Turk J Agric For 30 (2006) 383-386 © TÜB‹TAK

A Comparison of the Development Times of Trissolcus rufiventris (Mayr) and Trissolcus simoni Mayr (Hym.: Scelionidae) at Three Constant Temperatures

Müjgan KIVAN*, Nihal KILIÇ Nam›k Kemal University, Faculty of Agriculture, Department of Plant Protection, Tekirda¤, TURKEY

Received: 24.04.2006

Abstract: The effects of temperature on the development of the egg parasitoids Trissolcus rufiventris (Mayr) and Trissolcus simoni Mayr (Hym.: Scelionidae) were determined at 3 constant temperatures. Female development ranged from 6.9 days at 32 °C to 22.5 days at 20 °C for T. rufiventris, and from 9.2 days at 32 °C to 24.7 days at 20 °C for T. simoni. The average development time of males was shorter than that of females for each parasitoid species. The development of female T. rufiventris required 125.0 degree- days above the theoretical threshold of 15.5 °C and that of males required 111.1 degree-days above 15.3 °C. The lower threshold temperature and thermal requirement of T. simoni were estimated as 12.5 °C and 166.7 degree-days for females and 12.0 °C and 166.7 degree-days for males. The immature stages of T. rufiventris developed faster than those of T. simoni. It was concluded that T. rufiventris has an advantage in the biological control of Eurygaster integriceps Put. (Het.: ).

Key Words: Eurygaster integriceps, Trissolcus simoni, Trissolcus rufiventris, egg parasitoids, development, thermal requirement

Üç Sabit S›cakl›kta Trissolcus rufiventris (Mayr) ve Trissolcus simoni Mayr (Hym.: Scelionidae)’ nin Geliflmelerinin Karfl›laflt›r›lmas›

Özet: Yumurta parazitoitleri Trissolcus rufiventris (Mayr) ve Trissolcus simoni Mayr (Hym.: Scelionidae)’nin geliflimine 3 sabit s›cakl›¤›n etkileri belirlenmifltir. Difli geliflme süresi, T. rufiventris için 32 °C’de 6.9, 20 °C’de 22.5 gün, T. simoni için 32 °C’de 9.2 gün, 20 °C’de 24.7 gün aras›nda de¤iflmektedir. Her bir parazitoit türü için ortalama erkek geliflme süresi diflininkinden daha k›sa olarak bulunmufltur. T. rufiventris diflisi için 15.5 °C’ lik geliflme efli¤i üzerinde 125.0 gün-derece, erke¤i için 15.3 °C’ nin üzerinde 111.1 gün-dereceye gereksinimi vard›r. T. simoni’ nin en düflük geliflme efli¤i ve termal konstant gereksinimi difli bireyi için s›ras›yla 12.5 °C ve 166.7 gün-derece, erkek bireyi için 12.0 °C ve 166.7 gün-derece olarak hesaplanm›flt›r. T. rufiventris’ in ergin öncesi dönemlerinin T. simoni’ ye göre daha h›zl› geliflti¤i kaydedilmifltir. Eurygaster integriceps Put. (Het.: Scutelleridae) ile biyolojik mücadelede T. rufiventris türünün daha avantajl› oldu¤u kan›s›na var›lm›flt›r.

Anahtar Sözcükler: Eurygaster integriceps, Trissolcus simoni, Trissolcus rufiventris, yumurta parazitoitleri, geliflme, termal konstant

Introduction The scutellerid sunn pests Eurygaster integriceps Put. Scelionid egg parastioids play an important role in the and Eurygaster austriaca Schr., and E. maura L. (Het.: natural control of a number of populations, Scutelleridae) are among the most important insect pests including some important pests. The genera Trissolcus of wheat in the Thrace region of Turkey (Öncüer and and Telenomus, in particular, have received considerable K›van, 1995). Sunn pest populations could be reduced by attention as potential or useful biological control agents scelionid egg parasitoids in nature in the infested regions, against several pentatomids or scutellerids, such as the but these vary among regions and from year to year. In southern green stink bug, Nezara viridula (L.) (Het.: Turkey, several scelionids have been determined as Pentatomidae). biological control agents: Trissolcus semistriatus (Nees),

*Correspondence to: [email protected]

383 A Comparison of the Development Times of Trissolcus rufiventris (Mayr) and Trissolcus simoni Mayr (Hym.: Scelionidae) at Three Constant Temperatures

T. grandis Thom., T. basalis Woll., T. simoni Mayr., T. After the parasitization, parasitoids were removed and anitus Nixon, T. culturatus Mayr., T. rufiventris Mayr., T. parasitized eggs were maintained under the same choaspes Nixon, Telenomus chloropus Thom., T. temperature conditions until the immatures developed. truncatus Nees, T. tischleri Nixon, T. heydeni Mayr., and Observations were daily until parasitoid emergence Gryon monspeliensis Pic. (Lodos, 1982; Öncüer and was completed. The date and time of each observation K›van, 1995; Do¤anlar, 1998; Koçak and K›l›nçer, were recorded. The following data were recorded for 2001). each temperature: development time of both sexes, Considerable intra- and inter-specific variabilities have percentage of adult emergence, sex ratio, thermal been found in comparisons of scelionid egg parasitoids on requirement of immature stage, and development rate. pentatomids (Yeargan, 1982; Orr et al., 1985; Aswan et The data on development time and sexual ratio were al., 1989; Correa-Ferreira and Zamataro, 1989; subjected to analysis of variance (one-way ANOVA) and Cividanes and Figueiredo, 1996). To select a species with Duncan’s multiple range test (Aç›kgöz et al., 1994). To superior properties against the sunn pest, such as compare 2 egg parasitoid species, the values of fecundity, searching efficiency, overwintering survival, development and sex ratio for each species were alternative host species for survival, and mass rearing, subjected to a t-test (P ≤ 0.01). The effect of there is a lack of knowledge about native and important temperature on developmental rates (1/days) was egg parasitoids. Environmental conditions are important calculated by linear regression. The linear model was y = in the establishment of entomophagous (Doutt et a + bx, where a = intercept, b = slope, x = temperature al., 1976). Although temperature is one of the abiotic (°C), and y = development rate (1/days). The minimum factors influencing the population dynamics of insect developmental temperature threshold for each parasitoid pests and their natural enemies, it has a strong effect on species was found by extrapolating the regression line (T survival, development, generation time, and generation o number. These thermal characteristics may vary between = a/b). The degree-day requirements were determined as species. This study was conducted to determine and the inverse of the linear equation slope (DD = 1/b) compare the effects of temperature on the development (Sharov, 1996). times of T. semistriatus and T. simoni under laboratory conditions, to assess the availability of parasitoid species Results and Discussion for the biological control of E. integriceps. Both T. simoni and T. rufiventris completed their development at all temperatures examined. At each Materials and Methods temperature, all adults of T. rufiventris and T. simoni T. rufiventris and T. simoni were cultured in the emerged successfully. Thus, the temperature did not laboratory from samples originally collected in wheat affect the rate of adult emergence. fields in Tekirda¤ (Thrace region), Turkey. Parasitoids Development time from oviposition to adult were cultured in glass tubes with eggs from the emergence of T. rufiventris and T. simoni is reported in laboratory colony of E. integriceps as hosts, according to Table 1. Mean development time was inversely related to the methodology described by K›van and K›l›ç (2002). temperature and it was significantly longer at 20 °C than The culture was maintained at 26 °C temperature, 60 ± at other temperatures for both parasitoid species. Males 10% relative humidity and a L:D 16:8 h photoperiod. of both parasitoid species developed faster than females Effects of 3 constant temperatures (20, 26, and 32 at all the temperatures. T. rufiventris took about 21.6 °C) on the development and emergence of T. rufiventris days for males and 22.5 days for females to complete and T. simoni were compared. Two days after mating, a development at 20 °C, while it was 24.1 days for males pair (female and male) of parasitoids were kept in glass and 24.7 days for females of T. simoni. At 32 °C, it took tubes at constant temperature, in incubators with 16 h 6.4 and 6.9 days for males and females of T. rufiventris photoperiod and relative humidity of 60 ± 10%. Three and 9.1 and 9.2 days for males and females of T. simoni, clusters of E. integriceps eggs (approximately 3 x 14 = respectively. In comparison, the development time of T. 42 eggs) were offered to the females for parasitization. rufiventris was significantly faster than that of T. simoni, Each temperature treatment was replicated 4 times. at all temperatures (P ≤ 0.01).

384 M. KIVAN, N. KILIÇ

Table 1. Development time (days; mean ± SE) for Trissolcus simoni and Trissolcus rufiventris at 20, 26, and 32 °C.

Species Parameters 20 °C 26 °C 32 °C

T. simoni Development time (days) M 24.1 ± 0.134 a 12.2 ± 0.103 b 9.1 ± 0.100 c F 24.7 ± 0.113 a 12.4 ± 0.112 b 9.2 ± 0.040 c Sexual ratio (F/F + M) 0.810 0.880 0.90

T. rufiventris Development time (days) M 21.6 ± 0.357 a 10.2 ± 0.130 b 6.4 ± 0.128 c F 22.5 ± 0.202 a 10.5 ± 0.121 b 6.9 ± 0.109 c Sexual ratio (F/F + M) 0.700 0.820 0.800

Means followed by the same letter in the same row are not significantly different according to Duncan’s multiple range test (P ≤ 0.05). t value For development time M 36.226 21.975 12.863 (P ≤ 0.01) F 43.699 24.286 11.930 For sexual ratio 3.766 3.373 3.406

The relationships between temperature and The development rates (1/days) for parasitoid males development rates of T. simoni and T. rufiventris are and females increased linearly within the tested curvilinear, as is typically the case for insects, for example temperature range (Figures 1, 2; Table 2). The some scelionid species: Telenomus podisi Ashm. regression lines for the developmental rate of T. (Yeargan, 1980), Trissolcus euschisti (Ashm.) (Yeargan, rufiventris and T. simoni under 3 constant temperatures 1983), T. chloropus and T. basalis (Orr et al., 1985), for females are presented in Figure 1 and for males in Trissolcus oenone Dodd (James and Warren, 1991), Figure 2. Lower threshold temperatures differed from Trissolcus brochymenae (Ashm.) and T. podisi (Cividanes species to species (Table 2). The required temperatures and Figueiredo, 1996), and Trissolcus megallocephalus were higher for female parasitoids compared to males. (Ashm.) (Awadalla, 1996). The thermal threshold was lower for T. simoni (male, 12.0

0,16 T. rufiventris T. simoni 0,18 0,14 0,16 T. rufiventris T.simoni 0,12 0,14 0,1 y= -0.124+0.008x 0,12 y= -0.138+0.009x 0,1 0,08 0,08 0,06 0,06 0,04 y= -0.075+0.006x 0,04 y= -0.072+0.006x 0,02 0,02

Development rate (1/day) rate Development 0

0 Development rate (1/day) 0 5 10 15 20 25 30 35 0 5 10 15 20 25 30 35 Temperature (oC) Temperature (oC)

Figure 1. Female developmental rate of Trissolcus rufiventris and T. Figure 2. Male developmental rate of Trissolcus rufiventris and T. simoni under 3 constant temperatures. simoni under 3 constant temperatures.

Table 2. Parameters of the thermal unit values and regression coefficient for Trissolcus simoni and Trissolcus rufiventris.

Parameters T. simoni T. rufiventris

Male Female Male Female r2 0.988 0.990 0.999 1.0 P 0.25 0.25 0.10 0.10 Y = a + bx –0.072 + 0.006 –0.075 + 0.006 –0.138 + 0.009 –0.124 + 0.008 To (°C) 12.0 12.5 15.3 15.5 K (DD) 166.7 166.7 111.1 125.0

385 A Comparison of the Development Times of Trissolcus rufiventris (Mayr) and Trissolcus simoni Mayr (Hym.: Scelionidae) at Three Constant Temperatures

°C; female, 12.5 °C) than for T. rufiventris (male, 15.3 °C; and thermal constants were 15 °C/168.0 and 131.0 female, 15.5 °C), and consequently it could give a greater degree-day for T. chloropus and T. basalis, respectively. number of generations per season. However, the thermal These data indicate that T. rufiventris would be at an sum (DD) was higher for T. simoni, implying that, apparent advantage where higher temperatures are although T. simoni requires more DD, it accumulates them prevalent compared to T. simoni, because T. simoni will at a slower rate than T. rufiventris due to its lower To. come to fields from hibernating areas before T. The findings on development thresholds of T. simoni rufiventris due to the lower threshold temperature. and T. rufiventris were similar those reported by many However, T. rufiventris would have a competitive authors. Previous studies estimated that lower development advantage. T. rufiventris parasitizes the host eggs before thresholds and thermal constants were 14.1 °C/199.1 and T. simoni, because the immature stages of T. rufiventris 13.2 °C/150.7 degree-day for T. brochymenae and T. develop faster than T. simoni. Thus, the available host podisi, respectively (Cividanes and Figueiredo, 1996) and resource was reduced for the slower developing species. 12.4 °C/165.5 degree-day for T. oenone (James and Warren, 1991). The same data were determined for males and females: 15 °C/126.5 and 139.4 degree-day in T. Acknowledgments podisi (Yeargan, 1980), and 15 °C/118.2 and 142.2 The authors thank Dr. Erhan Koçak (Zirai Mücadele degree-day in T. euschisti (Yeargan, 1983). Orr et al. Merkez Araflt›rma Enstitüsü Müdürlü¤ü, Ankara, Turkey) (1985) also recorded that lower development thresholds for identifying the Trissolcus species.

References Aç›kgöz, N., M.E. Akafl, A. Moghaddam and K. Özcan. 1994. PC’ler için K›van, M. and N. K›l›ç. 2002. Host preference: parasitism, emergence veritaban› esasl› Türkçe istatistik paketi: TAR‹ST. In: Tarla and development of Trissolcus semistriatus (Hym., Scelionidae) in Bitkileri Kongresi, E.Ü.Z.F. Tarla Bitkileri Bölümü, ‹zmir, pp. various host eggs. J. Appl. Ent. 126: 395-399. 264-267. Koçak, E. and N. K›l›nçer. 2001. Turkiye Sune [Eurygaster spp. (Het.: Aswan, M.S., L.T. Wilson and M.P. Hoffman. 1989. Comparative Scutelleridae)] yumurta parazitoidi Trissolcus (Hym.: Scelionidae) biology of three geographic populations of turleri. Bitki Koruma Bülteni 41: 167-181. (: Scelionidae). Environ. Ento. 19: 387-392. Lodos, N. 1982. Türkiye Entomolojisi II (Genel, Uygulamali ve Awadalla, S.S. 1996. Influence of temperature and age of Nezara Faunistik). 591 s. Ege Üniversitesi Ziraat Fakültesi Yay. No. 429, viridula L. eggs on the scelionid egg parasitoid, Trissolcus Bornova, ‹zmir. megallocephalus (Ashm.) (Hym., Scelionidae). J. Appl. Ent. 12: Orr, D.B., D.J. Boethel and W.A. Jones. 1985. Development and 445-448. emergence of Telenomus chloropus and Trissolcus basalis Stink Cividanes, F.J. and J.G. Figueiredo. 1996. Development and emergence (Hymenoptera: Scelionidae) at various temperatures and relative of Trissolcus brochymenae (Ashmead) and Telenomus podisi humidities. Ann. Ent. Soc. Am. 78: 615-619. Ashmead (Hymenoptera: Scelionidae) at different temperatures. Öncüer, C. and M. K›van. 1995. Tekirda¤ ve çevresinde Eurygaster Lap. An. Soc. Entomol. Brasil 25: 207-211. (Heteroptera: Scutelleridae) türleri, tan›nmalar›, yay›l›fllar› ve Correa-Ferreira, B.S. and C.E.O. Zamataro. 1989. Reproductive bunlardan Eurygaster austriaca Put.’ in biyolojisi ve do¤al capacity and longevity of the egg parasitoids Trissolcus basalis düflmanlar› üzerinde araflt›rmalar. Turk. J. Agric. For. 19: 223- (Wollaston) and Trissolcus mitsukurii Ashmead (Hymenoptera: 230. Scelionidae). Revista Brasileira de Biologia 49: 621-626. Sharov, A. 1996. Quantitative Population Ecology. On-line lectures. Do¤anlar, M. 1998. Mass rearing of egg parasitoids of sunn pest Virginia Tech, Blacksburg. Available from: www.ento.vt.edu/ (Eurygaster austriaca Put.). In: Integrated Sunn Pest Control ~sharov/PopEcol/popecol.html. (Ed., K. Melan and C. Lomer). Plant Protection Central Research Institute, Ankara, pp. 89-94. Yeargan, K.V. 1980. Effects of temperature on developmental rate of Telenomus podisi (Hymenoptera: Scelionidae). Ann. Ent. Soc. Am. Doutt, R.L, D.P. Annecke and E. Tremblay. 1976. Biology and host 73: 339-342. relationships in parasitoids, pp. 143-168. In: Theory and practice of biological control. (Eds.: C.B. Huffaker and P.S. Messenger), Yeargan, K.V. 1982. Reproductive capability and longevity of the Academic Press, New York, pp. 143-168. parasitic wasps Telenomus podisi and Trissolcus euschisti. Ann. James, D.G. and G.N. Warren. 1991. Effect of temperature on Ent. Soc. Am. 75: 181-183. development, survival, longevity and fecundity of Trissolcus Yeargan, K.V. 1983. Effects of temperature on developmental rate of oenone Dodd (Hymenoptera: Scelionidae). J. Aus. Ent. Soc. 30: Trissolcus euschisti (Hymenoptera: Scelionidae), a parasite of 303-306. stink bug eggs. Ann. Ent. Soc. Am. 76: 757-760.

386