Temperature-Dependent Egg Hatch and Cold Storage of Eggs of Otiorhynchus ovatus (L.) (Coleoptera: Curculionidae) 1
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1 Temperature-Dependent Egg Hatch and Cold Storage of Eggs of Otiorhynchus ovatus (L.) (Coleoptera: Curculionidae) 1 James R. Fisher and David L. Edwards United States Department of Agriculture, Agricultural Research Service, Horticultural Crops Research Laboratory, 3420 NW Orchard Avenue, Corvallis, Oregon J. Agric. Urban Entomol. 19(2): (April 2002) ABSTRACT Egg hatch of the strawberry root weevil, Otiorhynchus ovatus (L.) was studied at constant temperature intervals from 6 to 36 C. Storage of eggs for use in rearing and pot and field infestations was studied at six lowtemperature treatments (<16 C) for storage intervals up to 15 wk. Limited hatch was obtained at 6 and 33 C but mortality was >85%. Preliminary studies had shown that there was 100% mortality at 3 and 36 C. We conclude that the lower threshold for egg development would be 4 C and the upper lethal temperature was between 33 and 36 C. There was <10% mortality at all other temperatures (>6 C <33 C). Rate of development of the eggs to hatch was fit to a nonlinear curve. The lowest mortality and least amount of time for duration of hatch were found at 21 C. After examining mortality, rate of development, and the overall duration of hatch, we concluded that the optimum temperature range for O. ovatus egg hatch was C. We found that eggs could be stored and be > 60% viable at a temperature of 4 C for up to 4 wk. Insecta, strawberry root weevil, low temperature, egg devel- KEY WORDS opment The strawberry root weevil, Otiorhynchus ovatus (L.), is a worldwide polyphagous pest. In the Pacific Northwest of North America, it has been a pest of peppermint, conifers, strawberries, and many other nursery and berry crops for more than 100 yr (Lovett 1913, Downes 1922, Wilcox et al. 1934). This species is univoltine, wingless, and parthenogenetic (Wilcox et al. 1934). The eggs are laid in late spring to late summer on the soil surface, in soil litter, or fall from leaves onto the soil surface. Reports have varied on the duration of egg incubation, 7 25 d (Lovett 1913, Treherne 1914, Downes 1922, Schread 1950). Brandt et al. (1995) recently reported that egg hatch was about 16 d at 15 C. Generally, eggs deposited in the field hatch within a week or two after oviposition. After egg hatch the neonate larvae seek-out and feed on the roots or rhizomes of a host plant. They overwinter in the larval stage. During the winter, larval feeding is presumed to be temperature dependent (Schuh & Zeller 1944). Efficacy of biological strategies and of new insecticides has been negatively affected by the paucity of knowledge about specific timing of life events and other 1 Accepted for publication 22 September Prod. #192-6
2 110 J. Agric. Urban Entomol. Vol. 19, No. 2 (2002) aspects of O. ovatus biology in North America. Detailed studies of O. ovatus biology in North America have been limited to enumeration of host plants (Treherne 1914) or development on specific crops: Emenegger & Berry (1978), and Cacka (1982) on mint, and Brandt et al. (1995, 1996) on conifers. Umble & Fisher (2000, 2002) studied the development of pupae and adults on strawberries. Presently, in Oregon and Washington, other than to spray insecticide for adults when they are visible, there are no pest management strategies for this species. There is a need for predictive models for life events of this species and for thermal thresholds for each stage to facilitate laboratory studies and to help develop more efficacious management strategies for this pest. In preliminary studies, this species appeared to be negatively influenced by high temperatures (>30 C). However, eggs are oviposited in mid-summer and, often, may be exposed to soil temperatures >30 C. Here we report on the effect of constant temperature regimes on egg development and mortality. We also report on a study with low-temperature storage of O. ovatus eggs. Branson (1978) found that Diabrotica virgifera virgifera LeConte eggs could be stored for as many as 52 wk at 10 C, just below their threshold of development, without a significant loss in viability. Later, Sutter & Branson (1986) used this technique to stockpile millions of D. v. virgifera eggs for use in artificial infestation of corn. Our laboratory and several others in the Pacific Northwest have need for many thousands to millions of O. ovatus eggs and other stages, for our rearing programs and for studies involving artificial infestation of nursery containers and field plots (many thousands to millions of eggs are needed for an experiment). We have a small rearing cadre, limited spring collection of larvae and adults, and a limited, weekly, egg production. We felt that if we could store eggs for even a limited period of time, we would be able to enhance our programs. This study also provides insight as to the adaptability of the eggs of this species to lowtemperature winters. Materials and Methods Source of insects. All eggs used in this study were obtained from adults that had been reared [21.0 ± 0.5 C; 16:8 h (light:dark)] in the laboratory from late instars collected from a strawberry field near Aurora, Oregon (L N; l ). Larvae were placed in 0.5-liter plastic deli containers (Reynolds Metal Co., Richmond, Virginia) that contained a 4-cm layer of moist peat moss. Pieces of longitudinally sliced carrots (Masaki & Sugimoto 1991) were supplied as food and replaced as necessary until pupation. Pupae were transferred to similar containers that contained only moist peat moss. As eclosion proceeded, callow adults were removed and placed in adult cages; similar containers that did not contain peat moss but had three strawberry leaves as food. The leaves were kept fresh by placing the leaf petioles in a floral waterpic. The leaves and cages were replaced every 5 d at which time the eggs were collected from the container. Egg collection. Weevils laid eggs on the strawberry leaves and on the bottom of the rearing container. One time each week the weevils were removed to new, rearing-oviposition containers. The used container was rinsed so that the eggs, frass and accumulated debris were in the bottom of the container. Excess water was removed. Eggs and debris were separated by differential floatation; 40%
3 FISHER & EDWARDS: Temperature and Egg Hatch of Otiorhynchus ovatus 111 aqueous solution of sucrose (specific gravity, 1.17) in a 1000-ml separatory funnel. The eggs floated to the surface while most of the debris sank. After the debris was elutriated from the funnel and nearly all of the eggs remained, water was added until it nearly filled the funnel. The eggs were allowed to settle. Eggs and water were then drained from the separatory funnel into a Buchner funnel-suction apparatus fitted with a 90 mm circle of filter paper. For experimentation, samples of 25 eggs were removed from the filter paper, using a three hair, camel hair brush, and placed on moistened, autoclaved filter paper in small (50 9 mm, Falcon ), snap-lid Petri dishes (Becton Dickinson Labware, Franklin Lakes, New Jersey). Samples were replicated ten times for each temperature treatment in the egg hatch experiment. For the egg storage experiments, we used 10 boxes of 25 eggs for each storage time and temperature regimen. Temperature treatments. For each study, egg hatch and egg storage, a series of growth chambers were used that maintained a constant set point temperature (±0.5 C). For the egg hatch study we used temperatures at 3 C intervals from 6 33 C, and for the study on low-temperature storage, we used temperatures of 2, 4, 6, 9, 12, and 15 C. In both studies, we use a photoperiod of 0:24 h (light:dark). Duration of the experiments and data collection. With the egg hatch experiment, we inspected the dishes with eggs daily after the fifth day of exposure. The number of eggs that hatched as well as the number of eggs whose embryos were determined to have died was recorded until all eggs had either hatched or died. For egg storage, eggs remained at a storage temperature from 1 15 wk. At the end of a prescribed time-period, the egg containers and eggs were placed in a 21 C growth chamber. Thereafter, egg hatch and mortality were recorded daily. Statistical analysis. Data from the temperature-dependent egg hatch study were submitted to a series of nonlinear relationships that are contained in the PMDS software system of Logan & Weber (1990). The equation that had the best fit (r 2 ) to the data was chosen to represent the development curve. Simple statistics (means and standard error) were used with the mortality and time-event data from the egg hatch study. Analysis of variance (Hintze 2001) was used to determine relationships of means of the time-event data from the egg hatch study. Response surface analysis (Hintze 2001) was used to delineate survival responses to the time-temperature storage study. Results and Discussion Understanding the effect of varying temperatures on life stage mortality as well as how those temperatures affect rate of development allows inference of optimal temperature ranges, and upper and lower lethal temperatures. This may assist in development of forecasting models for a particular species. Preliminary studies with O. ovatus eggs had indicated that there was 100% mortality at temperatures of 3 C and 36 C. In this study mortality was minimal at temperatures > 9 C and < 30 C (Fig. 1). Some hatch was obtained at 6 and 33 C. However, at these temperatures (6 and 33 C) many of the larvae never escaped the chorion or died shortly after hatching. Mortality within a regimen showed little variation about the mean.
4 112 J. Agric. Urban Entomol. Vol. 19, No. 2 (2002) Fig. 1. Mortality (% ± SEM) of Otiorhynchus ovatus eggs when kept at various constant temperature regimes. Rate of development (determined by hatching) followed a nonlinear logistic type of curve. Our data was fit to a Type III curve of Hilbert & Logan (1983): r (T) [(T adj 2 /{T adj 2 +D 2 }) 1/e (Tmax Tadj/ T) ] (Fig. 2). In this equation, r (T) the rate of development at temperature (T); (, D,and T were constants; T max the temperature at the maximum rate of development (calculated); T min the temperature at the minimum rate of development (calculated), and T adj T T min. The values of these constants were calculated iteratively through the PMDS system. The values were: 1.20, D 52.91, T min 1.12, T max 36.44, and T The equation fit our data extremely well, r Our tested maximum temperature was 27 C with a developmental rate of and the calculated curve maxim was 28 C with a developmental rate of 0.20/d. The rate of development at 33 C was equal to that at 15 C (0.08/d; Fig. 2). The egg hatch-time records were analyzed to determine the average time from the start of incubation at each temperature to the beginning (initiation) of hatch and the duration of hatch (Fig. 3). There were significant differences among the time to initiation of hatch at each constant temperature (F ; df 9, 90; P 0.05) and the last hatch (duration; F 161.3; df 9, 90; P 0.05). These statistics contribute additional information about the optimum temperatures for incubation and offer insight in determination if a temperature is, indeed, deleterious to the egg stage. Despite high mortality some eggs did hatch at 6 and 33 C. Very few hatched (<10%) at 33 C (Fig. 1). Thus, hatch times from 6 and 33 C may or may not be accurate as they are based on a small sample size. However, those at 6 C took >5 times the number of days to initiate hatch than at any other temperature studied. Hatch at 33 C started and lasted for about the same
5 FISHER & EDWARDS: Temperature and Egg Hatch of Otiorhynchus ovatus 113 Fig. 2. Days to hatch (squares) and rate of development (1/d) (circles) curves for egg hatch of Otiorhynchus ovatus eggs kept at various constant temperature regimes: r (T) [(T adj 2 /{T adj 2 +D 2 }) 1/e (Tmax Tadj/ T) ]. amount of time as at 18 and 15 C. Hatch for each cohort began in <10dat temperatures from C. The combination of the lowest mortality and shortest duration for hatch was found at 21 C even though the rate of development to hatch was slower than at C (Fig. 2). Because there was >85% mortality at 6 C (Fig. 1) and no hatch at 3 C after nearly 200 d (preliminary investigations) we concluded that the lower threshold for egg development would be 4 C. The upper lethal temperature must be just above 33 C, as there was >95% mortality at this temperature (Fig. 1) and in our preliminary studies we found that 36 C was 100% lethal. After considering our mortality data and our rate of development calculations, we concluded that the optimal temperature range for development of O. ovatus eggs was C. Because 21 C showed the lowest mortality and development was 15%/d or 7 d for an egg to hatch, we have chosen 21 C as our standard for egg incubation. We have also use 21 C as our control temperature in other investigations. It was often difficult to collect sufficient eggs at any one-collection time to provide the needed number of eggs, larvae or adults for other studies at our laboratory. Collection and subsequent storage was necessary to have adequate numbers of eggs for our programs. Storing eggs in anticipation of need for experimentation has been used with other insects, i.e. Diabrotica virgifera virgifera LeConte (Sutter & Branson 1986). Presumably, storage temperatures must be low enough to minimize metabolism without appreciable mortality, yet high enough that when eggs are exposed to a favorable temperature, hatch proceeds at
6 114 J. Agric. Urban Entomol. Vol. 19, No. 2 (2002) Fig. 3. Intervals (mean days per treatment ± SE) for duration of hatch (last mean hatch per treatment) and the period needed for incubation until first hatch (initiation) for eggs of Otiorhynchus ovatus at various constant temperature regimes. Letters above each bar that are the same, are not significantly different, Tukey Kramer test, P a normal rate. Usually, optimum storage temperatures are close to the lower thermal threshold of development. Because we wanted to determine the effects of exposure time (storage) at specific constant low-temperature treatments, we fitted our data to a response surface equation (Hintze 2001). The derived equation was: % hatch T 8.69W 1.20T W TW; T temperature, W wk, (F 81.1; df 5, 69; P 0.001) r (Fig. 4). All temperatures below 9 C worked well for storage. Above 9 C, eggs hatched in less than 2 wk and had ample development at 5 d (Fig. 2). Even at 9 C, some eggs were hatching at 3 wk. Thus, 9 C was too high a temperature for storage. We concluded that minimal development, in terms of time to hatch after storage and exposure to a constant temperature of 21 C, occurred at 4 and 6 C (Fig. 4). Maximum storage time with minimum mortality was 4 wk; after 4 wk hatch began to decrease due to increased mortality. We have chosen 4 C as the best storage temperature because the developmental rate at 4 C was at the threshold and mortality after 4 wk or less of storage was minimal (Fig. 4). The high viability and minimal development of eggs stored at 4 C is helpful in solving problems associated with obtaining enough eggs to conduct research projects. We are now able to store eggs for colony maintenance and experimentation over a 4-wk period and expect very little deviation in subsequent development as
7 FISHER & EDWARDS: Temperature and Egg Hatch of Otiorhynchus ovatus 115 Fig. 4. Response surface curve (% hatch T 8.69W 1.20T W TW) for Otiorhynchus ovatus egg hatch at 21 C after storage for up to 15 wk at various temperatures. compared with eggs that we would use that are 5 7 d old (> 60% hatch in < 2 wk). This knowledge has allowed us to maintain O. ovatus colonies with a sufficiently large and consistent number of insects throughout the year. O. ovatus has been a widespread pest of many different plants in many parts of the United States and Canada. Collection records in North America place the majority of collection sites north of 37 N, L (Warner & Negley 1976). Additionally, only a few collections were made north of 50 N, L. A majority of all collections were from areas where the weather is moderated by coastal and/or lake effects. There is no record of eggs of this species overwintering. The outcome of this study provides evidence that either overwintering egg survival or diapause that may enable eggs to overwinter is not probable; particularly when near soil surface temperatures regularly fall below 0 C. When the thermal relationships of eggs, pupae (Umble & Fisher 2000), and adult preoviposition and oviposition (Umble & Fisher 2002) are considered, the occurrence and possible establishment of this species beyond its present distribution in North America appears improbable. Acknowledgment The authors thank our student workers, Shannon Schowalter, Deborah Artimez, and Nathan Burch for their diligence and commitment to these studies. We also thank Richard Mankin, USDA, ARS, CMAVE and Glenn Fisher, Oregon State University and two anony-
8 116 J. Agric. Urban Entomol. Vol. 19, No. 2 (2002) mous reviewers for their comments and guidance in earlier versions of this manuscript. This research was supported, in part, by a grant from the Northwest Center for Small Fruit Research, Corvallis, Oregon. References Cited Brandt, J. P., S. M. Smith & M. Hubbes Bionomics of strawberry root weevil adults, Otiorhynchus ovatus (L.) (Coleoptera: Curculionidae), on young ornamental conifer trees in southern Ontario. Can. Entomol. 127: Brandt, J. P., S. M. Smith & M. Hubbes Distribution and sampling of root weevil larvae in young ornamental conifer plantations. Can. Entomol. 128: Branson, T. F Optimum temperature for long-term storage of eggs of Diabrotica virgifera (Coleoptera: Chrysomelidae). Entomol. Exp. Appl. 24: Cacka, J. F Biology, distribution and economic threshold of the strawberry root weevil, Otiorhynchus ovatus (L.) in peppermint. MS thesis, Department of Entomology, Oregon State University, Corvallis, 74 pp. Downes, W The strawberry root weevil with notes on other insects affecting strawberries. Dominion of Canada Department of Agriculture Pamphlet 5. New Series, Ottawa, Ontario, 13 pp. Emenegger, D. B. & R. E. Berry Biology of strawberry root weevil on peppermint in Western Oregon. Environ. Entomol. 7: Hilbert, D. W. & J. A. Logan Empirical model of nymphal development for the migratory grasshopper, Melanoplus sanguinipes (Orthoptera: Acrididae). Environ. Entomol. 12: 1 5. Hintze, J. L Number cruncher statistical system, 329 North 1000 East, Kaysville, Utah. Logan, J. A. & L. E. Weber Population Model Design System (PMDS). Department of Entomology, Virginia Polytechnic and State University, Blacksburg, 72 pp. Lovett, A. L Strawberry pests in Oregon. The strawberry root weevil, pp In Oregon Agriculture Experiment Station Biennial Crop Pest and Horticulture Report, , 316 pp. Masaki, M. & S. Sugimoto Rearing methods of larvae of black vine weevil, Otiorhynchus sulcatus (F.), and some other Otiorhynchid weevils (Coleoptera: Curculionidae). Res. Bull. Plant Prot. 27: Schread, J. C The strawberry root weevil in nursery planting. Connecticut Agricultural Experiment Station, Circular 174, New Haven, Connecticut, 8 pp. Schuh, J. & S. M. Zeller Insect pests and diseases of strawberry in Oregon. Oregon Agriculture Experiment Station Bulletin 419, Corvallis, 40 pp. Sutter, G. R. & T. F. Branson Artificial infestation of field plots, pp In J. L. Krysan and T.A. Miller [Eds.], Methods for the study of pest Diabrotica. Springer- Verlag, New York, 260 pp. Treherne, R. C The strawberry root weevil. Canadian Department Agriculture Experiment Farms, Entomological Bulletin No. 8 (Bull. No. 18, second series), Ottawa, 44 pp. Umble, J. R. & J. R. Fisher Temperature-dependent development of Otiorhynchus ovatus (L.) (Coleoptera: Curculionidae) pupae. Environ. Entomol. 29: Umble, J. R. & J. R. Fisher Influence of temperature and photoperiod on the preoviposition duration and oviposition of Otiorhynchus ovatus (L.) (Coleoptera: Curculionidae). Ann. Entomol. Soc. Am. 95: Warner, R. E. & F. B. Negley The genus Otiorhynchus in America North of Mexico (Coleoptera: Curculionidae). Proc. Entomol. Soc. Washington 78: Wilcox, J., D. C. Mote & L. Childs The root weevils injurious to strawberries in Oregon. Oregon Agricultural Experiment Station Bulletin 330, Corvallis, 109 pp.
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