Adult Parasitoids of the Southern Pine Beetle

Biocontrol Science and Technology, May 2005; 15(3): 243Á/254

Adult parasitoids of the southern pine beetle, Dendroctonus frontalis Zimmermann (Coleoptera: Scolytidae), feed on artiﬁcial diet on pine boles, pine canopy foliage and understory hardwood foliage

SHERAH L. VANLAERHOVEN1,2, FRED M. STEPHEN1,& LLOYD E. BROWNE3

1Department of Entomology, University of Arkansas, Fayetteville, AS, USA, 2Department of Biology, University of Windsor, Windsor, Ontario, Canada, and 3Entopath, Inc., Easton, PA, USA

(Received 13 February 2003; returned 1 April 2003; accepted 12 August 2004)

Abstract This study examined adult parasitoids of Dendroctonus frontalis Zimmermann (Coleoptera: Scolytidae) utilizing an artificial parasitoid food on locations with and without hosts. EliminadeTM was applied to bark on boles of infested pines, to pine canopy foliage and to understory hardwood foliage. Adult parasitoids were collected, identified and dissected to determine the presence of EliminadeTM within their guts. Individuals from eight parasitoid species were collected on pine boles within D. frontalis infestations in the Talladega National Forest (Alabama) in the summer of 1999 and 2000. Mean percentage of parasitoids feeding on TM Eliminade was 629/10% during both summers. Percentage of parasitoids feeding was the same 24 h after EliminadeTM application, regardless of food location or parasitoid species. Seven days later, level of parasitoid feeding on EliminadeTM was insignificant in the pine canopy and hardwood understory. In contrast, percent of parasitoid feeding on EliminadeTM applied to pine boles remained the same between 1 and 7 days of the application. Therefore, not only will adult parasitoids visit and feed on artificial food on pine boles with hosts, but also non-host locations such as pine canopy and understory hardwood foliage. These results have implications for potential sources of adult nutrition for parasitoids of D. frontalis.

Keywords: Coeloides pissodis, Dendrosoter sulcatus, Dinotiscus dendroctoni, Eurytoma tomici, Heydenia unica, Meteorus hypophloei, Roptrocerus xylophagorum, Braconidae, Eurytomidae, Pteromalidae, bark beetles, biological control, artiﬁcial food spray

Introduction The southern pine beetle, Dendroctonus frontalis Zimmermann (Coleoptera: Scolyti- Downloaded by [University of Arkansas Libraries - Fayetteville] at 08:52 06 December 2011 dae), an important pest of pines in the southeastern forests of the United States (Thatcher 1960; Price et al. 1992), has an associated parasitoid complex that in conjunction with predators, can potentially reduce both the size and number of

Correspondence: Dr. Sherah L. VanLaerhoven, Department of Biology Rm 119, 401 Sunset Ave, University of Windsor, Windsor, ON, Canada N9B 3P4. Tel: 1 519 253 3000, ext. 2713. Fax: 1 519 971 3609. E-mail: [email protected]

ISSN 0958-3157 print/ISSN 1360-0478 online # 2005 Taylor & Francis Group Ltd DOI: 10.1080/09583150400016878 244 S. L. VanLaerhoven et al.

D. frontalis infestations (Berisford 1980; Dahlsten & Whitmore 1989; Stephen et al. 1993). The D. frontalis parasitoid complex is composed of six to nine species that are usually present in active D. frontalis infestations (Stephen 1995; Stephen et al. 1997). Within large D. frontalis infestations, parasitoid adults do not need to disperse far to locate hosts. In contrast, the majority of D. frontalis infestations consist of fewer than 10 trees and eventually decline (Billings 1980). In these small infestations, hosts may not be available to emerging parasitoids and the ability of parasitoids to disperse and find patchy host resources within a forest ecosystem becomes important for reproduction. Southern pine beetle parasitoids are synovigenic (Berisford 1980). They produce a few large, nutrient rich eggs (Flanders 1950; Collier et al. 1994), with immature eggs often present at parasitoid emergence (Jervis et al. 2001). Some of their eggs are typically present at adult emergence, but they can produce more eggs if requisite nutrients are available to the adult. They can also resorb eggs when hosts are unavailable (King 1963; Drost & Carde 1992) and this allows adult parasitoids to extend their life while providing nutrients needed for dispersal. Parasitoids can produce more mature eggs when hosts are located, although the adults must have food to produce these eggs. Due to management strategies, the southern pine forest ecosystem often consists of single-species, even-aged stands that provide excess host material for D. frontalis (Thatcher et al. 1980). Host feeding by adult D. frontalis parasitoids is rare (Bushing 1967), likely due to the cryptic nature of their host larvae. Many species of parasitoids use floral and extrafloral nectar, pollen or honeydew as adult nutrition (Leius 1960; Powell 1986; Jervis & Kidd 1992; Jervis et al. 1993). Bark beetle parasitoids have never been observed visiting flowers (Jervis et al. 1993; Drumtra & Stephen 1999). In addition, intensely managed pine forest often lacks understory diversity and flowering plants that would potentially provide nectar and pollen sources for adult parasitoids (Hunter 1990). Honeydew may be a potential food source for parasitoids as initial data indicated that D. frontalis parasitoids will forage in the canopy of pines (Stephen & Browne 2000) where homopteran honeydew may be present. However, the distribution of honeydew in southern forests is variable and uncertain (VanLaerhoven 2001). EliminadeTM is an artificial insect food formulated by Entopath Inc. for adult parasitoids, comprised of 33% (dry wt.) protein, 65% sucrose, 2% vitamins, minerals, TM salts and dye, and an undetermined amount of lipids (B/10%). Eliminade has been shown to increase longevity and egg load of adult D. frontalis parasitoids (Hanano 1996; Mathews & Stephen 1997; Mathews & Stephen 1999). Because the food is non- attractive to parasitoids (unpublished data) and contains a dye that is detectable within insect guts, it can be used to determine where adult parasitoids forage for food

Downloaded by [University of Arkansas Libraries - Fayetteville] at 08:52 06 December 2011 within D. frontalis infestations. Adult parasitoids, especially synovigenic parasitoids, balance foraging for hosts with foraging for food and these may be found in different locations (Lewis et al. 1998). Although an initial study indicated that D. frontalis parasitoid adults will feed on EliminadeTM applied to D. frontalis-infested pine boles and pine canopy (Stephen & Browne 2000), foraging on understory vegetation was not examined. Because of inadequate replication, it was not possible to determine if there were differences in feeding between parasitoid species. The objectives of the current study were: (1) to Adult D. frontalis parasitoid food foraging 245

determine if parasitoids would utilize food on hardwood understory foliage; (2) to discover whether there are differences in feeding by parasitoid adults in the different tree habitats and the degree of feeding by each parasitoid species; and (3) to determine how feeding on one application of food changes over a fixed time period.

Materials and methods

The study was conducted in July 1999 and JuneÁ/September 2000 within active D. frontalis infestations each of ca. 75 infested Pinus taeda L. located in the Talladega National Forest in Alabama. The study sites consisted of mixed hardwood-pine stands, with the primary pine species being loblolly pine, P. taeda, with some longleaf pine, P.palustris (Mill.). In 1999, one D. frontalis infestation was used for the paintball gun applications of EliminadeTM. The food was applied to three or four trees (per treatment) within the infestation at a rate of 50 food balls per tree, evenly spaced along the bole to the base of the crown. In the first set of treatments, food was applied to either the bole or crown of pine trees using blue- and red-dyed EliminadeTM. In the second set of treatments 2 weeks later, food was applied to either the bole, crown or both, to determine if overall parasitoid feeding would be increased by additional locations. A second infestation was used to test the application of food to crown of pines by aerial spray from a helicopter. Aerial application of EliminadeTM was at a rate of 16 L/ha. Because there may have been some spatial overlap between treatments in the preliminary 1999 study, in 2000, 10 different infestation sites were used with EliminadeTM applied to only one habitat in each infestation. In three infestations, food was only applied to pine boles and in another three infestations, food was only applied to hardwood understory foliage. In two infestations, food was only applied to pine canopy foliage. In the last two infestations, food was not applied and used as a no-food application or control infestations. EliminadeTM was applied by three different methods. Food was applied to the boles of pines using a paintball gun, at a rate of 50 food balls per tree, evenly spaced along the bole to the base of the crown. In this treatment, food was reapplied once a week to all trees containing D. frontalis. In the understory hardwood treatments, EliminadeTM was applied using a backpack sprayer to all the understory foliage within the infestation at a rate of 14 kg/ha. Food was reapplied 3 weeks after the first application. In the pine canopy treatments, EliminadeTM was applied to all the pine foliage within an infestation using an aerial spray from an airplane at a rate of 14 kg/ha. Food was reapplied at 3 weeks after the first application. All the treatment sites in the 2000 study were monitored for a total of 6 weeks. Presence or absence of food on foliage or bark was visually assessed during each visit to the sites. In both 1999 and 2000 adult D. frontalis parasitoids were collected from the boles of

Downloaded by [University of Arkansas Libraries - Fayetteville] at 08:52 06 December 2011 pine trees using either an aspirator or dust buster vacuum. In 1999, parasitoids were collected each day for up to 4 days after application of EliminadeTM to trees. In 2000, parasitoids were collected on the day before and the day after food application and once a week between treatments. In pine canopy and hardwood treatments, food application took place twice during the 6-week period, at the beginning of the study and again 3 weeks later. Controls were sampled weekly. A maximum of 50 parasitoids were collected from each infestation on each collection date. Following collection, parasitoids were refrigerated, identified and dissected within 24 h of collection and the 246 S. L. VanLaerhoven et al.

gut contents examined for the presence of EliminadeTM. Parasitoid counts and percent feeding were analyzed by analysis of variance and least significant difference mean separations within JMP IN version 3.2.1 (SAS 1997).

Results Eight parasitoid species from three families were collected in both 1999 and 2000. In 1999, 1216 parasitoids were collected (Table I), while in 2000, 1166 parasitoids were collected (Table II). In 1999, parasitoids were only collected in July and no reduction in parasitoid numbers was observed over the 4-day collection period. However, in 2000, parasitoids were collected from June to September (Figure 1) and the number

of parasitoids collected decreased over time (F/6.47, P/0.001, df/3) as parasitoids became more difficult to find, possibly due to decreasing populations. The decline in parasitoids observed in 2000 was not influenced by the presence of EliminadeTM within the infestation, as this decline occurred in both control (no food application)

and treatment infestations (F/0.2. P/0.6. df/1). The relative abundance of the different parasitoid species collected was not consistent between 1999 and 2000. In 1999, the parasitoid species were more evenly distributed (Figure 2) than those collected in 2000 (Figure 3). In 1999, most species collected comprised between 10 and 20% of the total, with only two species having a relative abundance less than 5%, significantly less than that of the two most abundant

species (F/4.31, P/0.0003, df/7). In 2000, Coeloides pissodis (Ashmead) composed approximately 40% of the parasitoids collected, significantly greater than that of

any other species (F/16.95, P B/0.0001, df/7), while three species had a relative abundance less than 5%. The percentage of collected parasitoids feeding on EliminadeTM remained the same

from June to September in 2000 (F/1.02, P/0.46, df/3) (Figure 4) and was not

significantly different overall from parasitoid feeding in 1999 at 629/10% (F/0.76,

P/0.4, df/1). In 1999, the percentage of parasitoids feeding was the same regardless

of whether the parasitoids were collected 1Á/4 days after food application (F/0.02,

P/0.99, df/3) (Table III), or whether the food was applied to the pine bole, canopy

or both (F/2.12, P/0.14, df/3). Although fewer parasitoids appeared to feed on

Table I. Number of parasitoids collected within each EliminadeTM treatment in 1999.

Pine Pine Pine bole Pine canopy Total for Family and species bole canopy and canopy (aerial spray) species

Braconidae Coeloides pissodis 123 30 26 26 205 Spathius pallidus 6011219 Dendrosoter sulcatus 4111 7 Meteorus hypophloei 440151069 Downloaded by [University of Arkansas Libraries - Fayetteville] at 08:52 06 December 2011 Pteromalidae Dinotiscus dendroctoni 23 25 17 71 136 Roptrocerus xylophagorum 30 71 53 102 256 Heydenia unica 69 27 31 182 309 Eurytomidae Eurytoma tomici 21 44 40 110 215 Total for teatment 280 238 184 514 1216 Adult D. frontalis parasitoid food foraging 247 Table II. Number of parasitoids collected within each EliminadeTM treatment in 2000.

Pine Pine Understory Control Total for Family and species bole canopy canopy (no food) species

Braconidae Coeloides pissodis 85 100 80 195 460 Spathius pallidus 40 2 3 7 52 Dendrosoter sulcatus 6 4 10 4 24 Meteorus hypophloei 01449 Pteromalidae Dinotiscus dendroctoni 21 27 16 20 84 Roptrocerus xylophagorum 29 19 48 12 108 Heydenia unica 99 56 50 67 272 Eurytomidae Eurytoma tomici 52 51 21 33 157 Total for treatment 332 260 232 342 1166

food when applied by paintball gun to pine canopy compared to aerial spray, this

difference was not significant (a/0.05). Applying the food to the bole, canopy or hardwood understory did not influence the percentage of parasitoids that fed within 1 day of the application in 2000 (Table IV). Seven days later, the percentage of parasitoids that had fed in the infestations where food was applied to the pine canopy or understory was much lower and not different from the no-food control plots. Upon visual inspection of the understory foliage, no EliminadeTM was observed 7 days post-application. However, the percentage of parasitoids feeding in the pine bole application remained significantly higher TM (F/4.06, P/0.01, df/7). Eliminade was observed in crevices within the bark in the pine bole treatment 7 days post-application. Because the bole application plots

a 60

b 30

20 b

Downloaded by [University of Arkansas Libraries - Fayetteville] at 08:52 06 December 2011 b # # parasitoids per collection date 10

0 June July Aug Sept

Figure 1. Decline in adult parasitoids over time sampled from Dendroctonus frontalis Zimmermann infestations within the Talladega National Forest (Alabama) at each collection date during 2000. Means followed by the same letter are not signiﬁcantly different (P /0.05). 248 S. L. VanLaerhoven et al.

50%

40%

ab 30% aa

ab 20%

Mean Relative Abundance (%) ab ab 10%

b b 0%

Heydenia unica Eurytoma tomici Spathius pallidus Coeloides pissodis Meteorus hypophloei Dendrosoter sulcatus Dinotiscus dendroctoni Roptrocerus xylophagorum

Figure 2. Relative abundance of adult parasitoids collected from Dendroctonus frontalis Zimmermann infestations within the Talladega National Forest (Alabama) in 1999. Means followed by the same letter are not signiﬁcantly different (P /0.05).

had food applied once a week, there was no way to determine the percentage of parasitoids feeding more than 7 days post-application. Location of the food application did not influence the percentage of parasitoids feeding 1 day after application, nor did it influence the percentage of feeding by a

particular species (F/0.2, P/0.99, df/16). However, the relative numbers of parasitoids feeding on EliminadeTM varied by species. The percentage of C. pissodis, Heydenia unica Cook and Davis and Dinotiscus dendroctoni (Ashmead) feeding was approximately 65% (Figure 5). A significantly smaller proportion of Eurytoma tomici TM Ashmead were found with Eliminade in their gut (F/3.16, P/0.03, df/4). Roptrocerus xylophagorum Ratzeburg was not different from either group.

Downloaded by [University of Arkansas Libraries - Fayetteville] at 08:52 06 December 2011 Discussion Regardless of where EliminadeTM was applied, the number of adult parasitoids collected each week declined over the summer in 2000. The reasons for this are unclear but are probably due to decreasing parasitoid populations. In previous studies where adult parasitoid food has been applied or provided, parasitoid numbers increased as the presence of food retained adult parasitoids within the patch longer than in patches without food, even when hosts were available (Jervis et al. 1996; Jacob Adult D. frontalis parasitoid food foraging 249

50% a

40%

30%

20% bc bc Mean Relative Abundance (%) (%) Abundance Relative Mean 10% c c

c c

us id

HeydeniaEurytoma unica tomici Coeloides pissodis Spathius pall DendrosoterMeteorus sulcatus hypophloei Dinotiscus dendroctoni Roptrocerus xylophagorum

Figure 3. Relative abundance of adult parasitoids collected from Dendroctonus frontalis Zimmermann infestations within the Talladega National Forest (Alabama) in 2000. Means followed by the same letter are not signiﬁcantly different (P /0.05).

& Evans 1998). This has also been observed with predators (Tassan et al. 1979; Mensah & Madden 1994). Adult parasitoids were readily obtained from application sites in the 1999 study. In contrast, difficulty in locating and collecting parasitoids in 2000 could explain the different relative abundance of parasitoids collected between the 2 years. Because adult parasitoids were difficult to find in 2000, the distribution of parasitoids was biased towards the most easily observed parasitoids such as C. pissodis, which is the largest of the species and has a bright orange abdomen. Adult parasitoids balance searching for hosts and foraging for food, which may be in different locations (Lewis et al. 1998). Adult parasitoids of D. frontalis fed equally well TM Downloaded by [University of Arkansas Libraries - Fayetteville] at 08:52 06 December 2011 on Eliminade on the pine bole and canopy foliage within 4 days of the food application in 1999. This suggests that foraging for food is important to adult D. frontalis parasitoids, which can be important for longevity and egg load (Hanano 1996; Mathews & Stephen 1997). In 2000, parasitoids fed on EliminadeTM on the pine bole, canopy and understory hardwood foliage, while their hosts were only in phloem under bark within the pine bole. Because parasitoids located and fed on EliminadeTM in non-host locations (pine 250 S. L. VanLaerhoven et al.

80% a 70%

a 60% a 50% a

40%

30%

20% % Parasitoids Foraging Parasitoids %

10%

0% Jun July Aug Sept

Figure 4. Percentage of adult Dendroctonus frontalis Zimmermann parasitoids foraging on EliminadeTM over the summer of 2000. Means followed by the same letter are not signiﬁcantly different (P /0.05).

canopy and understory hardwood foliage), this suggests that these locations may be a source of adult nutrition, such as honeydew, in the forest ecosystem. In 1999 and 2000, the location of the food did not influence the percentage of parasitoids that had fed. However during the 2000 study, persistence of EliminadeTM was examined and the food remained on the boles of pines much longer than on pine canopy or understory foliage. Visual observations of the understory foliage in 2000 revealed that the food was no longer visible 7 days after application, whereas food was still readily observed on pine boles. Seven days after application, the percentage of parasitoids that had fed on the food from pine boles was the same as those that fed 1 day after application, while parasitoids collected from other treatments did not feed on EliminadeTM (same as control). Thunderstorms and rain events were common during the summer and due to the orientation of needles and leaves, the rain washed food off the leaves and was no longer visible by 7 days after the application. In contrast, fissures in the bark and the vertical orientation of the pine bole allowed the food to persist as it was still visible by observation of the pine boles and therefore, food was available to the parasitoids for much longer than in the other treatments. Because R. xylophagorum has been observed host feeding once (Bushing 1967), other sources of food may be less important than for other species of parasitoids

TM Table III. Mean (9/SE) percentage of adult Dendroctonus frontalis parasitoids foraging on Eliminade 1Á/4 days after its application to pine boles, canopy or both in 1999. Between treatment means are not

signiﬁcantly different (F/1.8, P/0.21, df/3). Between day means are not signiﬁcantly different (F/0.1, P/0.95, df/3). Downloaded by [University of Arkansas Libraries - Fayetteville] at 08:52 06 December 2011 Days since EliminadeTM application

EliminadeTM application 1 2 3 4

Pine bole 609/17% 669/16% 579/0% Pine canopy 409/24% 429/33% 459/34% Pine bole and canopy 809/0% 789/0% 669/0% Pine canopy (aerial spray) 779/0% 769/0% 779/0% 629/0% Adult D. frontalis parasitoid food foraging 251

TM Table IV. Mean (9/SE) percentage of adult Dendroctonus frontalis parasitoids foraging on Eliminade over a 3-week period in 2000 after its application to pine boles, canopy and understory hardwood foliage compared to control infestations with no EliminadeTM application. Means followed by the same letter are not signiﬁcantly different (P /0.05).

Days since EliminadeTM application

EliminadeTM application 1 7 14 21

Pine bole 399/8% a 399/18% a Pine canopy 569/9% a 29/2% b 49/4% b 49/4% b Understory hardwood 499/10% a 69/6% b 19/1% b 09/0% b Control (no Eliminade) 09/0% b 09/0% b 09/0% b 09/0% b

100%

90%

80% a a a 70%

ab 60%

50% b

40% % Parasitoids Feeding Parasitoids %

30%

20%

10%

0% Downloaded by [University of Arkansas Libraries - Fayetteville] at 08:52 06 December 2011 ca ni

Heydenia u Eurytoma tomici Coeloides pissodis Dinotiscus dendroctoni Roptrocerus xylophagorum

Figure 5. Percentage of feeding on EliminadeTM by each parasitoid species 1 day after EliminadeTM application in 1999 and 2000. Means followed by the same letter are not signiﬁcantly different (P /0.05). 252 S. L. VanLaerhoven et al.

collected. However, our results demonstrate that R. xylophagorum fed as much as other non host-feeding parasitoids in 2000. This lends support to the assumption that host feeding is rare for adult D. frontalis parasitoids. In contrast, there is no explanation for the significantly smaller degree of feeding by E. tomici. We demonstrated that foraging for food may be important for adult D. frontalis parasitoids as they may search for adult nutrition away from pine boles where their hosts are located. Applications of food to pine boles persist longer than applications to pine canopy or understory hardwoods. Studies have shown that starved parasitoids will choose foraging for food over hosts (Takasu & Hirose 1991; Wackers 1994) and will leave patches even with hosts available (Takasu & Lewis 1993, 1995, 1996; Stapel et al. 1997). Therefore, applying food to boles of pines would minimize the time taken to forage for food, maximizing searching for hosts by reducing the amount of distance parasitoids would have to move to find food and hosts and minimizing the frequency of food application as EliminadeTM persisted longer on pine boles than on foliage.

Acknowledgements We would like to thank T.J. Kring, M.V. Meisch, L.C. Thompson and K.G. Smith for support and guidance. This research could not have been conducted without assistance of V.B. Salisbury, D.L. Kinney, M.B. Kelley, K. Lindsay, S. Browne and K.J. Dodds. We thank E. Gbur for his statistical advice. We acknowledge the Talladega National Forest staff for their kind cooperation. S.L.V. is grateful to the Department of Entomology and the John Heiss family for their generous fellowships. This research was supported in part by the University of Arkansas, Arkansas Agricultural Experiment Station, and the Arkansas Forest Resources Center, Monticello, AR. Published with the approval of the Director, Arkansas Agricultural Experiment Station.

References Berisford CW. 1980. Natural enemies and associated organisms. In: Thatcher RC, Searcy JL, Coster JE, Hertel GD, editors. The southern pine beetle. United States Department of Agriculture Forest Service

Science, Education & Administration Technical Bulletin No. 1631. pp 31Á/52. Billings RF. 1980. Direct control. In: Thatcher RC, Searcy JL, Coster JE, Hertel GD, editors. The southern pine beetle. United States Department of Agriculture Forest Service Science, Education & Administra-

tion Technical Bulletin No. 1631. pp 179Á/192. Bushing RW. 1967. Parasites of the western pine beetle, Dendroctonus brevicomis Le Conte (Coleoptera: Scolytidae) with particular reference to Roptrocerus xylophagorum (Ratzeburg) (Hymenoptera: Torymi- dae). Ph.D. Dissertation, University of California, Berkeley. Collier TR, Murdoch WW, Nisbet RM. 1994. Egg load and the decision to host-feed in the parasitoid,

Aphytis melinus. Journal of Animal Ecology 63:299Á/306. Dahlsten DL, Whitmore MC. 1989. Potential for biological control of Dendroctonus and Ips bark beetles: the case for and against the biological control of bark beetles. In: Kulhavy DL, Miller MC, editors. Downloaded by [University of Arkansas Libraries - Fayetteville] at 08:52 06 December 2011 Potential for biological control of Dendroctonus and Ips bark beetles. Nacogdoches: Stephen F. Austin

State University. pp 3Á/19. Drost YC, Carde RT. 1992. Inﬂuence of host deprivation on egg load and oviposition behaviour of

Brachymeria intermedia, a parasitoid of gypsy moth. Physiological Entomology 17:230Á/234. Drumtra DW, Stephen FM. 1999. Incidence of wildﬂower visitation by Hymenopterous parasitoids of southern pine beetle, Dendroctonus frontalis Zimmermann. Journal of Entomological Science 34:484Á/ 488. Flanders SE. 1950. Regulation of ovulation and egg disposal in the parasitic Hymenoptera. The Canadian

Entomologist 82:134Á/140. Adult D. frontalis parasitoid food foraging 253

Hanano TL. 1996. Effect of nutrition on egg production in adult hymenopterous parasitoids of southern pine beetle Dendroctonus frontalis Zimmermann. M.S. thesis, University of Arkansas, Fayetteville. Hunter ML, Jr. 1990. Wildlife, forests and forestry: principles of managing forests for biological diversity. Englewood Cliffs: Prentice Hall. Jacob HS, Evans EW. 1998. Effects of sugar spray and aphid honeydew on ﬁeld populations of the parasitoid

Bathyplectes curculionis (Hymenoptera: Ichneumonidae). Environmental Entomology 27:1563Á/1568. Jervis MA, Kidd NA. 1992. Wild ﬂowers and forest Á/ natural enemies may beneﬁt too. Entopath News 1:5Á/ 6. Jervis MA, Kidd NAC, Fitton MG, Huddleston T, Dawah HA. 1993. Flower-visiting by hymenopteran

parasitoids. Journal of Natural History 27:67Á/105. Jervis MA, Kidd NAC, Heimpel GE. 1996. Parasitoid adult feeding behaviour and biocontrol Á/ a review. Biocontrol News Information 17:11NÁ/26N. Jervis MA, Heimpel GE, Ferns PN, Harvey JA, Kidd NA. 2001. Life-history strategies in parasitoid wasps:

A comparative analysis of ‘ovigeny’. Journal of Animal Ecology 70:442Á/458. King PE. 1963. The rate of egg resorption in Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae)

deprived of hosts. Proceedings of the Royal Entomological Society of London. Series A 38:98Á/100. Leius K. 1960. Attractiveness of different foods and ﬂowers to the adults of some Hymenopterous parasites.

The Canadian Entomologist 92:369Á/376. Lewis WJ, Stapel JO, Cortesero AM, Takasu K. 1998. Understanding how parasitoids balance food and host

needs: Importance to biological control. Biological Control 11:175Á/183. Mathews PL, Stephen FM. 1997. Effect of artiﬁcial diet on longevity of adult parasitoids of Dendroctonus

frontalis (Coleoptera: Scolytidae). Environmental Entomology 26:961Á/965. Mathews PL, Stephen FM. 1999. Effects of an artiﬁcial diet and varied environmental conditions on longevity of Coeloides pissodis (Hymenoptera: Braconidae), a parasitoid of Dentroctonus frontalis

(Coleoptera: Scolytidae). Environmental Entomology 28:729Á/734. Mensah RK, Madden JL. 1994. Conservation of two predator species for biological control of

Chrysophtharta bimaculata (Col: Chrysomelidae) in Tasmanian forests. Entomophaga 39:71Á/83. Powell W. 1986. Enhancing parasitoid activity in crops. In: Waage J, Greathead D, editors. Insect

parasitoids. London: Academic Press. pp 319Á/340. Price TS, Doggett CA, Pye JM, Holmes TP. 1992. A history of southern pine beetle outbreaks in the southeastern United States. Georgia Forestry Commission, Macon. SAS. 1997. JMP IN. SAS Institute Inc, SAS Campus Drive, Cary. Stapel JO, Cortesero AM, DeMoraes CM, Tumlinson JH, Lewis WJ. 1997. Effects of extraﬂoral nectar, honeydew and sucrose on searching behavior and efﬁciency of Microplitis croceipes (Hymenoptera:

Braconidae) in cotton. Environmental Entomology 26:617Á/623. Stephen FM. 1995. Potential for suppressing southern pine beetle populations by enhancing effectiveness of their hymenopteran parasitoids. In: Hain FP, Salom SM, Payne TL, Raffa KF, editors. Behavior, population dynamics and control of forest insects. Wooster: Ohio Agriculture Research & Development

Center, Ohio State University. pp 226Á/240. Stephen FM, Browne LE. 2000. Application of EliminadeTM parasitoid food to boles and crowns of pines (Pinaceae) infested with Dendroctonus frontalis (Coleoptera: Scolytidae). The Canadian Entomologist

132:983Á/985. Stephen FM, Berisford CW, Dahlsten DL, Fenn P, Moser JC. 1993. Invertebrate and microbial associates. In: Schowalter TD, Filip G, editors. Beetle-pathogen interactions in conifer forests. London: Academic

Press. pp 129Á/153. Stephen FM, Lih MP, Browne LE. 1997. Augmentation of Dendroctonus frontalis parasitoid effectiveness by artiﬁcial diet. In: Gregoire JC, Liebhold AM, Stephen FM, Day KR, Salom SM, editors. Proceedings, integrating cultural tactics into the management of bark beetle and reforestation Pests: Vallombrosa, Italy,

September 1Á/3 1996. United States Department of Agriculture Forest Service, Northeast Forest Downloaded by [University of Arkansas Libraries - Fayetteville] at 08:52 06 December 2011 Experimental Station, Radnor. pp 15Á/22. Takasu K, Hirose Y. 1991. Host searching behavior in the parasitoid Ooencyrtus nezarae Ishii (Hymenoptera:

Encyrtidae) as inﬂuenced by non-host food deprivation. Applied Entomology & Zoology 26:415Á/417. Takasu K, Lewis WJ. 1993. Host- and food-foraging of the parasitoid Microplitis croceipes: Learning and

physiological state effects. Biological Control 3:70Á/74. Takasu K, Lewis WJ. 1995. Importance of adult food sources to host searching of the larval parasitoid

Microplitis croceipes. Biological Control 5:25Á/30. Takasu K, Lewis WJ. 1996. The role of learning in adult food location by the larval parasitoid, Microplitis

croceipes (Hymenoptera: Braconidae). Journal of Insect Behaviour 9:265Á/281. 254 S. L. VanLaerhoven et al.

Tassan RL, Hagen KS, Sawall EF, Jr. 1979. The inﬂuence of ﬁeld food sprays on the egg production rate of

Chrysopa carnea. Environmental Entomology 8:81Á/85. Thatcher RC. 1960. Bark beetles affecting southern pines: A review of current knowledge. United States Department of Agriculture Forest Service, Southern Forest Experimental Station. Thatcher RC, Searcy JL, Coster JE, Hertel GD, editors. 1980. The southern pine beetle. United States Department of Agriculture Forest Service Science, Education & Administration Technical Bulletin No. 1631. VanLaerhoven SL. 2001. Foraging behavior and reproductive biology of the southern pine beetle, Dendroctonus frontalis Zimmermann, parasitoid complex. Ph. D. Dissertation, University of Arkansas, Fayetteville. Wackers FL. 1994. The effect of food deprivation on the innate visual and olfactory preferences in the

parasitoid Cotesia rubecula. Journal of Insect Physiology 40:641Á/649. Downloaded by [University of Arkansas Libraries - Fayetteville] at 08:52 06 December 2011