Effect of plant architecture and hail nets on temperature of codling moth habitats in apple orchards

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Blackwell Publishing Ltd

Effect of plant architecture and hail nets on

temperature of codling moth habitats in apple orchards

Ute Kührt, Jörg Samietz* & Silvia Dorn

Institute of Plant Sciences, Applied Entomology, Swiss Federal Institute of Technology (ETH), CH-8092 Zurich, Switzerland Accepted: 30 November 2005

Key words: habitat temperature, developmental rate, phenology, leaf area index, global site factor, global radiation, insect pest, Cydia pomonella, Lepidoptera, Tortricidae

Abstract Plant architecture of apple trees in commercial orchards was rapidly changed from traditional tall trees to dwarf trees to optimize yield and fruit quality. Additionally, hail nets are widely used to pre- vent yield loss by hail. These changes are expected to considerably influence the orchard microclimate and thus the developmental rates of pest insects in apple. However, these relationships have not yet been fully elucidated. The present study was conducted over the seasonal cycle to investigate the influence of plant architecture and hail nets on the habitat temperatures of the codling moth, Cydia pomonella (L.) (Lepidoptera: Tortricidae), in apple, Malus domestica Borkh. (Rosaceae). Within the canopies, leaf area index (LAI) and global site factor (GSF) were quantified using hemispherical photography.

Temperature was analysed for the main habitats of the different codling moth stages, i.e., air within the canopy, bark of tree stems, and apple fruit. In dwarf trees, LAI was lower, leading to a higher GSF than in tall trees. Hail nets did not influence LAI and GSF. Results for dwarf trees compare as follows with those for tall trees: Average air temperatures within the canopy were 0.7 °C higher during daytime, whereas 0.4 °C lower at night. Mean surface temperatures of bark were 0.9 °C higher on sunny and 0.4 °C on overcast days. Mean surface temperatures of apple fruits were 1.8 –2.7 °C higher on sunny days, but 0.6 °C cooler on overcast days. The effect of hail nets was confined to a reduction of the air temperature within the canopy by approximately 0.2– 0.8 °C. Bark and apple surface temperatures were not significantly affected. Based on the temperature differences in the habitats considered, the calculated development of the codling moth in dwarf trees was on average 3 days faster than in tall trees. The calculations imply a negligible effect of hail nets on codling moth development.

Introduction

In the last few decades, commercial growers have rapidly changed the plant architecture of apple trees, Malus domestica Borkh. (Rosaceae). In order to increase yield and fruit quality, light penetration within the canopy has been optimized (Jackson, 1970; Verheij & Verwer, 1973; Ferree, 1989; Kappel & Quamme, 1993; Widmer et al., 1997).

Thus, in commercial orchard systems, the tree shape was changed from traditional standard-sized tall trees, further referred to as ‘tall trees’, to dwarf trees, e.g., spindle trees with a slender pyramidal shape (Widmer et al., 1997).

Additionally, in recent years, hail nets have been imple- mented in orchards for crop protection. As plant architecture and hail nets directly influence the solar radiation influx, they may modify the microclimate and, in particular,

the radiation and temperature regimes. Such changes may influence the development time of insects on the tree, as ambient temperature conditions determine insect body temperature, especially in small ectotherms (Heinrich, 1993).

Considerable research has been carried out on the influence of different apple orchard systems on the radiation regime within the canopy (e.g., Looney, 1968; Proctor et al., 1972; Landsberg et al., 1973; Blackburn & Proctor, 1984; Widmer, 1997a,b). However, much less is known about the effects on pest-insect development or even on the microclimatic factors, in particular temperature conditions, within the pest’s habitats. To evaluate the consequences of plant architecture and hail nets on the temperature regime within an insect’s habitat, we used apple and the codling moth, Cydia pomonella L. (Lepidoptera: Tortricidae), the major pest insect in apple orchards worldwide (Dorn et al., 1999), as a model system.

*Correspondence: E-mail: joerg.samietz@faw.admin.ch

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The codling moth overwinters as a mature larva under the bark of apple trees or in litter on the ground, and pupates there in spring. Under the conditions in northern Switzerland, the main cohort of adults emerges at the end of May or beginning of June, depending on climatic conditions (temperature sum) (Bovey, 1966). After mating, the females deposit their eggs mainly on leaves near apple- fruit clutches, but also directly on the young apple fruits (Geier, 1963; Blomefield et al., 1997), particularly in the later part of the season. This shift is most likely due to the seasonal changes in plant volatile emissions and associated responses of codling moth (Vallat & Dorn, 2005). The newly hatched larvae enter apple fruits, and one larva per fruit develops inside until the fifth larval instar, often causing the fall of premature apples. The mature larvae leave the apple fruits and search for pupation sites under the bark or on the ground. Depending on photoperiod and genetic factors, a proportion of the larvae enters obligatory diapause at this stage and continues development in the following year. Under favourable climatic conditions, i.e., high temperatures, the remaining larvae complete their development and establish a second or even third generation in the same year (Bovey, 1966; Wildbolz & Riggenbach, 1969).

The integrated management of the codling moth relies heavily on the precise timing of intervention at the correct development stage of the first generation in spring. The temporal dynamics, in particular the beginning of flight or egg hatching, is estimated by modelling approaches. These prediction models use standardized air temperature measurements from weather stations and developmental rates from laboratory studies (e.g., Baker, 1980; Rock & Shaffer, 1983;

Blago & Dickler, 1990; Lischke & Blago, 1990; Pitcairn et al., 1992).

The simulation models in use predict adult flight of the overwintered generation and the egg stage of the first generation to a satisfactory degree. Nevertheless, there is often a timing discrepancy between simulation results and observations, particularly for the later generations (Shaffer

& Gold, 1985; Blago & De Berardinis, 1991; Blago, 1992;

Lischke, 1992). One likely source for this discrepancy is the difference between weather station temperatures used to drive the models and microenvironmental temperatures experienced by developing individuals (Blago & De Berar- dinis, 1991; Blago, 1992). In fact, there is already evidence that plant temperatures rise well above air temperature due to solar radiation influx in orchards (Schroeder, 1965;

Landsberg et al., 1973; Graf et al., 2001; Howell & Schmidt, 2002). For example, apples in full sunlight can reach surface temperatures of 13 –14 °C above air temperature and even 3 °C above air temperature on their cool side, i.e., opposite to the sun-exposed hemisphere (Thorpe, 1974).

Similarly, the change in plant architecture from traditional tall to dwarf apple trees and the use of hail nets may lead to substantially different temperatures in C. pomonella habitats due to different radiation regimes. In a study of light transmission in different apple-cropping systems, slender spindle trees (height 2.3 m, spread 1.6 m) showed lower leaf areas and higher light levels than larger pyramid hedgerow trees (height 4.5 m, spread 4.5 m) (Ferree, 1989).

The resulting differences in habitat temperature may cause differences in body temperature of the codling moth. Because insect development depends greatly on body temperature, developmental rates may vary substantially under different plant architectures and under hail nets. Thus, the aim of the present study was to investigate the consequences of changing plant architecture and the use of hail nets on temperature of codling moth habitats, i.e., on the microclimate the different stages experience passively or may choose from to select their favourable body temperatures (cf. Kührt et al., 2005, 2006).

In our study, traditional tall apple trees were compared to dwarf apple trees, and dwarf trees with hail nets to trees without hail nets, regarding their plant architecture and habitat temperatures. Plant architecture was characterized by leaf area index (LAI) and potential global radiation energy transmission over the seasonal vegetation cycle. In order to relate microclimate to codling moth life cycle, temperature measurements and analyses were focused spatially on the main habitats of the insect. We measured the temperature of the air within the canopy, of the bark of tree trunks, and of apple fruits. The developmental rates were calculated based on these habitat temperatures to estimate the impact of plant architecture and hail nets on the development and seasonal population cycle of the codling moth. For these calculations the ambient conditions of eggs, feeding larvae, and mature larvae and pupae were approximated by the temperatures of air within the canopy, of apple fruits, and of bark, respectively. Finally, implications for modelling of population development or phenology in codling moth as the major pest insect in apple are discussed.

Materials and methods

Study sites

The study was carried out in a commercial apple orchard with dwarf trees and in a traditional apple orchard with tall trees in northern Switzerland (47°34′N, 8°13′E, 436 m a.s.l.) in two consecutive years (2001, 2002). The traditional apple orchard is situated about 500 m southeast of the dwarf apple orchard. For the habitat temperature measurements, three tall trees were randomly chosen in the traditional apple orchard (tree 1: ‘Gravensteiner’ 4.5 m high; tree 2:

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Temperature of codling moth habitats ²⁴⁷

‘Reinette’ 5.5 m high; tree 3: ‘Berner Rose’ 6.0 m high). The approximate diameter of these trees was 3 – 4 m, and the between-tree distances were 10 –27 m (mean 15 m). The foliage of the selected tall trees started at a height of approximately 1.5 –2 m above ground.

The dwarf apple orchard was managed with slender spindles, trees that are pruned to develop a narrow column- like shape. Diameters of single trees were ca. 0.8 m, and all trees were of the same age, height (3.0 m), and pruning. In the first year, one row of ‘Gala’ spindle trees at the orchard border was chosen for data sampling. Plant architecture measurements were conducted in the section of this east–

west orientated tree row that was not protected by hail nets. In the second year, two rows of ‘Golden Delicious’

spindle trees in the orchard centre were chosen for data sampling. The tree rows were north–south orientated. The between-row and within-row spacing was 3.0 × 0.8 m.

One of these ‘Golden Delicious’ rows was kept protected with hail nets, whereas the hail net over the other row was removed for the first 100 m. To avoid hail net effects, the adjacent tree rows were either unprotected (west) or the hail net was not closed for the whole season (east). The black hail nets were closed from mid-May until the beginning of November in 2002.

Measurements of plant architecture and potential irradiation Plant architecture of tall and dwarf trees was characterized by the determination of LAI and global site factor (GSF).

In both tree shapes, LAI and GSF were determined at different heights using hemispherical photography. From the digital photographs obtained, the LAI and the GSF were calculated with Hemiview software algorithms (HEMIVIEW, Delta-T Devices, Cambridge, UK). The GSF was calculated as the proportion of global (direct plus diffuse) radiation under a plant canopy relative to that in the open (100%). The LAI was estimated as half of the total leaf area per unit ground area (HEMIVIEW MANUAL 2.1, Delta-T Devices). The value computed by this procedure represents the effective LAI as hemispherical photography does not distinguish photosynthetically active leaf tissue from other plant elements such as stem, branches, or flowers (Jonckheere et al., 2004).

Hemispherical photographs were taken with a digital camera (Nikon Coolpix 990) equipped with a fisheye lens (HemiView Self Levelling Mount – Type SLM2, Delta-T Devices). Measurements were made under diffuse radiation conditions, i.e., at evenly overcast sky or at predawn or post-sunset. For comparable results between tall and dwarf trees, the top of the canopy was used as reference point.

The photographs were taken each at heights starting 0.5 m below the canopy top and continuing downwards every 0.5 m, i.e., at 0.5, 1.0, 1.5 m, etc., down to 2.5 m (dwarf trees)

or 4.5 m (tall trees) below the top of the canopy. To do so, the self-levelling fisheye lens with digital camera was mounted on top of a monopod composed of connectable aluminium segments (0.5 m). At each sample site (tall trees, and dwarf trees with and without hail nets), five photographs per height were taken on each sampling day.

The sampling was conducted during the entire vegetation period in both years. In 2001, the data were sampled from April to October (weeks of the year: 16, 18, 19, 21, 22, 24, 28, 29, 31, 32, 34, 36, 37, 39, 40, and 42). In 2002, measurements were taken from March to December (weeks of the year: 11, 15, 19, 23, 25, 30, 33, 36, 38, 40, 44, 46, and 50).

Tall and dwarf apple trees were compared regarding LAI and GSF for both years, whereas dwarf trees with and without hail nets were compared only for 2002.

Measurements of habitat temperature

Temperatures were measured in the following habitats: the air within tree canopies, the bark of tree trunks, and apple fruits. Air temperature within the canopy was measured continuously throughout the season as well as on selected days at noon (local solar noon ± 90 min). Surface temperatures of bark and apple fruits were sampled on selected days at noon. To obtain measurements for both extreme weather conditions, the temperature measurements at noon were taken on clear sunny as well as on completely overcast, but rainless days.

Continuous readings of the air temperature within the canopy (Tc) were taken with shielded thermistors (Campbell Scientific, Logan, UK) from February to December 2002.

In the dwarf apple orchard, three thermistors were placed as follows: above the tree canopy, and 1 and 2 m below the canopy top. The shielded thermistors were fixed along the centre of the tree-row length. Three shielded thermistors were similarly placed in one of the traditional tall trees:

above the tree canopy, and 1 and 2 m below the canopy top.

In both orchards, air temperature within the canopy was measured at 1-min intervals, and 10-min averages were recorded by CR10 data loggers (Campbell Scientific).

Habitat temperatures at noon were measured with hand- held type T thermocouple probes (Physitemp Instruments, Clifton, NJ, USA). To avoid any bias, random measurements of air temperature within the canopy (Tc) were taken in the centre of the row length of dwarf trees and in the canopy of the tall trees. Surface temperatures of randomly chosen bark spots and apple fruits were taken by pressing the thermocouple onto their north-facing and south-facing sides and pairwise averaging the north-facing and south-facing values to achieve one sample. For comparable results between tall and dwarf trees, habitat temperatures were each sampled at heights of 0.5, 1.0, 1.5 m, etc., down to 2.5 m (dwarf trees) or 4.5 m (tall trees) below the treetop. Per height, five

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samples for air and bark temperature and six samples for apple temperature were recorded at independent randomly chosen sites. Air temperatures within the canopy and bark temperatures were simultaneously measured on 15 clear sunny days and on 14 overcast days from March to Novem- ber 2002 (sunny days: 26 March, 10, 25 April, 15, 21 May, 4, 18 June, 1, 20, 30 July, 16 August, 5, 16, 30, September, and 28 October; overcast days: 14, 22 March, 8 April, 1, 6, 23 May, 2, 16 July, 4, 19, 26 September, 11 October, 5 and 18 November). Surface temperatures of apple fruits were measured separately on six clear sunny days and on three overcast days from June to September 2002 (sunny days: 17 June, 5, 19, 29 July, 15 August, and 6 September; overcast days: 2, 26 July, and 19 September). To minimize the influence of rapidly changing solar elevation, hand-measured habitat temperatures at noon were always recorded at local solar noon (± max. 90 min).

All habitat temperatures were analysed with reference to the standard air temperature measured 2 m above ground.

This standard air temperature (Ts) was supplied at 12-min intervals by a standard agro-weather station (Lufft, Mess- und Regeltechnik GmbH, Fellbach, Germany) installed in the dwarf apple orchard. The weather station was located within a distance of 500 m from both study orchards. The contemporaneous Ts was subtracted from all habitat temperatures in order to standardize the data for analysis.

Continuously recorded Tc data were pooled for the analyses in several steps. First, Tc was averaged hourly (0:10 – 1:00 hours = hour 1; 1:10 –2:00 hours = hour 2, etc.). For each day, the hourly average of the standard air temperature was subtracted from the hourly Tc. To distinguish between days of high and days of low incident radiation levels, each day was assigned as either clear or cloudy. ‘Clear days’ were defined as having a mean radiation intensity higher than 500 W m⁻² above the canopy from 11:30 to 13:30 hours (CET) from April to September, and higher than 300 W m⁻² in March and October. Days with lower radiation intensities at noon were regarded as ‘cloudy days’.

This radiation intensity was measured with a tube solari- meter (Delta-T Devices) above the canopy from February to December 2002. It was measured at 1-min intervals, and the 10-min averages were recorded by a CR10 data logger (Campbell Scientific). Clear and cloudy days separately were grouped according to the development stages of the main cohort of overwintered C. pomonella (after Bovey, 1966; Table 2). Furthermore, diurnal changes regarding the influences of plant architecture and radiation on habitat temperatures were considered in the analyses. To do so, we divided the diurnal cycle into four periods: daytime (9:00 –17:00 hours CET, i.e., 3.5 h before to 4.5 h after local noon), dusk (17:00 –21:00 hours CET), night (21:00 –5:00 hours CET), and dawn (5:00 –9:00 hours CET).

Statistical analysis

The plant architecture parameters measured (LAI and GSF) and habitat temperatures were analysed using repeated- measure analyses of variance (RM ANOVA). For the analyses of LAI, GSF, and habitat temperatures measured at noon; the samples over the season were considered as repeated measurements. For the analysis of the continuously recorded Tc, the hourly means of the four periods in a diurnal cycle (daytime, dusk, night, and dawn) were regarded as repeated measurements. Data for clear days and cloudy days were tested separately. All these variables were tested for the respective influence of factors, i.e., tree shape (tall tree, dwarf tree), hail net (with, without), height (0.5, 1.0, 1.5, 2.0, or 2.5 m below the canopy top) and exposure (side of tree stem or apple fruit facing north and south) and interactions between these factors. The differences in LAI and GSF between the tree shapes per sampling week were tested for pairwise significant differences with Fisher’s protected least significant difference (PLSD). The differences between habitat temperature and standard temperature of air (measured 2 m above ground) were analysed by one-sample t-tests for deviation from zero. The ANOVAs were carried out on normally distributed raw data or differences from reference values.

All statistical analyses were performed using SPSS version 11.0 for Apple Macintosh except for the Fisher’s PLSD that was conducted using STATVIEW version 5.0 for Apple Macintosh.

Calculation of developmental rates

The developmental rates were calculated for the various codling moth stages in tall apple trees and in dwarf apple trees with and without hail nets. For these calculations, we used equations derived from linear regression for development data obtained from the literature (Table 1). The developmental rates were calculated per hour using the hourly standard air temperature (Ts) as basis temperature.

According to the particular developmental stage, the differences to the habitat temperatures with respect to time (seasonal change) and space were added to Ts. The habitat temperatures used were averaged according to the approximated developmental time for the different stages of the main cohort (Table 1). For the eggs, the mean hourly difference between the continuously recorded Tc and Ts

was added to Ts for each hour during daytime (9:00 – 17:00 hours CET). For the larvae and pupae, respectively, the mean difference between apple temperature and Ts or between bark temperature and Ts was added to Ts for each hour during daytime. To obtain fruit and trunk temperatures, the temperature averages between the sides of fruit or trunk facing north and south were used according to the sampling period. During dawn (5:00 –9:00 hours CET),

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dusk (17:00 –21:00 hours CET), and night (21:00 –5:00 hours CET), the habitat temperatures were assumed to equal Tc. Thus, for all development stages, the mean differences between Tc and Ts were added to Ts for each hour of these respective diurnal periods.

Our calculation of the developmental time started on day 31 of the year 2002 with the accumulation of the hourly developmental rates of the pupae. The cumulated developmental rate r = 1 corresponds to the transition from one stage into the next. Adult moths do not exhibit temperature-related behaviour (longevity, fertility) in our simulation. They were assumed to oviposit after 48 h, as oviposition was highest 2 days after mating (Vickers, 1997), and mating was assumed to take place shortly after emergence. Subsequently, accumulation of egg developmental rates is initiated.

Additionally, for the comparison of dwarf and tall apple trees, the developmental time for the codling moth was calculated regarding three scenarios: (1) different air temperatures within the canopy at night, dusk, and dawn;

(2) equal air temperatures within the canopy at night; and (3) equal air temperatures within the canopy at night, dusk, and dawn. Furthermore, the developmental time was estimated using only Ts, which represents the measurements of standard weather stations.

Results

Plant architecture and potential irradiation

The parameters LAI and GSF changed in the course of the vegetation period similarly in both tree shapes. In both years, LAI increased with progressing growing season and remained at relatively constant levels from June to September (Figure 1). Apple harvest and leaf fall were followed by a

decrease in LAI that reached the lowest values in winter after the entire foliage was shed. Accordingly, GSF decreased with progressing growing season and also remained relatively constant between June and September. It increased again during apple harvest and leaf fall and reached the highest values in winter.

In both years of observation, LAI as well as GSF were significantly influenced by the tree shape (LAI: F1,60 = 97.4, P<0.001 for 2001; F1,65 = 4.64, P = 0.035 for 2002; GSF:

F1,60 = 68.3, P<0.001 for 2001; F1,65 = 5.65, P = 0.020 for 2002). From June to September, the mean LAI of dwarf trees was on average 0.78 ± 0.11 and 0.45 ± 0.10 lower than that of the tall trees in 2001 and 2002, respectively. During the same period, GSF in dwarf trees was on average 0.22 ± 0.03 and 0.13 ± 0.03 higher than that in tall trees. From April to May and from October to November, when LAI and GSF changed, the differences between dwarf and tall trees were small or even reversed. During these periods, the dwarf trees developed their foliage approximately 3 – 4 weeks earlier and lost it approximately 2 weeks later than the tall trees.

The use of hail nets in the dwarf tree orchard, on the other hand, had no significant effect on LAI (F1,40 = 0.509, P = 0.48) and on GSF (F1,40 = 0.103, P = 0.75) (Figure 2).

Height within the canopy affected LAI both in dwarf trees (F4,40 = 75.4, P<0.001 for 2001; F4,45 = 52.6, P<0.001 for 2002) and in tall apple trees (F7,30 = 9.56, P<0.001 for 2001; F7,27 = 19.2, P<0.001 for 2002). In both tree shapes, LAI increased from the treetop downwards (Figures 1 and 2). The largest increase was found in the upper 1.0 –1.5 m, whereas this increase diminished in the lower strata. Height also altered GSF within dwarf trees (F4,40 = 49.1, P<0.001 for 2001; F4,45 = 87.3, P<0.001 for 2002) as well as in tall trees (F7,30 = 4.76, P = 0.001 for 2001; F7,27 = 8.59, P<0.001 Table 1 Linear rate functions (rh – development rate per hour) used for the calculations of development time in the different Cydia pomonella stages based on relevant temperature (T)

Stage Linear rate function (h⁻¹) R² T0 (°C) Literature source

Eggs rh = 0.0004298417 T – 0.0040891868 0.92 9.5 Pitcairn et al. (1991)

Butturini et al. (1993) Howell & Neven (2000)

Larvae rh = 0.0001255468 T – 0.0011757893 0.92 9.4 Pitcairn et al. (1991)

Butturini et al. (1993) Howell & Neven (2000)

Pupae rh = 0.0001877166 T – 0.0018344374 0.86 9.8 Pitcairn et al. (1991)

Butturini et al. (1993) Howell & Neven (2000) Williams & McDonald (1982) R² – regression coefficient for linear regression.

T₀ – zero development temperature.

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for 2002). GSF decreased from the treetop downwards (Figures 1 and 2) showing the highest reduction over the upper 1.5 m in both tree shapes. Hail nets did not affect the changes of LAI and GSF with height within the canopy (hail net*height, P>0.05; Figure 2).

Air temperature within the canopy

Plant architecture significantly influenced air temperature within the canopy (Tc) during daytime on clear days, but not on cloudy days. During daytime, Tc was consistently higher in dwarf trees than in tall trees, and all codling moth stages developing with progressing season are exposed to this temperature excess (Table 2). The largest differences in temperatures were measured in the afternoon (14:00 –15:00

hours), when Tc in dwarf trees exceeded that in tall trees by average values of between 0.7 and 1.9 °C, depending on the developmental stage affected (Figure 3A). Air temperatures at dusk and at night were significantly lower in the dwarf trees than in the tall trees, and this difference ranged on average from 0.2 to 0.7 °C (Table 2). Again, this temperature deficit was evident for every single developmental stage, as calculated for the main cohort of codling moth. It was further evident for both clear and cloudy days. At dawn, Tc

was found to be lower in dwarf trees both on clear and cloudy days. This temperature difference became constantly significant for the calculated time period where adults and eggs were present in the canopy, and thereafter (Table 2).

Figure 1Mean (± SEM) of the leaf area index (LAI; A–B) and global site factor (GSF; C–D) in dwarf and tall apple trees in 2002 in different heights below the canopy top. Development stages are of the main cohort of overwintering Cydia pomonella:

L5 – overwintering larvae, A + E – adults and eggs, L1–L5 – larvae, P – pupae.

Figure 2 Mean (± SEM) of the leaf area index (LAI) and global site factor (GSF) in dwarf apple trees with hail nets (circles) and without hail nets (squares) at different heights below the treetop averaged over the 2002 season.

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Temperature of codling moth habitats251 Table 2 Differences in air temperature within the canopy (∆Tc in °C) (A) between dwarf and tall apple trees, (B) between 1 and 2 m below the top of the canopy, and (C) between dwarf apple trees with and without hail nets for the time periods corresponding to the individual development stages of the main cohort of the codling moth. The asterisks indicate significant differences in RM ANOVA (P<0.05). Approximate phenology (date, day of year) of the development stages of the main cohort of overwintered codling moths over the season (0 = overwintered generation, 1 = first generation, 2 = second generation) according to Bovey (1966)

Difference in

temperature Stage

Approximate phenology Day time (9:00 –17:00 h) Dusk (18:00 –5:00 h) Night time (21:00 –5:00 h) Dawn (6:00 – 9:00 h)

Day of year Date

Clear

∆Tc± SEM

Cloudy

∆Tc± SEM

Clear

∆Tc± SEM

Cloudy

∆Tc± SEM

Clear

∆Tc± SEM

Cloudy

∆Tc± SEM Clear

∆Tc± SEM

Cloudy

∆Tc± SEM (A) Fifth-instar larvae (0) 32–135 1 Feb−15 May 0.38 ± 0.09* 0.05 ± 0.07 −0.37 ± 0.09* −0.32 ± 0.07* −0.33 ± 0.07* −0.34 ± 0.06* −0.04 ± 0.10 −0.18 ± 0.07*

Between dwarf Pupae (0) 120 –151 30 Apr−31 May 1.15 ± 0.17* 0.27 ± 0.19 −0.66 ± 0.15* −0.44 ± 0.14* −0.68 ± 0.11* −0.54 ± 0.11* −0.10 ± 0.18 −0.10 ± 0.15 and tall trees Adults (0) + eggs (1) 140 –181 20 May−30 June 0.99 ± 0.15* 0.19 ± 0.17 −0.63 ± 0.22* −0.52 ± 0.17* −0.70 ± 0.30* −0.63 ± 0.11* −0.80 ± 0.23* −0.63 ± 0.11*

Larvae (1) 161–212 10 June−31 July 0.53 ± 0.12* −0.14 ± 0.09 −0.60 ± 0.14* −0.52 ± 0.15* −0.56 ± 0.21* −0.54 ± 0.06* −0.50 ± 0.30* −0.38 ± 0.10*

Pupae (1) 196 –220 15 July−8 Aug 0.86 ± 0.19* 0.02 ± 0.08 −0.57 ± 0.18* −0.45 ± 0.16* −0.28 ± 0.09* −0.44 ± 0.06* −0.22 ± 0.13* −0.28 ± 0.10*

Adults (1) + eggs (2) 203 –243 22 July−31 Aug 0.64 ± 0.13* 0.09 ± 0.11 −0.39 ± 0.14* −0.47 ± 0.18* −0.22 ± 0.08* −0.38 ± 0.06* −0.23 ± 0.09* −0.26 ± 0.11*

Larvae (2) 213 –304 1 Aug−31 Oct 0.55 ± 0.10* 0.06 ± 0.07 −0.47 ± 0.15* −0.48 ± 0.10* −0.32 ± 0.07* −0.36 ± 0.05* −0.30 ± 0.08* −0.22 ± 0.06*

(B) Fifth-instar larvae (0) 32–135 1 Feb−15 May −0.38 ± 0.09* −0.19 ± 0.07* −0.42 ± 0.09* −0.22 ± 0.07* −0.32 ± 0.07* −0.21 ± 0.06* −0.49 ± 0.10* −0.24 ± 0.07*

Between 2 and Pupae (0) 120 –151 30 Apr−31 May −0.66 ± 0.17* −0.29 ± 0.19 −0.69 ± 0.15* −0.30 ± 0.14* −0.22 ± 0.11 −0.18 ± 0.12 −0.63 ± 0.18* −0.29 ± 0.15 1 m below the Adults (0) + eggs (1) 140 –181 20 May−30 June −0.46 ± 0.15* −0.32 ± 0.17 −0.46 ± 0.22* −0.30 ± 0.17 −0.24 ± 0.30 −0.18 ± 0.11 −0.32 ± 0.23 −0.18 ± 0.11 canopy top Larvae (1) 161–212 10 June−31 July −0.46 ± 0.12* −0.30 ± 0.09* −0.37 ± 0.14* −0.26 ± 0.15 −0.19 ± 0.21 −0.17 ± 0.06* −0.41 ± 0.30 −0.24 ± 0.10*

Pupae (1) 196 –220 15 July−8 Aug −0.39 ± 0.19* −0.33 ± 0.08* −0.50 ± 0.18* −0.27 ± 0.16 −0.18 ± 0.09 −0.16 ± 0.06* −0.43 ± 0.13* −0.20 ± 0.10*

Adults (1) + eggs (2) 203 –243 22 July−31 Aug −0.38 ± 0.13* −0.32 ± 0.11* −0.50 ± 0.14* −0.32 ± 0.18 −0.16 ± 0.08* −0.16 ± 0.06* −0.35 ± 0.09* −0.23 ± 0.11*

Larvae (2) 213 –304 1 Aug−31 Oct −0.42 ± 0.10* −0.30 ± 0.07* −0.40 ± 0.12* −0.23 ± 0.10* −0.17 ± 0.07* −0.15 ± 0.05* −0.28 ± 0.08* −0.16 ± 0.06*

(C) Fifth-instar larvae (0) 32–135 1 Feb−15 May 0.11 ± 0.09 0.11 ± 0.09 −0.07 ± 0.07 0.02 ± 0.09 −0.10 ± 0.06 −0.01 ± 0.07 0.13 ± 0.09 0.09 ± 0.09 Between dwarf Pupae (0) 120 –151 30 Apr−31 May 0.39 ± 0.17* 0.19 ± 0.20 0.05 ± 0.17 0.00 ± 0.15 −0.01 ± 0.12 0.02 ± 0.14 0.17 ± 0.1 0.11 ± 0.1 trees with and Adults (0) + eggs (1) 140 –181 20 May−30 June 0.43 ± 0.15* 0.24 ± 0.20 −0.01 ± 0.21 0.02 ± 0.2 −0.02 ± 0.28 0.01 ± 0.14 0.26 ± 0.36 0.23 ± 0.25 without hail nets Larvae (1) 161–212 10 June−31 July 0.42 ± 0.13* 0.22 ± 0.10* 0.03 ± 0.15 0.00 ± 0.18 0.00 ± 0.22 0.01 ± 0.07 0.20 ± 0.3 0.14 ± 0.1

Pupae (1) 196 –220 15 July−8 Aug 0.42 ± 0.21* 0.15 ± 0.08 0.05 ± 0.17 0.00 ± 0.15 0.02 ± 0.09 0.02 ± 0.06 0.17 ± 0.1 0.10 ± 0.1 Adults (1) + eggs (2) 203 –243 22 July−31 Aug 0.35 ± 0.13* 0.17 ± 0.11 0.05 ± 0.13 0.02 ± 0.19 0.01 ± 0.06 0.05 ± 0.06 0.14 ± 0.07 0.11 ± 0.11 Larvae (2) 213 –304 1 Aug−31 Oct 0.25 ± 0.10* 0.15 ± 0.07* 0.04 ± 0.11 0.02 ± 0.11 0.00 ± 0.06 0.02 ± 0.04 0.09 ± 0.07 0.07 ± 0.06

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Plant architecture significantly influenced Tc measured at noon on both sunny (F1,37 = 225.4, P<0.001) and overcast days (F1,39 = 22.0, P<0.001) (Figure 4A). At noon, the mean temperature differences between dwarf and tall trees amounted to 1.0 °C on sunny and 0.4 °C on overcast days.

Hail nets significantly affected air temperature within the canopy (Tc) during daytime on clear days, but not on cloudy days. On clear days, Tc under hail nets was reduced by an average of 0.1– 0.4 °C compared to Tc in unprotected apple trees. All codling moth stages are exposed to this temperature deficit in the progressing season, except the overwintered mature larvae ( Table 2). The mean temperature

deficit in hail-protected trees compared to unprotected trees showed two peaks: in the morning (8:00 –10:00 hours) and in the afternoon (13:00 –16:00 hours) with 0.3 – 0.7 °C and 0.2– 0.8 °C, respectively (Figure 3B). At noon (12:30 hours ± 90 min), on the other hand, this temperature difference was not significant (F1,35 = 0.921, P = 0.34).

On cloudy days, the difference in Tc between the trees with and without hail nets was only significant during the development time of the main larval cohorts (Table 2).

However, air temperatures measured at noon were significantly lower by 0.2 °C in the hail-protected trees (F1,37 = 27.5, P<0.001). During dusk, night, and dawn, hail nets had no effect on air temperature.

Generally, air temperature within canopies exceeded standard air temperature (Ts) during daytime, but Tc

decreased to the level of Ts or even below it for several hours at night (one sample t-test, P<0.05). These temperature differences were larger in dwarf trees than in tall trees and more striking on clear days (cf. RM ANOVA in previous text; Figures 3 –5). At noon, Tc in dwarf trees exceeded Ts by 1.9 °C on sunny days and by 0.9 °C on cloudy days. The average difference to Ts in tall trees amounted to 0.9 °C and 0.5 °C on sunny and cloudy days, respectively.

At night, Tc in dwarf trees dropped further below Ts (on average 0.3 – 0.9 °C) than in tall trees where Tc ranged close to Ts from 0.2 °C above to 0.4 °C below it on average (cf.

RM ANOVA in previous text).

Height significantly affected air temperature within the canopy in both tree shapes during day and night for most developmental stages. Tc decreased from 1 to 2 m below the top of the canopy (Table 2). However, the measurements at noon did not reveal any changes in Tc with height, independent of weather condition (sunny days: F4,37 = 1.18, P = 0.34; overcast days: F4,39 = 0.413, P = 0.80; Figure 4A).

However, hail nets had no effect on the temperature stratification within the trees.

Surface temperature of bark

Surface temperatures of bark were significantly higher in dwarf trees than in tall trees on both sunny days (F1,69 = 61.3, P<0.001) and overcast days (F1,78 = 17.7, P<0.001).

On overcast days, the mean temperature excess amounted to 0.4 °C (Figure 4B). On sunny days, this temperature difference changed with the exposure and the progress of season. Bark temperature in dwarf trees was higher than in tall trees by an average of 1.6 °C on the shaded north- facing side and 0.3 °C on the irradiated south-facing side (Figure 4B). The largest temperature differences of bark exposed to the north between the tree shapes were recorded in March (on average 2.1 °C) and October (on average 2.6 °C), when the foliage was sparse. These bark temperature differences changed only slightly with the progressing Figure 3 Mean differences (± SEM) in air temperature within the

canopy (Tc) between (A) dwarf and tall apple trees, and (B) dwarf trees with and without hail nets at different heights for the main cohort of adults and eggs of the first – A + E(1) – and second Cydia pomonella generation – A + E(2). T_c is averaged for clear days (open circles) and for cloudy days (filled circles). The zero reference line indicates equal T_c: (A) T_c>0 indicate higher temperatures in dwarf trees, Tc<0 indicate higher temperatures in tall trees; (B) T_c>0 indicates higher temperatures in apple trees without hail nets; Tc<0 indicates higher temperatures in apple trees with hail nets.

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Temperature of codling moth habitats ²⁵³

season. The temperature differences of bark exposed to the south, on the other hand, were small in spring and autumn (0.3 °C). But the differences between the tree shapes increased to approximately 1.2 °C in summer, when foliage was fully developed. The mean differences between the north-facing and the south-facing sides were higher in tall trees (sunny days: 2.1 °C, overcast days: 0.3 °C) than in dwarf trees (sunny days: 0.8 °C, overcast days: 0.1 °C).

Hail nets did not significantly influence the surface temperature of bark at noon on sunny days (F1,70 = 0.124, P = 0.726). On overcast days, hail nets reduced bark temperature by an average of 0.2 °C (F1,74 = 82.0, P<0.001).

However, bark temperature was more affected by exposure (Figure 5A; sunny days: F1,70 = 73.2, P<0.001; overcast days: F1,74 = 14.4, P<0.001).

In general, the surface temperature of bark exceeded Ts

at noon (one-sample t-test, P<0.05). This temperature excess was higher in dwarf trees than in tall trees, particularly on sunny days and for the south-facing bark surface (cf. RM ANOVA in previous text; Figure 4B). On sunny days, the mean temperature excess of the bark facing south was 3.4 °C in dwarf trees and 3.1 °C in tall trees, and the maximum temperature excess in spring was 13.9 °C and 19.6 °C, respectively.

Height within the canopy significantly affected bark surface temperature on sunny days (F4,69 = 10.1, P<0.001).

In both tree shapes, bark temperature decreased from the treetop downwards (Figure 4B). On overcast days, height had no significant effect on bark surface temperature in both tree shapes (F4,78 = 2.4, P = 0.053).

Figure 4 Mean ± SEM of the differences between habitat temperature in apple trees at different heights and standard air temperature (2 m above ground level).

Habitat temperatures were measured at noon (± 90 min) on sunny and overcast days. The temperature differences are averaged over the season for different heights for (A) canopy air temperature (B) bark-surface temperature, and (C) apple-surface temperature in tall and dwarf trees.

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254 Kührt et al.

Surface temperature of apple fruits

The plant architecture significantly influenced the surface temperature of apple fruits on sunny days (F1,206 = 116.0, P<0.001) as well as on overcast days (F1,244 = 118.8, P<0.001;

Figure 4C). On sunny days, apples in dwarf trees had a higher surface temperature than apples in tall trees. The mean temperature excess in dwarf trees was higher on the surface exposed to the south (2.7 °C) than on the surface exposed to the north (1.8 °C). Furthermore, both surface temperatures differed more in dwarf trees (0.2–1.9 °C) than in tall trees (0 – 0.9 °C). On overcast days, the surface temperature of apples was 0.6 °C constantly lower in dwarf trees than in tall trees, whereas exposure did not have any influence either.

Hail nets did not significantly affect the surface temperature of apple fruits, neither on sunny days (F1,218 = 0.306, P = 0.58) nor on overcast days (F1,300 = 1.44, P = 0.230) (Figure 5B). However, apple temperature was influenced by the exposure on sunny days (F1,218 = 32.5, P<0.001), but not on overcast days (F1,300 = 1.21, P = 0.273).

Generally, mean surface temperature of apple fruits exceeded Ts at noon on sunny days (one-sample t-test, P<0.05). This temperature excess was higher in dwarf trees than in tall trees, particularly for the south-facing apple surface (cf. RM ANOVA in previous text; Figure 4C). Then the mean temperature excess was 3.9 °C in dwarf trees and 1.2 °C in tall trees, and the maximum temperature excess was 11.7 °C and 10.3 °C, respectively. On overcast days, however, mean temperature of apples in dwarf trees did

not differ from Ts, whereas that in tall trees exceeded Ts (cf.

RM ANOVA in previous text; Figure 4C).

Significant changes in apple temperature at noon with height were found on overcast days (F4,244 = 8.2, P<0.001).

Apple temperature decreased from the treetop downwards, and increased again slightly in the lower parts of the tall trees. On sunny days, apple temperature did not change with height (F4,206 = 0.195, P = 0.94).

Developmental rates

The comparison of the calculated developmental rates of the codling moth between dwarf and tall trees revealed different results for the three different scenarios. In scenario 1, i.e., including the differences in air temperature at night, dusk, and dawn, the calculations showed that all codling moth stages in the dwarf trees appear 2–3 days earlier than in tall trees (Figure 6, Table 3). This advantage in development arose during the pre-imaginal phase in spring and the first- generation eggs, and then remained largely constant throughout the season. In scenario 2, with equal temperatures in dwarf and tall trees at night, the advantage in development increased to 2–5 days in dwarf trees. Scenario 3, with equal temperatures at night, dusk, and dawn led to a developmental advantage of 3 – 6 days in dwarf trees (Table 3). Overall, the lower temperatures in the dwarf trees during night, dusk, and dawn decreased noticeably the developmental time of eggs and pupae, rather than of larvae.

The comparison between dwarf trees with and without hail nets revealed only minor differences in the codling

Figure 5Mean differences (± SEM) between (A) bark-surface temperature, (B) apple-surface temperature of dwarf apple trees at different heights and standard air temperature (Ts; measured 2 m above ground level). Habitat temperatures were measured at noon (± 90 min) on sunny and overcast days. The temperature differences are averaged over the season for different heights for (A) bark-surface temperature and (B) apple-surface temperature in dwarf trees without hail nets and dwarf trees with hail nets.

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Temperature of codling moth habitats ²⁵⁵

moth developmental rates. Larvae of the first generation appeared 1 day earlier in hail-protected trees indicating a slightly faster development of eggs there (Table 4). Adults of the first and eggs of the second generation, on the other hand, appeared 1 day later than in unprotected trees. This small advantage in development arose during the pupal stage of the first generation. All other stages were not affected.

Generally, the developmental rates calculated were higher when using habitat temperatures than using only standard air temperature. The individual stages theoretically appeared 7–16 days earlier in tall trees and 10 –18 days earlier in dwarf trees (Figure 6, Table 3).

Discussion

The present study shows that plant architecture significantly influences the potential irradiation within a tree canopy and consequently, the temperatures in habitats of the codling moth. Comparing the two tree shapes studied, we documented that the LAI as a parameter of plant architecture is reduced in dwarf trees. This leads to a higher GSF, i.e., the transmission of global radiation, in dwarf trees. Due to these differences in plant architecture and radiation levels, temperatures in the typical habitats of the codling moth are higher in dwarf trees than in tall trees.

Consequently, differences in the phenology of codling moth between those inhabiting traditional tall and modern dwarf trees are to be expected.

For the first time, hail nets above dwarf trees are shown to reduce the temperature in some habitats of the codling moth, depending on weather and time of day. Significant temperature differences are noted between hail-protected and unprotected dwarf trees for the air within the tree canopy (Tc), and for the bark on overcast days, but not for apple fruits. Although there are some temperature differences, the hail nets exhibited a negligible effect on the calculated developmental rates of the codling moth.

Plant architecture

The plant architecture of traditional tall apple trees and of commercial dwarf apple trees differs not only with regard to the general shape of the trees, but also with regard to the LAI and GSF. In both years of investigation, the LAI of dwarf trees was significantly lower than that of tall trees. As the leaf area reciprocally influences the transmission of global radiation, the lower LAI in dwarf trees leads to a Figure 6 Cumulated development rates

(rh) of codling moth calculated for habitat temperature conditions in dwarf and tall apple trees, and calculated with standard air temperature (measured 2 m above ground). Dotted lines (rh = 1) correspond to the transition from one stage into the next.

Table 3 Appearance dates (day of the year) of the codling moth stages calculated for tall trees and deviation from these dates (in days) in dwarf trees for three scenarios: (1) including air temperature differences to tall trees at night, dusk, and dawn, (2) with equal air temperatures at night, and (3) with equal air temperatures at night, dusk, and dawn. Deviation of appearance dates calculated with standard air temperature (Ts) from that in tall trees. (0 = overwintered generation, 1 = first generation, 2 = second generation)

Stage

Tall trees

Difference to appearance dates in tall trees in Dwarf trees

scenario 1

Dwarf trees scenario 2

Dwarf trees scenario 3 T_s

Adults (0) 140 −2 −2 −3 +16

Eggs (1) 142 −2 −2 −3 +16

Larvae (1) 162 −3 −5 −5 +7

Pupae (1) 193 −3 −4 −5 +11

Adults (1) 219 −3 −5 −6 +13

Eggs (2) 221 −3 −5 −6 +13

Larvae (2) 233 −2 −3 −4 +12

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256 Kührt et al.

higher radiation transmission (GSF). Consequently, actual radiation intensity is expected to be higher in dwarf trees than in tall trees. Similarly, Ferree (1989) found in a study on light transmission in different apple-cropping systems that slender spindle trees (height 2.3 m, spread 1.6 m) had lower LAIs and higher light levels than larger pyramid hedgerow trees (height 4.5 m, spread 4.5 m).

Regarding hail nets, hemispherical photography reveals no differences in plant architecture parameters (LAI, GSF) between dwarf trees with and without protection by hail nets. In fact, threadlike structures like hail nets disappear during processing hemispherical images for analysis.

Therefore, no significant influence of hail nets on plant architecture parameters should be noted, provided all trees are of the same variety, pruning, etc. Nevertheless, hail nets have been shown to reduce actual radiation transmission (reviewed by Mantinger, 2003).

Habitat temperature

We can show here that plant architecture significantly influences temperature in the different habitats of the codling moth. Habitat temperature differed substantially between dwarf and traditional tall trees. These temperature differences were modified by weather conditions, daytime, and height within the canopy. Radiant heating by day and radiant cooling by night are considered the main impact factors leading to temperature differences in insect habitats (Wellington, 1950). This is well supported by our data: air temperature within the canopy (Tc) during the day was higher in dwarf trees than in tall trees. High incident radiation enhanced this temperature excess, and thus, we found a higher temperature excess on clear sunny than on cloudy days. Contrary to the results during daytime, Tc

decreased at night in dwarf trees below that in tall trees.

This can be explained by the rather open structure of a dwarf-tree orchard with its parallel rows. Such a structure is likely to facilitate radiation loss and dynamics of air layers, leading to faster cooling and an increase in forced convection as well as in evaporative cooling. The wide canopies of the tall trees, on the other hand, provide better thermal insulation due to air stratification under low wind speed.

Bark temperature at noon was generally higher in dwarf trees than in tall trees. Bark temperatures of both trunk sides on overcast days, as well as temperatures of the northern side of the trunk on sunny days, were similar to the corresponding Tc, which in turn is generally higher in dwarf trees. Thus, we postulate that bark temperature follows the daily course of air temperature within the canopy, which coincides well with relationships established for tall trees (Jermy, 1964). Solar radiation warms bark exposed to the south likewise in both tree shapes, leading to only small temperature differences on sunny days. As a further con- sequence, the temperature difference between north-facing and south-facing bark is lower in dwarf trees than in tall trees. In other studies of tall trees, temperature varied considerably between southern and northern trunk sectors, particularly in winter and early spring when tree trunks were heated by incident radiation (Graf et al., 2001). Bark- surface temperatures at distinct places of the trunk in tall trees have been shown to differ by up to 12.9 °C (Jermy, 1964).

Surface temperature of apple fruits was higher in dwarf trees than in tall trees on sunny days, but lower on overcast days, at noon. Due to tree architecture, the majority of apple fruits in dwarf trees grow in the periphery where they are more exposed to radiation and radiative heat-up.

Although single apples in the periphery of tall trees could reach similar temperatures, mean apple temperatures in Table 4 Appearance dates (day of the year) of the codling moth stages calculated using habitat temperatures in dwarf trees without (unprotected) and with hail nets, and using standard air temperature (Ts). The deviation in codling moth appearance (in days) was calculated as the difference between appearance dates in unprotected trees and trees with hail nets or Ts. (0 = overwintered generation, 1 = first generation, 2 = second generation)

Stage

Dwarf trees

Ts

Difference to appearance in unprotected trees in days

Unprotected With hail nets

Dwarf trees

with hail nets Ts

Adults (0) 138 138 +18 0 +18

Eggs (1) 140 140 +18 0 +18

Larvae (1) 159 158 +10 −1 +10

Pupae (1) 190 190 +14 0 +14

Adults (1) 216 217 +16 +1 +16

Eggs (2) 218 219 +16 +1 +16

Larvae (2) 231 231 +14 0 +14

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Temperature of codling moth habitats ²⁵⁷

tall trees ranged close to Tc. The higher apple temperatures in tall trees on overcast days may be attributed to the better insulation of the air layers within the canopy under low wind speed.

Hail nets reduce the actual radiation transmission (Giulivo & Ponchia, 1978; Widmer, 1997a,b; Mantinger, 2003), thus diminishing radiant heat exchange within the trees and reducing temperature fluctuations (Giulivo &

Ponchia, 1978). Reduction in photosynthetic active radiation within apple tree canopies due to black hail nets has been reported to range between 15% and 25%, measured 1 m above ground (Widmer, 1997a,b), or even between 7% and 35% (Giulivo & Ponchia, 1978). In line with expec- tations, the measured reduction in air temperature within the canopy by hail nets in the present study was most striking on sunny days, less on overcast days, and not measurable during the night, dusk, and dawn. The larger reduction in Tc by hail nets before and after noon compared to at noon is in accordance with the findings of Widmer (1997b). This latter study showed that the reduction in solar radiation by hail nets amounts to more than 20%

in the morning and towards evening, whereas the reduction is lower at noon. These changes in direct irradiation might also be the reason for the rather small or insignifi- cant temperature differences on apple fruits and on bark measured at noon. We expect a similar variation in bark and apple temperatures during the day as observed for Tc. The effect of height on air temperatures within the canopy varied with daytime. Air temperatures decreased during the day and night with decreasing height in both tree shapes, but did not change significantly at noon. This is in contrast to results of Landsberg et al. (1973) from a 7-year- old Cox’s Orange Pippin hedgerow in which temperatures increased at noon from the top to the bottom of the trees.

We also observed a decrease in surface temperature of bark and apple fruits from the treetop downwards. This stratification in habitat temperatures corresponds to a decrease in radiation intensities from the treetop downwards observed in apple trees (Looney, 1968; Proctor et al., 1972;

Lakso, 1980).

Consequences for codling moth development

Due to the small body size of the codling moth of a few millimetres, the body temperature of all stages should be determined nearly exclusively by ectothermic influences (Heinrich, 1993). This implies that the body temperature should be equal to the operative environmental temperature, which is mainly determined by ambient temperature, possible radiative heat-up, and also evaporative cooling (Bakken & Gates, 1975; Campbell & Norman, 1998). Thus, body temperatures (Tb) of adult moths and eggs are strongly influenced by air and substrate temperature and

radiation within the canopy. Tb of feeding larvae and that of mature larvae and pupae depends on the temperature of apple fruits and on bark temperature, respectively.

Accordingly, earlier field experiments show that the first moths hibernating in the southern trunk sectors emerged 80 day degrees (standard air temperature) earlier than those in northern trunk sectors due to higher trunk temperatures (Graf et al., 2001). Differences in the developmental time of the codling moth of 50 –100% are attributed to the location within the tree (Jermy, 1964).

The results of our calculations indicate that the differences in habitat temperatures caused by plant architecture have a clear, although small effect on the development of the codling moth. Thereby, pupae and eggs appeared to be the most affected stages. Developmental rates of the feeding larvae, however, did not differ conspicuously between dwarf and tall trees. Feeding larvae, however, could be even more influenced by the difference on the southern exposed sides of the apple fruit since they show a clear preference to the warmer apple hemisphere by cryptic basking inside the apples (Kührt et al., 2005). The general temperature excess in dwarf trees enhanced the development of the codling moths by up to 6 days. However, the higher air temperatures in the tall trees at night, dusk, and dawn partially compensated this developmental advantage in dwarf trees during daytime. Again, pupae and eggs experienced the strongest effect on their development of this temperature excess in tall trees at night, dusk, and dawn.

On the other hand, our calculations for dwarf trees with and without hail nets indicated no considerable change in the developmental rates of the codling moth under hail nets. Because air temperature was affected by hail nets, egg development should have been decelerated, leading to a delayed appearance of the larvae in apple trees with hail nets. However, the calculations demonstrated that only adults of the first generation and eggs of the second generation appeared 1 day later in the hail-protected trees than in the unprotected ones. In the basic modelling of developmental rates presented here, we did not consider the effect of solar radiation on the actual body temperature of the pest insect. By changing radiative heat-up of adult moths or eggs, however, hail nets may have indeed a further influence on developmental rate. To elucidate the latter, the next step will be to investigate such influences on the development and life cycle of the codling moth per se, and also the possible effect of thermoregulatory mechanisms in the insect that may alter influences of solar radiation.

Our simulations give further evidence that appearance dates for the distinct codling moth stages differ noticeably when calculations are based on standard air temperature compared to habitat temperatures. Common forecast models exhibit, especially for the second and third generation, a

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258 Kührt et al.

time delay of about 2– 4 weeks (Shaffer & Gold, 1985;

Blago & Dickler, 1990). This deviation between simulation results and field observations is partially due to the difference between weather-station temperatures and the internal fruit and cocoon temperatures experienced by developing larvae and pupae (Shaffer & Gold, 1985; Blago

& Dickler, 1990). We show here that apple and bark temperatures differed by as much as 11–19 °C from standard air temperatures. In our calculations, this difference between standard air temperature and habitat temperatures resulted in a deviation of almost 2 weeks in the codling moth phenology. Such a high discrepancy is not tolerable in integrated management, with its need for precise timing of control measures such as application of insect-growth regulators or codling moth granulosis virus.

We conclude that changing plant architectures in apple orchards indeed have consequences for temperatures of codling moth habitats. These differences in habitat temperatures per se are not large enough to influence the number of generations per year. However, they are suf- ficiently large to be given serious consideration in prediction models. The integration of habitat temperatures in addi- tion to standard air temperature may improve the accuracy of forecasting of the pest insect considerably. Another possible influence of plant architecture on developmental rate is connected to the effect of solar radiation on the actual body temperature of the pest insect. The possible influence of radiative heat-up of adult moths or eggs was not considered in the basic modelling of developmental rates presented here. The next step will be to investigate such influences on the development and life cycle of the codling moth per se, and also the possible effect of thermoregulatory mechanisms in the insect that may alter influences of solar radiation.

Acknowledgements

Thanks are due to Kurt Rennhard and Valentin Stocker for the possibility to use their orchards and to Roland Schmucki and Marco Hinnen for assistance with field measurements. We thank Kathrin Tschudi-Rein, Anja Rott, Hainan Gu, Stephen Simpson, and two anonymous referees for valuable comments on earlier drafts of the article. Temperature data from an agricultural weather station were kindly provided by the Kantonale Zentralstelle für Obstbau Frick, Kanton Aargau, Switzerland. This study was supported by a TH research grant (ETH Zurich) to Jörg Samietz and Silvia Dorn.

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