Appl. Entomol. Zool. 38 (1): 97–101 (2003)

Effect of temperature on development and reproduction of the russet , lycopersici (Massee) (: )

Mohd. Mainul HAQUE† and Akira KAWA I* National Institute of Vegetables and Tea Science, National Agricultural Research Organization; Ano, Mie 514–2392, Japan (Received 12 July 2002; Accepted 18 November 2002)

Abstract The effect of constant temperature on the development, reproduction and population growth of Aculops lycopersici reared on a tomato leaflet was investigated. Survival rates from egg to adult were more than 69% at temperatures be- tween 15°C and 27.5°C, but only 53% at 30°C. Developmental rates increased linearly as rearing temperature in- creased from 15°C to 27.5°C. A total of 81.2 degree-days above a developmental zero of 10.5°C were required to complete development from egg to adult emergence. Adult longevity decreased with increasing temperature. Fecun- dity was highest at 25°C with 51.7 eggs per female. The highest intrinsic rate of natural increase was observed at 25°C as 0.253 per day.

Key words: Aculops lycopersici; developmental zero; thermal constant; population growth; tomato

INTRODUCTION MATERIALS AND METHODS The tomato russet mite, Aculops lycopersici . A stock culture of A. lycopersici was col- Massee is an important pest of tomato, Lycopersi- lected from tomato plants in Mie Pref. in Novem- con esculentum Mill. It was first described in Aus- ber 1999. Mites were then cultured on potted tralia (Massee, 1937) but is now cosmopolitan tomato plants at 25Ϯ5°C in the laboratory of the (Perring and Farrar, 1986). In Japan, it was first National Institute of Vegetables and Tea Science. found in 1986 (Nemoto, 1991) and has since be- Development. In order to obtain an egg, a fe- come a serious pest (Nemoto, 2000). It increases male adult was put on the upper surface of a small rapidly on tomato and the infestation causes great tomato leaflet (cultivar ‘House Momotaro’). The injury to the plant (Haque and Kawai, 2002). A leaflet was then placed on filter paper in a plastic few life history studies on A. lycopersici have been container (60 mm dia.ϫ30 mm height) covered published (Rice and Strong, 1962; Abou-Awad, with a plastic lid having a 7 mm dia. hole. A small 1979). However, Rice and Strong (1962) calculated piece of cotton was placed at the base of the petiole the developmental period using the data of only of the leaflet. The cotton and filter paper were con- one to eight individuals in each category and stantly kept wet by soaking with water. The con- Abou-Awad (1979) showed only the data at 25°C tainers were then kept in an incubator at the experi- on leaves of Solanum nigrum. The effect of tem- mental temperature under long-day conditions perature on development and reproduction remains (L16:D8). After 24 h, a female adult was removed. unknown. Only one egg was left for rearing on each leaflet, In this study, the effect of temperature on the de- all others were removed. The stages were checked velopment and reproduction of A. lycopersici was every day to adult emergence. When leaflets lost investigated and the basic thermal requirements for their green color, A. lycopersici transferred to new development were determined. leaflets with a fine cotton single haired brush. This experiment was conducted at 15, 17.5, 20, 22.5, 25, 27.5 and 30°C. The number of eggs exposed to each temperature was 30–48. The relative humidity

* To whom correspondence should be addressed at: E-mail: [email protected] † Present address: Department of Zoology, Rajshahi University; Rajshahi 6205, Bangladesh

97 98 M. M. HAQUE and A. KAWAI

Fig. 1. Rearing unit for the experiments on fecundity and longevity of adult A. lycopersici. was not maintained exactly but fluctuated from 40 number of eggs laid was counted. The eggs were to 60%. removed and the adult mites were transferred to Reproduction. A. lycopersici adults were reared new rearing units. Since there is a possibility that individually in microcells. The rearing unit is some eggs were overlooked, the rearing units with- shown in Fig. 1. The microcells were made by out adults were maintained for four days at 27.5°C. drilling a hole of 10 mm dia. in a plastic plate If nymphs were found, they were considered as (40 mmϫ70 mmϫ5 mm). Each plate had four mi- eggs of the previous two days. The freshness of the crocells. Each rearing unit was prepared by placing leaflets was maintained by wetting the paper towel. a fresh green tomato leaflet on a 5 mm thick layer This experiment was conducted at 15, 20, 25 and of paper towel, which was supported beneath by a 30°C. 5 mm thick plastic plate. The top plastic plate con- taining the cells was placed on the leaflet and the RESULTS AND DISCUSSION whole unit held together with two rubber bands. Relative humidity was maintained constant by Development means of salt solutions as described by O’Brien The mean developmental periods and survival (1948). The salt solution was put in a tight box rate at each of seven temperatures are shown in (24 cmϫ17 cmϫ8 cm) and the plastic stage was Table 1. Egg duration decreased with an increase in placed inside the box. The rearing units were temperature up to 30°C. Egg duration at 15°C was placed on the plastic stage. The humidity chambers about four times as long as that at 30°C. Total with the rearing units were placed in incubators to nymphal duration gradually decreased with an in- maintain the desired temperatures. Mixtures of crease in temperature up to 27.5°C but at 30°C it

NaCl, NaNO3 and KNO3 (1:1:1); CaCl2·6H2O; again increased. At 15°C the nymphal stage was CaCl2·6H2O; MgCl2·6H2O were used to make sat- about four times as long as at 27.5°C. The duration urated solutions at 15, 20, 25 and 30°C, respec- from egg to adult at 15°C was 17.1 days, about tively. The humidity fluctuated from 30 to 33% in four times as long as at 30°C. Survival rate of the all cases. eggs was high between 15 and 30°C and that of The experiments on fecundity and longevity nymphs was high at temperatures lower than were started by placing four second instar nymphs 27.5°C, but decreased at 30°C. of A. lycopersici in each cell. The next day, only There was a significant linear relationship be- one adult was left in each cell for rearing and all tween temperature and developmental rates of eggs other adults and nymphs were removed. The rear- (between 15 and 30°C), nymphs (between 15 and ing units were checked every two days and the 27.5°C) and egg to adult (between 15 and 27.5°C). Development and Reproduction of Aculops lycopersici 99

Table 1. Developmental duration and survival rate of A. lycopersici at different temperatures

Duration in daysa Survival (%) Temp. (°C) Egg Nymph Egg to adult Egg Nymph Egg to adult

15 8.26Ϯ0.18 (38) 8.78Ϯ0.31 (27) 17.07Ϯ0.18 (27) 93.8 82.1 77.0 17.5 5.85Ϯ0.14 (39) 6.05Ϯ0.14 (38) 11.76Ϯ0.19 (38) 97.9 95.8 93.8 20 4.59Ϯ0.12 (32) 4.06Ϯ0.11 (32) 8.66Ϯ0.18 (32) 96.7 72.2 69.8 22.5 3.57Ϯ0.08 (47) 3.62Ϯ0.10 (45) 7.16Ϯ0.11 (45) 97.9 89.9 88.0 25 3.14Ϯ0.14 (29) 2.40Ϯ0.10 (25) 5.48Ϯ0.14 (25) 94.1 88.5 83.2 27.5 2.57Ϯ0.07 (47) 2.21Ϯ0.07 (47) 4.79Ϯ0.09 (47) 97.5 92.7 90.3 30 2.23Ϯ0.09 (30) 2.36Ϯ0.09 (28) 4.57Ϯ0.09 (28) 95.0 55.7 52.9

a x¯ϮS.E. Numbers in parenthesis indicate sample size.

Table 2. Regression equation between the velocity of development and temperature, developmental zero and thermal constant for A. lycopersici on tomato leaves

Stage Regression equation r2 Developmental zero (°C) Thermal constant (K) (degree-days)

Egg Yϭ0.0217XϪ0.2097 0.996 9.3 47.8 Nymph Yϭ0.0283XϪ0.3231 0.971 11.4 35.3 Egg to adult Yϭ0.0122XϪ0.1276 0.995 10.5 81.2

Table 3. Fecundity and longevity of ovipositing female A. lycopersici on tomato leaves at constant temperatures

Temp. (°C) Longevity of ovipositing femalea % of ovipositing femalesb Fecundity (Total egg/ovipositing female)

15 32.2Ϯ0.6 (26) 77.1 21.9Ϯ4.1 20 29.7Ϯ0.7 (31) 75.6 31.9Ϯ4.4 25 25.7Ϯ0.8 (27) 69.2 51.7Ϯ9.8 30 17.3Ϯ0.6 (23) 74.2 42.7Ϯ6.7

a x¯ϮS.E. Numbers in parenthesis of the longevity column show sample size. b No. of ovipositing females/No. of mites.

The developmental zero and the thermal constants peratures (Aceria mississippiensis; Chandrapatya are shown in Table 2. The developmental zero for and Baker, 1986; Phyllocoptruta oleivora, Allen et egg, nymph and egg to adult were 9.3, 11.4 and al., 1995; Eriophyes chibaensis, Kadono, 1995) 10.5°C, respectively, with thermal constants of have also been observed in other eriophyid mites. 47.8, 35.3 and 81.2 degree-days. Rice and Strong (1962) showed that high humid- Reproduction ity retarded development of A. lycopersici at high The longevity and fecundity of ovipositing fe- temperatures and 30–60% humidity was suitable male A. lycopersici are shown in Table 3 and sur- for development, because the humidity fluctuated vival and oviposition curves in Fig. 2. Since it is between 40 and 60% during the experiment. The impossible to distinguish females and males mor- results indicated that A. lycopersici develops suc- phologically, the rate of ovipositing females (No. cessfully over a temperature range of 15–27.5°C. of ovipositing females/No. of total adults tested) However, the survival rate of nymphs at 30°C was was calculated and shown to be between 69 and low and the developmental speed of nymphs was 78% regardless of temperature. Longevity of slowed at 30°C. A low survival rate at high temper- ovipositing females decreased with increasing tem- atures (Phyllocoptruta oleivora; Li et al., 1989) perature. Longevity at 15°C was 32.2 days, about and an elongation of the larval stage at high tem- 1.9 times as long as at 30°C. Most individuals 100 M. M. HAQUE and A. KAWAI continued oviposition until the day before death at est number of eggs per day was observed to be all temperatures. Egg laying was greatest from the 3.52 at 30°C and decreased with a decrease in tem- fourth to sixth day at 30°C, from the fourth to 16th perature. The greatest fecundity for ovipositing fe- day at 25°C, from the fourth to 22nd day at 20°C males was 51.7 eggs at 25°C. and from the fourth to 18th day at 15°C. The high- Parameters of population growth of A. lycoper- sici at four constant temperatures are shown in

Table 4. The intrinsic rate of natural increase (rm) increased with temperature to a peak of 0.286 at 25°C, however, this value at 30°C was 0.253. Net reproductive rate was largest and the generation time was shortest at 25°C. Not only temperature but also humidity affects the population growth of eriophyoid mites. The population growth rate of Phyllocoptruta oleivora decreased as the humidity dropped (Hobza and Jeppson, 1974). Since Rice and Strong (1962) showed that humidity affected the fecundity of A. lycopersici at high temperature and 30% R.H. was suitable for oviposition, the experiments on repro- duction were conducted at 30–33% R.H. for each temperature. Population growth of A. lycopersici is maximum at 25°C. The intrinsic rate of natural increase in P. oleivora peaked at 27°C as 0.114 (Allen et al., 1995) and that of Acaphylla theavagran was maxi- mum at 27°C as 0.181 (Mizuta, 2000). The intrin- sic rate of natural increase in A. lycopersici (0.286) was much higher than that of other eriophyoid mites. This rate is nearly equal to that of Tetrany- cus ulticae (0.292) or T. kanzawai (0.268) (Kondo and Takafuji, 1985), which are two of the most se- rious mite pests in greenhouses. In a greenhouse, A. lycopersici was shown to increase rapidly during six weeks after infestation in May and June (Haque and Kawai, 2002). A suitable temperature in the greenhouse as well as better food conditions and an absence of a natural enemy would have brought about a rapid population growth of A. lycopersici.

Fig. 2. Survivorship and oviposition curves of ovipositing female A. lycopersici at four constant temperatures. ––᭜––: survivorship curve, —᭡—: oviposition curve.

Table 4. Parameters of A. lycopersici population growth on tomato leaves at constant temperatures

Temp. (°C) Mean generation time (T0) Net reproductive rate (R0) Intrinsic rate of natural increase (rm)

15 20.7 17.5 0.138 20 20.2 24.4 0.158 25 12.8 38.7 0.286 30 13.0 27.1 0.253 Development and Reproduction of Aculops lycopersici 101

tern of two species of tetranychid mites. Res. Popul. REFERENCES Ecol. 27: 145–157. Abou-Awad, B. A. (1979) The tomato russet mite, Aculops Li, L. S., F. N. Huang and J. L. Chen (1989) Ecological char- lycopersici (Massee) (Acari: Eriophyidae) in Egypt. acteristics of the citrus rust mite, Phyllocoptruta oleivora Anz. Schadlingsk. Pflanzens. Umweltschutz. 52: 153–156. (Ashm.). Acta Entomol. Sinica 32: 184–191 (in Chinese Allen, J. C., Y. Yang and L. Knap (1995) Temperature effects with English summary). on the development and fecundity of the citrus rust mite Massee, A. M. (1937) An eriophyid mite injurious to tomato. (Acari: Eriophyidae). Environ. Entomol. 24: 996–1004. Bull. Entomol. Res. 28: 403. Chandrapatya, A. and G. T. Baker (1986) Biological aspects Mizuta, T. (2000) Effect of temperature on developmental of the geranium mites, Coptophylla caroliniani and Ace- period and oviposition of tea rust mite, Acaphylla theava- ria mississipiensis (Prostigmata: Eriophyidae). Exp. gran Kadono. Jpn. J. Appl. Entomol. Zool. 44: 95–99 Appl. Acarol. 2: 201–216. (in Japanese with English summary). Haque, M. M. and A. Kawai (2002) Population growth of Nemoto, H. (1991) Ecological and morphological studies on tomato russet mite, Aculops lycopersici (Acari: Eriophyi- the eriophyid and tarsonemid mites injurious to horticul- dae) and its injury effect on the growth of tomato plants. tural plants and their control. Spec. Bull. Saitama Hort. J. Acarol. Soc. Jpn. 11: 1–10. Exp. Stn. 3: 1–85 (in Japanese with English summary). Hobza, R. F. and L. R. Jeppson (1974) A temperature and Nemoto, H. (2000) Recent topics on pests; eriophyid mites. humidity study of citrus rust mite employing a constant Agric. Hort. 75: 181–187 (in Japanese). humidity air-flow technique. Environ. Entomol. 3: O’Brien, F. E. M. (1948) The control of humidity by satu- 813–822. rated salt solutions. J. Sci. Instr. 25: 73–76. Kadono, F. (1995) Taxonomic studies on eriophyid mites on Perring, T. M. and C. A. Farrar (1986) Historical perspective trees in Japan and ecological studies on the Japanese pear and current world status of the tomato russet mite (Acari: rust mite, Eriophyes chibaensis Kadono on pear trees Eriophyidae). Entomol. Am. Misc. Publ. No. 63: 1–19. (Acari: Eriophyoides). Spec. Bull. Chiba Agric. Exp. Rice, R. E. and F. E. Strong (1962) Bionomics of the tomato Stn. 30: 1–87 (in Japanese with English summary). russet mite, Vasates lycopersici (Massee). Ann. Ento- Kondo, A. and A. Takafuji (1985) Resource utilization pat- mol. Soc. Am. 55: 431–435.