Allochthonous blue spruce in Central Europe serves as a host for many native species of sawflies ( Hymenoptera , Symphyta )

In air-polluted mountain areas of the Czech Republic, including the Ore Mountains, pure forest stands of introduced blue spruce (Picea pungens) were established in the 1980’s. We studied the Symphyta (Hymenoptera) fauna in the canopies of these trees at four sites and in the canopies of adjacent Picea abies trees at one of these sites by beating tree branches. For the first time, Nearctic blue spruce is reported as a host for 17 European species of Symphyta (sawflies). Diprionids in the genus Gilpinia were the most abundant sawflies on P. pungens and were more abundant on P. pungens than on the native Picea abies. Spruce pamphiliids in the genus Cephalcia were also more abundant on P. pungens than on P. abies, while the abundances of representatives of the tenthredinid genera Pikonema, Pachynematus, and Pristiphora were similar on P. pungens and P. abies. Our results indicate that many species of European spruce Symphyta are able to use the allochthonous species P. pungens as a host.


Introduction
In Central Europe, P. abies (L.) Karst is the only native species of spruce (Schwenke 1978).Many introduced spruce species including of the blue spruce, Picea pungens Engelm, are occasionally cultivated in urban areas.Beginning in the 1980s, pure stands of P. pungens have been planted in an area of about 100 km 2 in the air-polluted mountain regions of the Czech Republic.P. pungens was thought to require only modest soil resources, to have a high tolerance to sulfur oxide air pollution, and to have the ability to resist or avoid ungulate herbivores (Šika 1976, Tesař 1981, Balcar 1986, Jirgle et al. 1983, Kubelka et al. 1992).The assumption about high resistance to air pollution was found to be incorrect, however, because the needles of young P. pungens and P. abies exhibit the same degree of damage in response to air pollutants (Soukupová et al. 2001).
Although the blue spruce P. pungens is planted in the extensive, air-polluted areas of the Czech Republic, the Symphyta fauna developing on this allochthonous plant have not been thoroughly studied.One reason is that serious outbreaks of pests have not occurred during the 25-to 30-year period following the establishment of pure stands of P. pungens in the Ore Mountains (Holuša and Holuša 2003).
The host status of P. pungens for European native Symphyta is unknown.The goals of this study were (i) to identify the sawflies that feed on P. pungens in the Czech Republic and (ii) to compare the abundances of these sawflies on the native P. abies and on the introduced P. pungens.

Methods
Sawflies were studied in three localities in the Ore Mountains (NW Czech Republic) (Table 1).Two localities (Jirkov, Dlouhá louka) had pure stands of P. pungens, and one locality (Sněžník) had a pure stand of P. pungens and a pure stand of P. abies that were 100 m apart.
Sawfly larvae and adults were sampled by beating tree branches and collecting the falling insects on a sheet stretched on a 0.5 × 1 m metal frame.On each sampling date, 10 samples were collected at each of the four stands.For each sample, two branches were selected at random in the crowns of 10 trees, the branches were located from 0.7 to 2.5 m above the ground, and the sampled trees were in a line with 10 m between adjacent trees.Trees were sampled on 17 May, 15 June, 14 July, 15 August, 15 September, and 15 October 2007.Thus, one sample consisted of insects collected from one stand (a total of 20 branches on 10 trees) across all six sampling dates.
The collected insects were stored in 75% ethanol.Larvae were identified using the keys of Beneš and Křístek (1979), Battisti and Jiang-hua Sun (1996), Battisti and Zanocco (1994), Martinek (1988), and Zanocco and Battisti (1995).Very young larvae (first and second instars) were identified only to genus (Cephalcia, Gilpinia, and Pristiphora).The current knowledge of larvae allows the identification of some Pachynematus s.l. and Pristiphora s.l.only to the subgeneric level and are here referred to as the Epicenematus and Sharliphora species groups, respectively.Adult sawflies were identified using the keys of Beneš and Křístek (1979), Viitasaari (2002), andZhelokhovtsev (1988).The nomenclature follows Taeger and Blank (2011), and host plants are given according to Taeger et al. (1998) unless stated otherwise.
The data of larvae per locality were not normally distributed.When the abundance of a sawfly species was > 10 on both P. abies and P. pungens at Sněžník, the values were compared with a Wilcoxon pair test in Statistica 12.0.

Results
In total, 748 larvae and 79 adults of 36 species of sawflies were collected (Table 2).Among the 36 species, 23 have been previously associated with spruce, and the 13 have been previously associated with other plant species (Table 2).Larvae obtained from the branches of P. abies (N=127) and P. pungens (N=621) belonged to 12 and 18 species of Symphyta, respectively.Five species in the genus Cephalcia were only found in small numbers and on several specimens of P. pungens, and two of these five species were found on P. abies (Table 2).The abundance of larvae belonging to Cephalcia species did not differ between samples from P. abies and P. pungens (Table 2).
Diprionids of the genus Gilpinia were the most abundant sawflies in the samples and represented 51.8% and 35.4% of the specimens collected from P. pungens and P. abies, respectively.Gilpinia abieticola and G. hercyniae were the most numerous species, while G. polytoma was recorded exclusively in the P. abies and P. pungens stands at Sněžník.Although the Gilpinia abundancy did not differ between P. abies and P. pungens stands, more first and second instar larvae of Gilpinia were found on P. pungens than on P. abies at Sněžník (Table 2).
Almost identical species (both larvae and adults) of spruce tenthredinids (Pristiphora, Pachynematus, and Pikonema) were found in the P. abies and the P. pungens samples, and the abundance of larvae of each species did not differ on P. abies vs. P. pungens.Based on larvae, Pachynematus (Epicenematus) sp.followed by Pristiphora compressa were the most abundant species in P. pungens samples (Table 2).

Discussion
In the current study, a total of 18 sawfly species were collected from P. pungens in the Ore Mountains of the Czech Republic.This represents 56% of the species of needlefeeding spruce sawflies in Central Europe (N=32) (Beneš and Křístek 1979, Holuša 2005, Jachym et al. 2005).P. pungens was recorded as a new host for 17 of these Palaearctic species.The 13 additional species have not been associated with spruce as a host, and their occurrence in the samples was accidental (Table 2).
The most abundant larvae collected from P. pungens were species of Gilpinia.All three spruce diprionids (G.abieticola, G. hercyniae, and G. polytoma) are common in spruce stands in Central Europe (Úradník andKulfan 2002, Holuša andRoller 2004), but the three species can differ in abundance, dominance, and frequency (Martinek 1960, Úradník and Kulfan 2002, Holuša and Roller 2004).Untill this study, G. hercyniae has been the only European diprionid known to feed on P. pungens (Balch 1939).
The numbers of spruce tenthredinids in the genera Pikonema, Pristiphora, and Pachynematus were similar on P. pungens vs. P. abies.We suspect that the L1 and L2 lar-vae identified as Pachynematus (Epicenematus) sp. are P. montanus, although Pachynematus (Epicenematus) pallescens (Hartig, 1837) and the extremely rare P. styx may also be present in the studied stands.The former species has the ability to rapidly increase (Kolubajiv 1939, Martinek 1994, Reisenberger and Krehan 1993) and is widespread not only in P. abies stands (Holuša 2002) but also in P. pungens stands (this study).Another species that can rapidly increase, Pikonema scutellatum, was rarely collected in the study area, although it is common in Central Europe (summarised by Holuša and Lubojacký 2008).Because one adult of the very rare species Pikonema insigne was found in the P. pungens stand at Sněžník, we suspect that P. pungens is a host for this species.
The larvae of eight Pristiphora species plus adults of P. (Sharliphora) pallida and P. (Sharliphora) parva were collected on P. pungens, but it is very probable that larvae of Pristiphora (Sharliphora) sp. were represented mainly by the larvae of Pristiphora nigella.P. abietina is a pest of Norway spruce in Central Europe (Pschorn-Walcher 1982) and often occurs in high numbers with Pikonema scutellatum and Pachynematus montanus (Kolubajiv 1939(Kolubajiv , 1958)).However, P. abietina prefers lower altitudes where it can rapidly increases (Martinek 1960, Holuša 2002).Thus, the low abundance of this species in the studied stands is in accordance with the aforementioned studies.P. compressa, the most common Pristiphora in P. pungens stands, could be even more abundant than P. abietina in mountain stands of P. abies (Úradník and Kulfan 2002).We also found P. pallida and P. robusta, that have been very seldom recorded in spruce stands (Forsius 1911, Křístek 1973).
In the investigated air-polluted areas the native P. abies stands are almost completely absent because this tree was not used for forest regeneration in the 1980's (Kubelka et al. 1992).Our study indicates that a range of P. abies defoliators use P. pungens as a substitute host plant.This phenomenon has also been documented for herbivorous moths.Of the 50 moth species that feed on P. abies in Europe, 31 have been found to develop on the needles and buds of P. pungens (Kulfan et al. 2010).
The spruce-feeding sawflies in Central Europe are not strictly monophagous on P. abies.Most of these species have been observed to feed on other Palaearctic spruces like Picea obovata (Ledeb.),Picea koraiensis Nakai, and Picea jezoensis (Sieb.& Zucc.) (Taeger et al. 1998).Before the current study, however, Nearctic spruces had not been reported as hosts for European Symphyta other than for G. hercyniae (Balch 1939).
Because the abundance of sawfly larvae and adults was low in the current study (compare with Holuša 1999, Holuša andLubojacký 2008), we did not observe substantial defoliation of trees in the P. pungens stands in 2007.Severe defoliation of P. pungens was reported in the 1970s and early 1980s even at altitudes of 900 m (Holuša and Holuša 2003).Many sawfly outbreaks occurred throughout the Czech Republic in the early 1980s.The most recent instance of severe defoliation and subsequent chemical treatment was in 1982 (Holuša and Holuša 2003).The regeneration of P. abies stands has recently increased in the Ore Mountains (Šrámek et al. 2008), and thus populations of sawflies living on P. pungens may recolonize the P. abies stands in the future.Although sawflies have not recently caused extensive damage to spruce in Central Europe, the spruce sawflies are in a latency period in this region (Holuša et al. in prep.), and local outbreaks have occasionally occurred (Egginger et al. 2014).

Conclusions
Our results demonstrate that European spruce sawflies are able to use the diverse allochtonous spruce species as hosts and may show stronger preferences for the new host, here especially P. pungens, than for the native host, P. abies.

Table 1 .
Characteristics of studied stands.

Table 2 .
Total numbers of sawflies (Hymenoptera: Symphyta) collected on P. abies and P. pungens in the Czech Republic (plus information on known host plants for each species of sawfly).The sawflies were collected from 20 branches per stand (two branches on each of 10 trees) in three P. pungens stands (at Jirkov, Dlouhá louka, and Sněžník) and in one P. abies stand (at Sněžník) on six sampling dates from spring to fall in of 2007.Sawfly species feeding on spruce are in bold.When the abundance of a sawfly species (larvae + adults) was > 10 on both P. abies and P. pungens at Sněžník, the values were compared with a Wilcoxon pair test (an asterisk indicates a significant difference, and n.s.indicates a non-significant difference).The information on known host plants isfrom Taeger et al. (1998)unless indicated otherwise.