PAN-PACIFIC ENTOMOLOGIST 70(4): 269-275, (1994) TEMPERATURE STUDIES ON A CHINESE STRAIN OF BACTROCERA CUCURBITAE (COQUILLETT) (DIPTERA: TEPHRITIDAE) P. Yang,15 C. Zhou,1 G. Liang,2 Robert V. Dowell,3 and James R. Carey4 6 Research Institute of Entomology, Zhongshan University, Guangzhou, People’s Republic of China 2Guangzhou Animal and Quarantine Service, People’s Republic of China California Department of Food and Agriculture, Sacramento, California 95814 4University of California, Davis, California 95616 Abstract. — We examined preadult and adult survival, development and fecundity of Bactrocera cucurbitae (Coquillett) from China at six constant temperatures between 19° and 36° C. Devel¬ opment of immature stages and ovaries was inversely related to temperature. Preadult mortality was greatest at 36° C. Average female longevity was inversely related to temperature but male longevity was not. The intrinsic rate of increase was greatest at 25° C. No eggs or larvae survived exposure to constant temperatures of 2° to 3° C for longer than seven days. Key Words.— Insecta, Bactrocera cucurbitae, commodity treatment, demographic parameters Bactrocera cucurbitae (Coquillett) (Diptera: Tephritidae) is a cucurbit pest found in Kenya, Mauritius, Sri Lanka, India, China, Malaya, Indonesia, and the Phil¬ ippines (White & Elson-Harris 1992). In the last century, it has expanded its range to a number of Pacific islands including Hawaii. It has been detected in California on two occasions. Each of these California infestations, along with those on several Pacific islands, have been eradicated (Dowell & Gill 1989; Shiga 1989; RVD, unpublished data). Bactrocera cucurbitae is one of five species of economically important fruit flies found in mainland China, and one of two species attacking cucurbits; the other is Bactrocera tau (Walker). Recent efforts by the Chinese to expand agricultural exports have increased the importance of developing information about the bi¬ onomics of B. cucurbitae in China, because the fly is quarantined by a number of countries including the United States (Yang et al. in press). Temperature is an important environmental factor influencing fruit fly popu¬ lation dynamics. Data on the effects of temperature on fruit fly development and survival are critical: to developing models that predict fly phenology, to estimate the age structure of field populations, to the timing of control activities, and to developing quarantine compliance protocols (Smith 1977, Carey 1993). We stud¬ ied the effect of temperature on the development, survival and reproduction of the immature and adult stages of a Chinese strain of B. cucurbitae. We also evaluated the survival of B. cucurbitae eggs and larvae when they were subjected to cold treatments similar to those used to meet USD A quarantine regulations for Ceratitis capitata (Wiedemann) (Fiskaali 1991). 5 Current address: 2729 Kapiolani Blvd. #203, Honolulu, Hawaii 96823. 6 To whom correspondence should be sent. 270 THE PAN-PACIFIC ENTOMOLOGIST Vol. 70(4) Table 1. Average developmental time and survival of immature B. cucurbitae reared at six constant temperatures. Temperature (° C) Stage 19= 22° 25° 28° 30° 36° Developmental timeab Egg 3.00 2.00 2.00 1.50 1.00 1.00 (1.1) (0.5) (0.7) (0.4) (0.1) (0.1) Larva 7.31 6.42 5.56 3.41 3.26 4.42 (1.4) (1.7) (2.5) (0.9) (0.9) (1.5) Pupa 14.80 14.30 10.20 9.00 7.90 6.50 (0.5) (0.5) (1.5) (0.6) (0.2) (0.8) Percent mortality Egg 5 4 4 5 5 12 Larva 15 16 19 9 14 7 Pupa 3 1 5 8 9 22 Total 23 21 28 22 28 41 a Days, mean ± (SD). b Three replicates, n = 30 eggs and 50 larvae or pupae per replicate. Materials and Methods Effect of Temperature on Growth and Survival. —Bactrocera cucurbitae were collected from the Parcel Islands, in the South China Sea, and maintained in a colony for several generations at the Guangzhou Animal and Plant Quarantine Service prior to use. Tests were conducted at 12:12 L:D cycle and 80% to 90% RH. Immature stages and adults were held at test temperatures (± 0.5° C) of 19°, 22°, 25°, 28°, 30°, or 36° C. All trials were replicated three times. Duration and survival of immature stages were determined as follows. Thirty newly-laid eggs were placed on a piece of wet black cloth in a petri dish and checked for hatch every eight hours. Fifty neonate larvae were placed on pieces Table 2. Adult longevity and reproduction of B. cucurbitae held at six constant temperatures. Temperature (° C) 19° 22° 25° 28° 30° 36° Longevitya'bc Female 103.0 100.8 97.8 72.2 69.0 31.7 (45.7) (62.1) (45.3) (51.9) (49.5) (21.5) Male 95.9 107.8 111.4 80.9 71.1 29.7 (50.8) (66.2) 50.8) (51.5) (48.9) (16.0) Reproduction Preoviposition period 33.0 19.0 16.0 12.0 11.0 9.0 Gross fecunditybd 317.9 644.5 509.8 452.0 468.2 434.7 Net fecunditybd 171.8 317.6 249.7 201.9 191.2 86.2 Eggs/day/female 1.7 3.2 2.6 2.9 2.8 2.7 a Average number of days. b Three replicates with 50 pairs of flies per replicate. 0 Mean ± (SD). d Eggs per female. 1994 YANG ET AL.: TEMPERATURE EFFECTS ON BACTROCERA 271 Y T I D N U C E F Figure 1. Daily gross egg production for B. cucurbitae female reared at six constant temperatures (19°, 22°, 25°, 28°, 30°, 36° C), given at left top of each graph. of cucumber (Cucumis sativus L.) held in glass bottles (10 cm dia x 10 cm high) containing a layer of moist sand. The larvae were checked daily and food was added as needed. The sand was sifted daily to recover pupae. Fifty newly formed pupae were held in petri dishes and checked daily for emergence. Adult life history traits were determined by placing 50 pairs of newly emerged adults in cages 25 cm on a side. Water was provided and fresh orange juice was used as adult food. A small piece of cucumber was placed daily in each cage for egg collection. Mortality was recorded daily until the last female died. Life history data were analyzed using the methods of Carey (1993). Effect of Cold Temperatures on Egg and Larval Survival.— The survival of B. cucurbitae larvae held in four host plants at low temperatures was determined by placing newly molted second instar larvae in bottles (10 cm dia x 10 cm high) with cut pieces of each plant (Table 4). The bottles were then held at 2° C for one to five days to simulate quarantine treatment conditions. Each day one-fifth of the bottles were removed and the number of living and dead larvae was deter¬ mined. All subsequent tests were run using cucumber as larvae feeding on it took the longest time to reach 100% mortality. Another series of tests was run as above holding third instars at 2° C, and eggs, first and third instars at 3° C for eight to ten days. Results Preadult Development and Survival.— Developmental times for B. cucurbitae eggs and larvae were inversely related to temperature from 19° to 30° C (eggs: r 272 THE PAN-PACIFIC ENTOMOLOGIST Vol. 70(4) Table 3. Demographic parameters for B. cucurbitae reared at six constant temperatures. Temperature (° C) Parameter 19° 22° 25° 28° 30° 36° Intrinsic rate of increasea 0.044 0.065 0.069 0.064 0.066 0.053 Mean generation timeb 95.7 65.2 65.2 65.4 62.8 51.8 Doubling timeb 16.9 10.7 10.1 10.9 4.7 5.7 a Per day. b Days. = -0.92, F = 20.49, P = 0.01, n = 5; larvae: r = -0.98, F = 71.23, P = 0.004, n = 4). The duration of the egg stage did not change at 36° C, but that of the larval stage increased. The duration of the pupal stage and total preadult devel¬ opment time were inversely related to temperature at all test temperatures (pupae: r — -0.95, F = 38.85, P = 0.003, n = 5; preadult: r = —0.95, F = 35, P = 0.004, n = 5) (Table 1). Egg mortality was relatively uniform between 19° and 30° C, but it increased Table 4. Mortality of second instar B. cucurbitae larvae reared at 2° C in four hosts. Host/days exposed Number alive Number dead Total Percent mortality Sponge Gourd3 1 13 40 53 75.4 2 3 8 11 72.7 3 1 15 16 93.8 4 0 21 21 100.0 5 0 15 15 100.0 Balsam Pearb 1 9 39 48 81.3 2 7 35 42 83.3 3 1 88 89 98.9 4 0 54 54 100.0 5 0 26 26 100.0 Cucumberc 1 14 7 21 33.3 2 8 58 66 87.9 3 4 80 84 95.2 4 1 19 20 95.0 5 0 15 15 100.0 Wax Gourdd 1 49 4 53 7.6 2 5 18 23 78.3 3 0 27 27 100.0 4 0 43 43 100.0 5 0 21 21 100.0 a Luffa aegyptiaca Miller. b Momordica charantia L. c Cucumis sativus L. d Benincasa hisida (Thunberg). 1994 YANG ET AL.: TEMPERATURE EFFECTS ON BACTROCERA 273 Table 5. Mortality of immature stages of B. cucurbitae in cucumber held at cold temperatures. Percent mortality Days Eggs* 1st instar* 2nd instar* 3rd instarb 1 21.7 14.0 12.4 13.3 2 14.6 43.8 11.1 64.7 3 40.2 41.0 100.0 100.0 4 81.8 35.2 40.3 100.0 5 94.7 79.1 94.4 100.0 6 97.5 90.1 96.9 86.7 7 100.0 100.0 100.0 100.0 8 100.0 100.0 100.0 100.0 9 100.0 10 100.0 a Test run at 2° C, n = 15 to 20 larvae per temperature per day. b Test run at 3° C, n = 15 to 20 larvae per temperature per day. 2.4 fold at 36° C. Larval mortality was lowest at 28° and 36° C and varied little among the other test temperatures. Pupal mortality increased 4.4 fold between 25° and 36° C. Preadult mortality was greatest at 36° C (Table 1). Adult Survival and Reproduction.— Survival of B. cucurbitae females was in¬ versely related to temperature (r = —0.96, F = 48.41, P = 0.002, n = 5), but that of the males increased with temperature between 19° and 25° C and decreased with increasing temperature thereafter. The preovipositional period was inversely related to temperature (r = —0.87. F = 12.65, P = 0.02, n = 5). Gross and net fecundity, and eggs per female per day were greatest at 22° C (Table 2) and were not related to temperature (r — 0.02, r = 0.64, r = 0.40 respectively, P > 0.05). Daily egg production fluctuated widely, with no clear trend regardless of rearing temperature. Females continued to lay eggs for at least 140 days at temperatures at or below of 30° C and for up to 180 days at 22° to 25° C (Fig. 1). The intrinsic rate of population increase was greatest at 25° C, but there was little difference among the values between 22° and 30° C. Mean generation time was shortest at 36° C and there was little difference among the values between 22° and 30° C. Population doubling time was shortest at 30° C, with nearly identical times between 22° and 28° C (Table 3). Effects of Cold Temperatures on Survival.— No second instar B. cucurbitae survived beyond four days when held at a constant 2° C in any of the test plants (Table 4). No third instars survived beyond six days when held at a constant 2° C and no eggs, first or second instars survived beyond six days when held at 3° C (Table 5). Increasing the temperature 1° C, from 2° to 3° C, increased the time needed to kill all second instars from four to six days (Tables 4 and 5). Discussion Our preadult developmental times and survivorships of B. cucurbitae fall within the range of those from previous studies of wild flies in culture six or fewer generations (Miyatake 1993). Egg and pupal development are mainly dependent upon temperature and larval development upon temperature and host (Tables 1 and 6). 274 THE PAN-PACIFIC ENTOMOLOGIST Vol. 70(4) Table 6. Stage specific duration and survival of wild B. cucurbitae from previous studies. Stage" • c Durationb Host Reference Eggs 20 2.0 (73) Bhatia & Mahto 1970 25 1.1 (77) Bhatia & Mahto 1970 25 1.0 (74) Carey et al. 1985 Larvae 20 6.7 (85) pumpkin Bhatia & Mahto 1970 25 3.7 (85) pumpkin Bhatia & Mahto 1970 27.5 3.4 (83) pumpkin Bhatia & Mahto 1970 25 4.1 (88) cucumber Carey et al. 1985 25 7.4 (38) eggplant Carey et al. 1985 24 9.8 (90) papaya Vargas & Carey 1990 25 9.0 (na) media Miyatake 1993 Pupae 20 15.1 (92) pumpkin Bhatia & Mahto 1970 25 7.8 (91) pumpkin Bhatia & Mahto 1970 28 6.8 (93) pumpkin Bhatia & Mahto 1970 25 13.0 (89) cucumber Carey et al. 1985 24 9.8 (61) papaya Vargas & Carey 1990 25 11.0 (na) media Miyatake 1993 Preoviposition 25 16.0 cucumber Carey et al. 1985 23.8 14.8 tomato Keck 1951 26.7 13.5 tomato Keck 1951 25 14.0 unknown Back Pemberton 1918 a Considered wild if in colony six or fewer generations (Miyatake 1993), na = not available. b Percent survival in parentheses. The adult reproductive parameters, however, differ considerably among the studies. The gross fecundity of wild B. cucurbitae from China is approximately half that of wild B. cucurbitae from Hawaii. Wild Chinese B. cucurbitae lay one- half to one-third the eggs per day and have population doubling times 1.5 times greater than those from Hawaii. The greater variation in adult responses suggests that this is the stage in which local environmental factors have their greatest influence and, thus, the stage in which the fly adapts to them (Tables 2, 3 and 7). In culture, the response time to selection for a characteristic of adult flies was faster than that for larvae (Miyatake 1993). Although not definitive, our results suggest that cold treatments may be effective as a disinfestation treatment for produce harboring B. cucurbitae eggs and larvae. Table 7. Adult demographic parameters for wild B. cucurbitae from previous studies. Parameter Value" Reference Gross fecundity 1293 eggs Carey et al. 1985 Net fecundity 709 eggs Carey et al. 1985 Doubling time 6.9 days Carey et al. 1985 12.0 days Vargas & Carey 1990 Eggs/female/day 7.2 eggs Carey et al. 1985 4.7 eggs (21.1° C) Keck 1951 8.9 eggs (23.9° C) Keck 1951 8.2 eggs (29.4° C) Keck 1951 a Considered wild if in colony for six or fewer generations (Miyatake 1993). 1994 YANG ET AL.: TEMPERATURE EFFECTS ON BACTROCERA 275 Further, large scale tests will be required before cold treatments of B. cucurbitae hosts can be certified for use as a quarantine treatment from countries having the pest. Literature Cited Back, E. A. & C. E. Pemberton. 1918. The melon fly. USDA Bull., 643. Bhatia, S. K. & Y. Mahto. 1970. Influence of temperature on the speed of development of melon- fly, Dacus cucurbitae Coquillett (Diptera: Tephritidae). Indian J. Agric. Sci., 40: 821-828. Carey, J. R. 1993. Applied demography for biologists with special emphasis on insects. Oxford Univ. Press., New York. Carey, J. R., E. J. Harris & D. O. Mclnnis. 1985. Demography of a native strain of the melon fly, Dacus cucurbitae, from Hawaii. Ent. Exp. Appl., 38: 195-199. Dowell, R. Y. & R. Gill. 1989. Exotic invertebrates and their effects on California. Pan-Pacif. Entomol., 65: 132-145. Fiskaali, D. A. 1991. Commodity treatment manual, Vol. I. Treatments. Calif. Dept. Food & Agric., Sacramento, California. Keck, C. B. 1951. Effect of temperature on development and activity of the melon fly. J. Econ. Entomol., 44: 1001-1002. Miyatake, T. 1993. Difference in the larval and pupal periods between mass-reared and wild strains of the melon fly, Bactrocera cucurbitae (Coquillett) (Diptera: Tephritidae). Appl. Entomol. Zool., 28: 577-581. Nakamori, H. 1987. Variation of reproductive characters in wild and mass-reared melon flies, Dacus cucurbitae Coquillett (Diptera: Tephritidae). Jpn. J. Appl. Entomol. Zool., 31: 309-314. Shiga, M. 1989. Current programme in Japan. Chap. 9.5.2. In Robinson, A. S„ & G. Hooper (eds.). Fruit flies, their biology, natural enemies and control. Elsevier, New York. Smith, E. S. C. 1977. Studies on the biology and commodity control of the banana fruit fly Dacus musae (Tryon), in Papau New Guinea. Papau New Guinea Agric. J., 28: 47-56. Vargas, R. I. & J. R. Carey. 1990. Comparative survival and demographic statistics for wild oriental fruit fly, Mediterranean fruit fly, and melon fly (Diptera: Tephritidae) on papaya. J. Econ. Entomol., 83: 1344-1349. White, I. M. & M. M. Elson-Harris. 1992. Fruit flies of economic significance: their identification and bionomics. C.A.B. Int., London. Yang, P., J. R. Carey & R. V. Dowel. 1994. Tephritid fruit flies in China: historical perspective and current status. Pan-Pacif. Entomol., 70: 159-167.