The sustainable management of invasive alien species: the case of Small Hive Beetle

CRISTINA SALVIONI1 AND GIOVANNI FORMATO2 1 Department of Economics - University of Chieti-Pescara [email protected] 2 IZSLT – Rome (Italy)

Paper prepared for presentation for the 166th EAAE Seminar Sustainability in the Agri-Food Sector

August 30-31, 2018 National University of Ireland, Galway

Galway, Ireland

Copyright 2018 by AUTHORS. All rights reserved. Readers may make verbatim copies of this document for non-commercial purposes by any means, provided that this copyright notice appears on all such copies.

The sustainable management of invasive alien species: the case of Small Hive Beetle

CRISTINA SALVIONI1 AND GIOVANNI FORMATO2 1 Department of Economics - University of Chieti-Pescara [email protected] 2 IZLT – Rome (Italy)

Abstract

Invasive alien species (IAS) are recognized as a key pressure on biodiversity and a priority for action by the European Commission. While in the past the impacts of IAS were underestimates, now there is general concern on this matter. The final goal is to reduce their potential ecological and economic impacts. Moreover, there is the common idea, shared among EU Member States, that IAS require major expenditures on projects focused on prevention, control and mitigation activities.

The internationally agreed hierarchical approach to reduce and control IAS includes three distinct types of measures: prevention, early detection, and rapid eradication. Another goal of the European Union is to avoid any further the spread of those IAS that are already well-established in the EU to minimize the harm they can cause.

The costs associated with the application of this approach are evaluated differently according to stakeholder positions but include damage to existing economic interests. This is frequent cause of conflict in IAS management. In addition to this, responsibility for IAS control is shared between various sectors at various levels and this is cause of institutional and administrative conflicts of interest. For the management strategy to be effective, stakeholders need to be engaged in the strategy and institutional coordination need to be strengthened.

In this paper we explore the case of the introduction in the Calabria region (Italy) in 2014 of the invasive alien specie Small Hive Beetle (SHB), Aethina tumida. Here it become clear that the engagement of stakeholders, together with good institutional coordination are vital to achieve sustainable and proper management in relation to IAS. SHB was first detected in southern Italy in 2014 and, despite the adoption of strong eradication measures, it is so far still present there. Infestations of SHB can cause considerable financial losses to beekeepers and to the Government. The main associated costs for beekeepers are the extra time spent managing the hives to detect and control the beetles, and the losses in honey. In fact, honey that is contaminated by the beetles is no longer saleable being it unpalatable. In the worse cases, A. tumida is able to heavily damage wax comb and reduce honey bee population up to colony losses. In addition to the private costs borne by beekeepers, there are the costs borne by public institutions in charge of IAS control. A surveillance system has been put in place to detect the presence of SHB in Italy. Eradication measures have been applied since 2014, including the destruction of all colonies at apiary sites whenever a single infested colony was found, and compensations paid to beekeepers for the destruction of infested apiaries. These measures resulted in SHB eradication only in the Sicily region. In the Calabria region, even though around 3600 apiaries were destroyed, there is still a low prevalence and slow spread of the pest.

Introduction

Invasive alien species (IAS) are recognized as a key pressure on biodiversity and a priority for action by the European Commission. While in the past the impacts of IAS were underestimates, now there is general agreement that IAS require major expenditures on prevention, control and mitigation projects in order to reduce their potential ecological and economic impacts. The internationally agreed hierarchical approach to combatting IAS includes three distinct types of measures: prevention, early detection, rapid eradication and, finally, when some IAS of Union concern are already well- established, management not to spread any further and to minimize the harm they cause.

IAS management is often driven by many heterogeneous public and private actors. Each group has different preferences over IAS control measures and what is an acceptable risk level of incurring an invasion (e.g. Garcia-Llorente 2008; Mills et al. 2011; Humair et al 2014; Reed and Curzon 2015). Under such circumstances, reaching an agreeable set of actions towards the control of an invader can prove quite challenging (e.g. Liu et al. 2012; Touza et al. 2014; Marzano et al. 2015).” This task is often further complicated by a fragmented Legal and Institutional Frameworks dealing with IAS, and by low levels of coordination between agencies responsible for sanitary matters, agriculture and nature conservation. All these are common problems in IAS management (Shine et al. 2000). Since engagement of stakeholders and institutional coordination are vital to achieve longer term sustainable management in relation to IAS, the IUCN - The World Conservation Union has called upon the use of a Strategic Planning Processes. The first step toward the definition of such strategy is to identify sectors and pathways associated with alien species introduction and/or use.

This paper is the first result of an on-going research project aiming to analyze costs and benefits of the strategy of eradication of Small Hive Beetle (SHB), Aethina tumida, in Italy. In the rest of the paper we first discuss the private, public and social costs associated with SHB, then we review existing control measures as well as legal and institutional frameworks to identify gaps, weaknesses and inconsistencies.

Damage cost of SHB

The SHBs are scavengers and parasites of social bee colonies originates from Sub-Saharan Africa. Within its natural range it is hardly regarded as a plague, as most honey bee colonies are able to cope with its presence

SHBs have emerged as an invasive species and were first noticed in November 1996 in South Carolina in the United States. Since then, they have spread rapidly and been recorded from Egypt (2000), Australia (2001), Canada (2002), Portugal (2004), Jamaica (2005), Mexico (2007), Hawaii (2010), Cuba (2012), El Salvador (2013), Nicaragua (2014), Italy (2014), the Philippines (2014), Brazil (2016), and South Korea (2017).

Only weakened and diseased colonies are susceptible to damage by the beetle. To some extend this is also the case in areas outside of its natural range, such as the United States, Australia and Italy. As the beetle is able to survive the climatic conditions of the United States and Canada, it is likely to become established in most parts of Europe.

Unlike the Varroa destructor mite, the small hive beetle does not directly attack bees. It harms the entire colony, moving into the hive and destroying the resources that the bees need to survive. The brood nest of honey bees offers adult beetles ideal conditions to reproduce. Their larvae feed on the stored honey and pollen and destroy the combs. They tunnel through the combs, undermining them and leaving behind slimy defecation products. The larvae contaminate the honey, causing it to ferment, spoil and then ooze out of the combs, making it useless to both the bees and the beekeepers. Bees protect themselves against the invasion by fleeing the hive, leaving the honey and their brood behind. The beetles are then able to reproduce undisturbed for some time, and the next generation then searches for new host colonies. Left to themselves, a heavy beetle infestation can completely destroy a bee colony within a week. For example, in the USA within two years from the discovery of A. tumida, at least 20,000 bee colonies had been destroyed by the mite.

A good management by beekeepers is necessary to protect against A. tumida. Maintenance of strong colonies, good husbandry and limited movements have proved to be key elements of protection. At present beekeepers in only a few countries have access to a limited number of insecticides to control the small hive beetle1. None of them are registered in Europe. In the absence of synthetic treatment options, beekeepers are forced to manually remove the beetles from their hives or lure them into traps.

Infestations of SHB can cause considerable financial loss to beekeepers (Delaplane, 1998). First, beekeepers experience a loss of products (sales) because the larvae defecate in the honey and cause it to ferment; this produces a frothy mess in supers and honey houses. Honey that is contaminated is no longer saleable and is also unpalatable to bees so it cannot be used as bee feed (Delaplane, 1998; Calderón et al., 2006). Second, beekeepers may experience a loss of assets, namely colony loss, since combs and entire colonies are sometimes abandoned by bees once they have become infested (Delaplane, 1998).Third, beekeepers experience an increase in production cost due to the extra time and labor needed to detect and control the beetles. In addition to these, beekeepers may bear additional costs to comply with obligations and requirements defined by control strategies established by (local, national or international) authorities. For example, they may incur in a loss of market (hence of revenues) as a consequence of the introduction of quarantines or bans on the movements of live bees out of the zone under protection.

Apart from the costs borne by the bee industry, invasions of SHB can cause large negative impacts on natural environment, i.e. external costs borne by the society as a whole. The decline in bee numbers due to infestations by SHB can result in a significantly negative impact on pollination in habitats where plants rely on bees (e.g. citrus trees). In this respect it is worth noting that the value of pollination is estimated to exceed the value of products from beehives many-fold (Delaplane and Mayer, 2000). Infestation can indirectly affect food production since bees pollinate more that 30% of the global crop production. Additionally, infestations by SHB affects the conservation of indigenous bees causing a decline in native bees, such as A. mellifera, with negative impact on bee biodiversity (Cuthbertson and Brown, 2009).

Finally, in case of regulation there is a burden paid by the public bodies (e.g. regional, government) for the eradication program including the costs for monitoring and surveillance (e.g. clinical inspections, sentinel apiaries), information campaign and control measures such as apiaries destruction and compensations paid to beekeepers (see next paragraph for details about these costs).

EU control strategy

In 2004, during an official import inspection, larvae morphologically attributable to SHB were intercepted in cages carrying Apis mellifera ligustica queens and accompanying workers, legally imported into Portugal from Texas, USA. The further spread of SHB was prevented by the total destruction, under official supervision, of all honey bees and hive materials in the apiary that had received the queen bees (Valerio da Silva 2014).

Given that the SHB is considered one of the major threats to the long-term sustainability and economic success of honey bee colonies in Europe, and that the risk of introduction into the EU had

1For example, in certain countries, such as the United States, Coumaphos (Bayer) can be used to combat SHB. been reported as moderate to high, and information sessions2 have been organized at regional and national level for stakeholders. In 2014, in the absence of an operational movement database, regional authorities asked beekeepers and their association to notify whether their apiaries represented a risk. “This is how the outbreak was identified in Sicily.” (DG(SANTE) 2016-8759 – MR)

The SHB was first reported in Italy on September 5th of 2014 (Mutinelli et al. 2014; Palmeri et al. 2015). The pest was reported for the first time in the municipality of Gioia Tauro, in the region of Calabria, an international port through which more than two million containers pass in transit per year from all over the world. A second outbreak was detected on 7 November in a migratory apiary located in the municipality of Melilli (37.27224 N, 15.06722 E), in the region of Sicily, southern Italy. This apiary was in the Gioia Tauro area from April to August 2014 and then returned to Sicily at the end of the productive season (Mutinelli et al. 2014). Until now (Table 2), this was the only apiary found to be infested by SHBs outside Calabria. Through December 2016, SHBs have been found in a total of 137 infested apiaries: 136 in Calabria and 1 in Sicily (INRC, 2017).

The potential risk of introduction and uncontrolled expansion of the SHB constitutes a legitimate concern in the EU. This concern has been reflected in the adoption of protective measures. Since being found in southern Italy, three EU decisions have been issued (EU 2014; EU 2015a, b) to enforce protective measures.

The EU strategy toward SHB eradication consists of the following measures

1. surveillance program based on Census/registry of apiaries and colonies and Clinical inspections 2. Destruction of infested apiary (2014 on) and compensation for destroyed apiaries 3. Requirement for bee movements (intra Eu and imports) 4. Movement restriction in the protection zone (IN and OUT)

1. surveillance program

The EU surveillance program to detect SHB was implemented in spring 2015. Monitoring for pest is a key step in the management of biological invasions as it allows to gain an understanding of the frequency with which a species is introduced into a specific area, the size of each introduction and the subsequent pattern of spread across the landscape (Moody and Mack 1988; Rouget and Richardson 2003). The data can for example be used to feed mathematical models aiming to forecast invasion and establishment patterns and determining the likelihood of success for control and eradication policies. In other words, monitoring forms the basis of adaptive management as it allows managers to learn about the responses to management actions and indicates whether a particular management strategy is effective or in need of amendments.

Apiaries in at-risk zones and throughout Italy were sampled and repeatedly inspected in accordance with the “Guidelines for the surveillance of the small hive beetle (A. tumida ) infestation” issued by the European Union Reference Laboratory for honey bee health in March 2015 (Chauzat et al. 2015). The surveillance activity was initiated by official veterinarians in collaboration with beekeepers to try and determine how far the beetle had already spread in the regions of Calabria and Sicily (Mutinelli et al. 2014; Mutinelli 2016a). In the protection zone (20 km around infected apiary) all apiaries were clinically inspected by official veterinaries of the Ministry of Agriulture (MoH) up to 8 times in a year. In case of SHB detection, the apiary is destroyed and beekeepers are eligible for compensation. If the inspection is negative, traps should be applied. In the 100 km surveillance zone,

2 Letters, emails, posters in municipalities were used to reach beekeepers and inform them about their duties and the risk posed by Aethina tumida. only apiaries selected on the basis of risk analysis or randomly are clinically inspected. Additionally, based on the size of the Italian national apiary registry, 164 non-migratory apiaries were randomly selected in northern, central and southern Italy, excluding Calabria and Sicily, and clinically inspected.

In addition to the inspection of apiaries in the protection and surveillance areas, a clinical inspection of the apiaries once back from migratory period based on risk evaluation and traps application

Table 1 – Beekeepers and apiaries in Calabria Region 2015 2016 2017 Beekeepers 685 756 966 Apiaries 1093 1491 2785 bee families 78456 Gross output 20 million

Table 2 – Inspected apiaries and positive cases by year and zones Inspected Positive apiaries cases 2014 Calabria Protection zone 20km 282 60 2014 Calabria Rest of C 808 0 2015 Calabria Protection zone C 20km 282 29 2015 Calabria Rest of C 808 0 2016 Calabria Protection zone C 20km 53 2016 Calabria Rest of C 147 2017 Calabria Protection zone C 20km Sentinel 86 2017 Calabria Rest of C 160 0 2014 Sicily Protection zone S 20km 185 1 2014 Sicily Rest of S 0 2014 Rest of Italy 492 2016 Sicily Catania siracusa Ragusa 134 2016 Sicily Rest of C 198 2017 Sicily Protection zone C 20km 164 2017 Sicily Rest of C 164 0

2. Destruction of infested apiary and compensation for destroyed apiaries

Eradication measures have been applied since 2014, including the destruction of all colonies at apiary sites whenever a single infested colony was found.

The control measures were taken at regional level (Calabria: Order 94 of 19/09/2014, Sicily: Order 01893 of 10/11/2014). The Health Minister issued a Decree law (19/11/2014) which confirmed the request of destruction of all hives in an infested apiary, and the financial compensation of affected beekeepers. These measures, while resulting in SHB eradication only in the Sicily region (European Commission, 2017), maintained a low prevalence and slow spread of the pest in the Calabria region.

So far, around 3600 apiaries were destroyed and 1.3 million euro were paid to beekeepers.

3. Restrictions on bee movements (intra Eu and imports) In addition to the measures used to create an automatic block on movements of bees in case an outbreak of exotic bee pests and diseases -for example, health requirements for intra EU movements of bees introduced by Directive 92/65/EEC, or animal health import requirements on live bees and bee products destined for use in apiculture adopted with Decision 2003/881/EC73- in 2014 the EU commission decision (Decision 2014/909/EU 12.12.2014) issued a ban on the dispatch of consignments of honey bees, bumblebees, unprocessed apiculture by-products, beekeeping equipment, comb honey intended for human consumption from Region Calabria and Region Sicily to other areas of the EU.

In addition to this, in 2016 the region of Sicily issued an act prohibiting the transfer of live bees in both directions between Sicily and Calabria, with possible derogations for pollination in Calabria (with no return).

Differences in preferences

IAS management is often driven by many heterogeneous public and private actors, such as beekeepers, farmers, landowners and managers, animal health professionals, veterinaries, agribusiness, conservation agencies, central government and local authorities, etc. IAS control measures damage existing economic interests, this explains why each group of actors has different preferences over IAS control measures and what is an acceptable risk level of incurring an invasion (e.g. Garcia-Llorente 2008; Humair et al 2014; Reed and Curzon 2015). These differences in preferences are frequent cause of conflict and reaching an agreeable set of actions towards the control of an invader can prove quite challenging (e.g. Liu et al. 2012; Touza et al. 2014; Marzano et al. 2015).

A key issue to contend with is justification of resource allocation between preventive measures (eradication) and actions in mitigation of existing problems (management framework).

In the case of SHB the EU Commission is in favor of eradication of SHB from the Region of Calabria in order to prevent the spreading of the mite to other regions and MS. The rationale of EU’s position is that preventing introductions is generally far more cost effective and environmentally desirable than measures taken following the establishment of an invasive, non-native species (Williamson 1989).

On the other side, beekeepers complain against the eradication strategy based on destruction of infested apiaries. In 2013, 70 beekeepers covering 60% of the regional sector started a group called “Save the bees” that called a halt of the eradication strategy and started looking for control measures alternative to the destruction under the assumption that, given after several years from the first identification the SHB has not been eradicated yet, a pragmatic acceptance of the invasion should be adopted.

Doubts have been recently cast about long term financial sustainability of an eradication strategy based on the destruction of infested apiaries and compensations paid to beekeepers. For example, in 2016, 3600 infected apiaries were destroyed and more than 1.3 million euro were paid to beekeepers. The total cost of the strategy is further increased by the expenses for official clinical inspections and for sentinel apiaries. This kind of considerations has led some researcher to support the pragmatic

3 In 2011 the European Parliament asked for a complete import ban on all live bees. However, it was noted that a complete ban on imports of live bees could encourage illegal imports of bees, which are difficult to control, particularly in the case of queen bees that can be easily hidden. This would have exposed the EU to an even higher risk of introduction of exotic bee pests and diseases. acceptance of the invasion and start a management strategy. Among other things, the management approach would allow researchers to test the use of traps and other management measures.

Another problematic issue is the restriction to movements. Long term movement prohibition for apiaries in protection zones represents a real challenge for beekeepers. For example, in Sicily, beekeepers explained that their hives became non-profitable, as they could produce only limited amount of honey, and needed to be fed the rest of the year. As a consequence, they were reducing the number of colonies in the blocked apiaries.

In Calabria, an important citrus production area (and used to be an area with intense transhumance), in 2015 the creation of artificial swarms for pollination in the protection zone was authorized. The registration of artificial swarms is not foreseen yet, and no measures have been adopted to ensure the destruction of the swarms after pollination (these weak colonies may be very susceptible to Aethina tumida).

Need for institutional coordination

In the case of SHB the effectiveness of the control strategy is mined by a fragmented Legal and Institutional Frameworks, and by low levels of coordination between agencies responsible for sanitary matters, agriculture and nature conservation. All these are common problems in IAS management (Shine et al. 2000). In consideration of such problems the IUCN - The World Conservation Union has called upon the use of a Strategic Planning Processes, the first step toward the definition of such strategy is to identify sectors and pathways associated with alien species introduction and/or use.

In Italy responsibility for SHB control is shared between various sectors at various levels. SHB quarantine, diagnosis of colonies and eradication measures are responsibility of Ministry of Health (MoH). Lower levels of government, i.e. Regions, are responsible for compensations (there is no co- funding by the Government or European Commission).

The absence of regional funds (as according to Law No 218 of 1988, Regions are initially responsible for compensation) caused significant delays in the delivery of compensation payments. In Calabria, no compensation was delivered to beekeepers before September 2015. In Sicily, the owner of the (2014) outbreak had not been compensated at the time of the mission: the regional authority explained that, although the compensation grid was straightforward for the loss of bee colonies, it took very long for all stakeholders to agree on the cost of destroyed equipment. Beekeepers’ associations also complained that compensation in Calabria did not cover 100% of the agreed loss (it covered 89% of the loss – according to Law No 218, the equipment is compensated up to 80% of its value.), and that the delay substantially affected the collaboration of beekeepers with the authorities,

The delays as well as the dissatisfaction with the amount of the compensation are mining the collaboration of beekeepers with the authorities and the notification of suspicions. For example, in 2014, eight of the 32 affected beekeepers had spontaneously reported the presence of A. tumida to the local veterinary services, while in 2015 all outbreaks were identified through official surveillance activities. The impression is that beekeepers have lowered their collaboration not to incur in the destruction of the apiary, hence in a loss of assets.

Another factor that may lower the collaboration of beekeepers with the control strategy is the lack of compensation for traps. The use of traps was found to be inconsistent, with half of the regions not using any, whereas the other half using them for both random and risk-based surveillance. The cost of purchase of traps was a factor that made some regions not using them; in some other regions, beekeepers’ associations purchased traps for their members. Finally, there is the risk that compensations may act as perverse incentive as there is the risk of fraudulent claims of the presence of the beetle in old apiaries in order to become eligible for compensation.

One possibility to enhance the incentive for cooperation among beekepers is through reward-based motivation. The inclusion of measures for the monitoring, prevention, eradication or control of invasive species can feasibly be incorporated into Agri-Environment schemes of the Rural Development Programmes. These schemes compensate farmers financially for any loss of income associated with measures that aim to benefit the environment or biodiversity. Unfortunately, the Region Calabria adopted a restrictive interpretation of the measures indicated by the Reg. UE 1308/13 and the National programme 2017-2018. The Reg. (UE)1308/2013 Section 5 “Aid to the apiculture sector” Article 55. 4. Indicate that “The following measures may be included in apiculture programmes:

(a) technical assistance to beekeepers and beekeepers' organisations;

(b) combating beehive invaders and diseases, particularly varroasis.

In other words, the Rural Development Program (RDP) can provide financial support for the cost of action and damage control (traps, inspections) in order to facilitate the collaboration of beekeepers with the control strategy. As a matter of fact, the regional program devotes all the financial support to combating varroasis only. It is not clear whether this is the result of explicit species prioritization or of lack of coordination between the MoH, the Ministry of Agriculture and the regional authorities.

Final considerations and future work

This paper is part of an on-going research project aiming to analyze the costs and benefits of the strategy of eradication of SHB in Italy. The final goal of the project is to perform a cost-befit analysis of the control measures used to eradicate the SHB in Italy.

This paper presents qualitative information describing the control measures currently in use, the conflicts of interests arising in the control of SHB and identifies the institutions in charge of the control measures. Our examples show the need for better coordination among institutions dealing with this invader. We explain that the eradication strategy poses problems of long term financial sustainability. In addition to this, we argue that the eradication strategy currently in use limits research on innovative controlling tools (e.g. traps, treatments, etc.).

In future research we intend to quantify the cost and benefits of the control strategy. As for benefits we intend to use a choice experiment approach. Choice experiments allow researchers to value goods by using individuals stated preferences in a hypothetical setting. More in detail we intend to elicit the beekeeper’s Willingness to Pay (WTP) to stipulate an insurance to protect apiaries against SHB. WTP can be regarded as an indicator showing if respondents are in favor or disfavor for a change from the status quo situation when comparing different alternatives. WTP results are particularly important where no market proxies or prices are available, as this is usually the case for public goods.

It is worth noting that insurance is not just a tool to elicit WTP. In view of the recent shift of Common Agricultural Policy(CAP) away from direct public intervention towards the support of public–private partnerships that help farmers to cope with the risks they face. Recent CAP reform has introduced three different risk management measures that are based on the developments of public–private partnerships within the framework of the EU Rural Development Policy (RDP) namely insurance premium subsidies, mutual funds, and Income Stabilization Tool (IST). In consideration of this, mandatory insurance against damage caused by SHB could be a viable alternative to compensations currently paid to beekeepers.

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