Dormancy in the Strawberry Leafroller (: )

J. J. OBRYCKI, A. D. GABRIEL, C. J. ORR, ANDJ. W. BING

Department of Entomology, Iowa State University, Ames, Iowa 500ll

Environ. Entomol. 19(4): 932-936 (1990) ABSTRACT A 2-yr study of strawberry leafroller, comptana (Froelich), populations in central Iowa showed that short daylengths and low temperatures maintain diapause during autumn and that this autumnal diapause ends without a specific cue by the end of December.

The completion of diapause does not require chilling. The postdiapause developmental rate Downloaded from https://academic.oup.com/ee/article/19/4/932/2480444 by guest on 27 September 2021 of A. comptana is linearly related to temperatures between 14 and 30"C; adult emergence requires 154 degree-days (DD) above a lower thermal threshold (t) of 10.5°C. Field cage studies demonstrated that 50% emergence of adult A. comptana from overwintering larvae can be predicted accurately based upon the accumulation of approximately 150 DD >10°C.

KEY WORDS Insecta, dormancy, , diapause

INSECT DORMANCYmay be separated into two Earliglow). On each sample date, larvae were placed phases: diapause and postdiapause development individually in a Petri dish containing moistened (Tauber et al. 1986). Photoperiod and temperature filter paper and one strawberry leaflet. Leaflets were are two key environmental factors that regulate changed when they began to mold or deteriorate. diapause development in several species. Temperatures were regulated within ± 1°C. Following the end of diapause, undergo a Voucher specimens are deposited in the Iowa State period of postdiapause development, which is reg- University insect collection, Ames. ulated by a range of factors (e.g., temperature, Diapause Maintenance and Termination. Our food, moisture) (Boyne et al. 1985, Tauber et al. methods followed those of Tauber & Tauber (1973), 1986, Nechols et al. 1987). An understanding of in which the quantification of responses during diapause and postdiapause developmental rates is dormancy is based upon periodic sampling of field necessary for the accurate prediction of the sea- populations throughout the entire period of dor- sonal activity of temperate-zone insects (Tauber et mancy. The overwintering populations of A. comp- al. 1986). tana consisted of field-collected (fall 1986 and 1987) The strawberry leafroller, Ancylis comptana late-stage larvae in rolled strawberry leaves from (Froelich), an occasional pest of strawberry (Fra- Ankeny, Iowa. These individuals were maintained garia x Ananassa) (Rosales: Rosaceae) in the Mid- outdoors in aluminum screen boxes (40 by 30 by west, is an introduced lepidopterous species (Ga- 10 cm) placed at ground level in a larger screen- briel 1989). Late-stage A. comptana larvae covered cage (100 by 70 by 15 cm) and covered overwinter in rolled strawberry leaves in the leaf with straw. We removed samples from the over- litter found in strawberry plantings (Webster 1918, wintering larval populations in September, Octo- Fink 1932, Bennett 1961). Previously, we deter- ber, and November in 1986 and in September, mined the influence of temperature and strawberry October, November, December, and January dur- cultivar on preimaginal development and the ovi- ing 1987-1988. Only three monthly samples were positional responses of A. comptana females to se- taken in 1986 because of high (>80%) mortality lected strawberry cultivars (Gabriel & Obrycki of overwintering A. comptana larvae. Larvae from 1990). In this study, we present results of a com- the field were distributed equally among the con- bined laboratory and field study in which we de- stant temperatures and photoperiods (Tables 1 and termined the roles of temperature and photoperiod 2). In the first year of this study, 22 and 14°C on diapause maintenance and termination and on conditions were used; in the second year, only 22°C postdiapause development of A. comptana. was used. Larvae were checked every second day for pu- pation in the September-December samples. In- dividuals in the January samples were checked dai- Materials and Methods ly for pupation. The sex of pupae was determined, Field-collected A. comptana larvae were main- and the pupae were placed in individual gelatin tained in plastic Petri dishes (100 mm) and pro- capsules (size 00) and checked daily for adult eclo- vided with fresh greenhouse-grown strawberry leaf- sion. To determine the role of chilling (defined as lets (cultivars Selva, Honeoye, Redcoat, or exposure to low temperatures [Tauber et al. 1986])

0046-225Xj90j0932-0936$02.00jO © 1990 Entomological Soc'iety of America August 1990 OBRYCKI ET AL.: DORMANCY IN Ancylis comptana 933

Table 1. Developmenlal responses to temperature (OC) and photoperiod by overwintering A. comptana; Ankeny, Iowa, 1986

Mean number of days ± SD to complete development Sample date No. adults emerging Photo- Larval Pupal period. L:D 22· 14· 22· 14· 22· 14· 26 Sept. 86" 16:8 28 21 14 ± 2 26 ± 4 11 ± 9 25 ± 2 13:11 2 4 53 ± 10 94 ± 22 9 ± 1 26 ± 4 10:14 2 6 52 ± 0 82 ± 17 12 ± 4 25 ± 6 16 Oct. 86a

16:8 17 12 15 ± 4 23± 5 11 ± 1 32 ± 4 Downloaded from https://academic.oup.com/ee/article/19/4/932/2480444 by guest on 27 September 2021 13:11 9 11 43 ± 15 74 ± 21 11 ± 9 30 ± 5 10:14 5 8 47 ± 10 66 ± 17 12 ± 1 27 ± 5 14 Nov. 86b 16:8 6 7 12 ± 2 25± 6 11 ± 1 32 ± 2 13:11 4 5 41 ± 14 66 ± 14 10 ± 3 26 ± 6 10:14 3 4 35± 9 49 ± 14 11 ± 4 39 ± 18

ANOV A statistics given in Table 3. a 50 A. comptana larvae placed at each photoperiod. b 20 A. camp/ana larvae placed at each photoperiod. in diapause termination, we began sampling A. 1988 at the Iowa State University Horticultural comptana larvae in the fall before the onset of low Research Farm, Gilbert. On 30 March 1989, three temperatures in the field. Lumite screen cages (1.8 by 1.8 by 1.8 m) (Chi- Effects of Temperature on Postdiapause De- copee Manufacturing Company, Gainsville, Ga.) velopmeni. Based upon the results of the study of were placed over these areas. The daily maximum diapause duration, we sampled overwintering lar- vae in February and March 1988 to determine the relationship between temperature and postdia- Table 2. Developmental responses to photoperiod by pause development. The larvae were placed in in- overwintering A. comptana", trom Ankeny, Iowa, 22OC; 1987-1988 dividual Petri dishes as previously described and maintained at five constant temperatures from 14 Sample date No. Mean no days ± SO to complete Photo- to 30"C and a photoperiod of 16:8 (L:D) (Table 4). adults development period These individuals were checked daily for pupation emerging and adult eclosion. L:O Larval Pupal Total Statistical Analysis. The mean number of days 24 Sept. 87a required for A. comptana pupation and adult eclo- 16:8 29 21 ± 3 9±2 30± 4 sion was calculated for each experimental condi- 10:14 8 57 ± 19 12 ± 3 69 ± 17 tion at each sample date. Data within a sample 15 Oct. 87 date were compared using one-way analysis of 16:8 27 14 ± 3 12 ± 3 26 ± 3 10:14 12 42 ± 9 12 ± 4 55 ± 9 variance (ANOVA) (P = 0.05). No significant dif- ference between long (16:8) and short (10:14) pho- 27 Nov. 87 toperiodic responses at a given temperature for a 16:8 38 13 ± 2 11 ± 1 24 ± 2 13:11 21 22 ± 11 12 ± 4 30 ± 7 sample date was used as the criterion for ending 10:14 18 22 ± 16 11 ± 4 32 ± 16 diapause in field populations of A. comptana. The reciprocal of the mean postdiapause devel- 22 Dec. 87 16:8 27 6± 2 14 ± 2 20 ± 3 (l/days) comptana opmental time for A. was re- 13:11 32 7± 6 11 ± 1 17± 5 gressed against temperature, and the resulting curve 10:14 31 6± 2 11 ± 1 16 ± 3 = was tested for linearity using ANOVA (P 0.05). 7 Jan. 88 The theoretical threshold for postdiapause devel- 16:8 43 6± 2 12 ± 1 18 ± 2 opment (tpd) was estimated by extrapolation, and 13:11 34 6± 1 11 ± 1 17± 1 the thermal constant (K) was calculated as 11m, 10:14 37 6± 3 11 ± 1 15 ± 1 where m is the slope of the line predicted from 26 Jan. 88 linear regression analysis (Campbell et al. 1974). 16:8 40 4± 9 ± 1 14 ± 2 Degree-day Summations for Postdiapause De- 13:11 31 5± 12 ± 1 16 ± 1 velopment. To determine the accuracy of the t 10:14 38 5± 10 ± 1 15 ± 1 and K values for predicting postdiapause devel- ANOVA statistics given in Table 3. opment under field temperatures, we allowed a 40 A. camp/ana larvae placed at each photoperiod on 24 known numbers of A. comptana to overwinter in September 1987;50 larvae placed in each photoperiod on all other three 3.2-m2 strawberry plots during the fall of dates. 934 ENVIRONMENTALENTOMOLOGY Vol. 19, no. 4

Table 3. ANOVA statistics for developmental responses by overwinteringA. comptana larvae to temperature aod photoperiod (see Tables I and 2) Larval Pupal Total Sample date 22· 14· 22" 14· 22· F df P F df P F df P F df P F df P 26 Sept.86 352 2,32 0.0001 ll8 2,43 0.001 3.6 2,29 0.04 NS 16 Oct.86 48 2,36 0.0001 48 2,44 0.0001 NS NS 14 Nov.86 16 2, 12 0.004 36 2,24 0.0001 NS NS 24 Sept.87 ll3 1,38 0.0001 13 1,35 0.001 138 1,35 0.0001 15 Oct.87 230 1,37 0.0001 NS 260 1,37 0.0001 27 Nov.87 II 2,95 0.0001 NS 6.5 2, 74 0.0025

22 Dec.87 NS 50 2,86 0.0001 4.6 2,86 0.01 Downloaded from https://academic.oup.com/ee/article/19/4/932/2480444 by guest on 27 September 2021 7 Jan.88 NS 8.4 2, III 0.0001 3.8 2,111 0.025 26 Jan.88 NS 33 2, 106 0.0001 30 2, 106 0.0001

and minimum temperatures were recorded from gens. A histological study indicated the two pre- 1 January to 1 June on a hygrothermograph located dominant pathogens were Penicillum sp. or Scopu- <300 m from the cages. The numbers of adult A. lariopsis sp. (A.D.G., unpublished data). In the comptana were counted and removed daily from conditions in which> 10 adults emerged, the per- these three cages when temperature maxima were centage of females ranged from 38 to 65%, with a >20"C; adults were collected every 3 d when tem- mean (± SD) of 50 ± 11% (n = 5 conditions). perature maxima were <20°C. The number of de- In 1987, the number of days needed for A. comp- gree-days> tpd accumulated daily were calculated tana larvae to pupate at 16:8 (L:D) decreased from from 1 January using the method of Baskerville & 21 d in September to 6 d in December (Table 2). Emin (1969). By contrast, those individuals placed at 10:14 (L: D) in September and October required >40 d to Results pupate. From November to December, the number of days to pupate at short daylengths (13:11 and Diapause Maintenance and Termination. An- 10:14 [L:DJ) decreased from 22 d to 6-7 d (Table cylis comptana larvae transferred from the field 2). In the two January samples, larvae required 4- during September, October, and November 1986 6 d to pupate at the three photoperiods. Pupal and placed at 16:8 (L:D) pupated within 15 d at development was not influenced by photoperiod 22°C and within 26 d at 14°C (Table 1). At 13:11 or sample date in a consistent pattern, averaging (L:D) and 22°C, larvae required between 43 and 9-14 d for all sample dates (Table 2). 53 d to pupate; at 14°C, 74-94 d were needed. The The percentage of survival of overwintering A. time from sampling to pupation at 10:14 (L:D) was comptana larvae was generally higher in the 1987 similar to that observed at 13:11 (L:D) at both samples. Survival at 16:8 and 13:11 (L:D) was typ- temperatures for the three monthly samples. Mean ically >50%, ranging from 42 to 86%. Under a times for pupal development at 22°C over the three photoperiod of 10:14 (L:D), the percentage of sur- photoperiods for the three monthly samples ranged vival increased from 20% in the September sample from 9 to 12 d. At 14°C, mean pupal developmental to 76% in the second January sample. The per- times ranged from 25 to 39 d and were not sig- centage of females under conditions with > 10 nificantly different over the three photoperiods for emerging adults ranged from 42 to 67%, with a each monthly sample (Table 3). mean (±SD) of 56% ± 9 (n = 15 conditions). Survival of A. comptana larvae in the 1986 sam- Postdiapause Development. Between 14 and ples ranged from 4 to 25% for individuals placed 26°C, there was a direct relationship between tem- at 13:11 or 10:14 (L:D). Survival at 16:8 (L:D) was perature and the rate of postdiapause larval de- higher, ranging from 24 to 56%. More than 50% velopment leading to pupation. The ANOVA for of the dead larvae were infected with fungal patho- linearity indicated that the larval postdiapause de-

Table 4. Postdiapause development times of A. comptana under constant temperatures ± IOC and 16:8 (L:D)

Temp,"C Lifestage 14 18 22 26 30 Larva 10.2 ± 1.9 7.5 ± 0.4 3.8 ± 0.7 2.7 ± 0.5 52.9 ± 0.5 Pupa 29.4 ± 0.8 16.2 ± 1.1 9.4 ± 0.2 6.1 ± 1.3 5.7 ± 0.4 Larvato adult 39.6 ± 1.1 23.6 ± 1.4 13.1 ± 0.3 8.7 ± 1.8 8.5 ± 0.1 No·/rep. 13, 13 10, 16 22,17 24,20 20,17

° Valuesare days(f ± SE). August 1990 OBRYCKI ET AL.: DORMANCY IN Ancylis comptana 935 velopmental rate was linearly related to temper- Table 5. Emergenceof overwinteredA. comptono from atures in this range (Y == 0.0247X - 0.2721) (F == lhree field cages, Gilbert, Iowa, 1989 62; df = 1, 6; P < 0.0002). The t value for larval Cage postdiapause development is 11 ± 4.5°C, the ther- Parameter mal constant K is 40.5 ± 9 DD. Pupal development 2 3 was linearly related to temperatures from 14 to No. A. camptana larvae, 300e (Y = 0.0098X - 0.1065; t = 10.8 ± 3.5, K == 7 Oct. 1988 164 93 84 101.7 ± 3.2). Total development from the end of Total no. adults emerged, diapause to adult emergence also was linearly re- 1989 59 8 31 lated to temperatures between 14 and 30°C (Y = % Overwintering 0.OO65X - 0.067), requiring 154 DD > 10.3°C. survival 36 9 37 Date of first emergence 25 April 25 April 25 April Adult emergence in field cages began on 25 April Downloaded from https://academic.oup.com/ee/article/19/4/932/2480444 by guest on 27 September 2021 DD> 1O"C 97 97 97 1989 (192 DD > 10.5°C); 50% emergence occurred Date of 50% emergence 9 May 8 May 10 May between 8 and 10 May (256-286 DD) (Table 5). DD> 1O"C 145 142 149 The last adult emergence was observed on 31 May Date of 90% emergence 21 May 22 May 15 May (540 DD). DD> 1O"C 224 231 176

(9.7°C) and total preimaginal development (1O.2OC) Discussion of A. comptana (Gabriel & Obrycki 1990). The responses of A. comptana in the fall samples We have shown previously that the occurrence during both years show the following character- of A. comptana larvae in the field can be predicted istics: (1) long daylengths 16:8 [L:D]) will end based upon degree-day accumulations> 10°C (Ga- diapause under laboratory conditions, (2) short briel & Obrycki 1990). Combined with our data, daylengths (13:11 and 10:14 [L:D]) and low tem- which accurately modeled 50% emergence of over- peratures (14°C) maintain diapause, and (3) chill- wintering A. comptana in the field based upon 150 ing or a specific photoperiodic cue is not required DD > lOOC,the seasonal occurrence of larval pop- to stop diapause. During autumn, the role of short ulations can now be predicted for the entire grow- daylengths and low temperatures in maintaining ing season in Iowa. Management of A. comptana diapause in A. comptana is shown by the increased is greatly facilitated by the ability to predict the developmental times under these conditions. The occurrence of early instars, which do not exhibit similar responses to 13:11 and 10:14 (L:D) in the leaf-rolling behaviors. September-November samples suggest an all-or- none response to daylength by A. comptana. This type of photoperiodic response has been observed Acknowledgment in several insect species and has been described as We thank James Robison-Cox, Iowa State University, an all-or-none response in relation to a critical pho- for statistical assistance. We also thank Maurice and toperiod (long versus short day lengths) (Tauber et Catherine Tauber, Cornell University, Ithaca, N.Y., for al. 1986). In this type of response, the sensitivity their critical review of this manuscript. This research to photoperiod diminishes as diapause progresses. was supported by a grant (#88-13) from the Leopold In our study, the larval response of A. comptana Center for Sustainable Agriculture, Iowa State Univer- to photoperiod can no longer be observed by the sity,and an Iowa State University Research Grant funded third week of December; i.e., the number of days through the Iowa State University Achievement Foun- from sampling to pupation are similar under long dation. This is Journal Paper J-13722 of the Iowa Agri- culture and Home EconomicsExperiment Station, Ames, and short photoperiods. Pupal development of A. Iowa. Project 2755. comptana was not observed to be consistently in- fluenced by photoperiod in any of the monthly samples. References Cited The requirements for postdiapause development Baskerville, G. L. & P. Emin. 1969. Rapid estimation for an insect species may differ from those for of heat accumulation from maximum and minimum nondiapause development. For example, prepupal temperatures. Ecology 50: 514-517. diapause development of two lacewing species, Bennett, S. E. 1961. The strawberry leaf roller com- Chrysopa oculata Say and C. nigricornis Bur- plex in Tennessee. J. Tenn. Acad. Sci. 36: 320-360. meister, requires a greater number of degree-days Boyne, J. V., G. C. Rock & L. A. Nelson. 1985. Dia- than nondiapause prepupal development (Propp et pause in P{atynota idaeusalts (Lepidoptera: Tortri- al. 1969, Tauber & Tauber 1972), whereas post- cidae): effects of temperature, photoperiod, and time diapausing alfalfa blotch leafminer (Agromyza of inoculation in the field on diapause termination. Environ. Entomol. 14: 790-796. fronteUa (Rondani)) pupae require fewer degree Campbell, A., B. D. Frazer, N. Gilbert, A. P. Gutierrez days for development than nondiapausing pupae & M. Mackauer. 1974. Temperature requirements (Nechols et al. 1983). The thermal threshold for of some aphids and their parasites. J. Appl. Ecol. 11: postdiapause development of A. comptana (1O.5°C) 431-438. is similar to the t values for nondiapause larval Fink, D. E. 1932. Biologyand habits of the strawberry 936 ENVIRONMENTAL ENTOMOLOGY Vol. 19, no. 4

leaf roller, Ancylis comptana (Froel.) in New Jersey. controlling dormancy in Chrysopa oculata (Neurop- J. Agric. Res. 44: 541-558. tera: Chrysopidae). J. Insect. Physiol. 33: 627-633. Gabriel, A. D. 1989. Ecological factors affecting Propp, G. D., M. J. Tauber & C. A. Tauber. 1969. strawberry leafroller, Ancylis comptana (Froelich), Diapause in the neuropteran Chrysopa oculata. J. biology. M.S. thesis, Iowa State University, Ames. Insect. Physiol. 15: 1749-1757. Gabriel, A. D. & J. J. Obryeki. 1990. Thermal re- Tauber, M. J. & C. A. Tauber. 1972. Larval diapause quirements for pre imaginal development of the in Chrysopa nigricornis: sensitive stages. critical pho- strawberry leafroller, Ancylis comptana (Froelich) toperiod, and termination (Neuroptera: Chrysopi- (Lepidoptera: Tortricidae). Environ. Entomol. 19(2): dae). Entomol. Exp. Appl. 15: 105-111. 339-344. 1973. Quantitative response to day length during dia- 1990. Cultivar acceptance and suitability for pre- pause in insects. Nature (Lond.) 244: 296-297. imaginal development of the strawberry leafroller Tauber, M. J., C. A. Tauber & S. Masaki. 1986. Sea- (Lepidoptera: Tortricidae). J. Econ. Entomol. 83: 514- sonal adaptations of insects. Oxford University Press, 518. New York. Downloaded from https://academic.oup.com/ee/article/19/4/932/2480444 by guest on 27 September 2021 Neehols, J. R., M. J. Tauber, C. A. Tauber & R. G. Webster, R. L. 1918. The strawberry leafroller. Iowa Helgesen. 1983. Environmental regulation of dor- Agricultural Experiment Station, Entomology Sec- mancy in the alfalfa blotch leafminer, Agromyza tion, Bull. 1979, Ames. frontella (Diptera: Agromyzidae). Ann. Entomol. Soc. Am. 76: 116-119. Neehols, J. R., M. J. Tauber & C. A. Tauber. 1987. Received for publication 6 November 1989; accepted Geographical variability in ecophysiological traits 15 February 1990.