Temporal Distribution of Phyllonorycter elmaella (Lepidoptera: Gracillariidae) and Its Major Parasitoid, Pnigalio flavipes (Hymenoptera: Eulophidae), in Washington Apple Orchards
BRUCE A. BARRETl'l AND JAY F. BRUNNER
Tree Fruit Research and Extension Center, Washington State University, Wenatchee, Washington 98801
Environ.Entomol.19(2): 362-369 (1990) ABSTRACT The seasonal occurrence of Phy!lonorycter elmaella Doganlar & Mutuura, a Downloaded from https://academic.oup.com/ee/article/19/2/362/468438 by guest on 25 September 2021 tentiform leafminer, and its parasitoid, Pnigalio flavipes (Ashmead), in insecticide-free blocks located in commercial apple orchards was determined. P. elmaella had three complete generations each year; population densities increased in each generation. P. elmaella sap feeders (first to third instars) were "abnormally" abundant in the blocks at the end of each season, possibly because of a delay in their development. P. flavipes had at least the same number of generations as P. elmaella. Parasitoid activity decreased as the season progressed. Phenology data showed adult P. flavipes emerged almost concurrently with adult P. elmaella during the spring and summer generations, 2-3 wk before tissue feeders (fourth and fifth instars), were present in the orchard. This emergence pattern may be caused by a reproductive advantage for female P. flavipes to feed on sap feeders before oviposition. The number of individuals of P. elmaella that are able to overwinter successfully, rather than the seasonal levels of parasitism, seems to determine the leafminer's year-to-year population dynamics. However, parasitoid activity reduced the leafminer's intraseasonal population increase and kept its densities below treatment threshold levels in all orchard blocks examined.
KEY WORDS Insecta, Phyllonorycter elmaella, phenology, parasitism
Phyllonorycter elmaella Doganlar & Mutuura is of P. elmaella on apple, development of resistance one of three major Phyllonorycter spp. attacking to it in the Pacific Northwest is of great concern. apple in North America. Phyllonorycter blancar- In addition, the use of oxamyl may disrupt the della (F.), the spotted tentiform leafminer, and P. already established integrated mite control pro- crataegella (Clemens), the apple blotch leafminer, gram used in many Washington apple orchards occur in eastern North America (Weires et al. 1980); (Hoyt 1983). A management program is needed P. elmaella occurs in western North America (Do- that would decrease the chance for resistance de- ganlar & Mutuura 1980, Gibb 1983). Before the velopment and be compatible with current Wash- late 1970s, P. elmaella was considered only a minor ington apple IPM programs. pest with infrequent outbreaks but in recent years, Worldwide evidence suggests that Phyllonoryc- infestations have become more severe and frequent ter populations are amenable to biological control in many fruit-growing areas of Washington and by hymenopterous parasitoids (Celli 1970, Swan Oregon (Orphart 1982). Larvae of Phyllonorycter 1973, Bassino et al. 1976). In central Washington, spp., which do not feed on the fruit but within the the major parasitoid species of P. elmaella is an leaves, have two feeding stages: sap feeders (first ectoparasitic eulopid, Pnigalio flavipes (Ashmead) to third instars) and tissue feeders (fourth and fifth (Barrett 1988). Occasional high levels of parasitism instars). Extensive leaf mining by Phyllonorycter in many commercial apple orchards indicated that, larvae has been reported to cause early leaf drop; through parasitoid conservation, biological control premature fruit ripening and drop; and reductions of P. elmaella by P. flavipes could play an impor- in terminal growth, fruit size, and fruit set the tant role in leafminer management. The success of following year (Pottinger & LeRoux 1971, Reissig any biological control project depends on appro- et al. 1982). priate biological, ecological, and population studies The cause of the increasing problems with Phyl- of the species involved (Miller 1983). Here we re- lonorycter spp. in eastern North America is thought port on the temporal distributions of P. elmaella to be their resistance to commonly used organo- and P. flavipes and present an assessment of P. phosphorous insecticides (Weires et al. 1978). Be- flavipes as a biological control agent of P. elmaella. cause the carbamate oxamyl (Vydate) is the only chemical registered in Washington for the control Materials and Methods From 1985 to 1987, three insecticide-free test I Current address: PennsylvaniaState University,Fruit Re- search Laboratory,Biglerville,Pa. 17307. blocks, each consisting of 25 'Red Delicious' apple
0046-225XI9010362-0369$02.00/0 © 1990 EntomologicalSocietyof America April 1990 BARRETT & BRUNNER: DISTRIBUTION OF P. elmaella AND P. flavipes 363 trees (5 x 5), were maintained at the commercial because they were intended to provide only a pas- Twin WW (WW), Ox Team (OX), and the Colum- sive estimate of adult occurrence. bia View (CV) orchards of the Washington State Sample Analysis. Density of P. elmaella (mines University Tree Fruit Research and Extension Cen- per leaf) was determined by dividing the number ter. All sites were in Douglas County. A second of mines found on the leaf samples by the total block at the Twin WW orchard (WB) was added number of leaves collected. Levels of parasitism in 1987 because levels of codling moth in the WW (%), referred to as parasitoid-induced mortality block required the application of azinphosmethyl (PIM), were obtained by dissecting each sampled (Guthion) that year, although samples were still mine and recording the stage (sap feeder, tissue taken from the WW site. The WB block was seven feeder, pupa, or emerged adult) and its condition rows south of the WW block. Trees at the OX, (healthy, death caused by parasitoid activity, or WW, and WB blocks were standard size (4.3-5.5 unknown mortality). PIM consisted of host-stinging Downloaded from https://academic.oup.com/ee/article/19/2/362/468438 by guest on 25 September 2021 m tall, 28-36 yr old). Trees at the CV block were with oviposition (P+), host-stinging without ovi- semidwarf (3.0-3.7 m tall, 15 yr old). Before 1985, position (P-), and adult host feeding (HF). Host- these blocks had existing populations of P. elmaella stinging without oviposition has been reported for and P. flavipes and were subject to routine pesticide parasitoid-attacked P. crataegella larvae (Van applications. Ten trees in the center of each block Driesche & Taub 1983). Larvae of P. elmaella killed were selected as sampling trees, with one buffer by host feeding had a characteristic appearance. row of trees not treated with insecticides separating The body was completely or partially void of its them from the surrounding orchard. liquid contents and usually was attached to the Sampling. The density of P. elmaella in each inner mine surface at a localized dark spot. PIM block was determined by randomly picking 30 was calculated by summing all P+, P-, and HF leaves from the lower inner and lower outer regions mines, dividing by the total number of mines sam- of three trees (180 leaves/block) once a week. Para- pled, and multiplying by 100 (Van Driesche 1983). sitoid activity and the seasonal occurrence of P. elmaella and P. flavipes stages were determined Results and Discussion by gathering the first 30 mines encountered in the lower inner and lower outer regions of two trees Seasonal Density of P. elmaella. Density (mines (120 mines/block) once a week. Mine selection was per leaf) increased in successive generations in all accomplished by choosing a shoot or cluster of leaves orchard blocks each year (Table 1). Similar pop- in a given region and turning the leaves over, ex- ulation dynamics have been reported for P. blan- posing their undersides. This was done to avoid a cardella (Johnson et al. 1976, Ridgway & Mahr biased selection of tissue-feeding mines because 1985). The increase in leafminer density from the mines of sap feeders are visible only from the un- first to the second generation ranged from 1.4 (WW, derside of the leaf, whereas those of tissue feeders 1986) to 20 times (OX, 1987) for an average in- are visible from both sides. To insure an accurate crease of 5 times. The increase in density from the estimate of parasitoid activity within the current second to the third generation ranged from 3.8 generation only, mines that were obviously old and (OX, 1987) to 39 times (OX, 1986) for an average from an earlier generation (indicated by their ap- increase of 16 times. Increases in density from the pearance) were not sampled. The weekly totals of third to the fourth generation (1987 only), ranged healthy leafminer and parasitoid stages from the from 1.1 (OX) to 3.4 times (CV) for an average mine samples provided the information we re- increase of 2.3 times. quired to determine the relative seasonal occur- There are two explanations for why the increase rence of P. elmaella and P. flavipes. Leaf and mine in density from the first to the second generation samples were taken from different trees each week. was much less than that from the second to the Sampling started in late April (1986-1987) or mid- third generation. The first is a possible generational May (1985) and ended in late September (1985- difference in leafminer fecundity. Yamada et al. 1986) or late November (1987). In 1985 through (1986) reported marked generational differences 1988, mine samples (70-140 mines/block) were in the average fecundity of Phyllonorycter rin- taken from the OX, CV, and WW blocks at the goniella Matsumura; secbnd-generation adults had end of October or November to determine the level the highest average. However, Pottinger & LeRoux of P. elmaella and P. flavipes pupation occurring (1971) reported no differences in P. blancardella in the overwintering generation. fecundity (eggs per female) between generations. In 1987, adult P. elmaella and P. flavipes also It is unknown if the fecundity of P. elmaella varies were monitored by hanging one white sticky-trap from generation to generation. (9 by 14 cm) (Pherocon Tent Liners No. 3329-50; The second and more likely reason for the small- Zoecon Corporation, Palo Alto, Calif.) vertically in er first-to-second-generation increase in density lies the lower inner and outer regions of five sampled in the development of the apple tree canopy. For- trees (10 traps/block). The traps were placed in shey et al. (1987), working with 'Macspur' Mc- the trees on 10 April and were checked or changed Intosh apple trees in New York, reported that tree (or both) once a week until mid-November. No canopy development occurred primarily in the pheromone was used in association with the traps spring and early summer, a pattern comparable 364 ENVIRONMENTAL ENTOMOLOGY Vol. 19, no. 2
Table 1. Density of P. elmaella (x ± SE mines per leaf) per orchard block per generation from 1985 to 1987 based on weekly leaf samples
Generation Orchard blocka Year 2 3 4 OX 1985 0.059 ± 0.008 0.182 ± 0.05 2.173 ± 0.17 1986 0 0.004 ± 0.002 0.158 ± 0.07 1987 0.043 ± 0.01 0.867 ± 0.17 3.316 ± 0.27 3.731 ± 0.07 CV 1985 0.024 ± 0.002 0.085 ± 0.017 0.695 ± 0.08 1986 0 0.002 ± 0.001 0.044 ± 0.02 1987 0.011 ± 0.003 0.044 ± 0.01 0.621 ± 0.13 2.140 ± 0.21 WW 1985 0.039 ± 0.001 0.138 ± 0.02 2.012 ± 0.31 1986 0.076 ± 0.017 0.108 ± 0.028 2.202 ± 0.22 Downloaded from https://academic.oup.com/ee/article/19/2/362/468438 by guest on 25 September 2021 1987 0.026 ± 0.005 0.110 ± 0.02 1.750 ± 0.36 4.517 ± 0.27 WB 1987 0.035 ± 0.008 0.104 ± 0.02 1.446 ± 0.26 3.134 ± 0.21 Average 1985 0.041 ± 0.004 0.135 ± 0.03 1.626 ± 0.182 1986 0.076 ± 0.017 0.108 ± 0.028 2.202 ± 0.223 1987 0.028 ± 0.006 0.281 ± 0.056 1.782 ± 0.239 3.380 ± 0.75
a OX, Ox Team Orchard; CV, Columbia View Orchard; WW, Twin WW Orchard; WB, Twin WW Orchard, block B. with that occurring on 'Red Delicious' apple trees density between the first and second generations in Washington (B. H. Barritt, personal communi- appeared not to be as great as the increase between cation). Using the McIntosh data, we estimated that second and third generations, when second-generation leafminer eggs were being In 1986, the OX and CV blocks experienced an deposited from the end of May to the first of June, almost complete disappearance of populations of the number of leaves on the tree had increased P. elmaella during the first two generations (Table about 4 times over the time when first-generation 1). By the third generation, leaf miner densities had eggs were deposited (middle to late April). But increased but were stilI 14-16 times less than third- when third-generation eggs were deposited during generation levels observed in 1985. A possible rea- mid-July, the number of leaves on the tree had son for this dramatic population decline is discussed increased only about 1.1 times since second-gen- later. In 1987, populations in these two blocks had eration eggs were deposited. The greater increase recovered and their levels were comparable to those in leaf number that occurred before second-gen- observed in 1985 and similar to the concurrent eration egg deposition resulted in the distribution levels in the WW orchard, whose population was of second-generation mines over a larger area. This not affected in 1986. Because of the absence of P. had the effect of diluting the density of second- elmaella during the first half of the 1986 season in generation mines (i.e., masking the actual popu- the OX and CV blocks, further reference to 1986 lation increase from the first to the second gener- leafminer populations and PIM levels consists only ation). Consequently, the difference found in of data from the WW block unless speCified oth- erwise. Seasonal Activity of P. jlavipes. The average level of PIM usually decreased in successive gen- Tabl.e 2. Level (x ± SE percentage) of parasiloid-in- duced mortality (PIM) per orchard block per P. elmaella erations (Table 2), but an exception occurred in generation from 1985 to 1987 based on weekly mine the OX and CV sites in 1986 when third-generation samples PIM levels increased with the recovering popula- tions of P. elmaella in those orchards (see Table Orchard Generation 1). The decrease in PIM from the first to the second a year------block 2 3 4 generation ranged from 3.2% (CV, 1987) to 33.4% OX 1985 63.8 ± 3.9 40.5 ± 6.6 46.3 ± 2.6 (WW, 1986), an average decrease of 17%. How- 1986 0 3.2 ± 3.2 11.8 ± 2.8 ever, the OX block (1987) had a slight (0.4%) in- 1987 35.3 ± 7.8 35.7 ± 7.5 43.6 ± 4.1 58.5 ± 1.9 crease, Decreases in PIM from the second to the CV 1985 68.9 ± 5.9 60.8 ± 3.9 40.4 ± 3.1 third generation ranged from 7% (WW, 1986) to 1986 0 0 4.8 ± 4.8 1987 33.1 ± 9.7 29.9 ± 3.1 21.9 ± 2.6 46.3 ± 3.7 21% (WW, 1985), an average decrease of 13%. In WW 1985 67.4 ± 3.7 60.6 ± 3.1 39.3 ± 6.1 contrast, second- to third-generation PIM levels in 1986 73.7 ± 6.2 40.3 ± 5.9 33.3 ± 4.7 the OX block for all three years increased up to 1987 44.4 ± 8.2 34.8 ± 2.0 23.7 ± 3.0 34.7 ± 1.3 8%. Considering the increases in the OX block, the WB 1987 43.8 ± 9.2 37.1 ± 4.9 28.9 ± 2.7 35.5 ± 4.9 average decrease in PIM from the second to the Average 1985 66.6 ± 4.2 53.6 ± 4.2 42.3 ± 2.9 third generation became 8%. In 1987, the intra- 1986 73.6 ± 6.2 40.3 ± 5.9 33.3 ± 4.7 seasonal decline in PIM was reversed as fourth- 1987 39.2 ± 7.7 34.4 ± 3.9 29.6 ± 4.9 43.7 ± 3.9 generation levels increased 6.6% (WB) to 24% (CV)
a OX, Ox Team Orchard; CV, Columbia View Orchard; WW, from third-generation levels, an average increase Twin WW Orchard; WB, Twin WW Orchard, block B. of 14%. April 1990 BARRETT & BRUNNER: DISTRIBUTION OF P. elmaella AND P. flavipes 365
In most blocks, the highest levels of PIM oc- 100 curred when leafminer densities were at their low- 80 est (first generation) and continued to decline as leafminer densities increased (Tables 1 and 2). Some 80 leafminer studies have reported percentage par- sitism declining from the first to the second gen- 40 eration then increasing again during the overwin- 20 tering generation (Maier 1982, 1984b). In contrast, others (Ridgway & Mahr 1985, Barrett & Jorgensen 1986) have reported percentage parasitism increas- 90 i,ng from the first to the second generation and 70 W decreasing in the overwintering generation. ... Downloaded from https://academic.oup.com/ee/article/19/2/362/468438 by guest on 25 September 2021 P. elmaella. D. Phenology of There were three :E 50 ct complete generations in all sampled blocks in 1985, 1IJ 1986, and 1987; portions of a fourth generation iii 30 CI were evident in the sap-feeding and tissue-feeding ct stages. In 1985 and 1987, mine samples revealed Iii 10 > an overlap between third- and fourth-generation :J: PUPA ~ sap feeders, but not as much in 1986 (Fig. 1). This ct 50 W late summer-early fall overlap in sap-feeder phe- :J: nology and the absence of a similar condition in !z the succeeding life stages cannot be explained en- W 30 0 a: tirely as an imbrication of generations alone be- w cause of variations in development. Because the D. time needed for a cohort to complete sap-feeding g 10 development was similar to that required for the ct tissue-feeding stage (Barrett 1988), it was expected 80 that tissue feeders also would exhibit a late-season abundance, but none occurred. 60 Several studies have reported a similar late-sea- son abundance occurring in P. blancardella sap 40 feeders (Pottinger & LeRoux 1971, Baumgartner et al. 1981, Maier 1984a, Laing et al. 1986). Laing 20 et al. (1986) concluded that the generational over- o lap among P. blancardella sap feeders in Ontario MAY JUN JUL AUG SEP OCT NOV was a result of a summer diapause in that life stage. Fig. 1. Average weekly occurrence, represented as They reported that the development of 35-90% of percentage of healthy stage per sample, of P. elmaella the sap feeders in the last summer generation was sap feeders, tissue feeders, pupae, and adults in 1985 delayed until the same stage occurred in the suc- (WW, CV, OX blocks), 1986 (WW block), and 1987 ceeding, overwintering generation. This explained (WW, CV, OX, WB blocks). Late-season abundances of the preponderance of sap-feeding mines they found P. elmaella stages in 1988 (WW, CV, OX blocks) also are given. in orchards during late summer and early fall. The exact nature of how the development of these sap feeders was extended over a period of time equal healthy P. elmaella sampled in the WW block were to two generations, as well as the advantages for tissue feeders and 1% were sap feeders. During this such behavior, were unknown (Laing et al. 1986). same time, a severe winter freeze occurred. Con- Whether or not portions of P. elmaella sap feeder sequently, P. elmaella in the CV and OX blocks populations have a similar delayed development suffered high levels of mortality which may have during late summer remains to be proven, yet it caused them to be nearly absent in those two blocks represents a viable explanation for their late-season in 1986 (see Table 1). Individuals in the WW block abundance found in all the sampled blocks. also were unprepared for overwintering, but the The overwintering stage of P. elmaella is as- tissue feeders may have tolerated the cold better sumed to be the pupal stage, as for P. blancardella than sap feeders and some individuals may have and P. crataegella (Pottinger & LeRoux 1971). But been able to pupate before winter. This may partly the late-summer delay in sap feeder development explain why the population in the WW block was apparently resulted in most third- and fourth-gen- apparently not affected in 1986. In late October eration individuals being in the sap feeding or tis- 1986, 70% of healthy P. elmaella sampled from sue feeding stage when winter conditions arrived. the WW block were sap feeders and 30% were In late October 1985, 93% and 96% of healthy P. tissue feeders. In mid-November 1987, sampled elmaella sampled in the CV and OX blocks, re- individuals from the OX, CV, WW, and WB blocks spectively, were sap feeders and 7% and 4%, re- consisted of 50% sap feeders and 50% tissue feeders, spectively, were tissue feeders. In contrast, 99% of 12% sap feeders and 88% tissue feeders, 6% sap 366 ENVIRONMENTAL ENTOMOLOGY Vol. 19, no. 2
90 initiates overwintering pupation in October; >95% EGll ---0--- 1985 --0-- 'GSS of the individuals sampled were in the pupal stage 70 -1987 by mid-November. The near absence of P. elmaella in the "proper" 50 overwintering stage by late October-early Novem- ber during all three years strongly suggests that 30 relatively few individuals survive the winter. This would account for the low first-generation density 10 each year and would partially explain why the 90 forecasting of leafminer population levels from year to year and from orchard to orchard has been very 70 difficult (S. C. Hoyt, personal communication). Fu- Downloaded from https://academic.oup.com/ee/article/19/2/362/468438 by guest on 25 September 2021 ...JIII ture studies are needed to examine the nature (ini- A- :::l! 50 tiation, maintenance, and termination) of the leaf- c( en miner's overwintering mechanism and specifics of iiJ 30 Cl its overwintering mortality. Such research might c( •.... 10 provide a biological or ecological explanation for en >- a life history strategy that appears to be detrimental :I: 80 PUPA ~ to P. elmaella. c( Phenology of P. flavipes. After the first gen- w ::a: 60 eration, separation of subsequent parasitoid gen- !z erations in each stage was difficult (Fig. 2). During III 40 0 most of each season, all parasitoid stages were pres- a: III ent concurrently in the blocks. This was a result of A- 20 d a rapid developmental rate, which (if there were > c( suitable host stages available) would permit P. fla- 90 vipes to complete almost two generations in the time required for one generation of P. elmaella 70 (Barrett 1988). As P. elmaella generations became overlapped later in the season, tissue feeders were 50 available most of the time, resulting in an almost 30 continuous host resource which allowed parasitoid generations to proceed without delay. P. flavipes 10 appears to have at least the same number of gen-
M4 V JUN JUL 4UG SEP OCT NOV erations as P. elmaella. Fig. 2. Average weekly occurrence, represented as Late-season sampling showed that P. flavipes ap- percentage of healthy stage per sample, of P. fiavtpes parently overwinters either in the larval or pupal eggs, larvae, pupae, and adults in 1985 (WW, CV, OX stage. In late October 1985 in the OX, CY, and blocks), 1986 (WW block), and 1987 (WW, CV, OX, WW blocks, 41, 67, and 75%, respectively, of WB blocks).Late-season abundances of P.fiavtpes stages healthy P. flavipes were in the larval stage and 13, in 1988 (WW, CV, OX blocks) also are given. 14, and 6%, respectively, were in the pupal stage. In mid-November 1987 in the OX, CY, WW, and WB blocks, 77, 55, 61, and 50%, respectively, of feeders and 94% tissue feeders, and 82% sap feeders healthy P. flavipes were in the larval stage and 11, and 18% tissue feeders, respectively, for an average 24, 17, and 25%, respectively, were in the pupal of 21 % sap feeders and 79% tissue feeders (Fig. 1). stage. During the last week of November 1988 in Again, no overwintering pupae were found in the the OX, CY, and WW blocks, the percentage of late-season samples. However, during the last week healthy P. flavipes in the larval stage was 65, 53, in November 1988, the percentage of healthy P. and 39%, respectively, for an average of 52%, and elmaella that had pupated ranged from 5% (CY) the percentages of pupae were 23, 42, and 59%, to 27% (OX) for an average of 18% (Fig. 1). This respectively, for an average of 41% (Fig. 1). A close was still a relatively low amount, considering that relative of P. flavipes, Sympiesis marylandensis most P. elmaella should have pupated at that time Girault, also is reported to overwinter in the larval of year. In contrast, Pottinger & LeRoux (1971) or pupal stage (Pottinger & LeRoux 1971). found that in Quebec, P. blancardella individuals The ability to overwinter successfully in more of the overwintering generation began to pupate than one stage may explain why parasitoids of P. by October; 60% were in the pupal stage by late blancardella and P. ringoniella are reported to suf- November (of those P. blancardella individuals that fer less overwintering mortality than their hosts successfully pupated, 83% survived to the spring). (Pottinger & LeRoux 1971, Yamada et al. 1986). The remaining 40%, mostly tissue feeders, were Perhaps the overwintering stage for P. flavipes is dead by February. Likewise, Dutcher & Howitt not as restricted and critical for survival as it is (1978) reported that in Michigan, P. blancardella with P. elmaella. Even if only the pupal stage of April 1990 BARRETT & BRUNNER: DISTRIBUTION OF P. elmaella AND P. flavipes 367
100 1885 1887 P. tI."'ptlS _ P. 'J.vlp•• '"w u W 80 ~ P. e/m.tllI. -'D.. --0- P. ./ma.lI. c•. 35 :E II: ~ 25 ~ m ::I !:i 40 ::> ~ z C not appear to affect parasitoid activity negatively. Downloaded from https://academic.oup.com/ee/article/19/2/362/468438 by guest on 25 September 2021 Gambino, P. & D. J. Sullivan. 1982. Phenology of The levels of PIM in the WW block were com- emergence of the spotted tentiform leaf miner, Phyl- parable with PIM levels in the insecticide-free WB lonorycter crataegella (Lepidoptera: Gracillariidae), block (seven rows south of the WW block) as well and its parasitoids in New York. J. N.Y. Entomo!. Soc. as in the other blocks (Table 2). Apparently the 90: 229-236. codling moth can be controlled chemically without Gibb, T. J. 1983. Biology of the western tentiform disrupting the biological control of P. elmaella by leafminer, Phyllonorycter elmaella in Utah. M.S. the- P. flavipes. Despite the inability of P. flavipes to sis, Brigham Young University, Provo, Utah. regulate P. elmaella populations, its conservation Hoyt, S. 1983. Biology and control of the western is recommended. It is likely that levels of P. el- tentiform leafminer. Proc. Wash. St. Hortic. Assoc. 79: 115-118. maella in commercial apple orchards would reach Johnson, E. F., J. E. Laing & R. Trottier. 1976. The treatment threshold densities in the absence of P. seasonal occurrence of Lithocolletis blancardella flavipes. (Lepidoptera: Gracillariidae), and its major natural enemies in Ontario apple orchards. Proc. Entomo\. Acknowledgment Soc. Ont. 107: 31-45. We thank Stanley Hoyt, Alan Berryman, and Garrell Laing, J. E., J. M. Heraty & J. E. Corrigan. 1986. Long (Department of Entomology, Washington State Summer diapause in Phyllonorycter blancardella University) for their critical reviews. We also thank Rob- (Fabr.) (Lepidoptera: Gracillariidae) in Ontario. Can. ert Fairchild and Lynn Smith, Tree Fruit Research and Entomo\. 118: 17-28. Extension Center, for their field and laboratory assis- Maier, C. T. 1982. Parasitism of the apple blotch tance. We acknowledge the Washington Tree Fruit Re- leafminer, Phyllonorycter crataegella, on sprayed and search Commission, which provided funding for this unsprayed apple trees in Connecticut. Environ. Ento- project (1477). mo\. 11: 603-610. 1984a. Seasonal development and flight activity of References Cited the spotted tentiform leafminer, Phyllonorycter blan- cardella (Lepidoptera: Gracillariidae), in Connecti- Barrett, B. A. 1988. The population dynamics of Pni- cut. Can. Entomo!. 116: 435-441. galio j1avipes (Hymenoptera: Eulophidae), the major 1984b. 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