Winter mortality in sub-corticolous populations of Ips typographus (Coleoptera, Scolytidae) and its parasitoids in the south-eastern Alps

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1 62 M. Faccoli: Winter mortality of Ips typographus and its parasitoids Anz. SchaÈdlingskunde / J. Pest Science 75, 62±68 ã 2002, Blackwell Verlag, Berlin ISSN Department of Environmental Agronomy and Crop Production ± Entomology, University of Padua, Italy Winter mortality in sub-corticolous populations of Ips typographus (Coleoptera, Scolytidae) and its parasitoids in the south-eastern Alps By M. Faccoli Abstract A study concerning the winter mortality of a sub-corticolous population of Ips typographus and its parasitoids has been carried out in the south-eastern Alps (Italy) during the winter 1997/98. Three attacked spruce trees were sampled three times (November, February and April) by collecting infested bark disks (1 dm 2 each). All insects that emerged from the bark or died in the samples before emergence were counted. The mean number of living Ips typographus occurring under the bark decreases by 49 % from November to April. Winter mortality mainly affects larval stages and young adults. The same trend was observed for the parasitoids Coeloides bostrychorum (48.5 %) and Roptrocerus xylophagorum (47.5 %). 1 Introduction The spruce bark beetle Ips typographus (Linnaeus) (Coleoptera, Scolytidae) is the most destructive scolytid attacking spruce forests (Picea abies Karsten) in Palaearctic regions (Christiansen and Bakke, 1988). The beetle also causes great damage to Italian spruce stands growing along the southern Alps (Ambrosi, 1981; Ambrosi and Angheben, 1986; Ambrosi et al., 1990; Lozzia, 1993; Faccoli, 1999). In central and north Europe, Ips typographus completes one generation per year with adults overwintering in the litter (AustaraÊ and Midtgaard, 1986; Christiansen and Bakke, 1988). However, due to the large European distribution of Ips typographus (Pfeffer, 1995), the beetle develops under very different weather conditions, which can affect both the number of generations and the duration of larval instars forcing the insects to face the winter at an unsuitable stage of development (Wermelinger and Seifert, 1999). In Italy as well as in other southern European countries, long warm summers very often allow Ips typographus to start a second generation (Annila, 1969; AustaraÊ et al., 1977; Christiansen and Bakke, 1988; Coeln et al., 1996; Faccoli, 1999). In this case, offspring usually do not complete development before winter and several individuals have to hibernate as larvae or pupae. However, in favourable environmental conditions also callow and young adults spend the winter under the bark of standing spruces (Ambrosi and Angheben, 1986). Investigations carried out in central Europe (Germany) showed that less than 10 % of Ips typographus young adults hibernated in the soil (Biermann, 1977), a proportion much lower than that recorded by many authors. Similarly, Zumr (1982) in southern Bohemia (Czechoslovakia) found a total number of overwintering beetles in litter not exceeding 5 % of the estimated population. Generally, direct control of bark beetle attacks is difficult through conventional insecticide treatments, as the scolytids are protected beneath the bark of the host trees during oviposition and juvenile development. Indirect control includes sanitation felling (Mills, 1991), pheromone mass trapping (Bakke, 1981) and biological control (Mills, 1983). In particular, the existence of approximately 140 arthropod species living on I. typographus has been documented in Europe (Hellrigl and Schwenke, 1985; Weslien, 1992). The most frequent larval parasitoids of Ips typographus are two braconids (Hymenoptera, Braconidae), Dendrosoter middendorffi Ratzeburg and Coeloides bostrychorum Giraud, and two pteromalids (Hymenoptera, Pteromalidae), Rhopalicus tutela Walker and Roptrocerus xylophagorum (Ratzeburg) (Kruger and Mills, 1990). All these species overwinter as preimmaginal stages under bark of spruce trees attacked by Ips typographus. Little is known, however, regarding the mortality of overwintering parasitoids of bark beetles, and how that is related to their population dynamics. In this respect, if a differential in winter mortality between I. typographus and its parasitoids were to occur, this may subsequently lead to changes in the numerical relationships between species in the following spring, with serious consequences for biological control (AustaraÊ and Midtgaard, 1986). However, how overwinter conditions influence insect populations is still not clear. At the end of the summer GreÂgoire et al. (1995) found attacked spruce trees sheltering 30,000 to 80,000 pre-emergent adults, while in spring only 10,000 to 16,000 individuals per tree could be found, even counting insects occurring in the litter at the base of the trees. As the population dynamic of Ips typographus depends on complex relationships between host trees, bark beetles and their natural enemies (Christiansen et al., 1987), factors stressing trees or inducing variations in the natural enemy consistence could lead to bark beetle outbreaks. In this respect, an accurate population estimation by measuring changes in time and space should be required to evaluate either outbreak risks or the effectiveness of the control methods (Gonzalez et al., 1996). Winter mortality from freezing could be an important determinant of population dynamics in Ips typographus. Understanding variations in cold tolerance and overwinter behaviour may help predict population dynamics and distribution of potential pests. To improve the knowledge concerning the spring relationships between host and natural enemies, a field experiment was carried out in the south-eastern Alps to assess the winter mortality of sub-corticolous populations of Ips typographus and its parasitoids. U.S. Copyright Clearance Center Code Statement: 1436±5693/2002/7503±0062 $15.00/0

2 M. Faccoli: Winter mortality of Ips typographus and its parasitoids 63 Table 1. Characteristics of the trees and number of samples collected during each sampling. Tree Diameter of the trees (cm) Height of the trees (m) Attacked area (m 2 ) Length of the attack (m) No. of samples % sampled bark A B C Table 2. Mean number of specimens obtained from the sampled bark (1dm 2 ) in different trees and months. Tree A Tree B Tree C Mean ± SD Species Nov Feb Apr Nov Feb Apr Nov Feb Apr Nov Feb Apr I. typographus ± ± ± 0.6 R. xylophagorum ± ± ± 2.4 ± ± ± 0.6 C. bostrychorum ± ± ± Materials and methods The study was carried out during the winter 1997/98 in a natural spruce stand growing up at about 1100 m a.s.l. in the southeastern Alps (Friuli ± Venezia Giulia ± Italy). In the previous years the stand was heavily attacked by Ips typographus, which killed several mature trees growing up along an exploitation road. In November 1997, three spruce trees 60/70 years old (trees A, B and C) naturally attacked by the second generation of Ips typographus were felled. According to Gonzales et al. (1996), from the trunk of each tree, circular bark samples (1dm 2 ) were taken using a piece of sharpened metal pipe driven into the bark with a hammer. In relation to the tree characteristics, various samples were collected, but in all cases samples were taken considering the possible variation in beetle distribution along and around the trunks. Per trunk, three sections were considered corresponding to 0 %±20 % (lower part), 20 %± 60 % (middle part) and 60 %±100 % (upper part) of the normalized infested length of the tree (Gonzales et al., 1996). In the lower and upper part the bark samples were taken at regular intervals (levels) of 0.5 m, while in the middle part they were taken every meter (fig. 1). Samples were taken around the trunk from three sides (expositions): upper (S), left (L) and right (R). The inferior side of the trunks was not sampled because it was not accessible without damaging the overwintering insects. Data concerning both the sampled trees and the sampling scheme are reported in table 1. Bark samples were separately placed into coded plastic bags, brought back to the laboratory and analysed by counting the numbers of individuals of each insect species and for each development stage. Then samples were individually maintained in rearing containers (labelled Petri dishes) and held at approximately 20 C until the complete emergence of all insects occurring in the bark. Number of hosts and parasitoids that emerged were recorded daily. After emergence, bark samples were individually dissected off and the numbers and stadia of living and dead Ips typographus and parasitoids were recorded. Mortality was assessed visually; insects were considered dead if they showed no sign of movement, or were deformed or showed signs of melanization or other discolouring of the integument due to fungal or bacteria infection. Sampling was repeated three times (23 November, 2 February and 8 April), each time collecting 63 bark samples from both tree A and C, and 42 from tree B (table 1). Finally, the minimum air temperature was recorded daily and compared with the monthly mean temperature observed in the same stand in the last 30 years (1961±91) (fig. 2). All data were log-transformed (X' = Log (X+1)) to meet assumptions of normality and homogeneity of variance (Zar, 1999), and analysed by a multivariate ANOVA test using the General Linear Model for randomized block designs by the STATISTICA 3.1 â program. Because each tree was colonized by a different number of insects, the density of colonization was employed as covariable to compare different trees. Means were compared by Tukey post hoc test at a = Results The mean numbers of I. typographus per dm 2, as estimated by both bark dissection and rearing, were significantly low in April and in the lower part of the trunks (df = 4; 140, F = 3.17, P < 0.01; Tukey test, P < 0.01) (table 2, figs 3 and 5). In November the sampled trees showed statistical differences, with tree B sheltering more beetles than A and C (df = 2; 165, P < 0.05) (table 2). However, the differences between trees disappeared in April. In the upper part the density of alive Ips typographus is almost the same during the winter (fig. 5), but due to low densities recorded in this stem section, meaningful comparison was difficult. In addition, some replicates contained no beetles, effectively reducing the level of replication. The correlation between the number of Ips typographus found in November and April is reported in fig. 4. Among the Ips typographus parasitoids, we mainly found Coeloides bostrychorum and Roptrocerus xylophagorum (R. xylophagorum was found only in tree A and B; see table 2). Several other natural enemies emerged from the bark samples, but their number was too low to allow statistical analysis. Concerning C. bostrychorum and R. xylophagorum, their spatial-temporal occurrences have the same trend as Ips typographus, with higher density in November and in the central and upper section of the stem (df = 4; 140, F = 2.76, P < 0.01and F = 6.29, P < 0.01, respectively). No statistical differences in densities were found between trees, indicating that a relatively ho-

3 64 M. Faccoli: Winter mortality of Ips typographus and its parasitoids Fig. 1. Sampling of the trunks. Level: distance of samples from the base of the tree; L, left side; S, upper side; R, right side. mogeneous population was sampled and that development was effectively suspended over winter. Variations in insect densities according to the trunk side (S, L and R) were not observed. 4 Discussion The stages of Ips typographus under bark were predominately young adults, pupae and larval instars, in that order of abundance. This under-bark population is very typical of the winter generation in low European latitudes. Passing from November to April there was a mean reduction of the live Ips typographus of about 49 % (fig. 3 and table 2). A similar trend was also observed for Coeloides bostrychorum and Roptrocerus xylophagorum, which showed a reduction in population size of 48.5 % and 47.5 %, respectively (fig. 3 and table 2). However, winter mortality was different in each sampled tree. In particular, the amount of Ips typographus found in November showed statistical differences between trees (B > A and C) mainly in the central part of the trunk, which usually is the more colonized part (Mayyasi et al., 1976). In this respect, the poor beetle density in the lower and upper trunk sections (fig. 5) has also been found by other authors (Weslien and Regnander, 1990; Gonzales et al., 1996). As the differences between trees disappeared in February and April, during the first part of the winter, mortality occurred with highest intensity in the central part of the stems that were heavier colonized (fig. 5). Although the mortality mechanisms in Ips typographus and its associated parasitoids are quite complex and need to be analysed and evaluated in each single case, the main factors inducing mortality during the winter could be low temperatures and poor lipid content necessary for insects to overcome the winter (Maslov and Matusevich, 1990). Regarding low temperatures, previous studies carried out in north Europe reported adults of Ips typographus as surviving at air temperatures near ±30 C (Annila, 1969). However, the temperature relevant for bark dwelling organisms is the phloem temperature, which may differ markedly from the air temperature due to radiation or insulation effects. In northern countries, where the winter usually is much longer and colder, most Ips typographus adults hibernate in the litter often covered by the snow, which is a very good thermal insulator (Botterweg, 1982; Christiansen and Bakke, 1988). In this respect, studies carried out in Estonia reported 33 % mortality in adults of various Ips species overwintering in the forest litter (Poolak, 1975). Similar values (40.5 % and 43.8 %) were found in Norway in a population of Ips typographus hibernating in the litter Fig. 2. Daily minimum temperatures of the winter 1997/98 compared with the monthly mean temperatures observed in the same stand over the last 30 years (1961±91).

4 M. Faccoli: Winter mortality of Ips typographus and its parasitoids 65 Fig. 3. Percentage of live specimens occurring during the winter ± standard deviation: different letters correspond to statistical differences calculated on mean values by pairwise comparison (Tukey test, P < 0.05). (AustaraÊ and Midtgaard, 1986). In Italy, however, most callow adults and all young adults spend the winter under the bark of standing spruces (Ambrosi and Angheben, 1986). Temperatures less cold than those observed in north Europe may have more devastating effects on insect populations, mainly on young stages. Winter mortality in immatures was postulated also by Coeln et al. (1996) and AustaraÊ et al. (1977), who indicated that survival of larvae and pupae during the winter is not possible. Similar studies showed that only completely developed Ips typographus adults survived through the winter, while both pupae and larvae had supercooling points of ±13 and ±17 C, respectively (Annila, 1969; Abgrall and Schvester, 1987). Lawson (1993) observed in under-bark populations that overwinter mortality of Ips grandicollis larvae (95 %) and pupae (86 %) was significantly higher than in adults (41%). Similarly, immatures of North American Ips species, which remained in the inner bark of their host trees, were especially vulnerable to mortality from freezing as they have lower lethal temperatures of ±5 to ±12 C (Lombardero et al., 2000), a temperature very similar to that recorded in our stand (fig. 2). Fig. 4. Linear regression between the number of live Ips typographus found in November and in April.

5 66 M. Faccoli: Winter mortality of Ips typographus and its parasitoids Fig. 5. Percentage of live specimens occurring during the winter in different months and stem sections (± standard deviation): different letters correspond to statistical differences calculated on mean values by pairwise comparison (Tukey test, P < 0.05). The long and warm Italian summer often allows Ips typographus to start a second generation (Faccoli, 1999). In this case, offspring cannot complete development before winter, and several individuals have to hibernate as immature stages, which have a lower cold resistance than callow adults (Annila, 1969; AustaraÊ et al., 1977). In our study, about half of Ips typographus specimens found in November were represented by pre-immaginal stages (larvae and pupae), whereas in April only adults were found alive under the bark. In February, a few days after the second sampling, the mean temperatures remained very low for several days (fig. 2). In this period the strongest Ips typographus mortality probably occurred, causing statistical difference between months (fig. 3). Because in the lower and upper part of the trunk the number of insects is about the same during the winter (fig. 5), the mortality occurred mainly in the central part of the stems, where there was the highest density of colonization. As known, the bark is an isolating material but strong larval colonization may modify its characteristics. In this respect, the poor insect density observed in the lowest part of the trunk associated with thick bark might reduce winter mortality in bark beetles and in their natural enemies. Between different stem sides no statistical differences were found in insect occurrences. Because insect distribution around the trunk is homogeneous in November, as previous studies have also reported (Weslien and Regnander, 1990; Gonzales et al., 1996), Ips typographus does not preferentially choose a stem side to overwinter. In addition, the study was carried out in a secondary pure spruce stand where the microclimatic conditions occurring `under canopy' are constant, independent of the exposition (Odum, 1983), causing equal insect mortality on all exposed bark. Concerning natural enemies, Roptrocerus xylophagorum and Coeloides bostrychorum are cosmopolitan parasitoids of bark beetles (Graham, 1969; Faccoli, 2000). Both of these species are ecto-parasitoids of immature scolytid, and the preferred stages for parasitization are third instar larvae and occasionally pupae (Samson, 1984; KruÈ ger and Mills, 1990). Their population density usually reaches a peak in late summer/early autumn. According to our observations, R. xylophagorum overwinter mainly as larvae. This finding contrasts with that of Reid (1957), who recorded Roptrocerus xylophagorum overwintering mainly as adults, with only few larvae and pupae present. Overwintering of adults was not observed in the present study, although this does not dismiss the possibility of adult overwintering in other countries. In our experiment the winter mortality in R. xylophagorum was 47.5 %. In a similar study carried out in south Australia for the same species, Lawson (1993) reports a much higher mean mortality (86 %), although there is no information about ecological conditions in the study area (i. e. altitude or mean temperatures). However, R. xylophagorum density was probably overestimated in April due to errors in visual assessment of mortality as bark saturation and associated fungal and bacteria diseases caused the extreme decomposition of many immatures. For C. bostrychorum, which spends the winter as mature larvae in cocoons spun under the bark at the end of the larval galleries of its host, mortality was very easy to assess. How low temperatures modify parasitoid populations is still poorly understood. For instance, overwintering as cocoon, C. bostrychorum should definitely be more resistant to low temperature (KruÈ ger and Mills, 1990), although in the present study a 48.5 % mean mortality is reported. However, studying the survival of Dendrosoter protuberans (Hym.,

6 M. Faccoli: Winter mortality of Ips typographus and its parasitoids 67 Braconidae), a braconid parasitoid of bark beetles having a biology very similar to that of C. bostrychorum, Hostetler and Brewer (1976) found a winter mortality ranging from 79 % to 89 %. In addition, peak mortality of D. protuberans occurred in the middle of the winter, associated with low January temperatures of ±11 C, climatic conditions similar to those observed in this study (fig. 2). Moreover, in some braconid belonging to the genus Perilitus, it is known that winter mortality ranges from 60 % to 75 % (Richerson and DeLoach, 1973; Cartwright et al., 1982). This decrease possibly was caused by the parasite consuming the fat reserves of its host, resulting in the death of both (Richerson and De- Loach, 1973). Not all the observed mortality can be related to overwintering alone, since in the case of Ips typographus some would have been caused by intraspecific larval competition occurring before the onset of colder weather caused development to halt (Lawson, 1993). In this respect, as the insects have to pass a long cold period of inactivity where they cannot feed, the amount of reserves is an important factor affecting survival (Atkins, 1967, 1975; Safranyik, 1976; Botterweg, 1982; Slansky and Haack, 1986; Anderbrant, 1988). Scolytids developed in high density suffered from a strong intraspecific competition extending the development time (Anderbrant et al., 1985). Consequently, beetles were forced to face the winter as larvae or young adults poorly resistant to low temperatures (Anderbrant et al., 1985; Anderbrant, 1988, 1990). In this way, competition may decrease the probability of bark beetles overcoming the winter, accelerating the decline of epidemic populations. Affecting the weight of the host larvae (Anderbrant et al., 1985), strong competition between beetles also influences the survival possibilities for parasitoids, which dispose of smaller hosts to complete the development with a consequently lower amount of reserves to overcome the winter. Moreover, overcrowding also affects offspring production, adult survival and fat content (Anderbrant et al., 1985). In particular, body fat is the main parameter describing the energy content of the beetles and may give information about insect resistance (Botterweg, 1982). Botterweg (1983) found higher fat content in beetles emerging in autumn than in summer, which was considered as a possible adaptation of the late developing beetles to prepare for the winter. During the winter the adults seem to lose 40 %±50 % of their fat (Botterweg, 1982). Because the carrying capacity of the breeding substrate is easily reached at a fairly low density (Berryman, 1976), in high density severe larval competition before pupation strongly affects the weight and fat content of new adults, and hence their resistance and longevity (Anderbrant, 1988). In this respect, our data give evidence of higher mortality in samples containing more insects (fig. 5), where the rate of beetles surviving the winter is positively correlated to the pre-wintering density (November) (fig. 4). In conclusion, if all development stages were able to overwinter successfully, the propagation of a population would continue in the spring where it ceased at the beginning of the previous winter. This means that the population grows rapidly over a few years. If, in contrast, winter mortality in immature stages is high, the effect of an unfinished generation entering winter as immatures is nil (Wermelinger and Seifert, 1999). This pattern of overwinter mortality tends to lead to early-spring preemergent populations of Ips typographus consisting mainly of adults. Although it is difficult to draw any definite conclusions, it seems that winter mortality mainly occurs in the middle of the winter, affecting larval stages or young adults of Ips typographus; it has various influences on natural enemies; and it has a greater impact in spruces that are heavily attacked, reducing the density differences existing among trees. The results shown do not support the view that parasitoids suffer less (or more) mortality than I. typographus over winter. However, since these results are based on only one season's data, follow-up research is necessary for confirmation. The results from the present study nonetheless demonstrate that further research into differential mortality between bark beetles and their associated parasitoids is needed. 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Correspondence: Massimo Faccoli, Department of Environmental Agronomy and Crop Productions ± Entomology, University of Padua ± Agripolis, via Romea 16/a, Legnaro (PD), Italy. massimo.faccoli@unipd.it