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1Department of Plant Protection, Faculty of Agriculture, Bu-Ali sina University, Hamedan, Iran. 2Seed and Plant Certification and Registration Research Institute, ...
Effect of temperature on development and fecundity of the brown mite, Bryobia rubrioculus Scheuten (Acari: Tetranychidae) 1 1 2 3 N. Honarparvar *, M. Khanjani , S.H.R. Forghani & A.A. Talebi 1

Department of Plant Protection, Faculty of Agriculture, Bu-Ali sina University, Hamedan, Iran Seed and Plant Certification and Registration Research Institute, Karaj, Iran 3 Department of Entomology, Faculty of Agriculture, Tarbiat Modarres University, Tehran, Iran 2

The brown mite, Bryobia rubrioculus Scheuten thrives on sweet cherry, sour cherry and plum orchards of Hamedan in the western region of Iran. Development and fecundity of this mite was studied on sweet cherry at nine constant temperatures (15, 17.5, 20, 22.5, 25, 27.5, 30, 32.5 and 35 °C), 60 ± 5 % relative humidity and a photoperiod of 16:8 h (light:dark). The developmental time from egg to adult ranged from 43.4 ± 0.63 days at 15 °C to 14.5 ± 0.37 days at 32.5 °C. The average longevity of adult females was 14.0 ± 0.88 days at 15 °C to 6.5 ± 0.67 days at 32.5 °C. The highest and lowest mean number of eggs laid by a female during life time was 13.8 ± 1.07 and 4.4 ± 0.88 at 20 and 32.5 °C, respectively. These results may be used to predict B. rubrioculus development and population fluctuations. Key words: Bryobia rubrioculus, developmental time, Iran, photoperiod, biology.

INTRODUCTION The brown mite, Bryobia rubrioculus Scheuten (Acari: Tetranychidae) infesting fruit trees has long been confused with B. pretiosa Koch as a grass species. Bryobia rubrioculus is also known as Bryobia arborea Morgan and Anderson. This thelytokous mite is widespread in orchards in Asia and Japan, Europe, north America (Ehara 1959; Herbert 1962, 1965; Helle & Pijnacker 1985; Incekulak & Ecevit 2002) in northern and southern Africa; in Tunisia (Kreiter et al. 2002), Mozambique (Rodrigues 1968), South Africa (Baker & Pritchard 1960), Zimbabwe (Goldsmid 1962), in Yemen (Smiley & Baker 1995; Meyer 1996), and in apple orchards in Turkey (Kasap 2008). The brown mite is known to lay two types of eggs, summer and winter eggs, and overwinters as winter eggs, particularly on young branches of fruit trees (Kremer 1956; Morgan & Anderson 1957; Herbert 1962; Meyer 1974). Its feeding causes whitish-grey spots on the upper surface of young leaves (Van de Vrie et al. 1972; Jeppson et al. 1975; Duzgunes 1977; Osakabe et al. 2000). This mite species was a well-known pest in most fruit orchards in the Pacific Northwest, but has been uncommon in the past few decades (Beers 2007). Currently, the brown mite infests sour cherry, Prunus cerasus L.; sweet cherry, Cerasus avium (L.) and plum, Prunus domestica (Borkh) trees in western regions of Iran (Khanjani *To whom correspondence should be addressed. E-mail: [email protected]

& Haddad Irani-Nejad 2009). It has been reported from the other parts of Iran on apple, Malus domestica Borkh, peach, Prunus persica (L.); grape, Vitis vinifera L.; pear, Pirus communis L., sweet cherry, plum and walnut, Juglans regia L. (KhalilManesh 1972; Sepasgozarian 1976; KeshavarzeJamshidian 2004; Khanjani 2004; Eghbalian 2007). A few biological studies on B. rubrioculus have been published on other host plants (Eghbalian 2007; Kasap 2008), but there are no studies on its development and reproduction at various temperature regimes on sweet cherry trees. Therefore, this study aimed to determine the relationship between biological parameters of B. rubrioculus and temperature, which might be useful in developing forecast models and predict its population levels and also to understand the thermal adaptation of this mite in different environmental conditions. MATERIAL AND METHODS

Mite colony The brown mites used in the experiments were originally collected from sweet cherry orchards in Hamedan region in western Iran, in late February 2008. The laboratory colony of the brown mite was reared on sweet cherry leaf discs in a growth chamber at 25 ± 1 °C, 60 ± 5 % relative humidity and a photoperiod of 16:8 h (light:dark). African Entomology 20(1): 69–75 (2012)

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Effect of temperature on the development of the mite Development time of the brown mite was studied at nine constant temperatures (15, 17.5, 20, 22.5, 25, 27.5, 30, 32.5 and 35 °C) in separate growth chambers, with 60 ± 5 % RH and a photoperiod of 16 L:8 D h. Petri-dishes (10 cm diameter) were used as arenas, with a piece of sponge soaked in water in each Petri-dish. A detached sweet cherry leaflet was placed on the sponge. A narrow strip of tissue paper was placed at the periphery of each leaflet. The soaked sponge and tissue paper kept the leaflet turgid. For each experiment, one female adult from the stock colony was transferred with the help of a fine camel hair brush (000) on to the arenas and was allowed to lay eggs for 24 hours. After this oviposition period, the adult and all the eggs except one were removed. For each temperature, 60 newly laid eggs were selected and were checked daily, under a dissecting microscope at magnifications of up to ×70 to record the developmental time. The observations were continued till the death of all individuals of the cohorts. The detached sweet cherry leaflets were replaced with fresh ones every two days during the study. Effect of temperature on fecundity The reproduction and longevity of adults were studied at nine constant temperatures (the same as above) until the last female died. The number of eggs laid by each female and the survival of adults were recorded daily (once in every 12 h), until the last female died. Data analysis The differences in developmental time, adult longevity and fecundity of the brown mite at various constant temperatures were compared using one-way analysis of variance (ANOVA). If significant differences were there, multiple comparisons were made using Tukey’s test (P < 0.05). Statistical analysis was carried out using SPSS software (SPSS 2007). The data were checked for normality prior to statistical analysis using the Anderson-Darling test (Minitab 2000). The relationship between temperature and the developmental rate was described using simple linear regression: Y = a + bx , where Y is the developmental rate, x is the temperature, a is the intercept and b is the slope of the line.

Chi-square tests were conducted to determine if there were significant differences in mortality for this mite reared at different temperatures (SAS 2002). RESULTS Developmental time The details of developmental periods of various stages of B. rubrioculus at different constant temperatures are shown in Table 1. There was an inverse relationship between the duration of development and temperatures within the range of 15 to 32.5 °C (Table 1). The brown mite successfully developed to adult at temperatures from 15 to 32.5 °C, but the eggs failed to hatch at 35 °C. Developmental time was longest at 15 °C and shortest at 32.5 °C. It varied between 20.7 ± 0.43 and 7.5 ± 0.22 days for eggs, 3.2 ± 0.17 and 1.2 ± 0.10 days for larvae, 2.5 ± 0.14 and 1.1 ± 0.08 days for protonymph, 2.9 ± 0.14 and 1.1 ± 0.08 days for deutonymph (Table 1). Eggs failed to develop at 35 °C, therefore temperatures of 35 °C and higher were not favourable for egg development. Mean pre-imaginal development time (from egg to adult) of B. rubrioculus differed significantly at various constant temperatures. The pre-imaginal developmental time required 43.4 ± 0.63 days at 15 °C, but only 14.5 ± 0.37 days at 32.5 °C (Table 1). The total mortality of the brown mite ranged from 50 % at 15 °C to 100 % at 35 °C (Table 4). Chi-square test indicated significant differences in mortality between temperatures. Adult longevity was significantly affected by various temperatures, which decreased from 14.0 ± 0.88 day sat 15 °C to 6.5 ± 0.67 days at 32.5 °C (Table 2). The total development of the mite ranged from 57.4 ± 1.24 days at 15 °C to 21.0 ± 0.57 days at 32.5 °C (Fig. 1). The linear regression equation for the developmental rate in relation to temperature is Y = 0.0025x – 0.0122 (Fig. 2). The lower developmental threshold (To) for B. rubrioculus was estimated from the linear regression equation to be 4.88 °C. The thermal constant has been estimated from the linear equation to be 400 degree-days (DD). Fecundity This study showed that the highest and lowest fecundity per female was 13.8 ± 1.07 at 20 °C and 4.4 ± 0.88 at 32.5 °C, respectively (Table 3). There was no significant difference between total fecun-

43.4 ± 0.63 a 30.5 ± 0.24 b 25.8 ± 0.22 c 22.2 ± 0.33 d 20.5 ± 0.29 de 18.1 ± 0.27 e 15.7 ± 0.55 f 14.5 ± 0.37 f 5.1 ± 0.08 a 3.8 ± 0.05 b 3.0 ± 0.05 c 2.6 ± 0.08 d 2.1 ± 0.06 e 1.1 ± 0.04 e 1.9 ± 0.10 ef 1.5 ± 0.14 f

DISCUSSION

Means followed by different letters within a column are significantly different at the 0.05 level (Tukey’s test).

4.2 ± 0.09 a 3.1 ± 0.05 b 2.5 ± 0.05 c 2.1 ± 0.07 d 1.1 ± 0.10 d 1.8 ± 0.07 d 1.2 ± 0.12 e 1.0 ± 0.00 e 2.5 ± 0.14 a 1.6 ± 0.07 b 1.4 ± 0.06 b 1.3 ± 0.08 b 1.3 ± 0.09 b 1.2 ± 0.07 b 1.2 ± 0.10 b 1.1 ± 0.08 b 4.7 ± 0.13 a 3.1 ± 0.05 b 2.8 ± 0.05 b 2.2 ± 0.06 c 2.1 ± 0.11 c 1.8 ± 0.08 c 1.2 ± 0.10 d 1.2 ± 0.12 d 3.2 ± 0.17 a 1.9 ± 0.09 b 1.5 ± 0.07 bc 1.3 ± 0.80 bc 1.3 ± 0.10 c 1.2 ± 0.06 c 1.2 ± 0.10 c 1.2 ± 0.10 c 20.7 ± 0.43 a 15.1 ± 0.12 b 12.9 ± 0.12 c 11.5 ± 0.28 d 10.6 ± 0.26 de 9.8 ± 0.21 e 7.1 ± 0.40 f 7.5 ± 0.22 f 30 29 28 20 19 14 10 9 0 15 17.5 20 22.5 25 27.5 30 32.5 35

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dity per female at temperatures of 15–27.5 °C, but significantly decreased with increasing temperature from 27.5–32.5 °C. The number of eggs laid per day was significantly greatest at 22.5 (2.3 ± 0.09), 25 (2.4 ± 0.15) and 27.5 °C (2.4 ± 0.14) from that at other temperatures (Table 3).

2.9 ± 0.14 a 1.9 ± 0.09 b 1.6 ± 0.06 bc 1.3 ± 0.11 bc 1.3 ± 0.11 c 1.2 ± 0.06 c 1.2 ± 0.10 c 1.1 ± 0.08 c

Pre-imaginal development time Deutochrysalis

Developmental stages

Protonymph Protochrysalis Larvae Eggs

n Temperature (°C)

Table 1. Developmental time (days) of Bryobia rubrioculus females at different temperatures.

Deutonymph

Teliochrysalis

Honarparvar et al.: Effect of temperature on development and fecundity of the brown mite

The results revealed the obvious effects of temperature on the development, mortality, survival and fecundity of B. rubrioculus. Hardly any study has covered the effect of temperatures on development and survival of B. rubrioculus in Iran. Incubation period at 25 °C (10.6 days) was relatively close to those reported for B. rubrioculus on two different apple varieties (8.7 days on Golden Delicious and 9.3 days on Starking Delicious) (Kasap 2008) and on sour cherry (9.7 days) (Eghbalian 2007). The mean developmental time of larvae was determined as 1.3 days at 22 °C on sour cherry (Keshavarze-Jamshidian 2004) and 3.0 and 3.7 days on Golden Delicious and Starking Delicious apple cultivars, respectively, at 25 °C (Kasap 2008), which are similar to the present findings. Significant differences between different life cycles of the B. rubrioculus including protochrysalis, protonymph, deutochrysalis, deutonymph and teliochrysalis reared at different temperatures were observed. Duration of protonymphs was reported to be 4.2 days on sour cherry at 25 °C ambient temperature (Eghbalian 2007), while it was reported to be 1.0 day at 22 °C (KeshavarzeJamshidian 2004), the latter is similar to the present results at 22.5 °C. The deutonymph life cycle was reported to be 1.1 days on apple variety Golden Delicious at 18.5 °C (Herbert 1962) and 4.6 days on sour cherry at 25 °C (Eghbalian 2007). The mean pre-imaginal development time (from egg to adult emergence) of B. rubrioculus ranged from 43.4 days (longest) at 15 °C to 14.5 days (shortest) at 32.5 °C. Kasap (2008) recorded the duration of the pre-imaginal development time (egg to adult) of B. rubrioculus as 18.5 and 20.5 days on Golden Delicious and Starking Delicious apple varieties at 25 °C, respectively, which was fairly close to that observed in this study at the same temperature (20.5 days). The lower developmental threshold for total immature stages was 4.9 °C, which was lower than that of 9.7 °C for Amphitetranychus viennensis on apple cultivars (Kasap 2003). A total of 400 DD

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Table 2. Female longevity of Bryobia rubrioculus at different temperatures. Temperature (°C) 15 17.5 20 22.5 25 27.5 30 32.5 35

n

Preoviposition period

19 20 22 16 14 11 7 5 4

3.6 ± 0.22 a 2.6 ± 0.11 bc 2.3 ± 0.10 bc 1.7 ± 0.10 c 1.6 ± 0.12 c 1.6 ± 0.12 c 1.9 ± 0.25 c 2.4 ± 0.21 bc 3.3 ± 0.49 ab

Oviposition period 8.2 ± 0.75 a 7.8 ± 0.48 a 6.3 ± 0.38 ab 5.3 ± 0.57 abc 5.1 ± 0.73 abc 4.8 ± 0.42 abc 3.0 ± 0.69 bc 3.0 ± 0.59 bc 1.9 ± 0.44 c

Postoviposition period

Adult longevity

2.2 ± 0.25 a 1.8 ± 0.24 a 1.6 ± 0.15 a 1.3 ± 0.21 a 1.3 ± 0.19 a 0.1 ± 0.21 a 1.7 ± 0.43 a 1.1 ± 0.35 a 1.8 ± 0.45 a

14.0 ± 0.88 a 12.2 ± 0.47 ab 10.2 ± 0.34 abc 8.3 ± 0.59 bc 8.0 ± 0.82 c 6.5 ± 0.52 c 6.6 ± 0.71 c 6.5 ± 0.67 c 7.0 ± 0.70 c

Means followed by different letters within a column are significantly different at the 0.05 level (Tukey’s test).

Table 3. Total fecundity and daily fecundity of the brown mite, Bryobia rubrioculus at different temperatures. Temperature (°C) 15 17.5 20 22.5 25 27.5 30 32.5

n

Daily fecundity

Total fecundity

19 20 22 16 14 11 7 5

1.3 ± 0.07 c 1.7 ± 0.06 bc 1.9 ± 0.06 ab 2.3 ± 0.09 a 2.4 ± 0.15 a 2.4 ± 0.14 a 1.4 ± 0.21 bc 1.5 ± 0.13 bc

11.6 ± 1.42 abc 13.7 ± 1.11 a 13.8 ± 1.07 a 13.3 ± 1.59 a 13.0 ± 2.08 a 12.9 ± 1.56 ab 4.5 ± 1.56 bc 4.4 ± 0.88 c

Means followed by different letters within a column are significantly different at the 0.05 level (Tukey’s test).

(degree-days) above the threshold temperature was required to complete development from egg to adult. The higher developmental threshold and lower degree-days (6.4 °C and 305 DD for females and 8.9 °C and 260 DD for males, respectively) were reported for Eutetranychus orientalis on lebbek leaf by Imani & Shishehbor (2009). In this study developmental rate decreased with the increase in temperature, as reported by Baradaran et al. (2001) for Tetranychus urticae on ornamental plants. Adult longevity of B. rubrioculus at 15 °C, 14.0 and at 17.5 °C was 12.1 days. This is in line the report on apple leaf (13.3 days at 18.3 °C) (Herbert 1962). The adult longevity of this mite species was reported

14.2 and 18.8 days on Golden Delicious and Starking Delicious apple varieties, respectively (Kasap 2008). These findings showed that host plants and varieties could influence adult longevity. Total development was reported as 45.3 at 25 °C and 35.2 days at 22 °C for B. rubrioculus on sour cherry and 31.0 days at 18.5 °C on apple (Eghbalian 2007; Keshavarz-Jamshidian 2004). The preoviposition, oviposition and postoviposition periods are shown in Table 2. Similarly, Kasap (2008) reported these periods for B. rubrioculus to be, respectively, 2.0, 9.0 and 3.2 days for Golden Delicious, and 1.8, 13.6 and 3.3 days for Starking apple varieties at 25 °C. Also, it was reported that the above-mentioned periods of this

Table 4. Total mortality of the brown mite, Bryobia rubrioculus at different temperatures. Temperature (°C) Total mortality (%)

15 50

17.5 51.67

20 53.33

22.5 66.67

25 68.33

27.5 76.67

30 83.33

32.5 85

35 100

Honarparvar et al.: Effect of temperature on development and fecundity of the brown mite

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Fig. 1. Total development of the brown mite, Bryobia rubrioculus at different temperatures. Means followed by different letters are significantly different at P = 0.05.

Fig. 2. Developmental rate of Bryobia rubrioculus versus temperatures.

mite are 3.2, 13.2 and 0.8 days on sour cherry at 22 °C (Keshavarz-Jamshidian 2004). By contrast, cycle periods found in the present research were shorter than the previous research results reported by Kasap (2008) and Keshavarz-Jamshidian (2004). The differences in the life cycles are probably due to the experimental conditions. High temperatures (30 and 32.5 °C) had a harmful effect on fecundity of B. rubrioculus compared to other temperatures (Table 3). The number of eggs laid per day was greatest between 22.5 and 27.5 °C. Kasap (2008) reported a total fecundity per female of 14.2 and 20.1 eggs and also daily fecundity of 1.3 and 1.2 eggs on Golden and Starking apple, respectively. The present findings showed that the daily fecundity at 25 °C (2.4) was higher than that observed by Kasap (2008) on apple at the same temperature of 25 °C. Previous studies showed that developmental

time of B. rubrioculus depends on some host plant characteristics and temperatures (Kasap 2008; Eghbalian 2007; Keshavarz-Jamshidian 2004; Herbert 1962, 1965). Yano et al. (1998) indicated that leaf characteristics of host plants play a vital role in their defence against Tetranychus urticae. Crooker (1985) reported the chemical composition of the leaf might influence the development of the immature stages of spider mites, especially the host plant’s nitrogen content. Also, Van de Vrie et al. (1972) showed that the different chemical contents of the leaf tissue extracted from plant species or varieties affect the reproductive potential, mortality and development rate. In addition, it was stated that population density of spider mites and their feeding times depend on the length of their stylets and characteristics of the host plant leaves (Tomczyk & Kropczynska 1986). In conclusion, the present study has shown that

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20 °C is the most suitable temperature for B. rubrioculus development on sweet cherry. The results obtained for constant temperatures will provide direction for future research on evaluating the performance of B. rubrioculus and the efficiency of its natural enemies in sweet cherry orchards under variable environmental conditions. Results of these studies can be used as bases for methods to conduct field experiments. Furthermore, the underly-

ing physiological mechanisms responsible for variation in B. rubrioculus fecundities and survival need to be identified under different temperature regimens in future studies. ACKNOWLEDGEMENTS We would like to thank J. Shaterian, Seed and Plant Certification and Registration Research Institute (SPCRI), Karaj, Iran.

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