Seasonal Abundance of Lutzomyia shannoni (Diptera: Psychodidae) on Ossabaw Island, Georgia FRANK J. BRINSON,1 DANIEL V. HAGAN,1 JAMES A. COMER,2 AND DOMINIC A. STROHLEIN 23
KEY WORDS Insecta, Lutzomyia shannoni, population dynamics, bionomics
PHLEBOTOMINE SAND FLIES are the suspected
vectors of several pathogens of public health importance, including protozoa of the genus Leishmania and several arboviruses (Tesh et al. 1971, Lewis & Ward 1987). The studies of Tesh et al. (1972, 1987) indicated that sand flies may be involved in the transmission of viruses within the VSV serogroup. The sand fly Lutzomyia shannoni Dyar has the widest known distribution of any New World sand fly (Young 1979), extending from Delaware in the United States south to Argentina (Young & Perkins 1984). Only three species of sand flies are known to occur in Georgia: Lutzomyia vexator Coq., L. cruciata Coq., and L. shannoni. In Georgia, L. shannoni has been collected in the Okefenokee Swamp area of Charlton, Clinch, and Ware counties (Young & Perkins 1984). L. shannoni also was the only sand fly collected on Ossabaw Island in Chatham County, Ga. (Corn et al. 1990). This species may occur in many hardwood forest areas of southeast Georgia (D. G. Young, University of Florida, Gainesville, personal communication). For the past 10 yr, researchers at the Southeastern Cooperative Wildlife Disease Study, College of Veterinary Medicine, University of 1 Department of Biology, Institute of Arthropodology and Parasitology, Georgia Southern University, Statesboro, Ga. 30460. 2 Southeastern Cooperative Wildlife Disease Study, College of Veterinary Medicine, University of Georgia, Athens, Ga. 30602. 3 Current Address: P.O. Box 350, Kresgesville, Pa. 18333.
Georgia, have studied the epidemiology of the New Jersey serotype of VSV on Ossabaw Island. Serosurveys detected exposure in six vertebrate species (Fletcher et al. 1985). Annual seroconversions in juvenile feral sentinel swine indicated that Ossabaw Island represented an enzootic focus of this virus (Stallknecht et al. 1985). Studies with penned domestic sentinel swine suggested that the virus was spread by flying insects (Stallknecht et al. 1987). Six isolations of the New Jersey serotype were obtained from pools of L. shannoni collected on Ossabaw Island in 1988 (Corn et al. 1990). Subsequent laboratory studies demonstrated that L. shannoni was a competent biological vector of the virus (Comer et al. 1990). In the latter study, transovarial transmission occurred in some groups of flies, demonstrating a possible overwintering mechanism for the virus at this focus. The probable involvement of L. shannoni in the transmission of VSV on Ossabaw Island stimulated our interest in investigating the seasonal abundance and bionomics of this insect. The objectives of our study were to describe the seasonal abundance of adult L. shannoni, examine the effects of meteorological factors on the seasonal abundance of the adults, determine the vertical distribution of adults in the forest canopy, and locate diurnal resting sites. Materials and Methods Ossabaw Island (Chatham County), Ga., has been described previously (Johnson et al. 1974,
0022-2585/92/0178-0182$02.00/0 © 1992 Entomological Society of America
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J. Med. Entomol. 29(2): 178-182 (1992) ABSTRACT Population dynamics of Lutzomyia shannoni were monitored from April 1986 through December 1987 on Ossabaw Island, Ga. Most (99%) of the 19,788 adult sand flies were collected in light traps supplemented with dry ice; :£l% were aspirated from diurnal resting sites. Adult sand flies first appeared in April and were followed by peaks of abundance during May 1986, and May and July 1987. Numbers of adults captured fell rapidly in October and November 1986 and in September and October 1987. No specimens were collected in December 1986 or in March, November, and December 1987. Light trap catch was affected positively by mean nightly air temperature and negatively by rainfall 14 d before collection, but not by wind speed or moon phase. Vesicular stomatitis viral activity, as measured by antibodies in feral and domestic swine, roughly corresponded to the seasonal appearance of adult L. shannoni during 1986 and 1987. Significantly more adults (72%) were collected in light traps at ground level (0.5 m) than at heights of 4 and 8 m. Most resting adults were collected from dark, moist tree holes and cavities of various hardwoods.
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Mathews et al. 1980). The island is dominated by a maritime forest of oak, hickory, holly, magnolia, slash pine, wax myrtle, cabbage palm, and saw palmetto. This vegetation provides suitable habitat for abundant populations of white-tailed deer, Odocoileus virginianus; feral swine; and other species of wildlife. Seasonal Abundance. Populations of adult L. shannoni were sampled using 10 CDC miniature light traps, which were supplemented with dry ice (Chaniotis 1983). Each trap was placed 0.5 m aboveground in close proximity to pen-style traps that were used to capture feral swine (Fig. 1). A circular piece of hardware cloth with 0.36cm2 openings prevented the collection of larger insects. Light traps were operated from sunset to sunrise approximately three nights per week from April through October 1986 and from March through October 1987. In November and December, when numbers of adults collected were ^ 1 sand fly per trap night, collections were reduced to one night per month. No collections were made in January or February 1987. The identification of representative specimens of L. shannoni was confirmed by D. G. Young, and voucher specimens were placed in the University of Florida museum collection. Environmental Factors. Meteorological data were obtained from the Federal Aviation Administration Weather Station, Savannah AirportTravis Field, Savannah, Ga. The weather station was 30 km north-northwest of the study site (25.2
179
km distance to nearest trap, and 34.1 km to most distant trap). Air temperature and wind speed were recorded once hourly, and means were calculated by dividing total hourly readings by the number of hours of trap operation. Rainfall was calculated for 7, 14, and 28 d before the night of light trap operation. Mean nightly temperatures, wind speed, rainfall, and moon phase were compared with the number of L. shannoni collected per trap night. These data were tested for significance by multiple regression and analysis of variance (ANOVA) using SPSS (Norusis 1988). Vertical Distribution. Vertical distribution of L. shannoni on Ossabaw Island was determined by the placement of light traps at 0.5, 4, and 8 m aboveground at sites 8 and 10 (Fig. 1). To test whether the vapor plume of the dry ice baited traps might affect vertical distribution of L. shannoni, light traps were positioned differently at the two sites. At site 8, the three light traps were set one above the other in a vertical line, whereas at site 10, each of the three light traps were separated horizontally by a distance of = 15 m. Traps were operated for =2 nights per week from May through August 1987 (total of 25 nights). Diurnal Resting Sites. Resting sites of adult L. shannoni were sought by searching ground litter, tree foliage, bark, and buttresses, and inside various holes and cavities in hardwood trees. Potential resting sites were examined from ground level up to 8 m at various times during daylight hours, from 2 h after sunrise until ~2 h before sunset. Collections were made by mouth aspiration approximately twice each week, concurrent with light trap operation in 1987. Results Seasonal Abundance. In total, 19,788 adult L. shannoni were collected on Ossabaw Island from April 1986 through December 1987. Of this total, 99% were captured in light traps. Adults were collected first during April in both years. The adult population then increased rapidly to maxima during May in both 1986 and 1987. However, sporadic peaks of abundance occurred during other months. The greatest numbers of adults captured per trap night in 1986 were 188 on 15 April, 46 on 19 July, and 40 on 21 September. In 1987, the greatest numbers of L. shannoni captured per trap night were 101 on 5 May and 52 on the nights of 2 May and 8 July. The numbers of sand flies captured by the light traps began decreasing in October 1986 and September 1987. A few flies (2 per trap night) were collected in November 1986. No flies were collected in December 1986 and in March, November, and December 1987 (Fig. 2). Significantly more adult male sand flies were collected in light traps each month than females (P < 0.001). The sex ratio varied per month from a
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Fig. 1. Location of light traps and swine traps on Ossabaw Island, Georgia, operated during 1986 and 1987. Light traps and swine traps indicated by numbered dark circles. Shaded areas are salt marshes, and clear areas are upland. Bar = 1 km.
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FEMALES Air Temp. (C)
LZ3 MALES Rain 14 days before
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Fig. 2. Monthly means of adult L. shannoni males and females captured per trap night (NTN) on Ossabaw Island, Georgia, from April 1986 through December 1987, with mean air temperatures (°C) and mean rainfall (cm) occurring 14 d before collections.
high of 13:1 (d:9) in July 1986 to a low of 3.4:1 in April 1987. The overall percentage of males collected in light traps was 83%, for a sex ratio of 4.9:1. Effects of Environmental Factors. Adult sand flies were not found at mean nightly air temperatures of 90% were collected in light traps when mean nightly air temperatures were between 17.1 and 30.6°C (Fig. 2). Stepwise multiple regression analysis indicated that light trap catches were affected positively by mean nightly air temperatures (P ^ 0.001) and negatively by rainfall occurring 14 d before collection (P < 0.02). These relationships are described (R2-. = 0.375) by the regression equation y = -0.784 + 0.025 (temperature) - 0.037 (14 d rainfall). Mean nightly air temperature was positively correlated with light trap catches (r = 0.558). Rainfall occurring 14 d before each trap night was negatively correlated with light trap catches (r = -0.179). Moon phase, wind speed, and rainfall occurring 7 and 28 d before collections had no significant effect on light trap catches of L. shannoni. Vertical Distribution. Overall, 72% of the 1,660 total adult L. shannoni were collected near ground level (0.5 m), during 25 nights of trap-
ping. Collections from sites 8 and 10 did not show any differences, and data from collections at the two sites were combined for analysis. At 0.5 m, 779 males and 420 females were collected for a sex ratio of 2.1:1 (6*: 9). At 4 m, 276 males and 102 females (23% of the total) were collected, with a sex ratio of 3.5:1. Only 5% (73 6*, 10 9) of the sand flies were collected at 8 m, and the sex ratio of these flies was 7.2:1. One-way ANOVA of light trap catches versus height indicated collections decreased significantly with elevation (P < 0.001). Diurnal Resting Sites. In total, 155 (80 8, 75 9) adult L. shannoni were collected in dimly lit moist holes and cavities in oaks, Quercus virginiana and Q. nigra; hickory, Carya spp.; and magnolia, Magnolia grandiflora. Specimens were collected only during periods of adult flight activity (April through October) as indicated by light trap collections. Relative humidity of the sites where adult sand flies were collected was high (73-98% RH). The sex ratio of these resting flies was 1:1.06 (8:9). Adult flies were not found in crevices on the exterior surface of trunks of trees or in ground litter. Cavities that contained adults were relatively close to the ground. No adults were aspirated from cavities 2 m aboveground. Cavities that pro-
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R a
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shannoni
duced sand flies tended to be small (0.2 m3), secluded portions of larger cavities. The typical cavity that contained sand flies yielded a mean of five adults (range, 1-15) after careful searching. Negative tree cavities were either dry, exposed to moderate-to-high levels of sunlight, or were higher than 2 m. Discussion
181
modify the effects of moonlight on sand fly activity. The finding that adult activity of L. shannoni was greatest at ground level generally is in accord with other studies that have addressed the vertical distribution of this species. In Panama, L. shannoni was aspirated in large numbers near bases of trees and crevices between support buttresses (Chaniotis et al. 1972), although some specimens were collected at an elevation of 30 m in the forest canopy (Chaniotis et al. 1974). In a study in Belize, however, the vertical location of adults was variable. The abundance of L. shannoni was greatest at ground level during 5 mo of the study, at 8 m for 10 mo, and at 10 m for 3 mo (Williams 1968). In that study, the author concluded that L. shannoni preferred to feed on humans as bait above the ground, but also would descend to the forest floor to feed. Differences in vertical distribution of L. shannoni between areas may reflect differences in collection methods, environmental conditions, stratification of the forest canopy, or host availability. The increase in sex ratio with increase in elevation is similar to the findings of a markrecapture study by Chaniotis et al. (1974) on the vertical movements of sand flies in Panama. There, only 1 of 96 female L. shannoni captured at ground level was recaptured 30 m above the release site, whereas 10 of 142 males were recaptured at this height, indicating a tendency for male L. shannoni to be active at higher elevations than female flies (Chaniotis et al. 1974). The preference shown by adult L. shannoni on Ossabaw Island for dark, moist holes and cavities in hardwoods as diurnal resting sites is similar to the work of Rosabal & Miller (1970) in Louisiana, who found adults of this species in hollow trees in swampy woodlands. In pine dominated forests, they found no L. shannoni, possibly indicating a repellency from the presence of terpenoid compounds. The findings of this study relate well to the observations of enzootic VSV activity on Ossabaw Island. The seasonality of adult sand flies corresponds well to the seasonality of seroconversions in sentinel swine (Stallknecht et al. 1987, Corn et al. 1990), and the abundance of female flies close to the ground provides increased opportunity for feeding on terrestrial mammals. Moist tree holes in old-growth hardwood forests may be an essential component of L. shannoni habitat in temperate zones. An investigation of the distribution of this forest type with presence of VSV might reveal an ecological association that implicates epidemiological involvement of L. shannoni in other foci of VSV activity.
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Seasonal dynamics of sand flies on Ossabaw varied only slightly from 1986 to 1987. Adults appeared in light trap catches at approximately the same time (15-28 April) each spring, were abundant for four months (May—August), and then declined in number. Only a few specimens were captured in November and none in December. In subsequent trapping in 1988, adult sand flies were first captured in late March and began to peak in abundance in late June (Corn et al. 1990). Findings on Ossabaw Island are in accord with those of Rosabal & Miller (1970) in Louisiana. In their study, adults were collected during summer months, declined in number in November, and were not collected in December. In our study, adult specimens were not collected when nightly temperatures were ^10°C, suggesting that adult populations of L. shannoni might enter a temperature-dependent quiescence during winter months on Ossabaw Island. However, because we could not locate adults during winter months, it is most likely that the population overwinters in immature stages, which emerge in the spring. The sex ratio in a laboratory colony of L. shannoni was =1:1 (Perkins 1982), and presumably this is the sex ratio that occurs in nature. Reasons for the apparent bias at light traps for males are unknown. However, male sand flies are attracted to vertebrate hosts (Miles & Christensen 1976), although they do not feed on blood (Downes 1958). The attraction of male sand flies to vertebrate hosts has been interpreted as a means of locating females for mating (Chaniotis & Anderson 1968). Male sand flies collected by the light traps in this study may have been attracted to the carbon dioxide given off by the dry ice or the light from the trap. Light traps operated without dry ice on Ossabaw Island, collected neither males nor females (data not included in number per trap night in our study). The lack of correlation between trapping success with moon phase on Ossabaw is similar to observations in the Sudan, where moonlight did not affect the biting activity of sand flies (Hoogstraal et al. 1962). Fog and cloudiness were not measured during nights when the light traps were run on Ossabaw Island, and these factors could have affected the light trap catches during periods of full moon. The influence of various factors such as temperature, cloud cover, and altitude of the moon from the horizon probably
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Acknowledgment J. A. Rafter (Georgia Southern University) provided assistance with statistical analysis of the data. P. V. Perkins (Department of Entomology, Walter Reed Army Institute of Research, Washington, D.C.), D. G. Young (University of Florida, Gainesville), and V. F. Nettles (Southeastern Cooperative Wildlife Disease Study, College of Veterinary Medicine, University of Georgia, Athens) critically reviewed the manuscript. We acknowledge the assistance of the Georgia Department of Natural Resources, and E. T. West and R. Parker (Ossabaw Island Foundation). Our appreciation is extended to the staff of the Southeastern Cooperative Wildlife Disease Study, who performed many of the light trap collections. This research was supported by the Georgia Southern Faculty Research Committee and grant 87-018, from the Veterinary Medical Experiment Station, University of Georgia, Athens.
Chaniotis, B. N. 1983. Improved trapping of phlebotomine sand flies (Diptera: Psychodidae) in light traps supplemented with dry ice in a neotropical rain forest. J. Med. Entomol. 20: 222-223. Chaniotis, B. N. & J. R. Anderson. 1968. Age structure, population dynamics and vector potential of Phlebotomus in northern California. Part II. Field population dynamics and natural flagellate infections in parous females. J. Med. Entomol. 5: 273292. Chaniotis, B. N., R. B. Tesh, M. A. Correa & K. M. Johnson. 1972. Diurnal resting sites of phlebotomine sand flies in a Panamanian tropic forest. J. Med. Entomol. 9: 91-98. Chaniotis, B. N., M. A. Correa, R. B. Tesh & K. M. Johnson. 1974. Horizontal and vertical movements of phlebotomine sandflies in a Panamanian rain forest. J. Med. Entomol. 11: 369-375. Comer, J. A., R. B. Tesh, G. B. Modi, J. L. Corn, & V. F. Nettles. 1990. Vesicular stomatitis virus, New Jersey serotype: Replication in and transmission by Lutzomyia shannoni (Diptera: Psychodidae). Am. J. Trop. Med. Hyg. 42: 483-490. Corn, J. L., J. A. Comer, G. A. Erickson & V. F. Nettles. 1990. Isolation of vesicular stomatitis virus New Jersey serotype from phlebotomine sand flies in Georgia. Am. J. Trop. Med. Hyg. 42: 476-482. Downes, J. A. 1958. The feeding habits of biting flies and their significance in classification. Annu. Rev. Entomol. 3: 249-266. Fletcher, W. O., D. E. Stallknecht, & E. W. Jenney. 1985. Serologic surveillance for vesicular stomatitis virus on Ossabaw Island, Georgia. J. Wild. Dis. 21: 100-104. Hoogstraal, H., D. R. Dietlein & D. Heyneman. 1962. Leishmaniasis in the Sudan Republic: 4. preliminary observations on man-biting sandflies (Psychodidae: Phlebotomus) in certain upper Nile endemic areas. Trans. R. Soc. Trop. Med. Hyg. 56: 411-422. Johnson, A. S., H. O. Hillestad, S. F. Shanholtzer & G. F. Shanholtzer. 1974. An ecological survey of the coastal region of Georgia. National Park Service Monograph Series. No. 3. Washington, D.C.
Lewis, D. J. & R. D. Ward. 1987. Transmission and vectors, pp. 235-262. In W. Peters & R. KillickKendrick [eds.], The leishmaniases in biology and medicine, vol. 1. Academic, London. Mathews, T. D., F. Stapor Jr., C. R. Richter, J. V. Miglarese, M. D. McKenzie, L. A. Barclay [eds]. 1980. Ecological characterization of the Sea Island coastal region of South Carolina and Georgia, vol. 1: physical features of the characterization area. FWS/ OBS-79/40. U.S. Fish and Wildlife Service, Office of Biological Services, Washington, D.C. Miles, C. T. & H. A. Christensen. 1976. Mating aggregations of male Lutzomyia sandflies at human hosts in Panama. R. Soc. Trop. Med. Hyg. 70: 531532. Norusis, M. J. 1988. SPSS/PC+studentware. SPSS, Chicago. Perkins, P. V. 1982. The identification and distribution of phlebotomine sand flies in the United States with notes on the biology of two species from Florida (Diptera: Psychodidae). Dissertation, University of Florida, Gainesville. University Microfilms, Ann Arbor, Mich. Rosabal, R. & A. Miller. 1970. Phlebotomine sand flies in Louisiana (Diptera: Psychodidae). Mosq. News 30: 180-187. Stallknecht, D. E., V. F. Nettles, W. O. Fletcher & G. A. Erickson. 1985. Enzootic vesicular stomatitis New Jersey type in an insular feral swine population. Am. J. Epidemiol. 122: 876-883. Stallknecht, D. E., W. O. Fletcher, G. A. Erickson & V. F. Nettles. 1987. Antibodies to vesicular stomatitis New Jersey type virus in wild and domestic sentinel swine. Am. J. Epidemiol. 125: 1058-1065. Tesh, R. B., B. N. Chaniotis & K. M. Johnson. 1971. Vesicular stomatitis virus, Indiana serotype: multiplication in and transmission by experimentally infected phlebotomine sand flies (Lutzomyia trapidoi). Am. J. Epidemiol. 93: 491-495. 1972. Vesicular stomatitis virus (Indiana serotype): Transovarial transmission by phlebotomine sandflies. Science 175: 1477-1479. Tesh, R. B., J. Boshell, G. B. Modi, A. Morales, D. G. Young, A. Corredor, C. F. Carrasquilla, C. Rodriguez, L. L. Walters & M. O. Gaitan. 1987. Natural infection of humans, animals, and phlebotomine sand flies with the Alagoas serotype of vesicular stomatitis virus in Colombia. Am. J. Trop. Med. Hyg. 36: 653-661. Williams, P. 1968. On the vertical distribution of phlebotomine sand flies (Dipt, Psychodidae) in British Honduras (Belize). Bull. Entomol. Res. 59: 637-646. Young, D. G. 1979. A review of the bloodsucking Psychodid flies of Columbia (Diptera: Phlebotominae and Sycoracinae). Ins. Food Agric. Sci. Tech. Bull. 806. University of Florida, Gainesville. Young, D. G. & P. V. Perkins. 1984. Phlebotomine sand flies of North America (Diptera: Psychodidae). Mosq. News. 44: 263-306. Received for publication 30 August 1990; accepted 20 October 1991.
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References Cited
Vol. 29, no. 2
KEY WORDS Insecta, Lutzomyia shannoni, population dynamics, bionomics
PHLEBOTOMINE SAND FLIES are the suspected
vectors of several pathogens of public health importance, including protozoa of the genus Leishmania and several arboviruses (Tesh et al. 1971, Lewis & Ward 1987). The studies of Tesh et al. (1972, 1987) indicated that sand flies may be involved in the transmission of viruses within the VSV serogroup. The sand fly Lutzomyia shannoni Dyar has the widest known distribution of any New World sand fly (Young 1979), extending from Delaware in the United States south to Argentina (Young & Perkins 1984). Only three species of sand flies are known to occur in Georgia: Lutzomyia vexator Coq., L. cruciata Coq., and L. shannoni. In Georgia, L. shannoni has been collected in the Okefenokee Swamp area of Charlton, Clinch, and Ware counties (Young & Perkins 1984). L. shannoni also was the only sand fly collected on Ossabaw Island in Chatham County, Ga. (Corn et al. 1990). This species may occur in many hardwood forest areas of southeast Georgia (D. G. Young, University of Florida, Gainesville, personal communication). For the past 10 yr, researchers at the Southeastern Cooperative Wildlife Disease Study, College of Veterinary Medicine, University of 1 Department of Biology, Institute of Arthropodology and Parasitology, Georgia Southern University, Statesboro, Ga. 30460. 2 Southeastern Cooperative Wildlife Disease Study, College of Veterinary Medicine, University of Georgia, Athens, Ga. 30602. 3 Current Address: P.O. Box 350, Kresgesville, Pa. 18333.
Georgia, have studied the epidemiology of the New Jersey serotype of VSV on Ossabaw Island. Serosurveys detected exposure in six vertebrate species (Fletcher et al. 1985). Annual seroconversions in juvenile feral sentinel swine indicated that Ossabaw Island represented an enzootic focus of this virus (Stallknecht et al. 1985). Studies with penned domestic sentinel swine suggested that the virus was spread by flying insects (Stallknecht et al. 1987). Six isolations of the New Jersey serotype were obtained from pools of L. shannoni collected on Ossabaw Island in 1988 (Corn et al. 1990). Subsequent laboratory studies demonstrated that L. shannoni was a competent biological vector of the virus (Comer et al. 1990). In the latter study, transovarial transmission occurred in some groups of flies, demonstrating a possible overwintering mechanism for the virus at this focus. The probable involvement of L. shannoni in the transmission of VSV on Ossabaw Island stimulated our interest in investigating the seasonal abundance and bionomics of this insect. The objectives of our study were to describe the seasonal abundance of adult L. shannoni, examine the effects of meteorological factors on the seasonal abundance of the adults, determine the vertical distribution of adults in the forest canopy, and locate diurnal resting sites. Materials and Methods Ossabaw Island (Chatham County), Ga., has been described previously (Johnson et al. 1974,
0022-2585/92/0178-0182$02.00/0 © 1992 Entomological Society of America
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J. Med. Entomol. 29(2): 178-182 (1992) ABSTRACT Population dynamics of Lutzomyia shannoni were monitored from April 1986 through December 1987 on Ossabaw Island, Ga. Most (99%) of the 19,788 adult sand flies were collected in light traps supplemented with dry ice; :£l% were aspirated from diurnal resting sites. Adult sand flies first appeared in April and were followed by peaks of abundance during May 1986, and May and July 1987. Numbers of adults captured fell rapidly in October and November 1986 and in September and October 1987. No specimens were collected in December 1986 or in March, November, and December 1987. Light trap catch was affected positively by mean nightly air temperature and negatively by rainfall 14 d before collection, but not by wind speed or moon phase. Vesicular stomatitis viral activity, as measured by antibodies in feral and domestic swine, roughly corresponded to the seasonal appearance of adult L. shannoni during 1986 and 1987. Significantly more adults (72%) were collected in light traps at ground level (0.5 m) than at heights of 4 and 8 m. Most resting adults were collected from dark, moist tree holes and cavities of various hardwoods.
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Mathews et al. 1980). The island is dominated by a maritime forest of oak, hickory, holly, magnolia, slash pine, wax myrtle, cabbage palm, and saw palmetto. This vegetation provides suitable habitat for abundant populations of white-tailed deer, Odocoileus virginianus; feral swine; and other species of wildlife. Seasonal Abundance. Populations of adult L. shannoni were sampled using 10 CDC miniature light traps, which were supplemented with dry ice (Chaniotis 1983). Each trap was placed 0.5 m aboveground in close proximity to pen-style traps that were used to capture feral swine (Fig. 1). A circular piece of hardware cloth with 0.36cm2 openings prevented the collection of larger insects. Light traps were operated from sunset to sunrise approximately three nights per week from April through October 1986 and from March through October 1987. In November and December, when numbers of adults collected were ^ 1 sand fly per trap night, collections were reduced to one night per month. No collections were made in January or February 1987. The identification of representative specimens of L. shannoni was confirmed by D. G. Young, and voucher specimens were placed in the University of Florida museum collection. Environmental Factors. Meteorological data were obtained from the Federal Aviation Administration Weather Station, Savannah AirportTravis Field, Savannah, Ga. The weather station was 30 km north-northwest of the study site (25.2
179
km distance to nearest trap, and 34.1 km to most distant trap). Air temperature and wind speed were recorded once hourly, and means were calculated by dividing total hourly readings by the number of hours of trap operation. Rainfall was calculated for 7, 14, and 28 d before the night of light trap operation. Mean nightly temperatures, wind speed, rainfall, and moon phase were compared with the number of L. shannoni collected per trap night. These data were tested for significance by multiple regression and analysis of variance (ANOVA) using SPSS (Norusis 1988). Vertical Distribution. Vertical distribution of L. shannoni on Ossabaw Island was determined by the placement of light traps at 0.5, 4, and 8 m aboveground at sites 8 and 10 (Fig. 1). To test whether the vapor plume of the dry ice baited traps might affect vertical distribution of L. shannoni, light traps were positioned differently at the two sites. At site 8, the three light traps were set one above the other in a vertical line, whereas at site 10, each of the three light traps were separated horizontally by a distance of = 15 m. Traps were operated for =2 nights per week from May through August 1987 (total of 25 nights). Diurnal Resting Sites. Resting sites of adult L. shannoni were sought by searching ground litter, tree foliage, bark, and buttresses, and inside various holes and cavities in hardwood trees. Potential resting sites were examined from ground level up to 8 m at various times during daylight hours, from 2 h after sunrise until ~2 h before sunset. Collections were made by mouth aspiration approximately twice each week, concurrent with light trap operation in 1987. Results Seasonal Abundance. In total, 19,788 adult L. shannoni were collected on Ossabaw Island from April 1986 through December 1987. Of this total, 99% were captured in light traps. Adults were collected first during April in both years. The adult population then increased rapidly to maxima during May in both 1986 and 1987. However, sporadic peaks of abundance occurred during other months. The greatest numbers of adults captured per trap night in 1986 were 188 on 15 April, 46 on 19 July, and 40 on 21 September. In 1987, the greatest numbers of L. shannoni captured per trap night were 101 on 5 May and 52 on the nights of 2 May and 8 July. The numbers of sand flies captured by the light traps began decreasing in October 1986 and September 1987. A few flies (2 per trap night) were collected in November 1986. No flies were collected in December 1986 and in March, November, and December 1987 (Fig. 2). Significantly more adult male sand flies were collected in light traps each month than females (P < 0.001). The sex ratio varied per month from a
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Fig. 1. Location of light traps and swine traps on Ossabaw Island, Georgia, operated during 1986 and 1987. Light traps and swine traps indicated by numbered dark circles. Shaded areas are salt marshes, and clear areas are upland. Bar = 1 km.
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FEMALES Air Temp. (C)
LZ3 MALES Rain 14 days before
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-30
N T N
T e m -20 P e - 15 r a
-25
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i
n A M J
J A S O N D J F M A M J
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- 10
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1987
Fig. 2. Monthly means of adult L. shannoni males and females captured per trap night (NTN) on Ossabaw Island, Georgia, from April 1986 through December 1987, with mean air temperatures (°C) and mean rainfall (cm) occurring 14 d before collections.
high of 13:1 (d:9) in July 1986 to a low of 3.4:1 in April 1987. The overall percentage of males collected in light traps was 83%, for a sex ratio of 4.9:1. Effects of Environmental Factors. Adult sand flies were not found at mean nightly air temperatures of 90% were collected in light traps when mean nightly air temperatures were between 17.1 and 30.6°C (Fig. 2). Stepwise multiple regression analysis indicated that light trap catches were affected positively by mean nightly air temperatures (P ^ 0.001) and negatively by rainfall occurring 14 d before collection (P < 0.02). These relationships are described (R2-. = 0.375) by the regression equation y = -0.784 + 0.025 (temperature) - 0.037 (14 d rainfall). Mean nightly air temperature was positively correlated with light trap catches (r = 0.558). Rainfall occurring 14 d before each trap night was negatively correlated with light trap catches (r = -0.179). Moon phase, wind speed, and rainfall occurring 7 and 28 d before collections had no significant effect on light trap catches of L. shannoni. Vertical Distribution. Overall, 72% of the 1,660 total adult L. shannoni were collected near ground level (0.5 m), during 25 nights of trap-
ping. Collections from sites 8 and 10 did not show any differences, and data from collections at the two sites were combined for analysis. At 0.5 m, 779 males and 420 females were collected for a sex ratio of 2.1:1 (6*: 9). At 4 m, 276 males and 102 females (23% of the total) were collected, with a sex ratio of 3.5:1. Only 5% (73 6*, 10 9) of the sand flies were collected at 8 m, and the sex ratio of these flies was 7.2:1. One-way ANOVA of light trap catches versus height indicated collections decreased significantly with elevation (P < 0.001). Diurnal Resting Sites. In total, 155 (80 8, 75 9) adult L. shannoni were collected in dimly lit moist holes and cavities in oaks, Quercus virginiana and Q. nigra; hickory, Carya spp.; and magnolia, Magnolia grandiflora. Specimens were collected only during periods of adult flight activity (April through October) as indicated by light trap collections. Relative humidity of the sites where adult sand flies were collected was high (73-98% RH). The sex ratio of these resting flies was 1:1.06 (8:9). Adult flies were not found in crevices on the exterior surface of trunks of trees or in ground litter. Cavities that contained adults were relatively close to the ground. No adults were aspirated from cavities 2 m aboveground. Cavities that pro-
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duced sand flies tended to be small (0.2 m3), secluded portions of larger cavities. The typical cavity that contained sand flies yielded a mean of five adults (range, 1-15) after careful searching. Negative tree cavities were either dry, exposed to moderate-to-high levels of sunlight, or were higher than 2 m. Discussion
181
modify the effects of moonlight on sand fly activity. The finding that adult activity of L. shannoni was greatest at ground level generally is in accord with other studies that have addressed the vertical distribution of this species. In Panama, L. shannoni was aspirated in large numbers near bases of trees and crevices between support buttresses (Chaniotis et al. 1972), although some specimens were collected at an elevation of 30 m in the forest canopy (Chaniotis et al. 1974). In a study in Belize, however, the vertical location of adults was variable. The abundance of L. shannoni was greatest at ground level during 5 mo of the study, at 8 m for 10 mo, and at 10 m for 3 mo (Williams 1968). In that study, the author concluded that L. shannoni preferred to feed on humans as bait above the ground, but also would descend to the forest floor to feed. Differences in vertical distribution of L. shannoni between areas may reflect differences in collection methods, environmental conditions, stratification of the forest canopy, or host availability. The increase in sex ratio with increase in elevation is similar to the findings of a markrecapture study by Chaniotis et al. (1974) on the vertical movements of sand flies in Panama. There, only 1 of 96 female L. shannoni captured at ground level was recaptured 30 m above the release site, whereas 10 of 142 males were recaptured at this height, indicating a tendency for male L. shannoni to be active at higher elevations than female flies (Chaniotis et al. 1974). The preference shown by adult L. shannoni on Ossabaw Island for dark, moist holes and cavities in hardwoods as diurnal resting sites is similar to the work of Rosabal & Miller (1970) in Louisiana, who found adults of this species in hollow trees in swampy woodlands. In pine dominated forests, they found no L. shannoni, possibly indicating a repellency from the presence of terpenoid compounds. The findings of this study relate well to the observations of enzootic VSV activity on Ossabaw Island. The seasonality of adult sand flies corresponds well to the seasonality of seroconversions in sentinel swine (Stallknecht et al. 1987, Corn et al. 1990), and the abundance of female flies close to the ground provides increased opportunity for feeding on terrestrial mammals. Moist tree holes in old-growth hardwood forests may be an essential component of L. shannoni habitat in temperate zones. An investigation of the distribution of this forest type with presence of VSV might reveal an ecological association that implicates epidemiological involvement of L. shannoni in other foci of VSV activity.
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Seasonal dynamics of sand flies on Ossabaw varied only slightly from 1986 to 1987. Adults appeared in light trap catches at approximately the same time (15-28 April) each spring, were abundant for four months (May—August), and then declined in number. Only a few specimens were captured in November and none in December. In subsequent trapping in 1988, adult sand flies were first captured in late March and began to peak in abundance in late June (Corn et al. 1990). Findings on Ossabaw Island are in accord with those of Rosabal & Miller (1970) in Louisiana. In their study, adults were collected during summer months, declined in number in November, and were not collected in December. In our study, adult specimens were not collected when nightly temperatures were ^10°C, suggesting that adult populations of L. shannoni might enter a temperature-dependent quiescence during winter months on Ossabaw Island. However, because we could not locate adults during winter months, it is most likely that the population overwinters in immature stages, which emerge in the spring. The sex ratio in a laboratory colony of L. shannoni was =1:1 (Perkins 1982), and presumably this is the sex ratio that occurs in nature. Reasons for the apparent bias at light traps for males are unknown. However, male sand flies are attracted to vertebrate hosts (Miles & Christensen 1976), although they do not feed on blood (Downes 1958). The attraction of male sand flies to vertebrate hosts has been interpreted as a means of locating females for mating (Chaniotis & Anderson 1968). Male sand flies collected by the light traps in this study may have been attracted to the carbon dioxide given off by the dry ice or the light from the trap. Light traps operated without dry ice on Ossabaw Island, collected neither males nor females (data not included in number per trap night in our study). The lack of correlation between trapping success with moon phase on Ossabaw is similar to observations in the Sudan, where moonlight did not affect the biting activity of sand flies (Hoogstraal et al. 1962). Fog and cloudiness were not measured during nights when the light traps were run on Ossabaw Island, and these factors could have affected the light trap catches during periods of full moon. The influence of various factors such as temperature, cloud cover, and altitude of the moon from the horizon probably
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Acknowledgment J. A. Rafter (Georgia Southern University) provided assistance with statistical analysis of the data. P. V. Perkins (Department of Entomology, Walter Reed Army Institute of Research, Washington, D.C.), D. G. Young (University of Florida, Gainesville), and V. F. Nettles (Southeastern Cooperative Wildlife Disease Study, College of Veterinary Medicine, University of Georgia, Athens) critically reviewed the manuscript. We acknowledge the assistance of the Georgia Department of Natural Resources, and E. T. West and R. Parker (Ossabaw Island Foundation). Our appreciation is extended to the staff of the Southeastern Cooperative Wildlife Disease Study, who performed many of the light trap collections. This research was supported by the Georgia Southern Faculty Research Committee and grant 87-018, from the Veterinary Medical Experiment Station, University of Georgia, Athens.
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References Cited
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