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1 December 2014 Behavioral Rhythms of Drosophila Suzukii and Drosophila Melanogaster
Author Affiliations +
Abstract

Drosophila suzukii and Drosophila melanogaster feed on various fruits, causing great economic losses. In order to find the optimum time for controlling D. suzukii and D. melanogaster, the daily rhythms of oviposition, egg hatch, pupation, adult eclosion, copulation, and feeding of these two pests were studied. We found the circadian rhythm of D. suzukii oviposition to have a single pattern with a peak from 20:00–24:00, while the peak oviposition of D. melanogaster was from 16:00–4:00 (the next day). Neither D. suzukii nor D. melanogaster showed a daily pattern of egg hatch; the single peak of egg hatch for D. suzukii occurred 24–32 h after oviposition, while that for D. melanogaster followed a bimodal pattern, with the first peak of egg hatch from 0–4 h after oviposition and the second from 32–36 h after oviposition. Pupation in D. suzukii showed a single peak from 8:00∼16:00, while in D. melanogaster pupation followed a bimodal pattern, with peaks from 4:00–8:00 and 12:00–20:00. Eclosion of of D. suzukii adults followed a unimodal pattern, and generally took place from 0:00–8:00, while that of D. melanogaster also showed a single peak, generally from 0:00–12:00. Meanwhile copulation of D. suzukii, which showed a bimodal pattern, was concentrated from 0:00–12:00 and 20:00–24:00 (the next day), while copulation of D. melanogaster showed a single peak, generally from 0:00–12:00. Both D. suzukii and D. melanogaster had a preference for feeding in light, and in a 24 h photoperiod the percentages of feeding insects were 80.8and 81.1, respectively.

Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) and Drosophila melanogaster Meigen (Diptera: Drosophilidae) are both important fruit pests. Drosophila suzukii is especially damaging to ripe cherries (Van der Linde et al. 2006). It's hard, serrated ovipositor can easily pierce the fruit skin, inserting eggs within intact fruits with little visible damage from oviposition on the fruit surface. The larvae hatching from eggs feed on the fruit, and cause it to soften, brown and completely rot. Many fruits are damaged by D. suzukii, including blueberry, blackberry, cherry, strawberry, plums, peaches, grapes, figs, kiwi fruit and pears (Dreves et al. 2009). In the United States, losses of strawberry, blueberry and raspberry caused by D. suzukii reached 80, 40, and 70%, respectively (Bolda et al. 2011). With increased planting of fruit trees in China, D. melanogaster has increased in importance as a pest of Chinese bayberry and cherries. In Tianshui, Gansu Province, some late-maturing varieties of cherries are especially susceptible to damage by D. melanogaster, and they suffer losses generally above 35%, and as high as 80% on some cultivars (Guo et al. 2007).

Fig. 1.

The ovipositional rhythms of Drosophila suzukii and Drosophila melanogaster. Data represent the mean values ± SEM (n = 4) for 4-h periods, and histograms with different letters indicate a significant difference (P = 0.05, Duncan's multiple range test), i.e., lower case letters show a significant difference for D. suzukii, and upper case letters C show a significant difference for D. melanogaster. Fecundity of D. melanogaster was much greater than that of D. suzukii. Lights were turned on at 4:30 am and off at 20:30 pm.

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Daily biological rhythms are common in insects (Pittendrigh 1993; Takahashi 1995). Many life activities of insects, such as phototaxis, body color change, migration, feeding, hatching, eclosion, mating and oviposition exhibit a rhythm (Saunders 2002). It is helpful to determine the activity rhythms of populations of both beneficial and harmful insects as a basis for developing and improving methods for preventing or controlling the latter (Tu & Chen 2013). Applications of insect pheromones in pest control developed in recent decades, are based to some extent on studies of the timing of eclosion and rhythms of sexual activities insect pest species, and it may be possible to further improve pheromone-based control technology through better understanding of the circadian rhythms of pest species (Ran et al. 2013). There have been many studies on the behavioral rhythms of D. melanogaster, but few on those of D. suzukii. This study examines the rhythms of both species with respect to oviposition, egg hatch, pupation, adult eclosion, feeding and copulation. This information further understanding of the biological characteristics of D. suzukii and D. melanogaster these species, and may provide an important basis and technical guidance for their integrated control.

Materials and Methods

Experimental Insects

Both D. suzukii and D. melanogaster were obtained as larvae from infested fruit from cherry orchards in Tai'an, Shandong Province in May 2012, and flies were then raised in an insectary for about 11 generations at 25 ± 1 °C, 70 ± 5% RH, and 16:8 h (L:D) with the lights were turned on at 4:30 am and off at 20:30 pm. This light regime approximated the local natural photoperiod. The off light intensity was 10,000 lux. Table grapes (‘Kyoho' grape cultivar, Vitis vinifera L.; Vitales: Vitaceae), purchased from the market, were rinsed 3 times in distilled water and dried and cut into halves for adult oviposition and larval development. The average weight of each grape was 20.38 g.

Fig. 2.

The incubation rhythms of Drosophila suzukii and Drosophila melanogaster. Data represent the mean values ± SEM (n = 5) at 4 h, and significant differences at P = 0. 05 by Duncan multiple range test. Most D. suzukii eggs hatched with a single peak at 24–32 h after the eggs were laid, but D. melanogaster eggs hatched with two peaks, one at 4 h and the second at 32–36 h after eggs were laid. Error bars topped with different letters are significantly different.Lights were turned on at 4:30 am and off at 20:30 pm.

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Oviposition Rhythm

Females 4–6 days after emergence were used for quantifying the oviposition rhythm. These females had mated and could have laid eggs for 2–3 days. Each group had 5 individual females with 4 replicates of either D. suzukii or D. melanogaster. They were placed into circular insectary bottles (2000 mL flat drum glass bottles) containing one fresh grape cut into halves. The grapes were replaced every four hours for 48 h, and the number of eggs laid was determined. The experiment was replicated 4 times.

Fig. 3.

The pupation rhythms of Drosophila suzukii and Drosophila melanogaster. Data represent values ± SEM (n = 5) in 4 h observation periods, at 4 h, and histograms with different letters indicate a significant difference (P = 0.05, Duncan's multiple range test). Most D. suzukii larvae pupated with a single peak between 8:00 to 16:00, but most D. melanogaster larvae pupated with two peaks, one at 4:00–8:00 and the second at 12:00–20:00. Error bars topped with different letters are significantly different. Lights were turned on at 4:30 am and off at 20:30 pm.

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Hatching Rhythm

Grapes were cut into halves and placed in the circular bottle described above with the cut surface upward to provide food for the fruit flies. A certain number of either mated D. suzukii or D. melanogaster females were selected and each cohort was held in a bottle usually for 4 h to lay eggs. The number of new larvae from hatched eggs was counted every 4 h after oviposition for a continuous 48 h observation period. The experiment was replicated 5 times for each species.

Pupation Rhythm

In this experiment, each group had 40 individual 3rd instar larvae of either D. suzukii or D. melanogaster. The larvae were reared in petri dishes (12 cm dia., 1.5 cm high), and fed mashed grapes. The number of pupae was counted every 4 h over 48 h. The experiment was replicated 5 times.

Adult Eclosion Rhythm

In this experiment, each group had 30 pupae of either D. suzukii or D. melanogaster. The pupae were placed in petri dishes (12 cm dia, 1.5 cm high) with cotton soaked in distilled water to stabilize the relative humidity. Total emergence and the numbers of eclosed males and females were calculated every 4 h over a 48 h observation period. The experiment was replicated 5 times.

Copulation Rhythm

Two hundred unmated male and 200 female D. suzukii flies were selected and held separately by sex in 2,000 mL flat drum bottles. After 12 h, the males and females were divided into 4 groups each with 50 of each gender, and the number of pairs of mated flies was counted every 4 h over 48 h. The identical experiment was conducted with D. melanogaster.

Feeding Rhythm

Two hundred healthy adults of either D. suzukii or D. melanogaster were released into a closed screened cage (1.0 × 0.8 × 0.8 m). A transparent plastic bottle filled with a 10 mL honeywater mixed with 1 mL emamectin benzoate (2.2%) solution was hung in the cage and the numbers of flies feeding from the bottle every 4 h over 48 h period were counted. The experiment was replicated 4 times.

Statistical Analysis

The means were assessed with one-way ANOVA, significant differences (P < 0.05) were tested with Duncan's test. All statistics were analyzed in SPSS 17.0.

Results

Oviposition Rhythm

In this experiment, Drosophila suzukii females laid a total of 1,297 eggs, with the egg-laying peak extending from 20:00–24:00. In this peak each female laid an average of 33 eggs, which accounted for 50.9% of the eggs one female laid in a single light cycle. Likewise D. melanogaster females laid a total of 2,743 eggs, with the egg-laying peak extending across 16:00–4:00 (the next day). During this protracted peak each female laid and average of 128.06 eggs, which accounted for 93.4% of the total per female in a single circadian period (Fig. 1).

Fig. 4.

The eclosion rhythms of Drosophila suzukii males and females. Most adults emerged during the hours that correspond to dawn. The number of females was larger than the number of males. Error bars topped with different letters are significantly different. Lights were turned on at 4:30 am and off at 20:30 pm.

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Egg Hatching Rhythm

In total, 132 D. suzukii eggs and 130 D. melanogaster eggs were observed to hatch per 5-female replicate; i.e., an average of 26.4 and 26.0 per female, respectively. Per replicate an average 19.8 D. suzukii eggs of hatched 24∼32 h after the eggs were laid; i.e., 75% of the eggs that hatched. Hatching of D. melanogaster occurred in 2 peaks, the first at 0∼4 h and the second 32∼36 h after oviposition. In the first peak 7.0 eggs hatched, and in the second peak, 11.0 eggs hatched. These two peaks accounted for 26.9% and 42.3% of the total eggs that hatched, respectively (Fig. 2). No photoperiodic rhythm of egg hatching was found in either species.

Fig. 5.

The eclosion rhythms of Drosophila melanogaster males and females. Most adults emerged during the hours that correspond to dawn. The number of females was larger than the number of males. Error bars topped with different letters are significantly different. Lights were turned on at 4:30 am and off at 20:30 pm.

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Pupation Rhythm

A total of 181 third-instar D. suzukii larvae pupated, i.e., an average of 36.2 pupae per 5-female replicate. Pupation occurred in a single major peak from 8:00∼16:00 during which 21.2 pupae were formed, accounting for 58.6% of the pupae. In contrast, 161 D. melanogaster larvae pupated, i.e., an average of 32.2 pupae per 5-female replicate. Most pupation occurred in 2 peaks from 4:00–8:00 and 12:00–20:00. During the first peak 7.6 pupae were formed and during the second peak 17.4 pupae were formed. These peaks accounting for 23.6% and 54.0% of the pupae, respectively (Fig. 3).

Adult Eclosion Rhythm

Adults emerged from 138 D. suzukii pupae and from 206 D. melanogaster pupae. Both species exhibited a unimodal pattern of emergence with a peak during the 0:00∼8:00 period. The eclosion rates for D. suzukii and D. melanogaster were 78.3% and 83.6%, respectively (Figs. 4 and 5).

Copulation Rhythm

Drosophila suzukii adults were observed to mate 192 times. Matings were distributed in a bimodal pattern and both two peaks occurred from 20:00∼12:00 (the next day). These two peaks accounted for 89.6% of the total matings. In contrast, the 217 matings of D. melanogaster were generally concentrated in the period 0:00∼12:00, and this peak accounted for 96.8% of the total copulations (Fig. 6).

Feeding Rhythm

A total of 638 D. suzukii and 752 D. melanogaster adults were trapped during the observation period. Both species were found to favor feeding during the photophase. During 4:00–20:00, 128.8 D. suzukii and 152.5 D. melanogaster adults were found to feed, i.e., on average 80.8% and 81.1%, respectively. The study revealed that slightly more flies of both species tended to feed during the forenoon than in the afternoon, i.e., 42.5% of D. suzukii and 45.0% of D. melanogaster fed during the forenoon (Fig. 7).

Discussion

Reports on the ovipositional rhythms of insects began to appear in the 1950s and have gradually increased in recent years (Haddow & Gillett 1957; Pittendrigh & Minis 1964; Minis 1965). These reports included research on Ostrinia nubilalis and Rhodnius prolixus (Skopik & Takeda 1980; Ampleford & Davey 1989). Several studies on the ovipositional rhythms of fruit flies have involved D. melanogaster, other Drosophila spp. and Zaprionus spp. (Rensing & Hardeland 1967; Gruwez et al. 1972; David & Fouillet 1973; Allemand 1974, 1976a, 1976b, 1976c, 1977). Fleugel (1978) studied the egg production of D. melanogaster individuals in weak light of the light-dark cycle, and found an oviposition rhythm under 12:12 h L:D conditions, which he held to be the hourglass timing mechanism, not an endogenous rhythm. Many recent studies, however, have found that wild and mutant varieties of fruit flies also display rhythmic oviposition (McCabe & Birley 1998; Sheeba et al. 2001). This study found the oviposition of both D. suzukii and D. melanogaster followed a circadian rhythm, with the effects of light having a greater effect on D. suzukii, which showed two oviposition peaks compared to one peak by D. melanogaster.

Fig. 6.

The copulation rhythms of Drosophila suzukii and Drosophila melanogaster. Data represent the mean values ± SEM (n = 4) in 4 h observation periods. Few matings of either species were observed between 12:00 and 20:00. Error bars topped with different letters are significantly different. Lights were turned on at 4:30 am and off at 20:30 pm.

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A previous study on Dacus tryoni found that the rhythm of egg hatching played a certain role in total egg development (Bateman 1955). Meanwhile, our study found that neither Drosophila species displayed a photoperiodic rhythm for egg hatch, nor while both species' eggs may contain a timing mechanism, it is not related to the circadian system.

Fig. 7.

The feeding rhythms of Drosophila suzukii and Drosophila melanogaster. Data represent the mean values ± SEM (n = 4) in 4 h observation periods. Both species fed more extensively during the photophase than during the scotophase. Error bars topped with different letters are significantly different. Lights were turned on at 4:30 am and off at 20:30 pm.

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While the behavior of Sarcophagidae larvae before pupation and adult eclosion were found to be rhythmic (Saunders 1986), pupation itself was not rhythmic (Richard et al. 1986), possibly because pupation occurred underground. The two Drosophila species in this study, however, both showed different pupation rhythms and the process occurred aboveground. As peak pupation of D. suzukii was in the morning, it seems likely that light promotes the formation of the puparium. The two peaks of D. melanogaster occurred in the morning and afternoon, and such a rhythm may serve to protect the newly emerged adults from the effects of intense sunlight.

Emergence rhythms of a variety of insects have been studied, but those of Drosophila spp. have been reported on in the most detail. The circadian rhythm period of Drosophila emergence is about 24 h, and the eclosion rhythms are endogenous. The emergence of Drosophila pseudoobscura, for instance, is usually concentrated at dawn, and the peak shifts with changing photoperiod (Pittendrigh 1965). For example, the emergence peak occurred before dawn under short illumination conditions (light periods shorter than 6–7 h), after dawn under long photoperiod conditions, and from 2∼3 h after the start of the photoperiod under 12:12 h L:D conditions (Bünning 1935). This study found that both D. suzukii and D. melanogaster had a single peak, generally concentrated from 0:00∼8:00 and 0:00∼12:00, respectively. One of the possible explanations is that relative humidity and cool air favor the expansion of wings in newly emerged adults, and high temperatures disturb the process of wing expansion significantly (Tanaka & Watari 2009; Shereen & Shakunthala 2012). In addition, among the newly emerged adults of the two species, females were found to outnumber males, and this may be related to the carbon/nitrogen ratio in the diet.

While a mating rhythm controlled by an endogenous biological clock has been confirmed in some insects (Smith 1979), the mating behavior of insects is affected to some extent by photoperiod. The mating rhythms of Anastrepha ludens (Flitters 1964) and Dacus tryoni (Tychsen & Fletcher 1971) both showed a certain light-based cycle. Our study found that D. suzukii mating had a bimodal pattern, with the peak concentrating in 20:00 ∼ 12:00 (the next day), indicating that individuals' mating ability might be affected by light duration in one photoperiod. The mating of D. melanogaster was unimodal, with more than 50% concentrated in the 4 h immediately after the dark period and more than 80% in the 8 h following the dark period, showing an extremely significant effect of photoperiod.

No research on the feeding rhythm of fruit flies has been found, but other studies found that cockroaches are the most active at night and usually feed in the dark. The American cockroach, Periplaneta americana feeds in the early to middark period, exhibiting an endogenous circadian rhythm (Lipton & Sutherland 1970). Nymphs and adults of the cricket Acheta domesticus also showed a feeding rhythm (Nowosielski & Patton 1963). In laboratory experiments, bumble bee foragers showed free-running circadian rhythms in both LL and DD, with mean free-running periods significantly shorter in LL than DD (Stelzer et al. 2010). In addition, Xiao et al. (2009) found that a wild variety of D. melanogaster exhibited an obvious bimodal feeding pattern with peaks in the morning and evening. In our study, both D. suzukii and D. melanogaster individuals preferred to feed in the light, with the percentage of feeding individuals in the morning being slightly larger than that in the afternoon.

The damage caused by Drosophila larvae feeding inside fruit is imperceptible at first, and as the systemic use of insecticides increases the risk of residues in fruit, adult trapping techniques are an important tool in the prevention and control of fruit flies (Sun et al. 2005). Behavioral rhythms factor into the control of D. suzukii and D. melanogaster, and an understanding of these patterns should be helpful in the forecasting populations and further improving the control of these pest species.

Acknowledgments

We would like to thank professor Dong Chu and Fangqiang Zheng for their generous help with editing. This work was supported by the Shandong Provincial Modern Agricultural Industry Technology System Innovation Team Foundation, China (SDAIT-03-022-08) and Ministry of Agriculture Agricultural Research Exceptional Talents and Innovation Team Foundation, China.

References Cited

1.

R. Allemand 1974. Importance evolutive du comportement de ponte chez les insects: comparaison du rythme circadien d'oviposition chez les six especes de Drosophila du sous-groupe melanogaster. Comptes rendus hebdomadaires des séances de l'Académie des Sciences 279: 2075–2077. Google Scholar

2.

R. Allemand 1976a. Importance adaptative du rythme circadien de ponte chez les drosophilides: comparaison de huit especes du genre Zaprionus. Comptes rendus hebdomadaires des seances Serie D. Sciences naturelles 282: 85–88. Google Scholar

3.

R. Allemand 1976b. Influence de modifications des conditions lumineuses sur les rythmes circadiens de vitellogenese et d'ovulation chez Drosophila melanogaster. J. Insect Physiol. 22: 1075–1080. Google Scholar

4.

R. Allemand 1976c. Les rythmes de vitellogenese et d'ovulation en photoperiode LD 12: 12 de Drosophila melanogaster. J. Insect Physiol. 22: 1031–1035. Google Scholar

5.

R. Allemand 1977. Influence de l'intensite d'eclairement sur l'expression du rythme journalier d'oviposition de Drosophila melanogaster en conditions lumineuses LD 12: 12. Comptes rendus hebdomadaires des seances. Serie D. Sciences naturelles 284: 1553–1556. Google Scholar

6.

E. Ampleford , and K. Davey 1989. Egg laying in the insect Rhodnius prolixus is timed in a circadian fashion. J. Insect Physiol. 35: 183–187. Google Scholar

7.

M. Bateman 1955. The effect of light and temperature on the rhythm of pupal ecdysis in the Queensland fruit-fly, Dacus (Strumeta) tryoni (Frogg.). Australian J. Zool. 3: 22–33. Google Scholar

8.

M. Bolda , L. Tourte , and K. M. Klonsky 2011. Sample costs to produce fresh market raspberries: central coast, Santa Cruz and Monterey Counties. Univ. California Coop. Ext.  http://coststudies.ucdavis.edu/files/raspberryccGoogle Scholar

9.

E. Bünning 1935. Zur Kenntniss der endogonen Tagesrhythmik bei Insekten und Pflanzen. Berichte Deutschen Bot. Ges. 53: 594–623. Google Scholar

10.

J. David , and P. Fouillet 1973. Enregistrement continue de la ponte chez Drosophila melanogaster et importance des conditions expeimentales pour l'etude du rythme circadien d'oviposition. Rev. Compare Animal 7: 197–202. Google Scholar

11.

A. J. Dreves , V. M. Walton , and G. C. Fisher 2009. A new pest attacking healthy ripening fruit in Oregon: spotted wing Drosophila: Drosophila suzukii (Matsumura). Corvallis, OR Ext. Serv., Oregon State Univ. Google Scholar

12.

W. Fleugel 1978. Oviposition rhythm of individual Drosophila melanogaster. Experientia 34: 65–66. Google Scholar

13.

N. Flitters 1964. The Effect of Photoperiod, Light Intensity, and Temperature on Copulation, Oviposition, and Fertility of the Mexican Fruit Fly. J. Econ. Entomol. 57: 811–813. Google Scholar

14.

J. Guo 2007. Bionomics of fruit flies, Drosophila melanogaster, damage cherry in Tianshui. Chinese Bull. Entomol. 44: 743–745 In Chinese. Google Scholar

15.

D. J. Guo , H. Jiang , Y. H. Zhang , C. L. Zhang , and H. B. Yang 2007. Occurrence of Drosophila melanogaster and Drosophila immigrans in Aba Prefecture. Plant Prot. 33 : 134–135 In Chinese. Google Scholar

16.

G. Gruwez , C. Hoste , C. Lints , and F. Lints 1971. Oviposition rhythm in Drosophila melanogaster and its alteration by a change in the photoperiodicity. Experientia 27: 1414–1416. Google Scholar

17.

A. Haddow , and J. Gillett 1957. Observations on the oviposition-cycle of Aedes (Stegomyia) aegypti (Linnaeus). Ann. Trop. Med. Parasitol. 51: 159–169. Google Scholar

18.

G. Lipton , and D. Sutherland 1970. Feeding rhythms in the American cockroach, Periplaneta americana. J. Insect Physiol. 16: 1757–1767. Google Scholar

19.

C. McCabe , and A. Birley 1998. Oviposition in the period genotypes of Drosophila melanogaster. Chronobiol. Intl. 15: 119–133. Google Scholar

20.

D. Minis 1965. Parallel peculiarities in the entrainment of a circadian rhythm and photoperiodic induction in the pink bollworm (Pectinophora gossypiella). Circadian Clocks 110(1): 333–343. Google Scholar

21.

J. Nowosielski , and R. Patton 1963. Studies on circadian rhythm of the house cricket, Gryllus domesticus L. J. Insect Physiol. 9: 401–410. Google Scholar

22.

C. S. Pittendrigh 1965. On the mechanism of entrainment of a circadian rhythm by light cycles, pp. 277–297 In J. Aschoff [ed.], Circadian Clocks. Amsterdam: North-Holland Publishing Co. Google Scholar

23.

C. S. Pittendrigh 1993. Temporal organization: reflections of a Darwinian clock-watcher. Annu. Rev. Physiol. 55: 17–54. Google Scholar

24.

C .S. Pittendrigh , and D. H. Minis 1964. The entrainment of circadian oscillations by light and their role as photoperiodic clocks. American Nat. 98: 261–294. Google Scholar

25.

H.F. Ran , Z.Y. Lu , W.X. Liu , Z.Q. Qu , and J. C. Li 2013. The sex ratio, circadian emergence rhythm and activity patterns of adult oriental fruit moth, Grapholitha molesta ( Busck) ( Lepidoptera: Tortricidae). Chinese J. Applied Entomol. 50(6): 1524–1531 (in Chinese). Google Scholar

26.

L. Rensing , and R. Hardeland 1967. Zur Wirkung der circadianen Rhythmik auf die Entwicklung von Drosophila. J. Insect Physiol. 13: 1547–1568. Google Scholar

27.

D. Richard , D. Saunders , V. Egan , and R. Thomson 1986. The timing of larval wandering and puparium formation in the flesh-fly Sarcophaga argyrostoma. Physiol. Entomol. 11: 53–60. Google Scholar

28.

D. S. Saunders , 1986. Many circadian oscillators regulate developmental and behavioural events in the flesh-fly, Sarcophaga argyrostoma. Chronobiol. Intl. 3: 71–83. Google Scholar

29.

D. S. Saunders 2002. Insect Clocks, 3rd edn. Pergamon Press, Oxford. Google Scholar

30.

V. Sheeba , M. Chandrashekaran , A. Joshi , and V. K. Shama 2001. Persistence of oviposition rhythm in individuals of Drosophila melanogaster reared in an aperiodic environment for several hundred generations. J. Exp. Zool. 290: 541–549. Google Scholar

31.

K. Shereen , and V. Shakunthala 2012. Eclosion behavior of three species of Drosophila under different light regimes. Indian J. Exp. Biol. 50(9): 1–5. Google Scholar

32.

S. D. Skopik , and M. Takeda 1980. Circadian control of oviposition activity in Ostrinia nubilalis. American J. Physiol. 239: 259–264. Google Scholar

33.

P. H. Smith 1979. Genetic manipulation of the circadian clock's timing of sexual behaviour in the Queensland fruit flies, Dacus tryoni and Dacus neohumeralis. Physiol. Entomol. 4: 71–78. Google Scholar

34.

R. J. Stelzer , R. Stanewsky , and L. Chittka 2010. Circadian foraging rhythms of bumblebee are monitored by radiofrequency identification. J. Biol. Rhythm. 25(4): 257–262. Google Scholar

35.

D. W. Sun , J. F. Cao , M. Y. Yang , H. Y. Yang , M. L. Yang , J. L. Yang , and W. Z. Yang 2005. Evaluation of Control Efficacy and Duration of 0.3% Azadirachtin emulsion against waxberry Drosophila Pesticides. Pesticides 44: 525–526 In Chinese. Google Scholar

36.

J. S. Takahashi 1995. Molecular neurobiology and genetics of circadian rhythms in mammals. Annu. Rev. Neurosci. 18: 531–553. Google Scholar

37.

K. Tanaka , and Y. Watari 2009. Is early morning adult eclosion in insect an adaptation to the increased moisture at dawn? Biol. Rhythm. Res. 40(4): 293–298. Google Scholar

38.

X. Y. Tu , and Y. S. Chen 2013. Circadian Behavioral Rhythms in Moths. Biol. Disaster Sci, 36(1): 18–21 (in Chinese). Google Scholar

39.

P. H. Tychsen , and B. S. Flether 1971. Studies on the rhythm of mating in the Queensland fruit fly, Dacus tryoni. J. Insect Physiol. 17: 2139–2156. Google Scholar

40.

K. Van Der Linde , G. J . Steck , K. Hibbard , J. S. Birdsley , L. M. Alonso , and D. Houle 2006. First records of Zaprionus indianus (Diptera: Drosophilidae), a pest species on commercial fruits from Panama and the United States of America. Florida Entomol. 89: 402–404. Google Scholar

41.

C. Y. Xiao , X. N. Cong , X. X. Liu , Q. W. Zhang , and Z. W. Zhao 2009. Circadian rhythms and diurnal time allocation in Drosophila melanogaster adults. Chinese Bull. Entomol. 46: 298–301. Google Scholar

42.

Y. S. Yang , G. Y. Ren , D. F. Yao , Y. Q. Li , and H. B. Lou 1998. Effect of killing Drosophila melanogaster with food bait in red bayberry. Guizhou Agric. Sci. 26: 25–29 In Chinese. Google Scholar
Qing-Cai Lin, Yi-Fan Zhai, Cheng-Gang Zhou, Li-Li Li, Qian-Ying Zhuang, Xiao-Yan Zhang, Frank G. Zalom, and Yi Yu "Behavioral Rhythms of Drosophila Suzukii and Drosophila Melanogaster," Florida Entomologist 97(4), 1424-1433, (1 December 2014). https://doi.org/10.1653/024.097.0417
Published: 1 December 2014
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