LIFE HISTORY AND SEASONAL DEVELOPMENT OF THE WESTERN WINTER , OCCIDENTALIS (: GEOMETRIDAE), IN WESTERN OREGON' JEFFREYC. MILLERand JANE. CRONHARDT Department of Entomology, Oregon State University, Corvallis, Oregon 97331

Abstract Can. Ent. 114: 62%636 (1982) In western Oregon, Operophtera occidentalis (Hulst) has four larval instars, is univoltine, and polyphagous. Adult activity peaked in early December, eggs overwintered, larvae were present from March to June, and pupae from May to December. Temperature thresholds for egg and larval development were estimated to be 2°C. Few species of natural enemies were observed and rates of parasitism averaged 2%. Resume Dans l'ouest de I'Oregon, Operophtera occidentalis (Hulst) passe par 4 stades larvaires, est univoltine et polyphage. L'activitk des adultes est passke par un sommet t6t en dicembre, les oeufs ont hivernk, les larves ont it6 observkes de mars a juin et les chrysalides de mai a dicembre. Les seuils themiques pour le dCveloppement de l'oeuf et le dCveloppement larvaire ont it6 estimis 2 2OC. Peu d'espkces d'ennemis naturels ont Ctk observies et les incidences de parasitisme Ctaient de 2% en moyenne

Introduction The genus Operophtera has four species in northwestern North America, three of which are native to North America. The western , 0. occidentalis (Hulst), and Danby's winter moth, 0. danbyi (Hulst), appear to be endemic to the Pacific Northwest while the Bruce spanworm, 0. bruceata (Hulst), has a northern distribution throughout the Nearctic region. The European winter moth, 0. brurnata (L.), is presumed to have been introduced from Europe into Nova Scotia prior to 1949 (Smith 1950) and is presumed to have occurred in British Columbia before 1972 (Gillespie et al. 1978) and in Oregon as early as 1958 (Ferguson 1978). Studies on 0. bruceata and 0. brumata have been conducted in North America by Brown (1962), Cuming (1961), Eidt and Embree (1968), Eidt et al. (1966), Embree (1966, 1967, 1970, 1971), Gillespie and Finlayson (1981), MacPhee (1967), and Sanford and Herbert (1966). These studies document a general life history as follows: mated, brachypterous females are active in the winter and deposit eggs which overwinter on the trunk and branches of deciduous trees; larvae emerge in the spring and feed on blossoms and foliage through four (0. bruceata) or five (0. brumata) instars; pupae occur in the soil through summer and early fall and adults emerge in late fall and early winter. Few native natural enemies of Operophtera have been found in North America. The biology of 0. occidentalis has not been documented as well as its congeners. A review of the literature on the biology of 0. occidentalis indicated only that adults occur in the late fall and early winter, and that larvae feed on leaves of various deciduous trees and shrubs (McFarland 1963; Sugden 1966; Tietz 1972; Furniss and Carolin 1977). A reference to 0. occidentalis larvae occurring on conifers and adults occurring in April does not conform to the general ecological characteristics of other Nearctic Operophtera (see Prentice 1963). These data suggest that additional research is needed and that the native 0. occidentalis and the exotic 0. brumata (which are presently sympatric in parts of Oregon) may be similar in

'Technical paper No. 5978. the Oregon Agricultural Experiment Station. 630 THE CANADIAN ENTOMOLOGIST July 1982 the ecology of their development. The degree of similarity in the ecology of Operophtera species is of importance as it affects the feasibility of biological control of 0. brumata in Oregon. This paper reports the life history and seasonal devel- opment of 0.occidentalis in western Oregon.

Methods Field. The life history of 0. occidentalis was investigated in western Oregon from the fall of 1979 through the spring of 1981. Principal field sites were in MacDonald Forest, 9.6 km northwest of Corvallis, Benton County, and in West Salem, 59 km distant in Polk County. The MacDonald Forest site (ca. 17,000 ha) was a mixed coniferous forest dominated by Douglas-fir, Pseudotsuga menziesii (Mirb.) Franco, with a mixture of deciduous trees, primarily oak, Quercus garryana Dougl.; maple, Acer macrophyllum Pursh; ash, Fraxinus latifolia Benth.; alder, Alnus rubra Bong.; hazel, Corylus cornuta Marsh var. californica (A.DC.) Sharp; and cherry, Prunus emarginata (Doug.) Walp. The Salem site was a commercial sweet cherry orchard (ca. 10 ha) with an adjacent stand (ca. 3 ha) of mixed deciduous trees primarily maple, oak, and hazel. Adults were collected with nets, beating sheets, emergence net traps (see Briggs 1957), and sticky band traps. Eggs and larvae were collected by clipping selected foliage and twigs in the field for evaluation in the laboratory. Also, a beating sheet and sweep net were used to collect larvae. Pupae were collected by sifting soil from 0.5 d trays which were placed in the field. Adult development was monitored between October and January with 30 sticky band traps twice a week in 1979 and 81 traps once a week in 1980. Larval development was monitored by collecting (at the Salem site) 80 leaf clusters twice a week from the same set of 10 trees through the spring of 1980. Also, 80 leaf clusters were collected twice a week from a single tree chosen at random. Through the spring of 1981, 175 leaf clusters were collected once a week from the same set of five trees. Larval development was also observed outside of the Salem site. Leaf clusters from a variety of plant species were collected for in field and laboratory evaluation. Laboratory. A culture of 0. occidentalis was started in the fall of 1979 and maintained for three generations. Field-collected adults were observed and reared under conditions of 4-6"C, 12L:12D photoperiod. Field-collected eggs and larvae were reared separately at 16"C, 14L: 10D photoperiod, and 70-85% relative humidity. Parasitoids reared from these larvae were preserved and were added to the laboratory culture. Adults used for laboratory observations on longevity and fecundity were obtained from larvae collected in the field during the previous generation, or from adults collected directly from the field. The developmental requirements of the eggs and larvae of 0. occidentalis were investigated under constant temperatures of 4", lo0, 16", 22", 28", and 34°C. Relative humidity ranged between 70% and 85% and the photoperiod was 14L:lOD. Eggs and larvae used in this study were F, progeny of field-collected adults. A total of 231 eggs were held at 4"-6'C for 3 months and then placed individually in one of the six constant temperature cabinets. At least 3 1 eggs were used in each temperature treatment. Eggs were observed at 12 h intervals until hatch or death due to desic- cation, which was indicated by collapse. A total of 192 larvae were placed indi- vidually in one of the six temperature cabinets. At least 29 larvae were placed in each cabinet except the 34°C cabinet which had only 19. The larvae were fed fresh, Volume 114 THE CANADIAN ENTOMOLOGIST 63 1 young cherry leaves as a standard diet and observed at 12 h intervals until death or pupation. Climatological data for field studies were obtained for the Salem airport from the National Oceanic and Atmospheric Administration.

Results and Discussion Sampling techniques. The technique most productive for collecting both male and female moths was sticky bands around tree trunks about m from the ground. However, specimens were damaged and not suitable for behavioral studies. Males for behavioral studies were captured with an aerial net just after dusk and females by beating tree branches over drop cloths. The stationary net trap described by Briggs (1957) did not capture as many females as did the other techniques. Eggs and larvae of all age classes were most easily collected by clipping branches from trees and inspecting blossom/leaf clusters in the laboratory. Middle and late instar larvae could be located easily by searching for foldedltied leaves. The technique of beating branches was more satisfactory for collecting late instar than early instar larvae. Pupae were difficult to locate in the field. The sifting of "native" soil and the placement/analysis of soil filled trays were too time-consuming and the recovery of specimens negligible. Life history. In western Oregon, 0.occidentalis is univoltine (Fig. 1). A major portion of the development time, 9 of 12 months, was spent either in the overwin- tering egg or oversummering pupal stage. Larval stages and active adults each occurred over a period of 8 weeks during the spring and late fall - early winter, respectively. Adults were most active between dusk and midnight. Prior to darkness, adults were found at the soil surface beneath leaf litter. Approximately '12-1 h after sunset, males would begin to fly and would remain active for a 6-h period. When temper- atures were below freezing, males would not fly but did ascend trees and could locate females. Also, the brachypterous females would ascend trees at dusk and presumably return to the ground litter. No females were collected from the tree canopy during daylight hours. Males and females in copulo were observed on tree trunks and branches from ground level to 2 m above ground between dusk and midnight.

I -Adults Eggs Larvae I

Larvae II: P -Larvae JK -Larvae IP Pupae

1'~~1~~.1,~b1~1,1,~,1,~#1*#11I~~+- Oct. Dec. Feb. April June-Sept.

FIG. 1. The seasonal distribution of Operophtera occidenzalis. Salem, Oregon, 1979-1981. 632 THE CANADIAN ENTOMOI.OGIS7 July 1982 Field-collected adults and adults from laboratory cultures were observed to document longevity and reproductive potential. Males from laboratory cultures were kept alive for an average of 9.4 days (n = 9, S.D. = 5.7) while field-collected males lived for an average of 6.3 days (n = 150, S.D. = 14.2). The maximum lifespan observed for a laboratory and field male was 20 and 27 days, respectively. Females from laboratory cultures were kept alive for an average of 5.3 days (n = 13, S.D. = 5.0) while field-collected females lived an average of 4.4 days (n = 27, S.D. = 3.6). The maximum lifespan observed for laboratory and field females was 15 days. The longevity of field-collected males and females decreased as the date of collection occurred later in the season. Laboratory-cultured females deposited an average of 57.9 eggs (n = 11, S.D. = 39.9) while females trapped on sticky bands in the field contained an average of 90.4 eggs (n = 71, S.D. = 57.2). A maximum number of 218 eggs was observed in a field-collected female. Eggs averaged 0.68 mm long (n = 5, S.D. = 0.0005) were heavily reticulated and spindle-shaped, and occurred singly in partially concealed locations such as bark crevices and among clusters of buds. Observations on the location of field-collected eggs and egg deposition in the laboratory suggested that females choose oviposition sites based on substrate texture. Eggs were a pale, light green for about a month and then changed to an orange color. Approximately 3-4 days prior to larval eclosion the eggs turned to a dark metallic blue color. The most suitable temperatures for embryonic development and larval eclosion ranged between 10°C and 22°C (Table I). A summation of 389 degree-days above a threshold of 2°C was estimated as the temperature requirement for embryonic development. In the field, the peak occurrence of early first instar larvae occurred during the second week of April in 1980 and the first week of April in 1981. Even though data on development requirements, climatic records, and population census were available, we could not accurately predict egg hatch because the point in time for accumulating degree-days has yet to be determined. Larvae developed through four instars which can be differentiated by head capsule width (Table 11). Larval coloration ranged from a pale yellow to a light green. Six prominent, white longitudinal lines extended the entire length of the thorax-abdomen. These lines occur dorsally, subdorsally, and laterally at the level of the spiracles. The most suitable temperatures for larval development ranged between 10°C and 22°C (Table 111). Average ambient temperatures in the spring were 11°C with a low-high range of 4"-18°C. A total of 500 degree-days above 2°C were required for development from larval eclosion to pupation. Using the data on developmental requirements, climatic records, and population census, the time required for larval development to pupation was predicted to within 7 days.

Table I. Survival and development of Operophtera occidentalis eggs under various constant temperatures

Percent Mean Temperature ("C) N survival developmental time (days)' 4 40 63 36.6 10 40 80 17.3 16 40 93 7.8 22 31 71 5.3 28 40 18 4.2 34 40 5 0.5

'Add 270 degree-days above base 2'C to the developmental time because eggs were held for 3 months at a temperature above the developmental threshold, Volume 114 THE CANADIAN ENTOMOLOGIST

Table 11. Head capsule widths of Operophtera occidentalis larvae

- Instar N x Ranae (mm)

Late fourth instar larvae dropped from the foliage to the soil where they constructed a silk-earthen cell below the soil surface. Pupation occurred in the cell. Pupae averaged 7.9 mm long (n = 300, S.D. = 0.90) and were dark brown. Adult tissues were formed over the entire summer-fall period. A total of 28 plant species have been associated with the life history of 0. occidentalis (Table IV). Plant records for larvae and adults should not necessarily be considered as food plants, but have been reported here to indicate potential food plants upon which larvae have been or should be looked for and to reflect the type of plant community in which 0. occidentalis may be found. The list of plants on which larvae occurred includes 20 species of which 12 were original observations made during the present study. The authors' observations do indicate plants upon which larval feeding occurred. Larvae were commonly collected on nine of these plants, particularly commercial cherry, bitter cherry, and hazel. Attempts to force feed larvae on Douglas-fir failed. Thus, there appeared to be a proclivity for Rosaceae as a larval food source. A number of horticulturally important plants are included in the host plant list for 0. occidentalis (Table IV). The presence of 0. occidentalis on these plants has occasionally resulted in the application of insecticides. Larvae of 0. occidentalis were prevalent on cherry, emerging prior to bud burst and gaining access to primordial floral and leaf tissues by boring through the bud scales. Often larvae had developed to the second instar by the time that the cherry buds had expanded and the scales had separated. Petals, anthers, and ovarian tissues were eaten more extensively than leaf tissues. Similarly, floral tissues of ornamental trees and shrubs were eaten more than leaf tissue. However, hazel floral tissues were not available when larvae were present, thus, feeding occurred exclusively on leaves. Few natural enemies of 0. occidentalis were observed. Although generalist predators such as chrysopids, hemerobiids, reduviids and spiders were encountered frequently in sample material, only three instances of a spider feeding on a larva were documented. No egg parasitoids were observed from 138 field-collected eggs or from 217 eggs placed in the field out of the laboratory culture. Larval parasitoids were uncommon with the most abundant being braconids, a gregarious Apanteles sp. and a solitary species of Rogas. A gregarious ectoparasitic eulophid and a

Table 111. Survival and development of 0.occidentalis larvae under various constant temperatures

Percent Mean Temperature ("C) N survival developmental time (days) 4 30 25 > 106.0 10 33 54 68.7 16 4 1 40 33.2 22 40 37 24.0 28 30 4 14.1 34 19 0 - THE CANADIAN ENTOMOLOGIST July 1982 Table IV. Host plants of Operophtera occidentalis

Species Larvae ' Sourcez Adult Source Abies grandis Lindl. grand fir Acer macrophyllum Pursh bigleaf maple Acer spp. maple Alnus rubra Nutt. red alder Alnus spp. alder Amelanchier jZorida Lindl. se~icebeny Arbutus menziesii Pursh madrone Corylus cornuta Marsh var. californica (A.DC.) hazel Corylus spp. filbert Crataegus spp. hawthorn Fraxinus latifolia Benth. Oregon ash Malus sylvestris Mill. apple Oemleria cerasiformis (H & A) Landon Indian plum, osoherry Physocarpus capitatus (Pursh) Kuntze ninebark Michx. quaking aspen Populus trichocarpa T. & C. black cottonwood Populus spp. Poplar Prunus spp. cherry Prunus spp. prune Pseudotsuga menziesii (Mirb .) Franco Douglas-fir Pyrus spp. Pear Quercus spp. oak Quercus garryana Dougl. white oak, Oregon oak Rosa spp. Mt. Rose Rubus spp. blackberry and raspberry Volume 114 THE CANADIAN ENTOMOLOGIST Table IV.(Concluded)

Species Larvae ' Source2 Adult' Source2 Tsuga heterophylla (Raf .) Sarg. western hemlock Salix spp. Symphoricarpos albus (Linn.) P snowbeny

' Occurrence of larvae and adults (females only) is represented on a relative scale of presence on a particular plant, not field abundance. P = preferred or often present. x = present on rare occasions, ? = unknown, - = no record. 'Sources as follows: 1 = Prentice, 1963 2 = McFarland, 1963 3 = Furniss and Carolin, 1977 4 = Tietz, 1972 5 = Sugden, 1966 6 = authors solitary ichneumonid Hyposoter sp. also were recovered. Parasitism of larvae in most samples was nonexistent and totaled only 2% after all samples were pooled. Gillespie and Finlayson (1981) also found parasitism of Operophtera spp. to be very low in British Columbia. The apparent absence of effective natural enemies in the regulation of 0.occidentalis suggests that other environmental factors, such as winter disappear- ance, may be influential in determining population densities (see Varley et al. 1973). Presently, two exotic parasitoids, a tachinid, Cyzenis albicans (Fall.), and an ich- neumonid, (Grav .) , are being considered as biological control agents for 0. brumata in Oregon. Since 0. brumata and 0. occidentalis now occur sympatrically and the ecology of each species is similar, the possibility exists that the exotic parasitoids also can exploit 0.occidentalis and contribute to the regulation of this native species. Acknowledgments Field assistance was provided by P. Hanson, S. Jennings, R. Madar, J. McIver, D. Penrose, L. Swezey, and C. VanLuchene. Access to field sites was provided by Mr. G. Walker and the OSU School of Forestry. Drs. J. D. Lattin and G. W. Krantz contributed comments on a previous draft of this manuscript. The research was funded in part by a grant to J. C. M. from the Oregon State Department of Agriculture. References Brig@, J. B. 1957. Some features of the biology of the winter moth Operophtera brumata (L.) on top fruits. J. hort. Sci. 32: 108125. Brown, C. E. 1962. The life history and dispersal of the Bruce spanworm, Operophtera bruceata (Hulst), (Lepidoptera: Geometridae). Can. Ent. 94: 1103 1 107. Cuming, F. G. 1961. The distribution, life history, and economic importance of the winter moth, Operophtera brumata (L.) (Lepidoptera, Geometridae) in Nova Scotia. Can. Ent. 93: 135-142. Eidt, D. C. and D. G. Embree. 1968. Distinguishing larvae and pupae of the winter moth, Operophtera brumata, and the Bruce spanworm, 0. bruceata (Lepidoptera: Geometridae). Can. Ent. 100: 536539. Eidt, D. C., D. G. Embree, and C. C. Smith. 1966. Distinguishing adults of the winter moth Oper- ophtera brumata (L.), and Bruce spanworm 0. bruceata (Hulst) (Lepidoptera: Geometridae). Can. Ent. 98: 258-261. Embree, D. G. 1966. The role of introduced parasites in the control of the winter moth in Nova Scotia. Can. Ent. 98: 115%1168. 636 THE CANADIAN ENTOMOLOGIST July 1982 -1967. Effects of the winter moth on growth and mortality of red oak in Nova Scotia. For. Sci. 13: 295299. -1970. The diurnal and seasonal pattern of hatching of winter moth eggs, Operophtera brumata (Geometridae: Lepidoptera). Can. Ent. 102: 75F768. -1971. The biological control of the winter moth in Eastern Canada by introduced parasites. pp. 217-226 in C. B. Huffaker (Ed.), Biological Control. Plenum Press, New York. Ferguson, D. C. 1978. Pests not known to occur in the United States or of limited distribution. Winter moth, Operophtera brumata (L.) (Lepidoptera: Geometridae). U.S. Dep. Agric. Coop. P1. Pest Rep. 3(48-52): 687-694. Furniss, R. L. and V. M. Carolin. 1977. Western Forest . U.S. Dep. Agric. Misc. Publ. 1339. Gillespie, D. R. and T. Finlayson. 1981. Final-instar larvae of native hymenopterous and dipterous parasites of Operophtera spp. (Lepidoptera: Geometridae) in British Columbia. Can. Ent. 113: 4555. Gillespie, D. R., T. Finlayson, N. V. Tonks, and D. A. Ross. 1978. Occurrence of the winter moth, Operophtera brumata (Lepidoptera: Geometridae) on Southern Vancouver Island, British Colum- bia. Can. Ent. 110: 223-224. MacPhee, A. W. 1967. The winter moth, Operophtera brumata (Lepidoptera: Geometridae), a new pest attacking apple orchards in Nova Scotia, and its coldhardiness. Can. Eni. 99: 82F834. McFarland, A. N. 1963. The Macroheterocera (Lepidoptera) of a mixed forest in western Oregon. M.S. Thesis, Oregon State University, Corvallis, Oregon. Prentice, R. M. (Compiler.) 1963. Forest Lepidoptera of Canada. Can. Dep. For. Publ. 1013. Sanford, K. H. and H. J. Herbert. 1966. The influence of spray programs on the fauna of apple orchards in Nova Scotia. XV. Chemical controls for winter moth, Operophtera brumata (L.), and their effects on phytophagous mite and predator populations. Can. Ent. 98: 991-999. Smith, C. C. 1950. Notes on the European winter moth in Nova Scotia. Can. Dep. Agric., For. Biol. Div., Bi-mon. Prog. Rep. 6: 1. Sugden, B. A. 1966. Annotated list of forest insects of British Columbia Part XIII, Brephinae, Geo- metrinae, Sterrhinae, and (Geometridae). J. ent. Soc. Br. Columb. 63: 4-10. Tietz, H. M. 1972. An index to the described life histories, early stages and hosts of the macrolepidoptera of the continental United States and Canada. A. C. Allyn, Sarasota, Florida. Varley, G. C., G. R. Gradwell, and M. P. Hassell. 1973. Population Ecology. An Analytical Approach. Univ. of Calif. Press, Berkeley. (Received 17 September 1981; accepted 2 February 1982)