Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors March 2010 1 Recommendations regarding Derogations to use alpha- Cypermethrin, Deltamethrin, Fenitrothion, Fipronil and Sulfluramid in FSC Certified Forests in Brazil Richard Isenring, Lars Neumeister September 2009, amended in March 2010 Contents 1. Scope 2. Recommendations I. Control of Leaf-Cutting Ants 1.1 Demonstrated Need for Insecticide Use 1.2 Risk Mitigation for Insecticide Use 1.3 Alternatives for Control of Leaf-Cutting Ants 1.4 Stakeholder Opinions on Insecticide Use 1.5 Conclusions II. Coleopteran Defoliating Insects (Costalimaita ferruginea) III. Lepidopteran Defoliating Insects (Thyrinteina arnobia) IV. Termites (Preventive Treatment) Annex I Studies on Herbivory of Leaf-Cutting Ants Annex II Research and Bibliography on Leaf-Cutting Ants Annex III Toxicologic and Environmental Properties of Active Ingredients Technical Advisors to the FSC Pesticides Committee Lars Neumeister (Dipl. Ing. Land Usage & Nature Protection) Fürstenwerder, Germany. Email: [email protected], Website: www.pestizidexperte.de Richard Isenring (M.Sc. in Chemistry, MGU Certificate / Environmental Studies) Basel, Switzerland. Email: [email protected]
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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
March 2010 1
Recommendations regarding Derogations to use alpha-Cypermethrin, Deltamethrin, Fenitrothion, Fipronil and Sulfluramid in FSC Certified Forests in Brazil
Richard Isenring, Lars Neumeister
September 2009, amended in March 2010
Contents
1. Scope
2. Recommendations
I. Control of Leaf-Cutting Ants 1.1 Demonstrated Need for Insecticide Use
1.2 Risk Mitigation for Insecticide Use
1.3 Alternatives for Control of Leaf-Cutting Ants
1.4 Stakeholder Opinions on Insecticide Use
1.5 Conclusions
II. Coleopteran Defoliating Insects (Costalimaita ferruginea)
III. Lepidopteran Defoliating Insects (Thyrinteina arnobia)
IV. Termites (Preventive Treatment)
Annex I Studies on Herbivory of Leaf-Cutting Ants
Annex II Research and Bibliography on Leaf-Cutting Ants
Annex III Toxicologic and Environmental Properties of Active Ingredients
Technical Advisors to the FSC Pesticides Committee
Lars Neumeister (Dipl. Ing. Land Usage & Nature Protection)
Trichoderma species, or combinations with B.t.), viruses (granulovirus or nucleopolyhedrovirus
(NPV) specific to lepidopteran insects), mass-rearing and release or preservation of natural
enemies (predatory insects such as Podisus nigrispinus or Supputius cincticeps), and explore the
possibility of using spinosad or azadirachtin for control of Thyrinteina (e.g. in tests based on a
temporary special registration);
F. The technical advisors recommend the FSC Pesticides Committee to approve a derogation to use
fipronil (dispersible granules Tuit® Florestal) for treating the roots of seedlings preventively against
termites (Cornitermes bequaerti and Syntermes molestus) prior to planting in forest plantations in
Brazil, provided that during the derogation period the certificate holders:
1. identify which termite species is present locally, monitor damage level and presence of termites
in nurseries or young forests, and locate areas where C. bequaerti or S. molestus are prevalent;8
2. reduce the amount of fipronil used to the necessary minimum, limit seedling treatment to areas
where C. bequaerti or S. molestus is present and to areas with seedlings of susceptible tree
species, and consider reduced tillage or no-till (e.g. combined with a cover crop such as Mucuna
bracteata);
3. if termite colonies are targeted directly (e.g. termites attacking buildings), use biological agents,
in particular pathogenic fungi Metarhizium anisopliae (e.g. M. anisopliae strain ESF1 or M.
6 Pereira L.G.P. A Lagarta-Parda, Thyrinteina arnobia, principal lepidóptero desfolhador da cultura do
Eucalipto. CETEC 2007. http://sbrtv1.ibict.br/upload/dossies/sbrt-dossie219.pdf 7 Branco EF. Aspectos econômicos do controle de Thyrinteina arnobia (...) com Bacillus thuringiensis (Berliner)
em povoamentos de Eucalyptus spp. Lab. de Proteção Forestal 1995. http://floresta.ufpr.br/~lpf/outras02.html 8 Dos Santos A. Plano de amostragem e nível de dano econômico de cupins subterrâneos (Isoptera) em plantios
de eucalipto. Doutorado em andamento, UFLA. http://buscatextual.cnpq.br/buscatextual/visualizacv.jsp?id=K4704676U6
Da Silva W.L., y Schoereder J.H. Formigas saúvas preferem diferentes tipos de solos? UFV 2005. http://www.insecta.ufv.br/iussibr/Modelo%20de%20Resumo.doc
Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
March 2010 15
1.2 Risk Mitigation for Insecticide Use
1.2.1 Legislation for Occupational Safety in Brazil (General Aspects)
Certified companies confirmed that they adhere to the national legislation on occupational safety and
have established operational procedures to mitigate risks of pesticides, including the use of appropriate
personal protective equipment by forest workers. Authorities periodically inspect if companies comply
with national regulations for protection of workers. In Brazil, forest plantations are required to maintain
a distance of 30 m from rivers. National legislation for chemical safety and guidelines are listed below.
Regulations for Occupational Safety and Risk Mitigation in Brazil Ministério do Trabalho e Emprego: Norma Regulamentadora de Segurança e Saúde no Trabalho na
Agricultura, Pecuária, Silvicultura, Exploração Florestal e Aqüicultura – NR 31. 2005. http://www.mte.gov.br/legislacao/normas_regulamentadoras/nr_31.pdf
NR 31 – Manual de Aplicação. 2005. http://www.higieneocupacional.com.br/download/nr31-cna.zip
NPR 4 – Equipamento de Proteção Individual. http://www.mte.gov.br/legislacao/normas_regulamentadoras/nr_rural_04.asp
NPR 7 – Programa de Controle Médico de Saúde Ocupaticional. http://www.mte.gov.br/legislacao/normas_regulamentadoras/nr_07_at.pdf
NPR 9 – Programa de Prevenção de Riscas Ambientais. http://www.mte.gov.br/legislacao/normas_regulamentadoras/nr_09.pdf
NR 17 – Ergonomia. http://www.mte.gov.br/legislacao/normas_regulamentadoras/nr_17.asp
NRR 2 – Serviço Especializado em Prevenção de Acidentes do Trabalho Rural – SEPATR. http://www.mte.gov.br/legislacao/normas_regulamentadoras/nr_rural_02.asp
NRR 3 – Comissão Interna de Prevenção de Acidentes do Trabalho Rural – CIPATR. http://www.mte.gov.br/legislacao/normas_regulamentadoras/nr_rural_03.asp
Guidelines
Associação Nacional de Defesa Vegetal ANDEF. Manual de uso correto e seguro de produtos fitossanitários
ANDEF. Manual de uso correto de equipamento de proteção individual. http://www.andef.com.br/epi/
Caldas L.Q.A. Intoxicações exogénas por insecticidas. Centro de Controle de Intoxicações de Niterói 2000. http://www.higieneocupacional.com.br/download/intoxicacoes-exogenas-luiz_querino_a_caldas.zip
Machín D.G. Tratamiento de las intoxicaciones. 2003. http://www.higieneocupacional.com.br/download_2/tratamiento-intoxicaciones.zip
FSC Guide to integrated pest, disease and weed management in FSC certified forests and plantations. 2009. http://www.fsc.org/fileadmin/web-data/public/document_center/international_FSC_policies/brochures/IPM_Guide/IPM_Guide_2009.pdf
UNEP (2009): Fifth meeting of the Persistent Organic Pollutants Review Committee (POPRC). Annotated
outline for a guidance document on perfluorooctane sulfonate alternatives. UNEP/POPS/POPRC.5/INF/10. http://chm.pops.int/Convention/POPsReviewCommittee/hrPOPRCMeetings/POPRC5/POPRC5Documents/tabid/592/language/en-US/Default.aspx
39 Cerqueira M.M. Annex F [Sulfluramid]. Secretariat of the Stockholm Convention. Geneva 2007.
Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
March 2010 20
the metabolite PFOS accumulated in various organs, mainly in the liver (US EPA 2001).46
Increased
levels of PFOA or PFOS in blood were linked to a higher risk of thyroid disease (Melzer et al 2010).
4. Sulfluramid is in WHO class III („Slightly hazardous‟), is moderately to highly toxic to fish, and
moderately to highly toxic to bird species (see annex III). Toxicity of sulfluramid and its primary
metabolite, PFOA, is based on the same mechanism. In animals, PFOA was several times more
toxic (Schnellmann et al 1990).47
The main metabolite of sulfluramide, PFOS, is immunotoxic in
rats and similar effects are likely in humans (DeWitt et al 2009).48
A risk assessment for sulfluramid
concluded that in the medium term less toxic methods of ant control can and should substitute
sulfluramid in Brazil (Porto & Milanez 2009).49
5. Water and also blood and fat from rats were analysed in areas where sulfluramid had been applied.
Sensitivity of chemical analysis was limited: the detection limit for sulfluramide in blood and fat was
13.6 part per billion (ppb = micrograms per litre) and for PFOA it was 187 ppb (less sensitive). In
water, the detection limit for sulfluramid was 0.027 ppb, while for PFOA it was 0.37 ppb (BioAgri
1997).50
To monitor influx of sulfluramid and its metabolites to the environment and gradual accu-
mulation in wildlife, up-to-date technology for chemical analysis with a high sensitivity is needed. 6. In animal tissue, metabolites PFOA and perfluorooctanesulfonate (= perfluorooctanesulfonic acid
salt PFOS) are now commonly detected (Giesy & Kannan 2002).51
PFOA and volatile precursors of
perfluorinated chemicals are transported through the atmosphere or sea over large distances and are
later metabolized to PFOS in animals (Stock et al 2007; Martin et al 2006).52
46 US Environmental Protection Agency (EPA). Sulflramid: Human health risk assessment for sulfluramid.
Washington DC 2001. http://www.epa.gov/opp00001/foia/reviews/128992/128992-053.pdf Melzer D., et al. Association betweens perfluoroctanoic acid (PFOA) and thyroid disease in the NHANES
study. Environmental Health Perspectives Online 20 January, 2010. http://dx.doi.org/10.1289/ehp.0901584 47
Schnellmann RG, and Randall O M. Perflurooctane sulfonamide: a structurally novel uncoupler of oxidative
phosphorylation. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1016(3): 344-348, 1990. (quoted in
Key et al 1997). http://dx.doi.org/10.1016/0005-2728(90)90167-3 48
DeWitt J.C., et al. Immunotoxicity of perfluorooctanoic acid and perfluorooctane sulfonate and the role of
Agência Nacional de Vigilância Sanitária: Relatório do Ingrediente Ativo [database]: Terra diatomácea. http://www4.anvisa.gov.br/AGROSIA/asp/frm_dados_ingrediente.asp?iVarAux=1&CodIng=379 Bequisa. Insecto
Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
March 2010 25
insects (Magalhães et al 2000; Sebrae 2008).76
Limonexic acid, an extract from Raulinoa echinata, was
highly toxic to leaf-cutting ants and reduced their life-span considerably (Biavatti et al 2005).77
Antifungal agents inhibit symbiotic fungi cultivated by leaf-cutting ants. This enables indirect control
of ants. Antifungal agents include plant extracts and other fungus species (see 5.1.1). Several research
groups are studying the role of symbiotic fungi and how these influence foraging of ants (e.g. Jackson
2007).77
Extracts from leaves of Ricinus communis were tested on Atta sexdens rubropilosa. Fatty acids
were toxic to the symbiotic fungus, while ricine was directly toxic to the ants (Bigi et al 2004).78
Pheromones: beta-eudesmol, a terpenoid, is extracted from eucalypt leaves. It can disrupt the order in
ant nests. In Atta sexdens rubropilosa, beta-eudesmol modified the behavior and resulted in mutilation
and death of ants. Beta-eudesmol interferes with mutual recognition of ants. This may be an additional
strategy to control leaf-cutting ants (Marinho et al 2005).79
Grass-cutting ants (Atta capiguara) are only
weakly attracted to baits. Alarm pheromones have the potential to improve the attractiveness of baits to
(Hughes et al 2002).80
Pheromones of different ant species have been identified (Pherobase 2009).81
1.3.3 Natural Enemies of Leaf-cutting Ants
Several species of insects, birds or other animals prey on leaf-cutting ants (Delabie et al 2007).82
Birds
are very important predators of during the flight of ant queens. Predatory insects include spiders, mites,
Cazal C.M., et al. Isolation of xanthyletin, an inhibitor of ants‟ symbiotic fungus, by high-speed counter-
current chromatography, J. of Chromatography A 1216(19), 2009 http://dx.doi.org/10.1016/j.chroma.2009.02.066 76
Magalhães C.P., et al. Biochemical basis of the toxicity of manipueira (…) to nematodes and insects. Phyto-
chemical Analysis 11(1), 2000. http://www3.interscience.wiley.com/journal/70001198/abstract?CRETRY=1&SRETRY=0 Sebrae (2008): O aproveitamento sustentável da manipueira. http://www.rts.org.br/noticias/destaque-
2/arquivos/cartilha.pdf; SBPC: Mandioca, a última fronteira? http://www.jornaldaciencia.org.br/Detalhe.jsp?id=27482
Farias A.R.N., et al. Manipueira e plantas armadilhas no controle de formigas cortadeiras na cultura da
Hughes WO, et al. Field evaluation of potential of alarm pheromone compounds to enhance baits for control
of grass-cutting ants (Hymenoptera: Formicidae). Journal of Economic Entomology 95(3), 537-543, 2002. http://www.bioone.org/doi/abs/10.1603/0022-0493%282002%29095%5B0537%3AFEOPOA%5D2.0.CO%3B2
81 The Pherobase. Semiochemicals of Atta species. http://www.pherobase.com/database/genus/genus-Atta.php
Semiochemicals of Acromyrmex species. http://www.pherobase.com/database/genus/genus-Acromyrmex.php 82
Delabie J.H.C., and Jahyny B. A mirmecosfera animal: relações de dependência entre formigas e outros
animais. Revista O Biológico 69(supl.), 2007. http://www.biologico.sp.gov.br/docs/bio/suplementos/v69_supl_2/p7-12.pdf
Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
March 2010 27
Chitin synthesis inhibitors have been tested on leaf-cutting ants. Diflubenzuron caused no significant
mortality in adult workers (Nagamoto et al 2007).89
Other insect growth regulators such as methoprene,
pyriproxyfen, teflubenzuron or fenoxycarb cause mortality in laboratory tests but seem to have limited
effectiveness on leaf-cutting ants in the field, since young ants feed on symbiotic fungi (Forti 2008).90
In the past, BASF marketed ant baits containing diflubenzuron under the name „Formilin 400‟. It seems
this product is not available as it is not listed by Anvisa. Diflubenzuron qualifies as „highly hazardous‟.
Chlorpyrifos is similarly effective as sulfluramid for control of leaf-cutting ants (Atta laevigata). Baits
of chlorpyrifos (0.45%) were applied to individual ant holes (at higher doses) or distributed over the
whole nest area (at a dose of 8 g/m2). Total number of baits used was greater when these were applied
to individual ant holes. Both methods were similarly effective (Zanuncio et al 1999).91
Due to its high
acute toxicity and octanol-water partition coefficient, the FSC rates chlorpyrifos as „highly hazardous‟.
Chlorpyrifos act as a nerve poison (cholinesterase inhibitor) of different species (FCES 1997).17
Leaf-
cutting ants are still often controlled with chlorpyrifos (Lorsban® powder). Methods to control ants
were compared in Colombia, including use of lime, lime mixed with chlorpyrifos (6:1), and manual
collection of ant queens. An effective method favored by farmers was lime mixed with decreasing
amounts of chlorpyrifos (requiring 3-7 repeat applications). Pure lime (requiring 9-10 applications) was
cheaper. Chemical methods reduced the number of active ant holes by over 80%. Although most
farmers used chlorpyrifos on ants (pouring it around ant holes or pumping it into nests), ant control failed, due to ineffective application and lacking coordination (Munk Ravnborg et al 2000).
92
Cypermethrin paste (6.7% a.i.) is used specifically for control of Atta capiguaira (ANVISA 2009).
Hydramethylnon resulted in 50% mortality in Atta sexdens rubropilosa, propoxur (Blattanex®) caused
less than 40% mortality and chlorpyrifos less than 20% (Coll 2003).21
In the USA, hydramethylnon is
used in baits for controlling the Texas leaf-cutting ant (TAE (no year)).23
Piperonyl compounds had high mortality (up to 82%) in Atta sexdens (Victor et al 2001, see annex II).
Rotenone is a botanical insecticide made from root extracts of timbó (Derris species) (Fang & Casida
1999).93
The powder (e.g. Rotenat pó) is used for ant control in organic agriculture (Santiago 2004).
89
Nagamoto N.S., Forti L.C., and Raetano C.G. Evaluation of the adequacy of diflubenzuron and dechlorane in
toxic baits for leaf-cutting ants (Hymenoptera: Formicidae) based on formicidal activity. Journal of Pesticide
Forti LC. Approach on the ants‟ biology, screening and desirable features of active ingredients and insect
growth regulators for control of leaf-cutting ants. UNESP, Botucatu, São Paulo 2008. http://chm.pops.int/Portals/0/Repository/addinfo_2008/UNEP-POPS-POPRC-SUB-F08-PFOS-LEAF6.English.pdf
91 Zanuncio J.C., et al. Control of Atta laevigata (Hymenoptera: Formicidae), with Landrin-F bait, in areas
previously covered with Eucalyptus. Ciencia Rural 29(4): 1999. http://www.scielo.br/pdf/cr/v29n4/a01v29n4.pdf 92
Munk Ravnborg H., et al. Collective action in ant control. CAPRi Working Paper 7. CGIAR, Washington DC
2000. http://www.capri.cgiar.org/wp/capriwp07.asp, http://www.capri.cgiar.org/pdf/CAPRIWP07.pdf 93 Fang N., and Casida J.E. Cubé resin insecticide: Identification and biological activity of 29 rotenoid constitu-
ents. Journal of Agricultural Food and Chemistry 47(5), 1999. http://pubs.acs.org/doi/abs/10.1021/jf981188x
Santiago J.P., and Guimarães V. Formigas cortadeiras: possibilidades de controle. AAO, São Paulo 2004. http://www.aao.org.br/dicas3.asp
Wilcken C.F. Manejo integrado de pragas em provoamentos florestais. UNESP, Botucato 2008. http://www.ipef.br/eventos/2008/ebs2008/18-wilcken.pdf
FSC Guide to integrated pest, disease and weed management in FSC certified forests and plantations. 2009. http://www.fsc.org/fileadmin/web-data/public/document_center/international_FSC_policies/brochures/IPM_Guide/IPM_Guide_2009.pdf
FSC step-by-step guide – Good practice guide to meeting FSC certification requirements for biodiversity and
High Conservation Value Forests in Small and Low Intensity Managed Forests. 2009. http://www.fsc.org/fileadmin/web-data/public/document_center/publications/FSC_Technical_Series/Step-by-step_guide.pdf
96 Ocaña-Vidal J. Natural forest management with strip clear-cutting. Unasylva 169(43), 1992.
Pereira L.G.P. Estratégias de controle de formigas cortadeiras. CETEC 2007. http://sbrtv1.ibict.br/upload/dossies/sbrt-dossie96.pdf?PHPSESSID=8097c61ce57048fc7d4ca763687fc962
Reis M.A. Avaliação e aperfeiçoamento de programas de manejo de formigas cortadeiras (Hymenoptera:
Formicidae) em eucaliptais. Tese, UFLA 2009. http://biblioteca.universia.net/ficha.do?id=43251896
Reis W. Filho, et al. Reconhecimento dos danos causados por formigas cortadeiras do gênero Acromyrmex
em plantios iniciais de Pinus taeda no sul do Brasil. Comunicado Técnico 189, 2007. http://www.cnpf.embrapa.br/publica/comuntec/edicoes/com_tec189.pdf
Reis W. Filho. Cultivo do Pinus: Pragas: Formigas cortadeiras. Embrapa 2005. http://sistemasdeproducao.cnptia.embrapa.br/FontesHTML/Pinus/CultivodoPinus/07_1_pragas_de_pinus_formigas.htm
Zanetti R., et al. Manejo integrado de formigas cortadeiras. Manejo Integrado de Pragas Florestais, 2007. http://www.den.ufla.br/Professores/Ronald/Disciplinas/Notas%20Aula/MIPFlorestas%20formigas.pdf
Zanetti R. Manejo integrado de formigas cortadeiras e cupins em areas de eucalipto da Cenibra. 2007. http://www.cenibra.com.br/pdf/LaudoFSC-Cenibra.pdf
Zanetti R. Monitoramento de formigas cortadeiras (Hymenoptera: Formicidae) em florestas cultivadas.
Revista O Biológico 69(supl. 2), 2007. http://www.biologico.sp.gov.br/docs/bio/suplementos/v69_supl_2/p129-131.pdf
1.3.6 Alternatives for Control of Leaf-Cutting Ants – Position of Technical Advisors
Pathogenic fungi, in particular Metarhizium anisopliae, Trichoderma viride and Beauveria bassiana,
effectively controlled leaf-cutting ants in studies. More field tests on pathogenic fungi are encouraged.
Research on control of fire ants (Solenopsis sp.) by combining a microbial pathogen and diatomaceous
earth is promising. Effectiveness of pathogenic fungi against ants was increased in combination with
B.t., extract from plants, or diatomaceous earth. Some of these agents may require a temporary special
registration if they are not currently authorised in Brazil for ant control. Requirements for registration
of new non-toxic products based on combinations of pathogenic fungi, plant extracts, or diatomaceous
earth need to be clarified. Plant extracts (of sesame, Ateleia glazioviana / Citromax®, etc) are promising
and merit field tests. The certified holders are recommended to collaborate with research institutions in
tests on pathogenic fungi in combination with B. thuringiensis, plant extracts, or diatomaceous earth.
Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
March 2010 32
research institutions (Brazilian Agricultural Research Corporation - Embrapa), associations of forest
plantations (Associação Brasileira de Produtores de Florestas Plantadas - Abraflor, Minas Gerais Silvi-
culture Association / Associação Mineira de Silvicultura AMS, Sociedade Brasileira de Silvicultura
SBS). The individual certificate holders consulted representatives of workers and subcontracted staff
(National Union of Workers CUT), regional government authorities, non-governmental organizations
(for social welfare or environmental protection), neighbours and representatives of local communities. Regional non-governmental organizations consulted include Fundação ABC / Agricultural Research &
Development, Adecav, Biodiversitas Foundation, Centro de Ação Voluntária / Center for Voluntary
Action, Centro Cultural do Vale do Jequitinhonha, Comissão Pastoral da Terra CPT / Pastoral Land
Commission, Conservação Internacional, Instituto de Conservação Ambiental / Nature Conservancy,
Instituto de Desenvolvimento Sustentável e Energias Renováveis IDER / Institute of Sustainable
Development and Energy, Instituto Socioambiental ISA, Macon Lodge, Mandalla Agency, O Boticario,
Raízes da Terra, and Serviço Nacional de Aprendizagem Rural / National Office for Rural Education.
A large proportion of the contacted stakeholders responded, and the majority of these were supportive.
Non-supportive answers will be replied to after a final decision of FSC-IC on derogation applications.
For sulfluramid, out of 3839 stakeholders who were consulted, 3447 responded. Of these, 3395 were
supportive and 52 (1.5%) did not support use of sulfluramid in forest management. According to the
applicant, non-supportive answers can be classified as follows: 71% without justification; 17% based
on technical or environmental aspects; 7% with unfounded justification; 5% based on toxicity aspects.
Table 4. Stakeholder Opinions on Use of ‘Highly Hazardous’ Insecticides
Stakeholders who responded to consultation
Number contacted / Number of responses
Opinion on derogation for ‘highly hazardous’ insecticide Supportive / Non-supportive
Classification of non-supportive opinions: A: without justification, B: with unfounded justification
C: based on technical/environmental aspects, D: based on toxicity
The National Council for Food Safety in Brazil demanded that sulfluramid and PFOS should be prohi-
bited under the Stockholm Convention (CONSEA 2009).102
This reflects concerns about the hazardous
102
CONSEA. Letter from Mr R.F. Maluf, president of CONSEA, to the President of Brazil, April 29, 2009. http://www.planalto.gov.br/consea/static/agenda/Plenarias2009/090429/EM_003_impactos%20da%20sulfluramida.pdf
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March 2010 33
properties of sulfluramid, in particular regarding food safety, as sulfluramid is used on a large scale to
control leaf-cutting ants in plantations of sugar and soja. The National Commission on Agriculture was
divided on this issue: the Ministry of Agriculture opposes an inclusion of PFOS in the list of prohibited
or restricted persistent organic pollutants, while the Ministry of Environment believes that sulfluramid
can gradually be substituted with alternatives. Organizations in ecological agriculture, represented by
ANA, oppose use of sulfluramid for ant control due to environmental/health risks (Cavalcante 2009).103
1.4.2 Stakeholder Consultation – Position of Technical Advisors
Certificate holders in Brazil conducted a very extensive stakeholder consultation from mid September
till November 2007. This was partly due to the large number of 43 certificate holders applying for a
derogation. In Brazil, plantations are very large compared to other countries. Many more stakeholders
are involved, directly or indirectly. Unfortunately, the comments of stakeholders were very voluminous
and some were difficult to read. Technical advisors had the opportunity to view copies of the original
comments but relied primarily on summary information provided by the applicants due to the enormous
volume of comments and limited time. Nearly 1000 government-funded agencies, non-governmental
organizations, associations, etc, are engaged in protecting human health or the environment in Brazil.104
(Amata, a company under certification, applied for a derogation in 2010 and consulted no stakeholders
(also not on a regional scale) as a derogation for sulfluramid was previously approved in Brazil.)
The proportion of stakeholders who did not support a derogation ranged between 1.5% for sulfluramid
(in south Brazil and in other regions) and 4.3% for fipronil baits (in south Brazil). This difference may
be due to more people knowing about hazardous properties of fipronil, or may result from the different
proportion of stakeholders in specific interest groups (such as the forest industry, government agencies,
environmental organizations, etc). While the great majority of stakeholders supported sulfluramid, 52
stakeholders objected to a derogation for sulfluramid. From these 52 non-supportive responses, 21% or
11 stakeholders gave a justification (5% based on toxicity, 17% on technical or environmental aspects).
The highest proportion of non-supportive opinions (40%) – but lowest total number (13) – occurred
with alpha-cypermethrin. Total number of non-supportive opinions for sulfluramid (52) was four times
higher than for alpha-cypermethrin. The reason for this could be that the relatively high acute toxicity
of alpha-cypermethrin is well-known, and that yellow beetles (Costalimeita ferruginea) are less widely
distributed than leaf-cutting ants. Stakeholders may be concerned about risks from alpha-cypermethrin
to workers and non-target species. Leaf-cutting ants are known to damage crops in many or most parts
of Brazil. But less people may know about the very high persistence of sulfluramid and its metabolites.
Additionally, a large proportion of stakeholders is connected directly or indirectly to the forest industry
and their position may not be totally independent. Concerns of the National Council for Food Safety
about the use of sulfluramid in field crops do not relate to use in forest plantations. But the concerns of
organizations promoting sustainable production, including sustainable forest management, are relevant.
103
Cavalcante I. Debate sobre controle de praga divide Comissão de Agricultura. Jusbrasil April 14, 2009. http://www.jusbrasil.com.br/politica/2342285/debate-sobre-controle-de-praga-divide-comissao-de-agricultura
104 Wiser Earth. Search database of organizations for country „Brazil‟. 2009. http://www.wiserearth.org/organization/search/q/country%3ABrazil
Wilcken C.F. Manejo integrado de pragas em provoamentos florestais. UNESP, Botucato 2008. http://www.ipef.br/eventos/2008/ebs2008/18-wilcken.pdf
FSC Guide to integrated pest, disease and weed management in FSC certified forests and plantations. 2009. http://www.fsc.org/fileadmin/web-data/public/document_center/international_FSC_policies/brochures/IPM_Guide/IPM_Guide_2009.pdf
Machado A.L. Estudos biologicos e comportamentais de Migdolus fryanus (Westwood, 1863) (Coleoptera:
vesperidae) e sua interação com nematoides entomopatogenicos, e outros agentes de mortalidade. Tese de
Doutorado, Unicamp 2006. http://libdigi.unicamp.br/document/?code=vtls000378083 121 Goettel M.S., et al. Entomopathogenic fungi and their role in regulation of insect populations. In: Gilbert L.I.,
et al. Comprehensive molecular insect science: Control. Vol. 6, pp. 361-405. Elsevier Publ., Amsterdam 2005 122 Souza R.M. Feromônios do besour-amarelo, Costalimaita ferruginea. Projeto de Doutorado.
Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
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2.6 Conclusions – Costalimaita ferruginea and other Coleopteran Defoliators
1. In the majority of plantations affected by yellow beetles Costalimaita ferruginea, infestation level
and damage was not sufficitly high to warrant chemical control. An exception is a large seedling
nursery. It appears that Costalimaita is controlled annually on the whole nursery area. But „routine‟
use of a non-selective insecticide (such as alpha-cypermethrin or deltamethrin) is not compatible
with integrated pest management. Besides being non-selective, regular use of pyrethroids increases
the risk of pest insects becoming resistant. Continued annual use in nurseries, where Costamilaita
can cause significant damage, is likely to result in lower effectiveness of control with time. Other
coleopteran defoliating insects caused less problems and were not controlled by certificate holders.
2. Alternatives for management of Costalimaita ferruginea include monitoring, less hazardous (more
selective) insecticides such as spinosad or neem combined with biological control, and preventive
practices. A preventive silvicultural practice which has proven very effective is to plant seedlings
between the old stumps of harvested eucalypt trees. Sprouts on tree stumps are very effective „traps‟
(distracting beetles from seedlings) and chemical control has not been necessary where this method
was practiced. Native plants or robust species of Eucalyptus can also be interplanted between crop
trees. Another preventive practice is to limit weed control to the rows of seedlings and to partially
retain weeds between seedling rows. This attracts natural enemies and reduces attack on seedlings.
Further alternatives include using a combination of B. thuringiensis and Beauveria bassiana. In the
longer term, tree species should be selected which are less susceptible to attack from defoliators.
3. In forest plantations with older trees, it appears feasible to control Costalimaita ferruginea and other
coleopteran defoliators (leaf-eating beetles Chrysomelidae, in particular) by regular monitoring of
beetles (also outside managed areas), combining preventive silvicultural with biological methods of
control, and, in case of infestations, using a less hazardous insecticide such as spinosad or neem. In
nurseries (viveiros), according to (proposed) revised FSC Principles and Criteria,126
a derogation for
using a „highly hazardous‟ pesticide shall not be required, providing that certain conditions are met.
2.7. Additional Publications on Costalimaita ferruginea and other Defoliators
Anjos N. Taxonomia, ciclo de vida e dinamica populacional de costalimaita ferruginea (…), praga de eucalyptus
(…). Tese de Doutorado, 1992. http://dedalus.usp.br:4500/ALEPH/POR/USP/USP/TES/FULL/0735580?
Baranek E.J. Estudo da suscetibilidade de Sitophilus zeamais (Mots., 1855) (Coleoptera: Curculionidae) ao óleo
de nim (Azadirachta indica A. Juss). UEPG 2008. http://www.uepg.br/colegiados/colagro/monografias/EdemarJoseBaranek.pdf
Garlet J., et al. Danos provocados por coró-das-pastagens em plantas de eucalipto. Ciência Rural 39(2), 2009. http://www.scielo.br/pdf/cr/v39n2/a79cr515.pdf
Mordue A.J., et al. Azadirachtin, a natural product in insect control. In: Gilbert L.I., et al (eds). Comprehensive
Pearce M.J. Termites: Biology and pest management. CAB International, Wallingford, UK 1997
Pereira L.G.B. Insetos broqueadores de species florestais. CETEC 2007. http://sbrtv1.ibict.br/upload/dossies/sbrt-dossie249.pdf?PHPSESSID=69256fdd8637bf04a9688a7d4228b596
Pinto R., et al. Flutuação populacional de Coleoptea em plantio de Eucalyptus urophylla no município de Três
Marias, Estado de Minas Gerais. Floresta e Ambiente 7(1), 2000. http://www.if.ufrrj.br/revista/pdf/Vol7%20143A151.pdf
Trisyono A, and Whalom M.E. Toxicity of neem applied alone and in combinations with Bacillus thuringiensis
to Colorado potato beetle (Coleoptera: Chrysomelidae). Journal of Economic Entomology 92(6): 1281-1288,
Zanetti R. Manejo de besouros desfolhadores. Manejo Integrado de Pragas Florestais, UFLA 2006. http://www.den.ufla.br/Professores/Ronald/Disciplinas/Notas%20Aula/MIPFlorestas%20besouros.pdf
Zanetti R. Manejo de insetos broqueadores de florestas. Manejo Integrado de Pragas Florestais, UFLA 2006. http://www.den.ufla.br/Professores/Ronald/Disciplinas/Notas%20Aula/MIPFlorestas%20broqueadores.pdf
Zanuncio J.C., et al. Sphallenum tuberosum (Coleopteria: Cerambycidae) em plantas de Eucalyptus spp. no
Município de Prado, Bahia. Revista Árvore, 29(2): 339-343, 2005. http://dx.doi.org/10.1590/S0100-67622005000200017
III. Thyrinteina arnobia and other Lepidopteran Defoliating Insects
3.1 Need for Deltamethrin to Control Thyrinteina arnobi and other Lepidopteran Defoliating Insects
Among various species, the eucalyptus brown looper Thyrinteina arnobia is the main lepidopteran
defoliator of eucalypts. In the past, it has infested very large areas of several 10'000 or 100'000 ha.
Defoliation delays tree development, reducing wood volume and quality. Successive defolation can
cause mortality. Levels of up to 50% defoliation reduced annual increment by 18%, and defoliation
above 50% caused reductions in increment between 53% (during the rainy season) and almost 80% in
periods of drought (Freitas 1988).126
Losses amounted to 8.3 m3/ha for 50 % defoliation or 25.6 m
3/ha
for 100 % defoliation (Oda & Berti Filho 1978).127
Damage from lepidopteran defoliators in E. saligna
126
Freitas S. de. Efeito do desfolhamento na produção de Eucalyptus grandis Hiil ex Maiden (Myrtaceae)
visando avaliar os danos causados por insetos desfolhadores. Tese de Doutorado, ESALQ/USP 1988 127
Oda S., y Berti Filho E. Incrementos anual volumétrico de Eucalyptus saligna sm. em áreas com diferentes
níveis de infestações de lagartas de Thyrinteina arnobia (…). IPEF 17: 27-31, 1978.
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3.2 Need for Deltamethrin to Control Thyrinteina arnobia and other Lepidopteran Defoliating Insects – Position of Technical Advisors
It appears that outbreaks of Thyrinteina arnobia occur only sporadically and cause relatively limited
damage. Opinions diverge whether Bacillus thuringiensis is suitable for controlling caterpillars of
Thyrinteina and other lepidopteran defoliators. B.t. has the advantage of being much more selective
than pyrethroids (such as alpha-cypermethrin or deltmethrin). The risk of B.t. to natural enemies and
prasitoids (insects that prey upon lepidopteran caterpillars and pupae) is limited. It seems uncertain if
Thyrinteina needs to be controlled with an insecticide if 1-2 application/s of Bacillus thuringiensis are
appropriately timed.
Other lepidopteran defoliators occurred on part of the area of several certificate holders. But damage
caused by these species was not large enough to warrant control except for Melanolophia species. In
2008, the certificate holder controlled this insect on 120 ha with B. thuringiensis. Several alternatives
are available for control of lepidopteran insects, including biopesticides (based on B. thuringiensis or
specific nucleopolydroviruses NPVs), IT-based decision support systems for evaluation of monitoring
data, use of natual enemies, pathogenic fungi, and use of less hazardous insecticides such as spinosad.
2.3 Risk Mitigation for Deltamethrin: See 1.2.1 (p. 14 above)
2.4 Stakeholder Opinions on Use of Deltamethrin: See 1.4 (pp. 29-31 above)
2.5 Alternatives for Control of Thyrinteina arnobia and other Lepidopteran Defoliators
Bacillus thuringiensis: products commercialized for the control of Lepidoptera are based on Bacillus
thuringiensis subspec. kurstaki and Bacillus thuringiensis subsp. aizawai (Van Driesche et al 2009).129
In laboratory tests B. thuringiensis controlled the lepidopteran defoliator Adeloneivaia subangulata
effectively in the third instar at a dose of 250 g/ha (Bressan & Santos 1985).130
Decision-support systems help to select appropriate method/s of control and optimum timing. The
distribution and density (approximate numbers per ha) of Thyrinteina or other defoliating insects need
to be monitored regularly. Use of a decision support system can facilitate the evaluation of monitoring
129
Van Driesche R., et al. Control of pests and weeds by natural enemies. Blackwell Publ., Oxford, UK 2008 130
Bressan D.A., y Santos H.R. Controle de lagartas de Adeloneivaia subangulata (…) com Bacillus
thuringiensis Berliner (1911) em condições de laboratório. Revista Florestas, 1985. http://ojs.c3sl.ufpr.br/ojs2/index.php/floresta/article/viewFile/6365/4565
(see also: http://ojs.c3sl.ufpr.br/ojs2/index.php/floresta/article/view/6360/4560)
Fritz L.L. Bactérias entomopatogênicas aplicadas no controle de insetos-praga. Unisinos 2006. http://www.unisinos.br/mostra2006/trabalhos_publicados/docs/eixo2/02-047.pdf
Gonzaga A.D., et al. Toxicidade de manipueira de mandioca (Manihot esculenta Crantz) e erva-de-rato
(Palicourea marcgravii St. Hill) a adultos de Toxoptera citricida Kirkaldy (Homoptera: Aphididae). Acta
Holtz A.M. Aspectos biológicos de Thyrinteina arnobia (Lep.: Geometriadae) provenientes de lagartas criadas
em folhas de Eucalyptus cloeziana ou de Psidium guajava sob condições de campo. Revista Árvore 27(6), 2003. http://www.scielo.br/pdf/rarv/v27n6/a16v27n6.pdf
Mordue A.J., et al. Actions of azadirachtin, a plant allelochemical, against insects. Pesticide Science 54(3), 1999. http://www3.interscience.wiley.com/journal/1724/abstract
Oliveira L.S., et al. Ocorrência de Glycaspis brimblecombei (…) (Hemiptera: Psyllidae) em Eucalyptus spp. no
Rio Grande do Sul, Brasil. Ciência Florestal 16(3), 2006. http://www.ufsm.br/cienciaflorestal/artigos/v16n3/A10V16N3.pdf
Oliveira H.G., et al. Atratividade de Atta sexdens rubropilosa por plantas de eucalipto atacadas previamente ou
não por Thyrinteina arnobia. Pesuisa agropecúria brasileira 39(3): 285-287, 2004. http://www.scielo.br/pdf/pab/v39n3/a12v39n3.pdf
Oliveira H.N., et al. Parasitism rate and viability of Trichogramma maxacalii (Hym.: Trichogrammatidae)
parasitoid of the Eucalptus defoliator Euselasia apison (Lep.: Riodinidae), on eggs of Anagasta kuehniella
(Lep.: Pyralidae). Forest Ecology and Management 130(1-3), 2000. http://dx.doi.org/10.1016/S0378-1127(99)00172-3
Pedrosa-Macedo JH. Manual de pragas em florestas: Pragas florestais do sul do Brasil. Volume 2, Laboratorio
de Proteção Forestal. http://floresta.ufpr.br/~lpf/livros03.html
Pereira F.F., et al. Potencial de Palmistichus elaeisis (Hymenoptera: Eulophidae) para o controle de Thyrinteina
ferruginea (Lepidoptera: Geometridae); Trichospilus diatraeae (…) um novo parasitóide de Thyrinteina arnobia.
X Simpósio de Controle Biológico 2007. http://www.cenargen.embrapa.br/publica/trabalhos/doc250.pdf (pp. 242-243)
Pereira J.M.M. Distribuição espacial e temporal de lepidópteros pragas de eucalipto em Montes Claros, Minas
Gerais. Tese de Doutorado, UFV 2005. http://www.controbiol.ufv.br/Teses/Tese_Jose_Milton.pdf
Prado D.T., et al. Eficiência de inseticidas biológicos no controle de Thyrinteina arnobia Stoll (Lepidoptera …)
Soares L.G.S., et al. Dinâmica populacional de Euselasia apisaon (…): avaliação da mortalidade e determinação
de parâmetros para a construção de tabela de vida. 2005. http://www.seb-ecologia.org.br/viiceb/resumos/802a.pdf
Wilcken C.F. Biologia de Thyrinteina arnobia (Stoll, 1782) (Lepidoptera: Geometridae) em especies de
eucalyptus e em dieta artificial. Tese de Doutorado, USP 1996. http://www.ipef.br/servicos/teses/arquivos/wilcken,cf.pdf (Wilcken 1991): http://dedalus.usp.br:4500/ALEPH/POR/USP/USP/TES/FULL/0734396?
Wilcken C.F. Occorrência do psilídeo-de-concha (Glycaspis brimblecombei) (Hemiptera: Psillidae) em florestas
de eucalipto no Brasil. Circular Técnica IPEF 201, 2003. http://www.ipef.br/publicacoes/ctecnica/nr201.pdf
Zanuncio J.C., et al. Monitoramento de Lepidoptera desfolhadores de Eucalypto no Brasil. Plagas Forestales
Zanetti R. Manejo de lagartas desfolhadoras. Manejo Integrado de Pragas Florestais, UFLA 2006. http://www.den.ufla.br/Professores/Ronald/Disciplinas/Notas%20Aula/MIPFlorestas%20lagartas.pdf
Zanetti R., et al. Coconut tree grashopper, Eutropidacris cristata (orthoptera: acrididae) feeding on eucalyptus
trees in Minas Gerais, Brazil. Revista Árvore 27(1), 2003. http://dx.doi.org/10.1590/S0100-67622003000100014
Zenner I., et al. Influence of parasitism by Chelonus insularis (…) on the susceptibility of Spodoptera frugiperda
(…) to insecticides. Neotropical Entomology 35(6), 2006. http://dx.doi.org/10.1590/S1519-566X2006000600015
IV. Termites – Preventive Treatment of Seedlings
4.1 Need for Fipronil to Treat Seedlings against Termites (Cornitermes bequaerti / Syntermes molestus)
In Brazil, termites cause 18% to 80% mortality of eucalyptus seedlings up to one year after planting.
The main period during which seedlings are susceptible to termite attack varies between eucalyptus
species. Attacks from termites of the species Syntermes occur in seedlings up to an age of 10 months.
Direct damage includes destroyed roots, resulting in death of seedlings. Termites can also affect the
development of trees indirectly by making these more susceptible to attacks from other pest insects.
Assuming that average mortality of seedlings attacked by termites is 20%, losses during establishment
amount to 48 m3/ha or 333 trees per ha. This corresponds to a loss of $288.00/ha at the end of a rotation
cycle of 6 years (Wilcken et al 2002).139
Without preventing termites from causing damage, plantations
of eucalyptus would not be viable.
139
Wilcken C.F., et al. Termite pests in Eucalyptus forests of Brazil. Sociobiology 40(1): 179-190, 2002. http://www.csuchico.edu/biol/Sociobiology/volume/sociobiologyv40n12002.html#14
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Immersion of seedling roots in an insecticide solution was developed as a new, preventive method of
termite control. This employs plastic tubes used in thecultivation of Eucalyptus seedlings. The main
advantages of root immersion are: high operational performance, decrease and control of the insecticide
amount applied per area, lower risk of exposure among rural workers, lower cost of control operations,
and no risk of exposure to wildlife (as the insectide is concentrated in substrate clay of the seedlings).
Fipronil is the active ingredient used in Brazil in insecticide formulations for treating seedlings against
termites of the species Cornitermes bequaerti and Syntermes molestus. These are among the insects
cause major damage in agricultural production or forestry. Immersing eucalyptus seedlings in fipronil
solution drastically reduces the losses incurred, since the product has a high efficiency control (99.7%)
in a single application pre-planting. This protects the forest stand and, as a consequence, inhibits attack
of other pest species under conditions of stress (during periods of drought, for instance). Immersing
seedlings in a solution of 0.4% fipronil provided preventive control from 90% to 100% of termites
(Wilcken & Raetano 1995; Galon 2008).140
100 liters of solution are sufficient to treat 7'000 to 12'000
seedlings by submersing these for 30 seconds in the solution (0.5% content of fipronil).
Tuit Florestal, which is based on fipronil, is the only termiticide registered in Brazil for use in forestry
(reforestation). Dispersible granules (containing 80% fipronil active ingredient) are diluted prior to use.
Hoja de Seguridad: Tuit Florestal (Basf). http://www.agro.basf.com.br/UI/_pdf/FISPQ/TUIT_FLORESTAL.pdf / Safety Data Sheet (http://www.ndscom.com.br/agrobasf/UI/Produtos.aspx?CodProduto=78&CodTipoProduto=2)
4.2 Need for Fipronil to Treat Seedlings against Termites – Position of Technical Advisors
Clearly, there is a neeed for preventing damage of seedlings caused by certain termite species. As the
product is not applied on the nest itself and as fipronil is used only once during the whole rotation (and
limited to newly established areas), the risk non-target animals appears to be low. This is corroborated
by the low water solubility of fipronil and its low potential for leaching. Although fipronil may have a
certain potential for bioaccumulation, based on its octanol-water partition coefficient (logKOW) of 4, the
indirect method of application is likely to preclude any significant exposure of non-target organisms.
At the low concentration used, toxic effects on non-target organisms (such as rodents eating seedling
roots) seem rather unlikely.
It appears that subterranean termites prefer softwoods (Eucalyptus robusta, Pinus speicies) to species
with wood of intermediate hardness suchas E. pellita and E. urophylla (Peralta et al 2004).141
It may be
possible to reduce damage by growing tree species that are less susceptible to attack from termites.
140
Galon J.A. (Bayer). Fórum nacional sobre carvão vegetal. 2008. http://painelflorestal.com.br/upload/bayer.pdf Wilcken C.F., Raetano C.G. Eficiência do inseticida fipronil no controle de cupins subterrâneos (Isoptera) em
eucalipto. Abstracts of XV Congresso Brasileiro de Entomologia, p. 547. Caxambu, Brazil 1995 141
Peralta R.C.G., et al. Wood consumption rates of forest species by subterranean termites (Isoptera) under
field conditions. Revista Árvore 28(2): 283-289, 2004. http://www.scielo.br/pdf/rarv/v28n2/20993.pdf
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4.3 Risk Mitigation for Use of Fipronil: See 1.2.1 (p. 14 above)
4.4 Stakeholder Opinions on Use of Fipronil: See 1.4 (pp. 29-31 above)
4.5 Alternatives for Direct Control of Termite Colonies (Cornitermes / Syntermes species)
Current practices of preventively treating eucalypt seedlings with fipronil have the great advantage of
reducing the amount of insecticide entering the environment to a very low level. This reduces the risk
to non-target organisms (such as natural enemies of termites) significantly, compared to direct chemical
control of termite nests. Preventive treatment of seedlings prior to planting should be the predominant
or only method of termite control. Stored wood is also often treated with preservatives such as borates.
In situations where termite colonies might be targeted directly (to control or eliminate a whole colony,
e.g. if termites are attacking buildings), biological agents should be used preferentially. Besides direct
application of an insecticide (e.g. in baits), several methods have a potential to control termite colonies.
Promising alternatives include pathogenic fungi. Alternative methods for direct termite control might
be used in exceptional situations where a certain termite colony is targeted. As preventive treatment of
seedlings protects these very effectively, direct control of termite colonies is usually not necessary.
Abamectin qualifies as „highly hazardous‟ under FSC criteria. Abamectin and fipronil were equally
effective for termite control. One application of abamectin (as a liquid concentrate) or of fipronil
(granules) both resulted in 100% mortality of Cornitermes cumulans (Valerio et al 1998).142
However,
fipronil achieved only 50% mortality in Syntermes species.
Borax preserves wood against attack by termites, especially when combined with smaller amounts of
copper hydroxide (Lebow et al 2005).143
In Brazil, borax is registered as a wood preservative (Anvisa
2009). Borate salts are applied to wood in various ways (UA 2006).144
Borax also acts as an insecticide.
When applied in baits, borax effectively controls termites and cockroaches (Quarles 2003).145
Botanical extracts from several plants were toxic to termites (Coptotermes gestroi) in laboratory tests,
e.g. extract of Ocimum basilicum / manjerição caused 12% mortality (Reis et al 2008).146
Combinations
142
Valerio JR et al. Controle químico e mecânico de cupins de montículo (Isoptera: Termitidae) em pastagens.
Anais da Sociedade Entomológica do Brasil 27(1), 125-131, 1998. http://dx.doi.org/10.1590/S0301-
80591998000100016 143
Lebow et al. Resistance of borax-copper treated wood in aboveground exposure to attack by subterranean
Formosan termites. US Forest Service 2005. http://www.fpl.fs.fed.us/documnts/fplrn/fpl_rn295.pdf 144
University of Arkansas (UA). Termite and other structural pest control. Little Rock, Arkansas, 2006. http://www.aragriculture.org/pesticides/training/manuals/AG1155/default.htm
145 Quarles W. IPM for termites – Termite baits. The IPM Practitioner 25(1-2), 2003. http://www.birc.org/JanFeb2003.pdf
146 Reis F.C., et al. Avaliação de produtos naturais no controle de Coptotermes gestroi (Isoptera: Rhinotermiti-
tidae) . Revista O Biológico 70(supl. 1), 2008. http://www.biologico.sp.gov.br/docs/bio/suplementos/v70_supl/37.pdf
Grace J.K., and Yates J.R. Termite resistant construction and building materials. Proceedings of the 3rd
Internat. Conference of Urban Pests 1999. http://www.icup.org.uk/reports%5CICUP450.pdf
Beyond Pesticides. Least toxic control of termites. Washington DC 2002. http://www.beyondpesticides.org/alternatives/factsheets/Termite%20Control.pdf
152 Fadini M.A.M, et al. Efeito da profundidade de aplicação e da distribuição de inseticidas líquidos no controle
de cupins de montículo em pastagens (Isoptera: Termitidae). Neotropical Entomology 30(1), 157-159, 2001. http://dx.doi.org/10.1590/S1519-566X2001000100023
Bezerra-Gusmão M.A., et al. Polycalic nest systems and levels of aggression of Constrictotermes cyphergaster
(Isoptera, Termitidae, Nasutitermitinae) in the semi-arid region of Brazil. Socioiology 53(1), 2009. http://www.csuchico.edu/biol/Sociobiology/volume/sociobiologyv53n12009.html#10
Campos M.B.S., et al. Seleção de iscas celulósicas para o cupim Heterotermes tenuis (isoptera: rhinotermitidae)
em cultura de cana-de-açúcar. Scientia Agricola 55(3), 1998. http://dx.doi.org/10.1590/S0103-90161998000300017
Castiglioni E.A.R. Efeito de derivados de meliáceas e isolados de fungos entomopatogênicos sobre o cupim
subterrâneo Heterotermes teunis (…). Tese de Doutorado, ESALQ 1992. http://www.teses.usp.br/teses/disponiveis/11/11146/tde-25072002-140640/
Costa-Leonardo A.M. et al. Estimates of foraging population and territory of Heterotermes tenuis colonies using
Garden Organic (HDRA). Termite control without chemicals. 2002. http://www.gardenorganic.org.uk/pdfs/international_programme/Termite.pdf
Grewal P. Insect parasitic nematodes. Publications: Termitidae. Ohio State University 2008. http://oardc.osu.edu/nematodes/keyword.asp?keyword=TERMITIDAE
Grewal P., et al. Entomopathogenic nematodes: potential for exploration and use in South America. Neotropical
Soares C.G., et al. Efeito de oleos e extratos aquosos de Azadirachta indica e Cymbopogon winterianus Jowitt
sobre Nasutitermes corniger Motschuls (Isoptera: Termtitidae). Revista ciênc. agr. 50: 107-116, 2008. http://www.ufra.edu.br/editora/revista_50/REVISTA%2050_artigo%2008.pdf
Su N.Y., and Scheffrahn R.H. A review of subterranean termite control practices and prospects for integrated
pest management programmes. Integrated Pest Management Reviews 3(1): 1-13, 1998. http://www.springerlink.com/content/g0u140414r853164/
UNEP. Finding alternatives to persistent organic pollutants (POPs) for termite management. Genevra 2003. http://portalserver.unepchemicals.ch/Publications/Alternatives-termite-fulldocument.pdf
Zanetti R. Manejo integrado de cupins. Notas de aula de entomologia 115, UFLA 2006. http://www.den.ufla.br/Professores/Ronald/Disciplinas/Notas%20Aula/MIPFlorestas%20cupins.pdf
Zhu B. C-R., et al.Repellency of vetiver oils from different biogenetic and geographical origins against formosan
168 Wirth R., Beyschlag W., Ryel R.J., and Holldobler B. Annual foraging of the leaf-cutting ant Atta colombica
in a semideciduous rain forest in Panama. Journal of Tropical Ecology 13(5): 741-757, 1997. http://links.jstor.org/sici?sici=0266-4674(199709)13%3A5%3C741%3AAFOTLA%3E2.0.CO%3B2-U
169 Ghazoul J. Plant-animal interactions in forest ecosystems. In: Burley et al. Encyclopedia of forest science.
Volume 1, pp. 57-62. Elsevier Publ., Oxford 2004 170
Herz H., Beyschlag W., and Hölldobler B. Herbivory rate of leaf-cutting ants in a tropical moist forest in
Panama at the population and ecosystem scales. Biotropica 39(4): 482-488, 2007. http://www.blackwell-
Florin W., et al. The effects of temperature, light, and nutrient conditions on the foraging of leaf-cutter ants
(Atta cephalotes) in forested and disturbed areas. In: Villalobos E., et al (eds). Summer Program on Tropical
Ecology, pp. 73-82, 2002. http://www.ots.duke.edu/en/education/pdfs/usap/coursebooks/te02.pdf 175
Mendes F.E.S., et al. Efeito da pressão de ataque de Atta sexdens na estrutura da vegetação em áreas de
sucessão secundária no médio Rio Doce. VI Congresso de Ecologia do Brasil, Fortaleza, 2003. pp. 234-236. http://seb-ecologia.org.br/anais/11.pdf
176 Cornelius J.P., et al. Swietenia (American Mahogany). In: Burley et al. Encyclopedia of forest science.
Volume 3, pp. 1720-1728. Elsevier Publ., Oxford 2004 177
Caffarini P., et al. Impacto del estrés hídrico y la procedencia de Eucalyptus globulus Labill. Sobre el
comportamiento de herbivoría de Acromyrmex lundi Guérin. Idesia 24(1), 2006. http://dx.doi.org/10.4067/S0718-34292006000100002
178 Meyer S.T., et al. Selecting the drought stressed: effects of plant stress on intraspecific and within-plant
herbivory patterns of the leaf-cutting ant Atta colombica. Functional Ecology 20(6), 2006. http://www3.interscience.wiley.com/journal/118572728/abstract?CRETRY=1&SRETRY=0
179 Meyer S.T. Ecosystem engineering in fragmented forests: Edge-mediated hyper-abundance of leaf-cutting
ants and resulting impacts on forest structure, microclimate and regeneration. 2008. http://kluedo.ub.uni-
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Brazilian plantations of eucalypt grow rapidly and are productive, which lessens the pressure on
indigenous forests. However, some eucalypt species are vulnerable to leaf-cutting ants. Certain species
(Atta spp.) together with other insects have become pests. Invertebrates (arthropods, worms, etc) are
greatly reduced in number and diversity in eucalypt plantations. Various species feed on leaf-cutting
ants. Ecological damages need to be prevented in plantations, and it is important to conserve forest
invertebrates and vertebrates (Majer & Recher 1999; Nair 2001).185
Although leaf-cutting ants or
termites cause non-specific (general) damage in plantations, these pests do not threaten monocultures
when they are controlled appropriately (Evans 1997).186
In Venezuela, the influence of predation on densities of mature ant colonies (Atta species) was studied.
Densities were significantly higher on islands (that had been isolated recently) than on the mainland.
When protected with wire mesh from predators such as the armadillo, ant colonies had a greater chance
of survival. Reduced predation appears to be an important factor for the higher densities observed on
these islands (Rao 2000).187
The impact of leaf-cutting ants (Atta laevigata) on the establishment of forests on abandoned land in
Amazonia was studied. Damage from herbivory affected survival and growth of tree seedlings
negatively. But after excluding leaf-cutting ants from plots for 20 months densities of tree seedlings
had not significantly increased. Smaller seedlings and species preferred by the ants suffered greater
mortality. Consumption rates remained approximately constant. As the number and size of seedlings
increased with time, the probability of an individual seedling being attacked declined. The impact of
ant herbivory on tree establishment appears to be greatest during the first few years of regeneration
(Vasconcelos et al 1997).188
Leaf-cutting ants appear to be important for the cycling and redistribution of critical macronutrients in
forests (Sternberg et al 2007).189
In the Cerrado, Brazil, the influence of leaf-cutting ants and fire on
soil nutrients was compared. Leaves of herbaceous and woody (shrub) species growing close to ant
nests had increased nutrient levels, while burning showed no positive effects (or resulted in a decrease).
Especially in nutrient-depleted soils, refuse from ant nests may be an important nutrient source (Sousa-
Souto et al 2007).190
185
Majer J.D., and Recher H.F. Are eucalypts Brazil's friend or foe? An entomological viewpoint. Anais da
Sociedade Entomológica do Brasil 28(2): 185-200, 1999. http://www.scielo.br/pdf/aseb/v28n2/v28n2a01.pdf
Nair K.S. Pest outbreaks in tropical forest plantations: Is there a greater risk for exotic tree species? CIFOR,
Jakarta, Indonesia 2001. http://www.cifor.cgiar.org/publications/pdf_files/Books/Nair.pdf 186
Evans J. Bioenergy plantations – Experience and prospects: Worldwide experience with high yield forest
plantations. Biomass and Bioenergy 13(4-5): 187-191, 1997. http://dx.doi.org/10.1016/S0961-9534(97)10007-1 187
Rao M. Variation in leaf-cutter ant (Atta spp.) densities in forest isolates: the potential role of predation.
Journal of Tropical Ecology 16: 209-225, 2000. http://www.journals.cambridge.org/action/displayAbstract?fromPage=online&aid=35257
188 Vasconcelos H.L., and Cherrett J.M. Leaf-cutting ants and early forest regeneration in Central Amazonia:
effects of herbivory on tree seedling establishment. Journal of Tropical Ecology 13(3): 357-370, 1997. http://links.jstor.org/sici?sici=0266-4674(199705)13%3A3%3C357%3ALAAEFR%3E2.0.CO%3B2-K#abstract
189 Sternberg et al. Plants use macronutrients accumulated in leaf-cutting ant nests. Proceedings of the Royal
Society B 274: 315–321, 2007. http://penguin.bio.miami.edu/leo/PDF%20articles/atta.pdf 190
Sousa-Souto L., et al. Leaf-cutting ants, seasonal burning and nutrient distribution in Cerrado vegetation.
US Department of Agriculture (USDA) Forest Service. Report 2004, Part 3: Conditions by region. http://www.fs.fed.us/foresthealth/publications/annual_i_d_conditions/ConditionsReport_04_Conditions_by_Region.pdf
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Annex II Research and Bibliography on Leaf-Cutting Ants
Scientific Experts and Research Groups on Leaf-Cutting Ants, IPM, Natural Products
Della Lucia, Terzinha Maria C. UFV – Pesquisa Basica e Aplicada com Formigas Cortadeiras. http://dgp.cnpq.br/buscaoperacional/detalhegrupo.jsp?grupo=0336204JGCL2JP
Bueno, Odair Correa. UNESP – Comportamento e Controle de Formigas Cortadeiras. http://dgp.cnpq.br/buscaoperacional/detalhegrupo.jsp?grupo=03305016DNZ8FP Centro de Estudos de Insetos Sociais. http://www.rc.unesp.br/ib/ceis/formigascortadeiras.php
Bragança, Marcos Antonio Lima. UFT – Ecologia e Controle Biológico de Formigas Cortadeiras. http://dgp.cnpq.br/buscaoperacional/detalhelinha.jsp?grupo=4609204T4ELV7G&seqlinha=1
Castellani, Maria Aparecida. UESB – Manejo Integrado de Pragas. http://dgp.cnpq.br/buscaoperacional/detalhegrupo.jsp?grupo=7490501JLRFUMF
Ide, Sérgio. Instituto Biológico – Grupo de Bionomia e Manejo de Insetos de Importância Sócio-Econômica. http://www.biologico.sp.gov.br/grupospesquisa/bionomia.php
Instituto Nacional de Pesquisas da Amazônia (INPA). Coleções Biológicas: 3. Coleções Microbiológicas de
Samuels, Richard Ian. UENFP – Manejo Integrado de Pragas, Vetores e Doenças de Plantas. http://dgp.cnpq.br/buscaoperacional/detalhegrupo.jsp?grupo=8325501ZRBL5T0
Zanetti, Ronald Bonnetti. UFLA – Manejo Integrado de Pragas; Produtos Naturais. http://dgp.cnpq.br/buscaoperacional/detalhepesq.jsp?pesq=4820678026031281
Zanuncio, Jose Cola. UFV – Manejo Integrado de Pragas Floretais; Embrapa – Unidade de Controle Biológico. http://dgp.cnpq.br/buscaoperacional/detalhepesq.jsp?pesq=7079506792953399
Wilcken, Carlos Frederico. IPEF (www.ipef.br); UNESP – Proteção Florestal. http://dgp.cnpq.br/buscaoperacional/detalhegrupo.jsp?grupo=0330502KDEJO9N
Barbosa V.S., et al. Influência da herbivoria de formigas cortadeiras no successo reprodutivo de espécies
vegetais de Floresta Atlântica. 2007. http://www.seb-ecologia.org.br/viiiceb/pdf/1679.pdf
Barbosa V.S. Efeito da fragmentação florestal na taxa de parasitismo de fungos associados ao jardim da formiga
cortadeira, Atta laevigata. Tese de Doutorado, UFPE 2004. http://www.bdtd.ufpe.br/tedeSimplificado//tde_busca/arquivo.php?codArquivo=377
Bellotti A.C., et al. Biological control in the Neotropics: A selective review with emphasis on cassava. Second
Internat. Symposium on Biological Control of Arthropods 2005. http://www.bugwood.org/arthropod2005/vol1/5a.pdf
Berti Filho E. Controle biológico e entomologia florestal. IPEF Boletim Informativo 5(14): 5-16, 1977. http://www.ipef.br/publicacoes/boletim_informativo/bolinf14.pdf
Bianchi-Santos M., et al. Efeito do ácido oléico sobre o metabolismo de operárias da formiga cortadeira Atta
sexdens rubropilosa. XXV Congr. Brasil. de Zool, resumo 536, 2006. http://www.unb.br/ib/zoo/CBZ/resumos/Insecta.pdf
Bieber A.G.D., et al. Recrutamento de plântulas sobre ninhos inativos da formiga cortadeira Atta cephalotes na
Floresta Atlântica Nordestina. Revista O Biológico 69(supl. 2): 329-333. 2007. http://www.biologico.sp.gov.br/docs/bio/suplementos/v69_supl_2/p329-333.pdf
Bizi R.M. Microrganismos Endofíticos. Laboratório de Proteção Florestal. http://floresta.ufpr.br/~lpf/contbio02.html
Boaretto et al. Response of the grass-cutting ant Atta capiguara Gonçalves, 1944 (Hymenoptera:
Formicidae) to sugars and artificial sweeteners. Scientia Agricola 60(3): 505-509 2003. http://www.fca.unesp.br/lisp/artigos/Boaretto%20et%20al%202003%20-%20sugars.pdf
Boaretto M.A., and Forti L.C. Perspectivas no controle de formigas cortadeiras. UNESP, Botucatu, São Paolo
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Biológico 69(supl. 2): p. 520, 2007. http://www.biologico.sp.gov.br/docs/bio/suplementos/v69_supl_2/p520.pdf
Carvalho Campos A.E. de. Isolamento de entomopatógenos em colônias de formigas invasoras e sua aplicação
para o controle. Instituto Biológico, Unidade Laboratorial de Referência em Pragas Urbanas, São Paolo, Brasil. http://www.biologico.sp.gov.br/bol_formigas.php (Contact: Dra A.E. de Carvalho Campos, [email protected])
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Club Amigos da Terra de Uberlândia. Controle de formigas-cortadeiras. http://www.catuberlandia.com.br/cooplantio/06.htm
Coordenadoria de Assistência Técnica Integral (CATI). Formigas cortadeiras. Campinas, São Paulo. http://www.cati.sp.gov.br/novacati/tecnologias/pragas_agricolas/manual_formigas/formigas_cortadeiras.htm
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INTA, AER Puerto Rico 2005. http://www.inta.gov.ar/montecarlo/INFO/documentos/forestales/moni_hormigas.pdf
Corrêa M.M., et al. Impact of Atta cephalotes (Hymenoptera: Formicidae) colonies on light availability
and vegetation composition in the Brazilian Atlantic Forest. Revista O Biológico 69(supl. 2): p. 498, 2007. http://www.biologico.sp.gov.br/docs/bio/suplementos/v69_supl_2/p498.pdf
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Corrêa M.M. Formigas cortadeiras (…) como agentes modificadores de disponibilidade de luz e da estrutura da
comunidade vegetal em Floresta Atlântica Nordestina. UFPE 2006. http://www.bdtd.ufpe.br/tedeSimplificado//tde_busca/arquivo.php?codArquivo=152
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por medio de distintos cebos granulados. INTA, E.E.A. Montecarlo, R.A. 2003. http://www.inta.gov.ar/montecarlo/info/documentos/forestales/controlatta.pdf
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Nova 30(3), 2007. http://quimicanova.sbq.org.br/qn/qnol/2007/vol30n3/26-RV06127.pdf 206
US Environmental Protection Agency (EPA). Reregistration Eligibility Decision for Fenitrothion.
Washington DC. 2006. http://www.epa.gov/pesticides/reregistration/REDs/fenitrothion_red.pdf US EPA. Reregistration Eligibility Decision (RED) Fenitrothion. Washington DC 1995. http://www.epa.gov/pesticides/reregistration/REDs/0445.pdf
US EPA. Fenitrothion Facts. Washington DC 2000. http://www.epa.gov/oppsrrd1/REDs/factsheets/0445tredfact.pdf
Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
March 2010 96
Environmental Fate of Sulfluramid and its Metabolites
Sulfluramid, a perfluorinated sulfonamide, is nonvolatile. It can be transformed to volatile fluorinated
compounds by microorganisms and subsequently move from the soil environment to the atmosphere. In
mammals it is de-ethylated to perflurooctane-sulfonamide, which is not known to undergo further
degradation, but is probably converted to perflurooctanesulfonic acid that is highly persistent toward
degradation as it is chemically inactive (recalcitrant). The toxic action of its primary metabolite,
perflurooctanesulfonamide, is based on the same mechanism and was found to be three times higher
than that of sulfluramid. Fluorinated compounds can be significant contaminants in the environment
due to their persistence. In particular, the combination of chemical inactivity and biological activity is a
cause for concern (Key et al 1997).
In animals, perflurooctanesulfonic acid or perflurooctanesulfonate (PFOS, acid salt) has a high
potential to bioaccumulate. PFOS is accumulating in animals at a higher level in the food chain at a
substantial degree (UNEP 2006). Elimination rate is lower for mammals than for birds, however,
bioaccumulation can occur in birds that are chronically exposed to PFOS.
Additional Publications on Sulfluramid, Metabolites, and Perfluorinated Compounds
Allsopp M., et al. Perfluorinated chemicals: an emerging concern. Greenpeace Research Laboratories, University
of Exeter, UK 2005. http://greenpeace.to/publications/perfluorinated_chemicals_2005.pdf
Arrendale R.F., et al. Determination of GX 071 and its major metabolite in rat blood by cold on-column injection
capillary GC/ECD. Journal of Agricultural and Food Chemistry 37 (4): 1130–1135, 1989. http://pubs.acs.org/doi/abs/10.1021/jf00088a069
Bossi R., et al. Preliminary screening of perfluorooctane sulfonate (PFOS) and other fluorochemicals in fish,
birds and marine mammals from Greenland and the Faroe Islands. Environmental Pollution 136(2), 2005. http://dx.doi.org/10.1016/j.envpol.2004.12.020
Case M.T., et al. Rat and rabbit oral developmental toxicology studies with two perfluorinated compounds. Intl.
Journal of Toxicology 20(2): 101-109, 2001. http://www.informaworld.com/smpp/content~db=all~content=a713936461
Coats J.R. Risks from natural versus synthetic insecticides. Annual Review of Entomology 39: 489-515, 1994. http://arjournals.annualreviews.org/doi/abs/10.1146%2Fannurev.en.39.010194.002421
Duong L. Assessment of fluorinated chemicals (FCs) on developmental toxicity in embryonic zebrafish. M.Sc.
thesis, Oregon State University 2008. http://hdl.handle.net/1957/8215
Environment Canada. Ecological screening assessment report on Perfluorooctane Sulfonate, its salts and its
precursors that contain the C8F17SO2, C8F17SO3 or C8F17SO2N moiety. Quebec, Canada 2006. http://www.ec.gc.ca/ceparegistry/documents/subs_list/PFOS_SAR/PFOS_TOC.cfm
European Commission. Proposal for a COUNCIL DECISION establishing the position to be adopted on behalf
of the European Community with regard to proposals for amending Annexes A, B and C of the Stockholm
Convention at the fourth meeting of the Conference of Parties on 4 – 8 May 2009. 1.5 Perfluorooctanesulfonic
Holmström K.E., et al. Temporal trends of PFOS and PFOA in guillemot gggs from the Baltic Sea, 1968-2003.
Environmental Science and Technology 39(1), 2005. http://pubs.acs.org/doi/abs/10.1021/es049257d
Jahnke A. Polyfluorinated alkyl substances (PFAS) in the marine atmosphere – investigations on their
occurrence and distribution in coastal regions. PhD thesis, University of Lüneburg 2007. http://dvsun3.gkss.de/BERICHTE/GKSS_Berichte_2007/GKSS_2007_8.pdf
Jahnke A., et al. Latitudinal gradient of airborne polyfluorinated alkyl substances in the marine atmosphere
between Germany and South Africa (53° N−33° S). Environmental Science & Technology 41 (9): 3055–3061,
Johansson N., et al. Neonatal exposure to PFOS and PFOA in mice results in changes in proteins which are
important for neuronal growth and synaptogenesis in the developing brain. Toxicological Sciences 108: 412-418,
2009. http://toxsci.oxfordjournals.org/cgi/content/abstract/108/2/412 Kannan K, et al. Perfluorinated compounds in aquatic organisms at various trophic levels in a Great Lakes food
chain. Archives of Environmental Contamination and Toxicology 48(4), 2004. http://www.springerlink.com/content/g234t72w574325kq/
Kannan K., et al. Concentrations of perfluorinated acids in livers of birds from Japan and Korea. Chemosphere
UNEP – Comité de Examen de los Contaminantes Orgánicos Persistentes. Evaluación de la gestión de riesgos
del sulfonato de Perfluorooctano. Ginebra 2007. http://chm.pops.int/Portals/0/docs/from_old_website/documents/meetings/poprc/POPRC3/POPRC3_Report_s/POPRC3_Report_add5_s.pdf (sp)