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Stable Fly Phenology in a Mixed Agricultural-Wildlife Ecosystem in Northeast Montana

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Kristina M. Friesen, Gregory D. Johnson
DOI: http://dx.doi.org/10.1603/EN12231 49-57 First published online: 1 February 2013

Abstract

The stable fly, Stomoxys calcitrans (L.), is a cosmopolitan species of blood-feeding Muscidae and an important pest of cattle. Although the cattle industry is the largest commodity in Montana, no research has been conducted on the abundance, distribution, or impact of stable flies in the state. Observations of stable flies attacking West Nile virus (family Flaviviridae, genus Flavivirus, WNV) -infected pelicans on a refuge in close proximity to pastured and confined cattle provided an opportunity to describe stable fly phenology in a mixed agricultural-wildlife ecosystem. Coroplast cards used to monitor and compare adult populations in three habitats (peninsula, pasture, confinement lot) located within 1.5-4.5 km of each other revealed that temporal dynamics differed by site. Adult abundance was generally lowest at the confinement lot, the only location where larval development was identified. Stable flies were collected on all traps placed in pasture, with traps adjacent to pastured cattle consistently collecting the most. Adults also were collected on the peninsula supporting the pelicans' nesting site, but whether the potential hosts or physical landscape served as an attractant is unclear. At all three sites, data indicated that overwintering was not successful and that a transition occurred from early season immigrating adults that used suitable local larval development substrates to subsequent autochthonous populations.

  • dispersal
  • cattle
  • pasture
  • peninsula
  • American white pelican

Introduction

Stable flies, Stomoxys calcitrans (L.), are cosmopolitan, blood-feeding muscids that will attack livestock, wildlife, and companion animals (Bishopp 1913, Hogsette and Farkas 2000). Both males and females feed daily, generally on the lower extremities of hosts. Painful bites and daily persistence of stable flies can cause decreased weight gains in cattle that, rather than feeding or grazing, will instead tightly aggregate, wade in water, or lie down to protect their legs. The potential annual economic impact of stable flies in the U.S. cattle industry may be as high as US$2 billion per year (Taylor et al. 2012), which, in addition to losses in the horse and tourist industries (Koehler and Kaufman 2006), has justified a nation-wide stable fly research program.

Control of stable flies has proven difficult, however, partially because of their opportunistic behavior between regions as well as within sites (Rasmussen and Campbell 1981, Lysyk 1993a). For example, population peaks in Kansas (Broce et al. 2005) and southern California (Mullens and Peterson 2005) tend to be associated with precipitation, whereas peaks in the cooler Alberta climate have been correlated mainly with temperature (Lysyk 1993b). The degree to which local or long-distance dispersal contributes to population dynamics at each site may also be variable with site-specific stimuli, including host availability, weather events, or both, resulting in different dispersal models (Hogsette and Ruff 1985, Taylor et al. 2007, Beresford and Sutcliffe 2009). Larval habitats are poorly characterized, ephemeral environments that require decaying organic matter and moisture, but may be dramatically different substrates ranging from stored manure in dairies (Meyer and Petersen 1983) to piles of peanut hulls (Simmons and Dove 1941), silage (Williams et al. 1980), animal pen litter (Haines 1955, Schmidtmann 1988), and even accumulated mayfly carcasses (Pickard 1968). Because stable flies are so opportunistic, basic phenological data are needed from diverse habitats and regions so that naturally-occurring trends may be more broadly defined, and, ultimately, so that control methods may be more effectively implemented.

Our objective was to describe adult stable fly populations in a mixed agricultural–wildlife ecosystem in northeast Montana. Although cattle comprise the largest agricultural commodity in Montana, no published records detailing stable fly populations exist for this area. Furthermore, most of our knowledge concerning stable fly population dynamics has been generated from medium- to large-scale confinement lots or dairies, leaving a need to describe populations near pastured cattle and small scale operations. In 2007, stable flies were documented feeding en masse on West Nile virus (family Flaviviridae, genus Flavivirus, WNV) -infected juvenile American white pelicans (Pelecanus erythrorhynchos Gmelin) nesting at Medicine Lake National Wildlife Refuge (MLNWR) in Montana (Johnson et al. 2010). This was considered unusual behavior because stable flies have only occasionally been observed feeding on birds (Golding 1946). Furthermore, within 1.5–4.5 km of the pelican’s nesting site, which is located on a peninsula in a 1,450-ha lake, are at least two herds of cattle, each containing ≈230 cow–calf pairs. During the summer, cattle often graze in pasture close to the lake’s shoreline as a part of MLNWR’s weed management program, then, before winter, are brought back into confinement lots that are also within 1.5–4.5 km of the peninsula. These parameters provided a unique opportunity to describe stable fly population dynamics in a mixed agriculture–wildlife ecosystem in northeast Montana.

Materials and Methods

Site Description

Medicine Lake National Wildlife Refuge (48° 27′ N, 104° 23′ W, elevation 597 m) is a wetland formed by glacial recession. Comprising 12,727 ha, including Medicine Lake (3,320 ha) and Homestead Lake (518 ha), MLNWR has been a protected breeding ground for American white pelicans since 1939 (Madden and Restani 2005). The main nesting site is typically located on the tip of Bridger-man Point, a peninsula that has historically supported ≈4,000 breeding pairs and is the location where stable flies were documented feeding on sick juvenile pelicans. The narrow peninsula (site 1), ≈0.7 km long, comprised mostly silty soils with a mixture of short season prairie grasses and shrubs and three windbreaks of green ash (Fraxinus pennsylvanica Marsh), chokecherry (Prunus virginiana L.), willow (Salix spp.), and elm (Ulmus spp.). An electric fence at the base of the peninsula excludes potential predators from this area. Approximately 1.6 km south of the peninsula, 230 cow–calf pairs were allowed to graze in 585 ha of pasture (site 2). A farm located ≈4.0 km southeast of the peninsula contained several confinement lots of variable sizes. One of these lots (site 3), measuring 43.5 by 60 m, contained a round hay bale and had hay–manure–soil mixture at least 61 cm deep in most of the area. Next to this lot was the sole water source for another herd of pastured cattle that would come back from grazing to visit the trough typically twice a day (noon and evening).

Immatures

Sites 1–3 were examined visually for immature muscids with a trowel 1–2 h per wk (July and August) or 1–2 h every other week (April - June and September–October) in 2008 and 2009. After macroscopic examination, material potentially containing immature stable flies was collected for further processing at Montana State University (Bozeman, MT) within 2 d of collection. Processing included identification of stable fly pupae (Greenberg 1971) that were removed, pooled in small cups, and placed into screened cages fitted with tubular stockinette sleeves. Emerged adults were aspirated, euthanized, and species identification was confirmed. After removal of visible pupae, remaining material was placed into emergence containers where adults were euthanized and identified. Material was classified either as containing stable flies or not (binomial model).

Adults

Adult stable fly populations were monitored weekly (July and August) and 1–2 times per month (April–June and September–October) in 2008 and 2009 with white 20.3- by 30.5-cm Coroplast cards (Coroplast, Great Pacific Enterprises Inc., Granby, Quebec) coated with Tangle-Trap adhesive (Contech Enterprises Inc., Victoria, BC) (Beresford and Sut-cliffe 2006). Cards were stapled to wooden stakes so the bottom edge of the card was 20 cm above underlying vegetation (Beresford and Sutcliffe 2008a). Cards were staked along the length of the peninsula (15 cards in 2008 and 16 in 2009), which spanned an approximate distance of 0.6 km. Cards also were placed in pasture along transects perpendicular to Medicine Lake’s shore with varying distances from pastured cattle (16 cards both years). Each transect consisted of four cards. Six cards were placed along the fence perimeter of the small confinement lot during both years. All cards were removed after 24-h exposure in the field. Data were ln(y + 1) transformed before an analysis of variance (ANOVA) to detect significant differences in stable fly abundance among and within transects in pasture. Abundance among habitats also was compared with an ANOVA that included habitat, date, and habitat:date interaction as variables. Stepwise multiple regression was used to determine if weekly average temperature, precipitation, or degree-day accumulations explained rate of change in overall abundance. Weekly changes in abundance were calculated as (Nt + 1 N)/Nt where Nt is the mean abundance of the previous week and N + 1 is the mean abundance of the current week. Daily mean, minimum, and maximum temperatures and precipitation were recorded by a weather station located adjacent to refuge headquarters and submitted to the National Climatic Data Center (www.ncd-c.noaa.gov). Mean temperatures were calculated as ([maximum + minimum]/2). Degree-day accumulations were calculated using a threshold of 10°C beginning 1 January (Lysyk 1993a). Akaike’s information criterion (Akaike 1974) was used for model selection. All statistics were performed with R software version 2.12 (R Development Core Team 2011).

Stable flies were removed with paint thinner, washed in ethanol, sorted according to site, collection date, and sex, and stored for up to 8 mo in 70% ethanol. Females were classified into one of six categories (0–5) of ovarian development (Scholl 1980) with stage 0 representing newly emerged females and stage 5 representing the last stage of ovarian development. Because flies were stored in ethanol for up to 8 mo before processing, insemination status and parity were not determined (sperm rapidly degrade in spermathecae after death). However, ovarian development in stable flies is such that females classified as stage 0, 1, and 2 are nulliparous females (Lysyk and Krafsur 1993). Females classified to stages 3–5 were not further categorized as nulliparous or parous. The mean ovarian stage of up to 50 females per site per date was calculated as Σovarian stageindividual/N where N is the total number of females dissected per group. Z-scores were calculated to test the hypothesis that males and females were collected in equal proportion.

Host Interactions

To determine if card collections reflected biting activity, weekly point counts of adult stable flies were taken from both front legs (inside of one and outside of the other) of seven to 25 cows while cards were deployed during 2008–2009. All observations were made by the same individual between 1100 and 1300 hours by using binoculars. The relationship between leg counts and trap data were determined by analyzing the average leg counts and average number of flies collected along the transect nearest the grazing cattle with Pearson product-moment correlation co-efficient. In addition, the pelican colony on Bridgerman Point was monitored 3–4 d/wk April–October in 2008 and May–October in 2009. Each of the two main crèches, or groups, were observed for at least 1 h/wk for signs of stable fly attacks similar to that described by Johnson et al. (2010) as well as symptoms indicative of WNV infection.

Results

2008

Immature stable flies developed in the confinement lot after mid- to late July in 2008. Larvae and pupae were recovered mostly in spilled feed close to the round hay bale in the confinement lot. After July, larval abundance in the confinement lot decreased and few were collected for the remainder of the season. Identification of potential larval habitats on the peninsula and in pasture was limited to a late-season accumulation of algae along the shoreline in August, from which no stable fly larvae were recovered. In 2008, a total of 484 cards were monitored on 14 collection dates from April to October. In pasture, abundance did not vary within transects (F = 0.01; df = 1, 84; P = 0.92), but did vary among transects (F = 5.2; df = 3, 84; P = 0.02) with the transect closest to grazing cattle collecting more stable flies (Fig. 1). Therefore, only this transect was used to compare abundance between habitats. Temporal variation in collections did differ between habitats (F = 7.4; df = 16,191; P < 0.001) (Fig. 2A, B). One stable fly was collected mid-May on the peninsula after 70 DD10, and by late June, most traps captured stable flies. The first small increase in collections was detected proximate to pastured cattle in July. After a peak average of 500 stable flies per card, collections in pasture decreased to an average of 200 stable flies until the end of August when cards ceased collecting adults. Females collected in both pasture and the peninsula were, on average, in ovarian stage 3.0 or higher in June (Fig. 3). By mid-July, average ovarian stage decreased to 2.0 and remained at this stage for the remainder of the season. Collections of adults on the peninsula tended to be more consistent than those in pasture with an average of 150 adults per card during July–August. With the exception of one collection in August, cards around the confinement lot were also consistent and collected the fewest adults with an average of 20 stable flies per card. Ovarian stage of females collected in the confinement lot was also initially higher than 3.0, but by mid-July averaged below 1.0 (Fig. 4). Overall, cards collected approximately two males per female (Z = 73.4, P < 0.001) with an early season exception of 4.5 males per female. Rate of weekly change was explained by temperature, precipitation, and accumulated DD10 (Table 1).

Fig. 1.

Average number of adult stable flies collected per trap per day along transects in pasture. Transects were arranged such that distance from cattle increased from transect one (closest) to transect four (farthest).

Fig. 2.

Average abundance of stable flies by habitat type in 2008 (A) and 2009 (C) and rates of change as a function of accumulated degree-days above 10°C by habitat type in 2008 (B) and 2009 (D).

Fig. 3.

Average ovarian stage of stable flies collected on Coroplast cards in 2008 and 2009 by habitat type.

Fig. 4.

Sex ratio of stable flies collected on Coroplast cards in 2008 and 2009 by habitat type.

View this table:
Table 1.

Flies first were documented feeding on cattle in mid-June. In total, 175 cattle were observed. The highest level of stable fly attack was early August (Table 2). Stable flies were not seen attacking pelicans.

View this table:
Table 2.

2009

Overall, fewer adult stable flies were collected in 2009 than in 2008. Similar to 2008, abundance varied according to habitat (F = 17.7, df = 14,270, P < 0.001) (Fig. 2). A total of 565 cards were monitored on 16 collection dates from May to September. After 491 DD10 in late June, stable flies first were detected simultaneously on the peninsula and pasture. Cattle were relocated from their originally designated pastures because of low quality of forage. Therefore, cards placed in pasture reflected cattle-free prairie and were similar both within (F = 0.5; df = 3,17; P = 0.70) and among (F = 0.12; df = 3, 17; P = 0.35) transects, and all cards were used for habitat comparisons. Few adults were collected in pasture throughout the season, with a mid-July peak averaging two adults per card. Early season females averaged ovarian stage 3.2 in pasture and on the peninsula (Fig. 3). After early August, ovarian stages decreased to an average of 2.1 or less. Peak collections on the peninsula occurred during August, and although the collecting period did not include the last caught fly, collections decreased through September. Collections around the confinement lot averaged two adults per card. Ovarian stage averaged 2.8 July through August, then decreased to 1.0 or less until it increased slightly in September. During mid- to late July, all three sites collected fewer than one male per female. Otherwise, cards collected approximately two males per female for the rest of the season (Z = 32.6, P < 0.001) (Fig. 4).

Close-range access to pastured cattle limited observations in 2009 and only 37 cattle were monitored. Stable flies first were seen feeding on cattle in early July (Table 2). Biting activity increased through July, after which cattle were moved beyond access of the observer. Leg counts were not correlated with Coro-plast collections (t = 0.80, df = 11, P = 0.44). Approximately 1,500 pelican nests were occupied in 2009 and 24 juveniles displayed WNV-like symptoms.

Discussion

Adult stable flies at MLNWR in northeast Montana are active at least between late June and late September, with peak activity occurring in July and August. Because trapping was concluded in September, undetected activity may have extended into October (such as what has been recorded in Nebraska [Taylor et al. 2007]). However, an average low of 1.7°C in October makes this an unlikely scenario at MLNWR. Population data from MLNWR appear to fit into a general pattern in North America whereby peak stable fly activity occurs later as latitude increases. In Florida (Pitzer et al. 2011), peak activity occurs between January and April. In late May and early June, peak activity is seen in southern and central California (Mullens and Peterson 2005). In eastern Nebraska (Taylor et al. 2007) and Iowa (Black and Krafsur 1985), stable fly populations peak in late June to mid-July, whereas in Alberta (Lysyk 1993a), heightened activity occurs in August and September.

Correlation of weather parameters with stable fly abundance also appears to vary by region, with precipitation explaining most of the population change in the southern regions (Mullens and Peterson 2005, Pitzer et al. 2011) and temperature being the main explanatory variable in northern regions (Berry et al. 1986, Lysyk 1993a). Conclusive statements regarding the relationship of stable fly abundance and weather at MLNWR cannot be made with 2 yr of data. It is noteworthy, though, that during the study, monthly average temperatures were similar, but rainfall patterns were not (Fig. 5). Compared with average, monthly precipitation was lower in 2008 with consistent trends. In contrast, precipitation in 2009 appeared to be more sporadic, with above average precipitation in April and July and below average in May and June. Potential local larval sites in 2009 may have fluctuated between being saturated or desiccated, affecting stable fly abundance.

Fig. 5.

Monthly average temperature and total precipitation for 2008, 2009, and 10-yr average.

Successful overwintering probably does not occur at the sites investigated. Instead, stable fly populations may be initiated by early-season immigrating adults locating and using suitable, local larval developmental sites. Traps placed in the vicinity of active emergence sites would reflect a high degree of newly emerged, nulliparous females. Therefore, if the sites investigated supported overwintering, early collections should have comprised a greater proportion of young females. Rather, our data indicated that, compared with the rest of the season, females initially collected were older. Because Coroplast cards may be biased toward nulliparous females (Beresford and Sutcliffe 2006), it is difficult to extrapolate from our data the true age of the population. Regardless, seasonal trends within the same set of traps may still be interpreted. In contrast to our findings, nulliparity averaged 75% in eastern Nebraska feedlots (Thomas et al. 1990) where stable flies were thought to successfully overwinter.

The only location of the three sites investigated that appeared to support larval development was the confinement lot after mid- to late July. Larval sites may have been present but not identified on the peninsula and in pasture. However, environmental conditions make this unlikely. Both areas, composed of silty and sandy loam soils (Ross and Hunter 1976), rarely accumulated decaying organic material, a prerequisite for larval development (Hogsette and Farkas 2000). During peak temperatures, green algal blooms formed in Medicine Lake. Although algal deposits have been described as sites of immature development (Simmons and Dove 1941), these were once-a-year occurrences at MLNWR that typically were not seen until August, during which weekly investigations did not reveal developing stable flies. Given that larval development occurred in the confinement lot and not on the peninsula and pasture, it is interesting to compare stable fly dynamics at these three sites.

Although the confinement lot was the only site identified as supporting larval development, trap data indicated that this site had the lowest adult abundance. Factors influencing adult dispersal and attraction currently are poorly understood (Gersabeck and Merritt 1985). Possibly, some portion of newly emerged adults immediately dispersed despite proximity to oviposition and resting sites, hosts, and mates. Or, females capable of exhibiting choice of oviposition substrate through chemostimuli (Romero et al. 2006, Jeanbourquin and Guerin 2007a) may have dispersed to locate more suitable oviposition sites, whereas male stable flies, which can mate at least nine times, may have dispersed to locate receptive females, which probably mate only once (Harris et al. 1966). Alternatively, additional, unidentified emergence sites supporting larger immature populations but lacking any of these elements necessitated adult dispersal, which was detected by traps placed next to pastured cattle or on the peninsula.

Clearly, the presence of cattle served as an attract-ant to stable flies in pasture. While stable flies were collected along each transect, abundance was highest on cards adjacent to grazing cattle. Both visual (Agee and Patterson 1983, Zacks and Loew 1989) and chemical cues (Warnes and Finlayson 1985, Birkett et al. 2004, Jeanbourquin and Guerin 2007b) are known to influence adult stable fly behavior. The extent of influence and interaction of these cues in various ecological and physiological settings is understudied (Alzogaray and Carlson 2000, Beresford and Sutcliffe 2008b) and merits further investigation. Leg counts of stable flies did not correlate with trap collections. Vegetation in the mixed-grass prairie or shadowed areas on the legs may have obscured visualization of stable flies and hindered accurate counts. Also, the amount of time spent assessing biting activity may not have been long enough. Leg counts were conducted in less than 1 min per cow per week, whereas cards were deployed for 24 h. Adult stable flies will feed one or two times a day, and may spend from less than a minute up to 10 min on the host, imbibing varying amounts of blood, depending on the weather (Voegtline et al. 1965, Smith and Hansens 1975), physiological status of the fly (Beresford and Sutcliffe 2008b), and the individual host (Torr et al. 2006), host species (Hafez and GamalEddin 1959), and host behavior (Mitzmain 1913, Schofield and Torr 2002). There is also some evidence that suggests that cattle in open environment may become habituated to stable fly attacks, allowing a longer feeding period (Mullens et al. 2006). In this case, increased leg counts would be a reflection of habituation rather than abundance. Because numerous factors may affect biting activity, in some situations, quick leg counts may not be the optimal method of quantifying stable flies.

Originally, investigations were initiated at MLNWR to describe the transmission of WNV in a colony of American white pelicans (Hale 2007). During this investigation, masses of stable flies were documented feeding on WNV-infected juveniles (Johnson et al. 2010) in numbers that rarely have been reported for any animal, especially for birds (Golding 1946, Friesen and Johnson 2012). Initially, this observation was made when the region’s potential primary vector of WNV, the mosquito Culex tarsalis Coquillett, was in very low abundance. Subsequent vector competency studies indicated that stable flies were not capable of biologically transmitting WNV, but could mechanically vector the virus (Doyle et al. 2011). In addition to vector potential, questions arose concerning the behavioral ecology of stable flies at MLNWR. Specifically, were stable flies developing on the peninsula that supported the colony’s roosting site? If not, were they following a physical landscape (i.e., the shoreline) or were they attracted to the colony despite being within 1.5– 4.5 km of grazing cattle? Our data indicate that stable flies did not develop on the peninsula. It is unclear whether the shoreline or potential hosts attracted stable flies, but it is noteworthy that adult stable flies were documented on the peninsula and in close proximity to the colony even when no apparent outbreak of WNV occurred and few juveniles exhibited symptoms of any disease. Although WNV outbreaks within the colony consistently resulted in 30– 45% juvenile mortality rates between 2003 and 2007 (Sovada et al. 2008), manifestations of WNV infection were not apparent during both years of this study. Unlike the quick leg counts, pelicans were monitored at least 1 hr a week to document stable fly interactions. In spite of the prolonged observation time, stable flies were not seen attacking the pelicans, potentially because of host defensive behaviors of healthy pelicans such as scratching, head rubbing, or dispersal into the water. Stable flies consistently were found in an area without oviposition substrate and, likely, a low rate of successful feeding. Qualifying the role of specific chemical and visual attractants in different habitats is clearly needed.

Acknowledgments

We thank Jerry Rodriguez and the staff at Medicine Lake National Wildlife Refuge for assistance and use of facilities. We also thank Tim Lysyk, Jerome Hogsette, Kevin O’Neill, and Clayton Marlow for helpful suggestions and criticisms, and Marni Rolston for aiding laboratory and logistical concerns.

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References

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