(Diptera: Cuterebridae), Emasculate Their Hosts?

J. Med. Entomol. Vol. 18, no.4: 333-336 3l July 1981

@ f98l by the Bishop Museum

DO BOT FLIES, CUTEREBftA (DIPTERA: CUTEREBRIDAE), EMASCULATE THEIR HOSTS?

Robert M. Timmr and Richard E. Lee, Jf

Abstract. Asa Fitch, in his description of a new species of that the squirrels in our country are emasculated." Cuterebra that he nzrr'ed, "emaseulator," was the first to suggest Fitch named the chipmunk bot Cuterebrae?llascu- that bot flies castrated their mammalian hosts. In recent years several major review papers and parasitology texts have contin- lator to reflect this belief. For the next 63 years, it ued to perpetuate this belief. A review of both the literature on remained established dogma that bot flies castrated bot flies and their hosts and of the life cycles of both bots and their male hosts; the mechanism was thought to be hosts provides no evidence to substantiate castration. Eastern total consumption of the testes.Ernest Thompson Chipmunks (Tamias striatus) experimentally infected with Cu- terebra ernascularlorexperienced no destruction of testicular tis- Seton, the famed naturalist, was the first to ques- sue. The concept of castration may have been perpetuated by tion whether bot flies actually do emasculate their observations of bots in the scotal sac of a host. Suoerficial ex- rodent hosts. Seton (1920: 95) stated that "There amination of a host with a bot(s) in the scrotum would suggest is no proof that the bot eats fibrous tissue, or any- that the bot had consumed the testis; this is demonstrated on a White-footed Motse (Peromyscusleucopus). We conclude that thing but juices," and ". . . at the season of all ob- there is no evidence to support the notion that bot flies castrate servations-August, September, and October-the their mammalian hosts. On extremely rare occasions,a bot may testes are normally reduced to almost nothing, slightly displace a testis, and perhaps this temporarily reduces drawn into the pelvis." Seton also noted that bots fertility. arejust "as often found in other parts ofthe body, The first published reference to bot flies of the and in the female as much as in the male." Seton's genus Cuterebra(Diptera: Cuterebridae) castrating doubts about castration were not confirmed at the their hosts was by Fitch (1857: 482). He wrote that time and most subsequent authors have ignored "the fact is well known to hunters, that of the grey his paper. and other squirrels killed in this vicinity, at least In recent years, several major review papers and one half of the males are castrated. It is the current texts have continued to perpetuate the belief that opinion with them that this deformity is caused by bot flies totally castrate their hosts, thereby effec- the squirrels' seizing and biting out the testicles of tively reducing the parasitized individual's future their comrades, some of them strenuously main- reproductive potential to zero (for example, see: taining that they have seen these animals engaged Askew l97l:263, Baudoin 1975, Cameron 1956: in this act. There are some hunters, however, that 184, Caullery 1952, Chandler & Read 1961:789, say they have found two grubs in the scrotum of Cheng 1973:844, Dalmat 1942, Krull 1969: 341, some squirrels, and they conjecture that it is by Noble & Noble 1976: 429). A typical quote from these that the testicles are destroyed . . . ." He a recent parasitology text (Cheng 1973: 844) went on to say that "I am therefore led to believe concerning host castration by Cuterebramakes this that these animals do attack each other in the man- blanket statement, with no reference cited: "Cute- ner that has been stated; not, however, for the pur- rebra emasculatorcan destroy its host's testes, caus- pose of emasculating their comrades, as has been ing parasitic castration." Krull (1969: 341) stated supposed, but for the purpose of coming at and "There is one species in the squirrel [presumably destroying these bot-grubs, the enemies of their C. emasculatorl that lives habitually in the scrotum, race." Fitch concluded: "I think that every one will destroys the testicles, and emasculates the host." agree with me in the opinion that it is by this fly Thus, this concept has been so thoroughly in- grained in the literature for the past 124 years that beginning students are taught it as a matter of fact. 1 Bell Museum of Natural History, University of Minnesota, Although a number of papers have been cited Minneapolis, Minnesota 55455, USA. Present address: Division in support of host castration by bot flies (Bennett of Mammals, Field Museum of Natural History, Roosevelt Road 1955, Goertz 1966, Hunter et al. 1972, Wecker at Lake Shore Drive, Chicago, Illinois 60605, USA. 2 Department of Biology, University of Houston, Houston, 1962), none provides clear-cut evidence for host Texas 77004, USA. castration. Wecker (1962: 563) suggestedthat the 334 J. Med. Entomol. Vol.18, no.4 presence of a bot fly in the inguinal region "could gust through mid-September. Larval development offer mechanical interference with the descent of is completed in 3Yz weeks, when 3rd-instar larvae the testes," but there is no mention of bot flies de- emerge through the breathing hole, burrow into stroying testicular tissue. Hunter et al. (1972: 28) the soil and pupate, overwintering in the pupar- make absolutely no mention of host castration by ium. bot flies on the White-footed Mouse, Peromyscus Effects of Cuterebra on hosts leucopus,but did conclude that "There is, therefore, no evidence for the botfly causing significant Despite the fact that the combined weight of the deermouse mortality." Goertz (1966) also made no bot fly larvae in multiple infections may constitute mention of host castration. Even though Bennett 3-bVo or more of the body weight of the chip- (1955: 75) is frequently cited in support of host munk, there appears to be little impairment dur- castration, he stated in his abstract that "No case ing infestation or marked long-term effect after of emasculation was noted." emergence. Infected hosts, including I naturally Numerous theories concerning the parasite's infected chipmunk from which 1l bots later "castration strategies" have been based on these emerged, appeared to forage normally as com- supposed "facts." We were prompted to write this pared to noninfected individuals. One of our ju- paper because, to our knowledge, all available data venile chipmunks increased its body weight by support the opposite hypothesis: that bots have lit- 124% (42.4 to 94.9 g), during which time it "pro. tle effect, upon the testes.First, we will briefly sum- duced" 6 bots. The larval cyst is found only in the marize the life history of Cuterebra emasculator,the subcutaneous layer and does not invade underly- bot fly parasitizing the Eastern Chipmunk (Tam'ias ing muscles or organs. Shortly after larval emer- striatus) and the one most frequently accused of gence, the larval cyst collapses and heals rapidly. castrating its host, based upon our field and labo- At I week postemergence it may be difficult to lo- ratory work in Minnesota and that of Bennett cate the exact site of the former breathing hole. (1955, 1972a,b,1973) in Ontario. Second, we will In northern regions, chipmunks reproduce pri- summarize the observed effects of Cuterebra on marily in the spring (Bennett 1955, Forbes 1966, their hosts. Pidduck & Falls 1973) and bot fly infestations occur in mid- to late summer; thus there is little or Life history of Cuterebra emasculator no overlap between reproduction in chipmunks Although rarely observed in the field, the adult and peak infestation by bots. Therefore, during bots emerge, mate, and oviposit during midsum- the time of most infestations, testes of male chip- mer. As in other Cuterebra(see Capelle l97t), fe- munks are normally reduced and ascended into males probably oviposit along runways and bur- the abdomen. The testes of 2 chipmunks were ex- rows of the hosts, with no direct contact between amined after 4 and 6 bot fly larvae had emerged the gravid female bot fly and the host. Egg hatch- from cysts in the scrotal region. A 3rd male died ing is triggered by a sudden rise in environmental after being artificially infected with 19 bot fly lar- temperature as would occur near a potential host' vae that were located in an extensive pouch cov- After hatching, the lst-instar larvae assume a ering the entire inguinal area including the scro- "questing position" by standing on their caudal tum. In all 3 males, the larvae were found only ends and attach quickly to any object coming in subcutaneously and did not invade the underlying contact with them. It is believed that the larvae muscle. Furthermore, the ascended testes ap- crawl over the body of the host and are only able peared normal and undamaged. Bennett (1955) to enter through a natural body orifice. For 7 to examined 34 larvae located subcutaneously in the 10 days after entering through the nose or mouth, scrotal region of several chipmunks and found that the larvae migrate dorsally and medially between none had penetrated the muscle layer into the the skin and muscle layers until the breathing hole scrotum. However, as the larvae matured the cyst is cut, marking the site of warble formation. The commonly bulged into the scrotal sac. larvae are typically located in the posterior }/s of In Fig. I an adult male White-footed Mouse the abdomen, although they are ciccasionally (P eromy s cus Ieu c opus n oueb or a c ensis ) from south-ce n- found on the neck, back, flank, and between the tral Minnesota is shown. A bot fly larva (Cuterebra forelegs. Commonly 1-3 larvae are found per host, sp., probably fontinella Clark) is located in the in- with similar infection rates for male and female guinal region of this mouse. Notice that the left chipmunks. Peak infections occur from mid-Au- side of the scrotum is enlarged and light in color. 198I Timm & Lee: Do bot flies emasculate their hosts? , c

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Frc. 1. An adult male White-footed Mouse, Peromlscus leucopus noueboracensis,with a single bot fly larva (Cuterebrasp., probably/ontinella) located in the scrotal region. A: The open breathing pore (bp) cut by the bot can be seen in the right scrotum; the left scrotum is enlarged, typical of mice in breeding condition. B: Removing the skin and underlying muscle layer reveals the larval bot (bot) opposite the left testicle (tes). C: The right testicle is entirely intact, but has been slightly displaced by the bot.

Just beneath the skin is an enlarged testicle, typical as much as the one shown in Fig. l. Generally, the of mice in breeding condition. The right side of testes retain their normal position in the scrotum. the scrotum is not enlarged and is darker. Beneath Bot fly larvae have physiological effects on their the skin on the right side is a bot fly larva. Its place- hosts. Significantly lower erythrocyte counts, he- ment in this particular mouse is exactly opposite matocrit percentages, albumin-globulin ratios, and the left testicle and the right testicle is not visible; hemoglobin concentrations were found in mice thus it appears as if the bot has consumed the right parasitized by cuterebrid larvae, while the leuco- testis. However, a closer examination reveals that cyte number, spleen size, and thymus size were sig- the right testis is present, but has been slightly dis- nificantly larger (see Bennett 1973, Childs & Cos- placed (dorsally) by the bot. The length, width, and grove 1966, Clough 1965, Dunaway et al. 1967, weight of both testicles were identical (I4 x 9 mm, McKinney & Christian 1970, Payne et al. 1965, Se- 0.5 g). Both the left and right epididymis con- lander 1961, Timm & Cook 1979).Tissue damage tained viable sperm and were highly convoluted. by Cuterebra was reported by Payne & Cosgrove The right testis did show increased vascularization (1966), but they found healing and repair of dam- in the area adjacent to the bot fly larva. A super- aged tissue tg be rapid once the bot emerged. ficial examination of this mouse would have sug- Smith (1977) reported a reduction in testessize in gested that the bot emasculated its host; however, Deer Mice (Peromyscusmaniculatus) artificially in- both testeswere present and producing sperm. fected with Cuterebra.Timm & Cook (1979) dem- Cryptorchidism, or undescended testes,may re- onstrated that, in adult female White-footed Mice sult in lowered fertility (see Baudoin 1976); how- parasitized by Cuterebrafontinella, there was no sig- ever, this probably is not a major factor in bot fly nificant decrease in the number of embryos, cor- parasitism. It is unusual for a testis to be displaced pora lutea, or placental scars; in adult male mice 336 J. Med. Entomol. Vol.18, no.4

the presence of I or 2 larvae had no effect on the Caullery, M. 1952. Parasitism and,qmbiosis. Sidgwick and Jack- size of the reproductive organs. A few authors son Limited, London. 340 p. Chandler, A. C. & C. P. Read. 1961. Introduction to parasitolog). have suggested that high populations of Cuterebra John Wiley & Sons, Inc., New York. 822 p. one year may cause a decrease in mouse popula- Cheng, T.'C. 1973. General parasitology. Academic Press, New tions the following year (Hensley 1976, Selander York. 965 p. 1961, Sillman 1955, Wecker 1962),but this has yet Childs, H. E., Jr & G. E. Cosgrove. 1966. A study of patho- logical conditions in wild rodents in radioactive areas. Am. to be carefully documented. The genus Cuterebra Mid.I. NaL 76:309-24. l is found only in the New World; Old World murid Clough, G. C. 1965. Physiological effect of botfly parasitism rodents and rabbits exposed to cuterebrids expe- on meadow voles. Ecologl 46: 34446. fly (Cuterebridae) from rience greater hardships and mortality than New Dalmat, H.T. 1942. A new parasitic the northern white-footed mouse../. N.Y. Entomol. Soc. 50: World cricetid rodents and rabbits (Catts 1965, 45-59. Baird 1979).Timm & Cook (1979) postulated that Dunaway, P, B.,J. A. Payne, L. L. Lewis &J. D. Story. 1967. many of the New World hosts have evolved a tol- Incidence and effects of Cuterebra in Peromlscus.J. Mammal. erance for cuterebrid parasitism. 48:38-51. Fitch, A. 1857. Third report on the noxious and other insects To summarize, costs to the host of added energy of the state of New York. Trans. N.Y. State Agric. Soc. 16z requirements and other physiological or behavior- 3 l5-490. al changes may or may not lower reproductive fit- Forbes, R. B. 1966. Studies of the biology of Minnesotan chipmunks. Am. Mid,I. Nat. 7& 290-308. ness,but we conclude that Cuterebradoes not emas- Goertz, J. W. 1966. 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