J. Appl. Entomol. 130(6-7), 368–376 (2006) doi: 10.1111/j.1439-0418.2006.01073.x

2006 The Authors Journal compilation 2006 Blackwell Verlag, Berlin

Thermal requirements and phenology of the snout scutellatus Gyllenhal

S. Santolamazza-Carbone, A. Rodrı´guez-Illamola and A. Cordero Rivera Grupo de Ecoloxı´a Evolutiva e da Conservacio´n, Departamento de Ecoloxı´a e Bioloxı´a , Universidade de Vigo, Pontevedra, Spain

Ms. received: January 28, 2006; accepted: May 11, 2006

Abstract: Laboratory experiments and field surveys were carried out to study the thermal requirements and phenology of the Eucalyptus snout beetle () and its parasitoid, nitens (Mymaridae). Developmental times were recorded for G. scutellatus life stages: egg to first instar larva, first instar to pre-pupal larva, prepupae to adults and the complete life cycle. Experiments were performed in temperature-controlled chambers maintained at 10, 15, 20, 25 and 30C with a photoperiod of 11 : 13 h of light : darkness and 50–60% RH. To calculate the minimum threshold temperature of the parasitoid, parasitized egg capsules were kept under similar conditions. During 1998 and 1999 we studied the phenology and the day-degree (DD) accumulation of G. scutellatus and its parasitoid in plots of at six different sites in NW Spain. Every 2 weeks, the numbers of snout beetle adults and egg capsules were counted in each plot. The rate of parasitism was estimated by collecting 90 egg capsules from each plot on each sampling date. We recorded the temperatures in each plot to test whether differences in temperature alone could account for the phenology of this snout beetle. To complete a full life cycle from egg to adult, the required a mean of 1119.83 ± 20.59 DD above a base temperature of 6.11C. The parasitoid had a base temperature of 5.09C and needed 318.16 DD to complete a life cycle. Our model indicated that three generations of snout beetle could develop each year, corresponding to peaks of snout beetle numbers in the field in March–April, June–July and November. In some years only one generation of G. scutellatus was recorded due probably to the effectiveness of the parasitoid. Differences in numbers of adults and egg capsule were recorded between neighbouring Ôcoastal plotsÕ and between neighbouring Ôinland plotsÕ. Hence, climate alone does not appear to explain the phenology of G. scutellatus.

Key words: , Eucalyptus globulus, day-degree, developmental thresholds, host–parasitoid interactions, pest management

1 Introduction Eucalyptus. Both the snout beetle adults and larvae eat the leaves, buds and shoots of the Eucalyptus trees, Predicting the timing of particular stages in the life which retards tree growth and contorts and eventually cycle of pest is important in studies of their kills branches of trees that are heavily infested (Tooke, population dynamics and for forecasting pest 1955). Female snout lay their hard brown egg attacks in cultivated crops (Nylin, 2001). The devel- capsules on shoots and young leaves. The egg capsules, opment of ectotherm organisms occurs within a composed mainly of faeces, contain about eight eggs. narrow range of temperatures, and this has a profound The neonate larvae emerge after 7–10 days and the effect on all aspects of their development. Physiological pass through four instars. The first instars feed on the time (PhT) is the amount of heat required over time for surface of the leaves, whereas the later instars consume an insect to complete a full life cycle or simply to the entire leaf blade. This snout beetle and its complete one specific stage of development (Taylor, parasitoid, A. nitens, have been studied since the start 1981). A day-degree (DD) is the amount of heat that of the 20th century primarily because of a combination accumulates above a specific base temperature during of the high pest status of the snout beetle and the good each 24-h period (Baskerville and Emin, 1968). This possibility of controlling it with the above parasitoid work provides the first detailed analysis of the thermal (Marelli, 1928; Tooke, 1955; Arzone and Vidano, requirements and phenology of the Eucalyptus snout 1978; Mansilla, 1992; Cordero Rivera et al., 1999; beetle Gonipterus scutellatus Gyllenhal (Col., Curculi- Hanks et al., 2000). onidae) and one of its natural enemies, the parasitoid The Eucalyptus snout beetle was introduced accident- Anaphes nitens Girault (Hym., Mymaridae). This snout ally into Galicia, NW Spain in 1991. The egg parasitoid beetle is of Australasian origin and feeds specifically on Thermal requirements and phenology of G. scutellatus 369

A. nitens was released towards the end of 1993 as a daily. To study the developmental time and thermal require- biological agent for controlling the pest and gave ments of the parasitoid A. nitens, we used egg capsules that promising results (Mansilla and Pe´rez Otero, 1996). were both laid and parasitized under laboratory conditions. However, following the initial success, control became Over the range of temperatures that are suitable for variable due to periodic fluctuations in the populations development, the relationship between the rate of develop- ment of a given insect and temperature is approximately of both the pest and its parasitoid (Santolamazza linear (Campbell et al., 1974). To estimate PhT, one of the Carbone 2002). Despite the economic importance of important parameters is the determination of the minimum this snout beetle, little information is currently available threshold temperature (MTT), the temperature above which on the thermal requirements and phenology of either development can start. The MTT is usually obtained by G. scutellatus or A. nitens in the field. Depending upon plotting the rate of development against temperature. The the country chosen and its climate, this weevil may either point where the projected line intersects the horizontal be restricted to one generation per year or breed temperature axis is taken as the MTT. PhT measured in continuously (Clark, 1931; Moutia and Vinson, 1945; DD can be calculated using the equation:

Tooke, 1955; Arzone and Meotto, 1978; Mansilla and PhT ¼ tðTm MTTÞ; Pe´rez Otero, 1996). In an earlier study in NW Spain we recorded only one generation of snout beetles in 1996 where t is the development time in days and Tm is the mean and three in 1997, as in 1996 the parasitoid gave almost treatment temperature. To record the time required for egg development of 100% control and this resulted in a local extinction of G. scutellatus, 50 fresh egg capsules (mean egg capsule the pest (Cordero Rivera et al., 1999). However, this size ¼ 8.14 ± 0.09 eggs) were placed individually into plastic, conclusion was based on data collected from only one 10 cm diameter, Petri dishes. Ten Petri dishes of eggs were then plot and so needs to be verified by collecting a more placed into each of five temperature-controlled chambers robust set of data. maintained at 10, 15, 20, 25 and 30C, and having a Knowledge of developmental times and phenology photoperiod of 11 : 13 h of light : darkness and 50–60% of pest insects in the field should enable to predict the RH. The egg capsules were checked daily and any larvae that timings of pest insect attacks and so improve pest had hatched were transferred to plastic boxes before being control (Gimeno Sevilla and Perdiguer Brun, 1993; returned to their respective chambers. To obtain a more precise Thomas, 1997; Milonas et al., 2001; Lobinske et al., estimate of the temperatures within the experimental cham- 2002). bers, each chamber contained a data logger that recorded the temperature every hour. Each day the larvae were provided We tested whether data from laboratory experiments with fresh leaves of E. globulus as food. However, the leaves and field samples could be used to construct a DD soon dried out in the 30C chamber and so the leaves were model that would help make more efficient the current renewed twice daily in this treatment. Despite the additional Integrated Pest Management (IPM) programme in the food, larval mortality was high at 30C and few individuals NW Spain (Santolamazza Carbone and Ferna´ndez de survived the treatment. The smaller larvae, instars 1–3, were Ana Maga´n, 2004). kept in 10 · 15 cm plastic boxes in groups of up to 10 Our aims in this study were to: (i) estimate the individuals. When larvae reached the fourth instar (pre-pupal developmental thresholds and DD requirements of stage) they were transferred to larger, 1 l boxes that contained the snout beetle and its natural enemy, (ii) study the 10 cm of sterile soil to allow the prepupae to burrow into the phenology of the two insects in six field plots over a soil prior to pupation. The date each prepupa started to burrow was recorded, and we then assumed that the first to 2-year period, and (iii) test the accuracy of a DD model burrow corresponded to the first adult to emerge from the soil. for predicting the phenology of G. scutellatus. In this way we recorded the duration of development of each Our hypothesis is that if the phenology of G. scu- individual. We also recorded the mean date of burrowing and tellatus is controlled mainly by temperature, then the the mean date of emergence at each temperature and used the phenology of this insect should be similar in localities difference as the estimate of mean development time. As both with similar climates. In contrast, if the biological methods gave similar values, only the second estimate is control agent proved to be the key mortality factor, presented in this study. then we might find differences in the phenology of the To study the thermal requirements of the parasitoid, 50 pest even between ÔneighbouringÕ populations. parasitized egg capsules were placed into 10 cm diameter plastic Petri dishes. Adults emerged from parasitized egg capsules that had been collected in the field and brought to the laboratory. To obtain parasitized egg capsules of known age, 10 fresh egg capsules were placed into a 10-cm diameter 2 Materials and Methods glass Petri dish, and then five 1-day-old parasitoids were 2.1 Developmental time introduced for 24 h. The parasitized egg capsules were then exposed to the five We recorded the time required for development for the different temperatures used for the snout beetle stages (10 egg various stages in the life cycle of G. scutellatus. The stages capsules per temperature) and were checked daily to record recorded were: (i) egg to first instar larva; (ii) first to fourth any emergence of parasitoids. instar larva (pre-pupal stage ready to burrow into the soil prior to pupation); and (iii) pre-pupae stating to burrow into the soil to eventual emergence of the snout beetle adults (see 2.2 Phenology Tooke, 1955, for details of the life cycle). Snout beetle adults We monitored six permanent plots of E. globulus in Galicia were collected from the field and kept in 5 l plastic boxes in (NW Spain, see fig. 1). In January 1998, ten 2–3 m high trees the laboratory. The beetles were provided with leaves of were selected, at random, in each of the six localities. The Eucalyptus globulus, which provided both food and oviposi- selected trees were marked and inspected every 15 days tion sites. This enabled fresh egg capsules could be collected

2006 The Authors Journal compilation 2006 Blackwell Verlag, Berlin, J. Appl. Entomol. 130(6-7), 368–376 (2006) 370 S. Santolamazza-Carbone, A. Rodrı´guez-Illamola and A. Cordero Rivera

Folgoso Cotobade

Tomba Bora Lourizán

Cotorredondo

Fig. 1. Sample site location in NW Spain of the six plots of Eucalyptus globulus sampled for infestations of Gonipterus scutellatus during a 2-year period of the survey. Snout beetle adults are specifically temperature, could explain the phenology of the highly mobile and rather cryptic, and therefore are difficult to snout beetle. In the first analysis we looked for differences sample accurately. Nevertheless, we tried to minimize this between plots, with month and year (nested) treated as sampling problem by examining all of the branches on the random factors, and plots treated as fixed factors. Differences selected trees. We also collected and counted all the egg between plots could be due either to climate and/or other capsules to determine whether oviposition was continuous variables. A second anova compared egg abundance between throughout the year or whether there was a reproductive plots with similar climates, again with month and year (nested) diapause, as in other beetles (Nahrung and Allen, 2004). as random variables. Differences would indicate that factors Parasitism rate was recorded by keeping up to 90 capsules, other than climate were affecting the life cycle of the snout collected from each plot on each sampling date, in the beetle. Statistical analyses were performed using Genstat 8.0. laboratory (see Cordero Rivera et al., 1999 and Santolam- To calculate the numbers of accumulated DD, the data azza Carbone and Cordero Rivera, 2003 for details). The rate were entered into the UC IPM Degree-day Calculator (http:// of parasitism was assumed to reflect parasitoid density www.ipm.ucdavis.edu/WEATHER/ddretrieve.html), select- (Cronin and Strong, 1993), and was measured because ing the modified double sine method and an intermediate parasitism was considered to have an important effect on cut-off, using 30C as the upper temperature threshold. snout beetle phenology. Distances between plots ranged from 3.3 to 32.4 km. The plot at Louriza´n was monitored from 1996 to 1999. Although the data for 1996 and 1997 have been published elsewhere 3 Results (Cordero Rivera et al., 1999), they have been included here to 3.1 Physiological time extend the time series. In 1999, and also in 1998 at Louriza´n, the air temperatures in each plot were recorded hourly using The MTT and the number of DD required to complete electronic data loggers (TinyTalk Gemini Data Logger, the different phases in the life cycle of G. scutellatus are Gemini Data Loggers Ltd., Chichester, West Sussex, UK). shown in table 2. As expected, there was a direct The complete weather data for 1998 were obtained from the relationship between temperature and rate of develop- National Institute of Meteorology (Ministry of Environment, ment in all parts of the life cycle. The regression Spain). These data were used in conjunction with our 2 measurements, to estimate the accumulation of DD. The equations for each phase of development had R values 1999 measurements were used to characterize each plot of 0.94–0.99 (data not shown), indicating that the (table 1). An anova, using egg capsule abundance as the overall variance was low. Figure 2 shows this relation- dependent variable, was used to test whether climate alone, ship for the complete life cycle of the snout beetle. To

Table 1. The locations and characteristics of the six sites sampled for Gonipterus scutellatus in 1999. The UTM (Universal Transverse Mercator) coordinates were obtained from the European 1950 datum and the monthly average temperatures from automatic data loggers

Locality x-UTM y-UTM Altitude (m) Dist. sea (km) Aspect Jan. Feb. Mar. Apr. May Jun. Jul. Aug. Sep. Oct. Nov. Dec.

Louriza´n 528 000 4 696 200 20 0.7 North 8.5 8.2 10.6 12.2 14.8 17.3 20.0 19.2 17.1 13.9 9.8 8.6 Bora 534 800 4 698 700 100 8.0 South 9.3 8.2 10.9 12.5 15.4 17.9 20.8 19.5 17.4 14.2 9.7 8.3 Tomba 528 000 4 699 300 200 2.5 South 9.4 9.2 11.2 12.4 15.1 17.4 20.6 19.6 17.6 14.5 10.6 9.0 Cotobade 538 000 4 705 600 280 13.8 North 8.6 8.4 10.4 12.2 14.8 – 20.1 – 17.1 14.3 10.8 9.7 Cotorredondo 527 800 4 690 300 350 4.7 Level 7.9 7.8 10.0 11.1 14.0 16.2 19.5 17.8 16.1 13.2 10.9 9.0 Folgoso 553 200 4 710 300 400 29.0 Level 6.4 6.2 8.2 9.5 12.7 15.1 18.7 17.1 15.0 11.8 7.5 6.5

2006 The Authors Journal compilation 2006 Blackwell Verlag, Berlin, J. Appl. Entomol. 130(6-7), 368–376 (2006) Thermal requirements and phenology of G. scutellatus 371

Table 2. Developmental time (DT) in days, physiolo- 1119 ± 83 DD above a base temperature of 6.11C, gical time (PhT) in degree-days (DD) and minimum whereas the PhT needed from the prepupa burrowing threshold temperature (MTT) for Gonipterus scutell- into the soil to subsequent emergence of the snout atus and Anaphes nitens recorded at five to six mean beetle adults was about 643 DD. temperatures The parasitoid had a base temperature of 5.1C (fig. 2) and required about 318.16 DD to complete its Mean temperature MTT PhT development and emerge from the eggs of the snout Phase n (C) DT (C) (DD) beetle (table 2). At the two extreme temperatures (10 G. scutellatus 10.51 255.95 6.11 1125.02 and 30C), larval development took 63.2 and 13 days Egg to adult 15.48 123.46 1156.33 respectively. However, due to the high mortality at 30C 20.05 75.55 1052.78 (actually 28.7C), only two adult parasitoids emerged. 25.09 61.44 1166.44 26.76 53.21 1098.59 Egg to larva 110 10.61 ± 0.54 38.42 6.47 158.87 3.2 Phenology 124 15.53 ± 0.29 13.79 124.91 157 19.98 ± 0.31 8.39 113.31 Figures 3 and 4 show the numbers of adults and egg 213 26.00 ± 3.09 7.08 132.26 capsules of G. scutellatus recorded in the six test plots 174 25.15 ± 2.49 6.44 125.79 together with the rate of parasitism. Throughout the 30 31.56 ± 1.03 5.16 129.41 sampling, which involved taking 45 samples/plot Larva to pupation 18 10.69 ± 0.50 83.39 5.04 471.37 12 15.62 ± 0.44 45.00 476.16 during the 2-year study, a mean of 6.43 ± 1.67 egg 14 19.84 ± 0.29 27.71 410.00 capsules was recorded per tree, but there were consid- 17 24.68 ± 2.26 22.12 434.45 erable differences between plots. Table 3 shows that 28 24.15 ± 0.90 19.29 368.58 the numbers of weevil egg capsules and the levels of 6 31.73 ± 2.05 17.00 453.67 parasitism changed markedly between years even in the Pupation to adult 7 10.24 ± 0.70 134.14 5.19 677.72 emergence 3 15.32 ± 0.34 64.67 655.23 same plot. Table 1 shows that Folgoso was the coldest 16 20.22 ± 0.65 39.44 592.99 site, followed by Cotorredondo, which, although near 11 25.19 ± 2.67 32.25 645.14 the coast, was situated 350 m a.s.l. The remaining four 7 28.58 ± 2.43 27.48 642.74 sites had similar monthly temperatures. Given their A. nitens 20 10.40 ± 0.74 63.16 5.09 334.83 Egg to adult 9 15.64 ± 0.45 32.65 344.50 geographical situation and temperatures, we predicted 42 20.08 ± 0.27 17.19 257.62 that the four ÔcoastalÕ plots, sited at Louriza´n, Bora, 4 25.53 ± 2.46 17.00 347.47 Tomba and Cotobade, should show similar phenolog- 2 28.66 ± 2.29 13.00 306.39 ical patterns. The two ÔinlandÕ plots at Cotorredondo n ¼ sample size (not given for total development due to variable and Folgoso were in colder areas, and so the phenol- sample size). Standard errors are not given, because mean values ogy of the snout beetle at these sites was expected to be are calculated by using the mean of differences between the mean different from that in the ÔcoastalÕ plots. Results of the dates. anova showed that the phenologies recorded at the coastal and the inland plots were only just different develop from egg to adult the snout beetle needs (F1,246 ¼ 3.69, P ¼ 0.056). Nevertheless, when the 256 days at 10.5C, but only 53 days at 26.8C. This analysis was restricted solely to the coastal plots, inverse relationship between developmental time and differences were detected among the four coastal plots temperature occurred through all stages of the life (F3,154 ¼ 5.95, P < 0.001). In addition, the number of cycle. The regression between the rate of development egg capsules recorded at the two inland plots also and temperature (fig. 2) indicated that G. scutellatus differed (F1,66 ¼ 4.55, P ¼ 0.037). Such differences are has a minimum temperature threshold between 5.0 and unlikely to be due solely to differences in climate. 6.5C, depending upon which stage in the life cycle was Tables 4 and 5 summarize the accumulated numbers being studied. Development from egg to adult required of DD calculated for each plot at the end of each

0.09

G. scutellatus y = 0.0032x - 0.0161 2 0.08 A. nitens R = 0.9352

0.07

0.06

0.05 T (days-1) 0.04 1/ Fig. 2. Rates of insect deve- 0.03 y = 0.0009x - 0.0054 lopment under laboratory MTT = 6.11ºC 2 R = 0.9929 conditions plotted against 0.02 MTT = 5.09ºC temperature to determine the minimum threshold tempera- 0.01 tures (MTT) for Gonipte- 0.00 rus scutellatus and its 0 5 10 15 20 25 30 35 parasitoid, Anaphes nitens Temperature (ºC) 2006 The Authors Journal compilation 2006 Blackwell Verlag, Berlin, J. Appl. Entomol. 130(6-7), 368–376 (2006) 372 S. Santolamazza-Carbone, A. Rodrı´guez-Illamola and A. Cordero Rivera

20 1 20 1 Lourizán, 1996 Lourizán, 1997 Egg capsules 0.9 0.9 Adults 0.8 0.8 15 15 0.7 0.7 0.6 0.6 10 0.5 10 0.5 0.4 0.4

0.3 rate Parasitism 0.3 rate Parasitism 5 5

Abundance (number/tree) Abundance 0.2

Abundance (number/tree) Abundance 0.2 0.1 0.1 0 0 0 0 fire 6-2-97 8-3-97 7-4-97 7-5-97 26-2-97 28-3-97 27-4-97 20-5-97 10-6-97 29-6-97 11-7-97 30-7-97 10-8-97 21-8-97 31-8-97 21-9-97 1-10-97 4-12-97 3-4-96 9-4-96 9-5-96 1-6-96 2-7-96 26-1-97 15-2-97 18-3-97 17-4-97 19-6-97 20-7-97 13-10-97 26-10-97 12-11-97 25-11-97 14-12-97 26-12-97 17-3-96 18-4-96 27-4-96 21-5-96 12-6-96 21-6-96 11-7-96 19-7-96 31-7-96 11-8-96 27-8-96 12-9-96 22-9-96 9-10-96 1-11-96 17-11-96

20 1 20 1 Lourizán, 1998 Lourizán, 1999 0.9 0.9 0.8 0.8 15 15 0.7 0.7 0.6 0.6 10 0.5 10 0.5 0.4 0.4 Parasitism rate Parasitism 0.3 0.3 rate Parasitism 5 5 Abundance (number/tree) Abundance 0.2 (number/tree) Abundance 0.2 0.1 0.1 0 0 0 0 5-8-98 8-5-99 5-6-99 5-7-99 3-9-99 9-1-98 5-2-98 1-3-98 8-4-98 3-5-98 11-1-99 28-1-99 13-2-99 27-2-99 28-3-99 24-4-99 22-5-99 19-6-99 19-7-99 25-9-99 3-11-99 4-12-99 13-6-98 10-7-98 24-7-98 20-8-98 15-9-98 3-10-98 4-11-98 5-12-98 13-3-99 10-4-99 9-10-99 22-1-98 18-2-98 12-3-98 26-3-98 22-4-98 16-5-98 30-5-98 27-6-98 17-11-99 18-12-99 20-10-98 21-11-98 17-12-98

Fig. 3. Abundance of Gonipterus scutellatus adults and egg masses (bars) recorded at Louriza´n from 1996 to 1999, and the rate of parasitism by Anaphes nitens (solid line). The snout beetle had only one generation in 1996 and 1999, but a variable number in 1997 and 1998

Table 3. Mean ± SE of Egg abundance Parasitism rate Gonipterus scutellatus and Locality 1998 (n ¼ 25) 1999 (n ¼ 20) 1998 (n) 1999 (n) the parasitism levels by Anaphes nitens recorded at Louriza´n 3.05 ± 0.70 1.29 ± 0.49 0.77 ± 0.06 (17) 0.76 ± 0.07 (7) Bora 6.04 ± 1.62 4.79 ± 1.50 0.60 ± 0.10 (17) 0.76 ± 0.07 (14) the six sites studied in NW Tomba 10.12 ± 2.37 2.28 ± 0.72 0.56 ± 0.08 (19) 0.61 ± 0.10 (13) Spain during 1998 and 1999 Cotobade 5.59 ± 1.17 9.97 ± 2.51 0.62 ± 0.06 (24) 0.65 ± 0.07 (20) Cotorredondo 7.39 ± 2.18 0.89 ± 0.23 0.62 ± 0.08 (22) 0.72 ± 0.07 (14) Folgoso 3.73 ± 0.91 22.66 ± 7.72 0.28 ± 0.08 (17) 0.43 ± 0.13 (14) Total 5.99 ± 0.68 (150) 6.98 ± 1.53 (120) 0.56 ± 0.03 (116) 0.65 ± 0.04 (82) month. Our model predicts three generations of snout In 1997, the only year when three generations beetle per year: the first after 643 DD from the start of occurred, the model produced a good forecast of the the year, the second after 1119 DD and the third after actual phenology of the snout beetle. The accuracy of a further 1119 DD. The peaks of snout beetle numbers the model was better for Louriza´n than for the other varied from 1 to 3 at Louriza´n, the only plot studied five sites, in which the second generation was separated during the entire 4 years of this research programme. from the first generation by only 600 DD.

Table 4. Day-degrees (DD) accumulated each month at Louriza´n, from January 1996 to December 1999. The maximum and minimum daily temperatures at each site were recorded hourly using a data logger. Numbers in bold indicate peaks of adults and egg capsules of Gonipterus scutellatus. Our model predicts a first generation (from pupae that overwintered) after an accumulation of 612 DD, a second generation after 1120 DD and a third gen- eration after an additional accumulation of 1120 DD

Jan. Feb. Mar. Apr. May Jun. Jul. Aug. Sep. Oct. Nov. Dec.

1996 141.92 241.33 418.24 636.67 900.99 1328.56 1774.81 2194.19 2525.71 2799.80 2962.88 3098.53 1997 119.95 270.93 533.25 835.09 1123.45 1438.97 1893.19 2329.88 2727.08 3078.64 3289.16 3438.86 1998 153.86 322.28 544.40 699.81 1005.65 1353.98 1789.22 2274.48 2634.78 2898.61 3066.89 3185.81 1999 132.71 250.05 439.48 657.59 953.80 1322.80 1778.31 2207.50 2564.81 2858.94 3013.67 3131.29

2006 The Authors Journal compilation 2006 Blackwell Verlag, Berlin, J. Appl. Entomol. 130(6-7), 368–376 (2006) Thermal requirements and phenology of G. scutellatus 373

Table 5. Day-degrees accumulated each month at the six sites monitored during 1998 and 1999. The air temper- atures were obtained from the National Institute of Meteorology (Ministry of Environment, Spain). The data for the sites at Bora, Cotobade and Cotorredondo were obtained from the same meteorological station. Numbers in bold indicate peaks of adults and egg capsules of Gonipterus scutellatus

Jan. Feb. Mar. Apr. May Jun. Jul. Aug. Sep. Oct. Nov. Dec.

1998 Folgoso 60.16 182.16 330.24 385.03 596.07 863.33 1220.37 1724.68 2051.46 2232.07 2326.95 2383.24 Tomba 109.31 292.47 541.34 655.83 909.48 1221.66 1627.27 2120.45 2459.80 2709.56 2873.26 2979.16 Bora 99.46 219.72 388.13 490.69 715.29 986.10 1350.85 1789.41 2087.65 2269.78 2437.01 2512.25 Cotobade 99.46 219.72 388.13 490.69 715.29 986.10 1350.85 1789.41 2087.65 2269.78 2437.01 2512.25 Cotorredondo 99.46 219.72 388.13 490.69 715.29 986.10 1350.85 1789.41 2087.65 2269.78 2437.01 2512.25 1999 Folgoso 49.44 106.49 200.83 318.91 509.59 800.22 1184.08 1519.42 1774.36 1946.30 2016.58 2061.34 Tomba 122.89 239.31 434.69 637.31 912.15 1252.68 1684.62 2073.08 2417.91 2683.43 2836.27 2928.91 Bora 49.92 125.30 251.20 407.03 649.38 953.47 1358.82 1707.56 2003.63 2220.34 2301.09 2457.91 Cotobade 49.92 125.30 251.20 407.03 649.38 953.47 1358.82 1707.56 2003.63 2220.34 2301.09 2457.91 Cotorredondo 49.92 125.30 251.20 407.03 649.38 953.47 1358.82 1707.56 2003.63 2220.34 2301.09 2457.91

4 Discussion development stages of the pest insect could help improve the efficacy of the chemicals applied. A good 4.1 Phenology model example in which control decisions are based on the As is usual for ectothermic , our results confirm use of DD models is in the control in Tasmania of the the existence of a linear relationship between the rate of chrysomelid beetle C. agricola (Nahrung et al., 2004), development of the snout beetle and temperature over another pest of Eucalyptus trees. temperatures ranging from 10 to 30C. The eggs of The climate of NW Spain is characterized by humid G. scutellatus failed to develop at temperatures below and mild winters (8–10C) and relatively warm 6.5C, which indicates that they are more tolerant to summers (20–25C) (Carballeira et al., 1983). These cold temperatures than the eggs of several other beetles, conditions are similar to SE Australia, where this snout such as the Hylobius transversovittatus (9.5C beetle is considered to originate, and where it achieves MTT) (McAvoy and Kok, 1999) and Euhrychiopsis one spring and one summer generation (Tooke, 1955). lecontei (9.8C MTT) (Mazzei et al., 1999), the chrys- In Italy, G. scutellatus has two generations per year: omelid Chrysophtharta agricola (8 ± 0.41C MTT) the first generation (hibernating adults) lay eggs in (Nahrung et al., 2004), and the coccinellid Scymnus February–May and the second generation in July– levaillanti (11.7C MTT) (Uygun and Atlihan, 2000). In October (Arzone and Meotto, 1978). Our results from addition, the DD required to complete the cycle from NW Spain show that G. scutellatus completed one to egg to adult was surprisingly high at 1119.83 DD: and three generations during the 4 years of the current almost twice as high as those reported for other beetles research project. In certain years, particularly in 1999, (Mazzei et al., 1999; McAvoy and Kok, 1999; Stathas, a lack of synchronization was recorded in the phenol- 2000; Uygun and Atlihan, 2000; Nahrung et al., 2004). ogy of the snout beetle from sites (e.g. Cotorredondo Nevertheless, the DD needed to complete one life cycle and Folgoso) separated by only a few kilometres, would enable three generations of the snout beetle to suggesting that differences in climate are unlikely to develop per year, as recorded on one occasion in the explain these differences. Furthermore, there were field. The time for larvae of the parasitoid A. nitens to considerable differences in snout beetle numbers develop at different temperatures were similar to the between the four coastal plots (table 3). The accumu- values published earlier for the closely related Anaphes lated temperature model predicts three generations of flavipes (Anderson and Paschke, 1969). The number of snout beetle per year and would appear to be useful for DD required to complete the life cycle indicates that the forecasting the overall pattern of beetle numbers, parasitoid could pass potentially through 10 generations although generation time in the field is expected to and hence be present throughout the year. Therefore, be somewhat longer or shorter because of differences with its high rate of host searching and its good host from the controlled conditions of the laboratory discrimination ability (Santolamazza Carbone et al., chambers and the circumstances in the plant canopy. 2004), the potential for this parasitoid to control the pest The first weevils appeared in most of the field plots is high. between March and April (after approximately 500– 600 DD) and probably represented those insects that had overwintered as pupae in the soil. Sometimes, a 4.2 Can we predict snout beetle phenology using second peak occurred in June–July separated from the accumulated temperature models? first peak by approximately 650 DD, and a third in Sampling insects in the field is time consuming. Hence, November, separated from the second peak by models, based on air temperatures, that are capable of 1400 DD. One cause of disparity between the predic- predicting snout beetle activity, would be greatly tions from the DD model and the actual development appreciated by pest managers. This is especially true of the snout beetle in the field, especially for mobile in systems of IPM, where the prediction of certain herbivorous insects, is what has been described as the

2006 The Authors Journal compilation 2006 Blackwell Verlag, Berlin, J. Appl. Entomol. 130(6-7), 368–376 (2006) 374 S. Santolamazza-Carbone, A. Rodrı´guez-Illamola and A. Cordero Rivera

50 1 120 1 Folgoso, 1998 Egg capsules Folgoso, 1999 0.9 0.9 Adults 100 40 0.8 0.8 0.7 0.7 80 30 0.6 0.6 0.5 60 0.5 20 0.4 0.4 40 Parasitism rate Parasitism 0.3 0.3 rate Parasitism Abundance (number/tree) Abundance Abundance (number/tree) Abundance 10 0.2 0.2 20 0.1 0.1 0 0 0 0 8-5-99 5-6-99 6-7-99 3-9-99 8-1-98 5-2-98 1-3-98 8-4-98 3-5-98 5-8-98 21-1-98 18-2-98 13-3-98 25-3-98 22-4-98 16-5-98 30-5-98 14-6-98 28-6-98 10-7-98 23-7-98 20-8-98 15-9-98 3-10-98 5-11-98 5-12-98 11-1-99 28-1-99 13-2-99 27-2-99 13-3-99 28-3-99 10-4-99 24-4-99 23-5-99 19-6-99 19-7-99 25-9-99 9-10-99 3-11-99 4-12-99 18-11-99 18-12-99 20-10-98 21-11-98 17-12-98

50 1 50 1 Bora, 1998 Bora, 1999 0.9 0.9 40 0.8 40 0.8 0.7 0.7 30 0.6 30 0.6 0.5 0.5 20 0.4 20 0.4 Parasitism rate Parasitism 0.3 rate Parasitism 0.3 Abundance (number/tree) Abundance

Abundance (number/tree) Abundance 10 0.2 10 0.2 0.1 0.1 0 0 0 0 9-1-98 5-2-98 1-3-98 8-4-98 3-5-98 5-8-98 8-5-99 5-6-99 6-7-99 4-9-99 21-1-98 18-2-98 13-3-98 25-3-98 22-4-98 16-5-98 30-5-98 13-6-98 27-6-98 10-7-98 23-7-98 20-8-98 15-9-98 3-10-98 5-11-98 5-12-98 11-1-99 28-1-99 13-2-99 27-2-99 13-3-99 28-3-99 10-4-99 24-4-99 22-5-99 19-6-99 19-7-99 25-9-99 9-10-99 3-11-99 4-12-99 20-10-98 21-11-98 17-12-98 17-11-99 18-12-99

50 1 50 1 Cotobade, 1999 Cotobade, 1998 0.9 0.9 40 0.8 40 0.8 0.7 0.7 30 0.6 30 0.6 0.5 0.5 20 0.4 20 0.4 Parasitism rate Parasitism

Parasitism rate Parasitism 0.3 0.3

Abundance (number/tree) Abundance 10 0.2 0.2 Abundance (number/tree) Abundance 10 0.1 0.1 0 0 0 0 8-5-99 5-6-99 6-7-99 4-9-99 11-1-99 28-1-99 13-2-99 27-2-99 13-3-99 28-3-99 10-4-99 24-4-99 25-5-99 19-6-99 19-7-99 25-9-99 9-10-99 3-11-99 4-12-99 9-1-98 5-2-98 1-3-98 8-4-98 3-5-98 5-8-98 17-11-99 18-12-99 21-1-98 18-2-98 13-3-98 25-3-98 22-4-98 16-5-98 30-5-98 13-6-98 27-6-98 10-7-98 23-7-98 20-8-98 15-9-98 3-10-98 5-11-98 5-12-98 20-10-98 21-11-98 17-12-98 Fig. 4. Abundance of Gonipterus scutellatus adults and egg masses (bars) and the respective rate of parasitism (solid line) recorded at Tomba, Bora, Cotobade, Cotorredondo and Folgoso during 1998 and 1999. The vertical scale on the Folgoso 1999 graph differs from the rest, to allow for the large numbers of egg capsules recorded at this site

Rate Summation Effect (Worner, 1992). This indicates lowering of the local snout beetle populations in some that under natural conditions the development of localities, to levels below which the snout beetle could insects is faster at low temperatures and slower at high not be detected, was due to the effect of parasitism by temperatures than would be predicted from laboratory A. nitens. This conclusion was based on the different studies. For example, basking in the sun allows insects phonologies we recorded for the weevils sampled from to increase significantly their own body temperatures plots that had similar climates (table 1). in relation to the ambient air temperature (Casey, We conclude that the introduction of the parasitoid 1981), and this could help account for discrepancies in A. nitens makes it difficult on some occasions to use the the DD estimates. Basking has been observed in DD model to forecast accurately the presence of G. scutellatus, which usually prefer to rest in sunny G. scutellatus in the field. We consider the model to be plots of Eucalyptus (Santolamazza Carbone S., pers. only a first step that will be improved by future studies obs.). on the longevity and fecundity of the snout beetle and Ecological theory indicates that the numbers of pest the parasitoid at different temperatures, and on the insects can be reduced by the action of parasitoids and preoviposition behaviour of the snout beetle. This that this results subsequently in the reduction of the should help us to construct a physiologically based parasitoid population due to a lack of suitable host model capable of separating the effects of the weather insects (Begon et al., 1996). We suggest that the from those of the parasitoid.

2006 The Authors Journal compilation 2006 Blackwell Verlag, Berlin, J. Appl. Entomol. 130(6-7), 368–376 (2006) Thermal requirements and phenology of G. scutellatus 375

50 1 50 1 Cotorredondo, 1998 Cotorredondo, 1999 0.9 0.9 40 0.8 40 0.8 0.7 0.7 30 0.6 30 0.6 0.5 0.5 20 0.4 20 0.4 Parasitism rate Parasitism 0.3 0.3 rate Parasitism Abundance (number/tree) Abundance 10 0.2 (number/tree) Abundance 10 0.2 0.1 0.1 0 0 0 0 5-2-98 1-3-98 8-4-98 3-5-98 5-8-98 8-5-99 5-6-99 5-7-99 4-9-99 10-1-98 21-1-98 18-2-98 13-3-98 26-3-98 22-4-98 16-5-98 30-5-98 13-6-98 27-6-98 10-7-98 24-7-98 20-8-98 15-9-98 3-10-98 4-11-98 5-12-98 11-1-99 28-1-99 13-2-99 27-2-99 13-3-99 28-3-99 10-4-99 24-4-99 22-5-99 19-6-99 19-7-99 25-9-99 9-10-99 3-11-99 4-12-99 20-10-98 21-11-98 17-12-98 17-11-99 18-12-99

50 1 50 1 Tomba, 1998 Tomba, 1999 0.9 0.9 40 0.8 40 0.8 0.7 0.7 30 0.6 30 0.6 0.5 0.5 20 0.4 20 0.4 Parasitism rate Parasitism 0.3 rate Parasitism 0.3 Abundance (number/tree) Abundance

10 0.2 (number/tree) Abundance 10 0.2 0.1 0.1 0 0 0 0 5-2-98 1-3-98 8-4-98 3-5-98 5-8-98 8-5-99 5-6-99 5-7-99 4-9-99 10-1-98 22-1-98 18-2-98 12-3-98 26-3-98 22-4-98 16-5-98 30-5-98 13-6-98 27-6-98 10-7-98 24-7-98 20-8-98 15-9-98 3-10-98 4-11-98 5-12-98 11-1-99 28-1-99 13-2-99 28-2-99 13-3-99 28-3-99 10-4-99 24-4-99 23-5-99 19-6-99 19-7-99 25-9-99 9-10-99 4-11-99 5-12-99 20-10-98 21-11-98 17-12-98 17-11-99 18-12-99

Fig. 4. Continued

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