Issues and gaps in international guidance and national regulatory systems affecting international live insect trade

Summary The distinct histories of exchange of insects and sheer diversity of the insect species shipped, their handling, and the purposes for shipments, have both created and been subject to a complex regulatory landscape. A review of global production, shipping and use experiences from a range of perspectives showed gaps and inconsistencies in international guidance and national implementation for this activity. Private carriers add another layer of uncertainty that is disproportionate to the risks, resulting in variable practices and charges. The issues identified relate to the various objectives and authorities which interface with international movement and trade in live insects. The potential benefits – from pollinator services, biological or genetic control of pests and disease vectors, and the enhancement of international scientific research and innovation – rely on a more evidence-based and efficient approach to trade in insects; this in turn requires an improved and widely accepted risk management landscape for insect trade.


Introduction -the challenge
Every year, billions of live insects, and other arthropods (mites, ticks, spiders, etc.) are shipped across political boundaries and ecological zones, as outlined throughout this thematic issue of the OIE Scientific and Technical Review. Some of the international transfers of insects are non-commercial trade but many of the shipments are for commercial purposes, both of which often contribute to societal priorities that would justify a public good approach to expedite the trade. The potential benefits supported by trade in live insects, outlined in the Introduction of this thematic issue (Mumford & Quinlan [1], this issue) can be 41_1_18_Quinlan et al -pre-print 4/34 this type of trade and the various objectives of the guidance and legal framework under which it was developed.
Guidance that is specific to a particular use has ensured safe and effective large-scale shipments of live insects for decades. Uses covered include biological control [5]; or for handling of a particular species, strain, or risk profile of insects or other arthropods (e.g., insects for large areawide control programmes [e.g., 6]); or insects moving from research lab to research lab. These examples of guidance, however, are not comprehensive in regard to the issues faced by shippers, carriers, and importers. Also, those successfully shipping using these usespecific guidelines often have greater purchasing influence or official recognition, e.g. as a government programme. In contrast, researchers working with smaller populations, such as laboratory-reared insects or those preparing pilot studies, or in the small or medium enterprise private sector, have reported barriers when trying to ship, even when the insects could be considered lower risk (e.g., if documented as infertile or sterile and thus not able to persist in the environment).
There are cases where small-scale shipment of live insects can cost as much as 100 times or more what it costs for a similar-sized or weight package of other material going on the same route, because the courier has classified the insects as hazardous (Wohlfarter et al. [7], this issue). This skews the market in favour of established, and/or larger-scale insect shippers and disproportionately affects research or academic institutes, public entities, or businesses that require small shipments to develop and pursue opportunities for innovation, such as seed colonies for specific genotypes (Simoni [8], this issue). These barriers do not appear to be evidence-based nor proportionate to the actual risks presented, in many cases [9]. Longer-term fair sharing of benefits can contribute to the opportunities for innovation and economic improvement of the source nations as they develop mechanisms linking insect resources to their own enhanced industry and innovation on the one hand, and the incentives required to promote conservation and sustainable use of biological diversity, on the other [11].
This review of the issues and gaps in the regulatory landscape was motivated by the need to address current barriers to shipping in order to facilitate the benefits, rather than particular concerns over any threats A few countries had a framework for insect trade, such as import of industrial species, before international guidance was available [17].
National regulation generally, however, follows or aims to implement international standards and obligations in matters relating to international trade. In the absence of national regulations specific to insect trade, in the past many countries simply apply regional or international standards [18; 19]. In fact, no comprehensive national regulation of insect trade has been found by the authors. Instead, there is a patchwork of different instruments, both legally binding and voluntary. A recent survey of those involved in live insect trade (described in Oliva et al. [20], this issue, although without details on this point) revealed a range of national authorities and institutions that would have a role in oversight of insect trade.

Insects with potential impact on plant health
Movement of insect pests that are potentially harmful to plant health (managed crops and forestry, or natural flora) is covered by the IPPC and its associated guidance, although many of the International  [19]. The intention was to support the benefits of integrated pest management that is designed to employ fewer chemical pesticides.

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In addition to global guidance, Regional Plant Protection Organizations (RPPOs) and regional trading blocs have developed related and complementary standards, aligning to standards and terminology endorsed by the member countries of the IPPC. In the case of intentional introduction of insects for beneficial purposes relating to plant health, regional standards for the introduction of biological control agents and/or other beneficial organisms generally provide far more detailed guidance than ISPM 3. For example, the standards under the Comité Regional de Sanidad Vegetal del Cono Sur (COSAVE) provide a regional framework, described by Sanchez et al. [13], this issue. The North American Plant Protection Organization (NAPPO) also has regional standards regarding the process for certification and for petition for first release of non-indigenous biocontrol agents and non- It is the opinion of the authors that there is insufficient guidance when the national Veterinary Services of the exporting country are asked to provide documentation on the health status of a specific population or consignment of insects, or for other arthropods. The request, therefore, can be open to interpretation by individuals, private businesses, and official authorities when faced with insect trade, thereby reducing confidence in the certification system [36].

Food and feed
At the international level, use of live insects for food or feed comes under the mandate of the Codex Alimentarius, which historically classes most insects as filth or contamination when present in food and feed products, rather than as a class of food themselves [37,38,39].
Therefore, it is not surprising that national regulation of live insects for human or animal consumption is fragmented or still emerging. In Europe, for example, regulatory approaches vary from outright bans to specific guidance on production conditions and food sources allowed 41_1_18_Quinlan et al -pre-print 10/34 for predatory insects [40,41]. Although insect trade for food and feed is not the focus of this special issue, Niassy et al. [42], this issue, join others to call for Codex Alimentarius to develop guidance for insects as food and feed. This would focus on the impact to end users (consumers and livestock), but also could contribute ideas for a hazard analysis and critical control point (HACCP) approach to maintaining quality and safety through the production process [42].
Risks associated with transport per se would generally lie outside of the Codex Alimentarius domain, other than the additional time allowing microbiological contamination, and possibly insects, to grow and develop further during transport.

Conservation considerations relating to insect trade
A wide range of species with various characteristics are being shipped or hand carried after field exploration by entomologists for research purposes. Collection, possession, import, export, and study of live or dead insects may be subject to restrictions relating to conservation of biodiversity, plant, and animal health, as laid out under international agreements. Insect species can be threatened from excessive harvesting in the wild for the purpose of trade, in particular for hobbyists or for use in alternative medicines (as the case presented by Goka [43], this issue, and [44,45]). There has been limited analysis of such risks, for example by the International Union for Conservation of Nature (IUCN), and thus limited restrictions under the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) despite global concern over a general reduction of insect numbers and diversity [46]. Many researchers, conservationists, and regulators [47] have called for a coordinated conservation and recovery plan addressing the decline in natural insect populations and proposed IUCN or the United Nations Environmental Programme (UNEP) to monitor progress.
There is no single intergovernmental treaty or entity that oversees trade in pollinators, either the entire range of species or insect pollinators. As already noted, the OIE recognised the risks from this trade, but has limited its work to date to Apis species. Currently, compliance with requirements aimed at protecting biodiversity and fair sharing of benefits from access to biocontrol agents, for example, does not have a well-defined process in the majority of cases [56,57]. To date, efforts to support access and sharing of benefits for the biocontrol agent collection and research -a largely non or low profit activity -has led to requirements for various types of documents, under different regulations, subject to a wide diversity of government agencies, and depending on the field of use and origin, with variation between countries even in the same region [58].
The complexity of overlapping authorities preventing the introduction and spread of invasive species can be seen with the example of forest pests: a recent review [59] includes an analysis of international instruments that directly or indirectly affect the management of potential pests to prevent invasion. Many of the recommendations for 41_1_18_Quinlan et al -pre-print 12/34 integrating the numerous sources of guidance to apply to one sector would hold true for preventing insects moving in trade from becoming an invasive species for the importing territory.
Even if a shipper is following ISPM 3, the dispute mechanism established under the IPPC could not be used for cases related to impacts of insect trade outside of plant health, but in theory the World Trade Organization's Sanitary and Phytosanitary Committee could possibly consider cases on a broader scale. It is unlikely that a country would use such a time consuming and politically charged forum to resolve any issues related to insect trade, however; it is more likely that contract law would be relied upon for ensuring delivery of live insects as required.

Specific rules for genetically modified insects
The export, transport, and import of transgenic insects are subject to requirements that are often additional to those noted above, although national frameworks may operate through biosafety committees that are comprised of representation of the same authorities already noted [60]. The international treaty of most relevance is the Cartagena Protocol on Biosafety to the CBD [61]. This lays out a global framework for notification of shipments of genetically modified organisms, including insects [62], for release in the importing country thereby allowing national authorities to manage risks and concerns in a timely manner.
As with other international guidance, the guidance is to be interpreted in regional or national legislation and regulations. One of the earlier examples was NAPPO's guidance on the importation of transgenic arthropods [63], which is since archived due to change in authorities in two of the member countries.

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Underlying this separate agreement is the idea that products from modern biotechnology are inherently different from those modified in other ways, such as by traditional breeding, introduced symbiosis, or in other ways; this assumption does not appear to be supported by the years of experience since its ratification, primarily with genetically modified crops. There is a sense, as well, that by restricting these frameworks to the understanding of genetic modification concurrent to the period of development of these instruments, rather than a scope that covers any novel traits, novel uses (such as [52], this issue), or production methods, that national legislation and regulations have already fallen behind the trends in use of altered insect populations.

Commercial issues, quality, and usefulness issues for insect trade
In addition to protection goals, insect trade is subject to requirements regarding fraud, protection of intellectual property, and other commercial requirements, which may be managed under contractual arrangements governed under international business law, memorandums of understanding, material transfer agreements or other means. These commercial issues associated with identity, ownership and some of the uses of live insect trade are not addressed here.
Another aspect of shipping any living product is maintaining quality to ensure that the insects serve the purpose behind the shipments in the first place. This means that some shipments also are managed under "fit for purpose" standards, relying on guidance about shipment of particular types of live insects in order to ensure utility upon arrival.  [68,69]. A detailed manual for quality control of Tephritid fruit flies is also available [70]. Guidance for mosquito programmes is also under development and addresses some aspects of safety and risk, but also discusses quality measures. All of these guidelines mention quality control, meeting phytosanitary requirements, and meeting export and import country documentation requirements. The potential role of sanitary (Veterinary Health) certificates is not noted in any of these guidelines.

Guidance from the transport sector
Much of the trade in live insects is via air freight. Environmental conditions of shipments are optimised for insect survival and quality (such as described for biocontrol agents by Vila et al. [10], this issue), as they move from a production site or wild harvest, through domestic and international transport, to the ultimate destination after clearing the usual border checks. These conditions aimed at maintaining the utility of the shipments, of course, also contribute to other types of risks by keeping the insects viable.
Therefore, the final aspect to the current regulatory landscape is the guidelines, norms, and standards applied to any type of commercial transport (see for example Simoni [8], this issue). The airline and freight courier industries refer to the International Civil Aviation Organization (ICAO) of the United Nations and the private International Air Transport Association (IATA) to guide them on handling potentially hazardous materials.
The IATA has cooperated with the biocontrol industry to provide specific details for packaging of mites and insects in the latest guidance Ideas for improved coordination appear below, with further discussion in Quinlan et al. [71], this issue.

Conclusions
Every year there is a number of shipments transporting a variety of species and strains, and representing a broad range of interests in trade of live insects. There is every reason to expect increases in trade in live insects and insect-based food and feed [e.g., 73,74]. Presently, trade occurs under a variety of regulations and oversight. This paper aims to highlight the importance of guidance and the need for evidence-based risk assessment and management to ensure safe international trade of insect while minimising unjustified trade barriers and simple inefficiencies in shipping. It also argues for arthropod-specific guidance, rather than working from the paradigm of insects as a subset of all animals. Where guidance exists, high level agreement on the integration of various authorities or the hierarchy of authorities is needed. Enhanced transparency in this guidance will support suppliers, users, shippers, and regulators.
In light of the current gaps and inconsistencies in guidance for shipping live insects and other arthropods -within the sector but also in comparison to other time sensitive trade -the authors propose further discussion among stakeholders to agree on pragmatic solutions.
Discussions should include international organisations with mandates relating to ways in which the insect trade affects both health protection and conservation, and economic and innovation objectives, including but not limited to: OIE, IPPC, CBD, IAEA and FAO; national bodies involved in regulation of insects and their trade, as well as those potentially using or advancing benefits based on trade and exchange of insects; recognized advisors and facilitators of these benefits, such as CAB International; associations or guidance bodies for the shipping sector in general, including ICAO and IATA; and research and academic bodies with objectives affected by this international trade.
Coordination should be aimed at promoting a more transparent and pragmatic process for live shipments, which will lead to rationally avoiding both potential risks and scientifically unjustified barriers. New initiatives must avoid imposing additional requirements for trade already moving effectively, such as several large volume sectors (e.g., for sterile insect technique [12,74]). A harmonised risk-based approach may also provide a more suitable platform than existing regulations or guidance for consideration of future innovations or emerging risks, and the most appropriate risk management options for these, as the trade in live insects grows and changes [75].
The range of issues reinforces the authors' view that discussions around rationalising regulation of or guidance for insect trade will need to be broad and flexible. We believe that basing decisions about shipping on evidence of risk and proportional management, where needed, is the best way to support the benefits supported by live insect trade -through research, industrial outputs, and field programmes relying on safe delivery of insects, when and where needed. contributions to early discussions that laid the foundation for identifying other topics for this special issue.    Table II Aspects of shipping live insects to be considered in coordinated guidance  Procedures for assessing risk, particularly for inactive life stages (eggs, pupae) or for strains modified in ways that alter risk  Characterisation of relevant health or other risks related to specific shipments (species, diseases, origin, and destination, conditions in transit)  Review of production and handling procedures as a proxy for health certification of individual shipments  The minimal required content/procedures to carry out health certification, if required, and appropriate expertise and qualifications to do so  Design and audit processes for certified production systems  System of notifications to shippers, inspectors, and recipients  Standardized approach to specification of approximate numbers, volume, or weight of insects  Documentation (labels, permits, handling instructions)  Importer/Exporter authority coordination and recognition  Shipper/Courier rules and acceptance of live cargo  Packaging requirements (security, viability, inspection access, temperature and humidity monitoring en route)  Routing permits (through specified official inspection ports and for ports of transit)  Transit point requirements  Liability related to survival of shipped insects given diverse and uncertain routes  Emergency destruction procedures 41_1_18_Quinlan et al -pre-print 33/34

Box 2 Cases when risk management based on biosafety measures can be evaluated generically
The key risks during the transport stage relate to maintaining the "usefulness" of the insects and avoiding their escape. If containment of the insects is secure throughout transport, then concerns around exposure of the environment or workers and around the integrity of the shipment and identity of the insects being shipped, become irrelevant. Packaging that is universally recognised for achieving containment can reduce the probability of escape and associated risks to a negligible level. Adding clear instructions about the proper actions to take if the consignment is lost or delayed past the point of utility further ensures that the risk of escape is managed. Special handling is already required for insects that are genetically modified or potential vectors, particularly if infected for research purposes [64].
In addition to evaluating the packaging, carriers, importers or inspectors may want information about the security of the facilities providing and receiving the live insects.
Beeckman & Rüdelsheim [65] review the regulations associated with biosafety in relation to facilities and labs. Hayes & Quinlan [66] note some characteristics relevant to insects, as does the Arthropod Containment Guidelines, such as potential mobility, and propose levels of containment by classification [35]. These consensus guidelines now include insects with gene drives as well [67], in other words insects with higher risk profiles.
None of these precautions guarantee that the quality of insects will be maintained, but the safety concerns are covered by proper containment. Biosafety and delivery on time under prescribed conditions should be the primary concerns of carriers, but they are likely to also look for reassurance that the documentation is in order so that delays at Customs in the importing country can be avoided.