Thermal Performance of Two Indigenous Pupal Parasitoids Attacking the Invasive Drosophila suzukii (Diptera: Drosophilidae)

Thermal Performance of Two Indigenous Pupal Parasitoids Attacking the Invasive Drosophila suzukii... Abstract Pachycrepoideus vindemiae (Rondani) and Trichopria drosophilae (Perkins) are among a few indigenous parasitoids attacking the invasive Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) in North America. Both parasitoid species occur in California, whereas only P. vindemiae has been reported from Oregon. We compared the thermal performance of the California populations of P. vindemiae and T. drosophilae, and the Oregon population of P. vindemiae at eight constant temperatures (12.6–32.8°C). Both P. vindemiae populations could develop at all tested temperatures. T. drosophilae failed to develop at or above 29.6°C. This species was, however, able to develop at a diurnal temperature regime of 15–32°C, and survival was higher in older developmental stages. T. drosophilae was less tolerant to both low and high temperatures than P. vindemiae, whereas the Oregon P. vindemiae population was more cold-tolerant but less heat-tolerant than the California population in terms of offspring survival, development, and reproduction. To develop storage strategies for mass-cultured parasitoids, we compared the cold tolerance of immature P. vindemiae and T. drosophilae of the California populations at 12°C for 1, 2, or 3 mo, followed by a 23°C holding period. Successful development to the adult stage decreased as cold storage duration increased. Successful development, however, increased when cold storage was initiated during the older developmental stages for 1-mo exposure for both parasitoid species. The results are discussed with regards to parasitoid thermal adaptation and the potential use of P. vindemiae and T. drosophilae for biological control of spotted-wing drosophila. Pachycrepoideus vindemiae, Trichopria drosophilae, spotted-wing drosophila, thermal tolerance, population variation Temperature plays an important role in shaping the distribution and abundance of insect pests and their parasitoids (Angilletta 2009, Colinet et al. 2015, Grassi et al. 2017). For insect parasitoids and predators, identifying environmental constraints that affect their potential geographic range is fundamental to their effective use as biological control agents, particularly for the control of invasive pests (Hoelmer and Kirk 2005, Wang et al. 2012). A classic example of temperature tolerance and parasitoid effectiveness was demonstrated with the establishment and geographic range of Aphytis lingnanensis (Compere) and Aphytis chrysomphali (Mercet) (Hymenoptera: Aphelinidae) as parasitoids of red scale, Aonidiella aurantii (Mask.) (Hemiptera: Diaspididae) (Debach and Sisojevic 1960). The introduced A. lingnanensis became dominant and displaced the long-established A. chrysomphali everywhere but in a few coastal areas in Southern California due to their different thermal tolerances. Therefore, understanding the impact of temperature on parasitoid and pest populations is critical for predicting their distributions and field performance (Hance et al. 2007, Bowler and Terblanche 2008). Here, we investigated the thermal performance of Pachycrepoideus vindemiae (Rondani) (Hymenoptera: Pteromalidae) and Trichopria drosophilae (Perkins) (Hymenoptera: Diapriidae), both pupal parasitoids of the spotted-wing drosophila, Drosophila suzukii (Matsumura) (Diptera: Drosophilidae). D. suzukii is native to East Asia but has invaded and established widely in the Americas and Europe (Cini et al. 2014, Asplen et al. 2015, Andreazza et al. 2017). The fly is highly polyphagous, being able to develop in numerous fruit crops such as blackberries, blueberries, raspberries, strawberries, and stone fruits (e.g., Lee et al. 2011, Burrack et al. 2013, Stewart et al. 2014), as well as in more than 100 reported wild plants (Lee et al. 2015, Poyet et al. 2015, Kenis et al. 2016) including the winter-bearing Hedera helix (Araliaceae) (Grassi et al. 2017). Its fast development and high reproductive potential can lead to explosive population increases (Wiman et al. 2014, Wiman et al. 2016, Grassi et al. 2017) and significant economic losses to commercial crops (e.g., Beers et al. 2011, Goodhue et al. 2011, Haye et al. 2016). Following the invasion of D. suzukii to North American and Europe, several studies surveyed resident parasitoids newly associated with this pest and reported that the pupal parasitoids P. vindemiae and T. drosophilae readily attacked D. suzukii in Europe (Gabarra et al. 2015, Rossi Stacconi et al. 2015, Mazzetto et al. 2016, Knoll et al. 2017) and North America (Miller et al. 2015; Wang et al. 2016a, 2016b). However, few larval parasitoids were found attacking D. suzukii in the invaded ranges. Although there are numerous parasitoids attacking the larvae of various drosophilid species worldwide (Carton et al. 1986), most of the larval parasitoids found in Europe or North America are unable to develop from D. suzukii because of host immune resistance (e.g., Chabert et al. 2012, Kacsoh and Schlenke 2012). Concurrent with classical biological control programs investigating D. suzukii larval parasitoids from Asia (Daane et al. 2016, Biondi et al. 2017, Wang et al. 2018), researchers are investigating the augmentative release of T. drosophilae, which showed some promise for D. suzukii suppression in Italian production systems (Rossi Stacconi et al. 2018). It is, therefore, important to experimentally test the thermal performance of these naturally occurring parasitoids that can attack D. suzukii in its invaded ranges. Numerous studies have reported on the biology of P. vindemiae and T. drosophilae as parasitoids of D. suzukii (Rossi Stacconi et al. 2015; Wang et al. 2016a, 2016b; Kaçar et al. 2017; Rossi Stacconi et al. 2017); however, the thermal adaptability of these parasitoids is still not fully understood. Rossi Stacconi et al. (2017) investigated the effects of five constant temperatures (15, 20, 25, 30, and 35°C) on parasitism efficacy and developmental time of northern Italian populations and reported that T. drosophilae had a wider developmental temperature range than P. vindemiae. These authors also reported that T. drosophilae was a more effective parasitoid at 20 or 25°C, whereas P. vindemiae was most effective at 25 or 30°C. Both P. vindemiae and T. drosophilae have been reported in South France, Italy, and Spain (Chabert et al. 2012, Gabarra et al. 2015, Rossi Stacconi et al. 2015). However, in Switzerland, Knoll et al. (2017) surveyed eight different locations and found T. drosophilae only in one Southern location but P. vindemiae in all locations. In the western United States, both parasitoids were found in California’s Central Valley (Wang et al. 2016a, 2016b), but only P. vindemiae was found in Oregon’s Willamette Valley (Miller et al. 2014). These results suggest that P. vindemiae has a wider distribution than T. drosophilae. Since both parasitoids attack various drosophilids including Drosophila melanogaster (Meigen) (Diptera: Drosophilidae) (Wang et al. 2016a, 2016b), climatic adaptability rather than host availability may limit their geographical ranges. It is also possible that there may exist populations within each species that are adapted to different environments, given the diversity of habitats and climates encompassed by their global distributions. The aim of this study was to compare the thermal performance among California populations of P. vindemiae and T. drosophilae, and an Oregon population of P. vindemiae. We first quantified the effect of temperature on three major thermal performance profiles (survival, development, and reproduction) at a wide range of constant and diurnal temperature regimes. Diurnal temperature regimes were included to more realistically reflect daily thermal fluctuations during the summer months (Wang et al. 2009, Daane et al. 2013b). Finally, we tested the survival and viability of P. vindemiae and T. drosophilae of the California populations after prolonged low temperature storage for possible use in mass production for biological control (e.g., Colinet and Boivin 2011, Daane et al. 2013a). Results are discussed with respect to the thermal adaptation and geographic distributions of these species, as well as mass-rearing of both parasitoids for augmentative field release against D. suzukii. Materials and Methods Insect Colonies Studies were conducted at the University of California’s Kearney Agricultural Research and Extension Center in Parlier, California, United States. Laboratory colonies of D. suzukii, P. vindemiae, and T. drosophilae were initiated from field collections of approximately 50–100 individuals of each species during 2013 in Parlier and maintained in a laboratory under controlled conditions (23 ± 1°C, 16:8 [L: D] h). The flies were collected from infested cherries, whereas the parasitoids were collected from traps baited with D. suzukii pupae in cherry orchards. Thereafter, field-collected insects of approximately 50 individuals for each species during each spring and/or fall were added to the colonies to maintain vigor. A second P. vindemiae colony was initiated in 2014 from specimens collected in Corvallis, Oregon, and was maintained in a separate room under the same conditions. Hereafter, we refer to the California population as P. vindemiae (CA) and the Oregon population as P. vindemiae (OR). In total, we tested three distinct parasitoid cultures. Rearing methods of all three insects have been described previously (Wang et al. 2016a, 2016b). Briefly, adult flies were held in Bug Dorm cages (BioQuip Products Inc., Rancho Dominguez, CA), while adult parasitoids were held in fine mesh-screened cages (30 × 30 × 30 cm) (Mega View Science Co. Ltd., Taichung, Taiwan); all adult insects were supplied with a 20% honey-water solution in vial as food. Fly larvae were reared on a standard cornmeal-based artificial diet in Petri dishes (1.5 cm high, 14.0 cm diameter). Adult flies could oviposit for 24 h on uninfested Petri dishes and, after the resulting fly progeny had developed into 1- to 2-d-old pupae (6–7 d from oviposition), the dishes were exposed to the adult parasitoids for 2–3 d. The parasitoid-exposed dishes were then transferred to new cages and held for the emergence of adult flies (emerging in 2–3 d) and parasitoids (emerging in ~20 d). Newly emerged female and male wasps were collected and placed in screen cages (8 × 11 × 14 cm) with 50% honey-water streaked on the screen as food for the wasps. The wasps were held for 3–4 d to allow mating and egg maturation prior to their use in any trial (Wang et al. 2016a, 2016b). Unless specifically indicated, all experiments used 2-d-old D. suzukii pupae and 4- to 6-d-old adult female parasitoids and were conducted in temperature cabinets (Percival Scientific Inc., Perry, IA; Model 136VL) set to specific temperatures. Effect of Constant Temperature The effect of temperature on development and survival was determined simultaneously for the three parasitoid cultures (P. vindemiae (CA), P. vindemiae (OR) and T. drosophilae) at eight constant temperatures (12, 16, 20, 24, 28, 30, 31, and 32°C) under a photoperiod of 14:10 (L: D) h. This temperature range covers the average daily minimum and maximum temperatures in much of the California’s Central Valley from March to November when both parasitoids were active in the field (Wang et al. unpublished data). The temperatures were monitored using HOBO data loggers (Onset Corporation, Bourne, MA) to record the exact temperatures, which were used for data analyses. Relative humidity was maintained between 40 and 60% by a pan of water placed inside each incubator. Test procedures were similar for each parasitoid culture at each temperature. For each replicate, parasitized hosts were obtained by exposing 10 D. suzukii pupae to a single female wasp for 24 h inside a Petri dish (1.5 cm high × 8.5 cm diameter) at the controlled laboratory conditions as described previously. The host pupae were placed on a wet tissue paper and a small streak of 50% honey-water streaked on the side of the Petri dish was provided as food for the adult parasitoid. Exposed dishes were randomly assigned to different temperature treatments; initial parasitism was therefore assumed to be consistent across the different temperature treatments. Droplets of water were applied to the tissue paper every 2–3 d, to maintain moisture and prevent desiccation of parasitized host pupae. The Petri dishes were monitored twice per day (early morning and late afternoon) for the duration of days during which emergence occurred. After adult emergence had ceased, all unemerged host pupae were checked under a microscope. Dead and dried D. suzukii pupae were soaked in water to reconstitute tissues for 1 d and then dissected under a microscope to determine the presence or absence of fly or parasitoid cadavers. Each parasitoid-temperature combination had 30–35 replicates and each temperature treatment had five control replicates of 10 host pupae that were not exposed to parasitoids. Data of development time from egg to adult were pooled from all replicates for each temperature treatment. Parasitoid survival (egg to adult) was estimated for each replicate based on the number of emerged adult parasitoids compared with initial parasitism. Initial parasitism was calculated by dividing the sum of emerged and dead parasitoids (those seen via dissection) by the total fly pupae. When mortality of the immature parasitoids occurred early (e.g., egg or first instar larvae), it was difficult to determine if the fly was dead before or after parasitism; for this reason, fly mortality in the control treatment was used to correct mortality (parasitism) estimates of exposed hosts using the Abbott’s formula. The effect of temperature on oviposition success was determined for each parasitoid culture, i.e., T. drosophilae, P. vindemiae (CA), and P. vindemiae (OR) at seven constant temperatures (12, 16, 20, 24, 28, 31, and 32°C). For each replicate, 20 D. suzukii pupae were placed on a wet tissue paper inside a small Petri dish as described previously and exposed to a single female wasp for 48 h in the corresponding temperature incubator, with small streak of 50% honey-water streaked on the side of the Petri dish as food for the adult parasitoid. After which, exposed host pupae were removed from the incubator and held at the controlled laboratory conditions as described previously until adult flies or wasps emerged. Five control replicates of 20 unexposed hosts were treated similarly. The number of offspring and their sex were recorded. As described previously, all dead hosts were checked and dissected, and the total number of hosts attacked at each temperature was calculated as the sum of emerged and dead parasitoids (those seen via dissection). There were 30 replicates for each parasitoid-temperature combination. Effect of Varying High Temperature on T. drosophilae Our results under constant temperatures showed that T. drosophilae failed to complete development at the higher constant temperatures (>30°C) tested, and for this reason, we explored whether fluctuating exposure to high temperature would influence T. drosophilae differently. We used a diurnal temperature regime of 15–32°C, and 14:10 (L: D) h photoperiod to mimic average daily summer temperature fluctuations typical to much of the California’s Central Valley (Wang et al. 2009, Daane et al. 2013b). The high temperature cycle (32°C) ran from 10:00 to 20:00 h, and the minimum temperature cycle (15°C) ran during the remaining hours, with the temperature cabinet taking about 30 min to shift between the maximum and minimum temperature cycles. Photophase ran from 06:00 to 20:00 h. Host pupae containing four different T. drosophilae developmental stages (egg, young larva, old larva, and pupa) were tested separately. For each replicate, parasitized hosts were obtained by exposing 10 D. suzukii pupae to a single female wasp for 24 h in a Petri dish at the controlled laboratory conditions as described previously. The exposed hosts were then randomly assigned to the different treatments, with different parasitoid development stages obtained by using the exposed hosts immediately (egg) or holding at 23°C for 3 d (young larvae), 9 d (mature larvae), or 14 d (pupae) before being placed into the incubator. Parasitized hosts are distinguishable from live unparasitized hosts after a few days because live D. suzukii after later pupal stage have visible red eyes. Therefore, all exposed hosts used in the T. drosophilae larval and pupal treatments were initially screened before being exposed to the temperature regime so that only parasitized D. suzukii were used (i.e., 100% initial parasitism). It was, however, difficult to determine if an exposed D. suzukii pupa contained a T. drosophilae egg and, for this reason, all exposed hosts were used for the T. drosophilae egg treatment. Five control replicates, each had 10 D. suzukii pupae that were not exposed to parasitoids, were set aside. Initial parasitism for the egg treatment was estimated based on adult emergence, dissecting dead hosts, and the unexposed hosts in the control treatment, as described previously. All dishes were monitored until adult fly or wasp emergence ceased, and the number of successful offspring was recorded. Each developmental stage treatment had 20 replicates. Cold Storage To compare cold tolerance between P. vindemiae (CA) and T. drosophilae, each of four different parasitoid developmental stages (egg, larva, pupa, and preadult) were held at 12°C, with a photoperiod of 14:10 (L: D) h, for a 1-, 2-, and 3-mo cold storage period. In each replicate, 10 D. suzukii pupae were exposed to a single female wasp for 24 h in a Petri dish at the controlled laboratory conditions as described previously, and the exposed hosts were then moved to 12°C either immediately (when parasitoids were at the egg stage), 6 d later (larval stage), 14 d later (pupal stage), or 18 d later (preadult stage). After cold exposure, host pupae were held at 23°C and observed daily for adult emergence, recording the developmental time and sex of emerged wasps. Each developmental stage-species combination had 25 replicates. To test the reproductive viability of cold-stored parasitoids, a subsample of 25–30 newly emerged adult female and male T. drosophilae or P. vindemiae from the 1-mo treatment were collected and placed in screen cages (8 × 11 × 14 cm) with 50% honey-water streaked on the screen as food for the wasps. The wasps were held at the laboratory conditions as described for 3–4 d to allow mating and 4- to 6-d-old adult female parasitoids were used for the test. Individual females were each provided with 20 host pupae for a 48-h exposure period. The exposed hosts were monitored for the emergence of adult flies or wasps, as described previously. Data Analysis A nonlinear developmental model (Briere et al. 1999) was used to describe the relationship between developmental rate from oviposition to adult emergence D(T) and constant temperature T (°C): D(T)=nT(T−Tb)(TL−T)1m Where Tb and TL are the lower and upper thermal thresholds of development, and n and m are empirical constants. We determined the operative temperature range, defined as the difference between Tb and TL, and the optimum temperature, defined as the temperature at which the insect develops at its maximal rate. Additionally, data in the midrange of the nonlinear developmental rate model were selected to determine the best-fit using a linear regression analysis: D(T)=a+bT where a is the development rate at T = 0°C, and b is the slope of the regression line. The lower development threshold for the linear regression Tb is calculated as Tb = −a/b, and the thermal requirement (degree day, DD) to complete immature development is calculated as DD = 1/b. Parameter estimates of both models were obtained using the TableCurve 2D Program (Jandel-Scientific 1996). All values were presented as mean ± SE. Data on the number of hosts attacked (i.e., oviposition success) or parasitoid offspring survival by different parasitoid cultures at different constant temperatures were analyzed using two-way analysis of variance (ANOVA), considering the effects of temperature and parasitoid culture, as well as the interaction between these two factors. The effect of the fluctuating diurnal temperature regime (15–32°C) on the survival of T. drosophilae offspring among different developmental stages was compared using one-way ANOVA. The effects of cold exposure at 12°C for different exposure durations (1, 2, and 3 mo) on the survival or poststorage time to emergence of P. vindemiae (CA) or T. drosophilae were analyzed for each species separately. Because most pupae and all preadults of both parasitoid species completed development during 2- or 3-mo storage treatments, data on the survival or poststorage time to emergence for these two older developmental stages were available only for the 1-mo storage treatment. Therefore, the developmental stage effect on the survival or poststorage time to emergence was compared only for the 1-mo storage duration treatment using one-way ANOVA. The effect of different storage durations on the survival or poststorage time to emergence for the egg or larval developmental stage was analyzed separately using one-way ANOVA. Data on the 48-h fecundity or offspring sex ratio of emerged adults of P. vindemiae (CA) or T. drosophilae after being exposed at different life stages for 1 mo were analyzed using two-way ANOVA, considering the effects of developmental stage exposed and parasitoid species, as well as the interaction between these two factors. Prior to the analyses, all percentage data (survival and sex ratio) were arcsine, square-root transformed to normalize the variance after checking the normality of residuals, and homoscedasticity with Shaqiro’s and Bartlett’s test. Mean values among different treatments were separated using Tukey’s honest significant difference (HSD). All analyses were conducted using JMP Pro 13 (SAS, Cary, NC). Results Effect of Constant Temperature The temperature-dependent developmental rates were well described for each of the three parasitoid cultures (P. vindemiae (CA), P. vindemiae (OR), and T. drosophilae) by the linear and nonlinear models (Fig. 1). Both California and Oregon populations of P. vindemiae could develop at all tested temperatures (12.6–32.8°C), with the developmental rate increasing below or at 30.7°C but decreasing above 30.7°C (Fig. 1, Table 1). T. drosophilae failed to develop at or above 29.6°C and only three individuals successfully developed at 12.6°C (Fig. 1, Table 1). The estimated optimal, lower, and upper threshold developmental temperatures were similar for California and Oregon P. vindemiae populations, and their optimal and upper threshold temperatures were higher than that of T. drosophilae (Table 2). The thermal requirements (DD) to complete development were estimated to be 276.1, 276.3, 292.7 DD for P. vindemiae (CA), P. vindemiae (OR), and T. drosophilae, respectively (Table 2). Table 1. Mean (±SE) developmental time (days) from egg to adult emergence of P. vindemiae (CA) (Californian population), P. vindemiae (OR) (Oregon population), and T. drosophilae at various constant temperatures (±0.5°C) Temp. (°C) P. vindemiae (CA)a P. vindemiae (OR)a T. drosophilaea Female Male Female Male Female Male 12.6 241.0 ± 6.4 (30) 221.0 ± 14.1 (8) 207.2 ± 6.8 (87) 205.6 ± 13.2 (14) 190.0 ± 0.0 (1) 168.0 ± 21.0 (2) 16.8 47.8 ± 0.3 (101) 45.3 ± 0.4 (29) 43.8 ± 0.2 (193) 41.5 ± 0.4 (30) 43.0 ± 0.4 (79) 39.7 ± 0.6 (33) 21.5 26.7 ± 0.1 (236) 25.6 ± 0.3 (53) 27.4 ± 0.0 (138) 25.7 ± 0.3 (25) 24.9 ± 0.2 (132) 23.1 ± 0.2 (116) 23.5 21.3 ± 0.1 (196) 20.5 ± 0.2 (57) 22.8 ± 0.1 (135) 21.7 ± 0.1 (30) 21.1 ± 0.1 (238) 20.4 ± 0.1 (125) 28.9 15.9 ± 0.1 (106) 15.0 ± 0.0 (23) 15.1 ± 0.0 (155) 15.0 ± 0.0 (35) 16.7 ± 0.1 (86) 15.8 ± 0.1 (41) 29.6 15.0 ± 0.2 (21) 14.4 ± 0.1 (8) 14.6 ± 0.1 (111) 13.7 ± 0.2 (13) b b 30.7 14.7 ± 0.0 (152) 14.1 ± 0.1 (53) 14.6 ± 0.0 (150) 14.3 ± 0.1 (30) b b 32.8 18.6 ± 0.4 (15) 17.5 ± 0.3 (8) 18.5 ± 0.0 (2) b Temp. (°C) P. vindemiae (CA)a P. vindemiae (OR)a T. drosophilaea Female Male Female Male Female Male 12.6 241.0 ± 6.4 (30) 221.0 ± 14.1 (8) 207.2 ± 6.8 (87) 205.6 ± 13.2 (14) 190.0 ± 0.0 (1) 168.0 ± 21.0 (2) 16.8 47.8 ± 0.3 (101) 45.3 ± 0.4 (29) 43.8 ± 0.2 (193) 41.5 ± 0.4 (30) 43.0 ± 0.4 (79) 39.7 ± 0.6 (33) 21.5 26.7 ± 0.1 (236) 25.6 ± 0.3 (53) 27.4 ± 0.0 (138) 25.7 ± 0.3 (25) 24.9 ± 0.2 (132) 23.1 ± 0.2 (116) 23.5 21.3 ± 0.1 (196) 20.5 ± 0.2 (57) 22.8 ± 0.1 (135) 21.7 ± 0.1 (30) 21.1 ± 0.1 (238) 20.4 ± 0.1 (125) 28.9 15.9 ± 0.1 (106) 15.0 ± 0.0 (23) 15.1 ± 0.0 (155) 15.0 ± 0.0 (35) 16.7 ± 0.1 (86) 15.8 ± 0.1 (41) 29.6 15.0 ± 0.2 (21) 14.4 ± 0.1 (8) 14.6 ± 0.1 (111) 13.7 ± 0.2 (13) b b 30.7 14.7 ± 0.0 (152) 14.1 ± 0.1 (53) 14.6 ± 0.0 (150) 14.3 ± 0.1 (30) b b 32.8 18.6 ± 0.4 (15) 17.5 ± 0.3 (8) 18.5 ± 0.0 (2) b aFigures in parentheses are individuals successfully reared. bNo parasitoid developed successfully. View Large Table 1. Mean (±SE) developmental time (days) from egg to adult emergence of P. vindemiae (CA) (Californian population), P. vindemiae (OR) (Oregon population), and T. drosophilae at various constant temperatures (±0.5°C) Temp. (°C) P. vindemiae (CA)a P. vindemiae (OR)a T. drosophilaea Female Male Female Male Female Male 12.6 241.0 ± 6.4 (30) 221.0 ± 14.1 (8) 207.2 ± 6.8 (87) 205.6 ± 13.2 (14) 190.0 ± 0.0 (1) 168.0 ± 21.0 (2) 16.8 47.8 ± 0.3 (101) 45.3 ± 0.4 (29) 43.8 ± 0.2 (193) 41.5 ± 0.4 (30) 43.0 ± 0.4 (79) 39.7 ± 0.6 (33) 21.5 26.7 ± 0.1 (236) 25.6 ± 0.3 (53) 27.4 ± 0.0 (138) 25.7 ± 0.3 (25) 24.9 ± 0.2 (132) 23.1 ± 0.2 (116) 23.5 21.3 ± 0.1 (196) 20.5 ± 0.2 (57) 22.8 ± 0.1 (135) 21.7 ± 0.1 (30) 21.1 ± 0.1 (238) 20.4 ± 0.1 (125) 28.9 15.9 ± 0.1 (106) 15.0 ± 0.0 (23) 15.1 ± 0.0 (155) 15.0 ± 0.0 (35) 16.7 ± 0.1 (86) 15.8 ± 0.1 (41) 29.6 15.0 ± 0.2 (21) 14.4 ± 0.1 (8) 14.6 ± 0.1 (111) 13.7 ± 0.2 (13) b b 30.7 14.7 ± 0.0 (152) 14.1 ± 0.1 (53) 14.6 ± 0.0 (150) 14.3 ± 0.1 (30) b b 32.8 18.6 ± 0.4 (15) 17.5 ± 0.3 (8) 18.5 ± 0.0 (2) b Temp. (°C) P. vindemiae (CA)a P. vindemiae (OR)a T. drosophilaea Female Male Female Male Female Male 12.6 241.0 ± 6.4 (30) 221.0 ± 14.1 (8) 207.2 ± 6.8 (87) 205.6 ± 13.2 (14) 190.0 ± 0.0 (1) 168.0 ± 21.0 (2) 16.8 47.8 ± 0.3 (101) 45.3 ± 0.4 (29) 43.8 ± 0.2 (193) 41.5 ± 0.4 (30) 43.0 ± 0.4 (79) 39.7 ± 0.6 (33) 21.5 26.7 ± 0.1 (236) 25.6 ± 0.3 (53) 27.4 ± 0.0 (138) 25.7 ± 0.3 (25) 24.9 ± 0.2 (132) 23.1 ± 0.2 (116) 23.5 21.3 ± 0.1 (196) 20.5 ± 0.2 (57) 22.8 ± 0.1 (135) 21.7 ± 0.1 (30) 21.1 ± 0.1 (238) 20.4 ± 0.1 (125) 28.9 15.9 ± 0.1 (106) 15.0 ± 0.0 (23) 15.1 ± 0.0 (155) 15.0 ± 0.0 (35) 16.7 ± 0.1 (86) 15.8 ± 0.1 (41) 29.6 15.0 ± 0.2 (21) 14.4 ± 0.1 (8) 14.6 ± 0.1 (111) 13.7 ± 0.2 (13) b b 30.7 14.7 ± 0.0 (152) 14.1 ± 0.1 (53) 14.6 ± 0.0 (150) 14.3 ± 0.1 (30) b b 32.8 18.6 ± 0.4 (15) 17.5 ± 0.3 (8) 18.5 ± 0.0 (2) b aFigures in parentheses are individuals successfully reared. bNo parasitoid developed successfully. View Large Table 2. Estimates of lower (Tb), optimal (Topt) and upper (TL) threshold temperatures (°C) and, degree day (DD) requirements for the development from egg to adult emergence of P. vindemiae (CA) (California population), P. vindemiae (OR) (Oregon population), and T. drosophilae using linear and nonlinear models Species or population Linear modela Nonlinear Briere modelb Tb DD a b r2 Tb Topt TL n (x 10–5) m r2 P. vindemiae (CA) 11.1 276.1 -0.040 ± 0.002 0.004 ± 0.0001 0.997 10.1 ± 0.8 30.3 33.4 ± 0.3 8.3 ± 0.6 3.9 ± 0.7 0.998 P. vindemiae (OR) 11.0 276.3 -0.039 ± 0.003 0.004 ± 0.0001 0.995 8.9 ± 1.5 30.7 33.0 ± 0.2 8.9 ± 0.6 5.5 ± 1.4 0.995 T. drosophilae 10.1 292.7 -0.035 ± 0.006 0.003 ± 0.0003 0.983 9.0 ± 0.2 27.9 29.6 ± 0.0 11.1 ± 4.0 6.7 ± 1.1 0.925 Species or population Linear modela Nonlinear Briere modelb Tb DD a b r2 Tb Topt TL n (x 10–5) m r2 P. vindemiae (CA) 11.1 276.1 -0.040 ± 0.002 0.004 ± 0.0001 0.997 10.1 ± 0.8 30.3 33.4 ± 0.3 8.3 ± 0.6 3.9 ± 0.7 0.998 P. vindemiae (OR) 11.0 276.3 -0.039 ± 0.003 0.004 ± 0.0001 0.995 8.9 ± 1.5 30.7 33.0 ± 0.2 8.9 ± 0.6 5.5 ± 1.4 0.995 T. drosophilae 10.1 292.7 -0.035 ± 0.006 0.003 ± 0.0003 0.983 9.0 ± 0.2 27.9 29.6 ± 0.0 11.1 ± 4.0 6.7 ± 1.1 0.925 aD(T) = a + b T, where D(T) is the developmental rate at constant temperature T (°C). b D(T)=nT(T−Tb)(TL−T)1m. View Large Table 2. Estimates of lower (Tb), optimal (Topt) and upper (TL) threshold temperatures (°C) and, degree day (DD) requirements for the development from egg to adult emergence of P. vindemiae (CA) (California population), P. vindemiae (OR) (Oregon population), and T. drosophilae using linear and nonlinear models Species or population Linear modela Nonlinear Briere modelb Tb DD a b r2 Tb Topt TL n (x 10–5) m r2 P. vindemiae (CA) 11.1 276.1 -0.040 ± 0.002 0.004 ± 0.0001 0.997 10.1 ± 0.8 30.3 33.4 ± 0.3 8.3 ± 0.6 3.9 ± 0.7 0.998 P. vindemiae (OR) 11.0 276.3 -0.039 ± 0.003 0.004 ± 0.0001 0.995 8.9 ± 1.5 30.7 33.0 ± 0.2 8.9 ± 0.6 5.5 ± 1.4 0.995 T. drosophilae 10.1 292.7 -0.035 ± 0.006 0.003 ± 0.0003 0.983 9.0 ± 0.2 27.9 29.6 ± 0.0 11.1 ± 4.0 6.7 ± 1.1 0.925 Species or population Linear modela Nonlinear Briere modelb Tb DD a b r2 Tb Topt TL n (x 10–5) m r2 P. vindemiae (CA) 11.1 276.1 -0.040 ± 0.002 0.004 ± 0.0001 0.997 10.1 ± 0.8 30.3 33.4 ± 0.3 8.3 ± 0.6 3.9 ± 0.7 0.998 P. vindemiae (OR) 11.0 276.3 -0.039 ± 0.003 0.004 ± 0.0001 0.995 8.9 ± 1.5 30.7 33.0 ± 0.2 8.9 ± 0.6 5.5 ± 1.4 0.995 T. drosophilae 10.1 292.7 -0.035 ± 0.006 0.003 ± 0.0003 0.983 9.0 ± 0.2 27.9 29.6 ± 0.0 11.1 ± 4.0 6.7 ± 1.1 0.925 aD(T) = a + b T, where D(T) is the developmental rate at constant temperature T (°C). b D(T)=nT(T−Tb)(TL−T)1m. View Large Fig. 1. View largeDownload slide Relationship between temperature and developmental rate (1/d) for (A) P. vindemiae (CA) (California population), (B) P. vindemiae (OR) (Oregon population), and (C) T. drosophilae (see Table 1 for the number of individuals successfully developed at each temperature). All data are fitted to a nonlinear model (solid line) and midrange data were fitted to a linear model (dashed line) (see Table 2 for the model parameters). Fig. 1. View largeDownload slide Relationship between temperature and developmental rate (1/d) for (A) P. vindemiae (CA) (California population), (B) P. vindemiae (OR) (Oregon population), and (C) T. drosophilae (see Table 1 for the number of individuals successfully developed at each temperature). All data are fitted to a nonlinear model (solid line) and midrange data were fitted to a linear model (dashed line) (see Table 2 for the model parameters). Number of hosts attacked was affected by parasitoid culture (F = 52.2, df = 2, P < 0.001), temperature (F = 90.7, df = 6, P < 0.001), and the interaction between these two factors (F = 29.8, df = 12, P < 0.001) (Fig. 2A). Although all parasitoid cultures oviposited at all tested temperatures, T. drosophilae attacked a greater proportion of hosts than both P. vindemiae cultures from 16.8 to 23.5°C. P. vindemiae (OR) attacked more hosts than P. vindemiae (CA) below 30.7°C, but less hosts at 32.8°C (Fig. 2A). Offspring survival was also affected by parasitoid culture (F = 42.8, df = 2, P < 0.001), temperature (F = 85.3, df = 7, P < 0.001), and the interaction between these two factors (F = 21.4, df = 14, P < 0.001) (Fig. 2B). Percentage survival of T. drosophilae was lower than that of P. vindemiae at 12.6°C, but higher at midrange temperatures (21.5 to 28.9°C). P. vindemiae (OR) survived better at 12.6, 28.9, and 29.6°C, while P. vindemiae (CA) survived better at 32.8°C. The two populations performed similarly in terms of offspring survival at midrange temperatures (16.8–23.5°C) tested. Effect of Varying High Temperature on T. drosophilae When different life stages (egg, young larva, old larva, and pupa) of T. drosophilae were exposed to a high-fluctuating diurnal temperature regime (15–32°C), percentage survival to adult eclosion was affected by the developmental stage exposed (F3,76 = 33.2, P < 0.001). Survival rate increased from egg to young larva to old larva life stages, but there was no difference in survival rate between the old larval and pupal life stages (Fig. 3). Fig. 3. View largeDownload slide Survival of T. drosophilae offspring when exposed to a fluctuating diurnal temperature regime (15–32°C) at four developmental stages (egg, young larva, mature larva, and pupa). The high temperature cycle (32°C) ran from 10:00 to 20:00 h, and the minimum temperature cycle (15°C) ran during the remaining hours. Photophase ran from 06:00 to 20:00 h. Bars refer to mean ± SE and different letters above the bars indicate significant differences (P < 0.05). Fig. 3. View largeDownload slide Survival of T. drosophilae offspring when exposed to a fluctuating diurnal temperature regime (15–32°C) at four developmental stages (egg, young larva, mature larva, and pupa). The high temperature cycle (32°C) ran from 10:00 to 20:00 h, and the minimum temperature cycle (15°C) ran during the remaining hours. Photophase ran from 06:00 to 20:00 h. Bars refer to mean ± SE and different letters above the bars indicate significant differences (P < 0.05). Cold Storage When placed in cold storage (12°C) for 1, 2, or 3 months as eggs or larvae, 30.1 ± 5.7% P. vindemiae (CA) larvae in the 3-mo treatment completed development into adults, requiring an average 74.4 ± 3.8 d; no other eggs or larvae of both P. vindemiae (CA) and T. drosophilae completed development until after removal from the cold storage. When pupae were placed in cold storage, no P. vindemiae (CA) emerged in the 1-mo treatment but 41.9 ± 5.1% and 69.4 ± 6.8% of the tested P. vindemiae (CA) formed adults during the 2-mo (41.8 ± 1.3 d) and 3-mo (50.5 ± 1.7 d) storage periods, respectively. T. drosophilae pupae developed faster than P. vindemiae (CA) under these cold storage conditions, with 58 ± 6.9% (29.2 ± 0.1 d), 100% (31.0 ± 0.7 d), and 100% (34.3 ± 0.6 d) of the tested pupae emerging in the 1-, 2-, and 3-mo treatments, respectively. When preadults were placed in cold storage, most P. vindemiae (95.7 ± 3.9%) and all T. drosophilae emerged before the 1-mo storage period concluded (P. vindemiae (CA) in 20.4 ± 0.3 d and T. drosophilae in 16.8 ± 0.5 d). Data from individuals that emerged during the cold storage period were combined with those held at 23°C after the storage period elapsed. Survival rate for stored eggs did not differ among 1-, 2-, or 3-mo periods for P. vindemiae (CA) (F2,72 = 3.1, P = 0.050; Fig. 4A) and T. drosophilae (F2,72 = 2.4, P = 0.102; Fig. 4C), but generally decreased with increased duration for P. vindemiae (CA) larvae (F2,72 = 5.2, P = 0.008) and pupae (F2,72 = 3.7, P = 0.029), and for T. drosophilae larvae (F2,72 = 5.4, P = 0.006). After 1-mo cold storage, survival to the adult stage increased with older life stages for P. vindemiae (CA) (F3,113 = 16.0, P < 0.001; Fig. 4A) and T. drosophilae (F3,96 = 7.2, P < 0.001; Fig. 4C). Pupae and preadults were the most cold-tolerant life stages, with >80% of exposed individuals surviving to adults. Because development proceeded at 12°C, albeit slowly (Table 1), the duration of development to emergence after removal to 23°C was less for parasitoids that were held longer in cold storage for both P. vindemiae (CA) (F = 99.4, df = 2, P < 0.001; Fig. 4B) and T. drosophilae (F = 27.4, df = 2, P < 0.001; Fig. 4D). Looking only at the 1-mo storage period, developmental time decreased with older life stages for both P. vindemiae (CA) (F = 302.1, df = 2, P < 0.001; Fig. 4B) and T. drosophilae (F = 19.6, df = 1, P < 0.001; Fig. 4D). For those individuals that did not emerge during the 1-mo storage period, after being held at 23°C, the remaining pupae emerged with 7 d and the preadults emerged within 3 d. Fig. 4. View largeDownload slide Effects of cold exposure at 12 ± 0.5°C with a photoperiod of 14:10 (L: D) h for 1, 2, or 3 mo on P. vindemiae (California population) (A) survival and (B) poststorage developmental time to emergence, and T. drosophilae (C) survival and (D) poststorage developmental time to emergence when different life stages were exposed. Bars refer to mean and SE and different letters above the bars indicate significant differences (P < 0.05). Data were compared among different exposure durations for each developmental stage separately (lower case) or among different stages for the 1-mo storage duration (upper case). Fig. 4. View largeDownload slide Effects of cold exposure at 12 ± 0.5°C with a photoperiod of 14:10 (L: D) h for 1, 2, or 3 mo on P. vindemiae (California population) (A) survival and (B) poststorage developmental time to emergence, and T. drosophilae (C) survival and (D) poststorage developmental time to emergence when different life stages were exposed. Bars refer to mean and SE and different letters above the bars indicate significant differences (P < 0.05). Data were compared among different exposure durations for each developmental stage separately (lower case) or among different stages for the 1-mo storage duration (upper case). A 48-h fecundity of emerged females from 1-mo storage at 12°C differed by parasitoid species (F = 22.8, df = 1, P < 0.001), development stages (F = 11.5, df = 3, P < 0.001), and the interactive effect of these two factors (F = 2.9, df = 3, P = 0.039). P. vindemiae (CA) produced fewer offspring than T. drosophilae (Fig. 5A). The life stage held in cold storage for 1 mo had little effect on the subsequent number of offspring produced by female P. vindemiae (CA), whereas T. drosophilae females placed in cold storage as eggs or larvae clearly produced more offspring than those placed in cold storage as pupae or preadults (Fig. 5A). Offspring sex ratio (% female) was not affected by the parasitoid species (F = 3.6, df = 1, P = 0.061) but was affected by the developmental stage held in cold storage (F = 24.7, df = 3, P < 0.001), and fewer females were produced when the parasitoids were stored as preadults than when storage was initiated with younger stages (Fig. 5B). Fig. 5. View largeDownload slide Effect of cold exposure at 12 ± 0.5°C with a photoperiod of 14:10 (L: D) h on the (A) reproduction and (B) offspring sex ratio (% female) of emerged adults of P. vindemiae (California population) and T. drosophilae when different life stages were exposed for 1 mo. Bars refer to mean ± SE and different letters above the bars indicate significant differences (P < 0.05). Data were analyzed for each parasitoid species separately. Fig. 5. View largeDownload slide Effect of cold exposure at 12 ± 0.5°C with a photoperiod of 14:10 (L: D) h on the (A) reproduction and (B) offspring sex ratio (% female) of emerged adults of P. vindemiae (California population) and T. drosophilae when different life stages were exposed for 1 mo. Bars refer to mean ± SE and different letters above the bars indicate significant differences (P < 0.05). Data were analyzed for each parasitoid species separately. Discussion Knowledge of thermal performance of resident natural enemies will help to identify their geographical gaps and implement potential future classical biological control strategies. This study provides detailed information on the thermal performance of resident arthropod natural enemies to effectively suppress targeted herbivorous pests (Hoelmer and Kirk 2005). P. vindemiae and T. drosophilae are cosmopolitan parasitoids and occur sympatrically in California (Wang et al. 2016a, 2016b). However, thermal profile differences reported herein show P. vindemiae can survive, develop, and reproduce in a wider range of temperatures than T. drosophilae. Our results are supported by their field distributions in the western United States, where P. vindemiae has been collected in Oregon and California, but T. drosophilae has been collected only in California (Miller et al. 2015; Wang et al. 2016 a, 2016b). Our temperature-dependent developmental rates are similar to those of northern Italian populations at 20–30°C (Rossi Stacconi et al. 2017). For example, the developmental times of northern Italian P. vindemiae were 30.9, 19.8, and 14.6 d compared to California P. vindemiae, which was 29.0, 19.8, and 16.6 d at 20, 25, and 30°C, respectively. These periods closely match for both sexes of the respective populations. In the optimal or mid-temperature range (16.8–28.9°C), T. drosophilae was more efficient than P. vindemiae, in terms of parasitism, functional response as well as life-time fecundity, as shown in the current and other studies (Wang et al. 2016a, 2016b; Kaçar et al. 2017; Rossi Stacconi et al. 2017). However, Rossi Stacconi et al. (2017) showed in northern Italy that P. vindemiae failed to develop at 15°C, and T. drosophilae could develop at 30 and 35°C. In contrast, we showed that the California population of P. vindemiae could develop at 12.6°C, but T. drosophilae failed to develop at or above constant 29.6°C. These differences in temperature tolerance may be explained by geographically separate populations adapting to local conditions. For example, we found slight differences in thermal performance between P. vindemiae (CA) and P. vindemiae (OR) populations, which are geographically relatively close together but the climates they live in differ significantly. The California’s Central Valley has hotter summer but colder winter temperatures than Oregon’s Willamette Valley (Wiman et al. 2014). Not surprisingly, survival was comparatively better for the Oregon population at the lowest temperature studied, whereas survival of the California population was better at the highest temperature studied (Fig. 2). Population variation in the thermal performance of insects has been widely cited and is often correlated with local climate regimes (Sinclair et al. 2012). Of course, different methodologies could also have impacted the results. Rossi Stacconi et al. (2017) exposed D. suzukii to parasitoids at each tested temperature (their results thus reflect both the adult parasitoids’ ability to first parasitize the hosts and then the successful development of the immature stage), whereas we exposed D. suzukii to parasitoids at room temperature and then placed the exposed hosts into each tested temperature to determine specifically immature developmental time and survival. The data presented here demonstrate that exposure to constant temperatures do not necessarily provide a real-world estimation of T. drosophilae thermal performance. Fluctuating temperatures generally improve the performance of insects, albeit when temperatures approach, and exceed lower or upper threshold limits for shorter periods of time there can be negative impacts (Sinclair et al. 2012, Colinet et al. 2015). We found that T. drosophilae failed to develop above a constant 29.6°C but could develop under a diurnal regime of 15−32°C (24.9°C diurnal mean) where the upper threshold (29.6°C, Table 2) was exceeded for 10 h every day. D. suzukii has a similar upper temperature threshold (Tochen et al. 2014), and while it occurs in California’s Central Valley, its population abundances are lower during the summer (Wiman et al. 2014, Kaçar et al. 2016, Wang et al. 2016c). Higher thresholds under fluctuating temperature regimes have also been reported for other species that are found in California’s Central Valley, including the braconid Habrobracon gelechiae (Ashmead) (Hymenoptera: Braconidae) (Daane et al. 2013b) and the tephritid Bactrocera oleae (Rossi) (Diptera: Tephritidae) (Wang et al. 2009). Diurnal temperature fluctuations ultimately result in lower mean temperatures, which may aid in the physiological recovery from stressful high-temperature periods (Colinet et al. 2015). This recovery therefore may allow insects to persist in regional suboptimal microclimates, albeit at lower densities. For P. vindemiae and T. drosophilae, the optimal developmental temperatures were different, although both thermal performance curves were left skewed (Fig. 1), while the thermal performance curves for the survival and reproduction were asymmetrically bell shaped. For example, T. drosophilae could oviposit at the high temperatures (>29.6°C, Fig. 2), but most eggs and larvae failed to complete development to the adult life stage (Table 1). Ultimately, the failure to successfully complete any of the life-history stages would limit a parasitoid’s field distribution. Finally, there exists age-related variations in both cold and/or heat tolerance by both parasitoids. Both theoretical and empirical evidence suggest that thermal tolerance declines in the older life stages, and it is expected that such declines can be compensated behaviorally by the increased mobility in older life stages (Bowler and Terblanche 2008). For these parasitoids whose entire immature development occurs within the host pupae, young stages seem to be particularly sensitive to extreme temperatures. This suggests that these parasitoids would mostly likely overwinter in the more cold-tolerant pupal stage. Nevertheless, it is important to consider fluctuating temperature regimes that may account for the natural thermal variability, as well as age-related variations, for more realistically predicting the seasonal patterns or field performance of these parasitoids. Fig. 2. View largeDownload slide Effect of constant temperature (±0.5°C) on (A) number of hosts attacked and (B) parasitoid offspring survival for P. vindemiae (CA) (California population), P. vindemiae (OR) (Oregon population), and T. drosophilae. Bars refer to mean ± SE and different letters above the bars indicate significant differences (P < 0.05). Fig. 2. View largeDownload slide Effect of constant temperature (±0.5°C) on (A) number of hosts attacked and (B) parasitoid offspring survival for P. vindemiae (CA) (California population), P. vindemiae (OR) (Oregon population), and T. drosophilae. Bars refer to mean ± SE and different letters above the bars indicate significant differences (P < 0.05). Low temperature exposure negatively affected the survival and reproduction of emerged adult P. vindemiae and T. drosophilae. These results are generally consistent with other studies that report the effects of cold exposure on parasitoid fitness (reviewed by Colinet and Boivin 2011). We found that cold tolerance varied among the parasitoids’ developmental stages, with pupa or preadult being more cold-tolerant in terms of survival rate. However, P. vindemiae females that survived cold storage at the preadult stage produced more male-biased offspring than those stored at younger immature stages. Low temperature exposure during the preadult stage can impact the adult stage (Colinet et al. 2015), and we suspect that longer periods of cold storage might have led to sterilized P. vindemiae males. This phenomenon has been documented in other studies on cold storage of parasitoids (e.g., Wang et al. 2009). Thus, pupae should be an ideal storage stage for these parasitoids because of lower lethal and sublethal effects on parasitoid fitness; moreover, this stage is most easily separated from the unparasitized hosts as described previously, which may also be important in mass culture programs. In conclusion, our results suggest that P. vindemiae may be better adapted to regions with more varied low and high temperatures, whereas T. drosophilae may be better suited to mild climates. Future augmentative releases may consider utilizing parasitoids that best-fit thermal conditions in the widely varying commercial fruit-growing regions. It is crucial to suppress D. suzukii in noncrop habitats that may provide source populations that infest early season fruits. For example, in California’s Central Valley, D. suzukii may overwinter as pupae that will emerge in early spring or as adults that emerge in later fall (Kaçar et al. 2016, Wang et al. 2016c). For this reason, we also tested parasitoid cold storage, which may help in the optimal rearing and augmentative release of P. vindemiae or T. drosophilae for biological control of D. suzukii. Parasitoid releases may be best suited to fall or spring periods to reduce the overwintering and early spring populations in noncrop habitats harboring high fly populations; therefore, the parasitoids’ different thermal tolerances herein may allow the release of both species at different seasons or different climate zones to improve overall D. suzukii suppression. Acknowledgments We thank Pahoua Yang, May Yang, and Robert Straser (University of California, Berkeley) for laboratory assistance. Funding was supported by the National Institute of Food and Agriculture, U.S. Department of Agriculture Specialty Crops Research Initiative under Agreement No. 2015-51181-24252, the California Cherry Board, and the University of California’s Agricultural and Natural Resources Competitive Grants Program. References Cited Andreazza , F. , D. Bernardi , R. S. S. Dos Santos , F. R. M. Garcia , E. E. Oliveira , M. Botton , and D. E. Nava . 2017 . 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Anfora , A. Biondi , J. C. Chiu , K. M. Daane , B. Gerdeman , A. Gottardello , K. A. Hamby , R. Isaacs , et al. 2016 . Drosophila suzukii population response to environment and management strategies . J. Pest Sci . 89 : 653 – 665 . Google Scholar CrossRef Search ADS © The Author(s) 2018. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Environmental Entomology Oxford University Press

Thermal Performance of Two Indigenous Pupal Parasitoids Attacking the Invasive Drosophila suzukii (Diptera: Drosophilidae)

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Oxford University Press
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© The Author(s) 2018. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
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0046-225X
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1938-2936
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10.1093/ee/nvy053
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Abstract

Abstract Pachycrepoideus vindemiae (Rondani) and Trichopria drosophilae (Perkins) are among a few indigenous parasitoids attacking the invasive Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) in North America. Both parasitoid species occur in California, whereas only P. vindemiae has been reported from Oregon. We compared the thermal performance of the California populations of P. vindemiae and T. drosophilae, and the Oregon population of P. vindemiae at eight constant temperatures (12.6–32.8°C). Both P. vindemiae populations could develop at all tested temperatures. T. drosophilae failed to develop at or above 29.6°C. This species was, however, able to develop at a diurnal temperature regime of 15–32°C, and survival was higher in older developmental stages. T. drosophilae was less tolerant to both low and high temperatures than P. vindemiae, whereas the Oregon P. vindemiae population was more cold-tolerant but less heat-tolerant than the California population in terms of offspring survival, development, and reproduction. To develop storage strategies for mass-cultured parasitoids, we compared the cold tolerance of immature P. vindemiae and T. drosophilae of the California populations at 12°C for 1, 2, or 3 mo, followed by a 23°C holding period. Successful development to the adult stage decreased as cold storage duration increased. Successful development, however, increased when cold storage was initiated during the older developmental stages for 1-mo exposure for both parasitoid species. The results are discussed with regards to parasitoid thermal adaptation and the potential use of P. vindemiae and T. drosophilae for biological control of spotted-wing drosophila. Pachycrepoideus vindemiae, Trichopria drosophilae, spotted-wing drosophila, thermal tolerance, population variation Temperature plays an important role in shaping the distribution and abundance of insect pests and their parasitoids (Angilletta 2009, Colinet et al. 2015, Grassi et al. 2017). For insect parasitoids and predators, identifying environmental constraints that affect their potential geographic range is fundamental to their effective use as biological control agents, particularly for the control of invasive pests (Hoelmer and Kirk 2005, Wang et al. 2012). A classic example of temperature tolerance and parasitoid effectiveness was demonstrated with the establishment and geographic range of Aphytis lingnanensis (Compere) and Aphytis chrysomphali (Mercet) (Hymenoptera: Aphelinidae) as parasitoids of red scale, Aonidiella aurantii (Mask.) (Hemiptera: Diaspididae) (Debach and Sisojevic 1960). The introduced A. lingnanensis became dominant and displaced the long-established A. chrysomphali everywhere but in a few coastal areas in Southern California due to their different thermal tolerances. Therefore, understanding the impact of temperature on parasitoid and pest populations is critical for predicting their distributions and field performance (Hance et al. 2007, Bowler and Terblanche 2008). Here, we investigated the thermal performance of Pachycrepoideus vindemiae (Rondani) (Hymenoptera: Pteromalidae) and Trichopria drosophilae (Perkins) (Hymenoptera: Diapriidae), both pupal parasitoids of the spotted-wing drosophila, Drosophila suzukii (Matsumura) (Diptera: Drosophilidae). D. suzukii is native to East Asia but has invaded and established widely in the Americas and Europe (Cini et al. 2014, Asplen et al. 2015, Andreazza et al. 2017). The fly is highly polyphagous, being able to develop in numerous fruit crops such as blackberries, blueberries, raspberries, strawberries, and stone fruits (e.g., Lee et al. 2011, Burrack et al. 2013, Stewart et al. 2014), as well as in more than 100 reported wild plants (Lee et al. 2015, Poyet et al. 2015, Kenis et al. 2016) including the winter-bearing Hedera helix (Araliaceae) (Grassi et al. 2017). Its fast development and high reproductive potential can lead to explosive population increases (Wiman et al. 2014, Wiman et al. 2016, Grassi et al. 2017) and significant economic losses to commercial crops (e.g., Beers et al. 2011, Goodhue et al. 2011, Haye et al. 2016). Following the invasion of D. suzukii to North American and Europe, several studies surveyed resident parasitoids newly associated with this pest and reported that the pupal parasitoids P. vindemiae and T. drosophilae readily attacked D. suzukii in Europe (Gabarra et al. 2015, Rossi Stacconi et al. 2015, Mazzetto et al. 2016, Knoll et al. 2017) and North America (Miller et al. 2015; Wang et al. 2016a, 2016b). However, few larval parasitoids were found attacking D. suzukii in the invaded ranges. Although there are numerous parasitoids attacking the larvae of various drosophilid species worldwide (Carton et al. 1986), most of the larval parasitoids found in Europe or North America are unable to develop from D. suzukii because of host immune resistance (e.g., Chabert et al. 2012, Kacsoh and Schlenke 2012). Concurrent with classical biological control programs investigating D. suzukii larval parasitoids from Asia (Daane et al. 2016, Biondi et al. 2017, Wang et al. 2018), researchers are investigating the augmentative release of T. drosophilae, which showed some promise for D. suzukii suppression in Italian production systems (Rossi Stacconi et al. 2018). It is, therefore, important to experimentally test the thermal performance of these naturally occurring parasitoids that can attack D. suzukii in its invaded ranges. Numerous studies have reported on the biology of P. vindemiae and T. drosophilae as parasitoids of D. suzukii (Rossi Stacconi et al. 2015; Wang et al. 2016a, 2016b; Kaçar et al. 2017; Rossi Stacconi et al. 2017); however, the thermal adaptability of these parasitoids is still not fully understood. Rossi Stacconi et al. (2017) investigated the effects of five constant temperatures (15, 20, 25, 30, and 35°C) on parasitism efficacy and developmental time of northern Italian populations and reported that T. drosophilae had a wider developmental temperature range than P. vindemiae. These authors also reported that T. drosophilae was a more effective parasitoid at 20 or 25°C, whereas P. vindemiae was most effective at 25 or 30°C. Both P. vindemiae and T. drosophilae have been reported in South France, Italy, and Spain (Chabert et al. 2012, Gabarra et al. 2015, Rossi Stacconi et al. 2015). However, in Switzerland, Knoll et al. (2017) surveyed eight different locations and found T. drosophilae only in one Southern location but P. vindemiae in all locations. In the western United States, both parasitoids were found in California’s Central Valley (Wang et al. 2016a, 2016b), but only P. vindemiae was found in Oregon’s Willamette Valley (Miller et al. 2014). These results suggest that P. vindemiae has a wider distribution than T. drosophilae. Since both parasitoids attack various drosophilids including Drosophila melanogaster (Meigen) (Diptera: Drosophilidae) (Wang et al. 2016a, 2016b), climatic adaptability rather than host availability may limit their geographical ranges. It is also possible that there may exist populations within each species that are adapted to different environments, given the diversity of habitats and climates encompassed by their global distributions. The aim of this study was to compare the thermal performance among California populations of P. vindemiae and T. drosophilae, and an Oregon population of P. vindemiae. We first quantified the effect of temperature on three major thermal performance profiles (survival, development, and reproduction) at a wide range of constant and diurnal temperature regimes. Diurnal temperature regimes were included to more realistically reflect daily thermal fluctuations during the summer months (Wang et al. 2009, Daane et al. 2013b). Finally, we tested the survival and viability of P. vindemiae and T. drosophilae of the California populations after prolonged low temperature storage for possible use in mass production for biological control (e.g., Colinet and Boivin 2011, Daane et al. 2013a). Results are discussed with respect to the thermal adaptation and geographic distributions of these species, as well as mass-rearing of both parasitoids for augmentative field release against D. suzukii. Materials and Methods Insect Colonies Studies were conducted at the University of California’s Kearney Agricultural Research and Extension Center in Parlier, California, United States. Laboratory colonies of D. suzukii, P. vindemiae, and T. drosophilae were initiated from field collections of approximately 50–100 individuals of each species during 2013 in Parlier and maintained in a laboratory under controlled conditions (23 ± 1°C, 16:8 [L: D] h). The flies were collected from infested cherries, whereas the parasitoids were collected from traps baited with D. suzukii pupae in cherry orchards. Thereafter, field-collected insects of approximately 50 individuals for each species during each spring and/or fall were added to the colonies to maintain vigor. A second P. vindemiae colony was initiated in 2014 from specimens collected in Corvallis, Oregon, and was maintained in a separate room under the same conditions. Hereafter, we refer to the California population as P. vindemiae (CA) and the Oregon population as P. vindemiae (OR). In total, we tested three distinct parasitoid cultures. Rearing methods of all three insects have been described previously (Wang et al. 2016a, 2016b). Briefly, adult flies were held in Bug Dorm cages (BioQuip Products Inc., Rancho Dominguez, CA), while adult parasitoids were held in fine mesh-screened cages (30 × 30 × 30 cm) (Mega View Science Co. Ltd., Taichung, Taiwan); all adult insects were supplied with a 20% honey-water solution in vial as food. Fly larvae were reared on a standard cornmeal-based artificial diet in Petri dishes (1.5 cm high, 14.0 cm diameter). Adult flies could oviposit for 24 h on uninfested Petri dishes and, after the resulting fly progeny had developed into 1- to 2-d-old pupae (6–7 d from oviposition), the dishes were exposed to the adult parasitoids for 2–3 d. The parasitoid-exposed dishes were then transferred to new cages and held for the emergence of adult flies (emerging in 2–3 d) and parasitoids (emerging in ~20 d). Newly emerged female and male wasps were collected and placed in screen cages (8 × 11 × 14 cm) with 50% honey-water streaked on the screen as food for the wasps. The wasps were held for 3–4 d to allow mating and egg maturation prior to their use in any trial (Wang et al. 2016a, 2016b). Unless specifically indicated, all experiments used 2-d-old D. suzukii pupae and 4- to 6-d-old adult female parasitoids and were conducted in temperature cabinets (Percival Scientific Inc., Perry, IA; Model 136VL) set to specific temperatures. Effect of Constant Temperature The effect of temperature on development and survival was determined simultaneously for the three parasitoid cultures (P. vindemiae (CA), P. vindemiae (OR) and T. drosophilae) at eight constant temperatures (12, 16, 20, 24, 28, 30, 31, and 32°C) under a photoperiod of 14:10 (L: D) h. This temperature range covers the average daily minimum and maximum temperatures in much of the California’s Central Valley from March to November when both parasitoids were active in the field (Wang et al. unpublished data). The temperatures were monitored using HOBO data loggers (Onset Corporation, Bourne, MA) to record the exact temperatures, which were used for data analyses. Relative humidity was maintained between 40 and 60% by a pan of water placed inside each incubator. Test procedures were similar for each parasitoid culture at each temperature. For each replicate, parasitized hosts were obtained by exposing 10 D. suzukii pupae to a single female wasp for 24 h inside a Petri dish (1.5 cm high × 8.5 cm diameter) at the controlled laboratory conditions as described previously. The host pupae were placed on a wet tissue paper and a small streak of 50% honey-water streaked on the side of the Petri dish was provided as food for the adult parasitoid. Exposed dishes were randomly assigned to different temperature treatments; initial parasitism was therefore assumed to be consistent across the different temperature treatments. Droplets of water were applied to the tissue paper every 2–3 d, to maintain moisture and prevent desiccation of parasitized host pupae. The Petri dishes were monitored twice per day (early morning and late afternoon) for the duration of days during which emergence occurred. After adult emergence had ceased, all unemerged host pupae were checked under a microscope. Dead and dried D. suzukii pupae were soaked in water to reconstitute tissues for 1 d and then dissected under a microscope to determine the presence or absence of fly or parasitoid cadavers. Each parasitoid-temperature combination had 30–35 replicates and each temperature treatment had five control replicates of 10 host pupae that were not exposed to parasitoids. Data of development time from egg to adult were pooled from all replicates for each temperature treatment. Parasitoid survival (egg to adult) was estimated for each replicate based on the number of emerged adult parasitoids compared with initial parasitism. Initial parasitism was calculated by dividing the sum of emerged and dead parasitoids (those seen via dissection) by the total fly pupae. When mortality of the immature parasitoids occurred early (e.g., egg or first instar larvae), it was difficult to determine if the fly was dead before or after parasitism; for this reason, fly mortality in the control treatment was used to correct mortality (parasitism) estimates of exposed hosts using the Abbott’s formula. The effect of temperature on oviposition success was determined for each parasitoid culture, i.e., T. drosophilae, P. vindemiae (CA), and P. vindemiae (OR) at seven constant temperatures (12, 16, 20, 24, 28, 31, and 32°C). For each replicate, 20 D. suzukii pupae were placed on a wet tissue paper inside a small Petri dish as described previously and exposed to a single female wasp for 48 h in the corresponding temperature incubator, with small streak of 50% honey-water streaked on the side of the Petri dish as food for the adult parasitoid. After which, exposed host pupae were removed from the incubator and held at the controlled laboratory conditions as described previously until adult flies or wasps emerged. Five control replicates of 20 unexposed hosts were treated similarly. The number of offspring and their sex were recorded. As described previously, all dead hosts were checked and dissected, and the total number of hosts attacked at each temperature was calculated as the sum of emerged and dead parasitoids (those seen via dissection). There were 30 replicates for each parasitoid-temperature combination. Effect of Varying High Temperature on T. drosophilae Our results under constant temperatures showed that T. drosophilae failed to complete development at the higher constant temperatures (>30°C) tested, and for this reason, we explored whether fluctuating exposure to high temperature would influence T. drosophilae differently. We used a diurnal temperature regime of 15–32°C, and 14:10 (L: D) h photoperiod to mimic average daily summer temperature fluctuations typical to much of the California’s Central Valley (Wang et al. 2009, Daane et al. 2013b). The high temperature cycle (32°C) ran from 10:00 to 20:00 h, and the minimum temperature cycle (15°C) ran during the remaining hours, with the temperature cabinet taking about 30 min to shift between the maximum and minimum temperature cycles. Photophase ran from 06:00 to 20:00 h. Host pupae containing four different T. drosophilae developmental stages (egg, young larva, old larva, and pupa) were tested separately. For each replicate, parasitized hosts were obtained by exposing 10 D. suzukii pupae to a single female wasp for 24 h in a Petri dish at the controlled laboratory conditions as described previously. The exposed hosts were then randomly assigned to the different treatments, with different parasitoid development stages obtained by using the exposed hosts immediately (egg) or holding at 23°C for 3 d (young larvae), 9 d (mature larvae), or 14 d (pupae) before being placed into the incubator. Parasitized hosts are distinguishable from live unparasitized hosts after a few days because live D. suzukii after later pupal stage have visible red eyes. Therefore, all exposed hosts used in the T. drosophilae larval and pupal treatments were initially screened before being exposed to the temperature regime so that only parasitized D. suzukii were used (i.e., 100% initial parasitism). It was, however, difficult to determine if an exposed D. suzukii pupa contained a T. drosophilae egg and, for this reason, all exposed hosts were used for the T. drosophilae egg treatment. Five control replicates, each had 10 D. suzukii pupae that were not exposed to parasitoids, were set aside. Initial parasitism for the egg treatment was estimated based on adult emergence, dissecting dead hosts, and the unexposed hosts in the control treatment, as described previously. All dishes were monitored until adult fly or wasp emergence ceased, and the number of successful offspring was recorded. Each developmental stage treatment had 20 replicates. Cold Storage To compare cold tolerance between P. vindemiae (CA) and T. drosophilae, each of four different parasitoid developmental stages (egg, larva, pupa, and preadult) were held at 12°C, with a photoperiod of 14:10 (L: D) h, for a 1-, 2-, and 3-mo cold storage period. In each replicate, 10 D. suzukii pupae were exposed to a single female wasp for 24 h in a Petri dish at the controlled laboratory conditions as described previously, and the exposed hosts were then moved to 12°C either immediately (when parasitoids were at the egg stage), 6 d later (larval stage), 14 d later (pupal stage), or 18 d later (preadult stage). After cold exposure, host pupae were held at 23°C and observed daily for adult emergence, recording the developmental time and sex of emerged wasps. Each developmental stage-species combination had 25 replicates. To test the reproductive viability of cold-stored parasitoids, a subsample of 25–30 newly emerged adult female and male T. drosophilae or P. vindemiae from the 1-mo treatment were collected and placed in screen cages (8 × 11 × 14 cm) with 50% honey-water streaked on the screen as food for the wasps. The wasps were held at the laboratory conditions as described for 3–4 d to allow mating and 4- to 6-d-old adult female parasitoids were used for the test. Individual females were each provided with 20 host pupae for a 48-h exposure period. The exposed hosts were monitored for the emergence of adult flies or wasps, as described previously. Data Analysis A nonlinear developmental model (Briere et al. 1999) was used to describe the relationship between developmental rate from oviposition to adult emergence D(T) and constant temperature T (°C): D(T)=nT(T−Tb)(TL−T)1m Where Tb and TL are the lower and upper thermal thresholds of development, and n and m are empirical constants. We determined the operative temperature range, defined as the difference between Tb and TL, and the optimum temperature, defined as the temperature at which the insect develops at its maximal rate. Additionally, data in the midrange of the nonlinear developmental rate model were selected to determine the best-fit using a linear regression analysis: D(T)=a+bT where a is the development rate at T = 0°C, and b is the slope of the regression line. The lower development threshold for the linear regression Tb is calculated as Tb = −a/b, and the thermal requirement (degree day, DD) to complete immature development is calculated as DD = 1/b. Parameter estimates of both models were obtained using the TableCurve 2D Program (Jandel-Scientific 1996). All values were presented as mean ± SE. Data on the number of hosts attacked (i.e., oviposition success) or parasitoid offspring survival by different parasitoid cultures at different constant temperatures were analyzed using two-way analysis of variance (ANOVA), considering the effects of temperature and parasitoid culture, as well as the interaction between these two factors. The effect of the fluctuating diurnal temperature regime (15–32°C) on the survival of T. drosophilae offspring among different developmental stages was compared using one-way ANOVA. The effects of cold exposure at 12°C for different exposure durations (1, 2, and 3 mo) on the survival or poststorage time to emergence of P. vindemiae (CA) or T. drosophilae were analyzed for each species separately. Because most pupae and all preadults of both parasitoid species completed development during 2- or 3-mo storage treatments, data on the survival or poststorage time to emergence for these two older developmental stages were available only for the 1-mo storage treatment. Therefore, the developmental stage effect on the survival or poststorage time to emergence was compared only for the 1-mo storage duration treatment using one-way ANOVA. The effect of different storage durations on the survival or poststorage time to emergence for the egg or larval developmental stage was analyzed separately using one-way ANOVA. Data on the 48-h fecundity or offspring sex ratio of emerged adults of P. vindemiae (CA) or T. drosophilae after being exposed at different life stages for 1 mo were analyzed using two-way ANOVA, considering the effects of developmental stage exposed and parasitoid species, as well as the interaction between these two factors. Prior to the analyses, all percentage data (survival and sex ratio) were arcsine, square-root transformed to normalize the variance after checking the normality of residuals, and homoscedasticity with Shaqiro’s and Bartlett’s test. Mean values among different treatments were separated using Tukey’s honest significant difference (HSD). All analyses were conducted using JMP Pro 13 (SAS, Cary, NC). Results Effect of Constant Temperature The temperature-dependent developmental rates were well described for each of the three parasitoid cultures (P. vindemiae (CA), P. vindemiae (OR), and T. drosophilae) by the linear and nonlinear models (Fig. 1). Both California and Oregon populations of P. vindemiae could develop at all tested temperatures (12.6–32.8°C), with the developmental rate increasing below or at 30.7°C but decreasing above 30.7°C (Fig. 1, Table 1). T. drosophilae failed to develop at or above 29.6°C and only three individuals successfully developed at 12.6°C (Fig. 1, Table 1). The estimated optimal, lower, and upper threshold developmental temperatures were similar for California and Oregon P. vindemiae populations, and their optimal and upper threshold temperatures were higher than that of T. drosophilae (Table 2). The thermal requirements (DD) to complete development were estimated to be 276.1, 276.3, 292.7 DD for P. vindemiae (CA), P. vindemiae (OR), and T. drosophilae, respectively (Table 2). Table 1. Mean (±SE) developmental time (days) from egg to adult emergence of P. vindemiae (CA) (Californian population), P. vindemiae (OR) (Oregon population), and T. drosophilae at various constant temperatures (±0.5°C) Temp. (°C) P. vindemiae (CA)a P. vindemiae (OR)a T. drosophilaea Female Male Female Male Female Male 12.6 241.0 ± 6.4 (30) 221.0 ± 14.1 (8) 207.2 ± 6.8 (87) 205.6 ± 13.2 (14) 190.0 ± 0.0 (1) 168.0 ± 21.0 (2) 16.8 47.8 ± 0.3 (101) 45.3 ± 0.4 (29) 43.8 ± 0.2 (193) 41.5 ± 0.4 (30) 43.0 ± 0.4 (79) 39.7 ± 0.6 (33) 21.5 26.7 ± 0.1 (236) 25.6 ± 0.3 (53) 27.4 ± 0.0 (138) 25.7 ± 0.3 (25) 24.9 ± 0.2 (132) 23.1 ± 0.2 (116) 23.5 21.3 ± 0.1 (196) 20.5 ± 0.2 (57) 22.8 ± 0.1 (135) 21.7 ± 0.1 (30) 21.1 ± 0.1 (238) 20.4 ± 0.1 (125) 28.9 15.9 ± 0.1 (106) 15.0 ± 0.0 (23) 15.1 ± 0.0 (155) 15.0 ± 0.0 (35) 16.7 ± 0.1 (86) 15.8 ± 0.1 (41) 29.6 15.0 ± 0.2 (21) 14.4 ± 0.1 (8) 14.6 ± 0.1 (111) 13.7 ± 0.2 (13) b b 30.7 14.7 ± 0.0 (152) 14.1 ± 0.1 (53) 14.6 ± 0.0 (150) 14.3 ± 0.1 (30) b b 32.8 18.6 ± 0.4 (15) 17.5 ± 0.3 (8) 18.5 ± 0.0 (2) b Temp. (°C) P. vindemiae (CA)a P. vindemiae (OR)a T. drosophilaea Female Male Female Male Female Male 12.6 241.0 ± 6.4 (30) 221.0 ± 14.1 (8) 207.2 ± 6.8 (87) 205.6 ± 13.2 (14) 190.0 ± 0.0 (1) 168.0 ± 21.0 (2) 16.8 47.8 ± 0.3 (101) 45.3 ± 0.4 (29) 43.8 ± 0.2 (193) 41.5 ± 0.4 (30) 43.0 ± 0.4 (79) 39.7 ± 0.6 (33) 21.5 26.7 ± 0.1 (236) 25.6 ± 0.3 (53) 27.4 ± 0.0 (138) 25.7 ± 0.3 (25) 24.9 ± 0.2 (132) 23.1 ± 0.2 (116) 23.5 21.3 ± 0.1 (196) 20.5 ± 0.2 (57) 22.8 ± 0.1 (135) 21.7 ± 0.1 (30) 21.1 ± 0.1 (238) 20.4 ± 0.1 (125) 28.9 15.9 ± 0.1 (106) 15.0 ± 0.0 (23) 15.1 ± 0.0 (155) 15.0 ± 0.0 (35) 16.7 ± 0.1 (86) 15.8 ± 0.1 (41) 29.6 15.0 ± 0.2 (21) 14.4 ± 0.1 (8) 14.6 ± 0.1 (111) 13.7 ± 0.2 (13) b b 30.7 14.7 ± 0.0 (152) 14.1 ± 0.1 (53) 14.6 ± 0.0 (150) 14.3 ± 0.1 (30) b b 32.8 18.6 ± 0.4 (15) 17.5 ± 0.3 (8) 18.5 ± 0.0 (2) b aFigures in parentheses are individuals successfully reared. bNo parasitoid developed successfully. View Large Table 1. Mean (±SE) developmental time (days) from egg to adult emergence of P. vindemiae (CA) (Californian population), P. vindemiae (OR) (Oregon population), and T. drosophilae at various constant temperatures (±0.5°C) Temp. (°C) P. vindemiae (CA)a P. vindemiae (OR)a T. drosophilaea Female Male Female Male Female Male 12.6 241.0 ± 6.4 (30) 221.0 ± 14.1 (8) 207.2 ± 6.8 (87) 205.6 ± 13.2 (14) 190.0 ± 0.0 (1) 168.0 ± 21.0 (2) 16.8 47.8 ± 0.3 (101) 45.3 ± 0.4 (29) 43.8 ± 0.2 (193) 41.5 ± 0.4 (30) 43.0 ± 0.4 (79) 39.7 ± 0.6 (33) 21.5 26.7 ± 0.1 (236) 25.6 ± 0.3 (53) 27.4 ± 0.0 (138) 25.7 ± 0.3 (25) 24.9 ± 0.2 (132) 23.1 ± 0.2 (116) 23.5 21.3 ± 0.1 (196) 20.5 ± 0.2 (57) 22.8 ± 0.1 (135) 21.7 ± 0.1 (30) 21.1 ± 0.1 (238) 20.4 ± 0.1 (125) 28.9 15.9 ± 0.1 (106) 15.0 ± 0.0 (23) 15.1 ± 0.0 (155) 15.0 ± 0.0 (35) 16.7 ± 0.1 (86) 15.8 ± 0.1 (41) 29.6 15.0 ± 0.2 (21) 14.4 ± 0.1 (8) 14.6 ± 0.1 (111) 13.7 ± 0.2 (13) b b 30.7 14.7 ± 0.0 (152) 14.1 ± 0.1 (53) 14.6 ± 0.0 (150) 14.3 ± 0.1 (30) b b 32.8 18.6 ± 0.4 (15) 17.5 ± 0.3 (8) 18.5 ± 0.0 (2) b Temp. (°C) P. vindemiae (CA)a P. vindemiae (OR)a T. drosophilaea Female Male Female Male Female Male 12.6 241.0 ± 6.4 (30) 221.0 ± 14.1 (8) 207.2 ± 6.8 (87) 205.6 ± 13.2 (14) 190.0 ± 0.0 (1) 168.0 ± 21.0 (2) 16.8 47.8 ± 0.3 (101) 45.3 ± 0.4 (29) 43.8 ± 0.2 (193) 41.5 ± 0.4 (30) 43.0 ± 0.4 (79) 39.7 ± 0.6 (33) 21.5 26.7 ± 0.1 (236) 25.6 ± 0.3 (53) 27.4 ± 0.0 (138) 25.7 ± 0.3 (25) 24.9 ± 0.2 (132) 23.1 ± 0.2 (116) 23.5 21.3 ± 0.1 (196) 20.5 ± 0.2 (57) 22.8 ± 0.1 (135) 21.7 ± 0.1 (30) 21.1 ± 0.1 (238) 20.4 ± 0.1 (125) 28.9 15.9 ± 0.1 (106) 15.0 ± 0.0 (23) 15.1 ± 0.0 (155) 15.0 ± 0.0 (35) 16.7 ± 0.1 (86) 15.8 ± 0.1 (41) 29.6 15.0 ± 0.2 (21) 14.4 ± 0.1 (8) 14.6 ± 0.1 (111) 13.7 ± 0.2 (13) b b 30.7 14.7 ± 0.0 (152) 14.1 ± 0.1 (53) 14.6 ± 0.0 (150) 14.3 ± 0.1 (30) b b 32.8 18.6 ± 0.4 (15) 17.5 ± 0.3 (8) 18.5 ± 0.0 (2) b aFigures in parentheses are individuals successfully reared. bNo parasitoid developed successfully. View Large Table 2. Estimates of lower (Tb), optimal (Topt) and upper (TL) threshold temperatures (°C) and, degree day (DD) requirements for the development from egg to adult emergence of P. vindemiae (CA) (California population), P. vindemiae (OR) (Oregon population), and T. drosophilae using linear and nonlinear models Species or population Linear modela Nonlinear Briere modelb Tb DD a b r2 Tb Topt TL n (x 10–5) m r2 P. vindemiae (CA) 11.1 276.1 -0.040 ± 0.002 0.004 ± 0.0001 0.997 10.1 ± 0.8 30.3 33.4 ± 0.3 8.3 ± 0.6 3.9 ± 0.7 0.998 P. vindemiae (OR) 11.0 276.3 -0.039 ± 0.003 0.004 ± 0.0001 0.995 8.9 ± 1.5 30.7 33.0 ± 0.2 8.9 ± 0.6 5.5 ± 1.4 0.995 T. drosophilae 10.1 292.7 -0.035 ± 0.006 0.003 ± 0.0003 0.983 9.0 ± 0.2 27.9 29.6 ± 0.0 11.1 ± 4.0 6.7 ± 1.1 0.925 Species or population Linear modela Nonlinear Briere modelb Tb DD a b r2 Tb Topt TL n (x 10–5) m r2 P. vindemiae (CA) 11.1 276.1 -0.040 ± 0.002 0.004 ± 0.0001 0.997 10.1 ± 0.8 30.3 33.4 ± 0.3 8.3 ± 0.6 3.9 ± 0.7 0.998 P. vindemiae (OR) 11.0 276.3 -0.039 ± 0.003 0.004 ± 0.0001 0.995 8.9 ± 1.5 30.7 33.0 ± 0.2 8.9 ± 0.6 5.5 ± 1.4 0.995 T. drosophilae 10.1 292.7 -0.035 ± 0.006 0.003 ± 0.0003 0.983 9.0 ± 0.2 27.9 29.6 ± 0.0 11.1 ± 4.0 6.7 ± 1.1 0.925 aD(T) = a + b T, where D(T) is the developmental rate at constant temperature T (°C). b D(T)=nT(T−Tb)(TL−T)1m. View Large Table 2. Estimates of lower (Tb), optimal (Topt) and upper (TL) threshold temperatures (°C) and, degree day (DD) requirements for the development from egg to adult emergence of P. vindemiae (CA) (California population), P. vindemiae (OR) (Oregon population), and T. drosophilae using linear and nonlinear models Species or population Linear modela Nonlinear Briere modelb Tb DD a b r2 Tb Topt TL n (x 10–5) m r2 P. vindemiae (CA) 11.1 276.1 -0.040 ± 0.002 0.004 ± 0.0001 0.997 10.1 ± 0.8 30.3 33.4 ± 0.3 8.3 ± 0.6 3.9 ± 0.7 0.998 P. vindemiae (OR) 11.0 276.3 -0.039 ± 0.003 0.004 ± 0.0001 0.995 8.9 ± 1.5 30.7 33.0 ± 0.2 8.9 ± 0.6 5.5 ± 1.4 0.995 T. drosophilae 10.1 292.7 -0.035 ± 0.006 0.003 ± 0.0003 0.983 9.0 ± 0.2 27.9 29.6 ± 0.0 11.1 ± 4.0 6.7 ± 1.1 0.925 Species or population Linear modela Nonlinear Briere modelb Tb DD a b r2 Tb Topt TL n (x 10–5) m r2 P. vindemiae (CA) 11.1 276.1 -0.040 ± 0.002 0.004 ± 0.0001 0.997 10.1 ± 0.8 30.3 33.4 ± 0.3 8.3 ± 0.6 3.9 ± 0.7 0.998 P. vindemiae (OR) 11.0 276.3 -0.039 ± 0.003 0.004 ± 0.0001 0.995 8.9 ± 1.5 30.7 33.0 ± 0.2 8.9 ± 0.6 5.5 ± 1.4 0.995 T. drosophilae 10.1 292.7 -0.035 ± 0.006 0.003 ± 0.0003 0.983 9.0 ± 0.2 27.9 29.6 ± 0.0 11.1 ± 4.0 6.7 ± 1.1 0.925 aD(T) = a + b T, where D(T) is the developmental rate at constant temperature T (°C). b D(T)=nT(T−Tb)(TL−T)1m. View Large Fig. 1. View largeDownload slide Relationship between temperature and developmental rate (1/d) for (A) P. vindemiae (CA) (California population), (B) P. vindemiae (OR) (Oregon population), and (C) T. drosophilae (see Table 1 for the number of individuals successfully developed at each temperature). All data are fitted to a nonlinear model (solid line) and midrange data were fitted to a linear model (dashed line) (see Table 2 for the model parameters). Fig. 1. View largeDownload slide Relationship between temperature and developmental rate (1/d) for (A) P. vindemiae (CA) (California population), (B) P. vindemiae (OR) (Oregon population), and (C) T. drosophilae (see Table 1 for the number of individuals successfully developed at each temperature). All data are fitted to a nonlinear model (solid line) and midrange data were fitted to a linear model (dashed line) (see Table 2 for the model parameters). Number of hosts attacked was affected by parasitoid culture (F = 52.2, df = 2, P < 0.001), temperature (F = 90.7, df = 6, P < 0.001), and the interaction between these two factors (F = 29.8, df = 12, P < 0.001) (Fig. 2A). Although all parasitoid cultures oviposited at all tested temperatures, T. drosophilae attacked a greater proportion of hosts than both P. vindemiae cultures from 16.8 to 23.5°C. P. vindemiae (OR) attacked more hosts than P. vindemiae (CA) below 30.7°C, but less hosts at 32.8°C (Fig. 2A). Offspring survival was also affected by parasitoid culture (F = 42.8, df = 2, P < 0.001), temperature (F = 85.3, df = 7, P < 0.001), and the interaction between these two factors (F = 21.4, df = 14, P < 0.001) (Fig. 2B). Percentage survival of T. drosophilae was lower than that of P. vindemiae at 12.6°C, but higher at midrange temperatures (21.5 to 28.9°C). P. vindemiae (OR) survived better at 12.6, 28.9, and 29.6°C, while P. vindemiae (CA) survived better at 32.8°C. The two populations performed similarly in terms of offspring survival at midrange temperatures (16.8–23.5°C) tested. Effect of Varying High Temperature on T. drosophilae When different life stages (egg, young larva, old larva, and pupa) of T. drosophilae were exposed to a high-fluctuating diurnal temperature regime (15–32°C), percentage survival to adult eclosion was affected by the developmental stage exposed (F3,76 = 33.2, P < 0.001). Survival rate increased from egg to young larva to old larva life stages, but there was no difference in survival rate between the old larval and pupal life stages (Fig. 3). Fig. 3. View largeDownload slide Survival of T. drosophilae offspring when exposed to a fluctuating diurnal temperature regime (15–32°C) at four developmental stages (egg, young larva, mature larva, and pupa). The high temperature cycle (32°C) ran from 10:00 to 20:00 h, and the minimum temperature cycle (15°C) ran during the remaining hours. Photophase ran from 06:00 to 20:00 h. Bars refer to mean ± SE and different letters above the bars indicate significant differences (P < 0.05). Fig. 3. View largeDownload slide Survival of T. drosophilae offspring when exposed to a fluctuating diurnal temperature regime (15–32°C) at four developmental stages (egg, young larva, mature larva, and pupa). The high temperature cycle (32°C) ran from 10:00 to 20:00 h, and the minimum temperature cycle (15°C) ran during the remaining hours. Photophase ran from 06:00 to 20:00 h. Bars refer to mean ± SE and different letters above the bars indicate significant differences (P < 0.05). Cold Storage When placed in cold storage (12°C) for 1, 2, or 3 months as eggs or larvae, 30.1 ± 5.7% P. vindemiae (CA) larvae in the 3-mo treatment completed development into adults, requiring an average 74.4 ± 3.8 d; no other eggs or larvae of both P. vindemiae (CA) and T. drosophilae completed development until after removal from the cold storage. When pupae were placed in cold storage, no P. vindemiae (CA) emerged in the 1-mo treatment but 41.9 ± 5.1% and 69.4 ± 6.8% of the tested P. vindemiae (CA) formed adults during the 2-mo (41.8 ± 1.3 d) and 3-mo (50.5 ± 1.7 d) storage periods, respectively. T. drosophilae pupae developed faster than P. vindemiae (CA) under these cold storage conditions, with 58 ± 6.9% (29.2 ± 0.1 d), 100% (31.0 ± 0.7 d), and 100% (34.3 ± 0.6 d) of the tested pupae emerging in the 1-, 2-, and 3-mo treatments, respectively. When preadults were placed in cold storage, most P. vindemiae (95.7 ± 3.9%) and all T. drosophilae emerged before the 1-mo storage period concluded (P. vindemiae (CA) in 20.4 ± 0.3 d and T. drosophilae in 16.8 ± 0.5 d). Data from individuals that emerged during the cold storage period were combined with those held at 23°C after the storage period elapsed. Survival rate for stored eggs did not differ among 1-, 2-, or 3-mo periods for P. vindemiae (CA) (F2,72 = 3.1, P = 0.050; Fig. 4A) and T. drosophilae (F2,72 = 2.4, P = 0.102; Fig. 4C), but generally decreased with increased duration for P. vindemiae (CA) larvae (F2,72 = 5.2, P = 0.008) and pupae (F2,72 = 3.7, P = 0.029), and for T. drosophilae larvae (F2,72 = 5.4, P = 0.006). After 1-mo cold storage, survival to the adult stage increased with older life stages for P. vindemiae (CA) (F3,113 = 16.0, P < 0.001; Fig. 4A) and T. drosophilae (F3,96 = 7.2, P < 0.001; Fig. 4C). Pupae and preadults were the most cold-tolerant life stages, with >80% of exposed individuals surviving to adults. Because development proceeded at 12°C, albeit slowly (Table 1), the duration of development to emergence after removal to 23°C was less for parasitoids that were held longer in cold storage for both P. vindemiae (CA) (F = 99.4, df = 2, P < 0.001; Fig. 4B) and T. drosophilae (F = 27.4, df = 2, P < 0.001; Fig. 4D). Looking only at the 1-mo storage period, developmental time decreased with older life stages for both P. vindemiae (CA) (F = 302.1, df = 2, P < 0.001; Fig. 4B) and T. drosophilae (F = 19.6, df = 1, P < 0.001; Fig. 4D). For those individuals that did not emerge during the 1-mo storage period, after being held at 23°C, the remaining pupae emerged with 7 d and the preadults emerged within 3 d. Fig. 4. View largeDownload slide Effects of cold exposure at 12 ± 0.5°C with a photoperiod of 14:10 (L: D) h for 1, 2, or 3 mo on P. vindemiae (California population) (A) survival and (B) poststorage developmental time to emergence, and T. drosophilae (C) survival and (D) poststorage developmental time to emergence when different life stages were exposed. Bars refer to mean and SE and different letters above the bars indicate significant differences (P < 0.05). Data were compared among different exposure durations for each developmental stage separately (lower case) or among different stages for the 1-mo storage duration (upper case). Fig. 4. View largeDownload slide Effects of cold exposure at 12 ± 0.5°C with a photoperiod of 14:10 (L: D) h for 1, 2, or 3 mo on P. vindemiae (California population) (A) survival and (B) poststorage developmental time to emergence, and T. drosophilae (C) survival and (D) poststorage developmental time to emergence when different life stages were exposed. Bars refer to mean and SE and different letters above the bars indicate significant differences (P < 0.05). Data were compared among different exposure durations for each developmental stage separately (lower case) or among different stages for the 1-mo storage duration (upper case). A 48-h fecundity of emerged females from 1-mo storage at 12°C differed by parasitoid species (F = 22.8, df = 1, P < 0.001), development stages (F = 11.5, df = 3, P < 0.001), and the interactive effect of these two factors (F = 2.9, df = 3, P = 0.039). P. vindemiae (CA) produced fewer offspring than T. drosophilae (Fig. 5A). The life stage held in cold storage for 1 mo had little effect on the subsequent number of offspring produced by female P. vindemiae (CA), whereas T. drosophilae females placed in cold storage as eggs or larvae clearly produced more offspring than those placed in cold storage as pupae or preadults (Fig. 5A). Offspring sex ratio (% female) was not affected by the parasitoid species (F = 3.6, df = 1, P = 0.061) but was affected by the developmental stage held in cold storage (F = 24.7, df = 3, P < 0.001), and fewer females were produced when the parasitoids were stored as preadults than when storage was initiated with younger stages (Fig. 5B). Fig. 5. View largeDownload slide Effect of cold exposure at 12 ± 0.5°C with a photoperiod of 14:10 (L: D) h on the (A) reproduction and (B) offspring sex ratio (% female) of emerged adults of P. vindemiae (California population) and T. drosophilae when different life stages were exposed for 1 mo. Bars refer to mean ± SE and different letters above the bars indicate significant differences (P < 0.05). Data were analyzed for each parasitoid species separately. Fig. 5. View largeDownload slide Effect of cold exposure at 12 ± 0.5°C with a photoperiod of 14:10 (L: D) h on the (A) reproduction and (B) offspring sex ratio (% female) of emerged adults of P. vindemiae (California population) and T. drosophilae when different life stages were exposed for 1 mo. Bars refer to mean ± SE and different letters above the bars indicate significant differences (P < 0.05). Data were analyzed for each parasitoid species separately. Discussion Knowledge of thermal performance of resident natural enemies will help to identify their geographical gaps and implement potential future classical biological control strategies. This study provides detailed information on the thermal performance of resident arthropod natural enemies to effectively suppress targeted herbivorous pests (Hoelmer and Kirk 2005). P. vindemiae and T. drosophilae are cosmopolitan parasitoids and occur sympatrically in California (Wang et al. 2016a, 2016b). However, thermal profile differences reported herein show P. vindemiae can survive, develop, and reproduce in a wider range of temperatures than T. drosophilae. Our results are supported by their field distributions in the western United States, where P. vindemiae has been collected in Oregon and California, but T. drosophilae has been collected only in California (Miller et al. 2015; Wang et al. 2016 a, 2016b). Our temperature-dependent developmental rates are similar to those of northern Italian populations at 20–30°C (Rossi Stacconi et al. 2017). For example, the developmental times of northern Italian P. vindemiae were 30.9, 19.8, and 14.6 d compared to California P. vindemiae, which was 29.0, 19.8, and 16.6 d at 20, 25, and 30°C, respectively. These periods closely match for both sexes of the respective populations. In the optimal or mid-temperature range (16.8–28.9°C), T. drosophilae was more efficient than P. vindemiae, in terms of parasitism, functional response as well as life-time fecundity, as shown in the current and other studies (Wang et al. 2016a, 2016b; Kaçar et al. 2017; Rossi Stacconi et al. 2017). However, Rossi Stacconi et al. (2017) showed in northern Italy that P. vindemiae failed to develop at 15°C, and T. drosophilae could develop at 30 and 35°C. In contrast, we showed that the California population of P. vindemiae could develop at 12.6°C, but T. drosophilae failed to develop at or above constant 29.6°C. These differences in temperature tolerance may be explained by geographically separate populations adapting to local conditions. For example, we found slight differences in thermal performance between P. vindemiae (CA) and P. vindemiae (OR) populations, which are geographically relatively close together but the climates they live in differ significantly. The California’s Central Valley has hotter summer but colder winter temperatures than Oregon’s Willamette Valley (Wiman et al. 2014). Not surprisingly, survival was comparatively better for the Oregon population at the lowest temperature studied, whereas survival of the California population was better at the highest temperature studied (Fig. 2). Population variation in the thermal performance of insects has been widely cited and is often correlated with local climate regimes (Sinclair et al. 2012). Of course, different methodologies could also have impacted the results. Rossi Stacconi et al. (2017) exposed D. suzukii to parasitoids at each tested temperature (their results thus reflect both the adult parasitoids’ ability to first parasitize the hosts and then the successful development of the immature stage), whereas we exposed D. suzukii to parasitoids at room temperature and then placed the exposed hosts into each tested temperature to determine specifically immature developmental time and survival. The data presented here demonstrate that exposure to constant temperatures do not necessarily provide a real-world estimation of T. drosophilae thermal performance. Fluctuating temperatures generally improve the performance of insects, albeit when temperatures approach, and exceed lower or upper threshold limits for shorter periods of time there can be negative impacts (Sinclair et al. 2012, Colinet et al. 2015). We found that T. drosophilae failed to develop above a constant 29.6°C but could develop under a diurnal regime of 15−32°C (24.9°C diurnal mean) where the upper threshold (29.6°C, Table 2) was exceeded for 10 h every day. D. suzukii has a similar upper temperature threshold (Tochen et al. 2014), and while it occurs in California’s Central Valley, its population abundances are lower during the summer (Wiman et al. 2014, Kaçar et al. 2016, Wang et al. 2016c). Higher thresholds under fluctuating temperature regimes have also been reported for other species that are found in California’s Central Valley, including the braconid Habrobracon gelechiae (Ashmead) (Hymenoptera: Braconidae) (Daane et al. 2013b) and the tephritid Bactrocera oleae (Rossi) (Diptera: Tephritidae) (Wang et al. 2009). Diurnal temperature fluctuations ultimately result in lower mean temperatures, which may aid in the physiological recovery from stressful high-temperature periods (Colinet et al. 2015). This recovery therefore may allow insects to persist in regional suboptimal microclimates, albeit at lower densities. For P. vindemiae and T. drosophilae, the optimal developmental temperatures were different, although both thermal performance curves were left skewed (Fig. 1), while the thermal performance curves for the survival and reproduction were asymmetrically bell shaped. For example, T. drosophilae could oviposit at the high temperatures (>29.6°C, Fig. 2), but most eggs and larvae failed to complete development to the adult life stage (Table 1). Ultimately, the failure to successfully complete any of the life-history stages would limit a parasitoid’s field distribution. Finally, there exists age-related variations in both cold and/or heat tolerance by both parasitoids. Both theoretical and empirical evidence suggest that thermal tolerance declines in the older life stages, and it is expected that such declines can be compensated behaviorally by the increased mobility in older life stages (Bowler and Terblanche 2008). For these parasitoids whose entire immature development occurs within the host pupae, young stages seem to be particularly sensitive to extreme temperatures. This suggests that these parasitoids would mostly likely overwinter in the more cold-tolerant pupal stage. Nevertheless, it is important to consider fluctuating temperature regimes that may account for the natural thermal variability, as well as age-related variations, for more realistically predicting the seasonal patterns or field performance of these parasitoids. Fig. 2. View largeDownload slide Effect of constant temperature (±0.5°C) on (A) number of hosts attacked and (B) parasitoid offspring survival for P. vindemiae (CA) (California population), P. vindemiae (OR) (Oregon population), and T. drosophilae. Bars refer to mean ± SE and different letters above the bars indicate significant differences (P < 0.05). Fig. 2. View largeDownload slide Effect of constant temperature (±0.5°C) on (A) number of hosts attacked and (B) parasitoid offspring survival for P. vindemiae (CA) (California population), P. vindemiae (OR) (Oregon population), and T. drosophilae. Bars refer to mean ± SE and different letters above the bars indicate significant differences (P < 0.05). Low temperature exposure negatively affected the survival and reproduction of emerged adult P. vindemiae and T. drosophilae. These results are generally consistent with other studies that report the effects of cold exposure on parasitoid fitness (reviewed by Colinet and Boivin 2011). We found that cold tolerance varied among the parasitoids’ developmental stages, with pupa or preadult being more cold-tolerant in terms of survival rate. However, P. vindemiae females that survived cold storage at the preadult stage produced more male-biased offspring than those stored at younger immature stages. Low temperature exposure during the preadult stage can impact the adult stage (Colinet et al. 2015), and we suspect that longer periods of cold storage might have led to sterilized P. vindemiae males. This phenomenon has been documented in other studies on cold storage of parasitoids (e.g., Wang et al. 2009). Thus, pupae should be an ideal storage stage for these parasitoids because of lower lethal and sublethal effects on parasitoid fitness; moreover, this stage is most easily separated from the unparasitized hosts as described previously, which may also be important in mass culture programs. In conclusion, our results suggest that P. vindemiae may be better adapted to regions with more varied low and high temperatures, whereas T. drosophilae may be better suited to mild climates. Future augmentative releases may consider utilizing parasitoids that best-fit thermal conditions in the widely varying commercial fruit-growing regions. It is crucial to suppress D. suzukii in noncrop habitats that may provide source populations that infest early season fruits. For example, in California’s Central Valley, D. suzukii may overwinter as pupae that will emerge in early spring or as adults that emerge in later fall (Kaçar et al. 2016, Wang et al. 2016c). For this reason, we also tested parasitoid cold storage, which may help in the optimal rearing and augmentative release of P. vindemiae or T. drosophilae for biological control of D. suzukii. 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Environmental EntomologyOxford University Press

Published: Apr 9, 2018

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