of light when switching on the kitchen light must have shocked them and they went shy. The only indication they had been together was a circle of slime on the tiles. Should I carry my camera with me as I walk around the house? I sometimes think so. I knew nothing about the yellow slug mating habits. The yellow slug Limax flavus is not as good-looking as its relative the Leopard Slug, Limax maximus of fame due to its acrobatic sex featured in David Attenborough's Life in the Undergrowth TV series (see also the fantastic photos in Snail's Tails). I found very little, well, yes, as snails they are hermaphroditic and exhange sperm, although self-fertilisation is not unheard of. I also found a clip of the start of courtship, which happens on the ground. So I am afraid I will have to wait and see if I can catch them again. I cannot believe I am going to look forward to see slugs at home.
