PHYSIOLOGICAL ECOLOGY Effect of Food Resources on Adult Glyptapanteles militaris and Meteorus communis (: ), of Pseudaletia unipuncta (Lepidoptera: Noctuidae)

A. C. COSTAMAGNA AND D. A. LANDIS

Department of Entomology, 204 Center for Integrated Plant Systems, Michigan State University, East Lansing, MI 48824Ð1311 Downloaded from https://academic.oup.com/ee/article/33/2/128/375331 by guest on 29 September 2021

Environ. Entomol. 33(2): 128Ð137 (2004) ABSTRACT Adult parasitoids frequently require access to food and adequate microclimates to maximize host location and parasitization. Realized levels of parasitism in the Þeld can be signiÞcantly inßuenced by the quantity and distribution of extra-host resources. Previous studies have demon- strated a signiÞcant effect of landscape structure on parasitism of the armyworm Pseudaletia unipuncta (Haworth) (Lepidoptera: Noctuidae). As a possible mechanism underlying this pattern, we inves- tigated the effect of carbohydrate food sources on the longevity and fecundity of armyworm para- sitoids under laboratory conditions of varying temperature, host availability, and mating status. Glyptapanteles militaris (Walsh) (Hymenoptera: Braconidae) adults lived signiÞcantly longer when provided with honey as food and when reared at 20ЊC versus 25ЊC. Meteorus communis (Cresson) (Hymenoptera: Braconidae) adults also lived signiÞcantly longer when provided with honey, although longevity was reduced when females were provided hosts. Honey-fed females of M. communis parasitized signiÞcantly more hosts because of their increased longevity, but did not differ in daily oviposition from females provided only water. Mating signiÞcantly increased parasitism by honey-fed M. communis, but not those provided water alone. These results indicate that the presence of both carbohydrate resources and moderated microclimates may signiÞcantly increase the life span and parasitism of these parasitoids. However, the greater longevity and lower daily rate of oviposition of M. communis suggest that food and microclimate resources are more critical for this species than for the shorter lived, gregarious G. militaris. These Þndings contribute to our understanding of how these two parasitoids respond to landscape complexity.

KEY WORDS longevity, fecundity, mating status, biological control, life history parameters

AMONG PARASITOIDS, IT IS PRIMARILY the adult stage that have a relatively diverse and abundant community of Þnds and selects adequate resources to complete their parasitoids (Landis et al. 2000). The few studies con- life cycle. These resources include food, refuges from ducted to test this hypothesis have shown a signiÞcant abiotic and biotic mortality factors, and hosts. The increase of parasitism associated with landscape com- spatial distribution of these resources can limit the plexity (Marino and Landis 1996; Menalled et al. 1999, range of host search (Krˇivan and Sirot 1997, 2003; Thies and Tscharntke 1999). However, detailed Lewis et al. 1998). Although some adult parasitoids are knowledge of the biology and pattern of resource able to host feed, many hymenopteran parasitoids rely utilization of different parasitoid species in any par- on nonhost food for maintenance and to support egg ticular system is still necessary to interpret the pattern production (Quicke 1997). In crop monocultures, the of parasitism observed at the landscape level. presence of nonhost adult food resources may be lim- Potential nonhost food sources for parasitoids in- ited in time and space and may not be in synchrony clude ßoral and extraßoral nectar, pollen, and aphid with the presence of hosts in the appropriate stage honeydew (Quicke 1997). Flowering plants are fre- (Landis and Menalled 1998, Heimpel and Jervis 2004). quently visited by parasitoids (Bugg et al. 1989, Jervis Many parasitoid species that attack crop pests beneÞt et al. 1993), and consumption of ßoral nectar has been from the presence of undisturbed extra-Þeld habitats shown to enhance adult longevity (Heimpel and Jervis that contain these resources, which contributes to the 2004). Parasitoids fed carbohydrate resources, such as establishment and retention of parasitoid populations honey, sucrose, glucose, fructose, and other sugars in near crop Þelds (Landis and Marino 1999, Landis et al. solution, frequently show increased longevity under 2000, Tscharntke 2000). At the landscape scale, areas laboratory conditions (Jervis and Copland 1996). Ac- that have high structural complexity and a greater cessibility of nonhost food is correlated not only with proportion of undisturbed Þelds are most likely to increased life span, but also with increased fecundity,

0046-225X/04/0128Ð0137$04.00/0 ᭧ 2004 Entomological Society of America April 2004 COSTAMAGNA AND LANDIS:FOOD RESOURCES IMPACT ARMYWORM PARASITOIDS 129 number of hosts parasitized, and proportion of time Materials and Methods searching for hosts instead of food (Lewis et al. 1998, . Colonies of G. militaris and M. communis Tscharntke 2000, Heimpel and Jervis 2004). Access to food resources also could interact with were initiated from P. unipuncta larvae recovered from other factors that affect longevity and fecundity of cornÞelds in Ingham County, Michigan, during the parasitoids. Mating status and host availability can 2000 and 2001 growing season, respectively. Adult affect adult parasitoid longevity (Godfray 1994, parasitoids were provided with solutions of 50% honey Michaud 1994, Lei et al. 1997, Jacob and Evans 2000), in distilled water and distilled water alone. The Þrst as can microclimatic conditions, especially tempera- laboratory generation was used for G. militaris exper- ture and relative humidity (Dyer and Landis 1996). iments, and the Þrst and second for M. communis High temperatures tend to reduce longevity, experiments. A colony of P. unipuncta from larvae particularly under high relative humidity in which the provided by the United States Department of Agri- culture-Agricultural Research Service Corn Insects potential for evaporative cooling is reduced (Chap- Downloaded from https://academic.oup.com/ee/article/33/2/128/375331 by guest on 29 September 2021 man 1998). Temperatures above the species optimum and Crop Genetics Research Unit (Iowa State Uni- reduce parasitoid longevity (Dyer and Landis 1996, versity, Ames, IA) was maintained and used as host for Jervis and Copland 1996). each parasitoid species. P. unipuncta larvae were fed Marino and Landis (1996) and Menalled et al. (1999, with an artiÞcial diet based on pinto bean (Costamag- 2003) demonstrated that parasitism of the armyworm, na 2002), and occasionally provided with fresh corn Pseudaletia unipuncta (Haworth) (Lepidoptera: Noc- leaves grown in a greenhouse. Adult moths were pro- tuidae), in Michigan can differ between landscapes of vided with distilled water, a sugar solution (30% beer different structural complexity. Two braconid and 20% honey in distilled water, and 7.5 g ascorbic dominate the parasitoid community of P. unipuncta in acid per 747 ml of solution), and folded paper strips to these studies: Glyptapanteles militaris (Walsh) and induce oviposition. Colonies were maintained at 24ЊC, Meteorus communis (Cresson). Both are generalist, 60% RH, and a 16:8 (L:D)-h photoperiod. native, koinobiont endoparasitoids that mainly attack Effects of Food Resources, Male Presence, and Tem- noctuid larvae (Tower 1915, Rolim 1983, Krombein et perature on Longevity of Adult G. militaris. We mea- al. 1979, West 1988, West and Miller 1989, Marino and sured the longevity of adult females with and without Landis 1996, Costamagna 2002). G. militaris has been males at 20 and 25ЊC, provided with either honey- reported as the most important parasitoid of P. water or water alone, or with neither food nor water unipuncta in several North American studies (Breel- (control). Containers with solitary females were in- and 1958, Calkins and Sutter 1976, Steinkraus et al. cluded as a control for the effect of males on female 1993), including Michigan (Untung 1978, Rolim 1983, longevity (Jervis and Copland 1996). Newly emerged Costamagna 2002, Menalled et al. 2003). It is a gre- adult G. militaris were placed in ventilated 500-ml garious parasitoid, producing 40Ð82 larvae per host on plastic cups and randomly arranged in pairs of one average, depending on the stage parasitized (Oliveira female and one male. Ten containers with male and et al. 1999). Most studies of this species focused on female pairs and 15 containers with females alone determining its potential as a biological control agent, were then randomly assigned to each treatment. Food and relatively little has been reported regarding its and water were offered to wasps inside the 500-ml basic biology. Fecundity of G. militaris under differ- container via 30-ml plastic cups (Solo Cup Company, ent conditions of temperature, host , and host Urbana, IL) with cotton wicks through their lids. To diet has been reported (Calkins and Sutter 1976; Ol- avoid fungal growth, cups with food resources were iveira et al. 1998, 1999; Reis et al. 2003). It has also been replaced once per week. shown that access to carbohydrates increased G. mili- taris adult longevity (Calkins and Sutter 1976), while Three food resource treatments were tested. The high temperature (35ЊC) killed G. militaris larvae in- honey-water treatment consisted of one cup Þlled side its host and reduced female fecundity (Kaya and with honey diluted in distilled water (50% by volume; Tanada 1969). M. communis is a solitary species, with hereafter honey treatment), and a second cup Þlled most reports concerned with its Þeld abundance (Bur- with distilled water. The water treatment consisted of butis and Stewart 1979; West and Miller 1989; Marino two cups Þlled with distilled water. Finally, a control and Landis 1996; Menalled et al. 1999, 2003; Costama- of no food or water consisted of two empty cups. Two gna 2002) and immature development (West 1988, temperature regimes were compared simultaneously Ϯ Њ Ϯ West and Miller 1989, Miller 1996). No data have been in different growth chambers: 20.1 0.5 C, and 25.0 Њ Ϯ reported regarding its longevity or use of adult food 0.2 C (mean SD). Relative humidity differed resources. slightly between temperature regimes: 62.8 Ϯ 4.0% The objective of this study was to determine the and 77.8 Ϯ 4.8% (mean Ϯ SD), at 20 and 25ЊC, re- effect of food resources on adult G. militaris and M. spectively. The same photoperiod of 16:8 (L:D) h was communis. SpeciÞcally, we tested the effects of: 1) used in both growth chambers. Temperature and rel- food resources and temperature on the longevity of ative humidity inside the 500-ml containers were mea- male and female G. militaris; 2) food resources, hosts, sured and compared with conditions inside the growth and mating on the longevity and fecundity of female chamber to control for any microclimate difference M. communis; and 3) food resources on the longevity among treatments. Adult survivorship was assessed of male M. communis. twice per day, in the morning and evening. Insects 130 ENVIRONMENTAL ENTOMOLOGY Vol. 33, no. 2 that did not move when touched were considered mate the effect of food resources on parasitoid fecun- dead. dity, a surplus of hosts must be provided (Jervis and Experimental Design and Data Analysis. Microcli- Copland 1996). However, no data were available con- mate conditions of temperature and relative humidity cerning daily fecundity of M. communis using P. were compared among treatments as Þxed effects us- unipuncta as host. Previous studies used Ͻ10 hosts per ing a completely randomized analysis of variance female per day to estimate parasitism by M. communis (ANOVA) (PROC MIXED, SAS Institute 2001). Two (West 1988, Miller 1996). We provided an equal num- separate three-way factorial ANOVA tests with Þxed ber of hosts to each female each day based on what our effects were performed (PROC MIXED, SAS Institute armyworm colony could provide. Females were pro- 2001). In the Þrst one, we tested the effects of tem- vided an average of 17.8 Ϯ 1.3 (mean Ϯ SD) host perature, food, and sex on the longevity of adult cou- larvae per day during the Þrst 3Ð7 d of life. This rate ples reared in the same cage. In the second one, we was subsequently reduced, because our results indi- tested the effects of temperature, food, and male pres- cated that females seldom parasitized more than 10 Downloaded from https://academic.oup.com/ee/article/33/2/128/375331 by guest on 29 September 2021 ence on the longevity of females. Independent vari- hosts per day (1.5% of cases). From 4Ð8 to 22Ð27 d, ances were estimated for each food treatment to avoid females were provided with 13.5 Ϯ 1.3 hosts per day. heterogeneity of variance effects, and the suitability of Finally, 8.4 Ϯ 1.7 hosts per day were provided for the these models was assessed using the ratio likelihood rest of female life. Four replicates were conducted Ͻ test (P 0.05, PROC MIXED, SAS Institute 2001). To using this protocol with females of the Þrst laboratory meet the assumption of normality, longevity data were generation. A second group of four replicates was transformed (ln [x]) before analysis (Sokal and Rohlf conducted with the second laboratory generation of 1995). Means were separated using least square means females and was provided with 8.8 Ϯ 2.6 hosts per day (LSM) differences (PROC MIXED, SAS Institute all life. 2001). For all experiments, all values are reported in Ϯ Second to fourth were used, because previ- the original scale of measure as mean SE, unless ous studies indicated these were most likely to be otherwise indicated. accepted as hosts (West and Miller 1989; Marino and A priori predictions were that adults would live for Њ Landis 1996, Menalled et al. 1999, 2003). Larvae were fewer days at 25 than at 20 C, that honey provision placed on a rectangular piece (7 ϫ 5 ϫ 1 cm) of would increase the longevity of adults under both artiÞcial diet in an open plastic petri dish. In addition, temperature conditions, and that water would en- a piece of fresh corn leaf (9 ϫ 5 cm) was included to hance adult survivorship, especially at the highest provide host plant cues. Diet was replaced as needed, temperature. In addition, we predicted that females and the corn leaf was renewed daily. Every 24 h larvae would live longer than males, and that the presence of were replaced, and those exposed to parasitoids were males would reduce female longevity. All effects were reared in 30-ml plastic cups with paper lids (Bio-serve, predicted to be less pronounced in the absence of Ϸ honey. Frenchtown, NJ), containing 10 ml of artiÞcial diet. Effects of Food Resources, Host Availability, and Larvae were checked periodically until death, - Mating Status on Female M. communis Longevity and tion, or emergence of the parasitoids. Diet for larvae Fecundity. We conducted an experiment that simul- was replaced as needed, typically once per week. taneously compared the effects of access to honey, Initial attempts to rear the larvae in groups of three or hosts, and males on the longevity and fecundity of M. two larvae per cup were substituted by individual communis females. In addition, we conducted a second rearing after observation of cannibalism. experiment to estimate the fraction of hosts that were Mating Status Treatment. Newly emerged females parasitized, but died before parasitoid emergence. Ex- were randomly assigned to a male during the Þrst 24 h periments were conducted at 24ЊC, 60% RH, and 16:8 (mating treatment) or were withheld from males (no (L:D) photoperiod, and survivorship of adults was mating treatment). M. communis mating occurs within checked daily. 30 min of male contact with virgin females (West Food Resource Treatment. Newly emerged M. com- 1988), and in preliminary trials we observed that males munis females were reared in 3.8-liter plastic contain- typically copulate with females immediately after in- ers (22 ϫ 14 ϫ 14 cm) with three openings closed by troduction into containers. However, some females a Þne polyester mesh no-see-um netting (Kaplan-Si- that were paired with males produced only male prog- mon Co., Braintree, MA) to allow air interchange. eny, indicating either that mating did not occur or was After 24 h with only distilled water provided, mated insufÞcient to allow production of fertilized eggs. and virgin females (see below) were randomly as- Based on this post hoc information, the category of signed to receive honey or water, following the meth- mated females was divided in two categories for anal- odology described for G. militaris. Because parasitoids ysis, resulting in a total of three mating conditions for are not typically water deprived in the Þeld (Dyer and females that had access to hosts. Females that had Landis 1996), the no food and no water treatment was access to males, but produced only male offspring, not included to reduce the number of treatment com- were grouped in a separate category, hereafter called binations. unsuccessfully mated. Females that had access to Host Availability Treatment. After an initial 24 h, males and produced both male and female offspring females were randomly assigned to receive a daily are referred as successfully mated. Finally, those that provision of P. unipuncta larvae or no hosts. To esti- never contacted males are termed unmated. April 2004 COSTAMAGNA AND LANDIS:FOOD RESOURCES IMPACT ARMYWORM PARASITOIDS 131

Larval Mortality and Parasitism. In the previous tions. It was also expected that mating would decrease experiment, we did not dissect dead larvae to establish female longevity in conditions of food absence and the occurrence of parasitism. Therefore, we con- host availability. Honey provision was expected to ducted a second experiment to assess the fraction of increase total and daily fecundity, while the absence parasitized host larvae that died before parasitoid of carbohydrate resources and absence of mating were emergence. In addition, we compared the mortality of predicted to delay reproduction. host larvae exposed to M. communis females versus Effects of food resources, host access, and mating larvae without parasitoid contact. Newly emerged fe- status on female longevity were compared using a males were placed in containers, as previously de- three-way factorial ANOVA with Þxed effects (PROC scribed, and provided water, honey-water, and two MIXED, SAS Institute 2001). Effects of food resources males (Ͼ1 d old). After 3Ð6 d, males were removed, and mating status on total fecundity were assessed and 20 second to third instar hosts were provided using a two-way factorial ANOVA with Þxed effects

without artiÞcial diet to minimize the potential of a (PROC MIXED, SAS Institute 2001). Daily fecundity Downloaded from https://academic.oup.com/ee/article/33/2/128/375331 by guest on 29 September 2021 physical refuge. The experiment was conducted for was estimated as the proportion of P. unipuncta larvae 72 h, and hosts were replaced daily and reared in parasitized per female per day, and analyzed by lo- individual cups, as previously described. The parasit- gistic regression using the logit link function and a ism level of larvae that died before parasitoid emer- binomial distribution (SAS GLIMMIX macro, Littell gence was assessed by dissection of a random sample et al. 1996). Food resources and mating status treat- (n ϭ 98, 39% of the dead larvae). Background larval ments were assigned in a two-way factorial design with mortality was assessed by including a set of control Þxed effects. The same model was used to estimate the host larvae (no ), randomly assigned to each effects of treatments on the proportion of P. unipuncta block. larvae missing because of cannibalism and larval mor- Experimental Design and Data Analysis. The Þrst tality, to establish absence of bias in the data. To avoid experiment was conducted in a complete randomized heteroscedasticity, independent variances were esti- block design, using starting day as the blocking factor. mated for each food treatment, and the suitability of Food resources, host access, and mating status were this model was assessed using the ratio likelihood test combined to produce eight treatments replicated in (P Ͻ 0.05, PROC MIXED, SAS Institute 2001), except four blocks: 1) honey ϩ hosts ϩ mating, 2) water ϩ for data of the prereproductive female period, which hosts ϩ mating, 3) honey ϩ no host ϩ mating, 4) water was previously transformed using (ln [x ϩ 1]) (Sokal ϩ no host ϩ mating, 5) honey ϩ hosts ϩ no mating, and Rohlf 1995). NonsigniÞcant block effects were 6) water ϩ hosts ϩ no mating, 7) honey ϩ no hosts ϩ removed from models. SigniÞcant interactions were no mating, and 8) water ϩ no host ϩ no mating. investigated by slicing by main effects to detect sig- Treatments 1Ð4 were replicated in four additional niÞcant differences between treatments at this level blocks, for a total of eight replicates. A total of 48 M. (Kuehl 2000). Treatments were separated within main communis females were reared, and 5,948 larvae of P. effects by comparing the marginal means using the unipuncta were used as hosts. LSM difference (PROC MIXED, SAS Institute 2001, The following responses to treatments were mea- Kuehl 2000). The effect of the different numbers of sured: female longevity (in days), total and daily fe- host larvae offered on the proportion of hosts para- cundity (estimated as number of hosts parasitized), sitized per day was assessed using simple linear re- prereproductive period (number of days before Þrst gression analysis (PROC REG, SAS Institute 2001). reproduction), number of days necessary to achieve The experiment to determine host mortality and half of total reproduction, and proportion male off- parasitism was conducted in completely randomized spring. Differences in total fecundity could be caused blocks, using female day of emergence as blocking by either: 1) differences in longevity, or 2) differences factor, for a total of 15 replicates. We estimated the in daily fecundity. To test differences in daily fecun- percentage of parasitized hosts that died before para- dity, the proportion of P. unipuncta larvae parasitized sitoid emergence, the percentage of mortality of host (number of larvae parasitized/number of larvae of- larvae, and percentage of parasitism per female per fered) was compared among treatments. Daily fecun- day. We expected to obtain similar levels of mortality dity was calculated for all females during the time between larvae exposed to wasps and control larvae. interval in which water-fed females were alive. The We also predicted that parasitism would increase with use of this period avoided underestimation of honey- time, because of wasp acclimation and/or learning. fed female rate of fecundity because of a decline in the The number of hosts parasitized was compared among rate of parasitism with female age, absent in water-fed the 3 consecutive days using a one-way ANOVA females (Costamagna 2002). To avoid potential bias, (PROC MIXED, SAS Institute 2001). parasitism values when less than 10 host larvae were Effect of Food Resources on Male M. communis provided were not included in the daily fecundity Longevity. Newly emerged males were placed under results, but were included in total parasitism. conditions as described for females, and allowed ac- We predicted an increase in longevity with honey cess to a female (Ͼ1 d old). After 24 h, females were provision and also in the absence of hosts and mating, removed and males randomly assigned to honey or based on the trade-off between longevity and repro- water treatments, following the same protocol as for duction (Roff 1992). In addition, host access was ex- females. Twenty-two replicates per treatment were pected to decrease female longevity, under all condi- conducted. We predicted that honey access would 132 ENVIRONMENTAL ENTOMOLOGY Vol. 33, no. 2

(Table 1. Results of tests for effects of three food resources (honey ؉ distilled water, distilled water alone, and neither honey nor water and two conditions of temperature (20 and 25°C) on G. militaris adult longevity

a) Females and males b) Females with or without males Source of variation df FP df FP Temperature 1, 25 9.29 0.01 1, 66 15.97 Ͻ0.01 Food resources 2, 29 37.51 Ͻ0.01 2, 83 100.49 Ͻ0.01 Sex (a) or male presence (b) 1, 23 5.70 0.03 1, 66 1.51 0.22 Temperature ϫ Food 2, 29 1.84 0.18 2, 83 3.06 0.05 Temperature ϫ sex (a) or male presence (b) 1, 23 0.27 0.61 1, 66 0.09 0.77 Food ϫ Sex (a) or male presence (b) 2, 27 1.64 0.21 2, 83 1.39 0.25 Temperature ϫ food ϫ sex (a) or male presence (b) 2, 27 0.76 0.48 2, 83 0.88 0.42 extend male longevity. Longevity was contrasted be- those with no resources (except for males reared at Downloaded from https://academic.oup.com/ee/article/33/2/128/375331 by guest on 29 September 2021 tween honey-fed and water-fed males using a one-way 25ЊC), but only by a mean increase of 1.3Ð0.5 d for ANOVA (PROC MIXED, SAS Institute 2001). females, and Ͻ0.5 d for males (Fig. 1). Across all treatments, females lived signiÞcantly longer than males, with female longevity approximately twice that Results of males when honey was available (Table 1a [sex Effects of Food Resources, Male Presence, and Tem- effect]; Fig. 1). The presence of males did not affect perature on Longevity of Adult G. militaris. Temper- female longevity under any food treatment or tem- ature and relative humidity did not differ signiÞcantly perature condition (Table 1b [male presence effect]; among rearing containers provided with different Fig. 1). No signiÞcant interactions of these three main food treatments (20ЊC growth chamber: temperature, effects were found, except for temperature ϫ food F ϭ 0.28; df ϭ 3, 12; P ϭ 0.84; RH, F ϭ 0.34; df ϭ 3, 12; (Table 1b), because of the absence of difference in the P ϭ 0.80; and 25ЊC growth chamber: temperature, F ϭ longevity between females and solitary females pro- 2.01, df ϭ 3, 11; P ϭ 0.17; RH, F ϭ 2.19; df ϭ 3, 12; P ϭ vided with water (test slicing by food treatment, F ϭ 0.14). Both males and females lived signiÞcantly 2.24; df ϭ 1, 42; P ϭ 0.14). longer at 20 than 25ЊC (Table 1 [temperature effects]; Effects of Food Resources, Host Availability, and Fig. 1). Access to honey signiÞcantly increased lon- Mating Status on Female M. communis Longevity and gevity over the other food resources, by approximately Fecundity. A post hoc analysis showed that cannibal- 3-fold at 20ЊC (20.3 Ϯ 4.0 d) and 2-fold at 25ЊC (7.7 Ϯ ism and larval mortality were not differentially asso- 2.7, Table 1 [food resources effects]; Fig. 1). Water ciated with speciÞc treatments. Treatments did not signiÞcantly improved the survivorship of adults over differ in the level of cannibalism (food resources, F ϭ 0.05; df ϭ 1, 12; P ϭ 0.83; mating status, F ϭ 0.04; df ϭ 1, 12; P ϭ 0.84; and food ϫ mating interaction, F ϭ 0.05; df ϭ 1, 12; P ϭ 0.82) or larval mortality (food resources, F ϭ 0.06; df ϭ 1, 18; P ϭ 0.81; mating status, F ϭ 0.00; df ϭ 1, 18; P ϭ 0.96; and food resources ϫ mating status interaction, F ϭ 0.00; df ϭ 1, 18; P ϭ 0.97). In addition, the higher number of hosts provided initially in blocks 1Ð4 explained only 6% of the increase in parasitism (regression for larvae parasitized and number of lar- vae offered, R2 ϭ 0.06; F ϭ 13.85; df ϭ 1, 228; P Ͻ 0.01). Thus, our results were robust against potential bias introduced by host larvae cannibalism and mortality, and variation in the number of hosts provided daily. Exposure to males during the Þrst 24 h of life did not affect female longevity nor interact with other treat- ments (Table 2 [mating status effect, mating status interaction terms]). Therefore, slicing by main effects was performed without mating status in the model. Access to honey signiÞcantly increased female lon- gevity (Table 2 [food resources effect]), independent of host availability (slicing by with hosts, F ϭ 103.38; ϭ Ͻ ϭ ϩ df 1, 23.7; P 0.01; slicing by without hosts, F Fig. 1. Longevity (mean SE) of G. militaris adults 193.43; df ϭ 1, 23.7; P Ͻ 0.01) or mating status (Table under three food resource treatments (honey ϩ distilled ϫ water, distilled water alone, and control of neither honey nor 2 [food resources mating status]; Fig. 2). In contrast, water), under (A) 20ЊC and (B) 25ЊC temperature regimes. access to host larvae signiÞcantly reduced female lon- Columns with different letters differed signiÞcantly within gevity when honey was provided (Table 2 [hosts ef- adult category (P Ͻ 0.05, LSM difference). Males and females fect], slicing by honey, F ϭ 7.36; df ϭ 1, 22; P ϭ 0.01), were reared together in pairs. but had no effect on females provided only water April 2004 COSTAMAGNA AND LANDIS:FOOD RESOURCES IMPACT ARMYWORM PARASITOIDS 133

Table 2. Results of the test for effects of food resources Honey increased fecundity for all mating conditions honey ؉ distilled water or distilled water alone), host access (hosts (main effect, F ϭ 52.15; df ϭ 1, 10.4; P Ͻ 0.01; slicing) versus no host access), and mating status (initial access to males or ϭ ϭ Ͻ no access) on the longevity of M. communis females by successfully mated, F 34.85; df 1, 9.87; P 0.01; slicing by unsuccessfully mated females, F ϭ 19.02; Source of variation df FPdf ϭ 1, 3.84; P Ͻ 0.01), but was only marginally sig- Block 7, 13.3 2.94 Ͻ0.04 niÞcant for unmated females (slicing by unmated fe- Food resources 1, 20.3 238.71 Ͻ0.01 males, F ϭ 4.29; df ϭ 1, 10.4; P ϭ 0.06). Hosts 1, 20.3 6.34 0.02 Honey did not increase daily fecundity, but signif- Food resources ϫ hosts 1, 20.3 6.47 0.02 icant differences were found among mating condi- Mating status 1, 21.4 1.13 0.30 ϭ ϭ ϭ Food resources ϫ mating status 1, 20.3 2.95 0.10 tions (food resources, F 1.19; df 1, 18; P 0.29; Hosts ϫ mating status 1, 20.3 0.00 0.99 mating status, F ϭ 3.50; df ϭ 2, 18; P ϭ 0.05; and food Food resources ϫ hosts ϫ mating status 1, 20.3 0.03 0.87 resources ϫ mating status interaction, F ϭ 1.98; df ϭ ϭ

2, 18; P 0.17). Successfully mated females parasitized Downloaded from https://academic.oup.com/ee/article/33/2/128/375331 by guest on 29 September 2021 32.9 Ϯ 4.4% of the hosts offered per day, and differed (slicing by water, F ϭ 0.01; df ϭ 1, 22; P ϭ 0.93; Fig. 2). signiÞcantly from unmated females that only parasit- Longevity of females reclassiÞed as unmated, success- ized 17.0 Ϯ 3.4% (LSM difference, t ϭ 2.64, P ϭ 0.02, fully mated, and unsuccessfully mated was also signif- n ϭ 8), while unsuccessfully mated females showed an icantly inßuenced by food resources (F ϭ 178.88; df ϭ intermediate value of 22.1 Ϯ 8.1% of the hosts offered 1, 10.4; P Ͻ 0.01), but not by mating status (F ϭ 0.66; per day, and did not differ from the other two. df ϭ 2, 10.5; P ϭ 0.54; food resources ϫ mating status We observed a signiÞcant delay in reproduction by interaction, F ϭ 1.76; df ϭ 2, 10.5; P ϭ 0.22). Females females offered honey (3.42 Ϯ 0.87 d) compared with provided with honey lived signiÞcantly longer than those provided water alone (1.58 Ϯ 0.19 d; F ϭ 3.93; those provided only water, under all three mating df ϭ 1, 18; P ϭ 0.05). Mating status did not affect this conditions. delay (F ϭ 0.18; df ϭ 2, 18; P ϭ 0.84). Also, we did not Total female fecundity was not affected by initial observe a signiÞcant interaction between food re- contact with males, and this condition did not interact sources and mating status (F ϭ 0.29; df ϭ 2, 18; P ϭ signiÞcantly with any other treatment (data not 0.75). Successfully mated females required 18.3 Ϯ 2.2 d shown). However, when females were reclassiÞed by (0.45 of life span), unsuccessfully mated females mating status, we observed a signiÞcant effect on fe- 19.8 Ϯ 1.7 d (0.46 of life span), and unmated females cundity (F ϭ 3.91; df ϭ 2, 10.5; P ϭ 0.05) and a 14.5 Ϯ 2.7 d (0.41 of life span) to lay half of their viable signiÞcant interaction with the effect of food re- offspring, differences that were not statistically sig- sources (F ϭ 4.70; df ϭ 2, 10.5; P ϭ 0.03; Fig. 3). Slicing niÞcant (F ϭ 0.18; df ϭ 2, 9; P ϭ 0.84). Females fed by food resources revealed that mating status only exclusively with water died before becoming pos- affected the fecundity of females provided with honey treproductive, whereas females fed with honey lived (slicing by honey, F ϭ 4.56; df ϭ 2, 9; P ϭ 0.04; slicing 5.5 Ϯ 4.8 d (mean Ϯ SD) without producing viable by water, F ϭ 0.21; df ϭ 2, 9; P ϭ 0.81). Successfully offspring before death. Of those females initially mated females produced signiÞcantly more offspring paired with males, proportionally more fed with than unmated females, while unsuccessfully mated honey did not successfully mate (0.625, n ϭ 8) than females were intermediate in fecundity (Fig. 3). those fed with water (0.325, n ϭ 8). The proportion of

Fig. 2. Longevity of M. communis females under different food resource treatments (honey ϩ distilled water and a control of distilled water alone), host access (hosts present or no hosts present), and mating status (initial access to males or no access). 134 ENVIRONMENTAL ENTOMOLOGY Vol. 33, no. 2 Downloaded from https://academic.oup.com/ee/article/33/2/128/375331 by guest on 29 September 2021

Fig. 3. Fecundity (number of P. unipuncta larvae parasitized per female throughout life) of M. communis females provided with different food resources (honey ϩ distilled water or a control of distilled water alone) and mating status (successfully mated, unsuccessfully mated, or unmated). Columns with different letters differed signiÞcantly within food resource treatments (P Ͻ 0.05, LSM difference). males produced by mated females (n ϭ 8) did not low 30s ЊC; Dyer and Landis 1996) probably are not differ signiÞcantly between females fed with honey favorable for this parasitoid species. The importance (0.66 Ϯ 0.18 males) and females fed with water alone of habitats with milder conditions surrounding corn- (0.51 Ϯ 0.09 males, F ϭ 0.68; df ϭ 1, 6; P ϭ 0.44). Þelds was demonstrated for Eriborus terebrans (Hy- Larval Mortality and Parasitism. Seven of the 15 menoptera: Ichneumonidae), a parasitoid with similar females tested produced offspring. Postmortem dis- temperature constraints as G. militaris (Dyer and Lan- section of larvae that died before parasitoid emer- dis 1996). gence revealed that 11.2% were parasitized. Mortality The prediction that honey would increase longevity of P. unipuncta larvae exposed to M. communis did not of G. militaris adults was also supported by this ex- differ from control larvae (F ϭ 3.33; df ϭ 1, 7.91; P ϭ periment. Calkins and Sutter (1976) reported that G. 0.11). Female daily fecundity was highly variable and militaris females provided with fresh halved grapes as did not increase with time (F ϭ 0.45; df ϭ 2, 18; P ϭ a carbohydrate source lived an average of 3 d more 0.64). An average of 2.7 Ϯ 3.3 (Ϯ SD) larvae were than those without food resources. When G. militaris parasitized per day, with a maximum of 11 larvae was provided with 10% honey diluted in water, at 22ЊC, parasitized per day (4.5% of the cases). These results 75% RH, and a photoperiod of 16:8 (L:D) h, Reis et al. indicate that in the previous experiment parasitism (2003) observed longevity within the range of our was likely to be only slightly underestimated (11.2% of results. As predicted, male longevity was shorter than the 3.3% that died before parasitoid emergence), that that of females when honey was provided, similar to P. unipuncta larvae mortality is independent of female the results of Reis et al. (2003). This trend has been oviposition, and that 10 hosts per day were sufÞcient shown for many species of Hymenoptera parasitoids to obtain accurate estimates of daily parasitism. (Quicke 1997). Effect of Food Resources on Male M. communis Frequent mating can reduce life span in both male Longevity. The longevity of mated males was signiÞ- and female insects (van den Assem 1986); however, cantly improved by access to honey. Males provided we did not observe an effect of males on G. militaris with honey lived 26.2 Ϯ 2.6 d in contrast to water-fed female longevity. Although G. militaris was reported males that only lived 4.6 Ϯ 0.6d(F ϭ 67.48; df ϭ 1, 21; to mate several times in consecutive days (Tower P Ͻ 0.01). 1915), and we observed successful mating in our col- ony under similar conditions, we did not check the occurrence of mating in our experiment. Therefore, Discussion we cannot reject the possibility that the absence of an Our results support the prediction of a reduction in effect on female longevity was caused by an absence G. militaris adult longevity at higher temperature. G. or reduction of mating. Previous studies with G. mili- militaris adults exposed to 25ЊC lived half as long as taris reported a male-skewed progeny, indicating a those at 20ЊC, suggesting that the optimal temperature possible mating reduction (Oliveira et al. 1998, 1999; for this species is Ͻ25ЊC. This result is consistent with Reis et al. 2003). prior studies that showed greater longevity of G. mili- Honey dramatically increased the longevity and fe- taris at lower temperatures (Calkins and Sutter 1976, cundity of M. communis. Thireau and Re´gnie`re (1995) Oliveira et al. 1998). Prevailing maximum tempera- observed similar longevities (22.0 and 23.8 d for males tures in southern Michigan cornÞelds (high 20s and and females, respectively) and higher fecundity (194.2 April 2004 COSTAMAGNA AND LANDIS:FOOD RESOURCES IMPACT ARMYWORM PARASITOIDS 135 eggs per unmated female) for M. trachynotus (Vier.), had similar egg loads (Jervis and Copland 1996). Stud- which was provided with a 10% honey-water solution. ies of other parasitoids, however, have not revealed Bautista et al. (2001) found a reduction in the number differences in fecundity of mated and unmated fe- of eggs produced by females of the braconid Fopius males (Jervis and Copland 1996, Sousa and Spence arisanus (Sonan) deprived of honey. Similarly, fe- 2000). males of the pteromalid Nasonia vitripennis (Walker) In arrhenotokous parasitoids such as G. militaris and fed honey (30% honey in water) showed an increase M. communis, virgin females produce only males in mature eggs 72 h after emergence (Rivero and West (Quicke 1997). Berndt et al. (2002) found a decrease 2002). In our study, the proportion of hosts parasitized in the proportion of Dolichogenidea tasmanica (Hy- per day was not greater for honey-fed females, indi- menoptera: Braconidae) males in plots provided with cating the increase in total parasitism caused by honey nectar resources. In our study, the proportion of male provision was a consequence of an increase in female offspring did not differ signiÞcantly in honey-fed and

longevity and not in fecundity. However, because water-fed females, but rather showed the opposite Downloaded from https://academic.oup.com/ee/article/33/2/128/375331 by guest on 29 September 2021 solitary braconid parasitoids are able to lay more than trend, a higher proportion of male offspring from hon- one egg per host (Wharton 1993), it is possible that by ey-fed females. Unsuccessfully mated M. communis assessing the number of parasitized hosts we under- females had an intermediate level of fecundity and estimated the potential fecundity of M. communis. rate of parasitization. Mated parasitoid females that We observed accelerated oviposition in food-de- receive nonviable sperm or have blocked spermathe- prived females, in contrast to honey-fed females that cal ducts caused by multiple matings also produce only exhibited more selective oviposition behavior, result- male progeny (Godfray 1994). Therefore, one possi- ing in fewer parasitized hosts initially. Increased ovi- ble explanation is that females received nonviable position in response to stress has been documented for sperm and used it as a source of energy to increase Leptopilina heterotoma (Hymenoptera: Eucoilidae) reproductive output over unmated females. Alterna- under conditions of low life expectancy (late in the tively, contact with males could elicit a higher rate of season) and low barometric pressure (increased risk oviposition, although fewer eggs were available for of mortality) (Roitberg et al. 1992, 1993). Olson et al. oviposition compared with mated females. Further (2000) obtained similar results for sugar-starved fe- research is necessary to elucidate the mechanism be- males of Macrocentrus grandii (Hymenoptera: Bra- hind this response. conidae) and suggest that the increase in the number The shorter life span and gregarious reproductive of mature eggs as a response to low life expectancy strategy of G. militaris suggest a possible mechanism may be a strategy that enhances opportunities for of egg limitation (Heimpel 2000). Successful repro- reproduction. However, because we did not measure duction of this parasitoid might be less dependent on egg load, we cannot assess whether this reduction was availability of food resources in close proximity to its caused by a decrease in the production of eggs or a hosts, because it should produce high levels of para- change in the oviposition behavior of the females. sitism in a short time. This is supported by the negative A trade-off between female reproduction and lon- response of this parasitoid to host density under Þeld gevity predicts a reduction in the life span of females conditions (Costamagna 2002). In addition, a recent that allocate resources to reproduction (Roff 1992). study on the braconid Macrocentrus grandii indicates Accordingly, access to hosts signiÞcantly reduced M. that sporadic (i.e., every 2Ð4 d) and continuous access communis female longevity. Females of the braconid to carbohydrate resources provides similar beneÞt to Cotesia melitaearum (Wilkinson) provided fresh ßow- longevity and fecundity (Fadamiro and Heimpel ers but prevented from contacting hosts, lived longer 2001). Conversely, M. communis is a solitary species than those allowed to parasitize hosts (Lei et al. 1997). with lower daily fecundity and higher longevity, sug- The same trend was observed for M. trachynotus fe- gesting a possible host limitation mechanism (Heim- males (Thireau and Re´gnie`re 1995). Mating stimulates pel 2000). Therefore, parasitism by this species could reallocation of resources from maintenance to oogen- be affected by the presence of adult food resources in esis and egg maturation (Jacob and Evans 2000), close proximity to its host larvae. Under Þeld condi- which could lead to a reduction in female longevity tions, this species parasitized proportionally more under conditions of low food quality. In contrast, it hosts in high host density patches (Costamagna 2002). may not have any effect when food quality is high, as Food resources dramatically increased longevity of shown for the ichneumonid Bathyplectes curculionis G. militaris under different temperature conditions, (Jacob and Evans 2000). In our study, mating did not and longevity and fecundity of M. communis under affect M. communis longevity, with or without the varying conditions of host access and mating status. provision of a carbohydrate resource. Therefore, an increase of carbohydrate resources in Total fecundity and rate of oviposition were greater the Þeld could increase the level of parasitism pro- for mated than unmated M. communis females. Higher duced by both parasitoid species. Moreover, we can numbers of hosts parasitized by mated than unmated further hypothesize that an increase in habitat com- females also have been reported for several parasitoid plexity, with its concomitant increase in food re- species (Michaud 1994), such as the braconid Cotesia sources (Landis et al. 2000), might be more favorable glomerata (L.). Dissections of ovaries of C. glomerata to M. communis than to G. militaris. A general trend proved that it was a behavioral rather than a physio- toward this pattern of association between landscape logical change, because mated and unmated females complexity and M. communis and G. militaris has been 136 ENVIRONMENTAL ENTOMOLOGY Vol. 33, no. 2 shown by several Þeld studies (Marino and Landis Hochberg and A. R. Ives (eds.), Parasitoid population 1996; Menalled et al. 1999, 2003; Costamagna 2002). biology. Princeton University Press, Princeton, NJ. Heimpel, G. E., and M. A. Jervis. 2004. An evaluation of the hypothesis that ßoral nectar improves biological control by parasitoids. In F. Wa¨ckers, P. van Rijn, and J. Bruin Acknowledgments (eds.), Plant-provided food and plant-carnivore mutual- We thank M. E. OÕNeal, G. E. Heimpel, M. J. Brewer, and ism. Cambridge Academic, Cambridge, UK (in press). the three anonymous reviewers for their valuable comments Jacob, H. S., and E. W. Evans. 2000. Inßuence of carbohy- on the manuscript. Special thanks to A. Gould, S. Clay, M. E. drate foods and mating on longevity of the parasitoid OÕNeal, C. Hemming, M. Soto Rodriguez, K. Newhouse, D. C. Bathyplectes curculionis (Hymenoptera: Ichneumoni- Sebolt, T. B. Fox, F. D. Menalled, M. Burns, and M. Smith for dae). Environ. Entomol. 29: 1088Ð1095. their assistance with the experiments. We are indebted to L. Jervis, M. A., and M.J.M. Copland. 1996. The life cycle, pp. Lewis and J. Dyer, United States Department of Agriculture- 63Ð161. In M. Jervis and N. Kidd (eds.), Insect natural

Agricultural Research Service, for the provision of the ar- enemies, practical approaches to their study and evalu- Downloaded from https://academic.oup.com/ee/article/33/2/128/375331 by guest on 29 September 2021 myworms used to initiate our colonies, and all the support ation. Chapman & Hall, London, UK. made available to maintain the colonies throughout this Jervis, M. A., N.A.C. Kidd, M. G. Fitton, T. Huddleston, and study. We thank J. Luhman for providing conÞrmation of the H. A. Dawah. 1993. Flower-visiting by hymenopteran identity of the parasitoid species studied. Statistical advice parasitoids. J. Nat. Hist. 27: 67Ð105. was provided by K. Kizilkaya and F. Cardoso (Statistical Kaya, H. K., and Y. Tanada. 1969. Responses to high tem- Consulting Center of the College of Agriculture and National perature of the parasite Apanteles militaris and of its host, Resources Biometry group, Michigan State University). the armyworm, Pseudaletia unipuncta. Ann. Entomol. Soc. Funding for this work was provided by an Instituto Nacional Am. 62: 1303Ð1036. de Technologõ´a Agropecuaria-Fulbright fellowship to A.C.C. Krˇivan, V., and E. Sirot. 1997. Searching for food or hosts: and by the Michigan Agricultural Experiment Station. the inßuence of parasitoidsÕ behavior on host-parasitoid dynamics. Theor. Pop. Biol. 51: 201Ð209. Krombein, K. V., P. D. Hurd, D. R. Smith, and B. D. Burks. References Cited 1979. Catalog of Hymenoptera in America north of Mex- ico. Smithsonian Institution, Washington, DC. Bautista, R. C., E. J. Harris, and R. I. Vargas. 2001. The fruit Kuehl, R. O. 2000. Design of experiments, statistical prin- ßy parasitoid Fopius arisanus: reproductive attributes of ciples of research design and analysis, 2nd ed. Duxbury, pre-released females and the use of added sugar as a PaciÞc Grove, CA. potential food supplement in the Þeld. Entomol. Exp. Landis, D. A., and P. C. Marino. 1999. Landscape structure Appl. 101: 247Ð255. and extra-Þeld processes: impact on management of pests Berndt, L. A., S. D. Wratten, and P. G. Hassan. 2002. Effects and beneÞcials, pp. 79Ð104. In J. R. Ruberson (ed.), Hand- of buckwheat ßowers on leafroller (Lepidoptera: Tortri- book of pest management. Marcel Dekker, New York cidae) parasitoids in a New Zealand vineyard. Agric. Landis, D. A., and F. D. Menalled. 1998. Ecological consid- Forest Entomol. 4: 39Ð45. erations in conservation of parasitoids in agricultural Breeland, S. G. 1958. Biological studies on the armyworm, landscapes, pp. 101Ð121. In P. Barbosa (ed.), Conserva- Pseudaletia unipuncta (Haworth), in Tennessee (Lepi- tion biological control. Academic, San Diego, CA. doptera: Noctuidae). J. Tenn. Acad. Sci. 18: 263Ð347. Landis, D. A., S. T. Wratten, and G. M. Gurr. 2000. Habitat Bugg, R. L., R. T. Ellis, and R. W. Carlson. 1989. Ichneu- management to conserve natural enemies of monidae (Hymenoptera) using extraßoral nectar of Faba pests in agriculture. Annu. Rev. Entomol. 45: 175Ð201. Bean (Vicia faba L., Fabaceae) in Massachusetts. Biol. Lei, G. C., V. Vikberg, M. Nieminen, and M. Kuussaari. 1997. Agric. Hortic. 6: 107Ð114. The parasitoid complex attacking Finnish populations of Burbutis, P. P., and J. A. Stewart. 1979. Blacklight trap col- the Glanville fritillary Melitaea cinxia (Lepidoptera: lecting of parasitic Hymenoptera. Entomol. News 90: 17Ð Nymphalidae), an endangered butterßy. J. Nat. Hist. 31: 22. 635Ð648. Calkins, C. O., and G. R. Sutter. 1976. Apanteles militaris and Lewis, W. J., J. O. Stapel, A. M. Cortesero, and K. Takasu. its host Pseudaletia unipuncta: biology and rearing. Envi- 1998. Understanding how parasitoids balance food and ron. Entomol. 5: 147Ð150. host needs: importance to biological control. Biol. Con- Chapman, R. F. 1998. The insects, structure and function. Cambridge University Press, Cambridge, UK. trol 11: 175Ð183. Costamagna, A. C. 2002. Agricultural landscape complexity Littell, R. C., G. A. Milliken, W. W. Stroup, and R. D. has mixed effects on patterns of parasitoid abundance and Wolfinger. 1996. SAS system for mixed models. SAS In- diversity. M.S. thesis, Michigan State University, East stitute, Cary, NC. Lansing. Marino, P. C., and D. A. Landis. 1996. Effect of landscape Dyer, L. E., and D. A. Landis. 1996. Effects of habitat, tem- structure on parasitoid diversity in agroecosystems. Ecol. perature, and sugar availability on longevity of Eriborus Appl. 6: 276Ð284. terebrans (Hymenoptera: Ichneumonidae). Environ. En- Menalled, F. D., A. C. Costamagna, P. C. Marino, and D. A. tomol. 25: 1192Ð1201. Landis. 2003. Temporal variation in the response of Fadamiro, H. Y., and G. E. Heimpel. 2001. Effects of partial parasitoids to agricultural landscape structure. Agric. sugar deprivation on life span and carbohydrate mobili- Ecosyst. Environ. 96: 29Ð35. zation in the parasitoid Macrocentrus grandii (Hymenop- Menalled, F. D., P. C. Marino, S. Gage, and D. A. Landis. tera: Braconidae). Ann. Entomol. Soc. Am. 94: 909Ð916. 1999. Does agricultural landscape structure affect para- Godfray, H.C.J. 1994. Parasitoids: behavioral and evolution- sitism and parasitoid diversity? Ecol. Appl. 9: 634Ð641. ary ecology. Princeton University Press, Princeton, NJ. Michaud, J. P. 1994. Differences in foraging behaviour be- Heimpel, G. E. 2000. Effects of parasitoid clutch size on tween virgin and mated aphid parasitoids (Hymenoptera, host-parasitoid population dynamics, pp. 27Ð40. In M. E. Aphidiidae). Can. J. Zool. 72: 1597Ð1602. April 2004 COSTAMAGNA AND LANDIS:FOOD RESOURCES IMPACT ARMYWORM PARASITOIDS 137

Miller, J. C. 1996. Temperature-dependent development of Sokal, R. R., and F. J. Rohlf. 1995. Biometry, 3rd ed. Free- Meteorus communis (Hymenoptera: Braconidae), a para- man and Co., New York sitoid of the variegated cutworm (Lepidoptera: Noctu- Sousa, J. M., and J. R. Spence. 2000. Effects of mating status idae). J. Econ. Entomol. 89: 877Ð880. and parasitoid density on superparasitism and offspring Oliveira, L., R. Melo, and J. Tavares. 1998. Response of Þtness in Tiphodytes gerriphagus (Hymenoptera: Scelion- Glyptapanteles militaris (Walsh) (Hymenoptera: Bra- idae). Ann. Entomol. Soc. Am. 93: 548Ð553. conidae), a larval parasitoid of the armyworm, Mythimna Steinkraus, D. C., A. J. Mueller, and R. A. Humber. 1993. unipuncta (Haworth) (Lepidoptera: Noctuidae), to dif- Furia virescens (Thaxter) Humber (Zygomycetes: Ento- ferent temperatures. J. Hym. Res. 7: 268Ð273. mophthoraceae) infections in the armyworm, Pseudaletia Oliveira, L., R. Melo, and J. Tavares. 1999. Host age of Pseu- unipuncta (Haworth) (Lepidoptera: Noctuidae) in Ar- daletia unipuncta (Lepidoptera: Noctuidae) and parasitic kansas with notes on other natural enemies. J. Entomol. capacity of Glyptapanteles militaris (Hymenoptera: Bra- Sci. 28: 376Ð386. conidae). Environ. Entomol. 28: 513Ð517. Thies, C., and T. Tscharntke. 1999. Landscape structure and Olson, D. N., H. Fadamiro, J. G. Lundgren, and G. E. He- biological control in agroecosystems. Science 285: 893Ð impel. 2000. Effects of sugar feeding on carbohydrate 895. Downloaded from https://academic.oup.com/ee/article/33/2/128/375331 by guest on 29 September 2021 and lipid metabolism in a . Physiol. En- Thireau, J. C., and J. Re´gnie`re. 1995. Development, repro- tomol. 25: 17Ð26. duction, voltinism and host synchrony of Meteorus tra- Quicke, D.L.J. 1997. Parasitic wasps. Chapman & Hall, Lon- chynotus with its hosts Choristoneura fumiferana and C. don, UK. rosaceana. Entomol. Exp. Appl. 76: 67Ð82. Reis, J., L. Oliveira, and P. Garcia. 2003. Effects of the larval Tower, D. G. 1915. Biology of Apanteles militaris. J. Agric. diet of Pseudaletia unipuncta (Lepidoptera: Noctuidae) Res. 5: 495Ð507. on the performance of the parasitoid Glyptapanteles mili- Tscharntke, T. 2000. Parasitoid populations in the agricul- taris (Hymenoptera: Braconidae). Environ. Entomol. 32: tural landscape, pp. 235Ð253. In M. E. Hochberg and A. R. 180Ð186. Ives (eds.), Parasitoid population biology. Princeton Uni- Rivero, A., and S. A. West. 2002. The physiological costs of versity Press, Princeton, NJ. being small in a parasitic wasp. Evol. Ecol. Res. 4: 407Ð420. Untung, K. 1978. The distribution and bionomics of the ar- Roff, D. A. 1992. The evolution of life histories: theory and myworm, Pseudaletia unipuncta (Haw.) in Michigan. M.S. analysis. Chapman & Hall, London, UK. thesis, Michigan State University, East Lansing. Roitberg, B. D., M. Mangel, R. G. Lalonde, C. A. Roitberg, van den Assem, J. 1986. Mating behavior in parasitic wasps, J.J.M. van Alphen, and L. Vet. 1992. Seasonal dynamic pp. 137Ð167. In J. Waage and D. Greathead (eds.), Insect shifts in patch exploitation by parasitic wasps. Behav. parasitoids. Academic, New York Ecol. 3: 156Ð165. West, K. J. 1988. Biology and host relations of Meteorus com- Roitberg, B. D., J. Sircom, C. A. Roitberg, J.J.M. van Alphen, munis (Cresson). M.S. thesis, Oregon State University, and M. Mangel. 1993. Life expectancy and reproduc- Corvallis. tion. Nature 364: 108. West, K. J., and J. C. Miller. 1989. Patterns of host exploi- Rolim, A. E. 1983. Laboratory comparison of the potential tation by Meteorus communis (Hymenoptera: Bra- of Apanteles ruficrus Haliday and Apanteles militaris conidae). Environ. Entomol. 18: 537Ð540. Walsh (Hymenoptera: Braconidae) for control of the Wharton, R. A. 1993. Bionomics of the Braconidae. Annu. armyworm, Pseudaletia unipuncta (Haworth) (Lepidop- Rev. Entomol. 38: 121Ð143. tera: Noctuidae) in Michigan. Ph.D. dissertation, Michi- gan State University, East Lansing. SAS Institute. 2001. SAS/STAT userÕs manual, version 8.2. Received for publication 14 June 2003; accepted 11 October SAS Institute, Cary, NC. 2003.