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Lobesia Botrana Stefanos S Blackwell Publishing, Ltd. Cold hardiness of diapausing and non-diapausing pupae of the European grapevine moth, Lobesia botrana Stefanos S. Andreadis1, Panagiotis G. Milonas2* & Mathilde Savopoulou-Soultani1 1Laboratory of Applied Zoology and Parasitology, Faculty of Geotechnical Sciences, Aristotle University of Thessaloniki, 541 24 Thessaloniki, Greece, 2Benaki Phytopathological Institute, Department of Entomology, Laboratory of Biological Control, 8 S. Delta St., 14561 Kifissia, Attikis Greece Accepted: 9 June 2005 Key words: supercooling point, acclimation, prefreezing mortality, Lepidoptera, Tortricidae Abstract Lobesia botrana (Denis & Schiffermüller) (Lepidoptera: Tortricidae) is a key pest of grapes in Europe. It overwinters as a pupa in the bark crevices of the plant. Supercooling point (SCP) and low temperature survival was investigated in the laboratory and was determined using a cool bath and a 1 °C min−1 cooling rate. Freezing was fatal both to diapausing and non-diapausing pupae. SCP was significantly lower in diapausing male (−24.8 °C) and female (−24.5 °C) pupae than in non-diapausing ones (−22.7 and −22.5 °C, respectively). Sex had no influence on SCP both for diapausing and non-diapausing pupae. Supercooling was also not affected by acclimation. However, acclimation did improve survival of diapausing pupae at temperatures above the SCP. Survival increased as acclimation period increased and the influence was more profound at the lower temperatures examined. Diapausing pupae could withstand lower temperatures than non-diapausing ones and lethal temperature was significantly lower than for non-diapausing pupae. Freezing injury above the SCP has been well documented for both physiological stages of L. botrana pupae. Our findings suggest a diapause-related cold hardiness for L. botrana and given its cold hardiness ability, winter mortality due to low temperatures is not expected to occur, especially in southern Europe. early larval stages are exposed to short-day photoperiods Introduction (Deseö et al., 1981). The European grapevine moth, Lobesia botrana (Denis & Insects of the temperate zone adopt a combination of Schiffermüller) (Lepidoptera: Tortricidae), is the most strategies to avoid the damaging effects of exposure to low harmful pest in vineyards of the Mediterranean region. temperature during the winter. At least part of the insect It completes two or three generations per year and populations must be able to tolerate the yearly minimum exceptionally a partial or complete fourth one in the temperature of their overwintering habitats. The majority southern regions (Tzanakakis et al., 1988). Larvae of the of them enter diapause or develop cold hardiness to cope first generation damage the inflorescences and those of with severe winter climates. Diapause and cold hardiness the following generations damage the green, ripening, and are often closely linked in time, but it is not clear how they ripe grape berries. In addition to direct damage, damage to are related, so there is conflicting evidence as to whether ripe or nearly ripe grapes is often accompanied by there is a relation or not (Salt, 1961; Denlinger, 1991; infection of the grapes by the gray mould fungus, Botrytis Hodkova & Hodek, 2004). cinerea Persoon (Sclerotiniaceae) (Savopoulou-Soultani Cold hardiness refers to the capacity of an organism to & Tzanakakis, 1988). Lobesia botrana enters a facultative survive exposure to low temperature and is influenced by autumn hibernal diapause-mediated dormancy in the a variety of factors, including low temperature acclimation pupal stage, which is induced when the embryonic and/or (Lee, 1991; Block, 1995). Acclimation for a few days at low temperatures considerably improved cold hardiness (Nedved, 1995; Ko8tál et al., 1998; Milonas & Savopoulou- *Correspondence: Panagiotis G. Milonas, Benaki Phytopathological Institute, Department of Entomology, Laboratory of Biological Soultani, 1999) although not always (Popham et al., 1991). Control, 8 S. Delta St., 14561 Kifissia, Attikis Greece. In spite of the fact that the biology of L. botrana has been E-mail: [email protected] studied extensively (Deseö et al., 1981; Savopoulou- © 2005 The Netherlands Entomological Society Entomologia Experimentalis et Applicata 117: 113–118, 2005 113 114 Andreadis et al. Soultani et al., 1998, 1999), studies on the impact of Determination of lethal temperature temperature are limited to the estimation of temperature The temperature, at which 50% and 90% of pupae died, limits for development, and defining day-degrees was determined by cooling groups of 30 individuals required for predicting developmental events in the field (three replicates of 10 pupae for each treatment and sex (Briere & Pracros, 1998; Milonas et al., 2001). separately) to a range of low and subzero temperatures In the present study, we examined the cold tolerance of for 2 h. Exposure temperatures ranged from −3 to −17 °C diapausing and non-diapausing pupae of L. botrana to depending on their physiological condition. Pupae were subzero temperature and determined the supercooling placed in thin-walled test tubes plugged with foam rubber point (SCP) and low lethal temperature (LTemp) of both and immersed in the circulating bath with a solution of physiological stages. We also evaluated the effect of low ethylene glycol and water where the temperature had acclimation in diapausing pupae with respect to their been preset to the desired level. After exposure, non- ability to supercool and to survive at subzero temperature diapausing pupae were transferred to 25 °C under a L16:D8 after a brief exposure at low temperature. photoperiod. Pupae were considered dead if they did not emerge after 30 days or if they had visible signs of deformation after emergence. In contrast, diapausing Materials and methods pupae were held first at 5 °C under a L8:D16 photoperiod Insects for 50 days following each treatment and then at 10 °C in A laboratory colony of L. botrana was established by continuous darkness for 10 days in order to terminate collecting larvae of different stages from vineyards in diapause. Afterwards, they were transferred to 25 °C under northern Greece (Kavala). Larvae were maintained on a L16:D8 photoperiod where mortality was recorded as for artificial diet (Savopoulou et al., 1994). Adults were placed non-diapausing pupae. in truncated transparent plastic cups covered with tissue paper. A hole was punched at the bottom of each cup and Evaluation of acclimation effect in diapausing pupae was plugged with dental roll wick, which provided the To test if acclimation could enhance survival of diapausing adults with a 5% sucrose solution. The eggs were laid on pupae, groups of pupae (three replicates of 10 pupae the inner walls of the cups and after the removal of adults, for each treatment and sex separately) were placed in pieces of artificial diet were provided for the neonate controlled environmental chambers at 5 °C (Precision larvae. Non-diapausing pupae were obtained by rearing Scientific, General Electric, Louisville, KY, USA) under the insects at 25 °C under a L18:D6 photoperiod. Pupal L8:D16 photoperiod for a period of 6, 12, and 18 days. diapause was induced by rearing larvae at 20 °C under Then they were cooled at −10, −12, −14, and −16 °C for a L8:D16 photoperiod. When larvae approached full 2 h. Mortality was observed the same way as mentioned growth, a strip of corrugated paper was added to each cup before. to provide suitable pupation sites. Paper strips with fully grown larvae or pupae were taken from the cups every Statistical analysis second day and maintained at 25 °C under a L18:D6 Differences between treatment means of SCP were photoperiod. Pupae not developing into adults within compared by t-test and one-way ANOVA (SPSS, 2000). 25 days, although remaining alive, were recorded as Lethal temperatures for 50% and 90% mortality of pupae dormant (Tzanakakis et al., 1988). were calculated by probit analysis after correction for control mortality using Abbott’s formula (Finney, 1952). Determination of supercooling points The effect of acclimation time at 5 °C of diapausing pupae Each pupa (5 days after pupation) was placed individually was estimated using the χ2-test (Sokal & Rohlf, 1995). into a transparent plastic capsule (16 × 7 mm) and immobilized with cotton. A copper constantan Results thermocouple (Digitron 2000T, Kalestead Ltd, UK) was attached to the surface of each pupa to monitor its body Supercooling points temperature. The capsule bearing the pupa with the sensor The mean supercooling point was −22.74 and −22.51 °C was placed in a test tube, which was then immersed in a for non-diapause male and female pupae, respectively. circulating bath (Model 9505, PolyScience, IL, USA) with The respective values of mean supercooling point for a solution of ethylene glycol and water. Cooling rate was set diapausing male and female pupae were −24.83 and at 1 °C min−1. The lowest temperature reached before an −24.53 °C. The difference between diapausing and non- exothermic event that occurred due to release of latent heat diapausing pupae was significant both for male (t = 0.035, was taken as the supercooling point of the individual. P<0.05) and female pupae (t = 0.011, P<0.05). Cold hardiness of Lobesia botrana 115 Table 1 Mean supercooling point (SCP) of diapausing and non-diapausing, male and female pupae of Lobesia botrana Mean SCP (°C ± SD) [range] Treatment (( n && n Non-diapausing −22.74 ± 0.63aA [−16.8–(–25.1)] 15 −22.51 ± 0.77aA [–17–(–25.5)] 15 Diapausing −24.83 ± 0.28bA [–22.9–(–25.9)] 12 −24.53 ± 0.45bA [–20.8–(–26.3)] 12 Means followed by the same lower case letter within a column and by the same capital letter within a line are not significantly different (t-test; P<0.05). (Table 1). No appreciable difference was observed between both sexes. In all cases, the values of LTemp50 and LTemp90 male and female pupae in both treatments, diapausing for females were slightly lower than those for males, (t = 0.575, P<0.05) and non-diapausing (t = 0.822, without being statistically significant.
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