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DEVELOPMENT, LIFE HISTORY

Temperature Effects on Development and Survival of Two Stable Flies, Stomoxys calcitrans and Stomoxys niger niger (Diptera: Muscidae), in La Re´union Island JEREMIE GILLES,1,2 JEAN-FRANCOIS DAVID,2

AND

GERARD DUVALLET2

J. Med. Entomol. 42(3): 260Ð265 (2005)

ABSTRACT Two stable ßy species, Stomoxys calcitrans (L., 1758) and Stomoxys niger niger Macquart, 1851, co-occur in La Re´ union, where they are important pests of cattle. The survival and developmental rate of the immature stages were compared at Þve constant temperatures from 15 to 35⬚C. In both species, immature survival was highest at 20 Ð25⬚C and markedly decreased at 15 and 35⬚C. At the lower temperatures, mortality was observed mainly for S. calcitrans larvae and S. niger eggs. At the higher temperatures, mainly pupae of both species died. At all temperatures, S. calcitrans survived better than S. niger. Developmental time was highly similar in both species, decreasing from 71 d at 15⬚C to 13 d at 30⬚C in S. calcitrans and from 69 d at 15⬚C to 14 d at 30⬚C in S. niger. Developmental times increased slightly at 35⬚C. Surprisingly, the tropical S. niger developed slightly faster than the cosmopolitan S. calcitrans at 15Ð20⬚C; the reverse was found at higher temperatures. Temperature summation models conÞrmed that S. niger had a lower developmental threshold than S. calcitrans (11.3 versus 12.2⬚C) and higher day-degree (DD) requirements to complete development (251 versus 225 DD). Overall, the results suggest that S. calcitrans is better adapted than S. niger, in terms of adult production from eggs, in the temperature range of La Re´ union. KEY WORDS stable ßies, temperature, developmental rate, stage-speciÞc survival, La Re´ union Island

STABLE FLIES (Stomoxys spp.) (Diptera: Muscidae) are blood-sucking insects associated with livestock and wildlife throughout the world. Occasionally, they also bite humans. They represent a serious nuisance because of their painful bites, blood predation, and transmission of pathogens (Zumpt 1973, DÕAmico et al. 1996). Their economic impact can be considerable (Campbell et al. 2001). Among the 18 Stomoxys species described, two occur in La Re´ union Island: the cosmopolitan Stomoxys calcitrans (L., 1758), and Stomoxys niger niger Macquart, 1851, which is also found in Africa, Madagascar, and Mauritius (Zumpt 1973). Both species occur from sea level to high-altitude plains (1,600 m) and are pests of cattle, particularly in dairy barns. During the wet and warm season (NovemberÐApril), large pullulations are observed, with daily catches of up to 5,000 ßies per Vavoua trap (unpublished data). In addition, stable ßies are considered mechanical vectors of 1 Centre de coope´ ration Internationale en Recherche Agronomique pour le De´ veloppementÐElevage et Me´ decine Ve´ te´ rinaire Tropicales, Programme Productions Animales, UMR C53 “Peuplements Ve´ ge´ taux et Bio-agresseurs en Milieu Tropical,” Poˆ le de Protection des Plantes, 7 chemin de lÕIrat, 97410 St Pierre de La Re´ union, France. 2 De ´ partement Ecologie des Arthropodes-UMR 5175 CEFE, Universite´ Montpellier 3, Route de Mende, F-34199 Montpellier cedex 5, France.

anaplasmosis, the primary agent of mortality in dairy cattle. They also could play an important part in the transmission of the bovine leukosis virus (Buxton et al. 1985). To control stable ßy populations and reduce their pathogenic and economic impacts in La Re´ union, a research project has been set up to study both species in the Þeld and in the laboratory. Adequate methods of control require thorough knowledge of the biology and ecology of the ßies (Batra 1982). When closely related species exploit the same resources, the biological and ecological characteristics of each species must be determined, and, ultimately, how the two species interact. Otherwise, measures against the most abundant species (S. calcitrans in La Re´ union) might favor the less common species. Many studies have been conducted with the cosmopolitan S. calcitrans, mainly in North America and South Africa. Seasonal changes in abundance were described in relation to temperature and rainfall (Mullens and Meyer 1987, Greene 1989, Lysyk 1993). Experimental studies clariÞed the inßuence of temperature on immature survival, developmental time, and adult longevity and reproduction (Berry and Kunz 1977, 1978; Kunz et al. 1977; Sutherland 1979; Lysyk 1998). Using those results, Lysyk (1998) calculated the intrinsic rate of increase of S. calcitrans at different temperatures. Such data are not available, however,

0022-2585/05/0260Ð0265$04.00/0 䉷 2005 Entomological Society of America

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GILLES ET AL.: DEVELOPMENT AND SURVIVAL OF STABLE FLIES

for S. niger. Most reports on this species relate to feeding habits. Some studies examined seasonal changes in abundance and their relationships with Þeld temperature and rainfall, in Africa (Kangwagye 1974) and Mauritius (Kunz and Monty 1976). Ramsamy (1979) developed rearing methods suitable for S. niger, but there have been no experimental studies of the inßuence of environmental factors on the life stages. In the ongoing research in La Re´ union, a systematic comparison between the two species has been undertaken to gather not only new information on S. niger but also further information on S. calcitrans. Traits may vary between populations of a cosmopolitan species, especially in islands (Hedrick 1984). In our study, the inßuence of temperature on the development of both species was determined in the laboratory. The survival and developmental rate of three life stages (eggs, larvae, and pupae) were compared between S. calcitrans and S. niger.

Materials and Methods Study Area. La Re´ union, the largest volcanic island of the Mascarene archipelago (2,507 km2), lies 800 km east of Madagascar (21⬚ 20⬘ S, 55⬚ 15⬘ E). This island rises to 3,069 m and has a tropical climate. Mean annual temperatures are 23Ð26⬚C at sea level. Annual rainfall ranges from 700 to 1,200 mm on the west coast to 3,000 Ð5,000 mm on the east coast. La Re´ union has ⬎36,000 heads of cattle, found mainly in moderately elevated areas. Biological Material. Insects were from recent stock colonies of S. calcitrans and S. niger (Þrst to third generation in the laboratory). Colonies were established in January 2002 during the annual pullulation period from ßies trapped at a dairy farm in the southeastern part of the island (910-m elevation). They were maintained at 25 ⫾ 1⬚C and 70 ⫾ 10% RH under a photoperiod of 12:12 (L:D) h, in the CIRAD-3P Laboratory, La Re´ union. Cages (30 by 30 by 30 cm) containing ⬇1000 adult ßies were placed above an oviposition substrate composed of elephant grass, Pennisetum purpureum Schumacher, crumbs. The same substrate was used as larval development medium. The ßies were fed daily with bovine blood collected twice a week from a slaughterhouse and citrated at 6 g liter⫺1. For this, sponges dampened with blood and warmed at 38⬚C in a water bath were laid on the top of each cage for 45 min. The oviposition substrate was changed daily. When pupae were observed, they were removed from the rearing medium by ßotation, dried, and transferred to new cages. Developmental Time and Survival of Life Stages. Experiments were conducted in climatic chambers (MLR-350, Sanyo, Japan) at Þve constant temperatures (15, 20, 25, 30, and 35⬚C) and 70 ⫾ 10% RH, under a photoperiod of 12:12 (L:D) h. These conditions were controlled daily by using a thermo-hygrograph (Jules Richards Instruments, Paris, France), a mercury thermometer, and a digital thermo-hygrometer.

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After the oviposition substrate was changed in the stock cultures, freshly laid eggs were collected with a brush and transferred onto moistened pieces of dark blotting-paper (3 by 3 cm). At least 750 eggs of each species were collected over several days. The time of transfer was considered the time of egg laying. The pieces of blotting paper were put into dishes (10 cm in diameter by 10 cm in height) containing P. purpureum crumbs and covered with mosquito tulle to prevent larvae from exiting. Eggs were then observed under a binocular microscope at 4-h intervals during the day (8 Ð10-h intervals at night) to count and remove empty chorions. This approach provided the number of young larvae hatched in each dish in the time interval. To assess the egg stage duration, hatching was assumed to occur at the middle of the time interval. After each observation, the unhatched eggs remaining on blotting paper were placed in a new dish, so that all dishes contained only larvae hatched in the same time interval. Eggs that did not hatch within 10 d were considered dead. The developmental time and survival of larvae were determined in the same way, by counting newly formed pupae in the medium. These were transferred to plastic boxes (8 by 4 by 1.5 cm) containing a slightly moistened sponge. Observations were continued to record the number of newly emerged adults in each box, which made it possible to determine the developmental time and survival of pupae. All stage durations were thus estimated, with errors ranging between 0 and 5 h (⬇0.2 d). The duration of development for each individual was obtained by summing its developmental times as egg, larva, and pupa. Temperature Summation Models. In both species, the linear regressions were established between developmental rate (1/developmental time, in days) and temperature. When the regression was signiÞcant, the lower threshold for development (T0), i.e., the theoretical temperature at which the developmental rate is zero, was calculated as the x intercept. The inverse of the slope of the regression line was the thermal constant (K), i.e., the number of heat units above T0, expressed as day-degrees (DD), that are required to complete development (Honek 1996, Danks 2000). Statistical Analyses. All analyses were conducted using SAS (SAS Institute 2001). The effects of temperature and species on the proportions of survivors were tested using PROC GENMOD. Two-way analysis of variance was used to test the effects of temperature and species on the developmental time (PROC GLM). In both types of analysis, pairwise mean comparisons were made with the Bonferroni signiÞcance level adjustment. Linear regressions of developmental rate on temperature were calculated using PROC REG. Results Survival. The total survival of the immature stages, from egg laying to adult emergence, differed signiÞcantly among temperatures (␹2 ⫽ 321.40, df ⫽ 4, P ⬍ 0.001) and species (␹2 ⫽ 54.88, df ⫽ 1, P ⬍ 0.001).

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Fig. 1. Total survival of the immature stages in S. calcitrans (Œ) and S. niger (f) reared at Þve constant temperatures. Proportions are given with 95% conÞdence intervals.

There was a signiÞcant temperatureÐspecies interaction (P ⬍ 0.001), because the differences in survival between species were not exactly the same at all temperatures. Although S. calcitrans consistently showed a higher survival than S. niger (Fig. 1), the differences were signiÞcant only at 20⬚C (␹2 ⫽ 10.69, df ⫽ 1, P ⬍ 0.01), 25⬚C (␹2 ⫽ 8.96, df ⫽ 1, P ⬍ 0.01), and 35⬚C (␹2 ⫽ 41.30, df ⫽ 1, P ⬍ 0.001). In both species, survival was highest at 20 and 25⬚C, without any signiÞcant difference between these temperatures. At 15⬚C, survival decreased signiÞcantly (␹2 ⫽ 40.66, df ⫽ 1, P ⬍ 0.001 for S. calcitrans; ␹2 ⫽ 23.43, df ⫽ 1, P ⬍ 0.001 for S. niger). Above 25⬚C, survival decreased slightly at 30⬚C, with the difference being signiÞcant in S. calcitrans only (␹2 ⫽ 3.92, df ⫽ 1, P ⬍ 0.05), but there was a dramatic decrease in both species at 35⬚C (␹2 ⫽ 48.11, df ⫽ 1, P ⬍ 0.001 for S. calcitrans; ␹2 ⫽ 129.19, df ⫽ 1, P ⬍ 0.001 for S. niger). At this temperature, only 35% of the S. calcitrans eggs and 6% of the S. niger eggs reached the adult stage (Fig. 1). Survival data for the life stages (Table 1) served to specify the least resistant stage to low and high temperatures in each species. At 15⬚C, mortality was observed mainly in larvae for S. calcitrans and in eggs for

Table 1.

Fig. 2. Duration of development from the egg to the adult stage in S. calcitrans (A) and S. niger (B) reared at Þve constant temperatures.

S. niger. In contrast, at 35⬚C, mainly pupae of both species died. Developmental Time. The developmental time from the egg to the adult stage differed signiÞcantly among temperatures (F ⫽ 13172.5; df ⫽ 4, 880; P ⬍ 0.001) and species (F ⫽ 11.09; df ⫽ 1, 880; P ⬍ 0.001), and there was again a signiÞcant interaction between the two factors (F ⫽ 25.58; df ⫽ 4, 880; P ⬍ 0.001). In both species, developmental time decreased for each 5⬚C increase in temperature between 15 and 30⬚C (Fig. 2). In contrast, developmental time increased

Proportions of survivors at different life stages, in S. calcitrans and S. niger reared at five constant temperatures

Stage Egg Larva Pupa Total development

Species S. calcitrans S. niger S. calcitrans S. niger S. calcitrans S. niger S. calcitrans S. niger

15⬚C n 150 210 135 129 92 119 150 210

20⬚C

mean 0.90a 0.61a 0.68a 0.92a 0.82a 0.76a 0.50a 0.42a

n

*** * ** NS

150 150 140 124 126 107 150 150

25⬚C

mean 0.93a 0.83b 0.90b 0.86a 1.00b 0.95b 0.84b 0.68b

** NS ** **

n 150 150 142 125 125 119 150 150

30⬚C

mean 0.95a 0.83b 0.88b 0.95b 1.00b 0.87c 0.83b 0.69b

n

** * *** **

150 150 144 118 112 112 150 150

35⬚C

mean 0.96a 0.79b 0.78ac 0.95b 0.99b 0.88c 0.74c 0.65b

n

*** *** *** NS

150 150 137 141 115 86 150 150

mean 0.91a 0.94c 0.84cd 0.61c 0.45c 0.10d 0.35d 0.06c

NS *** *** ***

Means followed by different letters within a line are signiÞcantly different at the 5% level. Asterisks indicate signiÞcant differences between species for a given stage at given temperature (*P ⬍ 0.05, **P ⬍ 0.01, ***P ⬍ 0.001; NS, not signiÞcant).

Total development

Pupa

Larva

Egg

Means followed by different letters within a line are signiÞcantly different at the 5% level. Sample sizes are given in Table 1. Asterisks indicate signiÞcant differences between species for a given stage at given temperature (*P ⬍ 0.05, **P ⬍ 0.01, and ***P ⬍ 0.001; NS, not signiÞcant).

1.17 ⫾ 0.01d*** 1.46 ⫾ 0.01d 6.58 ⫾ 0.09d*** 6.05 ⫾ 0.03d 5.17 ⫾ 0.05d*** 6.25 ⫾ 0.06d 12.92 ⫾ 0.08d*** 13.76 ⫾ 0.07d 1.62 ⫾ 0.03c** 1.78 ⫾ 0.03c 8.74 ⫾ 0.15c NS 8.44 ⫾ 0.07c 6.29 ⫾ 0.07c*** 7.15 ⫾ 0.06c 16.65 ⫾ 0.15c*** 17.36 ⫾ 0.10c 2.33 ⫾ 0.04b*** 2.85 ⫾ 0.01b 19.09 ⫾ 0.29b*** 15.87 ⫾ 0.29b 10.94 ⫾ 0.08b** 11.74 ⫾ 0.15b 32.36 ⫾ 0.31b*** 30.47 ⫾ 0.26b 4.47 ⫾ 0.04a*** 5.75 ⫾ 0.09a 42.02 ⫾ 0.47a*** 37.16 ⫾ 0.60a 24.17 ⫾ 0.20a*** 25.84 ⫾ 0.26a 70.66 ⫾ 0.42a** 68.75 ⫾ 0.59a S. calcitrans S. niger S. calcitrans S. niger S. calcitrans S. niger S. calcitrans S. niger

30⬚C (mean ⫾ SE) 25⬚C (mean ⫾ SE) 20⬚C (mean ⫾ SE) 15⬚C (mean ⫾ SE) Species Stage

Mean developmental times (in days) at different life stages, in S. calcitrans and S.niger reared at five constant temperatures Table 2.

1.14 ⫾ 0.01d*** 0.96 ⫾ 0.02e 6.49 ⫾ 0.08d* 7.12 ⫾ 0.36e 5.54 ⫾ 0.08e** 6.39 ⫾ 0.37d 13.17 ⫾ 0.10d*** 14.47 ⫾ 0.13e

GILLES ET AL.: DEVELOPMENT AND SURVIVAL OF STABLE FLIES 35⬚C (mean ⫾ SE)

May 2005

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Fig. 3. Relationships between temperature and developmental rate (1/developmental time) in S. calcitrans (Œ, Sc) and S. niger (f, Sn) based on the durations of total development at four constant temperatures.

slightly when temperature increased from 30 to 35⬚C. All differences were signiÞcant, except for the increase in developmental time at 35⬚C in S. calcitrans (see tests in Table 2). At all temperatures, developmental time differed signiÞcantly between the two species, but there was an obvious temperatureÐspecies interaction: at 15 and 20⬚C, development was signiÞcantly shorter in S. niger, whereas at 25, 30, and 35⬚C it was slightly but significantly shorter in S. calcitrans (Table 2). Data for the different life stages (Table 2) show that the fast development of S. niger at 15 and 20⬚C resulted only from the performance of the larvae. Temperature Summation Models. The durations of total development in both species resulted in highly signiÞcant linear relationships between developmental rate and temperature within the 15Ð30⬚C range (Fig. 3). The linear relationships between the developmental rate of each life stage and temperature were also highly signiÞcant (Table 3). The lower temperature thresholds (T0) were calculated both for the development of each life stage and for total development (Table 3). T0 for egg development did not differ signiÞcantly between species, but there were signiÞcant differences for larval, pupal, and total development, with lower values in S. niger. T0 for total development was 11.3⬚C in S. niger versus 12.2⬚C in S. calcitrans. The day-degree requirement to complete development (K) was higher in S. niger (250.6 DD) than in S. calcitrans (224.7 DD). Discussion Most of the results obtained on S. calcitrans in this study are consistent with previous results on the effects of temperature on the speciesÕ survival and developmental time (Kunz et al. 1977, Sutherland 1979,

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Table 3.

Vol. 42, no. 3

Regression equations of developmental rate on temperature (T) in S. calcitrans and S. niger

Stage Egg Larva Pupa Total development

Species

Equation

SigniÞcance

R2

T0

T0 95% CL

S. calcitrans S. niger S. calcitrans S. niger S. calcitrans S. niger S. calcitrans S. niger

⫺0.41455 ⫹ 0.04272T ⫺0.34714 ⫹ 0.03558T ⫺0.12248 ⫹ 0.00931T ⫺0.11727 ⫹ 0.00940T ⫺0.11651 ⫹ 0.01066T ⫺0.08019 ⫹ 0.00835T ⫺0.05441 ⫹ 0.00445T ⫺0.04525 ⫹ 0.00399T

⬍0.001 ⬍0.001 ⬍0.001 ⬍0.001 ⬍0.001 ⬍0.001 ⬍0.001 ⬍0.001

0.82 0.77 0.89 0.97 0.86 0.84 0.95 0.97

9.70 9.76 13.16 12.48 10.93 9.60 12.23 11.34

10.15Ð9.29 10.31Ð9.26 13.60Ð12.74 12.70Ð12.26 11.37Ð10.53 10.05Ð9.20 12.49Ð11.98 11.53Ð11.16

T0 indicates the lower threshold of development (⬚C).

Lysyk 1998). Mean developmental times observed in La Re´ union are similar to those reported for North American populations reared at constant temperatures. Minor differences may be because, in the current study, the developmental time of each life stage was based only on individuals that actually reached adulthood, excluding individuals that died before completing their development. For the latter, developmental times were generally longer than in successful individuals. The greatest difference between the results of this study and those previously conducted with S. calcitrans concerns the pupal survival at high temperatures, which was higher in La Re´ union. At 30⬚C, 99% of pupae survived in La Re´ union versus 60 Ð70% in most North American studies (Kunz et al. 1977, Lysyk 1998). The difference may reßect local adaptation to tropical climatic conditions. This observation is new for the cosmopolitan S. calcitrans, which generally shows little differentiation between widely distant regions, at least in terms of survival and developmental rate (Lysyk 1998). Note, however, that life history parameters have generally been measured from stock cultures maintained under standard laboratory conditions for many generations, which makes it difÞcult to compare populations (Tauber et al. 1986). Results on local adaptation that are more signiÞcant might be obtained by comparing samples recently collected in the Þeld, as in this study. For the Þrst time, life history traits were compared between S. niger and S. calcitrans under controlled laboratory conditions. Developmental time is highly similar in both species: it ranges from 69 d at 15⬚C to 14 d at 30⬚C in S. niger, compared with 71 d at 15⬚C and 13 d at 30⬚C in S. calcitrans. The pattern of immature survival in relation to temperature is also similar in both species, with the highest survival at 20 Ð25⬚C and a decrease at lower and higher temperatures. At low temperature, the least resistant stage differs between species (the egg in S. niger and the larva in S. calcitrans), but at high temperature the least resistant stage in both species is the pupa. In Diptera, this life stage is obviously the most susceptible to heat, probably because of harmful effects on the metamorphosis process (Bayoh and Lindsay 2004). The most obvious difference between the two species concerns the mean survival at each temperature, which was consistently lower in S. niger. Yet, it is difÞcult to know whether this difference reßects actual differences in

the Þeld or whether this relates to the experimental conditions. Although the rearing medium used (elephant grass) has been reported to favor S. niger (Kunz and Monty 1976, Ramsamy 1979), there may have been an undetected problem acting against the species in the laboratory. In such a case, survival differences between S. calcitrans and S. niger might be smaller in the Þeld. This point should be reexamined under a variety of rearing conditions. Another difference between the two species concerns the larval development at low temperatures. At 15⬚C, the larvae of S. niger develop faster and survive much better than the larvae of S. calcitrans. S. niger may temporarily take advantage of this trait in late winter, which should be taken into account in any attempt to explain how the two species coexist in La Re´ union. The developmental thresholds and day-degree requirements of the two species also suggest that S. niger is better adapted than S. calcitrans for development at low temperatures. When T0 and K vary inversely in directly comparable species, the species that exhibits the lower T0 and the higher K may have a competitive advantage in cold environments (Trudgill 1995, Honek 1996). Surprisingly enough, the tropical S. niger performs better below 20⬚C, whereas the cosmopolitan S. calcitrans performs better at higher temperatures, at least regarding developmental rates. In conclusion, the current study suggests that S. calcitrans is better adapted than S. niger in terms of adult production over the range of temperatures in La Re´ union. Despite the slightly shorter developmental time of S. niger at low temperatures, this speciesÕ advantage may be offset by its higher mortality during development when temperature reaches 20⬚C. At higher temperatures, S. calcitrans consistently shows a higher developmental rate and a better survival than S. niger. These results are consistent with the high incidence of S. calcitrans in La Re´ union, although some aspects remain unexplained. For example, the current study cannot account for the relatively high incidence of S. niger in the warm coastal area of the island, and its even higher incidence in Mauritius (Monty 1972, Kunz and Monty 1976), where the climate is warmer than in La Re´ union. Further data are needed to clarify the effects of temperature on the population growth potential of both species, especially data on the reproductive pattern and lifetime fecundity of females at different temperatures.

May 2005

GILLES ET AL.: DEVELOPMENT AND SURVIVAL OF STABLE FLIES Acknowledgments

We thank Gary Burkhart for critical reading of the manuscript. We are grateful to E. Tillard and K. Le Roux (Centre de coope´ ration Internationale en Recherche Agronomique pour le De´ veloppement [CIRAD], La Re´ union) and to the “Groupement Re´ gional de De´ fense Sanitaire du Be´ tail de La Re´ union” for assistance. This research was supported by funds from the CIRAD-3P, the Conseil Re´ gional of La Re´ union Island and the Centre National de la Recherche ScientiÞque (UMR 5175).

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