Biologia 65/5: 899—902, 2010 Section Zoology DOI: 10.2478/s11756-010-0097-4

Developmental rates of the Aphis pomi (Aphidoidea: ) and its parasitoid Aphidius ervi (Hymenoptera: Aphidiidae)

Radovan Malina1,JánPraslička2 &JankaSchlarmannová2

1Department of Biology & Ecology, Faculty of Natural Sciences, Matej Bel University, Tajovského 40,SK-97401 Banská Bystrica, Slovakia; e-mail: [email protected] 2Department of Zoology and Anthropology, Faculty of Natural Sciences, Constantine the Philosopher University, Nábrežie mládeže 91,SK-9497 Nitra, Slovakia

Abstract: Developmental rates of the aphid Aphis pomi and its parasitoid Aphidius ervi were compared at four constant temperatures (15, 20, 25, 30 ◦C). Aphis pomi required 159.07 degree-days (DD) above lover developmental threshold (LDT) of 0.3 ◦C. Aphidius ervi required 229.73 DD above LDT of 5.98 ◦C. Developmental rate of A. pomi is higher than the developmental rate of A. ervi at the same conditions. Key words: aphid; parasitoid; degree day; lover developmental threshold

Introduction development in various environments, including stored products, greenhouses and orchards (Subramanyam et Aphidius ervi Haliday, 1834 (Hymenoptera: Aphidi- al. 1990; Graf et al. 1996; Kindlmann & Dixon 1999; idae) is a cosmopolitan, solitary, endophagous para- Dixon 2000). sitoid (Marsh 1977) and a major biological control The effect of temperature on the development, per- agent of several aphid species damaging economically centage of parasitism and longevity of A. ervi reared on important crops such as legumes and cereals (Powell A. pomi have been studies recently (Malina & Praslička 1982; Starý et al. 1988). The impact of a parasitoid 2008). However, developmental rates of the host A. on its host population greatly depends upon its ability pomi have not been investigated in detail. Therefore to find and parasitize hosts and to increase offspring we carried out a study with the aim to compare the numbers in response to increasing host density (Waage development rates of A. ervi and A. pomi and evaluate & Hassell 1982; Mackauer 1983). That’s why an effec- the potential of A. ervi as a biological control agent of tive parasitoid should develop very quickly. Braconid A. pomi. species of the subfamily Aphidiidae have rapid larval development and short preoviposition intervals, giving Material and methods minimum life cycles of 10 to 15 days (Danks 2006). Sev- eral authors (Sigsgaard 2000; Deng & Tsai 1998; Bueno & van Cleave 1997; Miller & Gerth 1994; Tripathi & Aphid source Padney 1994) have studied temperature-dependent du- Aphis pomi colonies used in this study were initiated by a single collection of wild from the apple trees in Ban- ration of parasitoid development. ◦ ◦ Aphis pomi ská Bystrica city (Slovakia, 48 44 N, 19 08 E) in April The green apple aphid, deGeer, 1773 2006. The colonies were maintained on fresh apple tree is a common inhabitant of apple orchards. Dense popu- shoots (replaced every two days after all aphids migrated lations may cause abnormal growth of terminal shoots, from dry to fresh shots) in a thermostat at 25 ± 1 ◦C, 60 ± reduce the percentages of non-structural carbohydrates 5% RH and a photoperiod of 16:8 (L:D) hours. After one- in shoots, roots and leaves of apple trees and reduce the month rearing period, the ensuing colonies were used for crop (Kaakeh et al. 1993). Arbab et al. (2006) modelled experiments. the development period of A. pomi at six constant tem- peratures. Parasitoid source Aphidius ervi were obtained by a single collection of aphid The knowledge of thermal constants and lower de- mummies from apple trees in Banská Bystrica city in May velopment thresholds provide essential information to 2006. Mummies were kept individually in small glass vials determine the development rate of a particular species (5 × 1.5 cm) under the same temperature and humidity of (Jarošík et al. 2002). Thermal constants conditions as the aphids. Mummies were checked daily and are frequently used to create predictive models of pest adults retrieved as they hatched.

c 2010 Institute of Zoology, Slovak Academy of Sciences 900 R. Malina et al.

Table 1. Mean development time ± SD of Aphidius ervi from egg to mummy formation (E–M), from mummy formation to adult emergence (M–A) and from oviposition to adult emergence (E–A) at four constant temperatures.

Development (days) Temp. ( ◦C) E–M M–A E–A

15 17.54 ± 0.87a 7.46 ± 0.93a 25.00 ± 1.27a 20 11.15 ± 0.93b 5.50 ± 0.90b 16.65 ± 1.24b 25 8.11 ± 0.96c 4.00 ± 0.36c 12.10 ± 1.12c 30 6.26 ± 0.77d 3.06 ± 0.75d 9.53 ± 1.15d

Explanations: Within the columns means followed by the same letters are not significantly different at P < 0.05 (Tukey multiple comparison test). ANOVA statistics were: development day (E–M) F = 3702.389, df = 3, 531, P < 0.001; development day (M–A) F = 678.5791, df = 3, 531, P < 0.001; development day (E–A) F = 3852.051, df = 3, 531, P < 0.001.

Table 2. Mean development time ± SD for four immature stages (S1–S4) and complete development of Aphis pomi at four constant temperatures.

Development (days) Temp. ( ◦C) S1 S2 S3 S4 Comp. dev.

15 3.33 ± 0.20a 2.74 ± 0.09a 2.94 ± 0.09a 3.54 ± 0.14a 10.40 ± 0.96a 20 2.26 ± 0.03b 1.72 ± 0.09b 1.75 ± 0.08b 2.18 ± 0.12b 8.44 ± 0.99b 25 1.62 ± 0.06c 1.40 ± 0.07c 1.37 ± 0.16c 1.71 ± 0.12c 6.06 ± 0.57c 30 1.35 ± 0.09d 1.19 ± 0.12d 1.41 ± 0.11c 1.99 ± 0.09d 5.40 ± 0.62d

Explanations: Within the columns means followed by the same letters are not significantly different at P < 0.05 (Tukey multiple comparison test). ANOVA statistics were: S1 F = 1448.667, df = 3, 96, P < 0.001; S2 F = 1402.709, df = 3, 96, P < 0.001; S3 F = 1066.786, df = 3, 96, P < 0.001; S4 F = 1137.521, df = 3, 96, P < 0.001; Comp. dev. F = 202.364, df = 3, 96, P < 0.001.

Studies of Aphidius ervi developmental rate Wilk test before comparative analyses were performed. Ef- Colonies of about 100 aphids (mixed adults with nymphs) fect of temperature was analysed by one way analysis of vari- were reared on fresh apple tree shoots. Ten adult parasitoids ance (ANOVA) and means were separated using Tukey mul- were introduced into a ventilated plastic box (30 cm long, tiple comparison test. Linear regression (using all data) was 25 cm high and 10 cm wide) containing an aphid colony and applied to compute the lower developmental thresholds, us- were allowed to parasitize the aphids at 25 ± 1 ◦C for 24 h. ing developmental rate data (1/days) as dependent variables At least 10 aphid colonies each containing 100 individuals (y-axis) and constant temperature treatments of 15–30 ◦Cas of A. pomi were used for each temperature treatment. At independent variables (x-axis). In some cases (S3, S4 stage) the end of the oviposition period, the plants with exposed the development at 30 ◦C was outside the linear segment of ◦ nymphs were placed in a thermostat at 15, 20, 25, 30 C, 60 the growth curve and therefore excluded from the linear re- ± 5% RH, and a photoperiod of 16:8 (L:D) hours. Aphids at gression. The lower developmental threshold (i.e., the point each temperature treatment were checked four times a day where developmental rate presumably equal 0) was deter- (in 6 h intervals) for the presence of sedentary and bloated mined as x-intercept of the linear equation. The degree-day mummies. The mummies were collected into glass vials and (DD) required was determined as the value of the inverse of returned to the same temperature treatment. All mummies equation slope (Campbell et al. 1974). JMP software (Ver. were checked daily until all parasitoids had emerged. Indi- 6.0.0, SAS Institute) was used for all statistical analyses. vidual development time was recorded for the period from oviposition to mummy formation and from mummy forma- tion to adult emergence. The parasitized colonies were kept Results 14 days after the last parasitoids had emerged. Development of parasitoids Studies of Aphis pomi developmental rate The development time for the parasitoid Aphidius ervi Experiments at the same temperatures as for the parasitoid at four constant temperatures is presented in Table 1 were initiated with 10 aphid colonies each containing 25 newly born larvae (0–6 h old), produced by apterous adults and the Degree-day requirement (DD) and lower de- (2–3 days old). The larvae were reared on fresh apple tree velopmental threshold (LDT) are presented in Table 3. shoots set in ventilated plastic boxes (30 cm length, 25 cm As it was shown by Malina & Praslička (2008), the de- high and 10 cm width). The shoots were replaced with fresh velopment of A. ervi is depending on temperature, as ones whenever leafs appeared dry (usually every 2 days). follows: The aphids were transferred by a small painting brush. Lar- The development time of mummy formation lin- vae were observed at 12 h intervals. Individual development early decreased as temperature increased in the range of time was recorded for all developmental stages from first 15–30 ◦C (Table 1). The mummy development of Aphis larval instar to adults (S1 – S4). Instars were determined pomi required 146.25 DD above a LDT of 6.79 ◦C(Ta- by cast skins. ble 3). Data analysis The time from mummy formation to emergence of Normality of distribution was checked with the Shapiro- A. ervi was inversely correlated with temperature in the Developmental rates of Aphis pomi and Aphidius ervi 901

Table 3. Degree-day requirement (DD) and lower developmental threshold (LDT) of A. ervi and A. pomi.

Aphidius ervi Aphis pomi

E–MM–AE–AS1S2S3S4Comp.dev.

DD 146.25 85.30 229.73 33.56 31.77 25.76 33.25 159.07 LDT 6.79 3.9 5.98 4.88 2.61 5.92 5.32 0.03

Explanations: E–M – egg-mummy, M–A – mummy-adult, E–A – egg-adult development of A. ervi; S1–S4 – immature stages, Comp. dev. – complete development of A. pomi. range of 15–30 ◦C (Table 1). The theoretical LDT was estimated at 3.9 ◦C. Thus, the parasitoid required 85.30 DD to emerge from the mummy (Table 3). The development times from oviposition to emer- gence of adult parasitoids are presented in Table 1, too. The adult parasitoid required 229.73 DD above a LDT of 5.98 ◦C(Table3).

Development of aphids Development time of the immature stages of A. pomi at four constant temperatures is given in Table 2. De- velopmental rate was correlated with the temperature in the range of 15–30 ◦C for first and second stages (S1, S2) and for complete development, respectively. In the third and fourth stage (S3, S4), development time de- creased at the range of 15–25 ◦C and then increased at the temperature of 30 ◦C. A linear regression analysis comparing tempera- ◦ Fig. 1. Developmental rates (r) of A. pomi and A. ervi at four ture treatment (15–30 C) with developmental rate of different temperatures (t). aphid’s first development stage resulted in the equation R =0.029794t − 0.145538 (r2 =0.9954, P = 0.0023). Therefore, this youngest stage required 33.56 DD above a LDT of 4.88 ◦C (Table 3). In the second develop- perature range (Fig. 1). The deficiency is 0.056 at 15 ◦C ment stage the equation was R =0.031478t − 0.082242 while it is 0.080 at 30 ◦C. The aphid A. pomi requires (r2 = 0.9826, P = 0.0088). This stage required 31.77 159.07 DD for complete development above a lower de- DD above a LDT of 2.61 ◦C (Table 3). Development velopmental threshold of 0.03 ◦C, while the parasitoid in the third stage can be described by the equation A. ervi needs 229.73 DD above a lower developmental R =0.038826t − 0.22986 (r2 = 0.9882, P = 0.0692). threshold of 5.98 ◦C(Table3). Third stage required 25.76 DD above a LDT of 5.92 ◦C (Table 3). The fourth (oldest) development stage can Discussion be described by the equation R =0.030077t − 0.159989 (r2 = 0.9899, P = 0.0641). Therefore, the last stage Temperature is an important environmental variable af- required 33.25 DD above a LDT of 5.32 ◦C(Table3). fecting the rates of development. The relationship In the third and fourth stage, the temperature 30◦C between temperature and developmental rate is a ba- was omitted because of outliers. Complete develop- sic component of the population dynamics of all insect ment of all four stages is characterized by the equation species. The purpose of this study was to evaluate the R =0.006286t − 0.000203 ( r2 = 0.9744, P = 0.0129). response of A. pomi to selected constant temperatures The apple aphid requires 159.07 DD above a LDT of and compare it with developmental rate of the para- 0.03 ◦C to complete her development. sitoid A. ervi. Our results showed that development of all four Comparison of developmental rates stages of A. pomi is linear, depending on temperature The comparison of developmental requirements of A. in the range of 15–25 ◦C. The temperature 30 ◦C violated pomi and its parasitoid A. ervi is given in Table 3 and the linearity in the third and fourth stages. A similar Fig. 1. As shown in Fig. 1, the developmental rate of A. trend was also observed for A. pomi by Arbab et al. pomi is higher than in A. ervi at the same conditions. (2006). The developmental rate of A. pomi increases from 0.096 The developmental threshold for A. pomi was esti- at 15 ◦C to 0.185 at 30 ◦C, while developmental rate of mated at 0.03 ◦C; 159.07 DD were required to complete the parasitoid A. ervi is only 0.040 at 15 ◦C and is in- the development from first instar to adult. This tem- creasing to 0.105 at 30 ◦C. The slope for A. pomi is perature threshold is close to the threshold of 0.5 ◦C increasing slightly more than for A. ervi at this tem- reported by Aalbersberg et al. (1987) for the Rus- 902 R. Malina et al. sian wheat aphid Diuraphis noxia Kurdjumov, 1913 in (Hymenoptera: Aphelinidae). Southwest. Entomol. 22: 29– South Africa and –0.26 ◦CreportedbyZhou&Carter 37. Metopolophium dirho- Campbell A., Frazer B.D., Gilbert N., Gutierrez A.P. & Mackauer (1992) for the grain aphid M. 1974. Temperature requirements of some aphids and their dum (Walker, 1849). But it is lower than the estimate parasites. J. Appl. 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