DEVELOPMENT,LIFE HISTORY Life History and Seasonal Abundance of Fannia benjamini Complex (Diptera: Muscidae) in Southern California

BRADLEY A. MULLENS AND ALEC C. GERRY

Department of , University of California, Riverside, CA 92521

J. Med. Entomol. 43(2): 192Ð199 (2006) Downloaded from https://academic.oup.com/jme/article/43/2/192/1060117 by guest on 27 September 2021 ABSTRACT Seasonal abundance and life history of Fannia benjamini complex (Diptera: Muscidae) was studied in the coastal mountain community of La Habra Heights in Los Angeles County, California, with additional observations in drier, inland mountains in the Woodcrest area, Riverside County. The dominant (Ͼ95% of ßy collections) was Fannia conspicua Malloch, whereas Fannia benjamini Malloch also was present. Both species could be collected nearly year-round by netting adults (almost exclusively females) attracted to people, although F. benjamini was relatively more common in cooler weather (NovemberÐApril). In La Habra Heights, adult activity peaked in June and July (both species), whereas peak activity in Woodcrest was late April through June for F. conspicua and February through April for F. benjamini. Field-collected adult females provided only water died within 2Ð4 d, whereas females provided with water plus a dry milk and sugar mixture survived up to 128Ð130 d in the laboratory. Males of F. conspicua (1Ð40 individuals) swarmed at heights of 0.5Ð4.0 m near Aptenia cordifolia (L.f.) Schwantes, an exotic, succulent, low-growing ground cover plant. Eggs of F. conspicua were deposited singly on older, decaying leaves of this plant, and adult F. conspicua emerged from Aptenia-covered areas in the Þeld. In the laboratory, larvae of F. conspicua grazed on microbial surface Þlms associated with Aptenia. Emergence of F. conspicua from Þeld-collected soilÐAptenia mixtures (held in the laboratory) occurred from 1.5 to 5 mo after collection. Widespread Aptenia planting since the 1980s has probably resulted in F. conspicua becoming a severe human nuisance in some areas.

KEY WORDS Muscidae, Fannia, Fanniinae, Aptenia

THE Fannia benjamini Malloch complex (Diptera: tions of their orientation to feeding tabanids, two- Muscidae) is found primarily in upland coastal moun- dimensional visual targets, and survival and fecundity. tain and Sierra foothill habitats of California, with However, there have been no systematic studies of some distributed in Baja, Mexico, and Arizona (Chill- “canyon ßy” activity. The immature development sites cott 1960). Commonly called “canyon ßies,” they in the Þeld have remained unknown, with the excep- range from 3.5 to 4.5 mm in length, and the complex tion of a single pupa of F. benjamini taken from a wood consists of seven species (Turner 1976). One member rat nest (Chillcott 1960). The current study was de- of the complex, F. thelaziae Turner, supports devel- signed to determine species present in selected loca- opment of nematodes (eyeworms) in the Thela- tions in southern California, to document their sea- zia, which infect a variety of mammals, including peo- sonal adult activity, and to investigate other life history aspects, particularly immature developmental sites. ple (Weinmann et al. 1974, Turner 1976). Where they are abundant, these ßies also are very signiÞcant hu- Materials and Methods man and nuisance pests, ßying around and sometimes landing on the face and other parts of the Study Sites. Primary study sites were two residences and a horse riding ring area in coastal mountain habitat body. in the city of La Habra Heights, Los Angeles County Despite their abundance and pest status, very little (33Њ 57Ј N, 117Њ 57Ј W, 280-m elevation). This area has is known about “canyon ßy” biology. Winkler and numerous hills and canyons with both endemic and Wagner (1961) reared F. benjamini complex from eggs exotic trees, including coast live oak, Quercus agrifolia derived from wild-caught females, and superÞcially Nee; sycamore, Platanus racemosa Nutt.; Brazilian described larval development in the laboratory. Poor- pepper, Schinus terebinthifolius Raddi; and Eucalyptus baugh (1969) reared F. benjamini through two labo- spp., with arroyo willow, Salix lasiolepis Benth, and ratory generations, describing some aspects of its im- black willow, Salix nigra Marsh, in the drainages. The mature development, laboratory mating behavior, and natural habitat in treeless areas is coastal sage scrub, larval feeding behavior. Garcia and Rodovsky (1962) where common plants include California buckwheat, observed adult feeding behavior of wild-caught adult Eriogonum fasciculatum Benth, and California sage- female F. benjamini and made preliminary observa- brush, Artemisia californica Less. The area receives

0022-2585/06/0192Ð0199$04.00/0 ᭧ 2006 Entomological Society of America March 2006 MULLENS AND GERRY:CANYON LIFE HISTORY 193

Ϸ41 cm of rainfall per year, and Ͼ80% of this rainfall water in a vial, 4) liquid whole milk on tissues plus 10% occurs between November and April. Average high sugar water in a vial, and 5) fresh beef liver plus 10% and low air temperatures in January are 20.8 and 7.6ЊC sugar water in a vial. The liver and whole milk were and in July 28.0 and 17.3ЊC, respectively. replaced every 2 d. were maintained at 23 Ϯ1ЊC and Other observations were made in the Woodcrest natural photoperiod and monitored every 1 to2dfor area of western Riverside County (33Њ 53Ј N, mortality (dead ßies were removed) until all had died. 117Њ 21Ј W, 430-m elevation). This area is topograph- The numbers of adult females dying in the different food ically somewhat similar to La Habra Heights, but is treatments were subjected to survival analysis. drier, hotter in summer, and cooler in winter. Natural Observations on Mating Behavior and Immature areas (without irrigation) have essentially no trees Development Sites. Observations of male swarming except in the drainages, where sycamore, Eucalyptus behavior (location, time of day, and approximate num- spp., and black willow are common. The sage scrub ber of individuals) were made in the Þeld in May and habitat is more sparse but with many of the same June 2003 and 2004 in Woodcrest, and in July 2004 at Downloaded from https://academic.oup.com/jme/article/43/2/192/1060117 by guest on 27 September 2021 plants. The area receives 27 cm of rain per year, also the horse riding area in La Habra Heights. almost all between fall and spring. Average high and Large, tent-type emergence traps (Fig. 1) were de- low temperatures in January are 19.6 and 5.7ЊC and in signed and deployed in spring and summer 2004. July 30.7 and 17.3ЊC, respectively. Fiber-reinforced, brown plastic tarps (either 1.5 by Seasonal Adult Activity. Because adult “canyon 2.2 m or 2.5 by 3.1 m) formed the “skirt” of the trap and ßies” are attracted to the vicinity of people or , had a 12-cm hole cut in the center. Marine plywood their activity was documented by collecting ßies at- (two layers each 1.9 cm in thickness) was used as a top. tracted to the researchers using a short-handled, 45-cm The rectangular plywood pieces (25.4 by 15.2 cm) had diameter aerial sweep net. Collections initially were holes cut and offset toward one end- the top hole was made from both residences and the horse riding area in 10.9 cm in diameter and the bottom hole was 11.7 cm La Habra Heights. Weekly collections were made be- in diameter. A Þtted 2-liter clear polystyrene jar lid ginning 13 May 2003 and continued through 14 August (screw top) nested tightly in the opening, and a con- 2003. Collections continued at the horse riding area ical piece of clear plastic was formed into a cone and were made every 2 wk between 26 August and (glued to the lid) to impede exit of ßies that made their 29 January 2004. Weekly collections at the horse riding way into the trap container. One side of the jar itself area resumed on 4 March 2004 and continued through had a hole 9 cm in diameter and covered by 16 mesh 19 August 2004. Collections generally were made in the window screen to provide ventilation. The jars thus morning between 0900 and 1030 hours. could be easily removed and capped with a solid lid to On each sample date, a researcher stopped for 5 min obtain collected . at each of four consecutive, regular locations situated The tarp was held securely between the two pieces 30Ð75 m apart. Flies attracted to the person were of plywood, which were fastened together using bolts. collected by net, killed in a cooler with dry ice, and The underside of the plywood end opposite the hole placed in a labeled vial for transport back to the lab- had a metal screw base afÞxed, and a 1.3-cm-diameter, oratory for counting and identiÞcation. Flies were sturdy plastic pipe was screwed into it. The pipe was identiÞed using keys in Turner (1976) and through 61 cm in length for the larger tarp and 46 cm in length comparison with identiÞed material in the California for the smaller tarp. Academy of Sciences, San Francisco, CA. To deploy the trap, a 1-m-long piece of metal re- The two researchers were compared in La Habra inforcing bar (1 cm in diameter) could be hammered Heights for attraction and netting efÞciency on three into the soil, and the pipe slid down onto it. This formed dates in July and August 2003. On those dates, the two a tentlike center pole. Tent stakes were pounded researchers stood Ϸ4 m apart and netted ßies for through the grommet holes at the edges of the tarp, matched 5-min periods (n ϭ 10). Numbers of “canyon securely holding the trap in position. The edges of the ßies” collected were compared using a paired t-test. tarp were buried using soil. The 10 traps were deployed Net collections also were made in Woodcrest, in a variety of locations thought to be possible develop- where periodic observations were made on relative mental sites for canyon ßies. These included organic adult activity between April 2003 and July 2004. These debris accumulations beneath trees and shrubs, moist collections, although not done regularly as in La Habra areas near the bottom of drainages, loose soil into which heights, allowed determination of species present and seasonal grass growth had been plowed for Þre control, some assessment of seasonal activity in a drier, inland hillside areas with gopher burrowing activity, and hill- southern California location. side stands of Aptenia cordifolia (L.f.) Schwantes, an Adult Longevity. On the morning of 24 July 2003, a exotic, succulent ground cover planted extensively in the large number of F. conspicua adults were collected area since the 1980s for esthetics, erosion, and Þre con- from a researcher at the horse riding area in La Habra trol. Traps were left in place for 2Ð6 wk and then moved Heights. These were returned to the laboratory and to new locations. set up in 237-ml cardboard containers (20 females per Emergence from Field Soil or Vegetation. Samples container and Þve containers per treatment) with were taken from 0.25-m2 Aptenia-covered hillside ar- different food and water sources (treatments) as fol- eas on 30 July and 6 August 2004. Twelve small soil lows: 1) a deionized water vial with wick, 2) a water samples (80Ð150 g) from the top 6 cm under Aptenia vial plus a small dish of dry milk and sugar, 3) 10% sugar were removed on 30 July, returned to the laboratory, 194 JOURNAL OF MEDICAL ENTOMOLOGY Vol. 43, no. 2 Downloaded from https://academic.oup.com/jme/article/43/2/192/1060117 by guest on 27 September 2021

Fig. 1. Emergence trap used to survey for Fannia spp. immature developmental sites. weighed, oven-dried (50ЊC) for 3 d, and reweighed to coloring laterally on the dorsal, anterior abdomen calculate percentage of moisture. Separate samples of (gray in benjamini). Voucher specimens have been soil and vegetation (4 liters each) from the same gen- deposited in the Department of Entomology Research eral areas were removed on 6 August. These were held Museum, University of California, Riverside. in the laboratory for ßy emergence in plastic dishpans Overall, F. conspicua was far more common. It com- with emergence tops (Mullens et al. 1996) and prised between 94 and 98% of the total Fannia indi- checked every 1Ð3 d until 2 January 2005 (149 d after viduals collected at the three sampling locations in La initial collection). Sample 1 contained mostly vegeta- Habra Heights. All specimens collected by sweep net tion (Aptenia and pine needles) and was misted with at these sites were female. The seasonal activity of the deionized water periodically (usually every 1 to 2 d) two species is shown in Fig. 2. The dominant species, beginning on 6 August. This sample was allowed to dry F. conspicua, was collected from early April through out from 24 October (80 d after initial collection) December, with a distinct peak in activity in June and through 19 November (106 d after collection) and July. From mid-June through mid-July, collections then rewet and misted again through 2 January. Sam- ranging from 500 to 850 ßies/20 min (up to Ͼ40 ßies ple 2 contained Aptenia and soil (top 6 cm of soil). It per minute) were documented. Flies were persistent also was misted every 1 to 2 d beginning on 6 August. and ßew near the collectors, particularly the head, Three samples consisting primarily of the soil col- waist, and feet. F. benjamini was never abundant, but lected beneath Aptenia (top 6 cm of soil with some it also was most common in June and July in La Habra Aptenia leaves and roots) also were taken. One of Heights, and the correlation coefÞcient (r) between these samples (sample 3) was misted beginning on 6 its activity and that of conspicua was 0.797. However, August, the second (sample 4) was misted beginning F. benjamini seemed to be relatively more common in on 7 September (31 d after collection), and the third cooler months. Between May and October 2003 in La (sample 5) was misted beginning on 10 October (64 d Habra Heights (horse riding area), 2.5% of 3,087 can- after collection). Canyon ßies were collected every yon ßies were F. benjamini, whereas between Novem- 1Ð3 d to determine numbers and sex of emerging ßies and how long emergence from a given sample might ber 2003 and April 2004, 55.9% of 34 ßies were continue. F. benjamini. Collections from people in Woodcrest also were Results predominantly female F. conspicua. Activity of this Species and Seasonal Abundance. Two species in species was highest (up to Ϸ40 ßies per 5 min col- the complex, F. benjamini s.s. and F. conspicua, were lecting period) early and late in the day between late collected in southern California. F. benjamini could be April and early June, with another apparent activity separated morphologically from F. conspicua because peak in September and October. No F. conspicua were of the orange base of the arista in conspicua (black in taken between January and March. In contrast, can- benjamini). Specimens of F. conspicua also tended to yon ßies taken in February and March were F. ben- be slightly smaller and usually had pale, yellowish jamini, which was never as common as F. conspicua March 2006 MULLENS AND GERRY:CANYON FLY LIFE HISTORY 195 Downloaded from https://academic.oup.com/jme/article/43/2/192/1060117 by guest on 27 September 2021

Fig. 2. Seasonal abundance (ßies attracted to and collected in 20 min by a person using a sweep net) of Fannia spp. at the Las Palomas riding ring area in the city of La Habra Heights, CA. became later in the year. Occasional specimens of 2003 and maintained in the laboratory is shown in F. benjamini were taken in Woodcrest in August and Fig. 3. A survival analysis was performed on the num- October. bers dying per time interval by treatment (MINITAB We, both Ϸ72-kg males, did not differ in the number Release 14.12; Minitab, Inc., University Park, MD). of “canyon ßies” collected in the 10 matched, 5-min The mean times Ϯ SD to death for the treatments were time intervals using a paired t-test on the differences 1.1 Ϯ 0.1 d for water only, 7.8 Ϯ 6.1 d for 10% sugar (t ϭ 0.68, df ϭ 9, P ϭ 0.51). Individual 1 collected an water plus raw liver, 12.4 Ϯ 4.7 d for 10% sugar water average (ϮSE) of 65 Ϯ 34 females per 5-min period, plus liquid milk, 14.9 Ϯ 5.6 d for 10% sugar water, and whereas individual 2 collected an average of 48 Ϯ 17 43.2 Ϯ 37.6 d for water plus a mixture of dry milk and females per 5-min period. dry sugar. All ßies given water only were dead by 4 d. Adult Fly Survival. Proportional survival of adult Flies given 10% sugar water diets (alone or with milk female F. conspicua collected in the Þeld on 24 July or liver) survived for up to 24Ð26 d, and some ßies

Fig. 3. Survival of cohorts (100 females each) of Þeld-collected adult F. conspicua held in the laboratory with different food and water sources. 196 JOURNAL OF MEDICAL ENTOMOLOGY Vol. 43, no. 2

seemed to return to the approximate original location. In Woodcrest males repeatedly gathered near the peak of a single-story house roof at heights of 3 to 4 m. Swarms also were regularly seen at lower heights (0.5Ð2 m) above a hillside covered by Aptenia. The same locations were used on multiple days and for at least several weeks. Males rarely also were taken while sweep- netting near the collector in Woodcrest, and on one occasion mating with a captured female occurred almost immediately in the sweep net. In La Habra Heights, swarming males were observed at heights of 1 to2min the opening of a shed and near a line of short pine trees,

both in the vicinity of Aptenia-covered slopes. Downloaded from https://academic.oup.com/jme/article/43/2/192/1060117 by guest on 27 September 2021 The emergence traps initially failed to collect Fan- nia when deployed in La Habra Heights (AprilÐJune 2004) for 2Ð6 wk at a time over a variety of potential Fig. 4. Eggs of F. conspicua deposited in the Þeld on older habitats. These included leaf debris beneath trees, soil leaf of A. cordifolia. in the bottom of a wet drainage, damp soil on a grassy bank below a horse watering trough, soil that had been plowed to bury seasonal grasses for Þre control, and lived up to 128Ð130 d on the water plus dry milk and soil that had recent gopher activity. After observing dry sugar diet in the laboratory. In pairwise compar- males swarming directly above an Aptenia-covered isons of the survival curves, the differences were very slope in Woodcrest, an emergence trap was deployed highly signiÞcant statistically (␹2Ͼ 315.8, df ϭ 1, P Ͻ there in early June 2004, and it collected four to six ßies 0.000) for all comparisons except 10% sugar water per day for the next 3 d. To eliminate any possibility versus 10% sugar water plus milk (␹2 ϭ 2.61, df ϭ 1, P ϭ that ßies might have burrowed through small openings 0.107), 10% sugar water versus 10% sugar water plus at the base of the trap, the trap was removed and the liver (␹2 ϭ 0.73, df ϭ 1, P ϭ 0.393) and 10% sugar water Aptenia torn away from the area previously covered by plus milk versus 10% sugar water plus liver (␹2 ϭ 5.64, the trap. The top 5Ð7 cm of soil was removed and placed df ϭ 1, P ϭ 0.018). Whereas the 10% sugar water plus into plastic bags for transport to the laboratory, where it milk did differ statistically from 10% sugar water plus was placed into buckets sealed with a clear plastic lid liver, the differences were relatively subtle, and prob- coated with sticky material, except for small air exchange ably based on differences in the shape of the curve openings (1 mm in diameter). Multiple F. conspicua early in the trial (mortality in the Þrst several days was emerged from the soil as late as 7 wk after collection. nil in the liquid milk treatment, but was higher in the Subsequently eight more traps were deployed over liver treatment). Adult longevity clearly was ex- Aptenia-covered slopes in La Habra Heights near the tremely low with water only, intermediate with liquid horse riding area. Four of these were placed over a food sources, and high with liquid water plus dry milk recently covered (Ϸ1 to 2 yr) slope, whereas the and dry sugar. remaining four were placed over Aptenia that had Fannia eggs were observed when they were depos- been there for several years. Traps on the recently ited in clear view on the mesh screen of the containers, covered slope yielded occasional F. conspicua, or more rarely on the liver, milk-soaked tissues, or whereas the traps placed over the older Aptenia wicks. Statistical comparisons were not conducted be- growth often had 1Ð5 F. conspicua in the collecting cause of the differential mortality in the treatments heads when checked the following week. and the fact that speciÞc oviposition materials were The older mats of Aptenia were Ϸ10Ð20 cm in depth. not supplied. Still, ßies laid no eggs when provided They had newer growth on top and older leaves in water only. Despite their much longer average life various stages of decay beneath. When the top layers span, females given water, dry sugar, and dry milk were lifted back, the older leaves were observed to have deposited a total of only Ϸ20 eggs. Flies in the re- numerous Fannia eggs on them (Fig. 4). Eggs were laid maining treatments deposited Ϸ60 eggs (10% sugar singly and in depressions or folds in the vegetation. water), 80 eggs (10% sugar water and liquid milk), and The Þrst F. conspicua emergence from samples Ͼ400 eggs (10% sugar water and liver). taken 6 August was observed 52 d later. The sample Mating Behavior and Developmental Sites. Loose with only vegetation (sample 1, Aptenia plus some swarms of F. conspicua males were observed in AprilÐ pine needles) produced 78 ßies from 52 to 67 d post- June in Woodcrest and in July in La Habra Heights. collection (Fig. 5A). Weighted mean time of emer- Swarms in Woodcrest were seen primarily early (be- gence (through 67 d) for this group of ßies was 56.8 d fore 1000 hours) and late (after 1600 hours) in the day, for males and 59.8 d for females. After drying and then and the La Habra Heights males were observed being wetted again beginning 106 d after initial col- swarming in late morning (1100Ð1200 hours). Swarm- lection, two more ßies (males) emerged 145 d after ing sites contained from one up to Ϸ40 individuals. initial soil collection. The sample with Aptenia plus soil Individual males in the swarms would hover brießy (sample 2) produced 59 ßies from 52 to 80 d postcol- and pursue other males entering their area and then lection (Fig. 5B). Weighted mean time of emergence March 2006 MULLENS AND GERRY:CANYON FLY LIFE HISTORY 197 Downloaded from https://academic.oup.com/jme/article/43/2/192/1060117 by guest on 27 September 2021

Fig. 5. Emergence of adult F. conspicua from soil or vegetation samples collected in early August under A. cordifolia in La Habra Heights, CA. (A) ApteniaÐpine needle mixture (vegetation only) misted from day 0Ð80 after collection, allowed to dry, and then remisted beginning at day 106. (B) ApteniaÐsoil mixture misted from day of collection. (C) Soil with some Aptenia leaves and roots misted beginning at day 31 after collection. Females, F; males, Œ. was 53.6 d for males and 58.3 d for females. The soil (sample 4) produced 27 ßies Ϸ1 mo later, with males sample wetted from date of collection (sample 3) emerging after an average of 59.8 d and females after yielded no ßies. The sample with soil wetted after 31 d 63.3 d (Fig. 5C). The soil sample wetted after 64 d 198 JOURNAL OF MEDICAL ENTOMOLOGY Vol. 43, no. 2

(sample 5) produced a single male and a single female eggs, although they died in Ͻ25Ð27 d. Some of these 149 d after initial collection (85 d after wetting). Soil were laid on the liver itself, but most were deposited samples taken from beneath the Aptenia on 30 July on the mesh container screen, which all other ßy food (the week before emergence samples were taken) treatment groups also had. Poorbaugh (1969) fed ranged from 0.8 to 10.1% moisture. Periodic visual adult F. benjamini on liquid blood of various species, examination of the samples indicated that the larvae of supplemented with honey-soaked pads. Garcia and F. conspicua tended to feed on the moist and decaying Radovsky (1962) observed that F. benjamini fre- surface of Aptenia leaves and stems, grazing on surface quently fed on blood from tabanid wounds in the Þeld tissue and associated microßora. and on mouse blood in the laboratory. Garcia and Radovsky (1962) also dissected wild-caught females over time (gonotrophic status unknown at capture) Discussion that were held with or without blood as a protein

These are the Þrst substantial Þeld life history stud- source; both groups had access to sugar solution. Some Downloaded from https://academic.oup.com/jme/article/43/2/192/1060117 by guest on 27 September 2021 ies with members of the F. benjamini complex. In (two of Þve) sugar-fed females had eggs, but 12 of 13 general, the muscid subfamily Fanniinae is temperate blood-fed females had eggs, suggesting F. benjamini in distribution, but the benjamini group has a prepon- requires a protein source for oogenesis. A liquid form derance of Neotropical members (Chillcott 1960). of protein probably is necessary for proper egg de- Two other members of the genus, Fannia canicularis velopment in F. conspicua, but further studies are (L.) and F. femoralis (Stein), are common in southern needed. Although a few males were collected in California but are intolerant of high temperatures Woodcrest by sweep netting near the collector, the (above Ϸ27Ð30ЊC) (Meyer and Mullens 1988). It majority of ßies collected in this way at all sites con- seems that F. conspicua and particularly F. benjamini sistently were female. The attraction of almost exclu- share this trait, because their numbers drop with the sively females to a vertebrate also suggests vertebrates onset of very hot summer weather, and they seem to may be a source of materials required for oogenesis be far more common in coastal mountain range hab- and would explain the powerful attraction of female itats than in warmer inland areas. The current study canyon ßies to carbon dioxide (Gerry and Mullens suggests F. benjamini may be more sensitive to high 2006). temperatures than is F. conspicua, but more studies on Observations on mating behavior of F. conspicua in temperature relationships are warranted. The distinct the Þeld (small male swarms often near cover such as seasonal peak abundance of “canyon ßies”, especially low tree boughs) are consistent with other members F. conspicua, may reßect temperature variation, sea- of the subfamily (Chillcott 1960). It was the presence sonal rainfall (see below) or both. Winkler and Wag- of males near the succulent ground cover A. cordifolia ner (1961) reportedly worked with F. benjamini in the that prompted examination of soil under Aptenia (or laboratory using adults collected primarily in the San Aptenia itself) as a larval development site. Bernardino Mountain foothills (Lytle Creek area). As a group, Fannia spp. use a very wide array of They observed, but did not document, adult activity organic substrates for development, ranging from from early spring through fall; early season activity was fungi and rotting plant material to decaying animals or midday, whereas summer activity was early or late in manure (Chillcott 1960). The older stands of hillside the day. However, they did not address how the ßies A. cordifolia, which seem to be a key type of devel- were identiÞed; they may not have been aware of opment site for F. conspicua, represent a leaf litter or closely related species, and some species were added possibly fungiÐmold type habitat, but it is unclear to the complex subsequently (Turner 1976). exactly what immature F. conspicua are feeding on. Chilcott (1960) noted that Fannia spp. commonly Egg deposition in small depressions also was noted in feed on natural plant sugar sources such as honeydew the laboratory by Winkler and Wagner (1961). Poor- and plant sap. We are unaware of quantitative studies baugh (1969) observed that larvae of F. benjamini fed on prevalence of sugar feeding in nature, but the on the surface of moist (but not wet) microbial Þlms laboratory data show that sugar or food of some kind on fecal or alfalfa pellets in the laboratory and did not is essential for adult survival beyond a very few days. enter the substrate. This agrees with our observations Winkler and Wagner (1961) supplied adult F. ben- on feeding by larvae of F. conspicua. The pattern of jamini with either no food, sugar, or protein hydro- depositing eggs singly in depressions of old Aptenia lysate. Flies with no food died in Ͻ2 d, and they leaves was seen frequently in the Þeld and agrees with reported (but did not quantify) that ßies with access the single egg deposition patterns seen in the labora- to sugar lived longer than ßies with protein access. tory. Similarly, Garcia and Radovsky (1962) observed that At least two other local species, F. canicularis and ßies fed only blood in the laboratory lived only Ϸ2d, F. femoralis, tolerate rather low moisture levels (40Ð whereas ßies fed sugar solution lived Ϸ2 wk. Our data 47% moisture) in the poultry manure in which they show that ßies with no food die very quickly. The best develop (Mullens et al. 2002). The moisture of soil survival (up to 128Ð130 d) was by ßies given access to collected in La Habra Heights in July (near the end of water and to dry milk and sugar. peak adult abundance) beneath A. cordifolia was ex- Although egg production was not carefully quanti- ceedingly low (Յ10%). Despite this, live immatures of Þed, ßies with access only to sugar laid very few eggs. F. conspicua were present. With or without supple- In contrast, ßies with access to raw liver laid many mental moisture, adult ßies emerged 7Ð21 wk after March 2006 MULLENS AND GERRY:CANYON FLY LIFE HISTORY 199 sample collection in early August, and males tended spicua and especially F. benjamini, whose immature to emerge a bit earlier than females. Protandry in habitat we did not Þnd) must use other types of larval F. benjamini in the laboratory also was noted by Poor- habitats with which they evolved. People have unwit- baugh (1969), who documented emergence from rab- tingly supplied F. conspicua with a highly suitable but bit feces in 25Ð63 d (20Ð26ЊC). Winkler and Wagner unnatural habitat; the natural habitat could be similar (1961) reported emergence in “somewhat Ͼ15 d” at (e.g., leaf litter in well-drained slopes), especially if it temperatures of 20Ð25ЊC. receives some supplemental moisture via irrigation. Chillcott (1960) and Poorbaugh (1969) discuss the We did not evaluate whether removal of A. cordifolia possibility of a prepupal diapause in “canyon ßies”, and could reduce subsequent adult Fannia numbers, but it Poorbaugh (1969) documented extended develop- is a logical next step. If so, the beneÞts of reduced ment (prolonged larval or pupal stage) of F. benjamini “canyon ßy” nuisance would need to be balanced in rearing dishes that were allowed to dry out. Such a against beneÞts of A. cordifolia as an attractive ground phenomenon could inßuence the seasonal occurrence cover useful for erosion and Þre control. Downloaded from https://academic.oup.com/jme/article/43/2/192/1060117 by guest on 27 September 2021 of adult F. conspicua and possibly F. benjamini as well; the rather prolonged ßy emergence from our labora- tory-held samples does suggest stasis in dry conditions. Acknowledgments Very small numbers of adults emerged as long as 5 mo The observations and cooperation of several La Habra after collection from samples Þrst wetted 1 to 2 mo Heights residents, notably Carol Meisenbacher, Steve Blag- after collection. F. conspicua developed to maturity den, Shelley Andros and Francis Schultz are appreciated. We when given only vegetation, so soil is not absolutely also appreciate the assistance of Tamim Nawaey and Coralie necessary. Emerging ßies were presumably collected Szijj in sorting and identifying collected specimens. Financial very soon in the trap collecting heads, and no food support for this study was provided by the city of La Habra (e.g., protein) sources beyond the vegetation itself Heights. were available in the rearing pans. Thus the late- emerging ßies are assumed to have been present as References Cited immatures in the samples from the time of collection. Without knowing more about how temperature, Chillcott, J. G. 1960. A revision of the Nearctic species of moisture, and food quality inßuence canyon ßy de- Fanniinae (Diptera: Muscidae). Can. Entomol. Suppl. 14: “ ” 295. velopment, it is difÞcult to ascertain how many gen- Garcia, R., and F. J. Radovsky. 1962. Haematophagy by two erations they have per year. Some adult activity year- nonbiting muscid ßies and its relationship to tabanid round suggests that some emergence may occur most feeding. Can. Entomol. 94: 1110Ð1116. of the year. Larvae hatching from eggs laid between Gerry, A. C., and B. A. Mullens. 2006. Adult canyon ßy May and July in an area such as La Habra Heights enter (Fannia benjamini complex)(Diptera: Muscidae) activity a soil habitat that, although protected against temper- in southern California and use of CO2 as an attractant. ature extremes, is very dry. Seasonal rains typically do J. Med. Entomol. (in press). not occur until DecemberÐFebruary, when tempera- Meyer, J. A., and B. A. Mullens. 1988. Development of Fan- tures are cool and development may be prolonged. nia spp. (Diptera: Muscidae) at constant laboratory tem- peratures. J. Med. Entomol. 25: 165Ð171. Multiple generations of “canyon ßy” per year certainly Mullens, B. A., N. C. Hinkle, and C. E. Szijj. 1996. Impact of are possible; emergence under suitable laboratory alternating manure removal schedules on pest ßies conditions probably requires a minimum of Ϸ3to4wk (Diptera: Muscidae) and associated predators (Co- (Poorbaugh 1969). However, given the marked mois- leoptera: Histeridae, Staphylinidae; Acarina: Macroche- ture and temperature ßuctuations in nature (low or lidae) in caged layer poultry manure in southern Cali- high temperatures and dry conditions are assumed to fornia. J. Econ. Entomol. 89: 1406Ð1417. slow development), we think it is likely that there are Mullens, B. A., C. E. Szijj, and N. C. Hinkle. 2002. Ovipo- three to Þve generations per year. This deserves more sition and development of Fannia spp. (Diptera: Musci- study. dae) on poultry manure of low moisture levels. Environ. Entomol. 31: 588Ð593. Long-term residents of La Habra Heights report Poorbaugh, J. H. Jr. 1969. Laboratory colonization of the that numbers of adult “canyon ßies” have been dras- canyon ßy, Fannia benjamini Malloch, and speculation on tically higher since the early 1990s, which Þts with the the larval habitat. Calif. Vector Views 16: 21Ð24. present observations on emergence from A. cordifolia Turner, W. J. 1976. Fannia thelaziae, a new species of eye- and soil beneath it. This exotic (South African) ground frequenting ßy of the benjamini group from California cover was planted extensively for erosion and Þre and description of F. conspicua female. Pan.-Pac. Entomol. control in southern California beginning in the mid- 52: 234Ð241. 1980s. One can assume it takes several years to accu- Weinmann, C. J., J. R. Anderson, P. Rubtzoff, G. Connoly, mulate organic debris and develop a signiÞcant layer and W. M. Longhurst. 1974. Eyeworms and face ßies in California. Calif. Agric. 28: 4Ð5. of dead leaf litter in new plantings, and emergence Winkler, L. R., and E. D. Wagner. 1961. A cultured life trap data and direct observations suggest this is nec- cycle of the canyon ßy Fannia benjamini Malloch with essary for “canyon ßy” oviposition and development. observations on the natural history. Trans. Am. Microbiol. Large areas of A. cordifolia exist, and the present Soc. 80: 179Ð185. studies show that an area of only 0.25 m2 can produce 50Ð100 adult ßies. Both “canyon ßy” species (F. con- Received 24 May 2005; accepted 6 October 2005.