A Survey of Experts’ Opinions on the Management of the Small Hive Beetle in Italy

Abstract

The exotic alien species Aethina tumida, commonly known as the small hive beetle (SHB), was first detected in the Italian region of Calabria in 2014. The SHB is endemic in sub-Saharan Africa and is established in North and Central America, Australia, and many other world regions. Little is known about the effects of SHB introduction in new regions. This article focuses on the economic and regulatory aspects of SHB invasions. It presents the results of a survey questionnaire administered to Italian bee experts and extension agents in the spring of 2019, which documents opinions about the SHB invasion and its management in Italy. The results show that the SHB and Varroa are perceived as major threats to bee health. Over half of respondents agree that SHB eradication is no longer an attainable policy objective in Calabria, and support a policy shift from eradication to control of SHBs. Among respondents, extension agents are the most likely to agree with the need for a policy adjustment. Additional scientific and economic evidence and analysis can help resolve the differences in the opinions of stakeholders about feasible or preferable management policies for the SHB, and crucially, ensure the participation of beekeepers in the surveillance and control efforts.

1. Introduction

Aethina tumida, commonly known as the small hive beetle (SHB), is a scavenger and parasite of social bee colonies native to South Africa, where it is considered a minor pest [1]. In 1996, the SHB was first found outside its endemic range in the United States. Since then, it has spread rapidly and has been recorded in Egypt (2000), Australia (2001), Canada (2002), Portugal (2004, eradicated since), Jamaica (2005), Mexico (2007), Hawaii (2010), Cuba (2012), El Salvador (2013), Nicaragua (2014), Italy and Brazil (2014), the Philippines (2015), Belize, Canada and South Korea (2017), Mauritius (2018), Colombia (2020), and China (2017) [1,2,3]. Europe is free of SHBs except in the Italian region of Calabria. SHBs were previously found in the neighboring region of Sicily, but are no longer present there. Due to the potential for significant damage to bee colonies and honey production in these new regions [4,5], the SHB is often considered a major pest outside its native range. For instance, Neumann and Elzen [1] stated that:

“if introduced, the small hive beetle would swiftly become established in most of the range of the Western honeybee with major implications for apiculture. Also, the ability of small hive beetles to heavily infest the protected environment of honey houses may allow severe economic damage in any location worldwide.”

Unlike the mite Varroa destructor, the SHB does not directly attack adult bees, but feeds and reproduces in the combs of hives. In large and healthy colonies, the bees can often control small populations of SHBs and limit their reproduction [6,7]. Damages to beehives are caused mainly by sudden mass aggregation and the subsequent reproduction of SHBs, but the mechanism is not yet fully understood [5]. In addition to possible colony loss, an important component of economic damage to beekeepers is honey and wax destruction that can occur with moderate SHB infestations [8].

Economic damages caused by SHB infestations are not well documented. This is due to limited knowledge about the biological and ecological processes of SHB invasion in new regions, and the fact that beekeeping is a small industry in many world regions. The assessment of SHB invasions’ impacts on beekeeping industries is generally hampered by the lack of statistical information about bee-breeding production costs, revenues, and other economic data. This also means that SHB prevention and control policies have not been evaluated in economic terms or through cost-benefit analysis.

1.1. Cost Estimates of SHB Infestation and Eradication

The first published estimates of the economic damages of the SHB are those resulting from the early stages of the invasion of the United States. An estimated 20,000 bee colonies were destroyed in the initial SHB spread in Florida, causing losses of more than 3 million USD (2.4 million EUR) [9]. The costs of invasion in some regions of Australia have also been documented. Rhodes and McCorkell [10] provided a detailed assessment of SHB damages based on firm-level surveys in Australia, and recorded the loss of 4631 hives in 117 operations among 312 beekeepers surveyed. The average loss of bee inventory was estimated at 3300 AUD (1980 EUR) per operation or 84 AUD (50 EUR) per hive, with another 3400 AUD (2040 EUR) per operation for destroyed hive products and materials. To manage the invasion, the increased cost of production—increased travel to apiaries, purchase of chemicals, and other management costs—was estimated at 3800 AUD (2280 EUR) per operation and 140 additional hours per operation.

A survey conducted by Mulherin [11] in Queensland estimated a cost per hive of 400 AUD (240 EUR), including clean up, control, and restoration. A survey of 1302 beekeepers conducted by Biosecurity Queensland in November 2010 estimated a loss of 3 million AUD (1.8 million EUR), with a complete loss of 12 to 15% of hives [12]. According to a survey conducted between 2008 and 2016, the annual hive losses peaked at 5.5 million AUD (3.3 million EUR) during the 2010–2011 summer, decreasing to 1 million AUD (0.6 million EUR) in 2015–2016 as a result of both the steady uptake of various methods of SHB control and the unusually dry spring before the 2015–2016 summer [13].

In addition to direct bee inventory loss and hive or equipment damages caused by SHB infestation, beekeepers may further incur economic losses from regulatory measures undertaken to eradicate or control SHB spread. For instance, beekeepers may see decreased ability to migrate, or trade reduced due to restrictions on the movement of bees, hive products, and beekeeping equipment (e.g., quarantines or export bans). In Australia, SHBs did not initially cause significant problems in commercial beekeeping operations, but restrictions halted the export of live bees and queens out of Australia, worth around 2 million USD (1.6 million EUR) per year [14].

1.2. Policy Responses to SHB Invasions in the US, Australia, and Europe

Following the initial damages caused by the SHB invasion in the US, the species was given the status of major pest. The invasion also stimulated considerable research to understand the SHB better and help mitigate the economic impact on the beekeeping industry. However, no restrictions on hive movement or mandatory control and eradication practices were implemented. The SHB is no longer notifiable in the US, even if it is still a notifiable pest according to the World Organization for Animal Health (OIE).

In Australia, SHBs were initially managed as a notifiable disease. To prevent the spread to uninfected states or territories, the interstate and overseas movement of honey, bees, apiary products, and beekeeping equipment from the infected regions were subject to strict quarantine conditions for entry, and importers had to apply for permits. The SHB has since been removed from the notifiable disease list. However, by law, everyone in Australia has a general biosecurity obligation to take reasonable and practical steps to minimize the risks associated with invasive plants and animals under their control.

After the detection of SHBs in Australia in 2002, advisory sheets, booklets, and extension articles were produced in many countries, including the United Kingdom [15]. The SHB was often presented as a major threat to EU apiculture’s long-term sustainability and economic prosperity [4,16].

In 2003, the European Commission implemented additional measures to protect EU apiculture. The SHB was declared a notifiable pest throughout the community, and additional import controls were established to reduce the risk of further SHB introductions from third countries (Commission Decision 2003/881/EC, now Commission Delegated Regulation (EU) 2020/692 [17]). In 2020, the EU counted around 615,000 beekeepers and 18.9 million beehives [18]. The value of honey produced in the EU is estimated at about 140 million EUR [19].

1.3. SHB Eradication Policy in Italy

In 2014, when the SHB was first detected in the Italian region of Calabria [20], the EU mandated that Italy set up an SHB surveillance system and implement protective measures [21]. Accordingly, the Italian Ministry of Health (MoH) developed and started to conduct an eradication strategy [22].

The strategy developed since the first detection has several components: strict regulations of bee movements across national and regional borders, including the establishment of a protection zone covering all apiaries where the beetle has been detected, with a ban on the transport of any bees in and out such a zone; a surveillance system of sentinel apiaries and inspections of managed apiaries in the whole country; mandatory use of traps; the destruction of apiaries where a single infected colony is found, with indemnity payments to beekeepers for the destruction of honey bee colonies, equipment, and supers with honey to provide incentives for beekeepers to comply with reporting requirements in addition to the threat of fines, which can be harder to enforce.

In two years, around 6000 hives were destroyed, and 2 million EUR were paid to beekeepers by the Italian government as compensation [23]. The total financial burden borne by the state and regional governments for the control strategy also includes monitoring and surveillance costs (e.g., veterinary inspections of managed and sentinel apiaries), research, and information campaigns. According to the current National Plan of Surveillance of Aethina tumida (MoH 2020), around 4000 hives must be clinically inspected every year (including around 250 in Calabria), and around 1500 inspections of sentinel colonies occur yearly in Calabria and Sicily. Though a detailed cost accounting is not available, a rough estimate indicates that the cost of the inspection program alone is likely to exceed 100,000 EUR per year, including personnel salaries and travel costs.

The strategy launched by the MoH was effective in eradicating the SHB from Sicily. In 2017, after 2 years of surveillance without any positive case of SHBs since the initial outbreak, the EU Commission lifted all safeguard measures on Sicily while continuing surveillance. On 20 June 2019, an infested apiary was found in the province of Siracusa (Sicily region). The same control and surveillance measures previously applied were adopted. Based on the favorable epidemiological situation in February 2020, the Veterinary Service of the Sicily region ordered the withdrawal of the protection zone established in the outbreak area in Siracusa.

In Calabria, on the contrary, the protection zone (20 km around the infected apiaries) and the surveillance zone (5 to 10 km from the outer border of the protection zone) progressively expanded over time. Since 2017, the protection zone covers the entire Reggio Calabria and Vibo Valentia provinces [24]. Though the effort to eradicate the SHB was not successful, the prompt adoption of movement restrictions prevented the spread of SHBs to other regions. The model developed by the European Food Safety Authority [25] simulates that through the natural spread, it would take more than 200 years for the SHB to move across the 250 km from Calabria to Abruzzo (Central Italy). In contrast, the transportation of infested hives for migration or other management accelerates the speed of diffusion up to tenfold in model simulations. Cini, Santosuosso, and Papini [26] also found evidence that the two mechanisms of spread have very different rates. This finding is consistent with the observation that the spread of SHBs along the entire East Coast of North America took no longer than three years due to hive migration [1].

Zoning and other biosecurity measures are likely to have had significant economic impacts on the beekeeping industry in Calabria and other Italian regions, although no cost estimates have been published so far. The impact has likely been severe on the queen production industry, which generates between 9 and 17 million EUR in yearly revenues, with exports valued at around 2 million EUR in 2020. These figures are based on the Italian Queen Bee Farmers Association’s estimate of 600 to 700 thousand queen honeybees being produced in Italy every year, with a market price per queen ranging from 15 to 25 EUR [27]. In addition, around 150,000 queens are exported yearly, according to personal communication with the MoH. The ban on exports from the restriction zone has resulted in the shutdown of queen operations in Calabria, and is likely to result in further losses in beekeeping operations in Italian regions free from SHBs. Additionally, the interruption of annual migration from Abruzzo and other regions outside Calabria to the nectar-rich citrus groves of the region has likely had a significant impact on beekeeping activity.

Over time, dissatisfaction with the MoH’s eradication measures has grown among beekeepers in Calabria [28,29]. Compliance with reporting obligations of SHB presence in apiaries has eroded drastically [30]. The pattern is visible in the statistics reported by the veterinary institute responsible for tracking the invasion: the data available on the IZSVe website show that in 2014, 8 of the 32 affected beekeepers had spontaneously reported the presence of A. tumida to the local veterinary services, whereas from 2015 onward, all occurrences were identified through official surveillance activities (clinical inspections in managed apiaries and sentinel hives, see [31]). This erosion of compliance is consistent with findings from other studies of disease eradication campaigns, where the loss of stakeholder support grows as the duration and total cost of eradication efforts increase while effectiveness decreases [32]. Other studies have shown that the willingness of livestock owners to report disease is influenced by the amount of financial compensation paid in case of culling [33]. In this regard, beekeepers in the Calabria region complained about payment delays [29] and that indemnities only cover asset replacement value (e.g., destroyed hives and bee colonies, supers with honey) without accounting for costs related to business interruption. This latter cost cannot be covered by the MoH, which only covers losses directly related to eradication and containment measures; however, they could be considered by other agencies such as the Ministry of Agriculture. Other non-financial factors causing low compliance with the reporting requirements are the fear of the negative consequences of disease notification [32], the lack of trust in the efficacy of the eradication measures proposed by veterinary authorities [34,35], and the method of culling [36]. The destruction of entire apiaries where a single infected colony is detected has been increasingly perceived by beekeepers in Calabria as excessive and ineffective because the beetles may fly off the hive during the inspections, and can survive outside hives [28,37]. Low self-reporting increases the cost of monitoring SHB prevalence significantly, and is likely to limit the performance of any SHB management policy, eradication or other.

In September 2019, a new regulation was issued by the MoH that permits regional veterinary authorities in the protection zone to enforce the selective destruction of infected hives in the protection zones (where SHB is known to be established) only, provided a scientific opinion of the National Reference Laboratory is given for honeybee health. However, the mandatory destruction of a whole apiary when the SHB is found is maintained in surveillance zones or an SHB-free region [38]. This selective destruction is yet to be implemented due in part to the lack of appropriate regional regulation.

1.4. Documenting Experts’ Opinions on Eradication and Control Policy

In order to assess the barriers to the adoption of biosecurity measures, we present the results of a survey on the perception of the effectiveness of SHB management in Southern Italy among bee experts, such as extension agents, veterinarians, and researchers.

We test whether extension agents perceive SHB invasion and the damages it causes differently from the broader scientific and veterinary communities. Differences in perception may emerge when the biological and epidemiological characteristics of the pest in the specific local environment are poorly understood, as may be the case with the SHB invasion in Italy. The direct observation of SHB infestation in the field, and interactions with beekeepers in the invaded regions may lead extension agents to develop perceptions and local subjective beliefs regarding the likelihood and magnitude of damages from the SHB invasion. These may differ from the evidence derived from past invasions in other locations, or from an assessment based on general scientific knowledge.

Our interest in the difference of stakeholders’ opinions towards the effectiveness of SHB management is motivated by the important role played by the collaboration between beekeepers and veterinarians in the control of exotic invasive species. The resolution of disagreements between stakeholders is crucial to ensure the participation of beekeepers in the surveillance and control efforts and, hence, the success of the SHB management policy.

2. Materials and Methods

2.1. Survey and Questionnaire

The survey targets were veterinarians, scientists, civil servants working in central or local government on issues related to beekeeping (Ministry of Health and Ministry of Agriculture, Regions and Provinces), and extension agents working in beekeepers’ associations.

The survey was conducted from February to April 2019. From 13 to 15 February, the self-administered questionnaire was voluntarily completed by attendees at the international Apimondia honeybee health symposium held in Rome. Between 27 February and 27 April, invitation emails were sent to researchers working in the Departments of Veterinary Science in Italian Universities and the ten Italian Experimental Animal Health Prevention Institutes (Istituti Zooprofilattici Sperimentali). Invitations were also sent to the associations of beekeepers, requesting that they complete the online questionnaire and forward the invitation to their colleagues and research groups. Reminder emails were sent out to improve response rates, and all participants were given the option to complete the online or the paper version of the survey.

The complete questionnaire is reported in the Supplementary Material. Responses to some of the questions were deemed uninformative and are not presented in this article.

The survey’s purpose was twofold, and the questionnaire was organized in two sections, in addition to the initial collection of basic socio-demographic information. First, we aimed to assess experts’ perception of the threat posed by bee diseases and parasites subject to mandatory reporting, and evaluate how experts nationwide assess the strategy used so far to control SHBs in Italy.

The first section asked participants their opinions regarding the threat posed by the diffusion of notifiable bee diseases (i.e., subject to mandatory reporting). We used 5-point Likert-type scales (from 1 = not threatening, 5 = very threatening) to gain insight into experts’ perceptions about the risk posed by infestations by Varroa destructor, Tropilaelaps spp., and other parasitic mites, SHB, American and European foulbrood (bacterial infections), and Nosemosis (unicellular parasite). This first section of the survey also included questions about the distribution between beekeepers and the government of the financial burden associated with the culling of beehives infected by diseases subject to mandatory reporting. Furthermore, a set of questions assessed participants’ preferences for different economic instruments (compensation payments versus risk management tools) to offset economic losses suffered by beekeepers due to diseases and parasites with mandatory reporting.

The second section of the questionnaire included questions evaluating the SHB eradication strategy implemented in Italy in 2014. Questions included in this section were designed to assess: (i) the knowledge of the respondents about the control strategy adopted by the MoH thus far; (ii) the trust in the ability of the strategy currently in use to eradicate the SHB from the Calabria Region; and (iii) the perception of the need for a policy change for the management of the SHB.

2.2. Statistical Analysis

We performed both univariate and multivariate inference statistics. For comparison of means, we used the Wilcoxon signed-rank statistics. We then used an analysis of variance (ANOVA) (for continuous variables) and the chi-squared test (for categorical variables) to better characterize the differences in answers across respondents of different professional categories (extension agents, veterinarians, researchers, and others) and geographical origins, distinguishing between SHB-free and infested regions, namely Calabria and Sicily.

In addition, we performed a multivariate regression analysis to better understand the influence of the respondents’ characteristics on opinions about the likelihood of success of the eradication strategy and the attitude toward the shift from eradication to control. More specifically, we estimated two multinomial logit models to assess how the explanatory variables influence the probability to answer “Yes”, “No”, or “I do not know” in question Q25 (“is it appropriate to continue the eradication strategy?”) and Q26 (“is it appropriate to shift from eradication to control policy?”). In both models, the dependent variable refers to the three categories to select from, either “Yes”, “No”, or “I do not know”. The category “No” was used as the base outcome. The estimated coefficients are the probability of answering either “Yes” or “I do not know” relative to the base outcome. The explanatory variables included a dummy variable taking the value of 1 when respondents held a university degree, and 0 otherwise; a dummy variable taking the value of 1 if the respondent was less than 36 years old; a gender dummy (0 male, 1 female); and, finally, a dummy variable taking the value of 1 if the respondent was from the invaded region of Calabria. The set of explanatory variables was completed by three dummy variables indicating the profession of the respondents (extension agent, scientist, veterinarian, with other professions used as a base category). The relative importance of the respondents’ characteristics influencing the probability to answer “Yes”, “No”, or “Do not know” was assessed based on the results of the models (i.e., the statistical significance, sign, and value of the estimated coefficients).

3. Results

A total of 139 questionnaires were completed by the targeted population of Italian beekeeping experts. Although there is no exact number of relevant experts for the survey, an educated guess is that between 500 and 1000 experts work on issues related to bee health in Italy. Collected survey responses thus cover a third to a sixth of our potential target population.

3.1. Demographics and Expertise of Respondents

Respondents were mainly experts working as extension agents in beekeeping organizations (41%) and veterinarians (32%). Other respondents (27%) were researchers and scientists who specialized in bee pests and diseases, and civil servants working in central or local government on issues related to beekeeping. It is worth noting that 70.5% of respondents owned beehives, and among them, 79.59% were a member of a beekeeping association.

Respondents were mainly males (75% of total respondents) aged 51–60 (43.2% of total respondents) and 36–50 (34.5% of total respondents). On average, scientists and veterinarians had a high education level, whereas more than half of the respondents who qualified themselves as beekeeping experts had earned a secondary school diploma.

3.2. The Threat Posed by Notifiable Bee Diseases

More than 80% of respondents identified the SHB and Varroa as the diseases that pose the greatest threat to bee health (Figure 1). The Wilcoxon signed-rank test showed no statistically significant difference between the threat posed by the SHB and Varroa (z = −0.831; p = 0.406).

Apart from the cases of European foulbrood (EFB) and acariosis, the mean was significantly greater than the neutral midpoint (3 = threatening) of the scale (

Table 1. Mean responses from participants regarding the level of threat posed by notifiable bee diseases (Likert-type scales, 1 “not threatening” to 5 “very threatening”).

	Mean	Standard Deviation	Wilcoxon Signed-Rank Test z	p-Value
Varroa destructor	4.007	1.143	7.784	0.000
SHB	3.826	1.220	6.603	0.000
American foulbrood	3.453	1.211	4.110	0.000
Nosema apis and cerana	3.319	1.081	3.308	0.0009
European foulbrood	3.086	1.126	0.905	0.365
Tropilaelaps spp.	2.825	1.429	−1.437	0.151
Acariosis	2.394	1.314	−4.973	0.000

), indicating that respondents perceive Varroa, SHB, American foulbrood (AFB), and acariosis as the most threatening bee diseases.

We further analyzed the data to check whether (a) there was a difference in the perception of the threat posed by the SHB among professional categories (extension agents, veterinarians, researchers, and others), and (b) between respondents from free-from-SHB regions and those where SHB has been detected (Calabria and Sicily). One-way ANOVA (Kruskal–Wallis H-test) showed that the differences in opinions about the threat posed by the SHB across the four professional groups (Pearson χ² (3) = 4.414; p = 0.220) and between the two geographic groups (Pearson χ² (1) = 2.946; p = 0.086) were not statistically significant at the conventional significance level of 0.05.

3.3. Evaluation of the SHB Control Policy

The survey results showed that 46.4% of respondents claimed not to know the number of hives destroyed, whereas only 15.9% were aware that more than 3000 hives had been destroyed for the control of SHBs (

Table 2. Respondents’ knowledge of the number of hives that have been destroyed for SHB eradication so far (Q22).

	Profession				Regions
	Extension Agents	Veterinarians	Researchers	Other	Rest of Italy	Calabria and Sicily
	Percentages
I do not know	42.1	41.3	55.0	66.7	47.8	40.0
Less than 1000	35.1	28.3	5.0	6.7	28.3	12.0
1000 to 3000	10.5	15.2	10.0	13.3	11.5	16.0
Above 3000	12.3	15.2	30.0	13.3	12.4	32.0
Total	100.0	100.0	100.0	100.0	100.0	100.0
Total response count	57	46	20	15	25	113

). No statistically significant difference was found in the proportion of the answers given by respondents with different professional categories (Pearson χ² (9) = 13.347, p = 0.148), whereas it was almost significant (at the conventional significance level of 0.05) between respondents from different regions (Pearson χ² (3) = 7.691. p = 0.053).

More than 64 respondents out of 138 did not know the cost borne by the MoH, whereas only 20.9% knew that more than 1 million EUR had been spent on compensating beekeepers for the destruction of their hives (

Table 3. Respondents’ knowledge of the costs incurred by the MoH for compensation of hives destroyed (Q23).

	Profession				Regions
	Extension Agents	Veterinarians	Researchers	Other	Rest of Italy	Calabria and Sicily
	Percentages
I do not know	57.1	67.4	65.0	80.0	65.1	60.0
Less than 500 K€	5.4	2.3	10.0	0.0	5.5	0.0
500 K to 1000 K€	12.5	11.6	10.0	0.0	10.1	12.0
More than 1000 K€	25.0	18.6	15.0	20.0	19.3	28.0
Total	100.0	100.0	100.0	100.0	100.0	100.0
Total response count	56	43	20	15	109	25

). No statistically significant difference was found between professional categories (Pearson χ² (9) = 6.418, p = 0.697). The difference between geographical regions (Pearson χ² (3) = 2.273, p = 0.518) for this compensation cost question was found to be close to the significance threshold, but did not pass it.

Question Q18 aimed at assessing the belief in the ability of the current strategy to eradicate the SHB from the Calabria Region (

Table 4. Percentage of survey participants stating that the SHB can be eradicated in the time indicated in the first column (Q18).

	Extension Agents	Veterinarians	Researchers	Other	Total
Ever	70.6	26.5	73.3	46.2	54.9
>5 years	0.0	5.9	0.0	7.7	2.6
<5 years	11.8	47.1	13.3	38.5	25.7
I don’t know	5.9	8.9	13.3	0.0	7.1
Other	11.8	11.8	0.0	7.7	9.7
Total percentage	100.0	100.0	100.0	100.0	100.0
Total response count	51	34	15	13	113

). Around 55% of respondents believed that the insect could not be eradicated at that point (January 2019), whereas around 26% thought that eradication was still possible in less than five years. The observed differences in opinion between professional categories were significant (χ² (18) = 37.301, p = 0.005). On the contrary, no statistically significant difference was found between experts from the protection zone and experts from SHB-free regions (Pearson χ² (6) = 4.156, p = 0.656) at the conventional significance level of 0.05.

We then asked whether it was appropriate to continue the eradication strategy (Q25) and if it was desirable to change from eradication to control (Q26). Over half of the respondents (53.2%) stated that eradication was not the appropriate strategy (

Table 5. Opinions of survey participants about the appropriateness of continuing the eradication strategy (Q25).

	Profession				Regions
	Extension Agents	Veterinarians	Researchers	Other	Rest of Italy	Calabria and Sicily
	Percentages
No	72.0	29.8	55.0	53.3	50.0	68.0
Yes	14.0	49.0	25.0	20.0	32.5	8.0
I do not know	14.0	21.3	20.0	26.7	17.5	24.0
Total	100.0	100.0	100.0	100.0	100.0	100.0
Total response count	57	47	20	15	114	25

). This negative opinion was widespread among extension agents and respondents from the invaded regions. The difference in opinion between professional categories (Pearson χ² (6) = 21.675, p = 0.001) and between geographical origin (Pearson χ² (2) = 6.075, p = 0.048) were found to be statistically significant at the conventional significance level of 0.05.

As for the shift from eradication to control of the SHB, 73.0% of respondents were in favor, with none of the respondents from Calabria objecting to such change (

Table 6. Opinions of survey participants about the appropriateness of shifting from eradication to control (Q25).

	Profession				Location
	Extension Agents	Veterinarians	Researchers	Other	Rest of Italy	Calabria and Sicily
	Percentages
Yes	82.5	56.5	84.2	73.3	71.4	80.0
No	8.8	19.6	5.3	6.7	14.3	0.0
I do not know	8.8	23.9	10.5	20.0	14.3	20.0
Total	100.0	100.0	100.0	100.0	100.0	100.0
Total response count	57	46	19	15	112	25

). The opinions were found to be independent of the geographical origin (Pearson χ² (2) = 4.212, p = 0.122) and of professional categories (Pearson χ² (6) = 10.901, p = 0.091), significant at the conventional significance level of 0.05.

The results of the multinomial Logit regression for the question “is it appropriate to continue the eradication strategy?” (

Table 7. Results of multinomial regression for the question “is it appropriate to continue the eradication strategy?” (relative to base outcome “no”).

	Yes			I Do Not Know
	Coefficient	z	p > z	Coefficient	z	p > z
University	−0.797	−1.140	0.253	−1.241	−1.800	0.072
Gender	−0.378	−0.720	0.471	−0.031	−0.060	0.956
Young	0.658	0.980	0.327	0.628	0.960	0.336
Extension agent	−1.694	−2.190	0.029	−1.276	−1.630	0.103
Scientist	−0.214	−0.250	0.799	0.229	0.250	0.800
Veterinarians	1.200	1.670	0.094	0.893	1.130	0.259
Calabria	−1.501	−1.800	0.072	0.106	0.180	0.858
Constant	0.279	0.370	0.715	−0.089	−0.110	0.910

) confirmed the findings of the univariate statistics. Extension agents had a statistically significantly lower probability of believing that eradication was the adequate strategy to use in Calabria. The coefficient for veterinarians was positive and statistically significant (at the 0.1 level of significance); hence, this group of respondents had a higher probability to state that eradication was appropriate. In the model referring to the outcome “I do not know”, the coefficient associated with the variable “University” was negative and significant, albeit only at the 0.10 level of significance. It indicated that respondents with a higher level of education had a lower probability of choosing the uncertain outcome (“I do not know”) relative to respondents with a lower level of education.

The results of the multinomial regression for the question “is it appropriate to shift from eradication to control policy?” (

Table 8. Results of multinomial regression for the question “is it appropriate to shift from eradication to control policy?” (relative to base outcome “no”).

	Yes			I Do Not Know
	Coefficient	z	p > z	Coefficient	z	p > z
University	0.401	0.420	0.673	−2.553	−1.860	0.063
Gender	0.782	1.080	0.279	0.285	0.320	0.746
Young	−1.159	−1.380	0.168	−0.990	−0.890	0.372
Extension agent	1.830	1.840	0.065	0.157	0.130	0.900
Scientists	1.770	1.370	0.172	2.730	1.520	0.128
Veterinarians	−0.288	−0.340	0.733	1.792	1.340	0.181
Calabria	15.109	0.020	0.987	15.447	0.020	0.987
Constant	0.652	0.680	0.497	0.635	0.590	0.553

) show that being an extension agent was the only characteristic found to result in a higher probability of believing that a shift to control and away from eradication was preferable. Again, respondents with a high educational level had a significantly (albeit at the 0.10 level of significance) lower probability of choosing the “I do not know” outcome relative to the base outcome “no”.

4. Discussion

After the first detection of the SHB in Southern Italy in 2014, the scenario of rapid spread experienced in the 2000s along the East Coast of the United States has been avoided. Italian regions outside the protection zone centered on Calabria and the rest of the European territories remain free of SHB. This positive outcome can be attributed to the prompt implementation of a quarantine area with highly-restricted movements of bees.

Though the movement restrictions adopted in 2014 effectively controlled the spread, the eradication goal set by Italian veterinaries authorities has not been attained in Calabria. The SHB is now de facto established in the region. Beekeepers and extension agents continue to collaborate with researchers to identify successful management practices and increase knowledge about the biological and epidemiological features of the insect in the Mediterranean zone. However, the collaboration of beekeepers with the surveillance system and reporting has progressively eroded over time.

A conflict of opinions between stakeholders is a critical socio-economic factor contributing to the failure of control and eradication strategies of exotic and invasive species and animal diseases. We help in the understanding of attitudes towards SHB control policies by showing that the perceptions of experts working in the invaded areas, i.e., Calabria and Sicily, and in more direct contact with beekeepers (i.e., extension agents) differ from other experts’ perceptions.

Our survey results show that the SHB and Varroa were perceived as the greatest threats to bee health, with no significant difference among professional categories (extension agents, veterinarians, researchers, and others) or between respondents from SHB-free regions and SHB-invaded regions. However, differences were found in the perception of the effectiveness and appropriateness of biosecurity measures implemented for SHB control. Over half of the respondents agreed that five years after the first notified SHB detection, SHB eradication was no longer an attainable objective in Calabria. This opinion was particularly prevalent among extension agents (70%). Furthermore, over 70% of respondents supported the shift from eradication to control, with none of the Calabrian respondents objecting to such change. Veterinarians favored such change relatively less. The regression analysis showed that the profession of respondents is a statistically significant factor in the likelihood of supporting eradication.

The extent of agreement about the threat posed by the SHB suggests that the information effort by the EFSA about the risks of the SHB and other sources effectively produced a uniform perception among bee experts. The consensus about the threat likely promoted the collaboration of beekeepers with scientists and extension services to develop traps and lures to attract and detect the beetle and identify the practices that can help control SHBs.

In contrast, the conflict in opinions about implementing biosecurity measures (mandatory reporting with the destruction of the apiary) to achieve the eradication goal is consistent with the low collaboration with surveillance and reporting. Extension agents and beekeepers argue that the hives’ destruction is ineffective in limiting the SHB spread, unless the number of SHBs is very low, as it happened in Sicily in both 2014 and 2019 as a result of the illegal movement of colonies from Calabria [31]. The hypothesis, according to which, destructions are ineffective, is supported by the claim that adult beetles fly out of hives when hives are opened for inspection, and that SHBs may find viable habitat outside beehives. However, this phenomenon has not yet been demonstrated in the Calabria and Sicily regions. In addition, the possibility of maintaining beekeeping operations in the presence of SHBs—as observed in Australia or the United States—is likely to have reduced the perceived threat in the protection zone, therefore lowering the perception that stringent control measures were justified. The lack of trust of extension agents and beekeepers in the efficacy of destructions after reporting, and the lower probability of severe damages they associate with SHB invasion may lower the expected benefit and likelihood of reporting.

Given that reporting by individual beekeepers is a critical component of surveillance, the resolution of disagreements between stakeholders and the improvement in the collaboration of beekeepers are essential for an effective SHB control policy [39]. Possible options include changes in the amount of compensation, the type of culling, and the beetle’s status in the protection zone. Consideration of the costs and benefits of alternatives would help ensure both a choice of the best policy from a societal standpoint, and the design of compatible incentives for the participation of beekeepers.

First, paying a larger compensation after culling to cover the costs related to business interruption and asset replacement value (i.e., hives and bees), as sometimes requested by beekeepers’ associations, brings challenges in terms of incentives. The economic literature has shown that total compensation of all costs of apiary destruction can be inefficient, as it reduces incentives for preventative behavior [40] and may create perverse incentives [41].

Second, selective destruction of the infested hives in place of the whole apiary can reduce the loss incurred by beekeepers, making it more acceptable. It is not clear, though, what effects the selective destruction would have on the economic behavior of beekeepers. This measure, on the one hand, still entails some costs of business interruption, which are not covered by indemnities, but, on the other hand, does not entirely solve the problem of lack of trust.

Third, seven years after its first detection, the SHB is now de facto established in the protection zone. In such a zone, the long-term management of SHBs, designed to maintain the invasive species at acceptably low densities, may be a more effective target than the systematic destruction of infected hives. A change in official status and the shift from eradication to long-term control may help restore beekeepers’ willingness to report and improve the efficiency and effectiveness of the surveillance system. However, declaring the beetle as established in the protection zone does not imply the end of the eradication strategy in Italy. On the contrary, it may allow concentrated eradication efforts in the areas bordering the protection zone. In addition, recognizing an exotic parasite as endemic in a territory of a Member State of the EU may have consequences on restriction measures adopted by the other Member States.

5. Conclusions

Further analysis is needed to guide management of the SHB in the Southern Italian context, as well as in the rest of Europe. Several information gaps need to be filled to inform a cost–benefit analysis of policy alternatives. Surveys of beekeepers in both infected and SHB-free regions would help quantify the costs and revenue losses attributable to SHB presence in beekeeping operations, and thus, identify effective management strategies for the pest. In addition, an assessment of revenues from sales of live bees and queens, which are currently very poorly documented, would help track the impact of bee movement restrictions across regional and national boundaries. Restrictions to migratory beekeeping also constitute costs that are poorly quantified, but that should enter the cost–benefit analysis of policy options.