Research Article |
Corresponding author: Flavius Bălăcenoiu ( flavius.balacenoiu@icas.ro ) Corresponding author: Maarten de Groot ( maarten.degroot@gozdis.si ) Academic editor: Uwe Starfinger
© 2021 Flavius Bălăcenoiu, Anže Japelj, Iris Bernardinelli, Bastien Castagneyrol, György Csóka, Milka Glavendekić, Gernot Hoch, Boris Hrašovec, Silvija Krajter Ostoic, Marton Paulin, David Williams, Johan Witters, Maarten de Groot.
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:
Bălăcenoiu F, Japelj A, Bernardinelli I, Castagneyrol B, Csóka G, Glavendekić M, Hoch G, Hrašovec B, Krajter Ostoic S, Paulin M, Williams D, Witters J, de Groot M (2021) Corythucha arcuata (Say, 1832) (Hemiptera, Tingidae) in its invasive range in Europe: perception, knowledge and willingness to act in foresters and citizens. NeoBiota 69: 133-153. https://doi.org/10.3897/neobiota.69.71851
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The oak lace bug (OLB) Corythucha arcuata (Say, 1832) is an invasive alien species (IAS) that potentially could have many negative impacts on European oak health. Certain measures can be applied to counteract these effects. However, these measures may not be acceptable for forest managers or other stakeholder groups, such as private forest owners, environmental NGOs or the general public. Thereby, we set out to study the perception and knowledge of foresters and other stakeholders on the health status of European oak forests affected by oak lace bug and to investigate what forest health management measures would be acceptable to these target groups. An online survey questionnaire was designed and distributed via social networks, as well as professional networks via e-mails. The survey questionnaire was completed by 2084 respondents from nine European countries: Austria, Croatia, Belgium, France, Hungary, Italy, Romania, Serbia and Slovenia. Even though only a little over 60% of respondents reported they had noticed the discolouration of oak leaves caused by OLB, almost all (93%) considered it to be a problem. As respondents come from a country where C. arcuata is widespread and established, people’s general knowledge and awareness of OLB began to increase. The survey revealed that foresters thought that the insect affected photosynthesis, acorn crop and the aesthetics of the trees, but cannot cause death of trees. However, they assume that the value of the wood would decrease (this fact is also supported by the respondents who are connected to an environmental NGO), but that OLB does not affect property value. However, forest owners claim that the value of the property can be affected and that people would avoid entering the forest. In terms of potential control methods, respondents preferred biological or mechanical measures over chemical ones. We consider this study to be a good basis for further research on the topic of perception, knowledge and attitudes related to OLB since we can expect that the IAS, such as OLB, will certainly spread to European countries that were not included in this survey.
Attitude, citizen knowledge, Europe, forest health, IAS control measures, invasive alien species, survey
Humans rely on healthy forest ecosystems to provide a wide range of ecosystem services (
Negative effects of invasive alien species can be particularly profound in long-lived ecosystems, such as forests (
Corythucha arcuata, the oak lace bug (OLB henceforth), is an insect from North America that was first reported in Europe in 2000 in northern Italy (
Mechanical control measures have been tested in several countries, such as the UK, Czech Republic and Romania (
In the last three decades, out of 77 studies that analysed social perception of invasive alien species, only 13 targeted the taxonomic group of insects (
The objectives of our study were to investigate perception and knowledge of the health status of European oak forests affected by OLB as perceived by several stakeholder groups (foresters, private forest owners, environmental NGOs and the general public), as well as to explore attitudes of these stakeholder groups towards actual and potential measures targeting OLB. We hypothesised that: a) selected stakeholder groups perceive OLB or, at least, the effect of OLB on oak species, to some extent, b) that attitude of stakeholder groups towards possible measures for OLB management may differ and c) that the sociodemographic characteristics of respondents may be significantly connected to their perception, knowledge and attitudes. We expected differences in perception and knowledge between respondents from countries where OLB has been already established and those where it is still not present. When it comes to attitudes towards specific measures for controlling OLB, we also expected that support of different stakeholder and sociodemographic groups may differ.
The questionnaire was designed first in English (Suppl. material
We aimed to reach particular target groups – foresters, environmental activists, nature lovers, forest owners and members of environmental NGOs, as well as the general public. During the period the questionnaire was accessible, we surveyed the self-declared pre-defined categories of respondents and re-advertised the questionnaire through the relevant channels to reach under-represented groups.
The questionnaire did not focus exclusively on OLB, but addressed some issues generally related to invasive alien species and was split into three parts, namely: 1) questions on invasive species in general, 2) a section that was specifically dedicated to the issue, knowledge and perception of the OLB in European oak forests and 3) a part with questions on respondents’ socio-demographic characteristics. In this paper, we will present results related to OLB and sociodemographic characteristics of respondents.
The questionnaire was anonymous. There were no means by which respondents could be identified from their answers. By submitting their answers, respondents were informed that they will be analysed and used in the context of a research project, leading to publication in a scientific journal.
The questions were mostly a close-ended format, with several types of answers: binary answer (yes or no), multiple possible answers, Likert scale or open-ended. However, the open-ended questions (in which the respondent could give their own opinion) yielded a small number of responses and they were very diverse. We, therefore, did not perform any quantitative analysis, but instead extracted and synthesised the most frequent answers to be presented here.
To study the influence of OLB’s time since introduction on respondents’ perception and general knowledge of OLB and attitudes towards its management, the countries were grouped as described above into “not arrived”, “recently arrived” and “present for greater than 5-years” categories. After the questionnaire was distributed within 10 European countries, given that we only received 15 responses from the United Kingdom, this information was removed from any further data analysis.
We analysed closed ‘yes-no’ questions (questions 1, 2, 4 and 6–8) using generalised linear mixed models with binomial error distribution and logit link and with country included as a random effect. The questions 9–10 (multiple possible answers) were analysed with an ordinal mixed model, with again country included as a random effect. We first built a full model including the following independent variables (Suppl. material
Analysis and data visualisation were carried on using the R statistical programme (
Finally, in the nine remaining countries, the questionnaire was completed by 2084 respondents. Regarding socio-demographic characteristics, the questionnaire revealed respondents were as follows: foresters/non-foresters 37%/63%, forest owners/non-forest owners 21%/79%, environmental NGOs/non-NGOs 31%/69%, women/men 37%/63%.
Based on photos representing whole trees or single leaves impacted by the OLB, two thirds of respondents (66%) declared that they had seen such discolouration before (Fig.
Almost all respondents (93%) consider this discolouration to be a problem, with frequent forest visitors and women being more likely to hold this opinion (Fig.
In order to determine to what extent the respondents knew the cause of the discolouration, we listed several potential causal biotic and abiotic factors and offered them the possibility of a single answer. Only 5% of respondents perceived the colour of leaves normal given the season. Of the 95% of the respondents who recognised discolouration (i.e. abnormal leaf colour), 41% assumed it was caused by an insect, 36% by a pathogen, 14% attributed it to drought and 4% gave open answers (many respondents associated discolouration with pollution or climate change).
After we presented them with a picture with OLB, indicating that it had caused the discolouration, we asked if they had seen this insect before – half of the respondents declared having seen the insect before (Fig.
The extent to which people had seen the insect that causes leaf discolouration before the survey.
Respondents were further asked if they knew the name of the insect species they had seen or the one causing the leaf discolouration and offered them several responses. Most of the respondents correctly identified Corythucha arcuata (50%) or acknowledged their inability to recognise the species (42%). The rest of the respondents offered predefined answers, such as Corythucha ciliata, Cameraria ohridella Deschka & Dimić, 1986 or one of the native insect species.
We then informed our respondents that the correct answer was Corythucha arcuata (OLB) and asked them if they had ever heard of this species before. Half of respondents (51%) replied “yes” to this question (Fig.
Parameter estimates suggest that forest managers are of the opinion that even if OLB affects photosynthesis of the trees, it cannot cause their death in time, but it affects the aesthetics of the trees. None of the respondents considers that the insect has no effects on the trees. Forest owners (z = 2.489, P = 0.013) and younger people (older than 65 years: z = -2.580, P = 0.010) thought it affects the aesthetics of the trees. The likelihood that respondents are of opinion that OLB causes the die-off of infested trees in time was higher in countries where OLB already occurred (recent occurrence: z = 2.583, P = 0.010; established: z = 4.349, P = 1.37e-05) and higher amongst non-foresters (z = -4.675, P = 2.94e-06).
People who were not foresters (z = -2.065, P = 0.039), those who visit forests very rarely (once a day: z = -2.627, P = 0.009, once a week: z = -1.947, P = 0.052, once a month: z = -2.546, P = 0.011, once a year: z = -2.472, P = 0.013) and those who come from the countries where OLB had not yet been reported prior to the survey or only was established recently (spread group: z = -0.680, P = 0.496; established group: z = -3.020, P = 0.002), did not know what effects OLB might have on affected trees.
Respondents who are actively participating in an environmental NGO (z = 2.409, P = 0.016) and men (z = 2.517, P = 0.012) felt the need to add other effects besides the predefined list. They answered mainly in the same direction, highlighting that OLB was likely to affect oak growth, decrease the acorn crop or weaken the resistance system of trees to other factors.
Parameter estimates suggest that women (compared to men: z = -2.700, P = 0.007) or active members of an environmental NGO (z = 2.317, P = 0.02049) are more likely to be of the opinion that one of the impacts of OLB would be to decrease the value of wood, while forest managers are more likely to be of the opinion that OLB does not affect property value (z = -2.689, P = 0.007158). In addition, older people (z = 2.379, P = 0.0174) or people from established group countries, where OLB has been established longer (z = 2.297, P = 0.0216), are of the opinion that one of the effects would be that people will avoid entering the forest. Women (compared to men: z = -4.405, P = 1.06e-05) or young people (compared to mature people between 46 and 55: z = -2.679, P = 0.00739; between 56 and 65: z = -3.203, P = 0.00136), are more likely to consider that an important effect on society caused by OLB is the discomfort caused by the insect’s stings/bites on the human skin.
It was statistically significant that respondents from countries where OLB has not arrived or recently arrived (absent and spread group), in comparison to where OLB has been longer established, oppose the idea that it does not have any effect on society (z = -3.843, P = 0.000122). People who are less than once per year in the forest did not know whether this affects society compared to people who are relatively frequent visitors in the forest (once a month: z = -2.441, P = 0.0147). The same is observed for people living in areas without OLB (absent group) compared to areas where OLB has been established for a while (z = -3.992, P = 6.55e-05). In addition, respondents from countries where OLB occurs (spread group: z = -2.029, P = 0.04251, established groups: z = -2.344, P = 0.01907), forest managers (z = 2.359, P = 0.01832), people who are actively participating in an environmental NGO (z = 2.331, P = 0.01974) and people in the age class between 36 and 65 years (compared to people older than 65: 36–45 years: z = 2.804, P = 0.00505, 46–55 years: z = 2.437, P = 0.01482; 56–65 years: z = 2.889, P = 0.00386) completed the questionnaire citing other effects that were not in the predefined list of answers. Most answers were similar and were generally focused on similar themes as potential negative impacts, such as economic costs for the owner, increasing CO2, ecological imbalance and loss of social function of forests.
When asking respondents how strongly they would support removal of OLB to a certain extent, their attitudes towards certain measures differed. The respondents were more likely to support partial removal for the purpose of preventing further spread (Fig.
Attitudes of respondents towards the partial removal of oak lace bug (OLB). 0 = I do not support; 1 = I partially support; 2 = I mostly support; 3 = I fully support.
Attitudes of respondents towards the complete removal of OLB. 0 = I do not support; 1 = I partially support; 2 = I mostly support; 3 = I fully support.
Regarding the significant influence of socio-demographic characteristics, the results were more complicated. It appeared that, with increasing age (although not significantly), respondents were more likely not to support the removal of OLB. Men (compared the women: z = 2.750, P = 0.005956) or those who were between 36 and 45 years old (compare to people older than 65 years: z = 3.853, P = 0.000117) were more likely to support complete removal.
When asked how strongly they would support various removal measures, it was obvious that respondents preferred biological or mechanical control measures (69% mostly and fully support), over chemical ones with only 9% of the respondents who did not support mechanical removal. The degree of support for chemical control measures was more balanced, with 48% supporting them (full support: 9%, partial support: 39%), whereas 39% did not support chemical control measures. Biological control received more approbation, with 77% of the respondents supporting this approach to a large extent (from mostly to fully support), while only 4% of the respondents did not support this. Given that chemical control measures were unsupported, if we compare it to the other two approaches, data analysis showed that it was statistically significant and that foresters were more likely not to support mechanical control measures (z = -4.549, P = 5.4e-06), while passive NGO members strongly supported it (z = 2.232, P = 0.0256) (Fig.
The influences of socio-demographic characteristics (foresters/other, environmental NGO/other) on support for mechanical control measures. 0 = I do not support; 1 = I partially support; 2 = I mostly support; 3 = I fully support.
When asked what measures they would take if the species appeared on their private property (e.g. garden), a vast majority of respondents (81%) would support complete removal. Furthermore, 17% would support partial removal, while only 2% would not support removal of OLB at all (Fig.
A the extent to which respondents would be willing to remove OLB if it appeared on their private property B the extent to which respondents supported the removal of OLB from forests or parks.
The removal of OLB as a principal control approach was supported by a large majority of respondents, of these 2% supported insect removal only in forests and 4% in parks, while 91% of them in both settings. Only 2% of respondents did not support removal of OLB if it caused damage (Fig.
The results from the study were encouraging in that the foresters and NGOs were most likely to say that they had seen this discolouration before undertaking the survey, leading us to conclude that they had the basic professional training to distinguish a forest affected by diseases or pests. Furthermore, the fact that 93% of respondents considered this discolouration to be a problem, suggests that there is general public interest and awareness in the health of European oak forests.
The observation that half of the respondents who answered had seen this insect before undertaking the survey, despite its small size and relatively recent introduction into Europe, may be due, on the one hand, to the large numbers of foresters and frequent forest visitors who participated in the questionnaire. However, in part, it is also likely due to the media interest that, in the last few years, has intensely covered the invasions in several cities in Europe where OLB is already established and damage is more visible, such as in Belgrade, Bucharest, Budapest and Zagreb. In addition, the estimation parameters in this study tended to confirm the hypothesis of a previous case study (
Regarding the occurrence of OLB in the different countries, it was understandable that it is almost impossible to have seen or heard of this insect species before for residents of a country where OLB has only recently been reported or, moreover, if it has not yet been reported. Consequently, these people seem to underestimate the potential consequences of the species. Therefore, programmes to raise public awareness of various invasive species, such as OLB, should be part of a comprehensive future IAS early detection programme.
Although respondents declared having some concern about photosynthesis, forest managers did not consider OLB as a threat to trees and forest health. These results mirror current knowledge on OLB ecology, with severe attacks reducing tree photosynthesis by up to 60% (
Even though those respondents who were foresters and those associated with environment NGOs were of the opinion that OLB could decrease the value of the wood, it is difficult to quantify how much the value of timber might be influenced by the insects repeated attack until it is established exactly what impact OLB has on radial growth following years of damage.
In terms of property value, private forest owners in our survey were of the opinion that their property would be affected and that, at the same time, people would also avoid entering the forest. To the best of our knowledge, we are not aware of studies exploring the connection between property value and trees infested by OLB. However, another study showed that the invasive species, coqui frog (Eleutherodactylus coqui), after it was accidentally introduced into Hawaii, resulted in decreases of up to 64% in property value (
The discomfort/annoyance caused by the insect’s stings/bites on the human skin is perceived especially by the people who happened to be stung and will become more frequent as people visit infested oak forests and especially those who visit parks in cities where OLB is already present (
Our results on the level of support for the removal of OLB complement another study (
The respondents in the survey clearly rejected chemical control measures. This result was in line with both
Nevertheless, studies to date have shown that mechanical measures are recommended more for early detection, surveying and monitoring and tend not to be used for widespread control programmes. Interestingly, recent management knowledge regarding chemical measures to control OLB seems to suggest that they are also only effective to a certain extent (
Biological control has strong potential, because the public sees this as a sustainable solution. However, caution should be taken, especially as it can have unwanted side effects as has been seen with Harmonia axyridis that was introduced into Europe in 1964 as a biological control agent of aphids on fruit trees (
Our results show that our respondents (98%) would support removing OLB if it appeared on their private property, either partially or totally and the results are in line with the study of
The strength of our survey was that it was evaluating responses from numerous countries along the invasion gradient. Most comparable studies only cover a smaller geographical area and, therefore, only focus on management of one part of the biological invasion gradient. Taking the whole gradient into account, as done in this current study, enables researchers to see differences in attitudes towards the species in different stages on the invasion of OLB. Of course, cultural and social differences might also play an important factor and it is, therefore, important to focus on these changes in attitudes and use them in communication messages. Our results indicated that there were differences between the different country groups for OLB and, hence, it is important to take this into account for other IAS in the future.
This research is the first pan-European survey which studies the perception of the population on a gradient of invasion caused by OLB. Our study has certain limitations. The study is exploratory, voicing perception, knowledge and attitudes of our respondents and the results cannot be generalised on the entire targeted stakeholder groups in respective countries. However, our results are indicative and, despite not being representative, are still in line with similar studies. Hence, we consider this study to be a good basis for further research on the topic of perception, knowledge and attitudes related to OLB since we can expect that this IAS will certainly spread to other European countries that were not included in this survey.
This work was supported by the EUPHRESCO project – ‘Corythucha arcuata (Heteroptera, Tingidae): Evaluation of the pest status in Europe and development of survey, control and management strategies’.
FB was funded by the PN 19070201 project “Assessment of the risk of new species of harmful insects with potential for outbreak of deciduous forests in Romania”. Therefore, these results are part of F.B. PhD thesis (Bioecology of the invasive alien species Corythucha arcuata in Romania).
MdG was supported via the Administration of the Republic of Slovenia for Food Safety, Veterinary Sector and Plant Protection and the core research group “Forest ecology, biology and technology” funded by the Slovenian Research Agency.
BC was founded by the HOMED project, which received funding from the European Union’s Horizon 2020 Research and Innovation Programme under grant agreement No. 771271.
The Hungarian contribution was supported by the OTKA 128008 research project sponsored by the National Research, Development and Innovation Office.
Annex 1. The questionnaire
Data type: Survey
Explanation note: The questionnaire used to collect the survey data.
Appendix 2
Data type: docx. file
Explanation note: Independent variables descriptions.