EYEWORMS AND FACE in California

C. J. WEINMANN * J. R. ANDERSON * P. RUBTZOFF . G. CONNOLLY W. M. LONGHURST

YEWORM INFECTIONS are of eco- tor of T. californiensis, although the re- unknown reasons, and is much reduced E nomic importance in parts of Eu- port had not been substantiated. at present. rope, Asia, and Africa, where about a In the early 1960s it became apparent Early transmission studies were fo- dozen of of the genus that the westward movement of the in- cused on the canyon . Many hundreds Thelazia inhabit and irritate the eyes of troduced face fly, , of these elusive flies were caught at the a variety of large , including would soon involve California as it station during peak transmission periods such domestic as , , spanned the continent from its point of and dissected without finding eyeworm buffalo, camels, , etc. The half-inch entry into Nova Scotia from Europe in larvae. At the same time repeated at- long worms live on the surfaces of the 1950. This notorious livestock pest is a tempts were made by a variety of means eye membranes, under the eyelids, or known vector of at least two species of to infect wild-caught and laboratory- with some species, in the tear ducts or eyeworm, and there was concern about reared I;. ben jamini, but results were nasolachrymal canal. Ocular distur- its vector potential when it arrived in the almost always negative. Yet, in an oc- bances range from mild inflammation, area inhabited by T. californiensis. But casional fly, there would be some Thela- commonly manifested by excessive tear- before this question could be answered, zia development. ing and photophobia, to occasional se- it was necessary to learn something Three possibilities were considered : vere dysfunction, even blindness, of af- about how the native eyeworm was trans- (1) F. benjamini was the vector but con- fected eyes. mitted in nature. ditions were not right for infection; (2) The main study area was the Univer- the vector was an unrecognized species Life cycle sity of California Field Station at Hop- or variety that occasionally was present Female worms shed eggs which accu- land, some 100 miles north of San Fran- among the flies called F. benjamini; (3) mulate in eye and nasal secretions where cisco, where eyeworms were known to other kinds of vectors were involved. they are picked up by flies that feed on occur commonly in deer. Subsequent sur- While the first possibility seemed prob- these secretions. But the parasite will veys revealed consistently high levels of able, intensive efforts to improve infec- develop only in certain kinds of flies, transmission from 1964 to 1968, with tivity were fruitless. The second possi- the relationship generally being highly about 60% of the deer and 30% of the bility seemed least likely, considering specific and involving intracellular de- jackrabbits infected on this 4,700 acre the high transmission rate and the large velopment of the parasite within the fly. area. Occasional infections were also de- numbers of flies examined from the area. After molting and growing 10- to 20-fold tected in grey foxes, raccoons, and hunt- Representative specimens from this ma- over a month or so, the now infective ing dogs. Eyeworm prevalence then be- terial examined independently by two parasite is capable of pushing its way gan a steady decline at the station for experts on fly identification were refer- out of the mouthparts as the fly feeds on the eye secretions of another warm- blooded host. Once transmitted, the still in the eyes of a rabbit (photo by R. W. Merritt). barely-visible eyeworms grow to matur- ity in another month, mate, and soon be- gin laying eggs to complete the cycle. The only native species of mammalian eyeworm in North America is Thelazia californiensis, which is largely restricted to California and adjacent parts of neighboring states. Various mammals have been recorded as occasional hosts for this parasite, including dogs, , , horses, even man (8 recorded cases), but it occurs mainly in wild ani- mals such as deer, jackrabbits, and coy- otes in the foothill and mountainous areas of the state. In the late 1950s a group of investigators at Loma Linda University in Southern California re- ported the discovery of developing stages of this parasite in the canyon fly, Fannia benjamini, and since then, this fly has been widely listed in textbooks as the vec-

4 CALIFORNIA AGRICULTURE, NOVEMBER, 1974 able only to 8’. benjamini. So other pos- sible vectors were investigated. The focus on flies was supported by finding sev- eral sentinel jackrabbits infected with eyeworms after living in cages that essen- tially excluded all but flying insects. The arthropods regularly associated with these animals and with naturally in- fected captive dper (some 70 species or so) were examined for eyeworm larvae at all seasons of the year. All were even- tually ruled out as potential vectors, on one basis or another, except the canyon fly, which by process of elimination had to be the vector. During this effort many of the flies associated with deer, sheep, and cattle droppings (maggots as well as adult flies) were experimentally fed Thelazia eggs without significant para- site development. This was also the case with two shipments of face flies obtained from the Midwest before this fly’s inva- sion of California. But these results meant little if the infectivity of test para- Hereford with face flies, Musca autumnallis (photo by L. Dunning). sites could not be demonstrated. Obvi- ously there was more to learn about the that yielded negative results with the fection with foreign eyeworms intro- biology of F. benjamini. other flies. Early parasite growth was duced in imported animals. Such newly intracellular, within the fly’s fat-body introduced parasites could then be trans- Laboratory colonies cells. The parasites developed to the in- mitted to domesticated livestock. Indica- Occasionally in the laboratory colony fective stage in about a month and grew tions of this potential problem have come of F. benjamini, “strange” male flies into adult eyeworms when transferred to light in the last few years. Thelazia were seen. Initially these proved to be to the eyes of laboratory rabbits. This lacrymulis, an eyeworm of horses and male F. cannicularis, the , then had to be the vector of T. californi- donkeys in Europe and the Middle East, and at times a common pest fly about the ensis. Subsequent experiments with this has been found in native horses in On- laboratory premises and an occasional undescribed species of Fannia reaffirmed tario and Maryland, where face flies contaminant of the colonies. It had been these observations and provided a clue abound and are thought to carry this extensively tested as a host for Thelaziu, as to why only a few of the thousands of parasite. Larval stages of Thelaziu have and found to support little or no parasite benjamini-complex flies caught at Hop- recently been reported from face flies development. But “strange males” con- land contained developing stages of The- collected in Massachusetts. In 1971, T. tinued to be noticed even after added lazia. Some dexterity with a net is gulosa was reported occurring in the eyes precautions against outside contamina- needed to catch any of these flies (baits of a recently arrived giraffe at the Los tion had been taken. When examined and traps have not been useful) but the Angeles Zoo. This eyeworm commonly these males proved to be an unknown vector species seems to be particularly infects cattle in Europe and Asia, and is species of Fannia, tentatively identified elusive, judging from its behavior in the known to be transmitted by the face fly. as close to F. compicuu. laboratory. It probably was therefore Importers of livestock or wild animals The fact that the F. benjamini colony grossly underrepresented in the field should be alert to the possibility of such was actually a mixture of species was collections. introductions, so that the necessary pre- made much more apparent during a With the discovery of the native vector cautions may be taken. concurrent study on the egg-laying be- and its establishment in the laboratory, In summary, it might be asked havior of these flies. It was found that it was again possible to turn to the ques- whether the entry of the face fly into three distinctly different kinds of eggs tion of compatibility between the face fly California has changed the potential for were laid by females that could not and T. californiensis. By now, this fly eyeworm infections of domestic animals. otherwise be distinguished from one an- was established in California, indeed The answer is apparently “no” with re- other. With this discovery, separate col- even in the study area. Several experi- gard to the native eyeworm, but “yes” onization was possible, followed by tests ments involving exposure of local face with respect to foreign eyeworms. for eyeworm susceptibility. Flies from flies to the same pools of eyeworm eggs the now pure F. benjamini colony failed that were consistently infective for the C. J. Weinmann is Associate Professor to support any significant eyeworm de- vector species yielded no evidence of of Parasitology; 1. R. Anderson, Profes- velopment, as was the case with flies development in Mmca autumnalis, lead- sor of Parasitology; P. Rubtzofl, Re- from the colony tentatively designated ing us to conclude that the face fly is search Technician 11, University of Cdi- “near conspicua.” But in the third col- unlikely to serve as a vector for our fornia, Berkeley. G. Connolly is Research ony, both male and female flies could native eyeworm. Technician IV and W. M. Longhunt, readily be infected with eyeworms using However, the presence of face flies in Professor of Wildlife Biology, University the same pool of eggs and procedures the state does create a potential for in- of California, Davis.

CALIFORNIA AGRICULTURE, NOVEMBER, 1974 5