Emergence of the bot flies

The grisly subject of botflies revisits me at this time of year, because August and September is when I find them floating in the swimming pool.

My earlier unconfirmed discovery of a bot on a western tree squirrel elicited quite a few comments, including this one by bot fly expert Frank Slansky at the University of Florida. His webpage on the topic is worth a visit.

"Can you clarify-- was that pic of the sq on your website from California? It looked like a western gray squirrel, but I'm not certain.

[CW: Yes, it was a western gray squirrrel.]

"The issue is that there is only one known species of Cuterebra (C. emasculator, the "emasculating" bot fly, which actually doesn't emasculate its hosts!) that normally infests tree squirrels, and it only occurs east of the Mississippi. So there are three possibilities about the squirrel you photographed:

1. There is a western spp of Cuterebra that typically infests sqs which has not yet been 'discovered' and identified by entomologists;

2. The eastern species of Cuterebra that infests squirrels has somehow spread to the west coast, perhaps because some of the eastern gray squirrels that were introduced on the west coast were infested with Cuterebra;

3. The squirrel you photographed was 'accidently' infested by a species of Cuterebra that typically doesn't infest squirrels. Each species of Cuterebra is fairly specialized in its 'typical' hosts-- one species of Cuterebra may typically infest only wild mice, another only wild rats, another only rabbits, etc. But sometiumes an 'odd' host gets infested, such as a raccoon or house mouse-- sometimes even cats, dogs and people, although there are no species of Cuterebra that typically infest these animals. They just 'accidently' get infested when they encounter some bot fly eggs laid in the habitat of the 'typical' hosts.

"I think #3 would be the most likely explanation for that squirrel-- when running on the ground it may have encountered some eggs of a mouse-infesting or rabbit-infesting Cuterebra and became infested that way. Larvae of the mouse-infesting species often settle in the groin area of mice.

"Anyway, it's probably a very rare occurrence, but if you see other western tree squirrels with these bot fly lumps ('warbles), please let me know. And if you know any folks out your way who are wildlife rehabilitators, please ask them to keep an eye out for Cuterebra-infested sqs that they get in for rehab. Larvae should be removed (they can be carefully pulled out using forceps from a live squirrel through the hole they normally make in an animal's hide, and preserved in alcohol (isopropyl or ethanol). If I could get some photomicrographs of such larvae from western tree squirrels, we should be able to publish a paper about this since it would be a very unique situation.

So readers there you have it. Keep your eyes peeled and contact Frank if you see warbles on Western tree squirrels. (Don't bother him with eastern tree squirrels -- he already has plenty of bots from them.)

Bambi is cute fly bait

Cute, isn't it?

Well, the codger's reaction is less adoration than amusement tinged with cynicism.

Here the log-perching Bambi is displaying the heart-warming curiosity of juvenile deer, a fetching trait that renders it highly attractive as fly bait. In fact, a number of mammals are known to be more vulnerable to parasitic fly infestation as juveniles than as adults.

Entomologist John R. Anderson wrote a fascinating paper about the infestation tactics of nose bot flies that parasitize black-tailed deer. (Unfortunately, I can no longer find the paper among 3000 uncatalogued reprints in the garage, so I am jogging my memory and give you the reference below).

You see deer and cattle share a very long history of relations with various species of bot flies that detect their hosts by very general (e.g. CO2 and urine) and very specific chemical signatures, such as volatile compounds from scent glands.

Out here in the west, two species of nose bot flies infest our black-tailed deer. How they zero in on their hosts isn't well known, but Anderson spent a lot of time watching parasitic flies dupe deer.

One species (Cephenemyia apicata), he found, takes advantage of the deer's curiosity.

The gravid fly chooses a bush in plain view of Bambi, and then buzzes about in a come-hither-come-yon dance. Bambi approaches to inspect this curious thing, and is rewarded with a tiny fly larva squirted onto it's moist muzzle. If the deer doesn't lick and swallow it, the larva wriggles into the nostrils.

Cephenemyia jellisoni, the other species, is a stealth hunter. It approaches the deer out-of-sight and from behind, and slowly moves forward beneath the soft underbelly. Then it quietly hovers into position under the animal's throat and muzzle, taking care to remain undetected by tracking the animal's head movements. When the time is right it dashes into position and squirts its larva ('larvaposits') on the moist lips or muzzle. Numerous females may attack a single deer.

The larvae settle in the pharyngeal pouches at the back of the throat, where they feed on tissue secretions and grow into beautiful bots. (I'm kidding of course.)

I still recall my revulsion the first time I saw nasal bots in the throat of a necropsied deer. We were having a wonderful time being young biologists, measuring testes, preserving uteri, while eating curried venison and drinking beer.

When we started to pull mandibles for aging, there they were at the back of the throat: a writhing mass of inch-long white maggots. We gagged and came close to tossing our cookies, but we were tough.

So I don't turn up my nose to insects. They are here to stay, and when nature pits Bambi against flies there's just not much of a contest.


References:

Anderson JR. 1975. The behavior of nose bot flies (Cephenemyia apicata and C. jellisoni) when attacking black-tailed deer (Odocoileus hemionus columbianus) and the resulting reactions of the deer. Can J Zool., 53(7):977-92.

Anderson, JR. and & W Olkowski. 1968. Carbon Dioxide as an Attractant for Host-seeking Cephenemyia Females (Diptera: Oestridae). Nature, 220:190-191

Cogley, TP. 1987. Effects of Cephenemyia spp. (Diptera: Oestridae) on the nasopharynx of black-tailed deer (Odocoileus hemionus columbianus). Journal of Wildlife Diseases, 23(4):596-605

Olroyd, H. 1964. The natural history of flies. Weidenfeld and Nicholson, London

Tømmerås, BÅ., A. Wibe, AC. Nilssen, and JR Anderson. 1993. The olfactory response of the reindeer nose bot fly, Cephenemyia trompe (Oestridae), to components from interdigital pheromone gland and urine from the host reindeer, Rangifer tarandus. Chemoecology 4(2):115-119

Got you under my skin

Notice anything unusual about this squirrel?

Yeah, I've noticed that it's a male too, but that's not unusual. (Arrow "x" is there only for reference.)

What I'm talking about is the dark thing hanging down from the squirrel's belly? Can you see it? Look again below the scrotum. Arrow "y" points to it.

The luckless rodent seems to be carrying an alien from the underworld of the Arthropoda. What you probably see is a repugnant swelling with an oozing sore, a warble. It's the domicile of a bot, the parasitic larva of the bot fly.

As flies go, bot flies are rather pleasing. They are hairy, somewhat blocky in build, and resemble bees. They have small or vestigial mouthparts. The raison d'etre of their brief adult existence is reproduction, and during their quiet interlude under the skin of squirrels they accumulate the energy stores needed to go forth and procreate.



There are 34 species of the bot fly genus Cuterebra in the US, and their larvae, the bots, must feed on small mammals, mainly rodents and rabbits in order to reach maturity. Each species of Cuterebra has its preferred host. In other words, gophers, wood rats, white-footed mice, and squirrels have their own dedicated species of bot fly, but they are not totally loyal to one host. Occasionally they meet up with the wrong host. Forty species of insects, including bot flies have been known to "accidentally" parasitize people in the US.

Finding a bot on your own body or in something you intend to eat is not a pleasant experience. In the southern US, only 2% of squirrel hunters were reported to eat bot-infected squirrels. The rest of them got really turned off. So a lot of hunted squirrels cycle back into the food chain without benefit of human digestion.

The fly bot is the closest thing to the slimy xenomorph (read Alien) from Planet LV-426 that exploded from the chests of its human hosts. Surely you remember Sigourney Weaver and aliens that got scarier with each new movie.

The difference of course is that aliens are fictional. True, they are all pretty much based on biological themes, though embellished and recombined to be extremely scary. Bot flies and their parasitic larvae however are REAL. So let's concentrate on the kinds of zoological reality that gave the producers of Alien its wildest ideas. There's a good reason for this, because our youth often confuse reality and fantasy, and in the age of intelligent design people seem to be losing their curiosity about biology and the natural world.

You will recall that the infective phase of the Alien life cycle is the Facehugger, which leaps onto the head of the human host and shoves an egg down its throat. This is extremely disconcerting for the human host. Cuterebra have far more finesse.
The female uses olfactory cues to home in on the nests of rodents, and simply lays her eggs on the vegetation nearby. When the eggs hatch the tiny bullet-shaped larvae (the first instar) zero in on body heat and attach themselves to the passing rodent.

There is no need for forced entry. The tiny larva crawls undetected into the body through the eye, nose, or mouth -- for that matter any opening they find, natural or otherwise.

The Alien's embryo (the "crawler") settles in the thoracic cavity and matures in a remarkable 24 hrs. Our baby bot (the first instar) on the other hand, takes about a week to migrate from the point of entry to a comfortable space beneath the skin, often in the squirrel's hindquarters. There it prepares its lodging for the next several months. The first order of business is to rasp a small breathing hole to the outside word. It also uses this porthole as a latrine, periodically expelling its liquid brownish excreta on the surface, which the squirrel periodically grooms away.

For the next month and a half the bot is the squirrel's constant companion. The squirrel's body reacts to it by encapsulating it in a fibrous sac, not unlike a mummy bag which seals it off from the rest of the body. The host's white blood cells and antibodies also increase. but this has little effect on the bot. It is basically a couch potato. Its daily routine is to lounge in its mummy bag, feeding continually on tissue fluids and cellular debris.

When it reaches the stage known as the third instar, it's almost as big as the end of your thumb. But unlike the Alien, it doesn't explode through the body wall, killing its host and scaring the hell out of everyone. On the contrary, it goes gently into that good night of pupation by squeezing through the breathing pore and dropping to the ground. There it burrows and undergoes its final transformation. It may emerge as an adult in another month or pass into a diapause and emerge next year.

It is hard to say how squirrels and other bot-infested rodents feel about all of this. They seem to carry on normally and ignore the bot, but in the laboratory at least, rodents become inactive about the time the bots emerge, and we may infer from this that harboring a bot has its discomforts.

What else? Well, if you are a nestling squirrel and unfortunate enough to be selected by several bots, you may not live long. If you are an adult female and the bots settle in your back side (as they often do) you may develop a pseudo-scrotum, and fool all the other squirrels. Male's with a bot-infested scrotum on the other hand may sport an appendage that resembles a duffel bag, but this renders them reproductively useless for the time being.

The affinity of bots for the scrotum accounted for the name Cuterebra emasculator, but Drs Bob Timm and Robert E. Lee Jr showed that scrotal bots don't affect subsequent reproduction. Unlike a lot of other parasites, bot flies don't practice "parasitic castration" upon their hosts.

If that wasn't so, a lot of southern squirrel hunters might be wearing camou codpieces made of fly screen.


References

Baudoin, M. 1975. Host castration as a parasitic strategy. Evolution 29:335-52.

Bennett, G.F. 1973. Some effects of Cuterebra emasculator Fitch (Cuterebridae, Diptera) on the blood and activity of its host, the Eastern chipmunk. Journal of Wildlife Diseases 9:85-93.

Jacobson, H.A., D.C. Guynn, and A. Hackett. 1979. Impact of the bot fly on squirrel hunting in Mississippi. Wildlife Society Bulletin 7(1):46-48.

Scott, H.D. 1964. Human myiasis in North America (1952-1962 inclusive). The Florida Entomologist 47(4):255-261.

Slansky, F. 2006. Cuterebra bot flies (Diptera: Oestridae) and the indigenous hosts and potential hosts in Florida. Florida Entomologist 89(2):152-160.

Timm, R.M. and R.E. Lee Jr. 1982. Is host castration an evolutionary strategy of bot flies? Evolution 36(2):416-417.