# Reduction of damage by the exotic invasive conifer seed bug Leptoglossus occidentalis in mixed pine-birch plantations: A case of biotic resistance

Ana Farinha, Bastien Castagneyrol, Inge van Halder, Manuela Branco, Céline Meredieu, Hervé Jactel

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## To cite this version:

Ana Farinha, Bastien Castagneyrol, Inge van Halder, Manuela Branco, Céline Meredieu, et al., Reduction of damage by the exotic invasive conifer seed bug Leptoglossus occidentalis in mixed pine-birch plantations: A case of biotic resistance. Forest Ecology and Management, 2024, 569, pp.122193. 10.1016/j.foreco.2024.122193. hal-04792767

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# Reduction of damage by the exotic invasive conifer seed bug *Leptoglossus occidentalis* in mixed pine-birch plantations: A case of biotic resistance

Ana Farinha<sup>a</sup>, Bastien Castagneyrol<sup>b</sup>, Inge van Halder<sup>b</sup>, Manuela Branco<sup>a</sup>, Céline Meredieu<sup>b</sup>, Hervé Jactel<sup>b,*</sup>

## ARTICLE INFO

Keywords:

Biodiversity

Associational resistance

Non-native pest

Pinus pinaster

Betula pendula

## ABSTRACT

The number of invasive non-native pests is increasing rapidly in forests as a result of global change. It is therefore important to prevent their damage in order to preserve the integrity of forest ecosystems and the associated services. According to the biotic resistance hypothesis, species-rich communities are less likely to be invaded. The associational resistance hypothesis states that insect herbivores are more likely to colonise and exploit plants surrounded by conspecific neighbours than heterospecific, non-host plant species. More diverse forests would therefore be less damaged by non-native pests than tree monocultures. We tested these hypotheses by comparing the damage caused to seeds by the western conifer bug *Leptoglossus occidentalis*, an invasive insect native to North America, in plots of pure maritime pine and mixed plots of maritime pine and birch. These plots were in two tree diversity experiments in Europe. Mixed pine plots differed in terms of pine density (1250 versus 625 pines/ha), proportion of pine and birch (25 %, 50 %, 75 %) and spatial mixing pattern (aggregated versus dispersed). We sampled 635 cones in 37 plots. Overall, the proportion of seeds damaged by the invasive bug was significantly lower in mixed plots than in pure pine plots at both experimental sites. There was no significant effect of pine density or relative proportion in the mixtures on seed damage. Aggregated pines in the mixed plots were significantly more damaged than dispersed pines, suggesting that bugs may have done less damage when they had more difficulty locating their host trees. This is consistent with the hypothesis of lower plant apparency. These results support the view that forest plantations of mixed species, which are known to be less vulnerable to attack by native insects, may also be more resistant to infestation by exotic insects. Row-wise, intimate mixtures of two species represent a promising option for designing tree plantations that are more resistant and easier to manage.

## 1. Introduction

Biological invasions are one of the worst threats to biodiversity and ecosystem functioning (Boyd et al., 2013), causing considerable economic losses in direct control costs or indirect losses of services provision (Zenni et al., 2021). In forests, the rate of arrival and establishment of new invasive species is showing an exponential increase in most continents (Brockerhoff and Liebhold, 2017; Roques et al., 2020). This flow is clearly linked to the continuing increase in trade across biogeographic boundaries, particularly through the transport of plants for planting and the use of wood for packaging (Meurisse et al., 2019). In spite of the implementation of international phytosanitary regulation measures, the thousands of containers arriving every day in the major

cargo ports represent such a quantity of items to be controlled that it may seem illusory to hope to stop or slow down the arrival of these non-native species. It is therefore also important to consider methods of preventing their damage once they have established themselves in new forests. In this context, the biotic resistance hypothesis posits that species-rich communities are less likely to be invaded (Elton, 2020; Kennedy et al., 2002). Plant communities with high species richness would provide fewer vacant niches for invasive plant species, and their higher primary productivity would reduce the resources available for incoming species, while a higher diversity of herbivores could further reduce the fitness of non-native plant species (Tilman, 2004). At the higher trophic level, invasive species of herbivores would also be less able to develop in more diverse communities because of the lower

<footnote><sup>a</sup> Forest Research Centre, Associate Laboratory TERRA, School of Agriculture, University of Lisbon, Portugal</footnote>

<footnote><sup>b</sup> INRAE, University of Bordeaux, BIOGECO, F-33610, Cestas, France</footnote>

<footnote>* Corresponding author.</footnote>

<footnote>E-mail address: herve.jactel@inrae.fr (H. Jactel).</footnote>
density of suitable host plants and greater predator pressure. There is thus a strong convergence between this theory and the hypothesis of associational resistance (Barbosa et al., 2009), which states that herbivores are more likely to colonize and exploit plants surrounded by conspecific neighbours than by heterospecific, non-host plant species. This theory has received solid support in the case of forest ecosystems, with a meta-analysis of more than 600 cases showing that the damage of a given pest species on a given tree species is significantly lower when that species is managed in mixed stands than in pure stands (Jactel et al., 2021). However, this dataset included only three examples of non-native species, Lymantria dispar (Brown et al., 1988), Matsucoccus feytaudi (Jactel et al., 2006) and Drycosmus kuriphilus (Guyot et al., 2015; Fernandez-Conradi et al., 2018), making it difficult to generalize the principle of associational resistance to exotic pests in forests and by extension to confirm the biotic resistance hypothesis (Nunez-Mir et al., 2017).

One of the main mechanisms underlying the principle of associational resistance is that mixed forests harbour a greater abundance and diversity of natural enemies of insect herbivores than do pure forests (Stemmelen et al., 2022) and thus may benefit from better biological control by these predators and parasitoids. However, for this process of top-down regulation to work effectively on exotic insects and contribute to biotic resistance, it is expected that the exotic insects are phylogenetically close enough to the native insects that their specialized enemies can easily switch to these new hosts, or that the natural enemies are generalists enough to be able to attack new prey unrelated to the local prey (Carlsson et al., 2009), such as insectivorous birds (Vázquez-González et al., 2024). The first case was documented with Matsucoccus feytaudi, the invasive maritime pine bast scale in Corsica whose populations are better regulated in mixed stands with black pine because the latter is attacked by the indigenous scale *Matsucoccus pini* which serves as an alternative prey for the bug predator *Elatophilus nigricornis* (Jactel et al., 2006). The second case could be that of generalist predators such as insectivorous birds as shown by the regulation of exotic spiders in Hawaï (Gruner, 2005).

A second mechanism underlying both associational and biotic resistance is the decrease in the amount of host plants (resource concentration hypothesis) in mixed forests, limiting the ability of insect herbivores to exploit them for feeding and reproduction. A previous study showed that not only is the decrease in the proportion of host trees important in explaining the better resistance of mixed forests, but also the phylogenetic distance between host and non-host trees in the mixture (Castagneyrol et al., 2014), which has been recently confirmed (Gougherty and Davies, 2024). It is therefore plausible that the effect of this phylogenetic diversity is even greater for exotic insects, as they are less likely to have co-evolved with the native non-host tree species present in the mixture, and are therefore less able to recognise them as unsuitable for their development (Bertheau et al., 2010). Dilution of the host tree resource in mixtures with non-host trees not only reduces the amount of breeding substrate and thus the carrying capacity of mixed forests, it also makes it qualitatively more difficult for insect herbivores to locate and colonize host trees. In particular, several studies have shown that the vicinity of non-host trees reduces the apparentness of visual masking if the neighbour is taller (Castagneyrol et al., 2013) or through disruption of insect olfactory tracking when non-host volatiles are released (Jactel et al., 2011). Again, it is expected that the volatile organic compounds emitted by native non-host species will be even more disruptive to the foraging behaviour of non-native insects that have not coevolved with them in principle. However, the reverse could also happen; the bouquet of odours released by non-host native species could have no behavioural effect on invasive insect species due to the absence of coevolution.

However, interpretation of the outcomes under the resource con-
centration theory is not straightforward as studies have suggested that
variables such as the number of host plant (absolute density – number of
host plant per ha) and/or the proportion of host plant (relative density:

number of host plants to the total number of host and non-host plants) affect the results and thus need to be accounted for (Kim and Underwood, 2015). The absolute density (abundance) of the host may influence the quantity of food and breeding substrate for herbivores, thus increasing the likelihood of their damage (host concentration effect). The relative density of non-host plants may, in turn, reduce or increase the ability of herbivores finding host plants (Associational resistance or susceptibility hypothesis).

In this study we used the recently introduced Western Conifer Seed
Bug *Leptoglossus occidentalis* (hereafter called WCSB) in Europe as a new
opportunity to address the biotic resistance hypothesis and investigate
some of its underlying ecological mechanisms. We estimated the damage
inflicted on *Pinus pinaster* seeds in two tree diversity experiments having
in common the concomitant presence of pure plots of maritime pine and
mixed plots of maritime pine and birch, both native species of the re-
gion. Furthermore, in these experimental plantations, we manipulated
the absolute and relative density of hosts (pines) compared to non-hosts
(birches), while the trees were all the same age and genetic origin. Our
objective was to test the following hypotheses: 1) the proportion of seeds
damaged by the exotic bug was lower in mixed stands than in pure
stands of maritime pine; 2) the level of damage increased with the local
abundance of trees of the host species (resource concentration hypoth-
esis); 3) the level of seed damage decreased with increased proportion of
non-host birch trees (reduced host pine apparenty hypothesis). In doing
so our study aimed at designing mixed species plantations more resistant
to exotic forest pests.

2. Methods

2.1. Experimental sites

Damage to seeds by WCSB was assessed by collecting cones of
maritime pine in two different experimental sites, ORPHEE and its
demonstration trial ORPHEE-SO, in the southwestern region of France
during the year of 2020. The tree mixture that was investigated was the
same in both sites, the maritime pine (Pinus pinaster Ait.) and the silver
birch (Betula pendula Roth). Climate was similar in both sites, charac-
terized by a mean annual temperature of 13.4 °C and mean annual
precipitation of 997 mm and the soil was also similar, a sandy podzol on
sandstone bedrock.

2.1.1. Study site ORPHEE

ORPHEE is a tree diversity experiment (https://sites.google.com/vie
w/orpheeexperiment/home), belonging to the global network Tree-
DivNet (https://treedivnet.ugent.be/). Established in 2008 on a clear-
cut area (44°44′24.9″N; 0°47′48.1″W), it consists of 8 blocks (block
area of 1.28 ha) each with 32 randomly distributed plots of all the
possible combinations of one to five of the following tree species:
maritime pine (Pinus pinaster), silver birch (Betula pendula), pedunculate
oak (Quercus robur), pyrenean oak (Quercus pyrenaica) and green oak
(Quercus ilex). Plots are 20 m x 20 m large, and the planting distance
between two trees is 2 m. Thus, 100 trees were planted per plot (2500
trees per ha). Plots are 3 m apart from each other and separated by a
regularly mowed grass strip. Mixed plots were planted following a
substitutive design with a regular alternate pattern (Damien et al.,
2016). Half of the blocks are irrigated daily from May to October with
42 m³ of water (i.e. 3 mm precipitation per plot of 400 m² area) in order
to reduce the summer water stress in comparison with the non-irrigated
ones (Maxwell et al., 2020). Both pine (11.84 ± 0.04 m, mean ± stan-
dard error of tree height) and birch (9.39 ± 0.07 m) trees were much
taller than the Quercus species (2.45 ± 0.03 m) at the time of the survey.
Thus, we considered oaks as part of the understory vegetation of the
plots (mainly fern, gorse and heather). In this sense, mixtures of pines
and oaks were considered pine monocultures, and mixtures of pines,
birches and oaks were considered pine-birch mixtures.

For our objectives we used 6 blocks (3 irrigated and 3 not irrigated).
In each block we selected 4 plots to independently test the effects of mixture and host absolute density (abundance). We selected plots with the relative density (proportion) equal in mixtures, with always 50 % of pine and 50 % of birch. We therefore sampled one "pure" plot of maritime pine with 50 pines (plot composition of 50 pines and 50 small oaks; density of 1250 pines/ha) and one mixed plot with 50 pines and 50 birches (density of 1250 pines/ha), and one "pure" plot of maritime pine with 25 pines (plot composition of 25 pines and 75 small oaks; density of 625 pines/ha) and one mixed plot with 25 pines and 25 birches (plot composition of 25 pines, 25 birches and 50 small oaks; density of 625 pines/ha), for a total of 24 plots analysed.

### 2.1.2. Study site ORPHEE-SO

The experimental site ORPHEE-SO was established in 2013 in South-Western France (44°14'14.2"N; 0°36'59.7"W) as a demonstration trial of ORPHEE to provide an operational scale application of mixed pine and birch plantations for the local forestry sector. Different types of pine and birch association were evaluated by varying both the proportion of each species and their spatial distribution in the plot, in a complete factorial design. Pine relative density (proportion) varied from 0 % (pure birch plots), to 25, 50, 75 and 100 % (pure pine plots). The spatial distribution of the two species in the demonstration plots were of two types: "dispersed" with alternate rows and "aggregated" with alternate strips of several rows (see Fig. 1 for details). This trial consisted of 2 blocks, each with 8 randomly distributed rectangular plots of 4800 m² (Fig. 1.). Trees were planted at a density of 4 m x 2 m (1250 trees/ha) which corresponds to the classic management density for maritime pine in mono-specific plantations in the region.

## 2.2. Insect model

Native to Western North America, the Western Conifer Seed Bug *Leptoglossus occidentalis*, 1910 (Hemiptera: Coreidae) (WCSB) has a successful and rather recent history of invasion in Europe which started

in Italy in 1999 (Taylor et al., 2001). About 20 years later, it can be found in virtually all of Europe, North Africa and Asia (Lesieur et al., 2014). It feeds on seeds of many coniferous species (from genera Pinus, Picea, Abies, Cedrus, Tsuga and Pseudotsuga) quickly adapting to new hosts species when expanding its geographic range. While feeding, the bug damages the seeds of both developing and mature pine cones. The damage caused by WCSB has serious negative impacts for the productivity of seed orchards and the pine nut market in Southern Europe (Farinha et al., 2021).

## 2.3. Cone and seed sampling

A sample of 20 matured cones (second-year cones) from a minimum of five trees was randomly collected per plot in February - March 2020 when the cones were still closed with the seeds inside. Trees were preferably sampled in the central area of the plots to avoid the edge effect. The total number of mature cones available per plot was estimated by visual counting on all trees in the ORPHEE site. All collected cones were weighed, dried (at 35°C until opening) and their seeds extracted manually. Coated seeds were separated by weight between full and damaged using a wind machine optimized for *P. pinaster* seeds, then counted, and weighed. A subsample of 400 seeds per plot was x-rayed to categorize and quantify the proportion of damaged seeds assigned to WCSB feeding following the protocol in Farinha et al., 2018. Of the three damage categories, damage type I (seed with endosperm partially damaged) and type II (seeds with endosperm present but totally consumed) can be attributed to the bug feeding but not damage type III (absence of embryo, unfertilized seed) (Farinha et al., 2018). A preliminary analysis of all seeds submitted to x-ray using Kruskal-Wallis test showed that the proportion of seeds with damage type III was not different between mixed and pure plots (d = 0.040922, df = 1, p-value =0.8397), between pine densities (d = 0.2138, df = 1, p-value =0.6438) or irrigation regimes (d = 2.1722, df = 1, p-value =0.1405). The overall average value of damaged type III seeds was only 3.55 ± 0.44 % of all

<figure><img src="image_4.png" /><figcaption>**Fig. 1.** Field diagram of site ORPHEE-SO: 1) pure maritime pine (green); 2) pure birch (yellow); 3) 25 % pine + 75 % birch aggregated; 4) 25 % pine + 75 % birch dispersed; 5) 50 % pine + 50 % birch aggregated; 6) 50 % pine + 50 % birch dispersed; 7) 75 % pine + 25 % birch aggregated; 8) 75 % pine + 25 % birch dispersed.</figcaption></figure>
damaged seeds per plot. With the proportion of seeds with damage type III consistent between treatments all seeds separated by the wind machine as damaged were pooled together for the insect damage analysis in this study.

## 2.4. Statistical analysis

Due to differences in the design of the two sites sampled, ORPHEE and ORPHEE-SO, it was not possible to merge the data and the analysis was performed at each site. The plot was the statistical unit for all tests. All statistical analyses were performed using R Studio (version 1.4.1717 with R version 4.1.1), and were considered significant at *p* < 0.05.

### 2.4.1. ORPHEE: testing the effects of tree diversity and host pine density

The effect of tree diversity (pure maritime pine vs mixture of birch and maritime pine) and pine absolute density (1250 vs 625 pine trees per ha) were investigated together in a generalised linear mixed model (GLMM) using Template Model Builder ('glmmTMB' package, version: 1.1.2, published 2021-09-20), a beta binomial distribution and the maximum likelihood for parameter estimation. The response variable was the proportion of damaged seeds (number of damaged seeds per total number of seeds) per plot. The model had tree diversity (pure vs. mixed), pine density (1250 pines/ha vs. 625 pines/ha) as fixed factors, the number of cones as covariate (to take account of possible foraging behaviour depending on resource density), and block as random factor. The number of cones per plot was significantly higher in irrigated plots than in non-irrigated plots (p = 0.0009). We therefore did not include "irrigation" as an additional fixed factor in the model in order to avoid problems of collinearity. Residuals were checked using the 'DHARMa' package (v0.4.3) a simulation-based approach for glmmTMB models.

### 2.4.2. ORPHEE-SO: testing the effects of tree diversity, host pine proportion and mixing pattern

In ORPHEE-SO, the tested model was a generalised linear mixed model (GLMM) using the same procedure ad for the ORPHEE site, with tree diversity (mixture of birch and maritime pine vs pure pine), relative

pine proportion in the mixture (25 %-50 %-75 %-100 %), intermingling pattern of mixed species (aggregated vs. dispersed) as fixed factors and block as random factor. The response variable was the same as for ORPHEE site: the proportion of damaged seeds per plot.

The mixed plot in ORPHEE-SO with a relative density of 75 % pine and an aggregated distribution pattern was removed from the analysis due to heavy fungal attack, resulting in a low number of extractable seeds and confounding effects on the subsequent categorization of seed damage.

## 3. Results

In total we sampled 37 plots (ORPHEE: 24; ORPHEE-SO: 13) and collected 635 cones (ORPHEE: 387; ORPHEE-SO: 248; Table 1) corresponding to 41 778 seeds analysed (ORPHEE: 26 482; ORPHEE-SO: 15 296).

### 3.1. Effects of pine - birch mixtures on seed damage

#### 3.1.1. ORPHEE site

In the experimental site ORPHEE the mean proportion of damaged seeds in the mixed plots was 22.77 ± 1.87 and in pure plots, was 28.38 ± 2.19. The results from the GLMM model showed that tree diversity was the only significant factor explaining the variation in seed damage between plots (tree diversity: p=0.028; pine density: p=0.175; number of cones: p=0.095; SM1) with mixed plots showing a lower proportion of damaged seeds (Fig. 2).

#### 3.1.2. ORPHEE - SO site

In the experimental site ORPHEE-SO the mean proportion of damaged seeds in the mixed plots was 46.11 ± 2.41 and in pure plots, was 68.36 ± 5.45. When running the GLMM model, tree diversity (pure vs. mixed) and intermingling pattern in mixed plots (aggregated vs. dispersed) had significant effects on the proportion of damaged seeds in the plot (tree diversity p<0.001 and intermingling pattern, p<0.001, respectively; SM2). Mixed plots and plots with a dispersed pine

<caption>**Table 1**</caption>

Sampling effort and proportion of damaged seeds in the two experimental sites, ORPHEE and ORPHEE-SO.

<table><thead><tr><th>ORPHEE<br>Plot type</th><th>Pine<br>proportion</th><th>Plot composition</th><th>Planting density<br>(t/ha)</th><th>Irrigation</th><th>Number of<br>plots</th><th>Total number of<br>cones</th><th>Number of sampled<br>cones</th><th>mean % damaged<br>seeds</th></tr></thead><tbody><tr><td>pure</td><td>100 %</td><td>50 pines</td><td>1250</td><td>yes</td><td>3</td><td>185</td><td>56</td><td>30.26</td></tr><tr><td>pure</td><td>100 %</td><td>50 pines</td><td>1250</td><td>no</td><td>3</td><td>131</td><td>40</td><td>31.62</td></tr><tr><td>mixed</td><td>50 %</td><td>50 pines + 50<br>birches</td><td>2500</td><td>yes</td><td>3</td><td>225</td><td>56</td><td>27.46</td></tr><tr><td>mixed</td><td>50 %</td><td>50 pines + 50<br>birches</td><td>2500</td><td>no</td><td>3</td><td>88</td><td>38</td><td>19.30</td></tr><tr><td>pure</td><td>100 %</td><td>25 pines</td><td>625</td><td>yes</td><td>3</td><td>193</td><td>54</td><td>31.13</td></tr><tr><td>pure</td><td>100 %</td><td>25 pines</td><td>625</td><td>no</td><td>3</td><td>115</td><td>45</td><td>20.51</td></tr><tr><td>mixed</td><td>50 %</td><td>25 pines + 25<br>birches</td><td>1250</td><td>yes</td><td>3</td><td>160</td><td>44</td><td>22.17</td></tr><tr><td>mixed</td><td>50 %</td><td>25 pines + 25<br>birches</td><td>1250</td><td>no</td><td>3</td><td>171</td><td>54</td><td>22.15</td></tr><tr><th>ORPHEE-<br>SO</th><th>Pine<br>proportion</th><th>Plot composition</th><th>Planting density<br>(t/ha)</th><th>Mixing<br>pattern</th><th>Number of<br>plots</th><th>Total number of<br>cones</th><th>Number of sampled<br>cones</th><th>mean % damaged<br>seeds</th></tr><tr><td>pure</td><td>100 %</td><td>100 pines</td><td>1250</td><td>aggregated</td><td>2</td><td>n.a.</td><td>36</td><td>68.36</td></tr><tr><td>mixed</td><td>75 %</td><td>75 pines + 25<br>birches</td><td>1250</td><td>aggregated</td><td>1</td><td>n.a.</td><td>32</td><td>44.45</td></tr><tr><td>mixed</td><td>75 %</td><td>75 pines + 25<br>birches</td><td>1250</td><td>dispersed</td><td>2</td><td>n.a.</td><td>36</td><td>44.27</td></tr><tr><td>mixed</td><td>50 %</td><td>50 pines + 50<br>birches</td><td>1250</td><td>aggregated</td><td>2</td><td>n.a.</td><td>41</td><td>49.63</td></tr><tr><td>mixed</td><td>50 %</td><td>50 pines + 50<br>birches</td><td>1250</td><td>dispersed</td><td>2</td><td>n.a.</td><td>31</td><td>45.87</td></tr><tr><td>mixed</td><td>25 %</td><td>25 pines + 75<br>birches</td><td>1250</td><td>aggregated</td><td>2</td><td>n.a.</td><td>36</td><td>56.44</td></tr><tr><td>mixed</td><td>25 %</td><td>25 pines + 75<br>birches</td><td>1250</td><td>dispersed</td><td>2</td><td>n.a.</td><td>36</td><td>36.00</td></tr></tbody></table>
CRediT authorship contribution statement

**Hervé Jactel:** Writing – review & editing, Writing – original draft, Supervision, Methodology, Funding acquisition, Conceptualization. **Manuela Branco:** Writing – review & editing, Conceptualization. **Céline Meredieu:** Writing – review & editing, Methodology, Conceptualization. **Bastien Castagneyrol:** Writing – review & editing, Formal analysis. **Inge van Halder:** Writing – review & editing, Methodology. **Ana Farinha:** Writing – review & editing, Writing – original draft, Methodology, Investigation, Formal analysis, Data curation, Conceptualization.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Data Availability

Data will be made available on request.

Acknowledgements

The study was part of the European project HOMED (Holistic management of emerging forest pests and diseases), which received funding from the European Union's Horizon 2020 research and innovation programme under grant agreement No 771271. A. Farinha was supported by Post-Doc IdEx program EB 101 SG/1024R IdEx/1024-3127-1 BIOGECO (UBIFORTREE: Understanding Biological Invasions in FORESTREEs)

We thank the INRAE - Forest Experimental Facility UEFP (https://doi.org/10.15454/1.5483264699193726E12) for the management of the two ORPHEE sites especially Bernard Issenhuth and Laurent Séverin.

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