Survival and Development of Lymantria Monacha (Lepidoptera: Lymantriidae) on North American and Introduced Eurasian Tree Species

Home , Betula populifolia, Tilia cordata

FOREST ENTOMOLOGY Survival and Development of Lymantria monacha (Lepidoptera: Lymantriidae) on North American and Introduced Eurasian Tree Species

M. A. KEENA1

Northeastern Research Station, Northeastern Center for Forest Health Research, USDA Forest Service, Hamden, CT 06514

J. Econ. Entomol. 96(1): 43Ð52 (2003) ABSTRACT Lymantria monacha (L.) (Lepidoptera: Lymantriidae), the nun moth, is a Eurasian pest of conifers that has potential for accidental introduction into North America. To project the potential host range of this insect if introducedintoNorth America, survival anddevelopmentof L. monacha on 26 North American andeight introducedEurasiantree species were examined.Seven conifer species (Abies concolor, Picea abies, P. glauca, P. pungens, Pinus sylvestris with male cones, P. menziesii variety glauca, and Tsuga canadensis) andsix broadleafspecies ( Betula populifolia, Malus x domestica, Prunus serotina, Quercus lobata, Q. rubra, and Q. velutina) were suitable for L. monacha survival and development.Eleven of the host species testedwere ratedas intermediatein suitability, four conifer species (Larix occidentalis, P. nigra, P. ponderosa, P. strobus, and Pseudotsuga menziesii variety menziesii) andsix broadleafspecies ( Carpinus caroliniana, Carya ovata, Fagus grandifolia, Populus grandidentata, Q. alba, and Tilia cordata) andthe remaining 10 species testedwere ratedas poor ( Acer rubrum, A. platanoidies, A. saccharum, F. americana, Juniperus virginiana, Larix kaempferi, Liriodendron tulipfera, Morus alba, P. taeda, and P. deltoides). The phenological state of the trees hada major impact on establishment, survival, anddevelopmentof L. monacha on many of the tree species tested. Several of the deciduous tree species that are suitable for L. monacha also are suitable for L. dispar (L.) and L. mathura Moore. Establishment of L. monacha in North America wouldbe catastrophic because of the large number of economically important tree species on which it can survive anddevelop,and the ability of matedfemales to ßy andcolonize new areas.

KEY WORDS Lymantria monacha, host plant suitability, development, survival

Lymantria monacha (L.) (Lepidoptera: Lymantri- The best defenses currently used against this potential idae) (nun moth) is a Eurasian pest of conifers that pest are to monitor its abundance in Eurasian ports poses an ever-present threat of being introduced into (Munson et al. 1995), develop a good pheromone trap North America. Adults are readily attracted to artiÞ- to monitor for it (Morewoodet al. 1999), andeducate cial lights andhave been observedin Russian Far East people on how to identify it (Keena et al. 1998). ports (Munson et al. 1995). L. monacha has a high However, there is little useful information that ad- potential to be transportedvia commerce because, dresses the problems that would be encountered although eggs are normally laidin bark crevices, they should L. monacha be introduced into North America. also couldbe depositedincrevices on containers, To predict the risk of successful establishment in var- pallets, andships. L. monacha feeds primarily on nee- ious North American forest ecosystems andthe po- dles and male cones of conifers (Picea, Pinus, Abies, tential damage to those systems, knowledge of the nun and Larix spp.) but also can develop on leaves of mothÕs ability to survive anddevelopon various North deciduous trees and shrubs (Fagus, Carpinus, Betula, American host plants is required. and Quercus spp.) (Sliwa 1987). Its establishment in In Europe, the two species L. monacha prefers and North America wouldbe disastrousbecause of its most often damages are Picea abies (L.) (Norway polyphagous feeding habits, ability to colonize new spruce) and Pinus sylvestris L. (Scots pine) (Lipa and habitats, andcapacity to be spreadrapidlyby ßying Glowacka 1995). Sliwa (1987) provides an extensive adult females. Literature on the pheromones, micro- list of the intensity of natural feeding of L. monacha bial control, andgeneral biology andbiological control larvae on trees andshrubs in Polandduringthe last of L. monacha exists (Gries et al. 1996, Glowacka 1989, major outbreak there between 1978Ð1984. Laboratory Sˇvestka 1971, Jensen 1991, Silwa 1987, Grijpma 1989). investigations of nun moth preferences andutilization of Eurasian host plants providelimitedandcontradic- 1 E-mail: [email protected]. tory information (Bejer 1988). For example, labora- 44 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 96, no. 1 tory studies rank the preferred speciesÑspruce, pine, randomlyassignedto each foliage type andany larvae andlarchÑas intermediateto low in foodvalue (Bejer that haddiedwerereplacedwith extra larvae from the 1988). Most of the host plant work done on L. monacha same hatch removal date. has concentratedon the relationships between bud Voucher specimens of adults were deposited at the burst of the main hosts, P. abies and P. sylvestris, and Entomology Division, Yale Peabody Museum of Nat- hatching of L. monacha larvae. This work has shown ural History, New Haven, CT. that host phenology is as important as host preference Tree Species. Foliage of 1 to 7 trees of 26 North in determining the survival and successful develop- American and8 Eurasian tree species (Table 1) was ment of L. monacha larvae. For example, when larvae obtained, primarily from laboratory property at An- hatch before foliage budburst the presence of male sonia and Hamden (CT), for use in these studies. cones on Pinus spp. is critical to larval survival and Larvae were rearedto adultson 11 of the host species growth since Þrst andsecondinstar larvae cannot feed (A. rubrum, B. populifolia, F. grandifolia, Q. alba, on the previous yearÕs foliage because of the toughness Q. velutina, L. kaempferi, P. abies, P. glauca, P. strobus, of the needles and the secondary compounds they P. sylvestris (with male cones), and P. menziesii variety contain (Bejer 1988). glauca), which representeda range of genera and This studycomparedthe survival anddevelopment predicted suitability based on European literature, of L. monacha larvae during their Þrst 14 d on 26 North andservedas the basis for developingcriteria to pre- American and8 introducedEurasianhost plants. Lar- dict suitability of all the hosts after only 14 d of rearing. vae on 11 of the hosts usedfor the 14-dstudywere The setup period, 5Ð13 May, was chosen based on the allowedto complete their developmenton those predicted time of L. monacha hatch andbudbreak of hosts. The host plants usedwere from a broadrange trees at 41.3Њ N latitude. Because of the large number of tree genera, representing the major forest types of hosts that were to be tested, hosts on which the present in North America andincludedmanyof the larvae were to be rearedto adultsand12 of the 14-d major species of economic importance. Species from hosts were set up on 5 May (conifers) and6 May Eurasia provided a basis for comparison with the re- (deciduous) (Table 1). The remaining 12 of the 14-d sults of European research andprovidedinformation hosts were set up on 12 May (conifers) and13 May on exotic hosts commonly grown in urban areas of (deciduous)(Table 1). The only hosts included in North America. The risk of successful establishment both set up times were P. glauca and P. sylvestris (Þrst in various North American forest ecosystems, should setup without males cones andsecondsetup with L. monacha become established, is discussed. them); in both cases, the two sets are reportedsepa- rately in the results section. Initial Setup. Short branch tips (15Ð25 cm long) Materials and Methods with foliage were clippedfrom the trees. Clippings Insects. Eggs produced by 200 female L. monacha from conifers includedboththe current andprevious (thirdlaboratory generation) originally from Predin, yearÕs foliage, andßower buds/conesif available. Clip- Czech Republic, were pooledandchilledat 5 Ϯ 1ЊC pings from deciduous trees included both foliage and and Ϸ100% RH with L:D of 16:8 for 144 d(Þrst setup) ßowers, if available (see Table 1 for ßowering times or 151 d(secondsetup). From the pool of mixedeggs, relative to the setup for each species). For initial setup, 16 andeight packets of Ϸ500 eggs each were made for all branch tips came from the same tree andhad the Þrst andsecondsetups, respectively. The eggs foliage/ßowers of similar size andage present on were surface sterilizedto kill potential pathogens by them. For subsequent foliage changes, foliage was submerging the egg packets in 10% formalin for 15 min, collected from the other individual trees being used in rinsing in lukewarm tap water for 15 min andletting a sequential rotation. The trees usedvariedin their them dry in a hood for no longer than 60 min. The eggs phenology within each host species. The ends of the were incubatedat 25 Ϯ 1ЊC and60% RH a photoperiod branches that were clippedwere kept in de-ionized of 16:8 (L:H) h for 6Ð7 d. Date of Þrst hatch of egg water until usedlater in the day.Insects anddebris packets andtotal percentage hatch were recordedas foundon the foliage were removedor washedoff with quality control checks. de-ionized water. If the leaves were washed, they All larvae hatching from incubatedeggs were re- were allowed to dry before being used. movedevery other daywith a Þne camel hair brush The ends of each branch tip were inserted through into small, tight Þtting preweighedpetri dishes.Thirty a hole in a plastic lidof a 256-ml plastic cup that served larvae were placedin each petri dish,the larvae and as a de-ionizedwaterreservoir andthe tip recut un- petri dishwere weighedtogether, andthen the weight derwaterbefore the lidwas snappedonto the cup. One of the dish was subtracted to determine the weight of or more branch tips were placedin each plastic cup the larvae. Average initial weight of the larvae in each depending on the amount of foliage the larvae re- set was calculated. To prevent desiccation after weigh- quired. All plastic cups for a given tree species re- ing, the dishes with larvae were held in a water box at ceivedthe same number of branch tips at each foliage 5 Ϯ 1ЊC and100% RH with photoperiodof 16:8 (L:H) change. One plastic cup containing foliage and30 h. Additionally, L. monacha larvae generally spenda larvae was placedin each 3.8-liter rolledpaper-rearing few days resting near the egg mass before searching for container. A piece of clear plastic wrap was usedto food(Lipa andGlowacka 1995). All the dishesof replace the lid, allowing light to enter the container. larvae available for setup on a particular day were Three containers were set up (a total of 90 larvae) for February 2003 KEENA: Lymantria monacha SURVIVAL AND DEVELOPMENT 45

Table 1. Tree species tested as potential hosts for L. monacha in the spring of 1998

Leaf bud Setup ScientiÞc name Common name # Trees andtype a Native region breakb date Aceraceae A. rubrum L. Redmaple 7 large trees 13 April 6 May E North America A. platanoides L. Norway maple 1 large tree 20 April 13 May Europe A. saccharum Marshall Sugar maple 7 large trees 13 April 6 May E North America Betulaceae B. populifolia Marshall Gray birch 6 large trees 3 April 6 May NE North America C. caroliniana Walter American hornbeam 3 large trees 13 April 13 May E North America Fagaceae F. grandifolia Ehrhart American beech 1 large tree 5 May 6 May E North America Q. alba L. White oak 2 large trees 2 May 6 May E North America Q. lobata Ne´e California white oak 3, 1.5 m pottedtrees 20 April 13 May California, USA Q. rubra L. Northern redoak 5, 2.1 m pottedtrees 20 April 6 May E North America Q. velutina Lamarck Black oak 7 large trees 20 April 6 May E North America Juglandaceae C. ovata (Miller) Shagbark hickory 3 large trees 4 May 13 May E North America K. Koch Magnoliaceae L. tulipifera L. Yellow poplar 3 large trees 3 April 13 May E North America Moraceae M. alba L. White mulberry 1 large tree 13 April 13 May China Oleaceae F. americana L. White ash 3 large trees 20 April 13 May E North America Rosaceae P. serotina Ehrhart Wildcherry 5 large trees 3 April 13 May North America M. domestica (no author) Apple 2 large trees 3 April 13 May Eurasia Salicaceae P. deltoides Bartram Eastern cottonwood3 large trees 20 April 6 May E. North America P. grandidentata Michaux Bigtooth aspen 2 large trees 3 April 6 May NE North America Tiliaceae T. cordata Miller Littleleaf linden 3, 1.5 m potted trees 3 April 13 May Europe Cupressaceae J. virginiana L. Eastern redcedar 2 large trees 1 May 12 May E North America Pinaceae A. concolor (Gordon) White Þr 1, 1.5 m tree 8 May 5 May Western North America Lindley L. kaempferi (Lambert) Japanese larch 3 large trees 25 March 6 May Central Japan Carrie`re L. occidentalis Nuttall Western larch 3, 0.9 m pottedtrees 25 March 6 May W North America P. abies Karsten Norway spruce 3 large trees 30 April 5 May Europe P. glauca (Moench) Voss White spruce 4 large trees 30 April 5 May N North America 12 May P. pungens Engelman Colorado spruce 1 large tree 8 May 5 May Western U.S., North America P. nigra ArnoldBlack pine 4 large trees 15 May 5 May Europe P. ponderosa Lawson Ponderosa pine 3, 1.5 m potted trees 8 May 5 May W North America P. strobus L. Eastern white pine 7 large trees 5 May 5 May NE North America P. sylvestris L. Scots pine 3, 1.8 m pottedtrees 15 May 5 May Eurasia 2 large trees 12 Mayc P. taeda L. Loblolly pine 3, 1.5 m pottedtrees 30 April 5 May SE North America P. menziesii var. glauca Rocky Mountain 1 large tree 30 April 5 May Rocky Mountains, North (Beissner) Franco Douglas Fir America P. menziesii var. menziesii Coast Douglas Fir 1 large tree 8 May 5 May PaciÞc Coast, North America (Mirbel) Franco T. canadensis (L.) Eastern hemlock 4 large trees 8 May 12 May NE North America Carrie`re

a Large trees were either landscape or forest trees. Shorter trees that were not in pots were at a tree farm planted in the ground. b Before the study started, leaf bud break was checked weekly and the date given was the Þrst week that buds were open. After the study startedbudbreak was checkedthree times a week. c The secondsetup of P. sylvestris hadmale cones andfoliage but the Þrst setup hadonly foliage. each tree species with larvae that were assessedfor were set up on hosts on which the larvae were reared only the Þrst 14 dof development,andsix containers to adults in an attempt to have Ն30 individuals of each were set up (a total of 180 larvae) for each tree species sex survive to adult. All rearing containers for each host with larvae that went through their entire develop- species were set up on the same day with the exception ment. There was one exception to this; six containers of those for P. glauca. A perfume anddyefree facial tissue were set up for P. sylvestris without cones because was draped over the plastic cup to ensure that larvae that larvae initially were to be allowedto complete devel- fell to the bottom couldeasily climb back up to the opment on it, but because of high mortality, this treat- branch. The containers were heldat 25 Ϯ 2ЊC and60 Ϯ ment was terminated at 14 d. The additional larvae 5% RH with a photoperiodof 16:8 (L:D) h. 46 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 96, no. 1

Because only three pottedtrees of P. ponderosa with deformities observed were recorded along with the few leaders were available, cutting tips was not pos- weight, sex, andpupation date.Because the pupae sible. Instead, 30 larvae were placed in a mesh bag on were grouped, a correlation between pupal and adult each tree andthe trees were heldat the same envi- weights couldnot be obtained. ronmental conditions as the rearing containers. At 7 d, Pupae were checked daily, adults removed, and the bags were opened, all larvae removed, data col- eclosion recorded. Adult females were individually lectedas describedforthe other tree species, andthe placedin 473-ml paper containers labeledwith tree larvae put back in the bags on the trees. species, setup date, and eclosion date. Males that Foliage Changes. Deciduous foliage (which in- eclosedon the same daywere placedin groups (max- cluded the Larix spp.) was changedevery Monday, imum of 10) in 473-ml paper containers labeledwith Wednesday, and Friday. Conifer foliage was changed the same information as the females. Adults of both every Tuesday and Friday. The timing of foliage sexes were individually weighed and wing color was change was basedon previous experience indicating recorded. One male from the same tree species was that conifer foliage is more stable under these condi- placedin a 473-ml container with a female. The male tions than is deciduous foliage. For all foliage changes was chosen arbitrarily from those that hadeclosed the plastic cup with oldfoliage was removedand from that tree species; males that eclosed Ͼ2 dpre- placedon the rearing container lidin a safety hood.All viously generally were not used. The mating pairs frass andother debrisin the rearing container also were heldfor 2 din a dark,quiet container because were emptiedonto the lid.The rearing container, old previous tests have shown that L. monacha mates bet- leaves, anddebriswere searchedfor live anddead ter in a dark, quiet environment. larvae and their numbers recorded. Observations of Approximately 2 wk after mating, all eggs laidby what host tissues the larvae fed on were made at day each female were harvested, weighed, and embryo- 2 andat all subsequent foliage changes. If diseased nation evaluated. This length of time allowed embryo- larvae were found, all surfaces of the rearing container nation to proceedto the point that a color change were cleanedwith a weak Zephiran chloridesolution couldbe observed;embryonatedeggs turn dark before a new, clean cup containing fresh foliage was brown, while unembryonatedeggs are blue-green and placedin the container andall live larvae placedonto ßattened as a result of dehydration. The percentage of the foliage. successful matings for each tree species was calculated Larval Development (14 d). After the larvae had as the number of matings that produced Ͼ10 embry- been on the foliage for 14 d, the number of live larvae onated eggs divided by the total number of attempted andthe weight andinstar of each larva were recorded, matings. andthe average initial larval weight was subtractedto All eggs from an individual female were placed in a determine weight gain over the Þrst 14 d. Percentage separate taredglassine envelope andweighed.The survival was calculatedas the number of live larvae per envelope was then labeledwith tree species, setup rearing container minus the number of larvae that date, and egg mass number. Egg masses with Ͼ10 were lost or damaged, divided by the initial number of embryonatedeggs after a minimum of 22 dwere larvae. placedat 5 Ϯ 1ЊC, Ϸ100% RH with a photoperiodof For tree species on which the larvae were to con- 16:8 (L:D) h for 130 d. After incubation at 25 Ϯ 2ЊC and tinue their development to adult, the number of larvae 60 Ϯ 5% RH with a photoperiodof 16:8 (L:D) h, the per rearing container was reduced to a maximum of 15 percentage hatch of embryonatedeggs was calculated by increasing the number of containers usedandcom- and days to Þrst hatch was recorded for each egg mass. bining larvae from different containers as needed. This Host Suitability Ratings and Analyses. The 11 hosts was done to prevent the larvae from consuming all of that larvae were allowedto complete developmenton the foliage before the foliage was to be changed. The were assigneda host suitability rating basedon com- number of branches of foliage added was determined pletion of larval development. A host species was con- by the amount being consumed. All containers with sidered poor if Ͻ10% of the larvae were able to com- the same host foliage receivedthe same number of plete development, intermediate if Ն10% but Ͻ60% of branches at each foliage change. At each subsequent the larvae completeddevelopment,andsuitable if foliage change, the larvae that hadnot pupatedon Ͼ60% completeddevelopmentandproducedviable each foliage type were consolidated to maintain Ϸ15 eggs. To develop a host suitability rating for all species, larvae per rearing container. it was assumedthat the 14 dsurvival andweight gain Pupal and Adult Development. Pupae were re- data for larvae that completed development on 11 moved every Monday, Wednesday, Friday, and Sun- hosts was similar to that for all hosts. The 14-dsurvival day from deciduous foliage and every Tuesday, Thurs- andweight gain datawere analyzedfor larvae that day, Friday, and Sunday from conifer foliage. Pupae were allowedto complete development,by host suit- that were newly formedwere removedfrom each ability class, and thresholds were developed for each rearing container (if possible) andkept with their poor, intermediate and suitable class. Using the webbing intact in a labeled473-ml paper container thresholdsfor 14 dpercent survival andweight gain, andweighedthe next day.All other pupae were all species were assigneda host suitability rating. weighed individually the day they were found then To check for container effects on the 14-dweight groupedby tree species, setup date,andsex in 473-ml gain data, the data were ranked and an analysis of paper containers with clear plastic lids. Any pupal variance (ANOVA) of the ranks was carriedout to February 2003 KEENA: Lymantria monacha SURVIVAL AND DEVELOPMENT 47

Fig. 1. Percentage survival of L. monacha larvae on coniferous (A) and deciduous (B) tree species over the entire larval developmental period. g, P. menziesii variety glauca, andcones, males cones present with foliage. approximate a KruskalÐWallis two-way, nonparamet- hosts was either high early then leveledoff or oc- ric analysis with container nestedwithin host species curredat varying rates over the whole time periodto (SAS Institute 1989). The nonparameteric test was adults (Fig. 1). Representatives from each rating level necessary because of heteroscedasticity in the data were chosen: P. abies for suitable, P. strobus for inter- andno useful datatransformations. A KruskalÐWallis mediate, and A. rubrum for poor. P. abies was chosen two-way, nonparametric ANOVA followedb y a z test to represent the suitable level because it is a primary for comparison of groups (Statistix 1998) was run for host in Europe that does not depend on the presence each sex separately for days to adult and to compare of male cones for larvae to establish. The latter two weigh gain for suitability rating groups between the species were chosen because larvae on the other host 14dhosts andthe hosts that larvae were rearedto species in their rating level hadsuitable development adult. One-way ANOVA followed by Bonferroni com- and/or survival during part of their developmental parison of means (Statistix 1998) were run for each sex periodwhile larvae on P. strobus and A. rubrum con- separately, on pupal weight, days to pupation, adult sistently Þt the rating level throughout their develop- weight, days to adult, and fecundity to determine if mental period. there were signiÞcant differences between suitability When the number of individuals in each 14d weight rating groups. One-way ANOVA followedby Bonfer- gain group were analyzedfor the three representative roni comparison of means (Statistix 1998) was also run host species it was foundthat Ͼ90% of the larvae to assess sex differences in pupal weight. Linear re- weighing Ͻ10 mg at 14 dultimately died(allthree gression was usedto examine relationships between hosts), the majority of larvae from poor host weighed female adult weight and fecundity and total egg Ͻ10 mg, all larvae from intermediate host weighed weight andfecundity. Ͻ50 mg, andlarvae rearedon the suitable host weighted Ͼ50 mg (Fig. 2). Basedon this information, 14dsuitability criteria for weight gain were developed Results (poor, weight gain averaging Յ10 mg; intermediate, Host Suitability Ratings for Larval Development weight gain averaging Ͼ10 mg and Յ50 mg; andsuit- (14 d). Of the 11 host species where L. monacha able, weight gain averaging Ͼ50 mg) andapplied larvae were rearedto adult, B. populifolia, Q. velutina, (Figs. 3 and4). These weight gain categories also have P. abies, P. glauca, P. sylvestris (with male cones), and developmental signiÞcance; larvae that are still Þrst P. menziesii variety glauca were suitable, F. grandifolia, instars have gained Ͻ10 mg (5.7 Ϯ 1.1 mg [average Ϯ Q. alba, and P. strobus were of intermediate suitability SE] on suitable hosts), secondinstars gain Ͻ50 mg and A. rubrum and L. kaempferi were poor in suitabil- (30.9 Ϯ 1.6 mg on suitable hosts) before they molt, and ity (Fig. 1). There was little mortality after the Þrst thirdinstars on suitable hosts gain just over 50 mg 14 don suitable hosts while mortality on the other (55.7 Ϯ 1.3 mg) before they molt. Thirdinstars on 48 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 96, no. 1

Fig. 2. Number of individuals by weight gain at 14 d for a suitable (P. abies), intermediate (P. strobus), andpoor (A. rubrum) host. intermediateandpoor hosts tendto molt before they have gained50 mg (34.0 ϩ 6.1 for poor hosts and 37.0 ϩ 1.5 for intermediate hosts). When 14 d hosts Fig. 4. Conifer host species suitability ratings for Lyman- tria monacha basedon mean larval weight gain ( ϮSE) at 14 d. andhosts that larvae were rearedto adultwere com- Ͻ paredsigniÞcant differencesin 14 dweight gain be- Ratings: poor, mean weight gain 10 mg; intermediate, mean weight gain Ն10 mg and Ͻ50 mg; suitable, mean weight gain tween but not within each suitability-rating group Ն ϭ ϭ ϭ ϭ 50 mg. g, P. menziesii variety glauca; m, variety menziesii; were found( F 421, P 0.0000, df 5, 2077, z cones, males cones present with foliage; no cones, no males 2.94). Rearing container hada signiÞcant effect on cones present with the foliage; 1 andtwo refer to the Þrst and larval weight gain (F ϭ 2.93; df 98, 1949; P Ͻ 0.0001) secondsetups on this host. during the Þrst 14 d, but this did not appear to affect the suitability ratings for any of the hosts. Ͼ Ͼ Criteria for percentage survival after 14 dof larvae with weight gain 10 mg andsuitable 60% of sur- Ͼ with 14dweight gain of Ͼ10 mg also were assigned viving larvae with weight gain 10 mg) andapplied (poor, Յ10% of surviving larvae with weight gain Ͼ10 (Figs. 5 and6). All but three host species classify the mg; intermediate, Ͼ10% but Յ60% of surviving larvae same using 14 dweight gain and14 dpercent survival: P. sylvestris with males cones, T. canadensis, and P. serotina classify as suitable using the percentage survival criteria andas intermediateusing the weight gain criteria (Figs. 3Ð6). Two species on which the larvae were rearedto adultwere misclassiÞedusing the 14-d criteriaÐL. kaempferi and F. grandifolia (Figs. 3Ð6). Larvae on both of these host species initially devel- opedandsurvivedwell but experienceddifÞculties later. When larvae on L. kaempferi reachedthe late thirdto early fourth instar they refusedto feedon the foliage, began wandering, and chewing the clear plastic cover, and ultimately died. At 12 d on F. grandifolia, the larvae (about the fourth instar) began producing stringy, watery frass, signs of difÞculty in digesting the leaves. Feeding Observations. Lymantria monacha initiated feeding on all conifers tested (Table 2). On J. virginiana and P. sylvestris without male cones or newly expandedfoliagethe larvae fedlittle andspent most of their time off the host wandering and producing silk. On T. canadensis, larvae fedonly on newly ex- pandedfoliage,andon P. strobus larval feeding was light on both previous yearÕs andnewly expanded Fig. 3. Broadleaf host species suitability ratings for Ly- foliage. In both P. sylvestris and P. nigra, the larvae fed mantria monacha basedon mean larval weight gain ( ϮSE) at exclusively on male cones for the Þrst 2 wk until the 14 d. Ratings: poor, mean weight gain Ͻ10 mg; intermediate, new foliage appeared, covering themselves com- mean weight gain Ն10 mg and Ͻ50 mg; suitable, mean weight pletely in the yellow pollen. For most conifer species gain Ն50 mg. tested, the order of tissue preference of Þrst and sec- February 2003 KEENA: Lymantria monacha SURVIVAL AND DEVELOPMENT 49

Fig. 6. Conifer host species suitability ratings for Lyman- tria monacha basedon percentage survival of larvae with 14-d weight gain Ͼ10 mg (shaded plus open bars). Ratings: poor, Յ10% survival; intermediate, Ͼ10% but Յ60% survival and Fig. 5. Broadleaf host species suitability ratings for Ly- suitable Ͼ60% survival. Weight classes: black bars, Յ10 mg; mantria monacha basedon percentage survival of larvae with shaded bars, Ͼ10 and Յ50 mg; andopen bars, Ͼ50 mg. g, 14-dweight gain Ͼ10 mg (shaded plus open bars). Ratings: Յ Ͼ Յ P. menziesii variety glauca; m, variety menziesii; cones, males poor, 10% survival; intermediate, 10% but 60% survival cones present with foliage; no cones, no males cones present andsuitable Ͼ60% survival. Weight classes: black bars, Յ10 Ͼ Յ Ͼ with the foliage; 1 andtwo refer to the Þrst andsecondsetups mg; shaded bars, 10 and 50 mg; andopen bars, 50 mg. on this host. ondinstars was new needles,male cones or budscales, Pupal and Adult Development. On average, female andoldfoliage. In all cases where the larvae grew well, pupae (770 mg) weighedsigniÞcantly more than male they began feeding on older foliage at about the third pupae (414 mg, F ϭ 1667, P Ͻ 0.0000, df ϭ 1, 854, t ϭ molt. 1.96). Pupae of both sexes rearedon suitable hosts There was no observable feeding on three of the weightedsigniÞcantly more than those rearedon in- deciduous tree species, L. tulipifera, A. platanoides, termediate hosts, which weighed signiÞcantly more and M. alba. There were sporadic signs of feeding than those rearedon poor hosts (Table 3). Adult (pin holes in leaves, chewedspots on petioles, and frass) during the Þrst 2 wk on A. rubrum, A. saccharum, Table 2. Conifer tissues utilized by L. monacha larvae during C. ovata, F. americana, P. deltoides, P. grandidentata, the ﬁrst 14 d and T. cordata. Larvae fedonly on the green stems of Newly Previous Q. alba for the Þrst week while the new, unexpanded Bud Male Host species expanded yearÕs leaves were redin color; once green, expandedleaves scales cones were provided they ate them voraciously. L. monacha foliage foliage larvae on P. serotina left leaves to feedon the ßowers A. concolor ϩϩϩ ϩ 0NA ϩ when they became available. After the Þrst week, J. virginiana 00 NA L. kaempferi ϩϩϩ ϩ NA NA larvae on B. populifolia, F. gandifolia, Q. velutina, L. occidentalis ϩϩϩ ϩ NA NA Q. rubra, Q. lobata, and P. malus consumed Ͼ50% of P. abies ϩϩϩ ϩ 0 ϩ the leaf surface area provided before the next foliage P. glauca ϩϩϩ ϩ 0NA ϩϩϩ ϩ change, even with increasing amounts of foliage being P. pungens 0NA P. nigra 0 ϩ 0 ϩϩϩ added. P. ponderosa ϩϩϩ ϩ 0NA Larval ability to use different foliage types and P. strobes ϩϩϩNA host species changed over the developmental period. P. sylvestris w/o cones ϩ ϩϩϩ ϩ NA ϩ ϩϩϩ In addition to the difÞculties that larvae had with P. sylvestris w/cones 0 0 P. taeda ϩϩϩ ϩ ϩ NA L. kaempferi and F. grandifolia foliage when they P. menziesii var. glauca ϩϩϩ ϩ 00 reachedfourth andhigher instars that alreadyhave P. menziesii var. ϩϩϩ ϩ ϩ ϩ been mentioned, larvae did not use the old foliage of menziesii ϩϩϩ most of the species testedin the Pinceae family until T. canadensis 000 they reachedthe fourth instar. The exception to this NA, not available; 0, no observedsigns of feedingon this tissue; ϩ, was major utilization of oldfoliage of P. strobus, even infrequent andvery limited; ϩϩϩ, usedthrough out 14 daysandvery by newly hatchedlarvae (Table 2). obvious. 50 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 96, no. 1

Table 3. ANOVA results by sex for mean pupal weight, adult weight, days to adult and fecundity

Male Female Variable Poor Intermediate Suitable FP df Poor Intermediate Suitable FP df Pupal weight (mg) 105c 342b 439a 76 Ͻ0.0000 2,437 251c 634b 798a 58 0.0000 2,416 Adult Weight (mg) Ñ 129b 175a 35 0.0000 1,424 154c 370b 490a 53 0.0000 2,413 Days to Adult Ñ 43b 38a 113 0.0000 1,424 57b 47b 40a 51 0.0000 2,413 Fecundity Ñ 223b 299a 34 0.0000 1,225

Within each variable means followedby the same letter are not signiÞcantly differentat ␣ ϭ 0.05 (Bonferonni test or z test). One way ANOVA used except for the days to adult where a Kruskal-Wallis one way nonparametric ANOVA was used. weights followedthe same pattern as the pupal those rearedon intermediatehosts andthere were no weights, but the adults weighed less than the pupae eggs producedbyfemales rearedon poor hosts (Table andthe weight differencebetween males andfemales 3 andFig. 7). There was a signiÞcant relationship increased(Table 3). between adult female weight and fecundity (R2 ϭ Mean days to adult for both sexes reared on suit- 0.59, b ϭ 5.53 Ϯ 15.74, slope ϭ 0.60 Ϯ 0.03) and able hosts were shorter than for those rearedon inter- between the weight of the eggs a female laidand mediate or poor hosts; there were no adult males fecundity (R2 ϭ 0.87, b ϭ 4.59 Ϯ 7.33, slope ϭ 1.54 Ϯ from poor hosts (Table 3). The sex ratios of surviving 0.04). On average, for all tree species pooled, the eggs adults were Ϸ1:1 for all host species except F. gran- laidby a female accountedfor 29 Ϯ 1% of her body difolia (0.5:1, &:(), Q. alba (0.7:1, &:() A. rubrum weight. There was no signiÞcant difference in the (1:0, &:(), and L. kaempferi (1:0, &:(). percentage of embryonatedeggs that hatched(81 Ϯ For all tree species pooled, 21% of the females were 1%) between the suitable hosts andthe intermediate all black, 35% black with white markings, and44% hosts (F ϭ 0.08, P Ͻ 0.7770, df ϭ 1, 225). white with black markings. The females that were white with black markings tended to be more fecund than the all black females. Males tended to be darker Discussion with 71% all black, 19% black with white markings, and Basedon host suitability ratings seven conifer species 10% white with black markings. (A. concolor, P. abies, P. glauca, P. pungens, P. sylvestris Mating and Reproduction. For those species in the with male cones, P. menziesii variety glauca, and intermediate and suitable categories, the highest per- T. canadensis) andsix broadleafspecies ( B. populifolia, centage of successful matings was for adults reared on M. x domestica, P. serotina, Q. lobata, Q. rubra, and Q. alba andthe lowest percentage was for adults Q. velutina) testedwere suitable for L. monacha sur- rearedon B. populifolia, which also hadthe greatest vival anddevelopment. L. monacha shouldbe able to number of attemptedmatings (Fig. 7). Fecunditywas establish andincrease in numbers on these species if higher for females rearedon suitable hosts than for introduced into North America. L. monacha also shouldbe able to establish, but may not increase in numbers (because of higher mortality, slower development andlower fecundity)on the 11 hosts that were ratedas intermediatein suitabilityÐÞve conifer species (L. occidentalis, P. nigra, P. ponderosa, P. strobus, and P. menziesii variety menziesii) andsix broadleaf species (C. caroliniana, C. ovata, F. grandifolia, P. grandidentata, Q. alba, and T. cordata). The other 10 species testedwere ratedpoor ( A. rubrum, A. platanoidies, A. saccharum, F. americana, J. virginiana, L. kaempferi, L. tulipfera, M. alba, P. taeda, and P. deltoides), and L. monacha wouldlikely not be able to establish because few if any couldcomplete development on these species. In general, these results are in agreement with the reports of feeding intensity for the same or related tree species during the major L. monacha outbreak in Po- landin 1978Ð1984. Sliwa (1987) observedcommon or frequent feeding on species in the genera Abies, Betula, Fagus, Larix, Picea (except P. pungens), Malus, Fig. 7. Mean fecundity (bars with SE lines, number of successful matings inside bars) and percentage successful Pseudotsuga, and Quercus (except Q. rubra), andfor matings (dots) of L. monacha rearedon various tree species. P. sylvestris. There were four species on which Sliwa g, P. menziesii variety glauca; cones, males cones present with (1987) found sporadic or no signs of feeding that are foliage; one andtwo refer to the Þrst andsecondsetups on classiÞedas intermediateor suitable; P. pungens, this host. Q. rubra, P. nigra, and P. strobus. These differences February 2003 KEENA: Lymantria monacha SURVIVAL AND DEVELOPMENT 51 couldhave been a result of the presence of other more which they fed, which have been shown to reduce preferredspecies in outbreak areas, poor phenological growth rate, increase mortality, andextendthe larval synchrony of these tree species with L. monacha larvae periodin sawßies (Ikedaet al. 1977). Thus, the proper during the outbreak, or differences in the suitability of synchrony of L. monacha hatch with tree phenology the foliage when it is cut, as in the tests reportedhere. will be critical to its establishment in North America. The classiÞcation of the Larix species posses a dif- Several of the same deciduous tree species suitable Þculty because heavy feeding on larch was reported in for L. monacha are suitable for L. dispar (L.) (Lieb- the Polish outbreak, but the two species usedin this holdet al. 1995) and L. mathura Moore (Zlotina et al. study tested as intermediate or poor and, in fact, both 1998). These three species survive anddevelopwell may have been poor, but the larvae on L. occidentalis on several species of Quercus. Two species, P. gran- were not rearedfor a long enough periodto determine didentata and T. cordata, suitable for L. dispar (Lieb- if they wouldexperience the same problems as larger holdet al. 1995) were only intermediatelysuitable for larvae did on L. karmpferi. This couldbe explainedby L. monacha. Most Pinaceae species are suitable and the fact that the early instars do use this tree species even preferredby L. monacha, while they are only well and are wasteful feeders. Larvae began feeding marginally suitable andoften only usedduringthe near the base of the needle and most of the needle falls later instars by L. dispar and L. mathura (Liebholdet to the grounduneaten. The larvae may have fedon the al. 1995, Montgomery 1990, Zlotina et al. 1998). The larch trees then movedto other tree species to com- Acer, Liriodendron, Morus, and Fraxinus species tested plete development. This would explain why L. mona- are not suitable for either L. monacha or L. dispar cha does not go into an outbreak on larch (Bejer 1988). (Liebholdet al. 1995). These similarities in the suit- Earlier laboratory testing of tree species reported ability of tree species for larvae of the genus Lymantria faster development on suitable deciduous tree species may indicate they have similar abilities to deal with than on Pinaceae species (Maercks 1935, Sattler 1939). allelochemicals. For example, L. dispar will use leaves L. monacha did develop faster on suitable deciduous that contain tannins but tends to avoid leaves that tree species than on the intermediately suitable Pinus, contain alkaloids such as Acer, Liriodendron, and Pseudotsuga, and Tsuga species tested, but not faster Morus species (Barbosa andKrischik 1987). However, than the suitable Abies or Picea species tested. Timing just because a tree species is suitable in a no-choice of the testing couldexplain the differences. L. mona- test or outbreak situation does not mean it will be a cha gainedless weight anddevelopedsloweron preferredhost undernormal circumstances. P. glauca in the secondsetup than the Þrst, which was Should L. monacha become established, regions of 1 wk earlier. When newly hatchedlarvae were placed highest risk in North America, basedon host plant on P. glauca foliage in mid-June, there was only a 2-mg availability andclimate, includeforests west of the weight gain in 14 d(Withers andKeena 2001) com- Cascade Range, spruce/Þr/pines in the upper Mid- paredwith 100 mg and60 mg in these tests. When the west, andnortheastern North America (Wallner needles are older they are tougher and the mandibles 1996). In addition, many of the suitable species are of L. monacha are not strong enough to macerate them conifers andaffects of L. monacha feeding on conifers until they are in the thirdinstar (Jensen 1996). So, are more severe because they destroy more needles newly hatched L. monacha larvae neednewly ex- than they actually consume, feedon budsuntil new panded foliage of Abies, Picea, and Pinus (male cones foliage is available, andconifers are less able than until newly expanded foliage appears) species to es- deciduous trees to replace lost foliage. Defoliation tablish andgrow well. Ͼ70% of Picea species by L. monacha larvae results in The phenological state of the trees hada major tree death in Europe (Bejer 1988). Therefore L. mona- impact on establishment, survival, anddevelopmentof cha poses a serious threat to several forest ecosystems L. monacha on many of the tree species tested. Newly if introducedbecauseit can survive anddevelopon hatchedlarvae refusedto feedon unexpandedreddish many economically important North American and Q. alba leaves but fedandgrew rapidlywith little introduced Eurasian tree species. mortality once expanded green leaves were available. This resultedin an initial high mortality rate andan overall slower growth rate. When only oldneedlesof Acknowledgments P. sylvestris with no male cones were available to the I thank M. Montgomery andT. Withers for their critical L. monacha larvae, many diedandthosethat survived review of this paper, two anonymous reviewers andthe grew slowly. Jensen (1996) reportedthat L. monacha subject editor for suggestions that made this a better paper, larvae will not survive on P. sylvestris without male andJ. Gove for statistical review. Paul Moore, Carol ODell, cones because the oldneedlesare tough andlow in Diana Roberts-Paschall, and Alice Vandel provided technical nutritive value, andnew needlesappear later in the assistance. I also thank Milan Sˇvestka for his assistance in spring. The presence of male cones also was impor- obtaining egg masses to start the colony. tant for the development of larvae on P. nigra, and the absence of cones on P. strobus, P. ponderosa, and P. taeda may have affectedsurvival anddevelopment References Cited on these species. Additionally, the larvae on P. pon- Barbosa, P., and V. A. Krischik. 1987. Inßuence of alkaloids derosa and P. taeda may have been affectedby sec- on feeding preference of eastern deciduous forest trees ondary compounds present in the new needles on by gypsy moth Lymantria dispar. Am. Nat 130: 53Ð69. 52 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 96, no. 1

Bejer, B. 1988. The nun moth in European spruce forests, mone-baseddetectionof Lymantria monacha (Lepidop- pp. 211Ð231. In A. A. Berryman [ed.], Dynamics of forest tera: Lymantriidae) in North America. Can. Entomol. 131: insect populations: patterns, causes, implications. Ple- 687Ð694. num, New York. Montgomery, M. E. 1990. Variation in the suitability of tree Glowacka, B. 1989. Choroby epizootyczne brudnicy mniszki species for the gypsy moth, pp. 1Ð13. In: Gottschalk, K. W., (Lymantria monacha L.) I mozliwosci mikrobiologicz- M. J. Twery, and S. I. Smith (eds.), Proceedings, USDA nego jej zwalczania. [Epizootic diseases of the nun moth interagency gypsy moth review 1990, January 22Ð25, East (Lymantria monacha L.) andpossibilities of its microbi- Windsor, CT. USDA Forest Service, Northeastern Forest ological control.] In Polish, English summary. Prace In- Experiment Station Gen. Tech. Rep. NE-146. Radnor, PA. stytutu Badawczego Lesnictwa Nr. 691. Warsaw. 71 p. Munson, A. S., D. Leonard, V. Mastro, T. McGovern, J. Levy Gries, G., R. Gries, G. Khaskin, et al. 1996. SpeciÞcity of nun and D. Kucera. 1995. Russian Far East lymantridmoni- andgypsy moth sexual communication through multiple- toring project: project summary 1993Ð1994. USDA Forest component pheromone blends. Naturwissenschaften Service, Intermountain Region, Ogden, Utah. FPM Rpt. (abstr.) vol. 83(8): 382Ð385. 95Ð02. Grijpma, P. 1989. Overview of research on lymantrids in SAS Institute. 1989. SAS/STAT userÕs guide, version 6, 4th eastern andwestern Europe, pp. 21Ð49. In W. E. Wallner ed., vol. 2. SAS Institute, Cary, NC. and K. A. McManus [eds.], Proceedings, Lymantriidae: a Sattler, H. 1939. Die Entwicklung der none, Lymantria comparison of features of New andOldWorldtussock monacha, in ihrer Abha¨ngigkeit von der Nahrungsquali- moths. U. S. Department of Agriculture, Forest Service, ta¨t. Z. Angew. Entomol. 25: 543Ð587. Northeastern Forest Experiment Station, Gen. Tech. Rep. Skuhravy, V. 1987. A review of research on the nun moth NE-123. Broomall, PA. (Lymantria monacha L.) conducted with pheromone Ikeda, T., F. Matsumura, and D. M. Benjamin. 1977. Chem- traps in Czechoslovakia, 1973Ð1984. Anz. Schaedlingsk. ical basis for feeding adaptation on pine sawßies, Neo- Pßanzenschutz. 60: 96Ð98. diprion rugiforns and Neodiprion swainei. Science 197: Sliwa, E. 1987. Nun moth. PWRil, Warszawa, 220 pp. (In 497Ð498. Polish). Jensen, T. S. 1996. Folivore feeding on male conifer ßowers: Statistix. 1998. Statistix for Windows UserÕs Manual. Ana- defense avoidance or bet-hedging? pp. 104Ð111. In W. J. lytical Software, Tallahassee, FL. Mattson, P. Niemila¨, andM. Rossi [eds.],Dynamics of Sˇvestka, M. 1971. The nun moth in the past andpresent. forest herbivory: quest for pattern andprinciple. USDA [Lymantria]. Lesnicka. Prace. 50(2): 60Ð67. Forest Service, North Central Forest Experiment Station, Wallner, W. E. 1996. Exotic forest defoliators: some species Gen. Tech. Rep. NC-183. St. Paul, MN. of concern, pp. 76Ð79. In Fosbroke, S.L.C., Gottschalk, Keena, M., K. Shields, and M. Torsello. 1998. Nun moth: K. W. [eds.], Proceedings of USDA interagency gypsy potential new pest. USDA Forest Service, Northeastern moth research forum 1996, January 16Ð19, Annapolis, Area NA-PR-95-98. Radnor, PA. MD. USDA Forest Service, Northeastern Forest Experi- Liebhold, A. M., K. W. Gottschalk, R. M. Muzika, et al. 1995. ment Station Gen. Tech. Rep. NE-230. Radnor, PA . Suitability of North American tree species to gypsy moth: Withers, T. M., and M. A. Keena. 2001. Lymantria monacha a summary of Þeldandlaboratory tests. USDA Forest (nun moth) and L. dispar (gypsy moth) survival and Service, Northeastern Forest Experiment Station, Gen. development on improved Pinus radiata. N.Z.J. Forestry Tech. Rep. NE-211. Radnor, PA. Science 31: (66Ð77). Lipa, J. J., and B. Glowacka. 1995. Nun moth (Lymantria Zlotina, M. A., V. C. Mastro, D. E. Leonard, and J. S. Elkinton. monacha L.) in Europe andPoland,pp. 138Ð158. In Pro- 1998. Survival anddevelopmentof Lymantria mathura ceedings of the Annual Gypsy Moth Review, Traverse (Lepidoptera: Lymantriidae) on North American, Asian, City, MI; 1995 November 5Ð8. andEuropean tree species. J. Econ. Entomol. 91: 1162Ð Maercks, H. 1935. Der Einßuss der Nahrung auf die Ent- 1166. wicklung der Nonnenraupe. Arb. Physiol. Angew. Ento- mol. 2: 175Ð195. Morewood, P., G. Gries, D. Haussler, K. Moller, J. Liska, P. Received for publication 24 January 2002; accepted 24 Sep- Kapitola, and H. Bogenschutz. 1999. Towards phero- tember 2002.