Quarantine facilities and legal issues of the use of biocontrol agents in Brazil

The objective of this work was to address the classical biological control of pests in Brazil, regarding procedures to import and export native biological material. A brief introduction will be given on the current legal issues on the use of biocontrol agents, as well as some considerations on the existing quarantine pests and actions already carried out in the country. The safety in the introduction of exotic organisms is important for Brazilian phytosanitary defense and for a higher adoption of classical biocontrol, making it available for integrated pest management (IPM). Legal and normative aspects establish the procedures that must to be adopted, not only to protect bioprospecting and native organisms, but also to minimize risks to the national genetic patrimony associated with the introduction of exotic organisms. Furthermore, the import/export procedures adopted for vegetal and useful organisms for pest biological control and for other genetic material must be subjected to phytosanitary measures performed in government‐certified quarantine facilities and diagnostic laboratories. Finally, the quarantine activities listed here are strategic for safeguarding the country from potential problems arising from border transit of living organisms.


Introduction
Interest in the use of biological control techniques has grown worldwide as an alternative to chemical control, especially due to the adverse effects of chemicals on the environment and human health.In this context, international attention to agricultural production has come hand-in-hand with the use of alternative and less environmentally aggressive means of pest control, aiming at favoring the sustainable use of agroecosystems (Waage, 1996).
The classical biological control of pest organisms involves the introduction and the establishment of alien biological control agents.Some factors leading to an increase in the use of classical and other types of biological control include: the rapid growth in the international trade of agricultural products, stimulated by the General Agreement on Tariffs and Trade (GATT), with a consequent tendency for an increase in the introduction rate of new exotic pests; the global commitment to new international agreements based on Agenda 21, the standard document for development and environment, as well as for environmental policies from international research funding agencies for the use of integrated pest management (IPM); the growing concern with environmental conservation and biodiversity, according to the Convention on Biological Diversity, which emphasizes the use of biological control; and the growing number of biofactories, making biocontrol agents available for mass release (Waage, 1996).
When introducing alien organisms, safety is of vital importance, both for Brazilian phytosanitary defense and for a higher adoption of classical biological control, making it available for IPM.Legal aspects establish the procedures to be adopted, not only to protect native organisms, but also to minimize risks to the national genetic patrimony associated with the introduction of exotic organisms.Some of these organisms will be presented and discussed subsequently.

Procedures for the importation and exportation of biological material
The processes to import and export biological material are determined in specific norms and procedures established by Ministério de Agricultura, Pecuária e Abastecimento (Mapa), the Brazilian Ministry of Agriculture, Livestock and Food Supply (Brasil, 1994).
In general, the first step to import beneficial organisms as agents of biological control of pests is requesting an importation permit to Mapa.In order to do this, public and private institutions must submit one the form shown in the flowchart presented in addenda I and II of Ordinance 74 (Brasil, 1994).The parties interested in importing the beneficial organism must also justify the reason for doing so.Other information that must also be informed include: the number of shipments and of organisms to be received per shipment; the possible suppliers; and locations where the organisms to be introduced will be collected.Additionally, the interested party must previously contact the responsible quarantine facility, which must issue a written document agreeing to import and process the organism.
Regarding the exportation of organisms, the interested parties must also take into consideration the Convention on International Trade in Endangered Species of Wild Fauna and Flora (Cites), which regulates the exportation/importation of animal and plants, including their parts and derivatives.In Brazil, the exportation of organisms requires permits issued by Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (Ibama), the national environmental protection agency (Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis, 2015).
In case the quarantine facility agrees with the introduction of the exotic organism, operational procedures and predefined actions must be outlined in a quarantine technical document that will be sent to Mapa.The activities developed in the quarantine facility are performed to safeguard the country against the introduction of contaminants and/or the escape or dispersion of possible undesirable organisms, such as arthropods, mites, plant diseases, hyperparasitoids, and microorganisms in general, which can be associated with the beneficial organisms or with the substrate in which they are transported in.Therefore, the quarantine of biological control agents is a screening process to technically subsidize Mapa's final authorization for the release of exotic organisms in a new region, while simultaneously excluding all contaminants.Since Mapa may authorize the final release of an exotic organism.When considered inappropriate, the final release is prohibited and the imported organism is incinerated in the quarantine facility (Sá & Pessoa, 2015).

Current legal issues of the use of biocontrol agents in Brazil
Certain legal and normative aspects establish the procedures to be adopted in order to safeguard the use of prospecting and native organisms, but also to minimize risks to the national genetic patrimony associated with the introduction of exotic organisms.Therefore, the legal requirements in Brazil were elaborated to assure that all introductions, related to research activities or to commercial purposes, are done using official criteria, conducted by certified institutions and people responsible for specific activities, as defined both by Mapa and Law 13,123 of May 20 th , 2015 (Vasconcelos, 2012a(Vasconcelos, , 2012b;;Brasil, 2015).
Normative Instruction 03 of Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio), for the conservation of biodiversity, dated March 1 st , 2014, sets the rules for the collection of biological material and enables researchers to obtain permanent or temporary authorization to perform the collection, capture, and transportation of said material.When required, the researcher must request authorization to collect the material through one of the following systems of ICMBio or through equivalent state agency: "Sistema de Autorização e Informação em Biodiversidade" (Sisbio), an authorization and information system for biodiversity; or "Sistema Nacional de Gestão da Fauna Silvestre" (Sisfauna), an authorization and information system for fauna.In short, the interested researcher should perform the following steps: First, register the following data in the SisFauna or Sisbio systems: personal information, including name, individual taxpayer registration number, and mailing address; name of the scientific institution to which he or she is linked to or for which he or she was nominated; and curriculum at the Lattes platform, a curriculum database of Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), the national council for scientific and technological development.
Second, describe the research proposal, including, at least: objectives; activities to be carried out; methods to be used; taxa that will be collected, captured, marked, or transported; intended use of the collected material; areas and periods for sampling collection; and whether or not the access to the genetic resource or to the associated traditional knowledge is planned, as provided by Law 13,123/2015(Brasil, 2015).
Third, inform names and individual taxpayer registration numbers of team members, except field assistants and vehicle drivers, for which the authorization should also be issued to.
After this, a temporary authorization may be given for a specified period, according to the schedule of activities, and may be renewed, on an annual basis, upon the submission of a report on the activities conducted during this time.The authorization will be valid as long as the researcher remains with the same institution to which he was bond to when the permit was requested.Permanent authorizations will not be valid for the following activities: collection and transportation of species officially listed as endangered; temporary maintenance of specimens of wild animals in captivity; receiving or shipping biological material abroad; and research performed in a federal conservation unit or natural underground cavity.
However, authorization is not required for the following activities, except when conducted in a conservation unit or natural underground cavity: observation and recording of images or sounds; collection and transportation of feces, regurgitation, fur, feathers, and teeth, when catching the specimen is not involved; and collection and transportation of botanical, fungal, and microbiological material, except of vegetables living in water or species listed as endangered.

Fauna in private areas
Authorization from ICMBio, through SisFauna, or from equivalent state agency, is mandatory to collect fauna in private areas.For collections in indigenous areas, an authorization from Fundação Nacional do Índio (Funai), the national Indian foundation, is required.In addition, when there is an overlap of indigenous land with a conservation area, prior authorization from Ibama, or equivalent state agency, is also necessary.

Fauna, botanical, fungal, and microbiological material from conservation or protected area
Authorization is mandatory to conduct the collection of fauna, flora, fungi, or microorganisms in a conservation unit or protected area.This permit is issued by ICMBio, through Sisbio or SisFauna, or by equivalent governmental agency.There is no possibility of obtaining a permanent authorization in this case.

Botanical, fungal, and microbiological material from private areas
Authorization from ICMBio, or equivalent state agency, to collect and transport botanical, fungal, and microbiological material from private areas is not necessary, except for aquatic plants or species listed as endangered.However, researchers should use the voluntary registration, provided by Sisbio, to issue a certificate with guidelines to the correct collection and transportation of the material, in case of inspection during these processes.The registration needs to be done only once.

Foreigners' participation in collection activities
The participation of foreign researchers in expeditions to collect samples must be authorized in advance by Ministério da Ciência, Tecnologia e Inovação (MCTI), the national ministry of science, technology, and innovation.This participation is regulated by: Law 6,815, of August 19 th , 1980; Decree No. 98,830, of January 15 th , 1990; MCTI No. 55, of March 14 th , 1990; and Resolution No. 82, of Conselho Nacional de Imigração (CNIg), the national immigration council, of December 3 rd , 2008.It should be noted that one of the prerequisites for MCTI to issue an authorization is a joint project between a Brazilian institution -responsible for implementing it -and a foreign institution -responsible for employing researchers, who will participate in the sampling expedition.
The Brazilian institution must monitor and supervise the activities developed by the foreign researchers in Brazil.To do that, the Brazilian institution should: have high and recognized technical and scientific achievements in the field of research related to the work being undertaken; delegate the degree of participation and responsibility, including financial ones; monitor and supervise the activities carried out by the foreigner institution; provide the necessary support to the foreign participants; carry out prior recognition, screening, and selection of the collected material to ensure that the required specimens or their parts are deposited in a Brazilian institution; send partial and final reports to CNPq; ship abroad part of the collected material, after authorization from MCTI or before its delegation; and suspend any activity breaching the current law and immediately report it to CNPq and MCTI.
Foreign researchers must have a formal bond with the foreign institution counterpart in the project.Besides this requirement, the foreign institution must also follow these obligations and commitments, directly or through its researchers: submit a "résumé" in any format; be responsible for implementing financial activities; have knowledge of the rules governing collection activities in the country, especially regarding the shipment of the material collected; authorize MCTI and the Brazilian institution to translate, publish, and disseminate, in Brazil, the work produced; return to Brazil any material collected; report to the Brazilian institution, on a periodic basis or upon request, on the development of the work produced abroad with the material collected, providing partial or final scientific results.
These documents must be forwarded to CNPq, which will review formal aspects and issue technical opinions, forwarding the case to MCTI for final decision regarding an authorization or not.There is no need, however, to obtain authorization from MCTI for collections conducted by foreigners under scientific exchange programs linked to agreements on cultural, scientific, technical, and technological cooperation, signed by the government of Brazil, or to international programs approved in the country.

Biological control of agricultural pests in Brazil
The international exchange of beneficial organisms in the country, from 1991 to 2013, was reported to be around 773 species of organisms introduced for biological control and other purposes, responding to requests from up to 14 Brazilian states (Table 1).Although most species were introduced only once, some of them were introduced up to three times.Furthermore, 31 species of beneficial organisms were exported up to six countries in the same period (Table 2).In Brazil, the potential use of exotic natural enemies for the biological control of localized or widespread pests is high (Sá & Pessoa, 2015).Some exotic pests registered in the country were successfully controlled by native natural enemies, whereas others demanded more efficient ones brought from their respective countries of origin.Below are some examples of cases when the introduction of exotic biocontrol agents was necessary.
Huanglongbing (HLB, ex-greening), a citrus (Citrus spp.) disease caused by the bacterium Candidatus Liberibacter spp., was detected in Brazil in 2004 (Sá & Pessoa, 2015) and is currently the most important citrus phytosanitary problem.IPM strategies are focused on the control of the disease vector, the Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae).Its parasitoid Tamarixia radiata (Waterston) (Hemiptera: Eulophidae) was scheduled to be introduced in Brazil, but it was later found in the country, making its importation unnecessary.High levels of psyllid parasitism have been reached in the state of São Paulo, but low levels in northeastern Brazil (Sá & Pessoa, 2015).For this reason, the exotic parasitoid Diaphorencyrtus aligarhensis (Shafee, Alam & Agarwal) (Hymenoptera: Encyrtidae) was imported from the United States for studies aiming the increase in psyllid parasitism rates.The interaction of D. aligarhensis on T. radiata will also be studied in quarantine conditions.
Regarding the exportation of beneficial organisms, one example is the participation of Brazil in an extensive international project on the biological control of the cassava green mite, Mononychellus tanajoa (Bondar) (Acari: Tetranychidae) (Table 2).Cassava is one of the major sources of carbohydrate for many --countries, especially in the Americas and Africa.The cassava green mite and the cassava mealybug, Phenacoccus manihoti Matile-Ferrero (Hemiptera: Pseudococcidae), were first found in Africa in the early 1970s (Neuenschwander, 2001;Yaninek & Hanna, 2003).Within a short time, the cassava green mite became a major problem to cassava growers.An international program for the biological control of the pest was very successful, resulting in the establishment of three species of predaceous phytoseiid mites that controlled the pest (Yaninek & Hanna, 2003).It should be noted that this is one of the most important projects of classical biological control of agricultural pests.

Concluding remarks
This work deals specifically with the classical biological control of pests, which involves, in its initial phase, the discovery of prospective natural enemies to be used for control of exotic organisms, followed by their actual introduction and field colonization.All these activities are regulated by Brazilian norms aiming to protect national interests related to the use of biodiversity, in this case for biological control purposes and for environmental protection against possible detrimental effects of introduced organisms.
The increasing importance of biological control in Brazil has become evident by the growing interest of the private sector.Recently, a few companies involved with the production of biological control agents were established in the country and are now objectively implementing another important class of biological control, i.e., augmentation, with mass production and releases of biological control agents.The practical use of these biological control agents by many growers gives a new impetus and credibility to this type of pest control, and also promotes the general interest in continuing the use of this technique.
However, there are aspects that still refrain from the wider use of biological control, specifically the country's legislation.Constant progress in the field of biological control has raised the need to: create specific norms to allow its further development, produce biological control items, and make its use feasible by growers.The main concern refers to the current legislation regulating the registration, approval, use, and residue levels of the adopted control measures, which is the same for biological control and agrochemicals, despite the huge differences between these two methods of pest control.Therefore, exclusive norms for the production, registration, and commercialization of biological control items are urgently needed for the wider implementation of biological control in Brazilian agriculture.

Table 1 .
Groups of organisms imported from 1991 to 2013 through the Costa Lima Quarantine Laboratory of Embrapa Meio Ambiente, located in the municipality of Jaguariúna, in the state of São Paulo, Brazil.

Table 2 .
Groups of organisms exported from 1991 to 2013 through the Costa Lima Quarantine Laboratory of Embrapa Meio Ambiente, located in the municipality of Jaguariúna, in the state of São Paulo, Brazil.