International live insect trade: a survey of stakeholders

related arthropod) trade and potential challenges to safety and efficiency. Target respondents had experience in the areas of biocontrol, sterile insect technique, entomological research, and regulatory affairs. Although the survey was sent globally, the perimeter of answers was unintentionally biased towards Europe and European-related trade. Interest in Europe is high, as this region is developing a comprehensive framework to promote the use of beneficial insects to replace pesticides. The survey also explored knowledge and relevance of some international agreements on movement and risk management of beneficial or invasive insects, benefits sharing, and liability. Knowledge of the various regulations was generally poor, and those responding to the questionnaire highlighted a perceived lack of clarity regarding live insect shipments in existing international regulations and guidelines. Almost two thirds of the participants reported reluctance by couriers and carriers to accept live insects for shipment, and three quarters described occasional to systematic delays or rerouting that resulted in reduction in quality or viability. As a result, some respondents reported that they hand-carry live insects, mostly when dealing with small quantities. Respondents described being directly involved in trade covering 70 species of live insects and ticks being transported amongst 37 countries, with volumes that ranged from less than ten to over a million insects per shipment. Of these insects, 30% were potential vectors of pathogens to humans or animals, 42% were potential plant pest species (including, some used for biocontrol), and 17% were classical biocontrol agents. The results of this survey begin to define the current scope, scale, and issues for those exporting, carrying, importing, regulating, or otherwise involved in shipping live insects and ticks across political boundaries; the survey seeks to attract support from regulatory bodies and shipping operators to facilitate safety, efficiency, and consistency in this underdeveloped sector.


Introduction
The topic of live insect transport has been attracting more attention as the need internationally for such shipments has grown. Among the reasons for this emerging interest are: limiting risks related to invasive species or protecting biodiversity and facilitating trade activities related to biocontrol. Live insect shipments can cover a wide range of purposes, mainly biocontrol, pollination, and research activities, but also feed and food industry stock, insect product industries (e.g. silk, live bait), and personal or commercial collections (hobby, zoos and butterfly houses, pets). The overall volume of insect trade, however, has been unknown except for specific cases such as shipments of biocontrol agents by large companies or sterile insects as part of area-wide pest management programmes (1, as discussed in Enkerlin and Pereira [2], this issue).
Shipments of live insects for research projects are often infrequent and of limited numbers, although they might be of considerable value, sometimes being unique samples.
Be it for research or ongoing biocontrol programmes, it is paramount that shipments are handled according to good practice to improve the chance that a consignment arrives alive and in good condition to the recipients. Dominiak & Fanson (3) reported how stress related to transport conditions may affect the viability of sterile flies released as part of pest management programmes, which has a direct impact on the success of the protection services to growers. Shipping conditions also determine in many cases the appropriate life stage for transporting insects and the way in which they must be packed to travel well. Documentation, labelling, and logistics can affect the duration of shipments.
A scoping meeting on insect shipment issues held in 2018 reported the general views that (a) the current practices and regulations in place often differ between countries and there is a lack of consistent guidance for both senders and freight agents; (b) there were numerous constraints on shipping live insects (few carriers, delays, costs) for some stakeholders; and (c) that actions circumventing existing rules were Rev. Sci. Tech. Off. Int. Epiz., 41 (1) 41_1_3_Oliva -pre-print 4/36 sometimes taken to avoid administrative effort, loss, delays and costs (Quinlan et al. [4], this issue).

The survey
A survey was designed to explore solutions to facilitate, improve and secure insect shipments, and assess the risks associated with human, animal or plant health related to international live insect shipments. The World Organisation for Animal Health (OIE) was interested in the survey results because of its role to help protect animal health (5). The This survey was only an initial exploration of the issues of live insect shipment and was not intended to be representative of the many stakeholders likely to be involved in such shipments. The aim was to identify a broad range of interests and experiences, which could form the basis of a more representative analysis in the future. The results provide insights on the wide range and complexity of live insect shipments worldwide, which should be conveyed to the freight transport community, as well as national and international official bodies. Moreover, the survey supports the need to investigate further the potential risks associated with animal or plant health and the need to provide more guidance to help to mitigate these risks. A final section allowed the participants to rate their knowledge and understanding or applicability of various regulatory texts or guidelines.
Respondents were given the opportunity to provide their name and institution, although this was not required for completion of the questionnaire. All results shown here are anonymized, and no survey participant details are published.

Survey analysis
Analysis of the responses is primarily descriptive. Detailed statistical analysis is not appropriate with an unknown response rate and an unrepresentative sample. The number and diversity of responses proved sufficient to show a wide range of issues and scales of shipments. It is not possible to determine how many potential respondents were aware of the survey, but 164 initiated a response while only 72 completed the survey. All respondents except two identified their institution and location, indicating that repeat voting is not a concern for interpretation of the results. One participant who reported being involved only in dead insect transport was removed from the analysis.

Limitations of the study
The study only focuses on live insects and ticks. The movement of dead insects or parts of insects, bees, spiders, and other arthropods is out of the scope of the survey. The study does not distinguish the health status of the insects being traded. It focuses on the shipping conditions of the insects and not on the rearing procedures or husbandry details of the insects, which may also affect risk.
As regulations and guidelines are different between regions, some of the presented data might not be scalable at the global level. The survey study population is also more biased towards the EU countries in comparison to the rest of the world, due to the sampling approach.
The survey is unintentionally more biased towards the biological control sector, as well, because the authors belonged mostly to this field and the questionnaire was disseminated towards their network extensively. The community using insects for recreational purposes (pets, collections) was not reached by the survey dissemination. The insects for food and feed sector were limited in our survey since they are primarily traded as processed insect products rather than living insects.

Global data
In total, 45 participants answered as mainly 'importer' or 'exporter', while 26 participants responded 'neither'. This last group is then referred to as regulator/advisor.

Importers or exporters
The 45 respondents in this group were from 34 organisations, 14 countries and one oversea territory. The participants were mainly from research organisations (63%) or commercial industries (14%) (Fig. 1).
Of these, 61% have been involved in shipment of live insects and/or ticks for more than ten years, indicating a substantial level of experience.
They were asked if their organisation was certified as a 'known consignor'; which was described in the survey text as follows: The Known Consignor scheme means a consignor who originates cargo or mail for its own account and whose procedures meet common security rules and standards sufficient to allow carriage of cargo or mail on any aircraft. Regardless of destination, international outbound cargo that originates from a Known Consignor does not require further examination before uplift onto an aircraft. [6] The majority of the respondents did not know (59%, N=44). Only two respondents answered positively, one was mainly exporting (Biological control), the other mainly importing (Research); they reported to be involved in live insect transport for six to ten years.

Regulators or advisors
The participants declaring to be neither directly involved in export or import shipment belonged to various categories: Government or regulatory bodies, United Nations organisations, non-governmental organisations (NGOs), industry federations, grower organisations, consultants, or research centres. They are referred to hereafter as 'Regulators or advisors'.

Diversity of insect shipped
Participants could rank up to ten species of live insects and/or ticks that they regularly ship, according to volume. A total of 70 species were reported. Eleven species were cited by multiple participants. Table I describes some characteristics of the ones shipped by more than two different participants Of the insect species listed, three main categories of insects emerged (based on risks or use): 30% were potential vectors for human and/or animal diseases, 42% were (potential) plant pests, and 17% were biological control agents (Fig. 2).
Insert Figure 2 here Three cases involved weekly shipment of sterile insects, shipped as adults, maintained at a specific temperature. One of these shipment sets was reported at a weekly frequency for an annual number of specimens shipped of over a million, representing an estimated 500−1,000 kg in total annual shipments. The other two were weekly or seasonal shipments, representing annually under a million individuals for an annual total of 10 to 100 kg of insects. One case involved shipment at the pupal stage, but no information was given on the shipment conditions.
Among the plant pest insects, five species represent exotic biocontrol agents usually used against invasive plant pests. Insects shipped for biocontrol activities were described to be shipped as eggs, larvae, or adults. Another respondent reported the shipment of adults from a plant pest (Aphid species) intentionally infected with a plant pathogen; they were transported via hand-carriage at a specific temperature range, in small numbers of insects (10 to 100 annually) and declared as live insects for research. Six species of ticks (from the genera Dermacentor, Ixodes and Rhipicephalus) and samples to be identified were reported to be sourced from wild or confined rearing (or a combination of both); they were shipped mostly as adults and sometimes as eggs. Potential insect vectors of human and animal pathogens (e.g. mosquitoes, culicoides, tsetse flies) were sourced from the wild or confined rearing, and were shipped within and across continents.

Insects transport worldwide
The conditions of shipment were examined for each case of shipment described, that is, for given respondents and given species (up to three 10/36 species described per respondent). Most of the cases involved transport by air (85%, N=52), while 4% were by rail and 4% by road; none involved transport by sea.

Transboundary movement
The shipments described involved a diversity of routes between neighbouring countries or between continents ( Europe (particularly France), which is a bias due to reaching more stakeholders from this region.

Insert Figures 3, 4, 5
Sourcing Wild sourced (harvested) accounted for 33% of the shipment described, while another 33% were from confined rearing (with no free movement outside the designated farm or laboratory premises) (Fig. 6A). The sourcing could differ for a given species, as reported by 23% of the respondents. Among the shipment of wild sourced insects, 56% were insects of agricultural interest and 44% were potential human/animal disease vectors. Some respondents indicated shipping them as eggs, larvae, pupae, or adults; however, most respondents did not report this information.

Physical conditions
There were few answers regarding the developmental life stage of the insect and the physical conditions of shipment. However, the data  6B).

Hand-carrying
Most respondents (64%) reported that they never hand-carry their insect packages (Fig. 6C) Dermacentor marginatus, D. marginatus). These shipments were mostly monthly, then quarterly or seasonally (so could be repetitive shipments during a season). They were done between European countries (continental and overseas) and between continents.
Shippers have a responsibility to be aware of when declarations are legally required. Reasons given as to why to avoid this declaration are discussed elsewhere.

Declared shipments
The majority of the shipments described (54%) were done with declarations regarding the status of live insects. About a third of them were shipments of under 100 individuals, and another third were shipments between 100 to 10,000 individuals, while one shipment concerned over a million insects. Of those shipments with declarations, 29% were annual, 39% were seasonal, 14% monthly, while 18% were weekly.

Import and export documentation
The most common documentation reported as accompanying shipments was a material transfer agreement (MTA) (43%, n=19) and import permit (41%, n=18). However, it is important to note that 23% (n=10) of the participants often do not provide any documents; one of those participants considers that no declaration is required. Another 9% (n=4) indicated that they are not aware of the documents required, among which an e-commerce shipper sent weekly shipments of 10,000−100,000 specimens of two species of biocontrol agents within Europe.
Rev. Sci. Tech. Off. Int. Epiz., 41 (1) 41_1_3_Oliva -pre-print 13/36 It should be noted that failing to provide required documentation for international shipments, whatever the material, could lead to fines or prosecution, depending on the case.
For 23% of the shipments, a sanitary/veterinary certificate was attached.
A wide range of alternative documents were also provided by some respondents, such as: CITES declaration (n=4), mutual agreed terms (MAT; n=4), quarantine license (n=5), letter of authority (LOA; n=8), but also invoices, insurance forms, origin of goods statement, packing list, etc. Exporters and importers described a similar range of documentation.

Regulatory knowledge and applicability
Regarding the regulations section, the questionnaire focused on the relevant regulatory texts and international guidelines in the field as listed in Table II (details on these texts and guidelines can be found in Quinlan et al. [3]). Respondents indicated low levels of proficiency and a lack of familiarity with the relevance of these agreements to their work.
Insert  (15), which relates to production of insects for food and feed, was unknown to all respondents and considered not relevant for their activity of shipping live insects.

Regulation of insect movement
Some 43% of respondents declared that the country in which they are based has a national regulation relevant to insect shipping, while an equal proportion did not know about their national regulation status.
Four respondents declared that there was no national regulation in their field, and that they had no private or academic guidelines either.

Procedures and regulations
Difficulties were also reported due to the unavailability or the lack of guidelines for insect/tick shipments (70%,) and the lack of a regulatory body for the authorisation of those shipments (80% The lack of appropriate commercial insurance covering living biological products (insects) was reported as never being a difficulty by 73% of respondents. It was sometimes considered an issue for 13% of participants.

Regulators or advisors' perception of international movement of live insects/ticks
Only 27% of the respondents in this group belonged to institutions in charge of drafting, implementing, or enforcing legislation or protocols related to international movement of live insects/ticks (Fig. 8A). Over half (57%) reported knowing the national institution regulating the authorisation of the international movement of live insects/ticks in their country (Fig. 8B). When asked whether they considered that there is a need for more specific guidelines and/or support, at the national or international level, for the international movement of live insects/ticks, 88% of respondents agreed (Fig. 8C). The only two responding negatively did not belong to regulatory bodies but were in the advisor category.

Type of support to improve international movement of live insects/ticks
Most respondents, whether involved in the shipment or in the regulators group, would recommend greater harmonisation of policy, guidelines or international standards and national legislation regulating live insect shipments. Regulators and advisors, in addition, agree on needs for better enforcement and stakeholder training (Fig. 9).
Insert Figure 9 Discussion

Knowledge of regulations and guidelines
Participants were asked to rate their knowledge and level of applicability of various international regulatory texts and guidelines related to live insect movements. The applicability of the Nagoya Protocol (7) to international insect movement should be high as several instances relate to wild samples. However, the results of the survey showed that there is still a lack of knowledge or compliance even from users involved in research activities from field-sourced samples. The