Open Access
Issue
Parasite
Volume 20, 2013
Article Number 17
Number of page(s) 7
DOI https://doi.org/10.1051/parasite/2013016
Published online 15 May 2013

© J. Phasuk et al., published by EDP Sciences, 2013

Licence Creative CommonsThis is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Introduction

Stable flies belong to the subfamily Stomoxyinae in the family Muscidae (Diptera). Among 18 Stomoxys species described, six species are recorded from Thailand, of which one is cosmopolitan, S. calcitrans (Linnaeus, 1758) [9, 22, 24]. Stable flies resemble house flies but can be easily distinguished by their piercing-sucking mouthparts which are conspicuous, long and project straightforward from under the head. They are important and widely distributed insect pests of livestock, wildlife and sometimes humans. Adult stable flies of both sexes are blood-sucking flies and cause painful bites and significant blood loss in some animals. High populations of biting activity can reduce animal productivity and disturb feeding resulting in reduced weight gain and milk production [25, 23]. Moreover, they may act as both biological and mechanical vectors for pathogens such as trypanosomes [19]. Stable flies may also act as an intermediate host of the nematode Habronema [21]. In Thailand, little is known about the presence of different stomoxyine fly species, their distribution and their biology. However, Masmeatathip et al. [11] and Muenworn et al. [13] described the seasonal abundance and daily activity of Stomoxys species in Thailand. Muenworn et al. [12, 13] conducted stable fly surveys and reported their distribution in Thailand. A better understanding of the seasonal and daily activity of the flies will facilitate and make fly control programs more effective. This study had the objective to evaluate the seasonal abundance and daily activity of Stomoxys species.

Materials and methods

Study sites

This study was conducted on two dairy farms in Muak Lek district, Saraburi Province (Figure 1). Saraburi is located in the central highlands of Thailand, an area of relatively high plains and plateaus about 140 km Northeast of Bangkok. The study sites are 355 and 460 m above sea level (a.s.l.). Thailand has three seasons: hot (March to May), rainy (June to October) and dry (November to February). At the time of the study, farm 1 (14° 48′ N, 101° 17′ E; 460 m a.s.l) had 10 cows and farm 2 (14° 47′ N, 101° 15′ E; 355 m a.s.l) had 57 cows in milk production.

thumbnail Figure 1.

Location of Muak Lek district (study area) in Saraburi Province, Thailand.

Specimen collection

At each site, four Vavoua traps [8] were randomly installed around sample sites at least 5 m apart from each other. The traps were placed at 5–10 cm above the ground. Stable flies were observed monthly during a one-year study (September 2010 to August 2011). Flies were captured every hour between 0600 and 1800 h. After trapping, flies in the Vavoua traps were killed using ethanol spray and preserved in 80% ethanol. Air temperature, relative humidity and light intensity were also recorded every hour by using a digital thermometer and a digital light meter at each farm. The specimens were brought back to the Department of Parasitology, Faculty of Veterinary Medicine, Kasetsart University, Bangkok, Thailand, for identification using the keys of Zumpt [24] and Tumrasvin & Shinonaga [22].

Data analysis

The total numbers of each sex of stable flies collected from traps at each collection site were analyzed using a one-way analysis of variance (ANOVA) and the time intervals were considered as treatment effects. Variations in the numbers of each sex between seasons were compared using the least significant difference (LSD) test. Stepwise multiple regression analysis was used to determine the relationship between the abundance of stable fly species and weather parameters. The data were analyzed using SPSS (Version 17, SPSS Inc., Chicago, IL, USA). All statistical significance levels were set at p < 0.05.

Results

In total, 2,520 individuals of Stomoxys species were collected during the one-year study, of which 1,622 were trapped on farm 1 and 898 on farm 2 (Table 1). The following four species were captured: S. bengalensis Picard, 1908 [15], S. calcitrans (Linnaeus, 1758) [9], S. indicus Picard, 1908 [15] and S. sitiens Rondani, 1873 [17].

Table 1.

Total numbers of Stomoxys spp. collected and their relative abundance (RA) on two dairy farms, Muak Lek district, Saraburi Province from September 2010 to August 2011.

The highest temperature was recorded in May and the lowest temperature was in October. The average relative humidity was lower in December to January during the dry season and the highest relative humidity was in September. The average light intensity was high in March to May during the hot season (Figure 2). Seasonal variations in the abundance of Stomoxys species are presented at the species and site levels in Figures 3 and 4. The highest numbers of each species were recorded in September and gradually decreased in number toward February. The second peak of most species occurred between March and April. The most abundant species was S. calcitrans (89–96%) which was found on both farms. S. calcitrans was present throughout the year. Collections of other species were too low to be meaningful for the analysis (Table 1 and Figure 7).

thumbnail Figure 2.

Mean monthly temperature and relative humidity (right axis scale) and light intensity (left axis scale) on the experimental sites (two dairy farms) from September 2010 to August 2011.

thumbnail Figure 3.

Mean number of Stomoxys spp. captured in four traps on dairy farm 1 from September 2010 to August 2011.

thumbnail Figure 4.

Mean number of Stomoxys spp. captured in four traps on dairy farm 2 from September 2010 to August 2011.

thumbnail Figure 5.

Mean numbers ± standard error bars of Stomoxys calcitrans males and females collected during three seasons on two dairy farms.

thumbnail Figure 6.

Mean numbers ± standard error bars of Stomoxys calcitrans males and females collected during one-hour intervals in three seasons on two dairy farms.

thumbnail Figure 7.

Mean numbers ± standard error bars of Stomoxys spp. males and females collected during one-hour intervals on two dairy farms from September 2010 to August 2011.

On both farms, the numbers of males of S. calcitrans were significantly (p < 0.05) greater than the females in each season (Figure 5). On farm 1, seasonal variations in the numbers of females were significant (p < 0.05), except between the hot and rainy seasons, whereas for males, seasonal variations were significant (p < 0.05), except between the hot and dry seasons and the hot and rainy seasons. On farm 2, seasonal variations in the numbers of both sexes were significant (p < 0.05). The abundance of S. calcitrans peaked in the rainy season and declined in the dry season.

On farm 1, the total number of females of S. calcitrans collected did not differ significantly among time intervals in the dry, hot and rainy seasons. The numbers of males collected showed a significant (p = 0.005) difference among time intervals in the dry season, but there was no significant difference among time intervals in the hot and rainy seasons (Figure 6). On farm 2, the total number of females collected showed a significant (p = 0.009) difference among time intervals in the rainy season, but there was no significant difference among time intervals in the dry and hot seasons. Males showed significant differences in time intervals between the hot and rainy seasons (p = 0.007, p = 0.028, respectively), but not in the dry season (Figure 6).

During the whole collection period, S. calcitrans abundance was not related to air temperature but showed a positive correlation with relative humidity and light intensity (Table 2).

Table 2.

Stepwise multiple regression analysis with correlation between total number of Stomoxys calcitrans and weather parameters in Muak Lek district, Saraburi Province from September 2010 to August 2011.

Discussion

The present study extends our understanding of the seasonal abundance and daily activity of stable flies in Thailand. In Saraburi Province, there were four species in the genera Stomoxys collected from both farms and S. calcitrans was active throughout the year. Muenworn et al. [13] found S. calcitrans to be the most abundant species followed by S. indicus. Stomoxys populations peaked in September, corresponding to the rainy season. This finding agreed with earlier work by Masmeatathip et al. [11] and Muenworn et al. [13]. This may have been due to an increase in the rainfall causing a widespread increase in suitable breeding sites which is a critical factor for eggs to hatch and the larvae to survive and successfully develop to pupae and adults. Earlier work shows that immature stages of Stomoxys (eggs and larvae) are highly sensitive to the following environmental conditions to survive and successfully develop to pupae and adults: temperature, humidity and rainfall [6, 18].

The numbers of male S. calcitrans were significantly higher than females, in agreement with the reports of Masmeatathip et al. [11] and Muenworn et al. [13]. More female S. indicus were collected than males on both farms. Similar findings were reported by Masmeatathip et al. [11].The sex ratios of S. sitiens varied between farms. Only one male of S. bengalensis was seen and that was on farm 2. The variation in the abundance of Stomoxys species that were observed may have depended on the temperature, precipitation, types of trap, trap locations and trap height [1, 7, 10, 16]. Further studies are needed to evaluate whether these differences are associated with the location or other factors that attract Stomoxys species.

The season seemed to play a major role in the daily activity patterns of S. calcitrans. In the dry and rainy seasons, the number of S. calcitrans increased throughout the day until 1500 h and gradually decreased in number toward 1800 h. In the hot season, this species was present throughout the day and peaked in abundance in the evening and a secondary peak occurred in the late morning although the numbers of females were not statistically significant among the time intervals. In previous studies, S. calcitrans was reported to have a bimodal pattern of feeding with a major peak during 0800–1000 h and a minor peak occurred during the afternoon [11]. Muenworn et al. [13] showed a bimodal activity of male S. calcitrans with peaks at 0800–1000 and 1400–1600 h while female activity increased throughout the day until 1600 h, when the activity of both males and females declined steadily until it was dark. Masmeatathip et al. [11] reported bimodal activity of S. indicus and S. sitiens with population peaks in the early morning and in the late afternoon. This finding was similar to that observed in this study. Stable flies require blood for successful mating and ovarian development, but also require nectar as a supplemental energy source for flight activity and successful blood-feeding [20]. Müller et al. [14] conducted studies on the diurnal feeding behavior of three Stomoxys species in Mali and found bimodal blood-feeding and unimodal sugar-feeding activity periods. The differences in feeding activity patterns were dependent upon the protein and nectar sources, local conditions, sampling methods and seasons. Analysis of the data showed the abundance of S. calcitrans was significantly and positively correlated with relative humidity and light intensity although the relationship was weak (R = 0.317). There were probably other factors that affected the flight activity patterns of this species. The current study has provided a step in the evolution of planning and developing control systems for insects.

Acknowledgments

We thank the Thailand Research Fund (Senior Research Scholar: RTA5280007) for financial support. We also thank Mr. Dan Guyot who assisted with English editing in a draft and the owners of the dairy farms for permission to sample on their land.

References

  1. Beresford DV, Sutcliffe JF. 2008. Stable fly (Stomoxys calcitrans: Diptera, Muscidae) trap response to changes in effective trap height caused by growing vegetation. Journal of Vector Ecology, 33, 40–45. [CrossRef] [Google Scholar]
  2. Bruce WN, Decker GC. 1958. The relationship of stable fly (Stomoxys calcitrans) abundance to milk production in dairy cattle. Journal of Economic Entomology, 51, 269–274. [Google Scholar]
  3. Campbell JB, Berry IL, Boxler DJ, Davis RL, Clanton DC, Deutscher GH. 1987. Effects of stable flies (Diptera: Muscidae) on weight gain and feed efficiency of feedlot cattle. Journal of Economic Entomology, 80, 117–119. [PubMed] [Google Scholar]
  4. Campbell JB, Skoda SR, Berkebile DR, Boxler DJ, Thomas GD, Adams DC, Davis R. 2001. Effects of stable flies (Diptera: Muscidae) on weight gains of grazing yearling cattle. Journal of Economic Entomology, 94, 780–783. [CrossRef] [PubMed] [Google Scholar]
  5. Catangui MA, Campbell JB, Thomas GD, Boxler DJ. 1997. Calculating economic injury levels for stable flies (Diptera: Muscidae) on feeder heifers. Journal of Economic Entomology, 90, 6–10. [PubMed] [Google Scholar]
  6. Cruz-Vazquez C, Mendoza IV, Parra MR, Garca-Vazquez Z. 2004. Influence of temperature, humidity and rainfall on field population trend of Stomoxys calcitrans (Diptera: Muscidae) in a semiarid climate in Mexico. Parasitologia Latinoamericana, 59, 99–103. [Google Scholar]
  7. Gilles J, David JF, Duvallet G, Rocque S De La, Tillard E. 2007. Efficiency of traps for Stomoxys calcitrans and Stomoxys niger niger on Reunion Island. Medical and Veterinary Entomology, 21, 65–69. [CrossRef] [PubMed] [Google Scholar]
  8. Laveissière C, Grébaut P. 1990. Recherches sur les pièges à glossine (Diptera: Glossinidae). Mise au point d’un modèle économique: le piège « Vavoua ». Tropical Medicine and Parasitology, 41, 185–192. [Google Scholar]
  9. Linnaeus C. 1758. Systema naturae per regna tria naturae, secundum classis, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. 10th edn., Vol. 1, Laurentii Salvii, Stockholm. [Google Scholar]
  10. Lysyk TJ. 1993. Seasonal abundance of stable flies and house flies (Diptera: Muscidae) in dairies in Alberta, Canada. Journal of Medical Entomology, 30, 888–895. [PubMed] [Google Scholar]
  11. Masmeatathip R, Gilles J, Ketavan C, Duvallet G. 2006. First survey of seasonal abundance and daily activity of Stomoxys spp. (Diptera: Muscidae) in Kamphaengsaen Campus, Nakornpathom Province, Thailand. Parasite, 13, 245–250. [CrossRef] [EDP Sciences] [PubMed] [Google Scholar]
  12. Muenworn V, Duvallet G, Thainchum K, Tuntakom S, Akratanakul P, Chareonviriyaphap T. 2010. Stable fly (Diptera: Muscidae) distribution in Thailand. Kasetsart Journal (Natural Science), 44, 44–52. [Google Scholar]
  13. Muenworn V, Duvallet G, Thainchum K, Tuntakom S, Tanasilchayakul S, Prabaripai A, Akratanakul P, Sukonthabhirom S, Chareonviriyaphap T. 2010. Geographic distribution of stomoxyine flies (Diptera: Muscidae) and diurnal activity of Stomoxys calcitrans in Thailand. Journal of Medical Entomology, 47, 791–797. [CrossRef] [PubMed] [Google Scholar]
  14. Müller GC, Hogsette JA, Beirt JC, Traore SF, Toure MB, Traore MM, Bah S, Doumbia S, Schlein Y. 2012. Attraction of Stomoxys sp. to various fruits and flowers in Mali. Medical and Veterinary Entomology, 26, 178–187. [CrossRef] [PubMed] [Google Scholar]
  15. Picard F. 1908. Description de deux nouveaux Stomoxys du Bengale (Dipt.), Bulletin de la Societé Entomologique de France, 20–21. [Google Scholar]
  16. Pitzer JB, Kaufman PE, Hogsette JA, Geden CJ, Tenbroeck SH. 2011. Seasonal abundance of stable flies and filth fly pupal parasitoids (Hymenoptera: Pteromalidae) at Florida Equine Facilities. Journal of Economic Entomology, 104, 1108–1115. [CrossRef] [PubMed] [Google Scholar]
  17. Rondani C. 1873. Muscaria exotica Musei Civici Januensis observata et distinct a Prof. Camillo Rondani. Fragmentum I. Species aliquae in Abyssinia (Regione Bogos) lectae a Doct. O. Beccari et March. O. Antinori, anno 1870–71. Annali del Museo Civico di Storia Naturale Giacomo Doria, Genova, 4, 282–294. [Google Scholar]
  18. Skoda SR, Thomas GD, Campbell JB. 1991. Developmental sites and relative abundance of immature stages of the stable fly (Diptera:Muscidae) in beef cattle feedlot pens in eastern Nebraska. Journal of Economic Entomology, 84, 191–197. [PubMed] [Google Scholar]
  19. Sumba AL, Mihok S, Oyieke FA. 1998. Mechanical transmission of Trypanosoma evansi and T. congolense by Stomoxys niger and S. taeniatus in a laboratory mouse model. Medical and Veterinary Entomology, 12, 417–422. [CrossRef] [PubMed] [Google Scholar]
  20. Taylor DB, Berkebile D. 2008. Sugar feeding in adult stable flies. Environmental Entomology, 37, 625–629. [CrossRef] [PubMed] [Google Scholar]
  21. Traversa D, Otranto D, Iorior R, Carluccio A, Contri A, Paoletti B, Bartolini R, Giangaspero A. 2008. Identification of the intermediate hosts of Habronema microstoma and Habronema muscae under field conditions. Medical and Veterinary Entomology, 22, 283–287. [CrossRef] [PubMed] [Google Scholar]
  22. Tumrasvin W, Shinonaga S. 1978. Studies on medically important flies in Thailand V. On 32 species belonging to the subfamilies Muscinae and Stomoxyinae including the taxonomic keys (Diptera: Muscidae). Bulletin of Tokyo Medical and Dental University, 25, 201–227. [Google Scholar]
  23. Wieman GA, Campbell JB, Deshazer JA, Berry IL. 1992. Effects of stable flies (Diptera: Muscidae) and heat stress on weight gain and feed efficiency of feeder cattle. Journal of Economic Entomology, 85, 1835–1842. [PubMed] [Google Scholar]
  24. Zumpt F. 1973. The Stomoxyine Biting Flies of the World. Diptera: Muscidae, Taxonomy, Biology, Economic Importance and Control Measures. Gustav Fischer Verlag, Stuttgart, Germany. [Google Scholar]

Cite this article as: Phasuk J, Prabaripai A & Chareonviriyaphap T: Seasonality and daily flight activity of stable flies (Diptera: Muscidae) on dairy farms in Saraburi Province, Thailand. Parasite, 2013, 20, 17.

All Tables

Table 1.

Total numbers of Stomoxys spp. collected and their relative abundance (RA) on two dairy farms, Muak Lek district, Saraburi Province from September 2010 to August 2011.

Table 2.

Stepwise multiple regression analysis with correlation between total number of Stomoxys calcitrans and weather parameters in Muak Lek district, Saraburi Province from September 2010 to August 2011.

All Figures

thumbnail Figure 1.

Location of Muak Lek district (study area) in Saraburi Province, Thailand.

In the text
thumbnail Figure 2.

Mean monthly temperature and relative humidity (right axis scale) and light intensity (left axis scale) on the experimental sites (two dairy farms) from September 2010 to August 2011.

In the text
thumbnail Figure 3.

Mean number of Stomoxys spp. captured in four traps on dairy farm 1 from September 2010 to August 2011.

In the text
thumbnail Figure 4.

Mean number of Stomoxys spp. captured in four traps on dairy farm 2 from September 2010 to August 2011.

In the text
thumbnail Figure 5.

Mean numbers ± standard error bars of Stomoxys calcitrans males and females collected during three seasons on two dairy farms.

In the text
thumbnail Figure 6.

Mean numbers ± standard error bars of Stomoxys calcitrans males and females collected during one-hour intervals in three seasons on two dairy farms.

In the text
thumbnail Figure 7.

Mean numbers ± standard error bars of Stomoxys spp. males and females collected during one-hour intervals on two dairy farms from September 2010 to August 2011.

In the text

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