Invasive species are known to cause severe dam- ages on forest ecosystems worldwide. In Eu- rope two such examples are Dutch Elm Disease (Ophiostoma ulmi and O. novo-ulmi) (Gibbs
1978, Brasier 1991) and the pine wood nema- tode (Bursaphelenchus xylophilus) (Soliman et al. 2012) both which are vectored by insects. The number of non-native insect species recorded
Tetropium gabrieli and Ips cembrae (Coleoptera;
Cerambycidae and Curculionidae) – invasion of two potential pest species on larch in Sweden
ÅKE LINDELÖW, GUNNAR ISACSSON, HANS PETER RAVN & MARTIN SCHROEDER
Lindelöw, Å., Isacsson, G., Ravn, H.P. & Schroeder, M.: Tetropium gabrieli and Ips cembrae (Coleoptera; Cerambycidae and Curculionidae) – invasion of two potential pest species on larch in Sweden. [Tetropium gabrieli och Ips cembrae (Coleoptera; Cerambycidae och Curculionidae) – invandring av två möjliga skadeinsekter på lärk till Sverige.] – En- tomologisk Tidskrift 136 (3): 103-112. Uppsala, Sweden 2015. ISSN 0013-886x.Invasive insect species cause severe damages on forest ecosystems worldwide. One ex- ample of this is when non-native tree species are planted and some of their associated insect species also manage to establish in the new area. In Sweden, different species of larch (Larix spp.) are non-native tree species which has been planted over increasing ar- eas during the last 50 years. The aim of the present study was to investigate if non-native bark- and wood-boring insects on larch have established in Sweden and, if so, their area of distribution. We used felled larch trees in 17 larch stands as a survey method for a broad spectrum of bark- and wood-boring species and pheromone-baited traps in seven ports and 47 larch stands for the bark beetle Ips cembrae during the years 2009-2014. Two non-native species were recorded: the cerambycid Tetropium gabrieli and the bark beetle I. cembrae.
Tetropium gabrieli dominated in the felled larch trees and is distributed in the south-eastern part of Sweden. Within its range of distribution it seems to be present in most larch stands with suitable breeding material. Prior to our study this species was only recorded in dead larch trees close to a port. Ips cembrae was caught in traps in nine larch stands in the most southern part of Sweden demonstrating for the first time that the species have established in Sweden. The first individuals were caught in two nearby stands in 2011 and inspections of the stands revealed that the species had reproduced already in 2007 or 2008 in standing killed trees. The trapping demonstrated that the population level of I. cembrae increased more than four times from 2012 to 2014. Both T. gabrieli and I. cembrae are potential pest species and should be considered in the management of larch stands.
Åke Lindelöw, Swedish University of Agricultural Sciences, Department of Ecology, P.O.
Box 7044, S-75007 Uppsala, Sweden. E-mail: ake.lindelow@slu.se
Gunnar Isacsson, The Swedish Forest Agency, P.O Box 63. SE-281 21 Hässleholm, Swe- den; E-mail: gunnar.isacsson@skogsstyrelsen.se
Hans Peter Ravn, University of Copenhagen, Department of Geosciences and Natural Resource Management, Rolighedsvej 23, DK-1958 Frederiksberg C. Denmark. E-Mail:
hpr@ign.ku.dk
Martin Schroeder, Swedish University of Agricultural Sciences, Department of Ecology, P.O. Box 7044, S-75007 Uppsala, Sweden. E-mail: martin.schroeder@slu.se
Ent. Tidskr. 136 (2015)
in Europe has increased exponentially in re- cent years as a result of the strong increase in global trade which facilitates introductions and establishments (Roques 2010). Well known spe- cies are Anoplophora glabripennis and Agrilus planipennis, both posing a large threat to broad leaf trees in Europe. Also insect species native to Europe may spread to new areas within Europe and become a problem. One such risk is when European tree species is planted outside their natural distribution and associated pest species also manage to establish in these new areas.
In Europe, larch (Larix spp.) have been plant- ed in many countries outside their natural distri- butions. In Sweden, larch has been planted since the 19
thcentury but for a long time only as single trees or small stands. But in the last 50 years the area reforested with larch has increased, and especially during the last decades. More than 90
% of the seedlings planted in Southern Sweden belong to the hybrid Larix x eurolepis (Larix decidua (Mill.) x Larix kaempferi Sarg.) (Jonas Bergquist pers. comm.).
The total volume of larch in Götaland is about 0.6 million m
3corresponding to 0.1% of the total forest volume including all tree spe- cies (Anonymous 2012). But, since most stands are still young the volume will increase in the future. With an increasing area of larch forest accurate information about the establishment of non-native pest insects on larch is of interest.
One important pathway of introduction of bark- and wood-boring insects is timber imports
(Hulme 2009). During the last decades sub- stantial volumes of unbarked larch timber have been imported to Sweden. Inspections of such imports, stored in ports or at sawmills, have re- vealed live individuals of two larch insects: the cerambycid beetle Tetropium gabrieli (Fig. 1) and the bark beetle Ips cembrae (Fig. 2) (Lund- berg 1986, 1988, Lundberg & Pettersson 1997).
Both T. gabrieli and I. cembrae are consid- ered as pest species because they occasionally kill living larch trees (Gorius 1955, Bevan 1987, Ravn 2012a, Arac & Pernek 2014). Both spe- cies have also established in several European countries outside their natural distribution in the Alps in central Europe. In UK the first observa- tion of T. gabrieli dates to 1903 and already in 1923 the species was considered distributed in UK except Scotland (Anonymous 1923, Duff 2007). In Denmark T. gabrieli was first recorded in 1890 and later 1892, 1930, 1934, 1950, 1954 but considered rare (Hansen 1964), rather rare (Bejer 1979) or scattered mainly in eastern part of the country (Fugle og Natur 2015).
Ips cembrae was discovered in UK 1955 and timber imports were suggested as the main path- way (Crooke & Bevan 1957). In the mid 1990´s, I. cembrae was detected in Denmark (Ravn &
Harding 1995) and since then has spread rap- idly and is now widely distributed in the country (Ravn 2012b).
Previous to the present study T. gabrieli was the only non-native bark- and wood-boring in- sect on larch recorded from Swedish forests (Er-
Figure 1. Larch longhorn beetle Tetropium gabrieli, femaleand male. Scale bar is 5 mm. Foto Åke Lindelöw.
Lärkbock (Tetropium gabrieli), hona och hane. Skalstreck ca 5 mm.
Figure 2. Large larch bark beetle Ips cembrae. Scale bar is 1 mm. Foto Göran Liljeberg.
Lärkborre (Ips cembrae). Skalstrecket är ca 1 mm
icson 2010). At the distance of 4 km from the main port of Karlshamn in the province of Ble- kinge in southeastern Sweden one dead adult of T. gabrieli was found in 2007 in a branch from a standing larch tree. In the same year at 1 km distance from the port, larval galleries of Tetro- pium were found in 5 trees and several adults were reared from larvae. In 2008 galleries of Tetropium were found in a dead larch tree about 6 km from the port.
The aim of the present study was to conduct the first systematic survey for non-native bark- and wood-boring insects on larch in Swedish forest.
Material & Methods
The study was conducted in southern Sweden during six years 2009 - 2014. Two survey meth- ods were used: (1) living larch trees that were
felled in spring and inspected for colonization by bark- and woodboring beetles after one sum- mer and (2) traps baited with the pheromone of I. cembrae.
Felled trees
Trees of larch (Larix sp.) were cut in totally 17 larch stands in 2009-2011: in eight respectively nine stands in 2009 and 2010 (provinces of Ble- kinge and Småland, seven of the stands were the same between the years), and in seven additional stands in 2011 (provinces of Halland, Småland, Västergötland, and Östergötland) (Fig. 6). Three trees were felled in each stand in the spring be- fore the start of the flight periods of bark- and wood-boring insects: one tree in a shaded po- sition, one in semi-shaded and the third one in a sun-exposed position. In one stand only two trees were felled in 2009 and in 2010, and in two
Figure 4. Tetropium gabrieli larval galler-ies and entrance into the sap wood where the larvae pupate. Foto Claes Hellqvist.
Ingångshål i lärkved gjorda av larver till lärkbock. Larven äter av kambiet och gna- ger en gång några cm in i veden och gör en puppkammare. Ur hemtagna vedpro- ver kläcktes enbart lärkbockar Tetropium gabrieli.
Figure 3. Debarking and inspection of a larch tree. Foto Claes Hellqvist.
Med barkspade och kniv avbarkades de fällda lärkarna. Spår av bark- och vedle- vande skalbaggar noterades och provbi- tar togs hem för kläckning.
Ent. Tidskr. 136 (2015)
stands in 2011. In total 66 cut trees were inspect- ed with a mean diameter at 1.3 m of 15.8 cm (SD=3.7 cm) (unfortunately a few trees were re- moved before inspected). The inspections were conducted in the spring the year after cutting.
Both tree stems and branches were debarked and carefully searched for signs of insect coloniza- tion (Fig. 3). Larval galleries, larvae and adults were noted and identified to species when pos- sible. Tetropium species cannot be determined to species level based on larval galleries (Fig. 4).
Thus, colonized stem sections were cut from the felled trees in 2009 (8 sections from six stands) and 2010 (9 sections from 7 stands) and brought to the lab for rearing out of adults. The stem sec- tions were put into rearing boxes at 20°C and
all emerging beetle adults were determined to species. All beetle adults were determined using Pfeffer (1995), Ehnström & Holmer (2007) and cerambycid larvae using Švácha & Danilevsky (1986). Some specimens of I. cembrae were sent to Milos Knížek for confirmation of identifica- tion. The nomenclature follows the Catalogues of Palaearctic Coleoptera (Danilevsky 2010, Alonso-Zarazaga 2011, Knížek 2011).
Trapping
Occurrence of Ips cembrae was surveyed us- ing pheromone-baited traps in ports and in larch stands. In each port two traps were used. A total of seven ports, with a history of larch timber im- ports, were surveyed in 2009-2011: five in 2009 (Sölvesborg, Karlshamn, Mönsterås, Västervik, Norrköping), three in 2010 (Karlshamn, Harg- shamn, Skutskär) and two in 2011 (Hargshamn, Skutskär).
A total of 47 larch stands were surveyed with traps in 2009-2014. One trap was used in each stand. In 2009-2010 traps were placed in the same stands in which larch trees were cut and in 2011 traps were placed in new stands, 8 with and 4 without felled trees (Fig. 5). In 2011 I.
cembrae was caught for the first time in Swe- den in the traps in the most southern sites (the first year traps were used in these locations). To get better data on the distribution of the species the number of trapping sites was increased to 27 larch stands in 2012 and 25 in 2013-2014 in the most southern part of Sweden (Fig. 7). In the two stands in which I. cembrae was caught in 2011 two traps were placed per stand in 2012 (distance 50-100 m between traps) and thus the average of the catches are given in results.
Multiple funnel traps (NOVE
©), baited with Cembrawit
©in 2009-2011, and with Cemsan
©in 2012-2014, were used. The trapping period included May-August (May-June in 2011 and 2014) targeting the main flight period of I. cem- brae. The traps were emptied once or twice dur- ing the trapping period.
To be able to compare the catch levels of I.
cembrae between the years when Cembrawit
©and Cemsan
©were used a small experiment was conducted in Denmark (Grib Skov, northern Själland) in 2012. In each of three larch stands one pair of pipe traps (Norwegian model 79),
Figure 5. Felled larch (Larix sp) tree and a pheromone trapto catch Ips cembrae. Foto Claes Hellqvist.
Fälld lärk (Larix sp.) och plastfälla betad med feromon för fångst av lärkborre Ips cembrae.
about 10 m apart, were baited with the two baits in 9 May and emptied four times until 17 August. On average the catch per trap was 2.2 times higher (range 2.0-2.5) for Cemsan
©(mean number caught 172) than for Cembrawit
©(mean number 77).
Results
Felled trees
Tetropium gabrieli was the only non-native bark- and wood-boring insect species recorded from the cut larch trees. In the years 2009-2011 the species was recorded from nine of the 17 larch stands with cut trees (Fig. 6). In total, 89 adult T. gabrieli were reared from stem sections of the felled trees from six stands 2009-2010 (no other Tetropium species emerged). Larvae from three additional stands were determined to T. ga- brieli. Additional specimens were reared from a dead larch tree and one adult T. gabrieli was caught in a trap baited with the pheromone of I.
cembrae in 2012 in Skåne.
Nine native species/taxa of bark- and wood- boring beetles were recorded from the felled larches (Table 1). Among the Curculionidae were the following species found: Pissodes sp. (larvae in stems), Pityogenes chalcogra- phus (galleries and adults, mainly in branches), Cryphalus asperatus (galleries and adults in branches), Ips typographus (galleries and adults in stems), Trypodendron sp. (galleries in stems);
Figure 6. Larch stands with experimentally cut trees for surveying Tetropium gabrieli, and four other sites where the species has been recorded. Observe that some of the lo- calities were situated close to each other (thus not visible as separate symbols on the map). The two stars in south-east (close to Karlshamn) represent the first finding of Tetropium gabrieli in Sweden (Ericson 2010). The most southern star represents one individual caught in a pheromone-baited trap for Ips cembrae. The lines represent borders of Swed- ish counties and green areas forest.
Lokaler med fällda lärkträd där Tetropium gabrieli inventer- ats samt fyra ytterligare fynd. Observera att en del punkter ligger mycket nära varandra. Två stjärnor (nära Karlshamn i Blekinge representerar de första fynden i Sverige (Ericson 2010). Den sydligaste stjärnan representerar en individ som påträffades i en feromonfälla för Ips cembrae. Grän- serna representerar länsgränser och grön färg skog.
Table 1. Number of felled larch trees colonized by bark- and wood-boring species in 2009-2011. Total number of inspect- ed larch trees was 23 in 2009, 24 in 2010, and 19 in 2011.
Antal fällda lärkträd som koloniserats av bark- och ved- levande skalbaggar 2009-2011. Totalt antal inspekterade lärkträd var år 2009 23 st, 2010 24 st och 2011 19 st.
Species 2009 2010 2011
Tetropium gabrieli 15 17 0
Rhagium sp. 0 8a 5
Pogonocherus sp. 0 0 1
Monochamus sp. 0 1 0
Pityogenes chalcographus 8 6 5
Cryphalus asperatus 1 0 1
Ips typographus 0 0 1
Trypodendron sp. 0 1 0
Pissodes sp. 0 0 4
Chrysobothris sp. 0 0 1
a) In the stump
Ent. Tidskr. 136 (2015)
among the Buprestidae Chrysobothris sp. (lar-
vae in stems); and among the Cerambycidae:
Rhagium sp. (larvae in stems), Pogonocherus sp. (larvae in stems), and Monochamus sp. (gal- lery in stem) (Table 1).
Trapping
No I. cembrae were caught in the traps in ports.
In larch stands the first individuals were caught in 2011 in the two southernmost sites, one km apart, in the province of Skåne (one individual in one trap and 17 in the other) (Fig. 7a). In 2012 a total of 150 I. cembrae were caught in seven larch stands (Fig. 7b), in 2013 a total of 662 in- dividuals were caught in four stands all of which were also occupied in 2012 (Fig. 7c) and in 2014 a total of 621 individuals were caught in nine stands including three new localities (Fig. 7d).
Discussion
Our study demonstrates that T. gabrieli is well established in Sweden and widely distributed in the southeast. The first record from Swed- ish forests was in 2007 close to a port (Ericsson 2010). But the species may have been present in Sweden long before that. The presence of T.
gabrieli may easily be overlooked, especially if trees are not killed and observed by forest own- ers. Also only few amateur entomologists search for beetles in dead trees.
The results from the experiment with felled larch trees indicate that T. gabrieli, within its area of distribution, occur in most larch stands.
Larch stands in Sweden have a fragmented dis- tribution and are generally small which means that they cannot be expected to host a continu- ous supply of breeding material (i.e. dying trees or logging residues). This suggests that T. ga- brieli have a high dispersal capacity. An alterna- tive explanation would be that the species also is able to reproduce in Norway spruce or Scots pine but there are no reports of this in the litera- ture thus this seems unlikely (Gorius 1955).
By using pheromone-baited traps we could for the first time demonstrate the presence of I.
cembrae in Swedish forest in 2011 by the catch- es in the two most southern localities. This was the first year these sites were surveyed. Subse- quent inspections of these sites in the autumn of 2011 demonstrated a few dead standing larch
trees in one of the sites in which I. cembrae had reproduced already in 2007 or 2008. We cannot exclude the possibility that the species have oc- curred in the region even earlier.
Our results suggest that so far I. cembrae is only distributed in the provinces of Skåne and Blekinge (most western part bordering to Skåne). The area of distribution can be divided into three parts: one southern part isolated from the rest by large areas of non-forest land, one eastern part with records from only one stand and one western part with records from several stands. Since 2012 (the first year of the inten- sive trapping in southernmost Sweden) there has been no dramatic increase in the number of occupied stands. But the total population level has increased more than four times from 2012 to 2014 (especially considering the shorter trap- ping period in 2014). If this population increase continues a spread to more localities is probable.
It is a general trend for newly established spe- cies that it takes some time before they start to spread, as a result of a low colonization capac- ity when the population size is low, depending on e.g. mechanisms such as Allee effects (Tobin et al. 2011). Most beetles have been caught in four of the stands (including the eastern local- ity, the two southern localities where the spe- cies was first detected and one of the western localities): 95% in 2012, 100% 2013 and 96% in 2014. Thus, these areas probably have resident local populations. No more colonized standing trees have been recorded despite search for such trees in the trapping sites and colonized logging residues has only been found in the most eastern locality during one year (tops of cut larches), despite presence of such material in several of the sites.
The most plausible explanations for the es-
tablishment of T. gabrieli and I. cembrae in
Sweden are natural spread from Denmark and
imports of colonized larch timber. A natural
spread is most likely for the occurrences in
the western part of the province of Skåne. The
shortest distance between Sweden and Denmark
is less than 5 km over the sea and I. cembrae is
abundant in the neighboring region in Denmark
(Ravn 2012 b). It might even be that some of the
individuals caught in the traps are immigrants
from Denmark. The most eastern occurrence of
Figure 7. Larch stands in which Ips cembrae was surveyed with pheromone-baited traps, – a-d) represent different years.
Figures indicate the number of speciemens caught. The localities in the most southern province were included in 2011. The lines represent borders of Swedish counties and green areas forest.
Lärkbestånd med feromonfällor för fångst av lärkborre: – a-d) visar fångsten olika år. Siffror visar antalet fångade individer.
Svarta linjer är länsgränser och det gröna är skog.
a) 2009-2011 b) 2012
c) 2013 d) 2014
Ent. Tidskr. 136 (2015)
I. cembrae seems to be isolated from the other
ones and timber imports are a more probable way of introduction since it is situated within 3 km from a large port to which large quantities of timber have been imported.
For both T. gabrieli and I. cembrae a further spread northwards in Sweden will probably not be limited by the climate because the species are native in the Alps. Once established out- side its natural range T. gabrieli is considered as a potential pest species favored by dry and warm summers as well as larch being planted in suboptimal sites. I. cembrae is normally a secondary species colonizing dead or dying trees. But at high population density it may kill living trees. During outbreaks I. cembrae may also colonize young trees (Schimitschek 1931, Schwenke 1974, Grodzki 2008, Ravn 2012b).
Thus, it is important to continue to monitor the population development. Forest owners within the area of distribution should restrict the quan- tities of wind-felled or cut larch trees that are left in the forest over the summer including small- diameter material because the species can repro- duce in trunks and branches less than five cm in diameter (Schimitschek 1931).
Since 2005 five non-native species of bark beetles (two non-European and three European) have been found in Swedish forests except I.
cembrae (Lindelöw 2012). These species have been detected more or less by chance. Thus, most probably several more species remains to be detected and in addition an increasing num- ber of species can be expected to establish in the future. Our study demonstrates that systematic surveys are important for increasing the prob- ability of detection. As long as invasions do not result in high tree mortality, which often is the case also for aggressive species in the early phase of establishment, such species may remain unnoticed for many years (Bevan & King 1983, Shigesada & Kawasaki 1997, Poland & Mc- Gullough 2006). Ips cembrae in Sweden is such an example, without our study with pheromone- baited traps this species would most probably still not have been detected. The recent develop- ment of generic odor baits, that strongly attracts many different bark- and wood-boring insects, has provided us with an efficient method of de-
tecting bark- and wood-boring insect species (Rassati et al. 2014). Thus, a national net-work of traps at forest sites close to ports, or other localities receiving large quantities of imported goods, should be established. Early detection of invasive species increases the possibility of establishing appropriate measures before severe and more widespread damages may occur.
Acknowledgements
The study was financed by Environmental Monitoring and Assessment (Swedish University of Agricultural Sciences), Swedish Forest Agency and the Swed- ish Research Council for Environment, Agricultural Sciences and Spatial Planning (project 2010-1052).
Kjell Gustafsson and Elin Larsson (Sveaskog) pro- vided larch stands for the survey with cut trees, Claes Hellqvist and Henrik Nordenhem did most of the field work. The determination of Ips cembrae was kind- ly confirmed by Milos Knížek, Forestry and Game Management Research Institute, Czech Republic. A photo of I. cembrae was kindly provided by Göran Liljeberg.
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Svensk sammanfattning
Lärkbock och lärkborre - invandring av två möj- liga skadeinsekter på lärk till Sverige
Fram till nyligen har det i Sverige inte funnits några vedlevande insekter som primärt lever på lärk. Söder om vårt land finns dock både lärk- bock (Tetropium gabrieli) och lärkborre (Ips cembrae) som båda kan vara aggressiva på levande lärkträd. För att ta reda på om dessa ar- ter invandrat till vårt land gjordes ett experiment med fångstträd och feromonfällor.
På 17 platser i Götaland fälldes under 2009- 2011 lärkträd som fick ligga kvar över som- maren (Fig. 6). Kommande vår barkades träden och alla spår av skalbaggar identifierades till art.
Vedstycken med larver togs hem för kläckning.
I de fällda lärkträden påträffades lärkbock (Tet- ropium gabrieli) och nio andra skalbaggsarter (Tabell 1), varav den sextandade barkborren (Pityogenes chalcographus), tillsammans med lärkbock, var den vanligaste arten. Alla 89 indi- vider som kläcktes hemma var lärkbock.
Under 2009-2014 placerades plastfällor, be-
tade med feromon för att locka lärkborre ut i 7
hamnar och på 47 platser i lärkskog i Götaland
och Svealand. 2011 fångades totalt 18 exemplar
av lärkborre (Ips cembrae) i två närstående fällor
Ent. Tidskr. 136 (2015)
