PHYSIOLOGICAL ECOLOGY Parasitism of Greenbug, graminum, by the Parasitoid at Winter Temperatures

1 2 3 DOUGLAS B. JONES, KRISTOPHER L. GILES, N. C. ELLIOTT, AND M. E. PAYTON

Department of Entomology and Plant Pathology, Oklahoma State University, Stillwater, OK 74078Ð3033

Environ. Entomol. 36(1): 1Ð8 (2007) Downloaded from https://academic.oup.com/ee/article/36/1/1/491129 by guest on 27 September 2021 ABSTRACT Functional responses by Lysiphlebus testaceipes (Cresson), a common parasitoid of small grain , on greenbug, (Rondani), were measured at seven temper- atures (14, 12, 10, 8, 6, 4, and 2ЊC) during a 24-h period (12-h light: 12-h dark). Oviposition by L. testaceipes ceased at temperatures Ͻ4ЊC. At all experimental temperatures, a type I, rather than a type II or type III, functional response was determined to be the best Þt based on coefÞcient of determination (r2) values. L. testaceipes was observed to oviposit in greenbugs at temperatures below the developmental temperature of both the greenbug host (5.8ЊC) and the parasitoid itself (6.6ЊC). This ability to oviposit at subdevelopmental temperatures enables the parasitoid to increase the percentage of greenbugs that are parasitized while the greenbugs are unable to reproduce. The implications of these Þndings regarding population suppression of greenbugs are discussed.

KEY WORDS Lysiphlebus testaceipes, Schizaphis graminum, functional response, biological control, winter hardiness

Winter (Triticum aestivum L.) is an important L. testaceipes has been observed to suppress greenbug multipurpose cereal crop grown in the Southern Great populations below economic injury levels in wheat Plains. More than 12 million acres are planted annually directly through mortality and indirectly by reducing for grain, forage, or as a combination grain/forage crop reproductive potential (Spencer 1926, Eikenbary and in Oklahoma and Texas (Epplin et al. 1998, USDA Rogers 1974, Giles et al. 2003). Additionally, L. testa- 2005). In this region of the United States, winter wheat ceipes causes aphids to drop from the plant in an is attacked primarily by phloem-feeding cereal aphids, attempt to avoid parasitism. Once on the ground, resulting in reduced forage and grain yields (Gerloff aphids are highly subject to desiccation and attack by and Ortman 1971, Burton 1986, Niassy et al. 1987, other natural enemies (Losey and Denno 1998). Peters et al. 1988, Kindler et al. 2002, 2003, K.G., un- Because of the relatively moderate climate in Okla- published data). One of the most damaging of the homa and Texas, greenbugs and other cereal aphids cereal aphids commonly found attacking winter wheat are able to feed on wheat throughout fall, winter, and is the greenbug, Schizaphis graminum (Rondani). spring months (Elliott et al. 2003, Royer et al. 2005). Greenbug can have a large impact on wheat produc- Adult parasitoids have been observed actively forag- tion. Its economic impact in Oklahoma has ranged ing on cool sunny days in Oklahoma throughout the from $0.5 to $135 million annually (Starks and Burton winter months (D.B.J., unpublished data). However, 1977, Webster 1995). when winter temperatures are at the lower extremes Greenbug populations can be suppressed below commonly encountered during wheat production, lit- economic injury levels through the actions of tle is known about the relationship between L. testa- parasitoids such as Lysiphlebus testaceipes Cresson ceipes and its greenbug host. (: Aphidiidae) (Jones 2001, Giles et al. Our previous work on L. testaceipes attack rates 2003). L. testaceipes is a solitary endoparasitoid whose were based on assumptions by integrated pest man- geographic range is Nearctic, Neotropical, and Oce- agement (IPM) practitioners (Patrick and Boring anic, in addition to being Paleartic because of inten- 1990, Royer et al. 1998). They suggested that parasi- tional introductions (Mackauer and Stary´ 1967). It has toids could not suppress greenbug populations at been observed to attack Ͼ100 aphid species (Mack- cool temperatures such as Ͻ14ЊC because parasitoid auer and Stary´ 1967, Stary´ et al. 1988, Pike et al. 2000). development was delayed relative to their aphid hosts. Indeed, studies showing lower developmental thresholds for greenbug (5.8ЊC; Walgenbach et al. 1 _ Corresponding author, e-mail: jonesd [email protected]. 1988) versus L. testaceipes (6.6ЊC; Royer et al. 2001) 2 USDAÐARSÐPSWCRL, Stillwater, OK 74075. 3 Department of Statistics, Oklahoma State University, Stillwater, and dramatic reductions in attack rates by L. testa- OK 74078Ð3033. ceipes as temperatures were decreased to 14ЊC (Jones

0046-225X/07/0001Ð0008$04.00/0 ᭧ 2007 Entomological Society of America 2ENVIRONMENTAL ENTOMOLOGY Vol. 36, no. 1 et al. 2003) support this assumption. However, recent covered with netting that was held in place by a rubber Þeld observations on the suppression of greenbug by band. Greenbugs from the colonies reared on wheat L. testaceipes during cold winter months suggest that were introduced by placing second and third instars adult parasitoids are actively foraging at temperatures on wheat tillers in each conetainer with a Þne brush. below greenbug developmental thresholds and effec- By only using similar-aged greenbugs, possible com- tively preventing populations from increasing (Jones plicating factors such as host age preference by the 2001, Giles et al. 2003). wasps were avoided. We established greenbugs in The primary objective of this study was to measure conetainers at densities that ranged from 5 to 80 green- the 24-h functional response of L. testaceipes on green- bugs per conetainer at each of the following seven bugs infesting winter wheat at 14ЊC and repeat these temperatures in growth chambers: 2, 4, 6, 8, 10, 12, and measurements at progressively colder temperatures 14ЊC. Because greenbugs are somewhat fragile, mor- until L. testaceipes failed to parasitize greenbug hosts. tality from handling made it difÞcult to establish a Additionally, we studied the relationship between predetermined density of greenbugs. Additionally, temperature and the proportion of L testaceipes fe- pedogenesis, reproduction by nymphs, occurs in Ϸ2% Downloaded from https://academic.oup.com/ee/article/36/1/1/491129 by guest on 27 September 2021 males that oviposited at each temperature. of immature greenbugs (Wood and Starks 1975). Be- cause of these difÞculties, we targeted four density ranges (Յ20, 21Ð40, 41Ð60, and 61Ð80 greenbugs/ Materials and Methods conetainer) at each experimental temperature. This Greenbug and Parasitoid Colonies. Biotype “E” ensured a sufÞcient range of densities necessary to greenbugs were obtained from colonies maintained at describe the functional response (Jones et al. 2003). the USDAÐARS Plant Science and Water Conserva- Actual numbers of greenbugs in each conetainer were tion Research Laboratory at Stillwater, OK; some determined when greenbugs were later dissected. were established on grain (cultivar SG-925), Greenbugs were allowed to acclimate at each tem- and others were established on wheat (cultivar 2137) perature for 4 h before parasitoids were introduced. A grown in a fritted clay and sphagnum moss mixture. minimum of six conetainer replicates were evaluated colonies and all plants were kept inside double- at each temperature and density range. Because all walled Þne mesh cages located within a climate-con- temperatures and densities could not be run at the trolled greenhouse (Ϸ22ЊC). The double-walled cages same time, temperatures and density combinations prevented contamination of colonies by feral green- were run in a random order. bugs and parasitoids while permitting ample airßow. To have naõ¨ve parasitoids that developed in green- Fresh plants were rotated as needed into cages hous- bugs reared on wheat, conetainers of wheat were ing colonies. infested with 25Ð35 third-instar and older greenbugs Three parasitoid colonies were maintained at 22 Ϯ from the wheat stock colony. By limiting the number 1ЊC and a photo-period of 12:12 (L:D) in double- of greenbugs, the Þtness of emerging parasitoids was walled Þne mesh cages in growth chambers. L. testa- not inßuenced by plant health (Fuentes-Granados et ceipes was isolated from specimens collected in Caddo al. 2001). These greenbugs were allowed to feed over- County, OK, in the spring of 2003 (40 L. testaceipes night, after which Þve male/female pairs of L. testa- adults isolated from greenbug mummies). Using sub- ceipes parasitoids were released into each conetainer samples of parasitoid offspring, we veriÞed the para- cage. Parasitized greenbugs were allowed to develop sitoids as L. testaceipes by keys (Pike et al. 1997) and into mummies, after which they were removed from polymerase chain reaction (PCR) analysis (Chen et al. the colony and placed individually into 1.5-ml micro- 2002, Jones et al. 2005). Pots of grain sorghum infested centrifuge vials. These isolated mummies were al- by greenbugs were placed in the colonies every 3Ð4 d lowed to develop until they emerged as adults. On to maintain a steady supply of parasitoids. Parasitoid emergence, the parasitoids were sexed and paired to colonies were maintained on grain sorghum because allow mating. Only parasitoids that had emerged on wheat stock plants succumbed relatively quickly to the day of the experiment were used in that dayÕs greenbug feeding damage. work. Parasitoids destined for evaluation were placed Functional Response Evaluations. Wheat seed (cul- into the growth chamber to acclimatize at each ex- tivar 2137) was planted in 5-cm-diameter by 20-cm-tall perimental temperature for 4 h before being released Ray Leach “conetainers” (Stuewe & Sons, Corvallis, into designated conetainers with greenbugs. OR). When plants were Ϸ30 cm tall (Ϸ3Ð4 wk), they Parasitoids were released as a mated pair in each were thinned to two similar sized tillers that were experimental conetainer during the dark cycle. The threaded through a 0.6-cm-diameter hole in a 5-cm- lights came on the next morning at 0600 hours and diameter by 0.6-cm-thick circular Plexiglas disk. The turned off 12 h later at 1800 hours, after which both disk was Þtted into the conetainer at soil level and parasitoids in each conetainer were removed, and cotton Þlled up the remaining area of the hole to their survival was recorded. If a female wasp did not create a sealed experimental arena ßoor that pre- survive, data from that conetainer were not used. Sur- vented access to the soil. A 5-cm-diameter by 30-cm- vival of the male wasp was noted, but did not inßuence tall clear acetate tube cage with two 5-cm holes cov- whether data were discarded. During the 24-h period ered with Þne mesh polyester netting in the sides (to that the parasitoids were exposed to greenbugs, they allow ventilation) was Þtted around the top of the were only active during the 12-h light period and were conetainer. The top of each tubular cage was also quiescent when lights were off (D.B.J., unpublished February 2007 JONES ET AL.: RESPONSE OF L. testaceipes AT LOW TEMPERATURES 3 data). After the removal of parasitoids, conetainers This decrease in the proportion of ovipositing parasi- were placed in a chamber at 22ЊC for 2Ð3 d to allow toids may help to describe L. testaceipes biology at parasitoid eggs to develop into larvae before dissec- suboptimal temperatures and the resulting dynamics tions were attempted. Subsequently, conetainers were with greenbug populations in Þeld situations. While held at 5ЊC to arrest parasitoid development, until all including nonparasitizing parasitoids in the analyses greenbugs were dissected. Eggs of aphid parasitoids was not typical of functional response models, these are quite difÞcult to detect, thus delaying dissections nonovipositing parasitoids are viable, potential attack- until after hatching greatly improved accuracy of ers of aphids that may only need warmer temperatures data (Hofsvang and Hågvar 1978, van Steenis 1993, to become active. Jones et al. 2003). Encapsulation could hinder accu- Voucher Specimens. Voucher specimens of L. testa- racy, but encapsulation of L. testaceipes by S. grami- ceipes adults and mummies and S. graminum adults num has yet to be observed (D.B.J., unpublished data). were deposited in the Department of Entomology and Dissections were performed in an aqueous solution Plant Pathology museum at Oklahoma State Univer- of 2% saline (NaCl) and 1% dishwashing detergent to sity in Stillwater. Downloaded from https://academic.oup.com/ee/article/36/1/1/491129 by guest on 27 September 2021 act as a surfactant. Greenbugs were dissected by grasp- ing the head with a pair of Þne forceps and pricking “ ” Results and Discussion the caudal region with a second pair of Þne forceps, opening the body cavity. Contents were gently Parasitism at Low Temperatures. Previous work by squeezed from the greenbug into the dissecting solu- Jones et al. (2003) suggested that L. testaceipes should tion and examined for the presence of parasitoid lar- be able to oviposit at temperatures Ͻ14ЊC. This ex- vae. Although L. testaceipes is solitary, superparasitism periment conÞrmed that assumption as we observed frequently occurs (Jones et al. 2003). Therefore, num- that 23.3% of L. testaceipes females assayed success- bers of larvae present in each greenbug and the total fully oviposited at 4ЊC (Fig. 1). This minimum tem- numbers of greenbugs per experimental unit (cone- perature is very close to observations by Hunter and tainer cage) dissected were recorded. Although some Glenn (1909), who, with limited observations, re- eggs may fail to hatch, the total number of parasitoid ported that L. testaceipes could oviposit at 3.3ЊC. This larvae present was assumed to be equal to the total result also compares well with Þeld observations that number of eggs laid per female in 24 h (Hofsvang and L. testaceipes can be active during typical Oklahoma Hågvar 1978, van Steenis 1993). winter temperatures (Pomeroy and Brun 1999, Giles Statistical Analyses. All statistical analyses were per- et al. 2003). formed using PC SAS version 8.2 (SAS Institute 1999) These observations are interesting because L. testa- at a signiÞcance level of P ϭ 0.05. CoefÞcients of ceipes is actively ovipositing at temperatures below its determination (r2 values) were calculated using developmental threshold of 6.6ЊC (Royer et al. 2001) PROC NLIN to determine which functional response and below the developmental temperature threshold model (type I, II, or III) best described the number of of its greenbug host (greenbug developmental thresh- greenbugs parasitized at each temperature over the old ϭ 5.8ЊC; Walgenbach et al. 1988). Provided adult range of host densities. The following models were females are present in wheat Þelds during the winter, evaluated: this ability to oviposit at temperatures below the de- ϭ Type I: NA aTN (Holling 1959a) velopmental threshold of the host enables the para- ϭ ϩ Type II: NA aTN/(1 aThN) (Holling 1959b) sitoid to effectively increase its population levels ϭ Ϫ Ϫ ϩ Type III: NA N{1 exp[ aT/(1 aThN)]} (within greenbug hosts) while the host cannot in- (Hassell et al. 1977)

In these models, NA is the number of hosts parasit- ized, N is the initial host density, T is the time available for searching during the experiment, a is the instan- taneous attack rate, and Th is the amount of time the parasitoid spent handling the host. For the type I models, the parameter a, along with the parameters a and Th for the type II and type III models, were estimated using PROC NLIN (Donnelly and Phillips 2001, Jones et al. 2003). Although these parameters can be measured by observation (Mills and Gutierrez 1999), it was not practical to do so in this experiment. Typically, functional responses are calculated for only those predators or parasitoids that actually attack their prey or host and are perceived of as normally functioning . However, in this paper, we also estimated functional response for all of the female parasitoids including those that remained alive but did Fig. 1. Bar graph with SE bars, showing the percent of not oviposit. We did this because our observations L. testaceipes females who successfully oviposited in green- indicated that as temperatures decreased the propor- bug, S. graminum, over 24 h (12:12 L:D) at 2, 4, 6, 8, 10, 12, tion of parasitoids that oviposited decreased as well. and 14ЊC. 4ENVIRONMENTAL ENTOMOLOGY Vol. 36, no. 1

Table 1. Coefficients of determination for functional response Table 3. Estimates of instantaneous attack rates (a) for regression models for L. testaceipes at 2, 4, 8, 10, 12, and 14°C L. testaceipes females that successfully oviposited, calculated from (12:12 L:D) on greenbugs experimental data fit to type I and II functional response models

Temperature Type I Type II Type III Functional Instantaneous Parasitoid speciesa Temperature Handling time (Ϯ1ЊC) (r2) (r2) (r2) response attack rate (ЊC) (Th Ϯ SE)a model (a Ϯ SE)a L. testaceipes 2b NA NA NA 4b 0.150 0.150 0.150 Type I 2 NA NA 6b 0.335 0.335 0.335 4 0.10 Ϯ 0.03a NA 8b 0.461 0.461 0.461 6 0.12 Ϯ 0.03a NA 10b 0.344 0.398 0.398 8 80.29 Ϯ 0.06ab NA 12b 0.283 0.308 0.308 10 0.22 Ϯ 0.04ab NA 14b 0.405 0.406 0.406 12 0.24 Ϯ 0.07ab NA 2c NA NA NA 14 0.34 Ϯ 0.06b NA 4c 0.655 0.669 0.669 Type II 2 NA NA c Ϯ Ϯ 6 0.483 0.524 0.524 4 0.25 0.41a 0.10 0.12a Downloaded from https://academic.oup.com/ee/article/36/1/1/491129 by guest on 27 September 2021 8c 0.625 0.625 0.625 6 0.61 Ϯ 1.00a 0.09 Ϯ 0.06a 10c 0.667 0.719 0.720 8 0.29 Ϯ 0.17a 0.00 Ϯ 0.00a 12c 0.480 0.523 0.524 10 0.87 Ϯ 1.20a 0.05 Ϯ 0.03a 14c 0.721 0.730 0.730 12 0.68 Ϯ 1.07a 0.04 Ϯ 0.04a 14 0.48 Ϯ 0.35a 0.01 Ϯ 0.02a a Lysiphlebus testaceipes host densities ranged from 5 to 80 green- bugs per experimental unit. Type I, II, and III functional response a a and Th estimated by PROC NLIN. equations were evaluated using SAS PROC NLIN to generate coef- Means sharing the same letter are not signiÞcantly different at ␣ ϭ Þcients of determination (r values), indicating best Þt. 0.05. b Functional response r2 values calculated using all parasitoids at NA, not applicable. that temperature. c Functional response r2 values calculated using only those para- sitoids that oviposited at that temperature. unable to determine which functional response model NA, not applicable. (type I, II, or III) provided the best Þt at 4, 6, and 8ЊC (Table 1). None of the models provided a best Þt because the coefÞcients of determination (r2) were crease its population. As experimental temperatures only 0.15 for each model at 4ЊC, 0.34 for each model increased, so did the percentage of ovipositing fe- at 6ЊC, and 0.46 for each model at 8ЊC. At 10, 12, and males (Fig. 1). However, percentages were similar at Њ Њ 14 C, a type II functional response model better de- 8Ð14 C. As environmental temperature increased scribed the relationship between greenbug density above the developmental threshold for greenbugs, and the attack rate of L. testaceipes than a type I model, several factors including numerical and functional re- but was indistinguishable from a type III model. How- sponses inßuence the dynamics between L. testaceipes ever, the r2 values for the type II and type III models and its host. were only marginally better than for a type I model Functional Response Calculations. When consider- (Table 1). Because of little to no differences in r2 ing all experimental parasitoids including those that values, we used the linear type I model for making did not oviposit, because of large amounts of variation comparisons between temperatures. Comparisons of in attack rates between individual parasitoids, we were instantaneous attack rates (a) estimated from type I functional response models (a type I model is the Њ Table 2. Estimates of instantaneous attack rates (a) for all simplest of the three models) revealed that the 4 C L. testaceipes females evaluated calculated from experimental data functional response model was not signiÞcantly dif- fit to type I and II functional response models ferent from the 6ЊC model but was signiÞcantly dif- ferent (lower) than the models for all other experi- Functional Instantaneous Temperature Handling time response attack rate mental temperatures (Table 2). When instantaneous (ЊC) (Th Ϯ SE)a model (a Ϯ SE)a attack rates (a) were calculated for the type II models, no signiÞcant differences were observed (Table 2). Type I 2 NA NA 4 0.02 Ϯ 0.01a NA Handling time (Th) estimates were also generated for 6 0.08 Ϯ 0.02ab NA the type II models; however, no signiÞcant differences 8 0.22 Ϯ 0.04b NA were observed among temperatures. 10 0.12 Ϯ 0.03b NA When those parasitoids that did not oviposit were 12 0.14 Ϯ 0.05b NA 14 0.19 Ϯ 0.05b NA removed from the calculations, the functional re- Type II 2 NA NA sponse coefÞcients of determination improved con- 4 0.16 Ϯ 0.66a 0.67 Ϯ 0.70a siderably. Again the r2 values were only marginally 6 0.08 Ϯ 0.02a 0.00 Ϯ 0.00a better for type II or type III functional response mod- 8 0.22 Ϯ 0.04a 0.00 Ϯ 0.00a 10 0.58 Ϯ 1.16a 0.10 Ϯ 0.07a els over the coefÞcient of determination values for a 12 0.35 Ϯ 0.55a 0.06 Ϯ 0.08a type I model. Instantaneous attack rates (a) estimated 14 0.21 Ϯ 0.18a 0.01 Ϯ 0.06a from type I functional response models revealed that the 4 and 6ЊC models were signiÞcantly different from a a and Th estimated by PROC NLIN. the 14ЊC model but were not signiÞcantly different Means sharing the same letter are not signiÞcantly different at ␣ ϭ 0.05. from the 8, 10, and 12ЊC models. Conversely, the 14ЊC NA, not applicable. model was also not signiÞcantly different from the 8, February 2007 JONES ET AL.: RESPONSE OF L. testaceipes AT LOW TEMPERATURES 5 Downloaded from https://academic.oup.com/ee/article/36/1/1/491129 by guest on 27 September 2021

Fig. 2. Scatter plots with linear regression trend lines (type I functional response) for L. testaceipes attack rates (excluding those parasitoids that did not oviposit) at 4, 6, 8, 10, 12, and 14ЊC (12:12 L:D). The 2ЊC scatter plot was omitted because no oviposition occurred.

10, and 12ЊC models (Table 3). When instantaneous vide little predictive power when describing the attack rates (a) and handling time estimates (Th) were relationship between greenbug density and attack calculated for the type II models, no signiÞcant dif- rates of L. testaceipes. At temperatures Ͼ14ЊC, a type ferences were observed (Table 3). III functional response model provided the best Þt Whether we considered only L. testaceipes females for describing the attack rate of L. testaceipes on that oviposited or all of the experimental parasitoids, greenbug at increasing host densities (Jones et al. type II and type III models provided only a slightly 2003). However, we were unable to determine which improved Þt with regard to r2 values (Table 1). Ad- functional response model best describes changes in ditionally, the extremely small handling times ob- L. testaceipes attack rate on greenbug at temperatures served seem to be biologically insigniÞcant and pro- Ͻ14ЊC. Again using the simple linear model (type I) 6ENVIRONMENTAL ENTOMOLOGY Vol. 36, no. 1 Downloaded from https://academic.oup.com/ee/article/36/1/1/491129 by guest on 27 September 2021

Fig. 3. Scatter plots with linear regression trend lines (type I functional response) for L. testaceipes attack rates (including those parasitoids that did not oviposit) at 4, 6, 8, 10, 12, and 14ЊC (12:12 L:D). The 2ЊC scatter plot was omitted because no oviposition occurred. for comparisons of L. testaceipes attack rates between temperatures Ͻ14ЊC, functional response models are temperatures, we determined that the slopes describ- poor predictors of L. testaceipes attack rates (Fig. 2). ing these attack rates are quite similar between 8 and Despite this poor predictive ability of the models, we 14ЊC; however, the slope is signiÞcantly different at observed suppression of greenbug and other cereal 4ЊC (Figs. 2 and 3). aphid populations by L. testaceipes during the cold Implications for Winter Ecology of L. testaceipes. A winter months in Oklahoma (Jones 2001, Giles et al. functional response is deÞned as the change in attack 2003). rate of a parasitoid or a predator exposed to increasing Our study adds additional information toward un- host densities per deÞned unit of time (Solomon derstanding why L. testaceipes can be such an effective 1949). The results of this experiment show that, at natural enemy in the Southern Great Plains during February 2007 JONES ET AL.: RESPONSE OF L. testaceipes AT LOW TEMPERATURES 7 winter months. When L. testaceipes is present in winter production. A future model with all of these factors wheat Þelds during the mild autumns (Ͼ14ЊC during will allow us to validate Þeld collected population August to November), this parasitoid is able to con- dynamics data. tribute toward suppression of aphid populations by a combination of (1) a high attack rate (Jones 2001, Giles et al. 2003), (2) sterilization of attacked aphids Acknowledgments (Spencer 1926, Hight et al. 1972, Eikenbary and Rogers 1974), (3) dislodgment of aphids from the plant We thank J. Dillwith and T. Phillips for critically reviewing (Losey and Denno 1998), and (4) its reproductive this manuscript and C. OÕNeil, D. Kastl, J. Chown, N. Jones, (numerical) response from attacked aphids (Giles P. Jones, and T. Johnson for contributions toward this re- et al. 2003). These factors are also important contri- search project. This work was approved for publication by butions toward aphid suppression during the mild the Director of the Oklahoma Agricultural Experiment Sta- spring months from February to May. During Decem- tion and supported in part under Projects OKLO2334 and

OKLO2455. Downloaded from https://academic.oup.com/ee/article/36/1/1/491129 by guest on 27 September 2021 ber and January, when temperatures are often Ͻ14ЊC, the reproductive response may be relatively unim- portant. As temperatures continue to drop, a devel- opmental advantage occurs with greenbugs (5.8ЊC; References Cited Walgenbach et al. 1988) that have a developmental Њ Archer, T. L., C. L. Murray, R. D. Eikenbary, K. J. Starks, and threshold lower than L. testaceipes (6.6 C; Royer et al. R. D. Morrison. 1973. Cold storage of Lysiphlebus testa- 2001). ceipes mummies. [Schizaphis graminum, grain pest con- Providing that temperatures do not drop below trol]. Environ. Entomol. 2: 1104Ð1108. the threshold for aphid development, aphids should Archer, T. L., C. L. Murray, R. D. Eikenbary, and R. L. continue to numerically increase at rates higher than Burton. 1974. Cold storage of Lysiphlebus testaceipes L. testaceipes. Despite weak functional response rela- adults. Environ. Entomol. 3: 557Ð558. tionships at cool temperatures, a signiÞcant propor- Burton, R. L. 1986. Effect of greenbug (Homoptera: Aphi- tion of female L. testaceipes parasitoids continue to didae) damage on root and shoot biomass of wheat seed- attack greenbugs as temperatures decrease below de- lings. J. Econ. Entomol. 79: 633Ð636. Chen, Y., K. L. Giles, M. E. Payton, and M. H. Greenstone. velopmental thresholds for both the host greenbug 2002. Molecular evidence for a species complex in the and the parasitoid (Fig. 1). Under these low temper- genus Aphelinus (Hymenoptera: Aphelinidae), with ad- ature conditions, L. testaceipes adult females can con- ditional data on aphidiine phylogeny (Hymenoptera: tinue to parasitize, sterilize, and dislodge greenbugs ). Ann. Entomol. Soc. Am. 95: 29Ð34. without signiÞcant development or reproduction by Donnelly, B. E., and T. W. Phillips. 2001. Functional re- the host. Additionally, L. testaceipes are longer lived at sponse of Xylocoris flavipes (: Anthocoridae): colder temperatures and are able to inßict mortality effects of prey species and habitat. Environ. Entomol. for extended periods of time (up to 3 wk; D.B.J., 30: 617Ð624. unpublished data). Eikenbary, R. D., and C. E. Rogers. 1974. Importance of These characteristics of L. testaceipes could enable alternate hosts in establishment of introduced parasites. Tall timbers conference on ecological control by the parasitoid to keep its population expanding (rel- habitat management, 28 FebruaryÐ1 March, Tallahassee, ative to aphid hosts) even when the weather is not FL. optimal for reproduction and subsequent develop- Elliott, N. C., K. L. Giles, T. A. Royer, S. D. Kindler, F. L. Tao, ment. Eventually adult parasitoids will die and/or ex- D. B. Jones, and G. W. Cuperus. 2003. Fixed precision haust their egg load during this period. However, the sequential sampling plans for the greenbug and bird- parasitoid progeny within their greenbug hosts are cherry-oat aphid (Homoptera: ) in winter in a state of reduced or arrested development. The wheat. J. Econ. Entomol. 96: 1585Ð1593. progeny is alive and able to develop once tempera- Epplin, F. M., R. R. True, and E. G. Krenzer, Jr. 1998. tures increase (Archer et al. 1973, 1974, Royer et al. Practices used by Oklahoma wheat growers by region. 2001). Indeed, we collected apparently healthy green- Oklahoma: Current Farm Economics. 7: 14Ð24. Fuentes-Granados, R. G., K. L. Giles, N. C. Elliott, and bugs from winter wheat Þelds in January and early D. R. Porter. 2001. Assessment of greenbug-resistant February, which were all or mostly all parasitized wheat germplasm on Lysiphlebus testaceipes Cresson (Giles et al. 2003). (Hymenoptera: Aphidiidae) oviposition and develop- Understanding interactions between greenbugs and ment in greenbug over two generations. Southwest. L. testaceipes during cold winter weather in the South- Entomol. 26: 187Ð194. ern Great Plains requires information on the inßuence Gerloff, E. D., and E. E. Ortman. 1971. Physiological of decreasing temperatures on parasitoid ecology/ changes in barley induced by greenbug feeding stress. biology. The observed low r2 values for functional Crop Sci. 11: 174Ð176. response models evaluated in our study indicate that Giles, K. L., D. B. Jones, T. A. Royer, N. C. Elliott, and attack rates at temperatures Ͻ14ЊC would be difÞcult S. D. Kindler. 2003. Development of a sampling plan in winter wheat that estimates cereal aphid parasitism levels to predict. The actual within-Þeld interactions be- and predicts population suppression. J. Econ. Entomol. tween S. graminum and L. testaceipes during the winter 96: 975Ð982. will depend on multiple factors including the rela- Hassell, M. P., J. H. Lawton, and J. R. Beddington. 1977. tionship between microclimate temperatures and ac- Sigmoid functional responses by invertebrate predators tivity (attack by L. testaceipes), development, and re- and parasitoids. J. Anim. Ecol. 46: 249Ð262. 8ENVIRONMENTAL ENTOMOLOGY Vol. 36, no. 1

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