J. New York Entomol. Soc. 99(4):654-663, 1991 OVIPOSITION BEHAVIOR OF THE APPLE BLOTCH LEAFMINER, PHYLLONORYCTER CRATAEGELLA (CLEMENS) (LEPIDOPTERA: GRACILLARIIDAE) Thomas A. Green and Ronald Prokopy J. Department of Entomology, University of Massachusetts, Amherst, Massachusetts 01003 — Abstract. Observations ofoviposition by apple blotch leafminer moths, Phyllonorycter cra- taegella (Clemens), on apple foliage in the field and in the laboratory indicated oviposition occurred solely on the undersides of leaves, and primarily on the middle third of the leaf (between petiole and apical tip), midway between the mid-vein and margin. A stereotypical sequence ofevents lastingca. 1 min was observed prior to eggdeposition. This included walking while tapping the leafunderside with the antennae, probing a small area (ca. 1 cm2) ofthe leaf with the ovipositor, and violent side-to-side shaking ofthe abdomen at egg deposition. Results of choice tests in the laboratory suggest apple blotch leafminer moths do not discriminate against oviposition sites previously occupied by freshly deposited conspecific eggs. Our results indicate commercial apple growers may improve control of this pest by applying adulticides just prior to or during the first warm, calm evening in early spring when foliage and leafminer adults are present. The apple blotch leafminer, Phyllonorycter crataegella (Clemens) (ABLM), one of several gracillariid species infestingapple in North America, is distributed throughout much of New England, west to the Hudson River Valley, and south to Virginia (Beckham et al., 1950; Weires et al., 1980; Coli and Prokopy, 1982; Maier, 1983; Van Driesche and Taub, 1983). It parasitizes at least 17 host plants in 7 genera in New England (Maier, 1985). The ABLM completes three generations per year, with the first adults emerging in early spring from pupae in the previous season’s leaves. ABLM Female deposit eggs singly on the undersides ofhost leaves from mid- to late ABLM afternoon until dark (Green and Prokopy, 1984). Adult and larval mines are concentrated in the lower part ofapple tree canopies in commercial orchards during the first generation, spreading upwards in succeeding generations (Beckham et al., 1950; Green et al., 1987). ABLM has achieved major pest status in commercial apple orchards in New York and New England over the past 13 years due to its development of resistance to organophosphate insecticides (Weires, 1977; Weires et al., 1982; Van Driesche et al., 1985). Heavy infestations can cause premature fruit ripening and drop, reduced fruit size and reduced fruit set the following season (Reissig et al., 1982). The oviposition behavior of this insect may have important implications for pest management pro- grams (Green et al., 1987). Competition for resources could be more important for leaf-mining insects than for species that are more mobile in larval stages (Bultman and Faeth, 1985), as leafminers typically spend their entire larval life within one leafor portion ofa leaf. Intraspecific competition has been demonstrated for other leaf-mining insects (Parel- 1991 OVIPOSITION BEHAVIOR 655 la, 1983; Quiring and McNeil, 1984; Potter, 1985), including gracillariid species (Martin, 1956; Bultman and Faeth, 1986). Ifcompetition is important, evolution may favor the development ofmechanisms allowing individuals to detect and avoid resources already occupied by conspecifics (Prokopy, 1972; McNeil and Quiring, 1983; Prokopy et al., 1984). Some of these mechanisms may have potential in pest management programs (Prokopy, 1981; Roitberg and Prokopy, 1987). The objectives ofthe following study were to describe the oviposition behavior of female ABLM, and examine possible discrimination against host leaves previously occupied by conspecific eggs. MATERIALS AND METHODS ABLM All observations of oviposition in the field (experiment 1) were conducted in commercial apple orchards in New England during 1983 and 1984, as part of a larger study ofABLM behavior (Green and Prokopy, unpubl. data). An area within the canopy of an apple tree was selected at random, and the undersides of leaves ABLM were searched until an adult was located. The activity of the moth was recorded for 5 min, or until the moth flew out ofsight ofthe observer. We recorded the number ofovipositions, leaves visited, repeat visits to the same leaf, and whether a moth arrived on a leafby flight or by walking. ABLM observed in the laboratory (experiments 2, 3, 4) were collected as pupae in leaves from commercial apple orchards in western Massachusetts. The portions of leaves containing mines were held individually in 30 ml plastic cups until adult emergence. Upon emergence, males and females were placed collectively in a 3.8 1 glass jar, the opening of which was covered with organdy cloth to permit air circu- lation. Each morning, mating pairs were removed from thejar and placed in the cups ABLM until females were used for experimentation the following day. Throughout, adults were provided free access to spring-water-soaked dental wicks, and maintained undernatural lighting in front ofa large screened window. All laboratory experiments, conducted on a table placed in front ofthis window, occurred from 600-2 00 hours 1 1 ABLM (Eastern Standard Time), the time of peak oviposition in the field (Green and Prokopy, unpubl. data). Foliage used in laboratory experiments was collected daily from unsprayed apple trees and carefully examined to exclude leaves with leafminer eggs or larval mines. Only basal leaves (or fruit cluster leaves, experiment 4) of growing terminals were selected for use in the choice tests to provide uniform leaf age and quality. Leaves were maintained on the terminals, held in water-filled vials. Average leaf size in experiments 2 and 3 was 6.2 by 4.2 cm. Duringthe summerof 984, 23 ABLM were observed individually in the laboratory 1 for 3 hr each (experiment 2). Each moth was held in a vertical cylindrical cage of clear acetate (14 cm diameter, 25 cm height), containing an apple terminal with 8 leaves. The base of the terminal extended through a hole in the floor of the cage (a plasticpetri dish bottom) into a vial containingwater. The top ofthe cage was covered ABLM with organdy cloth to allow air circulation. females were placed singly in a stoppered vial within the cage, and were allowed to acclimate for 5 min before the cotton stopper was removed (remotely, by pulling a string) and observations were 656 JOURNAL OF THE NEW YORK ENTOMOLOGICAL SOCIETY Yol. 99(4) begun. The number and sequence ofleafvisits, number and location ofovipositions, and the sequence of behaviors involved in oviposition were timed and recorded. After 3 hours, the moth was removed from the cage. The number of ovipositions was confirmed by examination of leaves under a microscope, and the length and width ofeach leafwas measured and recorded. The location ofthe first egg only (to eliminate any influence ofprevious ovipositions) on each leafwas plotted according to distance from petiole, margin, and midrib. In experiment 3, conducted during the summer of 1984, individual ABLM females (caged as in experiment 2) were provided with a terminal of2 leaves, one containing or 8 ABLM eggs (oviposited <30 hr previously) and one without prior ovipositions 1 (=clean). Each female was observed 30 min or until the first oviposition. Each female was pre-tested by being allowed to oviposit freely on a clean leafuntil it left the leaf. Only females which oviposited at least once in the pretest were used in the experiment. ABLM In experiment 4, conducted in July of 1987, individually-caged females were provided with 2 small leaves (average size 2.3 by 1.4 cm), one clean and one with 1 or 2 prior ovipositions. The leafhalf(right or left ofthe midvein) containing ABLM or receiving eggs was noted. females were pre-tested by being offered 3 pairs ofclean leaves in succession, the next pair being offered after one oviposition. Only females which oviposited three times prior to the assay were used. RESULTS ABLM In commercial apple orchards, 25 females were observed exhibiting ovi- position behavior (Table 1), all between 1645 and 2035 hours. Of the 25, 8 moths were observed probing the leaf underside with the ovipositor but did not oviposit while under observation. All ovipositions occurred on the undersides of leaves, though arrival was on the upper surface ofleaves in about halfofall visits (N = 102 total visits). Overall, 19.1% of leaves visited received an egg, and 8.8% of all leaf visits were repeat visits by the same female to the same leaf. No moths oviposited more than once per leaf visit. In one instance a second egg was placed on a leaf previously oviposited on by the same female during a prior visit. About two-thirds ofleafvisits were via walking from the stem or adjacent leaves (Table 1), and about one-third were by flight. Repeated attempts to observe oviposition in the laboratory under artificial lighting were unsuccessful, although females confined for several days with foliage under We those conditions did eventually oviposit. succeeded in observing oviposition by offering foliage to females in front of a screened window, under natural lighting, temperature, and humidity, and during the time period within which oviposition occurs in the field. Of the 23 moths observed in the laboratory for 3 hr, 19 visited foliage and 15 oviposited at least once, for an overall average of 6.7 eggs per female (range = 0- 20). After tarsal contact with a leaf, females spent an average of 30 s (±3.1 s, SE) walking on the leaf, during which they continuously tapped the leafsurface with the antennae, gradually narrowingdown the area “searched” bywalking in an increasingly tightercircle. Once ovipositorcontact with the leafoccurred, females spent an average of 29 s (±3.4 s) probing a small area of the leaf (ca. < 1 cm2) with the ovipositor, often taking short, backward steps. This period ended with the abdomen bent at a 1991 OVIPOSITION BEHAVIOR 657 ABLM Table 1. Observations of exhibiting oviposition behavior (=ovipositor in contact with leaf) in commercial apple orchards in New England, 1983-1984.a Mean per moth (±SE) Minutes observed 3.7 ± 0.69 Number leafvisits 4.1 ± 0.52 Number different leaves visited 3.8 ± 0.47 Number ovipositions observed 0.8 ± 0.62 Proportion ± SE Proportion leaves visited By walking 69.6 ± 0.01 By flight 30.4 ± 0.01 a Twenty-five moths were observed individually for 5 min or until leaving sight ofobserver. ABLM Data include 9, 12 and 4 during first through third generations, respectively. near 90° angle to the rest of the body and the ovipositor firmly planted against the underside ofthe leaf. The female then shook violently 3-5 times from side to side, for a total of about 1 s, after which time the egg was deposited on the leaf surface. The moth then quickly lifted the abdomen and ovipositor off the leaf surface, and crawled away from the egg an average of 13.1 s (±3.4 s) after the ovipositor was firmly in place on the leaf underside. On the first leafvisit by laboratory-observed moths, females frequently oviposited more than once before leaving (mean 1.7 eggs/first leaf visit/female). They did so much less frequently on subsequent leaf visits (mean 0.7 eggs/leaf visit/female). Among the 15 replicates in which oviposition occurred, 78% of leaf visits did not result in an oviposition. Females oviposited significantly more eggs (P < 0.5, (T-test, Sokal and Rohlf, 1981) on the middle of three lateral sections of the leaf (sectioned perpendicular to mid- vein, Fig. 1a), and the second and third quarters longitudinally (sectioned parallel to mid-vein, Fig. lb). Among the 8 leaves on each terminal, no preference was exhibited for any particular leaf position relative to the most basal or apical leaf. In experiment 3, no significant differences were detected in the number of new ovipositions on clean leaves vs. leaves with one (N = 26) or eight prior ovipositions (N = 29), although substantially more new eggs were placed on clean leaves vs. leaves ABLM with 8 prior ovipositions (19 vs. 10, respectively). females oviposited on the first leaf visited (53 of 55 replicates, or 96%), regardless of the presence or absence ABLM ofprior ovipositions. For some unknown reason, females were not nearly as selective as they were in the field or in experiment 2, where only 19% and 32% of leaf visits resulted in oviposition, respectively. Resolving these concerns was the rationale for the final experiment, in which small leaves were used and the leaf-half receiving the new egg was noted (Table 2). By restricting the amount ofleafarea available and comparing oviposition on the basis of a portion of the leaf, discrimination by females against small occupied areas of the leaf might become apparent. Pretesting each female on 3 clean leaves (vs. only 1 in experiment 3) was intended to accentuate “choosiness” by reducing any effect of oviposition deprivation and by providing uniform pre-assay oviposition experi- ence which could be necessary for recognition ofconspecific eggs or host markers. 658 JOURNAL OF THE NEW YORK ENTOMOLOGICAL SOCIETY Vol. 99(4) b. ABLM Fig. 1. Lateral (a) and longitudinal (b) distribution of eggs according to leafsurface area ±SE. Eggs deposited during 3 hr observations in laboratory. Only the first egg deposited on any leafwas included, N = 58 eggs, 15 moths. “Choosiness” was greater in this experiment (56% of leaf visits resulted in an oviposition) than in experiment 3, but still not equal to levels observed in orchards or in experiment 2. The first leaf visited received the first oviposition in 56% of all replicates. No discrimination was detected against entire leaves or leafhalves containing one or two previous ovipositions. Leaves with one prior oviposition received new eggs as often as did clean leaves (Table 2). Of the 14 new eggs placed on leaves with a prior oviposition, 7 were placed on the same half(right or left side ofthe mid-vein) of the leaf underside as the initial egg. Leaves with 2 prior ovipositions received significantly more new eggs than did clean leaves. DISCUSSION Results of this study agree with observations by Beckham et al. (1950) of a con- ABLM centration of oviposition by on the mid-section of the leaf. Pottinger and 1991 OVIPOSITION BEHAVIOR 659 ABLM Table 2. Comparison ofoviposition by individually caged females provided with 2 leaves, one free ofconspecific eggs (=:clean) and one with 1 or 2 ABLM eggs deposited <30 hr previously. For leaves with prior oviposition, comparison is between halves of leaves (leaf divided by the midvein) receiving the new egg. Leafreceivingnew egga Treatment N With egg(s) Clean previous egg 28 14a 14a 1 2 previous eggs 13 11a 2b Leafhalfreceiving new egg Halfwith egg(s) Clean half previous egg 14 7a 7a 1 2 previous eggs 7 5a 2a ABLM a First egg on leaf only. were allowed a single oviposition on each of 3 clean leaves <30 min prior to testing. Data within a row and followed by the same letterare not significantly different (P > 0.05, G-test, Sokal and Rohlf 1981). LeRoux (1971) found no preference for the proximal or distal leaf half in a related species, the spotted tentiform leafminer (STLM), P. blancardella (F.), but they did not report distribution by thirds as presented here. Otherwise, their description of oviposition behavior is similar to what we observed in ABLM. They speculated that the violent side-to-side shaking by females immediately prior to egg deposition might clear the leaf surface and/or ready the egg for deposition. The extent and importance of inter- and intraspecific competition in regulating natural populations has been a topic ofconsiderable interest in the recent literature (Lawton and Strong, 1981; Schoener, 1982, 1983). Intraspecificcompetition for larval resources is unlikely in leafminer populations maintained at low densities by natural ABLM enemies (Faeth and Simberloff, 1981). Regulation of population densities by parasites has been noted by many workers (Dean, 1940; Gambino and Sullivan, 1982; Maier, 1982; Van Driesche and Taub, 1983; Van Driesche et al., 1985; Drum- mond et al., 1985). However, competition might occur, even at low ABLM densities, ifthe supply of superior leaves or portions of leaves is limiting. ABLM As in mostbutnotall lepidopteranleafminers (Gross, 1986), the is restricted for its entire larval life to one portion ofa leaf(larvae do not cross major leafveins), ABLM chosen by the female adult. Results of this and previous studies indicate females oviposit preferentially on the mid-section of leaves, within the interior half of the tree canopy throughout the season, and in the lower portion of the canopy during the first generation (Beckham et al., 1950; Green and Prokopy, unpubl. data). This part of the canopy may be preferred due to less wind interference with ovipo- sition, closer proximity to emergence sites (Beckham et al., 1950), or a reduced tendency for interior leaves to abscise prior to completion of larval development (Bultman and Faeth, 1986b). Other factors that might limit availability of favorable oviposition sites include the lesser amount of apple foliage in early spring and proximity to shelter (Martin, 1956). Selection of leaves by leafminers according to leaf size (Bultman and Faeth, 1986a), nutrient content, or exposure to the sun (Faeth et al., 1981), or selection against leaf noxious compounds or damaged leaves (Faeth, 1985) may also occur. 660 JOURNAL OF THE NEW YORK ENTOMOLOGICAL SOCIETY Vol. 99(4) The “choosiness” ofABLM noted here (i.e., visitingmany leaves without ovipositing, Table 1), suggests that these or other factors may operate in ABLM oviposition site selection. Restricted availability ofsuperior oviposition sites may lead to over-utilization of existing sites. Interference competition among larvae, including cannibalism, has STLM been demonstrated in other gracillariids, including (Pottinger and LeRoux, 1971) and the aspen blotch leafminer, P. salicifoliella (Chambers) (Martin, 1956), and in the dipteran leafminers Agromyzafrontella (Rondani) (Quiring and McNeil, 1984) and Liriomyza trifolii(Burgess) (Parrella, 1983). Interference competition with- out cannibalism has been observed in another dipteran, the native holly leafminer, Phytomyza ilicicola Loew (Potter, 1985). Besides cannibalism, the presence of con- specifics may also result in a general depletion of resources, leaf abcission, or in induction of plant defenses. Possible restricted availability of favorable oviposition sites, limited mobility of ABLM larvae and adults (Beckham et al., 1950; Green and Prokopy, 1986), and relatively permanent host plants (present over 3 generations) are ecological charac- teristics which have been positively correlated with host marking ability, used to avoid reduced fitness or mortality due to overcrowding in other species (Prokopy, ABLM 198 Roitbergand Prokopy, 1982, 1987). The broad host range of (17 species, 1; Maier, 1985) is one characteristic not generally found in species which mark hosts. ABLM Given the concentrated searching behavior by prior to oviposition coupled ABLM with the presence of eggs on the surface ofthe leaf(as opposed to eggs inserted internally), host marking may not be required for ABLM to recognize previously occupied sites. Energetic costs and potential costs due to use of host-marking cues by natural enemies may outweigh any benefits (Roitberg and Prokopy, 1987). Oviposition twice on the same leaf by a single female in the field (experiment 1), ABLM lack ofdiscrimination by females against leaves with one egg (experiment 3), concentrated “searching” behavior over a small leafarea prior to oviposition in the ABLM lab (experiment 2) and the ability of a single apple leaf to support several larvae (Reissig et al., 1982) suggest that the biologically significant unit chosen for egg laying by a female may be a portion of the leaf rather than the entire leaf. The substantially though not significantly greater new oviposition on clean leaves vs. leaves with 8 prior ovipositions (experiment 3) suggested possible discrimination on the basis of prior egg density. However, in all but 2 of the replicates, the first leaf visited received the first oviposition. Any discrimination against the leaves with 8 prior ovipositions would have been on the basis ofcues other than contact with the leaf or eggs. The significant preference for leaves with 2 prior ovipositions suggests that some other factors, possibly related to leafquality per se, may be more important in ABLM selection ofleaves foregg layingthan the presence ofconspecificeggs, orthat clumping of eggs may be advantageous. Alternative hypotheses for the apparent failure of ABLM females to discriminate against previously egg-occupied host leaves or parts ofhost leaves include (1) reduced “choosiness” in this assay; (2) discrimination only at egg densities greater than those tested, or only against sites occupied by larvae or by eggs that are more mature; (3) a conspecific egg recognition/discrimination system may not have developed in ABLM because ofinsufficient selection pressure for such a system. 1991 OVIPOSITION BEHAVIOR 661 ABLM mate at temperatures at least as low as 7°C (Green and Prokopy, unpubl. data), but oviposition by ABLM and STLM may be restricted to periods of higher temperature (>9-15°C) and low wind speeds (Trimble, 1986; Green and Prokopy, ABLM unpubl. data). Therefore, a considerable buildup ofmated female in sheltered locations may be possible until conditions are appropriate for oviposition. Once these ABLM conditions occur, females are capable of ovipositing up to 20 eggs each (average = 6.7 eggs per female) during a single 3-hr period. Thus, when needed, ABLM orchardists should apply adulticides against just prior to or during the first warm (>9-12°C), calm evening in the spring when foliage and ABLM adults are present. ABLM Aspects needing additional work include examination ofthe distribution of eggs and larvae in the field for clumped, random or uniform dispersion, density dependent effects on larvae occurring from presence ofconspecifics on the same leaf or different leaves on the same tree, and possible discrimination by ovipositing adults against leaves or portions ofleaves occupied by larvae or by more mature conspecific eggs. LITERATURE CITED Beckham, C. M., W. S. Hough and C. H. Hill. 1950. Biology and control of the spotted tentiform leaf miner on apple trees. Va. Agric. Exp. Stn. Tech. Bull. 1 14:1-19. Bultman, T. L. and S. H. Faeth. 1985. Patterns ofintra- and interspecific association in leaf- mining insects on three oak host species. Ecol. Entomol. 10:121-129. Bultman, T. L. and S. H. Faeth. 1986. Experimental evidence for intraspecific competition in a lepidopteran leafminer. Ecology 67:442-448. Bultman, T. L. and S. H. Faeth. 1986a. Leafsize selection by leaf-mining insects on Quercus emoryi (Fagaceae). Oikos 46:31 1-316. Bultman, T. L. and S. H. Faeth. 1986b. Selective oviposition by a leaf miner in response to temporal variation in abscission. Oecologia 69:1 17-120. Coli, W. M. and R. J. Prokopy. 1982. Biology, monitoring and control of leafminers in Massachusetts. Proc. Mass. Fruit Growers Assoc. Annu. Meet. 86:30-44. Dean, R. W. 1940. Spotted tentiform leafminer. Proc. N.Y. State Hortic. Soc. 85:192-193. Drummond, F. A., R. G. Van Driesche and P. A. Logan. 1985. Model for temperature- dependent emergence of overwintering Phyllonorycter crataegella (Clemens) (Lepidop- tera: Gracillariidae), and its parasitoid Sympiesis marylandensis Girault (Hymenoptera: Eulophidae). Environ. Entomol. 14:305-311. Faeth, S. H. 1985. Host leafselection by leafminers: interactions among three trophic levels. Ecology 66:870-875. Faeth, S. H. and D. S. Simberloff. 1981. Population regulation of a leaf-mining insect, Ca- meraria sp. nov., at increased field densities. Ecol. 62:620-624. Faeth, S. H., S. Mopper and D. S. Simberloff. 1981. Abundances and diversity ofleaf-mining insects on three oak host species: effects of host plant phenology and nitrogen content ofleaves. Oikos 37:238-251. Gambino, P. and D. J. Sullivan. 1982. Phenology of emergence of the spotted tentiform leafminer, Phyllonorycter crataegella (Lepidoptera: Gracillariidae) and its parasitoids in New York. J. N. Y. Entomol. Soc. 90:229-236. Green, T. A. and R. J. Prokopy. 1984. Daily activity ofapple blotch leafminer adults. Mass. Fruit Notes 49:19-22. Green, T. A. and R. J. Prokopy. 1986. Visual monitoring trap for the apple blotch leafminer 662 JOURNAL OF THE NEW YORK ENTOMOLOGICAL SOCIETY Vol. 99(4) moth, Phyllonorycter crataegella (Lepidoptera: Gracillariidae). Environ. Entomol. 15: 562-566. Green, T. A., S. L. Butkewich, W. M. Coli, K. Leahy and R. J. Prokopy. 1987. Monitoring and control ofapple blotch leafminer: an update. Mass. Fruit Notes 52:12-15. Gross, P. 1986. Life histories and geographic distributions oftwo leafminers, Tildenia georgei and T. inconspicuella (Lepidoptera: Gelechiidae), on solanaceous weeds. Ann. Entomol. Soc. Am. 79:48-55. Lawton, J. H. and D. R. Strong, Jr. 1981. Community patterns and competition in folivorous insects. Amer. Nat. 1 18:317-338. Maier, C. T. 1982. Parasitism of the apple blotch leafminer, Phyllonorycter crataegella, on sprayed and unsprayed apple trees in Connecticut. Environ. Entomol. 1 1:603-610. Maier, C. T. 1983. Relative abundance of the spotted tentiform leafminer, Phyllonorycter blancardella (F.), and the apple blotch leafminer, P. crataegella (Clemens) (Lepidoptera: Gracillariidae) on sprayed and unsprayed apple trees in Connecticut. Ann. Entomol. Soc. Am. 76:992-995. Maier, C. T. 1985. Rosaceous hosts ofPhyllonorycter species (Lepidoptera: Gracillariidae) in New England. Ann. Entomol. Soc. Am. 78:826-830. Martin, J. L. 1956. The bionomics ofthe aspen blotch miner, Lithocolletissalicifoliella Cham. (Lepidoptera: Gracillariidae). Can. Entomol. 88:155-168. McNeil, J. N. and D. T. Quiring. 1983. Evidence ofan oviposition-deterring pheromone in the alfalfa blotch leafminer, Agromyza frontella (Randani) (Diptera: Agromyzidae). En- viron. Entomol. 12:990-992. Parrella, M. P. 1983. Intraspecific competition among larvae of Liriomyza trifolii (Diptera: Agromyzidae). Ann. Entomol. Soc. Am. 78:429-432. Potter, D. A. 1985. Population regulation of the native holly leafminer, Phytomyza ilicicola Loew (Diptera: Agromyzidae), on American holly. Oecologia 66:499-505. Pottinger, R. P. and E. J. LeRoux. 1971. ThebiologyanddynamicsofLithocolletisblancardella (Lepidoptera: Gracillariidae) on apple in Quebec. Mem. Entomol. Soc. Can. 77. 437 pp. Prokopy, R. J. 1972. Evidence for a marking pheromone deterring repeated oviposition in apple maggot flies. Environ. Entomol. 1:326-332. Prokopy, R. J. 1981. Epideictic pheromones that influence spacing patterns ofphytophagous insects. Pages 181-213, in: D. A. Nordlung (ed.), Semiochemicals: Their Role in Pest Control. Wiley & Sons, Inc., N.Y. Prokopy, R. J., B. D. Roitberg and A. L. Averill. 1984. Resource partitioning. Pages 301- 330, in: W. J. Bell and R. T. Carde (eds.), Chemical Ecology of Insects. Chapman and Hall Ltd., London. Quiring, D. T. and J. N. McNeil. 1984. Exploitation and interference intraspecific larval competition on the dipteran leafminer, Agromyza frontella (Rondani). Can. J. Zool. 62: 421-427. Reissig, W. H., R. W. Weires and C. G. Forshey. 1982. Effects ofgracillariid leafminers on apple tree growth and production. Environ. Entomol. 1:958-963. 1 Roitberg, B. D. and R. J. Prokopy. 1982. Resource assessment by adult and larval codling moths. J. N.Y. Entomol. Soc. 90:258-265. Roitberg, B. D. and R. J. Prokopy. 1987. Insects that mark host plants. BioScience 37:400- 406. Schoener, T. W. 1982. The controversy over interspecific competition. Amer. Scientist 70: 586-595. Schoener, T. W. 1983. Field experiments on interspecific competition. Amer. Nat. 122:240- 285. Sokal, R. R. and F. J. Rohlf. 1981. Biometry, 2nd. ed. Freeman, San Francisco. Trimble, R. M. 986. Effect oftemperature on oviposition and eggdevelopment in the spotted 1 tentiform leafminer, Phyllonorycter blancardella (Lepidoptera: Gracillariidae). Can. En- tomol. 18:781-787. 1 1991 OVIPOSITION BEHAVIOR 663 Van Driesche, R. G. and G. Taub. 1983. Impact ofparasitoids on Phyllonorycter leafminers infesting apple in Massachusetts, U.S.A. Prot. Ecol. 5:303-317. Van Driesche, R. G., J. M. Clark, M. W. Brooks and F. J. Drummond. 1985. Comparative toxicity oforchard insecticides to the apple blotch leafminer, Phyllonorycter crataegella (Lepidoptera: Gracillariidae), and its eulophid parasitoid, Sympiesis marylandensis (Hy- menoptera: Eulophidae). Econ. Entomol. 78:926-932. J. Weires, R. W. 1977. Control of Phyllonorycter crataegella in eastern New York. J. Econ. Entomol. 70:521-523. Weires, R. W., D. R. Davis, J. R. Leeperand W. H. Reissig. 1980. Distribution and parasitism of gracillariid leafminers on apple in the northeast. Ann. Entomol. Soc. Am. 73:541— 546. Weires, R. W.,J. R. Leeper, W. H. ReissigandS. E. Lienk. 1982. Toxicityofseveralinsecticides tothe spottedtentiform leafminer(Lepidoptera: Gracillariidae)anditsparasite,Apanteles ornigis. J. Econ. Entomol. 75:680-684. Received 23 October 1989; accepted 21 February 1991.