Research Article |
Corresponding author: Dragos Cocos ( dragos.cocos@slu.se ) Academic editor: Andrea Battisti
© 2023 Dragos Cocos, Maartje J. Klapwijk, Martin Schroeder.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Cocos D, Klapwijk MJ, Schroeder M (2023) Tree species preference and impact on native species community by the bark beetle Ips amitinus in a recently invaded region. In: Jactel H, Orazio C, Robinet C, Douma JC, Santini A, Battisti A, Branco M, Seehausen L, Kenis M (Eds) Conceptual and technical innovations to better manage invasions of alien pests and pathogens in forests. NeoBiota 84: 349-367. https://doi.org/10.3897/neobiota.84.86586
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Non-native bark beetle species represent a major threat to forest ecosystems. The bark beetle Ips amitinus has recently expanded its range from Finland into northern Sweden. In the present study, we asked the following questions: (i) What is the distribution status in Sweden? (ii) Is there a difference in preference and reproductive success between Norway spruce and Scots pine? (iii) How common is the species after range expansion and does it influence the native community of bark- and wood-boring beetle species?
We established the presence of I. amitinus and co-existence with the native community through checks of logging residues at 382 localities in northern Sweden. In addition, attack densities and reproductive success were compared between spruce and pine through investigating field material and by a no-choice rearing experiment.
We found that I. amitinus is distributed over large parts of northern Sweden. Within its distribution area, it was found in 58% of all checked localities. It is one of the most common bark beetle species in logging residues and a higher proportion of Norway spruce objects compared to Scots pine were colonised. Attack density and reproductive success were higher in Norway spruce in field material and in the rearing experiment. There was no significant difference in the number of native bark- and wood-boring beetle taxa between localities where I. amitinus was present or absent.
community ecology, ecological impact, invasion range, small spruce bark beetle, species interactions
Non-native forest pests present a major threat to forest ecosystems globally (
One example of the second type of range expansion is the bark beetle Ips amitinus (Eichhoff, 1872). The distribution of I. amitinus ranges from the mountainous regions of central and south-eastern Europe to France, Belgium and The Netherlands to the West (
In the present study, we assessed the distribution range of I. amitinus in Sweden, its performance in Norway spruce (Picea abies L. Karst) and Scots pine (Pinus sylvestris L.) and its influence on the native community of bark- and wood-boring beetles. Ips amitinus reproduces in both Norway spruce and Scots pine (
Although range expansions have been documented for several bark beetle species (
We asked the following questions for I. amitinus: (i) What is the current distribution in Sweden? (ii) Is there a difference in preference and reproductive success between Norway spruce and Scots pine? (iii) How does the presence of the invading species influence the native community of bark- and wood-boring beetle species?
The study consists of: (1) a survey of I. amitinus in northern Sweden to assess its current distribution, commonness, host tree preferences and potential impact on native bark- and wood-boring beetle species, (2) investigation of naturally colonised material for assessing colonisation density and reproductive success and (3) a rearing experiment comparing I. amitinus reproductive success in Norway spruce and Scots pine (hereafter spruce and pine).
To assess the current distribution of I. amitinus in Sweden, we conducted two surveys in the counties of Norrbotten and Västerbotten in northern Sweden. Norrbotten is bordering Finland from where the species is expected to have spread. When the species were found in large parts of Norrbotten, we continued the survey further south in Västerbotten to find the southern range limit (Fig.
Numbers of the five types of locations surveyed for presence of Ips amitinus. The first survey was conducted in 2016–2017 and the second in 2018–2019.
Year | Total no. localities | Location type | ||||
---|---|---|---|---|---|---|
Clear-cut | Along Road | Stand | Thinning | Power lines | ||
2016 | 12 | – | 10 | – | 1 | 1 |
2017 | 153 | 45 | 63 | 12 | 20 | 13 |
2018 | 118 | 100 | – | – | 18 | – |
2019 | 99 | 92 | – | – | 7 | – |
Numbers of spruce and pine objects and of each of the five types of objects, surveyed in the first (2016–2017) and second (2018–2019) survey.
Year | Tree species | Type of objects | Total no. objects | |||||
---|---|---|---|---|---|---|---|---|
Spruce | Pine | Tops | Branches | Logs | Small trees | Large trees | ||
2016 | 11 | 10 | – | – | 2 | 5 | 14 | 21 |
2017 | 831 | 873 | 499 | 23 | 100 | 988 | 95 | 1705 |
2018 | 2255 | 1216 | 1470 | 31 | 114 | 1815 | 42 | 3472 |
2019 | 2981 | 2301 | 3407 | – | – | 1875 | – | 5281 |
A locations checked for presence of Ips amitinus in northern Sweden in 2016 – 2019. Red symbols = presence and blue symbols = absence. Green symbol = first record in 2012. 2016 = pentagon, 2017 = diamond, 2018 = triangle and 2019 = circle. Umeå (63°49.877'N, 20°15.651'E) B Ips amitinus southern distribution limit in 2017, 2018 and 2019 in northern Sweden. Localities are with (red symbols) and without (blue symbols) findings of I. amitinus in the surveys. Diamond symbols represent the 2017 survey, triangle – 2018 and circle - 2019 survey. Black horizontal lines denote the most southern location with I. amitinus for each year. The distance from the first find in 2012 (green circle in Fig.
In 2016, the survey focused on confirming the establishment of I. amitinus in Sweden. Trap logs of spruce and pine were cut close to the location of the first discovery in Sweden in 2012. Material such as wind-felled trees, found while driving between the trap log locations, was inspected as well. In 2017, the survey focused on establishing the presence of I. amitinus along the Finnish border, the assumed entry of the species to Sweden (
In the second survey (conducted in the summers of 2018–2019), we adjusted the survey methodology, based on experience gained in the first survey and only included clear-cuts and thinnings harvested during previous winter (between October and March) (Table
For each inspected object during the second survey, we also recorded the presence of other (native) bark beetle species and other bark- and wood-boring beetles. Species identification was based on adults and gallery systems (
Field-collected colonised material was used to assess I. amitinus performance in spruce and pine. The material was collected between 21 and 26 May 2018, prior to emergence of offspring resulting from colonisation earlier in spring (no exit holes present), from seven clear-cuts harvested during the previous winter. Most of the collected material were spruce tops and small spruce trees (60 objects from 7 clear-cuts), but also some small pine trees were collected (11 objects from 2 clear-cuts) (Table
Number, mean length and diameter of naturally colonised objects used for evaluating the performance of Ips amitinus in Norway spruce and Scots pine.
Tree species | No. objects | Length (cm) | Range | Diameter (cm) | Range |
---|---|---|---|---|---|
Mean ± SE | Mean ± SE | ||||
Norway spruce | 60 | 61.67 ± 0.51 | 48–70 | 8.9 ± 0.4 | 4–15.5 |
Scots pine | 11 | 56.54 ± 1.95 | 41–61 | 12.4 ± 0.41 | 11–15.5 |
The objects were grouped by tree species and location before being placed in separate emergence cages (seven cages with spruce and two cages with pine) in a climate chamber (20 °C, 20 hours day length). When adult emergence had ceased, we recorded for each object, diameter, length, I. amitinus attack density (number of male entrance holes and maternal galleries per mantel area) and number of maternal galleries per mating chamber. Emerging I. amitinus were collected daily from cages and stored in boxes with moist paper at 5 °C to be used later in the rearing experiment (see below).
We used the I. amitinus adults reared from the naturally colonised spruce and pine for a no-choice experiment with stem sections of spruce and pine. From seven spruce and five pine trees, a 60 cm long stem section was cut (at 3 m from the base of the trees) between 9 and 10 July near Uppsala. The diameter of the stem sections was 17.6 ± 0.4 cm (mean ± SE) and they were stored at room temperature for 48 hours after which cut surfaces were waxed to prevent desiccation. Subsequently, the stem sections were stored at room temperature for another 24 hours before being moved to a climate chamber (20 °C, 20 hours day length). Each section was placed standing in a separate cage (70 × 53 × 50 cm). The following day, 90 I. amitinus adults were released into each cage. All reared beetles were mixed together prior to release. As colonisation success was deemed insufficient (based on amount of boring dust), an additional 70 adults were released into each cage after three days. Low vitality adults (slow in movement) were discarded prior to release.
All dead beetles were collected from each cage prior to the emergence of the new generation. These dead beetles were parent beetles that left the stem section after mating and egg laying, in addition to beetles that never entered the logs. The emerging offspring were collected daily and colour-classified during the first weeks to ensure that they were not parent beetles (darker). After emergence ended, density and length of I. amitinus maternal galleries, number of maternal galleries per mating chamber and number of male entrance holes were recorded. We also noted the success or failure of maternal galleries, based on presence (success) and absence (failure) of larval galleries.
All statistical analyses were performed in R, version 2021.09.2 (
All data collected during the surveys from 2016 to 2019 were used to calculate the distribution area. The speed of range expansion was calculated using the latitudinal difference between the most southern record for each survey year, from 2017 to 2019. During the 2018 and 2019 survey, we checked 13.5% and 13%, respectively, of all fresh clear-cuts along the yearly southern distribution limit (on an approximate 66 × 10 and 65 × 12 km area).
For analysis of observational data from the second survey, we used generalised linear mixed models with a binomial error distribution (glmer, lme4 package;
To assess I. amitinus performance in the field-collected material, we used attack density per m2 of bark (two measures: male entrance holes and maternal galleries), reproductive success (number of daughters per maternal gallery) and the number of offspring produced per m2 bark area as the response variables. Cage was the level of replication for the reproductive success. The attack densities were recorded for each object (level of replication). We used a linear model with the explanatory variable tree species (two levels: spruce or pine). We used Levene’s test to check for homogeneity of variance in the residuals (LeveneTest; car-package). When the model assumption of homogeneity of variance was violated, the response variable was log-transformed (natural logarithm), to comply with model assumptions.
We performed the same analyses for the no-choice rearing experiment. One spruce log was excluded from the analysis because of lack of reproductive activity. We used the same response variables, which we calculated in the same way, as for the field-collected material.
To assess the co-occurrence of I. amitinus with the native species, we used manyglm model (mvabund package;
Ips amitinus was found in 184 out of 382 inspected localities in the years 2016–2019. North of its southern distribution limit, the species was recorded in 57.9% of all checked localities during the four-year study. Our observations show that the species is presently distributed from the border of Finland in the north-eastern part of the Province of Norrbotten (67°29.915'N, 23°17.330'E) and south to the northern part of the Province of Västerbotten (65°11.628'N, 20°46.218'E) (Fig.
Based on the yearly surveys, we found that the estimated speed of expansion varied yearly from 17 km from 2017 to 2018 and 11 km from 2018 to 2019, suggesting an average range expansion of 14 km per year (Fig.
The average proportion of objects colonised by I. amitinus per occupied locality was 16.6 ± 1.9% in 2018, ranging from 3% to 57% and 11.6 ± 1.2% in 2019, ranging from 3% to 37%. Ips amitinus was not detected in any of the 64 localities checked south of the 2019 distribution limit. No overwintering adults were found under bark in colonised substrates in any of the 33 clear-cuts (79 attacked objects) that were colonised in 2018 and checked in early spring 2019.
Ips amitinus was present in 23.4% (376 colonised objects) of sampled spruce tops and small trees in 2018 and 16.2% (236 colonised objects) in 2019, within its distribution limit. The colonisation rate in pine was lower in both 2018 (3.0%, 25 colonised objects) and 2019 (0.2%, two colonised objects). The interaction between tree species and object type indicated that, for pine, I. amitinus prefers small trees compared to tops, whereas for spruce, no clear difference was detected (Fig.
Anova (type III test; Anova; car-package) and estimates for the generalised linear mixed effects model testing the effect of tree species, object type, number of other bark beetle taxa and diameter on I. amitinus colonisation probability. The Table shows the final model with the chi-squared value, degrees of freedom (df), estimates and the standard error of the mean (SE). The standard deviation for intercept (for the random effects) is given as well. The variables printed in bold are significant at p < 0.05. The intercept represents the overall mean. Values were obtained by using sum contrasts, as we wanted to compare the intercept to the overall mean.
Response | Explanatory | X² | df | Est | SE | P | Random effects: Site, Year | |
---|---|---|---|---|---|---|---|---|
Std. dev. | Intercept | |||||||
Site | Year | |||||||
I. amitinus | Intercept | 312.88 | 1 | -6.20 | 0.35 | <0.0001 | 0.96 | 0.10 |
colonisation | Tree species (pine) | 164.45 | 1 | -1.74 | 0.14 | <0.0001 | ||
Object type (small tree) | 0.12 | 1 | 0.06 | 0.18 | – | |||
Other bark beetle taxa | 0.76 | 1 | -0.10 | 0.12 | – | |||
Diameter | 127.39 | 1 | 0.31 | 0.03 | <0.0001 | |||
Tree species (pine) × Object type (small tree) | 25.02 | 1 | 0.66 | 0.13 | 0.0001 | |||
Object type (small tree) × Other bark beetles | 10.21 | 1 | 0.36 | 0.11 | 0.001 |
The probability of attack between the two different tree species and object types, based on the results from the 2018 and 2019 survey. The central lines of the box plot represent the median, the box indicates lower and upper quartiles and the whiskers represent the largest and smallest observations that fall within 1.5 times the box size from the nearest quartile. Black circles represent outliers.
The interaction between object type and the number of other bark beetle taxa present indicates that, in small trees, the presence of more species is associated with a higher probability of colonisation by I. amitinus. We found a positive significant relationship with object diameter independent of object type (0.31 ± 0.03; X2 = 127.39, p < 0.0001) and this relationship is also independent from other explanatory variables (Table
Attack density, expressed as density of male entrance holes per m2 of bark (F1,69 = 8.261, p = 0.005; Fig.
However, there was no significant difference in the number of maternal galleries per mating chamber between spruce (3.08 ± 0.08) and pine (3.27 ± 0.26; F1,69 = 0.267, p = 0.61). Reproductive success, expressed as number of daughters per mother (i.e. per maternal gallery), was significantly higher in spruce (4.53 ± 0.70), compared to pine (1.90 ± 0.06; F1,7 = 5.369, p = 0.05). In addition, the number of offspring produced per m2 was significantly higher in spruce (1447 ± 469) compared to pine (328 ± 96), (F1,7 = 5.056, p = 0.05). Maternal gallery length was significantly longer in pine (11.97 ± 0.78 cm) compared to spruce (8.92 ± 0.28 cm; F1,69 = 16.88, p = 0.0001). The density of I. amitinus male entrance holes did not differ between the pine objects with and without the bark beetle Tomicus piniperda (L.) (F1,9 = 3.006, p = 0.11). However, the density of I. amitinus maternal galleries per m2 was more than two-fold higher within pine when T. piniperda was absent (108 ± 27), compared to when both species were present in the same object (47 ± 7.6; F1,9 = 5.379, p = 0.04). No living adult I. amitinus beetles were found under the bark at the end of the rearing of naturally colonised material though a few dead individuals were found.
The density of male entrance holes per m2 of bark was significantly higher in spruce compared to pine (F1,9 = 5.155, p = 0.05; Fig.
The results from the no-choice rearing experiment with Ips amitinus. Male entrance holes per m2 bark (A), maternal galleries per m2 bark (B), reproductive success (log transformed), (C) and number of offspring produced per m2 bark (D). Means with different lowercase letters are significantly different at p < 0.05. There were six replicates for Norway spruce and five for Scots pine.
Maternal gallery length did not differ between the pine and spruce (13.8 ± 5.6 cm for spruce and 10.6 ± 4.7 cm for pine, F1,9 = 1.93, p = 0.19). We did not find a difference in the number of maternal galleries per mating chamber, between spruce and pine (2.4 ± 0.2 and 2.1 ± 0.3 respectively, F1,9 = 1.291, p = 0.28). The emergence time of the new generation did not differ between the two tree species. No adult beetles remained under the bark at the end of the experiment.
A total of 16 native bark beetle, weevil and long horn beetle species/taxa were recorded in the study (Suppl. material
Ips amitinus was the third most common species colonising the inspected wood objects within its distribution limit. When looking at only spruce objects, I. amitinus was the second most common species and, on only pine objects, the fourth most common species (Suppl. material
In this study, we set out to establish the range distribution of I. amitinus in Sweden and the preferred tree species and host material used in the new range. We found that I. amitinus has expanded its range south approximately 200 km over land from the Finnish border (Fig.
Due to the lack of I. amitinus records around Umeå (Fig.
In earlier studies, spruce has been recorded as breeding material more often than pine (
To our knowledge, this is the first study to show that both I. amitinus preference and performance are highest in spruce within its invaded range. In the native range,
Our surveys show that I. amitinus is one of the most common bark- and wood-boring species in fresh logging residues, even though the species has most probably only been present for a rather short time (See
We find that the community of bark boring insects in spruce is not different when I. amitinus is present or absent (Fig.
The significant difference observed for T. piniperda, in relation to the presence of I. amitinus, might be explained by the earlier flight period for T. piniperda than for I. amitinus. The earlier flight period will give T. piniperda the opportunity to colonise breeding material before I. amitinus, potentially leading to competitive exclusion of I. amitinus.
As our study merely scratches the surface of potential ecological effects of I. amitinus invasion, we see a need for more detailed studies into the effects on reproductive success and enemy pressure on I. amitinus and its community. We expect that the space available for brood production on logging residues by native species have been reduced to some extent, especially since only a small proportion of the inspected objects were not colonised and some of these may have been too dry or in some other way unsuitable for native bark beetle colonisation. Our observations strongly suggest that I. amitinus will continue expanding its range south in Sweden.
In conclusion, the range expansion of I. amitinus in Sweden does not appear to markedly affect the native community of bark- and wood-boring insects. In areas where pine is dominating, the invasion success of I. amitinus might be slowed down because of its lower reproduction success and stronger competition with T. piniperda. The low impact of I. amitinus in its invaded range might be related to the similarities with the community in its native range. Future studies of and comparisons with other species expanding into a naïve range and potential host switching will be needed to understand the importance of this similarity.
The forest company SCA provided information about clear-cuts and thinnings for the survey. Jan ten Hoopen helped with fieldwork, Åke Lindelöw confirmed the correct identification of I. amitinus adults. Andrew (Sandy) Liebhold improved earlier drafts of the manuscript by providing useful discussion and comments.
Ips amitinus description, table S1
Data type: pdf file
Explanation note: Ips amitinus adults were collected for identification in the laboratory when possible. Ips amitinus differ from other Ips species present in Sweden by a shiny declivity at the back of the elytra (Knižek 2001; Nierhaus-Wunderwald and Forster 2004; Åke Lindelöw, pers. communication). The gallery system is highly characteristic for the species. It has a very large nuptial chamber in the late stages, as the male usually attracts between two and seven females. The mother galleries often start away from the direction of the wood fibre, then turn after about one centimetre and continue along the wood fibre in a rather windy way. The gallery system could be confused to other bark beetles in the early stages (like Orthotomicus spp.), but it is rather specific in the later stages (for a visual comparison, see Knižek 2001); table S1. Percentages of localities and wood objects colonised by bark- and wood-boring beetle taxa north and south of the Ips amitinus 2019 southern distribution limit. The number of colonised localities and objects is given within parenthesis. Species were ordered, based on the percentage (and number) of colonised localities north of Ips amitinus distribution limit. Taxonomic group: B = bark beetle; L = longhorn beetle; W = weevil (except bark beetles). Host tree: S = Norway spruce; P = Scots pine. The percentage of colonised objects is calculated, based on the number of objects from their host tree species.