In the warm, but very rainy, first weeks of June I had a couple of enquiries from gardeners who had observed strange worms waving around blindly, climbing anything they touched, especially the wet foliage of nearby plants. These smooth, pale-coloured worms were probably the Grasshopper Nematode (Mermis nigrescens), a roundworm of the phylum Nematoda, which develops as an internal parasite of grasshoppers (and perhaps earwigs). For a nematode, it is extremely large, 5-20 cm, far larger than the nearly microscopic entomopathogenic nematodes often used to control various soil insects. The overall body color is very pale brown. The adults crawl on vegetation, usually following rainy periods and lay tiny goldenbrown eggs which they attach to plants. Grasshoppers become infected when they incidentally consume the eggs as they feed. The young nematodes burrow into the body cavity of the insect, feeding on the blood (hemolymph) reaching full size in a few months. The infected grasshopper eventually dies and the nematodes leave the host and move into the soil. Within the soil the nematode moults to the adult stage and has a long period as a free living organism, living many years.

In some parts of the world, where grasshoppers are significant pests of crops, Mermis has been tried as a biological control.

Two other callers mentioned finding long, thin worms in water which were rather stiff and rigid, looking a bit like bits of plant root. These were almost certainly Horsehair worms, a strange group of animals, superficially similar to nematodes, but with some unique physical features that cause them to be classified in their own phylum, the Nematomorpha (from the Greek: nemat =thread, morph = shape). Nematomorphs are sometimes also called cabbagehair, gordiid or ‘Gordian worms.’ They often squirm and twist, knotting themselves into a loose, ball-like shape, and hence the reference to the ‘Gordian knot’. With very few exceptions, free-living, adult horsehair worms are found only in water; although only 1-3 mm in diameter, they can be very long (10-80 cm in Britain, records from the United States mention worms over 1 m), varying in colour from light to dark brown. They are nearly uniform in body appearance, with a slightly blunt head and small cleft in the hind end.

Grasshopper nematode

Gordian worm

Like the Mermis nematode, horsehair worms also parasitize insects such as Grasshoppers, Crickets and Beetles. The minute larvae are ingested by the host insects when they drink or are consumed as cysts on vegetation at the water’s edge; they then penetrate the gut and move into the body cavity, feeding on host tiNovember 19, 2011 9:03ce eggs and die prematurely. When development is complete the adult worms need to emerge into water and this is where the story takes a bizarre turn. The worm is able to affect the behaviour of its host causing it to seek out and move to water where it will often drown itself. A piece in New Scientist (http://www.newscientist.com/article.ns?id=dn7927) headlined this as ‘Parasites brainwash grasshoppers into death dive’ and described how the worm produces proteins which directly and indirectly affect the grasshopper’s central nervous system. Some of these proteins were linked to neurotransmitter activities; others included those linked to geotactic behaviour which is the oriented movement of an organism in response to gravity. There is even a video of this behaviour online at http://www.canal.ird.fr/canal.php?url=/programmes/recherches/grillons_us/index.htm

Thanks to Adrian Chalkley for drawing my attention to this clip which he describes as ‘fascinating but a little too much like ‘Alien’.

Four species are found in Britain: Gordius villoti, Parachordodes pustulosus, Gordionus violaceus and G. wolterstorffi. Little is recorded about their frequency and distribution, the NBN Gateway only lists, Gordionus violaceus, but that is a blank distribution map! Any confirmed Suffolk records would be welcome.

These worms are sometimes seen after crushing pests that have invaded the house. When crushed, worms are released and crawl indoors. Some are found in toilets where infested pests (e.g. crickets) have been discarded, in pet dishes where an infested insect has crawled, or in gardens on vegetable plants. They are harmless to humans.

The ability of parasites (which usually don’t kill the host) and parasitoids (usually killing the host, only acting as parasites when young) to influence the behaviour of their hosts is quite a widespread phenomenon. Some ‘enslaver’ fungi make their hosts die perched in a position that favours the dispersal of spores by the wind. The Enterophthora fungi are transmitted by airborne spores. Most species are very host specific, infecting only a certain species of insect or a group of closely related insects. E. muscae is pathogenic only to certain types of flies (higher Diptera, in the Cyclorrhapa). When a spore settles on an appropriate fly’s body, it germinates and penetrates through the fly’s exoskeleton, often through one of the many intersegmental membranes between the harder parts of the exoskeleton. The fungal hyphae grow throughout the body of the fly, growing enough to distend the abdomen by the time the fly dies. As the body is distended, the light colored membranes between the darker hard segments are exposed, giving the fly a characteristically striped appearance (see photo).

Flies showing symptoms of Enterophthora infestation

Once inside a fly, fungal hyphae grows into the fly’s brain, causing a distinct change in behaviour, often called “summit disease.” Instead of acting normally, the fly crawls upwards as high as possible, going to the tip of the branch or stem it is on. This behavioural alteration is also accompanied by formation of specialized fungal structures or glue-like materials secreted by the hyphae for attachment. The fly securely attaches itself by its extended proboscis to the surface it is on, where it may remain for days or even weeks. Before it dies, it spreads out its legs, stretches opens its wings above the thorax, and angles the abdomen away from the surface. The elevated location and distinct posture improves the chances that any fungal spores that are produced will leave the cadaver and infect new hosts. This fungus can also be transmitted in another way. Male house flies are attracted to dead female flies infected with the fungus, and can pick up spores when attempting to mate with the corpse. About 90% of such encounters result in infection. Before they die, infected males can mechanically transmit spores to female flies during mating. E. syrphi (which infects only hoverflies) may even mimic pheromones used to attract a mate.

Fungi in the genus Cordyceps operate in a similar way on ants, causing them to climb to the top of plants and fasten their mandibles to the stem before dying. The fungus produces chemicals which act on the host’s brain and appear to alter its perception of pheromones. That well known parasite, the Liver fluke, has a similar effect on ants. Adults infected with the fluke larvae are made to climb to the top of blades of grass where they are eaten by grazing sheep (the main host).

There are many parasitic wasps which utilise a wide variety of hosts to shelter and feed their larvae. Insect prey is often dead; but in central and North America Braconid wasps in the genus Glyptapanteles do not kill the caterpillar they lay their eggs in. Up to 80 fully grown larvae emerge from the living host to pupate leaving one or two within the caterpillar like little puppet masters causing it to thrash about violently when potential predators on the wasp pupae approach (the caterpillar does not normally respond to these predators). In Costa Rica an ichneumonoid wasp Hymenoepimecis argyraphaga parasitizes spiders, causing them to modify their web building behaviour to make a specially reinforced construction strong enough to support the wasp’s pupal cocoon.

One of the most impressive parasitic wasps is the emerald cockroach wasp Ampulex compressa, a small solitary species that lays eggs in a (relatively) large cockroach host. The female wasp delivers two precise stings: one to the roach’s midsection, causing its front legs buckle and a second, more precise, sting to the head. This sting is exactly placed within the ganglia (brain) and has the effect of neutralising the insect’s escape reflex. The wasp does not paralyze the cockroach; it is able to lift up its front legs again and walk, but now it cannot move of its own accord. The wasp takes hold of one of the roach’s antennae and is able to lead it like a dog on a leash. The ‘zombie’ roach crawls where its master leads, which is to the wasp’s burrow where it sits quietly while the wasp plugs up the burrow with pebbles and lays an egg on its underside. The wasp larva consumes the roach’s internal organs in an order which guarantees the roach will stay alive, at least until the pupal stage. Video of the wasp’s attack can be seen online at:
http://www.bgu.ac.il/life/Faculty/Libersat/movies/Wasp_movie_short.mpg

We might think that it is only insects with ‘simple’ brains that can be affected in this way, but there are interesting examples in mammals. Toxoplasma gandii is a parasitic protozoan usually transmitted in cat faeces. Infection can cause toxoplasmosis, usually a minor disease but one which is potentially fatal to foetuses in early pregnancy. The infection can be carried by most warm-blooded animals and is often found in rats and mice. It seems to have the ability to change their behaviour, making them drawn to, rather than fearful of, the scent of cats. This effect is advantageous to the parasite, which will be able to sexually reproduce if its host is eaten by a cat. The infection is almost surgical in its precision, as it does not affect a rat’s other fears such as the fear of open spaces or of unfamiliar smelling food. There has been speculation that human behaviour may also be affected in some ways, and correlations have been found between latent Toxoplasma infections and various characteristics such as decreased novelty-seeking behaviour, slower reactions, and feelings of insecurity. Perhaps those Halloween horror stories of zombies are not so far fetched!

Martin Sanford
SBRC, Ipswich Museum, High Street, Ipswich, Suffolk IP1 3QH

martin.sanford AT et.suffolkcc.gov.uk