Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
Recommendations regarding Derogations to use alphaCypermethrin, 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
1.2
1.3
1.4
Demonstrated Need for Insecticide Use
Risk Mitigation for Insecticide Use
Alternatives for Control of Leaf-Cutting Ants
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]
March 2010
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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
1. Scope
FSC certificate holders have applied for a derogation to use „highly hazardous‟ insecticides in forest
plantations in Brazil, including deltamethrin, fenitrothion, fipronil and sulfluramid for control of leafcutting ants (Atta and Acromyrmex species); deltamethrin and alpha-cypermethrin for controlling the
yellow beetle (Costalimaita ferruginea) and other defoliating insects; deltamethrin for control of the
eucalyptus brown looper (Thyrinteina arnobia); and fipronil for control of termites (Cornitermes and
Syntermes species). The following approved certifiers submitted the derogation applications: SCS
Scientific Certification Systems, SGS System & Service Certification, and SmartWood – Imaflora.
Table 1 lists the applicants and requested active ingredients.
Table 1. Derogation Applications for ‘highly hazardous’ Insecticides in FSC Certified Forests, Brazil
FSC Certificate Holder
Certificate Number
Active Ingredient (formulation)
Fipronil* (dispersible granules)
Sulfluramid (granular baits)
Deltamethrin (dust)
Adami S/A. Madeiras, South Brazil
SW-FM/COC – 002665 Fipronil (granular baits)
Sulfluramid (granular baits)
Agro-Florestal Motrisa Ltda., South Brazil SW-FM/COC-1808
Sulfluramid (granular baits)
Fenitrothion (liquid)
Amapá Florestal e Celulose Ltda – Amcel SCS-FM/COC-000114P
Sulfluramid (granular baits)
Amata S/A. – Unidade Castanhal, Pará
Candidate FMO (SW) Sulfluramid (granular baits)
Deltamethrin (liquid)
Candidate FMO
Aracruz Celulose S/A
Fipronil (dispersible granules)
(undefined CB)
Sulfluramid (granular baits)
Arauco Florestal Arapoti S.A
Candidate FMO (SW) Sulfluramid (granular baits)
Arauco Forest Brasil S/A., South Brazil
SW-FM/COC-1059
Sulfluramid (granular baits)
Deltamethrin (liquid)
ARAUPEL S/A (com COC serraria)
SW-FM/COC-180
Fipronil (dispersible granules)
Sulfluramid (granular baits)
alpha-Cypermethrin (liquid)
Deltamethrin (dust)
ArcelorMittal Energética Jequitinhonha
SGS-FM/COC-004161 Deltamethrin (liquid)
Ltda (formerly Acesita Energética Ltda.)
Fipronil (dispersible granules)
Sulfluramid (granular baits)
alpha-Cypermethrin (liquid)
Deltamethrin (dust)
ArcelorMittal Florestas Ltda.
Deltamethrin (liquid)
SGS-FM/COC-1943
(formerly CAF Santa Bárbara Ltda.)
Fenitrothion (liquid)
Fipronil (dispersible granules)
Sulfluramid (granular baits)
Battistella Florestal, Unidade Lages, S. BR Candidate FMO (SW) Sulfluramid (granular baits)
A.W. Faber-Castell S.A.
*
SCS-FM/COC-00081P
Application withdrawn in 2009
March 2010
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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
Battistella Florestal, Unidade Rio Negrinho,
SW-FM/COC-1070
South Brazil (formerly Mobasa, South BR)
Caceres Florestal S.A.
SCS-FM/COC-091P
CAXUANA Reflorestamento S/A (com
COC serraria)
SW-FM/COC-215
Celulose Irani S/A., South Brazil
Candidate FMO (SW)
Cenibra – Celulose Nipo-Brasileira S.A.
SGS-FM/COC-2167
Conpacel – Consórcio Paulista de Papel e
Celulose (formerly Ripasa S.A. Celulose e SCS-FM/COC-00076P
Papel)
Duratex S.A.
SCS-FM/COC-00029P
Eucatex S.A. Ind. E Com.
SCS-FM/COC-00040P
Florestal Vale do Corisco, Ltda.
SCS-FM/COC-00038P
Floresteca Agro Florestal Ltda.
SGS-FM/COC-0079
Flosul Indústria e Comercio de Madeiras
SW-FM/COC-087
Ltda., South Brazil
Grim – Grupo de Reflorestadores do Imbaú,
SW-FM/COC-1820
South Brazil
Fipronil (granular baits)
Sulfluramid (granular baits)
Sulfluramid (granular baits)
Deltamethrin (dust)
Fenitrothion (liquid)
Fipronil (dispersible granules)
Sulfluramid (granular baits)
Deltamethrin (dust)
Fipronil (dispersible granules)
Sulfluramid (granular baits)
Deltamethrin (liquid)
Fipronil (dispersible granules)
Sulfluramid (granular baits)
alpha-Cypermethrin (liquid)
Deltamethrin (liquid)
Fenitrothion (liquid)
Fipronil (dispersible granules)
Sulfluramid (granular baits)
alpha-Cypermethrin (liquid)
Deltamethrin (dust)
Deltamethrin (liquid)
Fenitrothion (liquid)
Fipronil (dispersible granules)
Sulfluramid (granular baits)
alpha-Cypermethrin (liquid)
Deltamethrin (liquid)
Fipronil (dispersible granules)
Sulfluramid (granular baits)
Deltamethrin (dust)
Sulfluramid (granular baits)
Deltamethrin (dust)
Deltamethrin (liquid)
Sulfluramid (granular baits)
Sulfluramid (granular baits)
Sulflurarnid (granular baits)
Deltamethrin (liquid)
SCS-FM/COC-00077P Fenitrothion
Sulfluramid (granular baits)
Deltamethrin (dust)
Candidate FMO
Deltamethrin (liquid)
José Ailton Thomaz, Bahia (south)
(undefined CB)
Fipronil (dispersible granules)
Sulfluramid (granular baits)
Juliana Florestal Ltda., South Brazil
SW-FM/COC-130
Sulfluramid (granular baits)
Deltamethrin (dust)
Candidate FMO
Jurandir de Souza Boa Morte, Bahia (south)
Deltamethrin (liquid)
(undefined CB)
Fipronil (dispersible granules)
Jari Celulose S.A.
March 2010
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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
KLABIN S/A - ANGATUBA
Candidate FMO (SW)
KLABIN S/A - PARANÁ (com PFNM)
SW-FM/COC-NTFP
038
KLABIN S/A - SANTA CATARINA (com
SW-FM/COC-1301
COC serraria)
Lwarcel Celulose e Papel Ltda.
SCS-FM/COC-0093P
Madecal Agro-Industrial Ltda, South Brazil SW-FM/COC-000205
Madepar Indústria e Comércio de Madeiras
SCS-FM/COC-00048P
Ltda., South Brazil
MASISA do Brasil Ltda.
SW-FM/COC-1531
Norske Skog Florestal Ltda.
Candidate FMO (SCS)
Ouro Verde Agrosilvopastoril Ltda.
Candidate FMO (CB?)
Plantar S.A.
SCS-FM/COC-00057P
Reflorestadora Sincol Ltda., South Brazil
SW-FM/COC-001135
Renova Floresta Ltda., South Brazil
SW-FM/COC-1777
SATIPEL Florestal
SW-FM/COC-1409
Seiva S/A, South Brazil
SW-FM/COC-003580
March 2010
Sulfluramid (granular baits)
Deltamethrin (dust)
Deltamethrin (liquid)
Fenitrothion (liquid)
Fipronil (dispersible granules)
Sulfluramid (granular baits)
Deltamethrin (dust)
Deltamethrin (liquid)
Fenitrothion
Fipronil (dispersible granules)
Sulfluramid (granular baits)
Deltamethrin (dust)
Deltamethrin (liquid)
Fenitrothion (liquid)
Fipronil (dispersible granules)
Sulfluramid (granular baits)
alpha-Cypermethrin (liquid)
Deltamethrin (dust)
Deltamethrin (liquid)
Fenitrothion (liquid)
Fipronil (dispersible granules)
Sulfluramid (granular baits)
Fipronil (granular baits)
Sulfluramid (granular baits)
Fipronil (granular baits)
Sulfluramid (granular baits)
Deltamethrin (dust)
Deltamethrin (liquid)
Sulfluramid (granular baits)
Deltamethrin (dust)
Sulfluramid (granular baits)
Sulfluramid (granular baits)
Deltamethrin (dust)
Deltamethrin (liquid)
Fenitrothion (liquid)
Fipronil (dispersible granules)
Sulfluramid (granular baits)
Deltamethrin (dust)
Fipronil (granular baits)
Sulfluramid (granular baits)
Fipronil (granular baits)
Sulfluramid (granular baits)
Deltamethrin (dust)
Deltamethrin (liquid)
Fipronil (dispersible granules)
Sulfluramid (granular baits)
Fipronil (granular baits)
Sulfluramid (granular baits)
4
Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
Seta S/A - Sociedade Extrativa de Tanino
de Acácia, South Brazil
SW-FM/COC-1274
Sulfluramid (granular baits)
Deltamethrin (dust)
Fenitrothion (liquid)
Sulfluramid (granular baits)
Fipronil (granular baits)
Souza Cruz- S/A, South Brazil
SCS-FM/COC-00116P
Sulfluramid (granular baits)
alpha-Cypermethrin (liquid)
Deltamethrin (dust)
SUZANO Papel e Celulose S/A - Unidade
SW-FM/COC-1377
Deltamethrin (liquid)
Mucuri
Fipronil (dispersible granules)
Sulfluramid (granular baits)
alpha-Cypermethrin (liquid)
Deltamethrin (dust)
SUZANO Papel e Celulose S/A - Unidade
SW-FM/COC-2093
Deltamethrin (liquid)
Suzano
Fipronil (dispersible granules)
Sulfluramid (granular baits)
Deltamethrin (liquid)
Tanagro S.A.
SGS-FM/COC-1664
Sulfluramid (granular baits)
Timbó Empreendimentos Florestais Ltda. SCS-FM/00065P
Sulfluramid (granular baits)
Deltamethrin (dust)
Deltamethrin (liquid)
Vanda Almeida Mattos, Bahia (south)
Candidate FMO (SW)
Fipronil (dispersible granules)
Sulfluramid (granular baits)
alpha-Cypermethrin (liquid)
Deltamethrin (liquid)
Votorantim Celulose e Papel, Ltda. (VCP) SCS-FM/COC-00085P
Fipronil (dispersible granules)
Sulfluramid (granular baits)
Sguario Florestal S.A.
Certifier
SGS-FM/COC-2745
Contact
Forest management reports
SGS do Brasil Ltda – Qualifor Program
Ms P. Azambuja
http://www.forestry.sgs.com/fore
São Paulo, Brazil
[email protected] st-management-reports.htm
Website: www.br.sgs.com/pt_br/fsc__qualifor
Scientific Certification Systems – SCS
Ms V. Shimoyama
www.scscertified.com/nrc/forest_
vanilda.shimoyama@brturbo.
Emeryville, CA, USA
certclients.php#southamerica
com.br
Website: www.scscertified.com
Rainforest Alliance SmartWood Program
Mr R. Camargo Cardoso www.rainforest– Imaflora. Programa de Certificação
alliance.org/forestry/public_docu
[email protected]
Florestal. São Paulo, Brazil
ments_country.cfm?country=3
Website: ww2.imaflora.org
FSC has rated the requested five active ingredients as „highly hazardous‟ under its current indicators
(criteria). Table 2 lists below indicators which exceed the current threshold (FSC 2007).1
1
Forest Stewardship Council. FSC Pesticide Policy: Guidance on Implementation (FSC-GUI-30-001 V2-0),
Annex IIa: FSC list of „highly hazardous‟ pesticides. Bonn 2007. http://www.fsc.org/internationalpolicies.html
March 2010
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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
Table 2. Insecticides rated as ‘highly hazardous’ under FSC indicators (thresholds)
Active ingredient
Indicator
Acute toxicity
(LD50)
Aquatic toxicity Octanol-water parti(LC50)
tion coefficient (Kow)
Cypermethrin
x
alpha-Cypermethrin
x
x
x
Deltamethrin
x
x
x
Fenitrothion
Fipronil
Sulfluramid
Persistence
(half life)
x
x
x
x
x
x
*
*
Sulfluramid and its metabolites are highly persistent but data on their degradation (half-life) in soil is lacking.
2. Recommendations
A. The technical advisors recommend the FSC Pesticides Committee to approve a derogation to use the
following insecticides for control of leaf-cutting ants (Atta and Acromyrmex species) in nurseries
and forest plantations in Brazil: deltamethrin (dust formulation K-Othrine), fenitrothion, fipronil,
and sulfluramid, provided that during the derogation period the certificate holders:
1. identify which species of leaf-cutting ant causes most damage, estimate level of damage, define
a critical nest density (maximum acceptable density for achieving silvicultural objectives),
monitor distribution of ant nests, and locate infested areas with a critical density of nests;2
2. reduce the amount of deltamethrin, fenitrothion, fipronil, and sulfluramid used to the minimum
needed for effective control, limit use to highly infested areas (where estimated nest density
exceeds critical density) or nurseries or young plantations during establishment (in the first 1-3
years), and complement these with alternatives, e.g. spinosad, borax, rotenone, pathogenic fungi
combined with diatomatomaceous earth and extracts of Manihot esculenta, Ateleia glazioviana /
Citromax®, etc;
2
Zanetti R. (UFLA). Programa de manejo de formigas cortadeiras e de cupins em Eucaliptais. Ministério da
Ciência e Tecnologia. http://sigcti.mct.gov.br/fundos/rel/ctl/ctl.php?act=nav.prj_vis&idp=9219
Zanetti R., Zanuncio J.C. Monitoramento de formigas cortadeiras em florestas cultivadas no Brasil. Plagas
Forestales Neotropicales 17, 2005. http://web.catie.ac.cr/informacion/RMIP/rev75/BoletinPlagasForestales.pdf
Zanetti (2006): http://www.den.ufla.br/Professores/Ronald/Disciplinas/Notas%20Aula/MIPFlorestas%20formigas.pdf
Pinto R. Amostragem e distribuição espacial de colônias de formigas cortadeiras (...) em Eucaliptais. UFV
2006. http://www.controbiol.ufv.br/Teses/Rosenilson_doutorado.pdf
Cantarelli E.B. Silvicultura de precisão no monitoramento e controle de formigas cortadeiras em plantios de
Pinus. UFSM 2005. http://cascavel.cpd.ufsm.br/tede/tde_busca/arquivo.php?codArquivo=756
March 2010
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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
3. reduce risks to non-target animals (mammals, birds, reptiles and amphibians) to an acceptable
level by identifying season and time of day when ants are most active and applying baits to nests
during that season and time to ensure maximum collection of baits by ants (and minimum
remnant baits), limit the application of insecticide baits to the ant nest (entrances or trails on
surface of nest);
4. set a reduction target for sulfluramid use (for example, −20% reduction in amount of sulfluramid
active ingredient (kg) per year), and apply sulfluramid baits in dispensers (porta-iscas) or sachets
(mipis) unless a specific need for open application of baits is shown in audit reports (e.g. based
on costs-benefit analysis) and evidence is provided that measures for risk mitigation are effective
(e.g. by analyzing the environment and non-target animals for residues of sulfluramid and
metabolites);3
5. conduct or participate in field tests on ant control with pathogenic fungi (Beauveria bassiana,
Metarhizium anisopliae, Paecilomyces species or Trichoderma viride) combined with Bacillus
thuringiensis, diatomaceous earth, plant extracts,4 or an antifungal agent (which inhibits
symbiotic fungi) such as Trichoderma harzianum or Escovopsis weberi; explore the possibility of
using spinosad or borax for ant control (e.g. based on a temporary special registration); and
collaborate with research institutions in tests on improving bait attractiveness with plant extracts
(of Hovenia dulcis or Aleurites fordii), attractant pheromones or the alarm pheromone betaeudesmol;5
6. during the derogation period, keep records on number of ant nests treated annually, estimated
(approximate) number of ant nests per hectare in treated areas, total annual use of deltamethrin,
fenitrothion, fipronil and sulfluramid (kg of bait applied per ha and percent content of
insecticide), age of trees in treated areas, result of control operations (estimated nest density and
percentage of damaged trees – before and after control) and include this information in forest
management reports;
7. take the greatest care that handling and application of deltamethrin, fenitrothion, fipronil and
sulfluramid does not endanger human health and natural enemies (mammals, birds, or predatory
insects such as spiders), implement measures to reduce risk to acceptable levels, and strictly
follow all legal requirements in Brazil for the use of pesticides, in particular the controls for
occupational and environmental safety required by the national and regional authorities and
specific guidelines.
3
4
5
Ukan D. Avaliação qualitativa e quantitativa de micro-porta-iscas para o controle de formigas cortadeiras (…).
UFPR 2008. http://www.floresta.ufpr.br/pos-graduacao/defesas/pdf_ms/2008/d497_0701-M.pdf
E.g. extract of Ateleia glazioviana, Canavalia ensiformis, Centrosema brasilianum, Citrus sinensis, Helietta
puberula, Hymenaea courbaril, Ipomea batata, Manihot esculenta, Myroxylon peruiferum, Pilocarpus grandiflorus, Piper cenocladum, Raulinoa echinata, Ricinus communis, Sesamum indicum, or Trichillia glauca.
Formigas cortadeiras, UFPEL. http://dgp.cnpq.br/buscaoperacional/detalhegrupo.jsp?grupo=0045501JCB22SZ
Produtos Naturais, UFSCAR. http://dgp.cnpq.br/buscaoperacional/detalhegrupo.jsp?grupo=0335106CJGECN1
Laboratório de formigas cortadeiras, UNESP. http://www.rc.unesp.br/ib/ceis/formigascortadeiras.php
Formigas cortadeiras, UNESP. http://dgp.cnpq.br/buscaoperacional/detalhegrupo.jsp?grupo=03305016DNZ8FP
March 2010
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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
B. The technical advisors recommend the FSC Pesticides Committee to reject the application for a
derogation for alpha-cypermethrin to control yellow beetles (Costalimaita ferruginea) or other
lepidopteran or coleopteran defoliating insects forest plantations in Brazil, as the evidence provided
of a need for alpha-cypermethrin did not demonstrate that this is the only feasible way of controlling
the targeted pest insects and that these species are causing severe damage (e.g. based on field tests
with alternative non-chemical or less toxic methods of pest management, cost-benefit analysis,
social and environmental impact assessment, as required by FSC (2007) Procedure: Processing
pesticide derogation applications), and also as more selective alternatives are available.
C. The technical advisors recommend the certificate holders who applied for a derogation for alphacypermethrin to:
1. monitor distribution of Costalimaita ferruginea or other coleopteran defoliators, locate infested
areas with a high density of Costalimaita or other defoliators, identify the type of defoliating
insect (genus and, if possible, species), estimate damage level, and define a critical density of
Costalimaita or of other defoliators (maximum acceptable density for achieving silvicultural
objectives);
3. retain old tree stumps and plant seedlings between stumps to provide „trap stumps‟ (with sprouts
distracting Costalimaita from seedlings), assess the potential of inter-planting trap plants to
distract beetles (preferred plants or robust eucalyptus species), promote natural enemies (e.g.
parasitic wasps Trichogramma, Anaphes nitens) by preserving fragments of native vegetation
in/around Eucalyptus plantations or reducing weed control to the minimum (retaining weeds
partially between tree rows), limit control of Costalimaita and of other coleopteran defoliators to
the most highly infested areas (where estimated density of Costalimaita or defoliators exceeds
critical density) and areas with susceptible tree species, and if necessary use a low-toxicity
insecticide (spinosad or azadirachtin);
3. conduct field tests on control of coleopteran defoliators with Bacillus thuringiensis (B.t. subsp.
tenebrionis or B.t. subsp. kurstaki), pathogenic fungi (Metarhizium anisopliae, Trichoderma
species, Beauveria bassiana combined with B.t., etc), viruses (granuloviruses or nucleopolyhedroviruses (NPVs) specific to coleopteran insects), use of natural enemies (predatory or
parasitic insects) and explore the possibility of using spinosad or azadirachtin (neem extract) for
control of Costalimaita or other coleopteran defoliators (e.g. in tests based on temporary special
registration RET);
D. The technical advisors recommend the FSC Pesticides Committee to reject the application for a
derogation for deltamethrin (liquid formulation Decis 25 CE) to control Eucalyptus brown looper
(Thyrinteina arnobia) or other lepidopteran or coleopteran insects in forest plantations in Brazil, as
evidence provided of a need for deltamethrin did not demonstrate that this is the only feasible way
of controlling the targeted pest insects and that these species are causing severe damage (e.g. based
on tests with alternative non-chemical or less toxic methods of pest management, cost-benefit
analysis, social and environmental impact assessment, as required by FSC (2007) Procedure:
Processing pesticide derogation applications), and also as more selective alternatives are available.
March 2010
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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
E. The technical advisors recommend the certificate holders who applied for a derogation for deltamethrin (liquid formulation Decis® 25 CE) to:
1. monitor the distribution of Thyrinteina arnobia or other defoliating insects, locate infested areas
with a high density of Thyrinteina or defoliators, identify the type of defoliating insect (genus
and, if possible, species), estimate level of damage, and define a critical density of Thyrinteina or
other defoliating insects (maximum acceptable density for achieving silvicultural objectives);6
2. promote the establishment of natural enemies (such as Trichogramma wasps and parasitic wasp
Anaphes nitens) by preserving fragments of native vegetation surrounding Eucalyptus
plantations, limit control of Thyrinteina and defoliators to highly infested areas (where estimated
density of Thyrinteina or of defoliators exceeds the critical density) and areas with susceptible
tree species, and if necessary use Bacillus thuringiensis (B.t. subspecies kurstaki or B.t.
subspecies aizawai) or B. t. combined with a selective, low-toxicity insecticide (such as spinosad,
azadirachtin, or neem);7
4. conduct field tests on alternatives, in particular Bacillus thuringiensis (B.t. subspecies kurstaki,
B.t. subsp. aizawai), pathogenic fungi (Beauveria bassiana, Metarhizium anisopliae,
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
7
8
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
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
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
March 2010
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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
anisopliae var. acridum), Beauveria bassiana combined with Bacillus thuringiensis (e.g. B.t.
subsp. sooncheon or B.t. subspecies roskildiensis), Trichoderma species, combinations of
glucono delta-lactone and pathogenic fungi (e.g. glucono delta-lactone combined with Beauveria
bassiana and Bacillus thuringiensis), parasitic nematodes (Steinernema or Heterorhabditis
species), and consider using borax or spinosad if biological agents are not sufficiently effective;9
4. during the derogation period, keep records on total annual use of fipronil (kg of active ingredient
used) for preventive treatment of seedlings, and include this information in audit reports;
5. take the greatest care that handling and application of fipronil does not endanger human health
and natural enemies (mammals, birds, or predatory/parasitic insects), implement measures to
reduce risk to acceptable levels, and strictly follow all legal requirements in Brazil for the use of
pesticides, in particular the controls for occupational and environmental safety required by the
national and regional authorities and specific guidelines.
Further, the technical advisors recommend the certificate holders to:
G. collaborate in tests – with experts and PhD students at research institutions, commercial enterprises,
government agencies and/or other forest companies – on alternatives to substitute deltamethrin,
fenitrothion, fipronil and sulfluramid, and gradually reduce use of insecticides through integrated
pest management: monitoring pest insect/s and damage level, defining a critical density of pest
insect, using insecticides only in highly infested areas where the critical density is exceeded or if
damage levels are unacceptably high, applying insecticides at minimum effective rates (kg/ha or
g/m2), and complementing these with biological control and preventive silvicultural practices;10
H. establish a common framework (general procedure) for integrated management of leaf-cutting ants;
I. in the medium to long term, develop preventive silvicultural practices that reduce occurrence of pest
insects and damage to trees, by planting more robust tree species (e.g. mixed forests, native species)
that are well-adapted to local conditions and have a low susceptibility to pest insects, reducing weed
control (leaving part of herbaceous vegetation on the ground), growing cover crops (such as Mucuna
bracteata), limiting area of clear-felling, protecting natural enemies (insects) and rare species (birds,
mammals, reptiles, amphibians) in zones with natural forest on part of managed area (appropriate in
size to scale and intensity of forest management operations);11
J. consult with directly or potentially affected parties where insecticide baits are used and, especially
near nature reserves (parks) or sensitive areas (wildlife habitats, surface waters), consult with local
or regional authorities for environmental protection and scientific experts on wild life conservation.
9
Laboratório de cupins, UNESP. http://www.rc.unesp.br/ib/ceis/cupins.php
Chemicals that are currently not authorized in Brasil can be registered on a temporary basis for research:
Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA), Registro Especial
Temporário. http://www.ibama.gov.br/qualidade-ambiental/areas-tematicas/agrotoxicos/registro-especial-temporario-ret/
11
Principios y Criterios del FSC para el Manejo Forestal – Versión completa de la Versión 5-0 Borrador 2-0 de
los PyC del FSC (Principios 6.2 - 6.6, pp. 55-59; Criterio 10.5 original, p. 84), 2009 (This working document
is no longer online; see website on the review of FSC Principles and Criteria: http://www.fsc.org/pcreview.html)
10
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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
I. Control of Leaf-Cutting Ants (Atta / Acromyrmex species)
1.1 Demonstrated Need for Use of Deltamethrin, Fenitrothion, Fipronil and Sulfluramid
In most places in Brazil, leaf-cutting ants present a major pest organism. Throughout the year, leafcutting ants attack fruit and vegetable crops, pastures, and trees. The ants can damage field crops or
forests by consuming large quantities of leaves. In eucalypt and pine plantations, estimated annual
losses of wood appear to be significant. These may result in substantial monetary losses. Ant species
causing damage mainly belong to the genus Atta (saúva) or genus Acromyrmex (quenquéns) (Thomas
1990).12 According to a study, a single nest of leaf-cutting ants (Atta species) can harvest up to 1 ton of
green leaves (wet weight) per year. It has been reported that one nest of leaf-cutting ants harvested or
damaged up to 86 eucalypt and (or) up to 161 pine trees/seedlings in one year. Based on an average
density of four ant nests per hectare, this corresponds to tree losses of 14% to 14.5% (Forti & Boaretto
1997).13 If this level of damage occurred nationwide on all 6 million ha of forest plantations in Brazil,
economic losses of timber products could reach US$ 6.7 billion (or triple this on price of wood pulp).
Although alternative methods of ant control have been studied in the past, chemical control remains the
only method that is practical for control of leaf-cutting ants. Granular baits containing an insecticide are
used most widely, are highly effective at low cost and present a smaller hazard than applying a liquid
insecticide or thermal fogging. Sulfluramid is highly effective for control of leaf-cutting ants, due to the
delayed toxic action and as it is odourless. Nearly all timber companies in Brazil use insecticide baits to
control ants in forest plantations. Baits (small pellets) are applied on the ground. Organochlorines used
previously (aldrin and dodecachlor) are now banned in Brazil. Aldrin is internationally banned under
the Stockholm Convention due to the high persistence and risk of bioaccumulation. Methylbromide, a
highly toxic gas previously used against ants, is being phased out under the Montreal Protocol (UNEP
2000).14 In forest planations in Brazil, insecticide baits are applied on nearly 100% of managed areas.
Baits are „becoming the most relevant product for an appropriate handling‟, according to applicants. In
Pará, Amata manages 650 hectares (of which 47% are protected areas) and deforested areas (pastures
or abandoned land) are being reforested with native species such as paricá (Schizolobium amazonicum).
· Reasons for Control of Leaf-Cutting Ants
Leaf-cutting ants of the genera Atta and Acromyrmex are considered a pest insect as they cause damage
in forestry and agriculture. The ants cut leaves during the whole season and this can result in substantial
losses. To guarantee economic productivity of plantations, these ants must be controlled effectively.15
· Areas Affected by Damage from Leaf-Cutting Ants
Plantations of pioneer species such as pine and eucalyptus are at an increased risk of ant herbivory. Ant
nests occur particularly at the forest edge, after an intense disturbance of habitat (clear-felling), in areas
with loose soil and where numbers of natural enemies are low (e.g. if ground vegetation is removed).
12
13
14
15
Thomas JC. Formigas cortadeiras: instruções básicas para o controle. EMATER-PR, Curitiba 1990
Forti L.C., y Boaretto M.A.C. Formigas cortadeiras: Biologia, ecologia, danos e controle. UNESP 1997
United Nations Environment Programme (UNEP). The Montreal Protocol on substances that deplete the
ozone layer. Nairobi, Kenya 2000. http://www.unep.org/OZONE/pdfs/Montreal-Protocol2000.pdf
Della Lucia T.M.C., y Araújo M.S. Formigas cortadeiras: atualidades no combate. In: Zambolim, L. (ed.).
Manejo integrado: doenças, pragas e plantas daninhas. Editora UFV 2000, pp. 245-273.
March 2010
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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
· Ecosystem Functions of Leaf-Cutting Ants: Ants enrich soils with nutrients and transfer these to the
upper soil layer, reduce understory vegetation surrounding nests, and disperse the seeds of forest plants.
· Leaf-Cutting Ants and Indigenous Forests: Leaf-cutting ants eat native and exotic tree species but
indigenous forests appear to be resistant toward the attack from leaf-cutting ants. (This may be due to
lower palatability of native tree species, less intense disturbances, and a greater number of enemies.)
· Distribution of Leaf-Cutting Ant Species
In North Brazil, the Midwest and on the plateaus of Santa Catarina state, the predominant genus of
leaf-cutting ants is Acromyrmex. In South Brazil, Acromyrmex occurs mainly in pine reforestations.
Besides the species Atta and Acromyrmex, ants of the species Sericomyrmex may also cause damage.
· Alternatives for Control of Leaf-Cutting Ants: Alternatives include biological control (using fungal or
bacterial pathogens), use of plant extracts, pheromones, mechanical control, promoting natural enemies
(predators and parasitoids), and long-term cultural methods (e.g. growing more robust tree species) So
far, many alternatives were not sufficiently effective in the field (Marinho et al 2006; Araújo et al 2003).16
1.1.1 Effectiveness of Deltamethrin, Fenitrothion, Fipronil and Sulfluramid for Ant Control
Strategies of chemical control differ mainly according to the type of formulation. Available products
are formulated as a powder/dust, liquid or granular baits. Fenitrothion liquid is applied by fogging.
Dust and liquid formulations are used on new ant nests, while fogging is used on large nests. Among
available formulations, granular baits have the advantage of being less dangerous for workers who
conduct control, and allow nests to be treated on sites where access is difficult. Insecticides formulated
as baits include sulfluramid, chlorpyrifos, fipronil, and a mixture of fipronil/sulfluramid. Sulfluramid
was first introduced in 1993 to substitute the organochlorine mirex (= dechlorane) which was banned.
Sufluramid, a fluorinated sulphonamide, blocks the ant organism‟s energy production. It becomes
more toxic in the organism as a metabolite inhibits energy production of ants (FCES 1997).17 When
compared to most other insecticides, the acute toxicity of sulfluramid is relatively low. 90 days after
application of sulfluramid (0.3% in baits) to nests of Atta sexdens rubropilosa, level of control was
close to 100% (Laranjeiro & Zanuncio 1995).18 Sulfluramid (0.3%) reduced colonies of Atta sexdens
rubropilosa three days after application, resulting in control levels of 84-90% (Zanetti et al 2004).19
16
Marinho C.G.S., et al. Fatores que dificicultam o controle das formigas cortadeiras. Bahia Agrícola 7(2),
2006. http://www.seagri.ba.gov.br/pdf/comunicacao3_v7n2.pdf
Araújo M.S., et al. Estratégias alternativas de controle de formigas cortadeiras. Bahia Agrícola 6(1), 2003.
http://www.seagri.ba.gov.br/pdf/V6N1_pesq_formigas.pdf
17
18
Florida Cooperative Extension Service (FCES). Insecticides used in the urban environment: Mode of action.
Florida 1997. http://edis.ifas.ufl.edu/IN077
Laranjeiro AJ, y Zanuncio JC. Nota Técnica: Avalição da isca a base de sulfluramida no controle de Atta
sexdens rubropilosa pelo processo dosagem unica de aplicao. IPEF 48/49: 144-152, 1995.
http://www.ipef.br/publicacoes/scientia/nr48-49/cap16.pdf
19
Zanetti R, et al. Eficiência de iscas granuladas (sulfluramida 0,3%) no controle de Atta sexdens rubropilosa
(…). Ciência e Agrotecnologia 28(4): 878-882, 2004. http://www.editora.ufla.br/revista/28_4/art21.pdf
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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
Sulfluramid is formulated as granular baits which contain 0.3% sulfluramide, fruit pulp (usually from
oranges) and plant-based fat/oil. Certificate holders use the following products: Attamex-S, Dinagro-S,
Mirex-S Max, Pikapau-S, and Tamanduá Bandeira-S. In addition to these products, in south Brazil
companies also use Fluramim, Formicida Isca Agripec, Mirex-S and Mirex-S Plus.
Fipronil achieves good control of most species of leaf-cutting ants except Atta capiguara (Nagamoto
et al 2007).20 In Atta sexdens rubropilosa and Acromyrmex species, fipronil caused mortality of over
80% (Coll 2003).21 However, fipronil and chlorpyrifos were not very effective in baits tested on grasscutting ants (Atta capiguara), and sulfluramid resulted in higher levels of control (Forti et al 2003).22
Granular baits commercialised under the name Blitz contain 0.003% fipronil (active ingredient).
Deltamethrin for ant control is formulated as powder/dust. Companies in south Brazil use the product
K-Othrine 2P (containing 0.2% deltamethrin. The soil must be dry. In the U.S.A. resmethrin, which is
also a pyrethroid like deltamethrin, effectively controlled Texas leaf-cutting ants (TAE (no year)).23
Fenitrothion is applied as vaporised liquid (using a thermal fogger) directly to the entrances of ant
nests. The product Sumifog 70 contains 7% fenitrothion and mineral oil. Acephate, chlorpyrifos and
diazinon (other organophosphats) did not effectively control Texas leaf-cutting ants (TAE (no year)).23
1.1.2 Need for Chemical Control of Leaf-Cutting Ants – Position of Technical Advisors
There is clear evidence that leaf-cutting ants of the genera Atta and Acromyrmex present a problem in
forest plantations, particularly during establishment. In Brazil, fast-growing exotic tree species such as
eucalypt species and subtropic pine species (e.g. Pinus taeda) are grown on an increasing scale. This
allows companies to achieve higher net returns and to some extent contributes to reducing pressure on
native forests. Demand for quality wood for furniture led companies to harvest older trees, while an
increasing demand for resin and wood pulp is pushing companies to expand pine plantations further
(Oliveira 2005).24 Certain Eucalyptus species such as E. grandis are more frequently subject to attack
from leaf-cutting ants (Anjos 2008).25 Ants of the species Acromrymex subterraneus showed the least
20
21
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
Science 80: 9-13, 2007. http://dx.doi.org/10.1007/s10340-006-0143-8
Coll O.R. Detección y control de hormigas cortaderas (Hymenoptera-Formicidae) en plantaciones forestales
en Misiones y noreste de Corrientes. SAGPyA Forestal 28: 2-6, 2003. http://www.sagpya.mecon.gov.ar/new/00/forestacion/revistas/revista28/hormig28.pdf, http://www.cababstractsplus.org/google/abstract.asp?AcNo=20033189361
22
Forti LC, et al. Eficiencia de sulfluramida, fipronil y clorpirifos como sebos en el control de Atta capiguara
Gonçalves (Hymenoptera: Formicidae). Pasturas Tropicales 25(3): 28-35, 2003.
http://www.fca.unesp.br/lisp/artigos/Eficiencia%20de%20sulfluramida,%20fipronil%20y%20clorpirifos%2003.pdf
23
Texas Agricultural Extension Service (TAE). Texas leaf-cutting ant.
http://entowww.tamu.edu/extension/bulletins/uc/uc-033.html
24
25
Oliveira M. Valuable wood. Pesquisa FAPESP 115, 2005. http://www.revistapesquisa.fapesp.br/?art=1561&bd=1&pg=1&lg=en
Anjos N., et al. Árvores e formigas cortadeiras (Hymenoptera: Formicidae) em Viçosa, Minas Gerais. Revista
Trópica 1(2): 11-16, 2008. http://www.unilueneburg.de/umanagement/csm/content/naoek/downloads/downloads_publikationen/Anjos_et_al_2008_Revista_Tropica.pdf
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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
preference for E. citriodora and E. acmenioides (Della Lucia et al 1995).26 Further, the clear-felling of
extended areas of plantations creates open spaces which facilitate colonization by leaf-cutting ants such
as Atta cephalotes (Jaffe & Vilela 1989).27 After clearing a mature forest, nests of Acromyrmex and
Atta species increased strongly in number; numbers of ant nests declined later in the secondary forest
but remained higher than before (Vasconcelos & Cherrett 1995).28 Higher intensity of disturbances of
habitat was generally associated with an increased number of ant nests (Da Silva & Schoereder 2005).29
Estimates of biomass consumed by leaf-cutting ants vary significantly in the literature. The applicants
quote only one publication (Forti & Boaretto 1997).17 Several authors have estimated or reported lower
losses, however (see annex I). Density of ant nests (number per heactare) depends on numerous factors
including site conditions, silvicultural practices, and the presence of natural enemies. Intensive forest
management (based on fast-growing, exotic species and short rotation times) necessitates control of
leaf-cutting ants. But forest managers ought to recognize that intensive management can exacerbate
problems with leaf-cutting ants. It appears that companies are not utilizing the potential of preventive
practices sufficiently. In the long term, damage from leaf-cutting ants can be partially reduced through
cautious planning of forest management e.g. by growing robust tree species adapted to local conditions.
In the short term, alternatives can substitute chemical control only partially. Sulfluramid controls leafcutting ants very effectively, achieving up to 100% mortality. But its extremely high persistence is a
problem. Under the Stockholm Convention, perfluorooctane sulfonate (main precursor of sulfluramid)
will be restricted (or may possibly be prohibited) sometime, although critical uses may be exempted
(UNEP 2007).30 Production and use of sulfluramid might be included in an exemption if these are
considered critical uses. However, use of sulfluramid for ant control should be substantially reduced to
reduce the influx of sulfluramid to the environment and gradual accumulation in wildlife and humans.
FSC certificate holders would be well advised to gradually reduce the amount of sulfluramid used, by
substituting this chemical with other insecticides and alternative methods of control within the 5-year
derogation period. Alternative insecticides are available and biological methods can complement these.
Therefore it should be possible to discontinue the use of sulfluramid after the end of March 2015 in FSC
certified plantations.
26
27
28
29
Della Lucia T.M.C., et al. Avaliação da não-preferência da formiga cortadeira Acromyrmex subterraneus (…)
ao corte de Eucalyptus. Revista Árvore 19(1): 92-99, 1995 (quoted by Boaretto & Forti 1997)
Jaffe K., and Vilela E. On nest densities of the leaf-cutting ant Atta cephalotes in tropical primary forest.
Biotropica 21(3): 234-236, 1989. http://atta.labb.usb.ve/Klaus/art45.pdf
Vasconcelos H.L., and Cherrett J.M. Changes in leaf-cutting ant populations (Formicidae: Attini) after the
clearing of mature forest in Brazilian Amazonia. Studies on Neoptropical Fauna and Environment 30(2): 107113, 1995. http://www.informaworld.com/smpp/content~db=all~content=a905708940
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
30
UNEP – POPs Review Committee. Risk management evaluation on perfluorooctane sulfonate. Geneva 2007.
http://chm.pops.int/Portals/0/docs/from_old_website/documents/meetings/poprc/chem_review/PFOS/PFOS_RME_e.pdf (en)
UNEP – Comité de Examen de los COPs. Evaluación de la gestión de riesgos del sulfonato de Perfluorooctano. Ginebra 2007. http://chm.pops.int/Portals/0/Repository/poprc3/UNEP-POPS-POPRC.3-20.Spanish.PDF (sp)
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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
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 5 – Produtos Quimcos. http://www.mte.gov.br/legislacao/normas_regulamentadoras/nr_rural_05.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
/ agrotóxicos. 2002. http://www.higieneocupacional.com.br/download_2/manual-fitossanitario-agrotoxicos.zip
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
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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
1.2.2 Risk Mitigation for Control of Leaf-Cutting Ants with Insecticides
Insecticides in dust or liquid formulations have the disadvantage that workers may be more exposed
during application. Use of granular baits is less dangerous for workers as exposure is low. Insecticide
baits are applied close to active entrances of ant nests, or trails on anthills. Baits are commonly applied
with backpack granular applicators (allowing dose to be adjusted) or are applied directly from packages
without manual contact. Granular baits are considered to be less hazardous to the environment than
applying a liquid formulation by fogging. For example, application of sulfluramid in baits is expected
to pose a low risk to the environment due to the low concentration of the active ingredient, low amount
applied to treated areas, safer formulation as there is no risk of drift, and shorter period of exposure of
non-target animals as ants quickly remove baits.
Baits enclosed in small sachets (micro-porta-iscas / mipis) have been used for over 15 years (Laranjeiro
1994).31 This allows using baits in humid weather. Applying baits in sachets (mipis) also reduces the
risk to non-target animals by preventing these from eating baits. Baits can also be applied in larger bait
dispensers (porta-iscas) (Sousa 1996).32 Bait dispensers are considered practical, cost-effective, and
also increase security for workers applying baits (Pereira 2007).33
Measures implemented to mitigate risks of insecticides differ between certificate holders. These assert
that they comply with national legislation, directions of manufacturers and FSC‟s standards. The FSC
encourages certificate holders to practice integrated pest management (FSC 2009).34 In South Brazil,
companies have implemented several measures to mitigate risks: evaluating ant densities in managed
areas, estimating the amount of baits needed for individual nests, recommendations on appropriate
method and timing of application, evaluating bait consumption and effectiveness of control, monitoring
distribution of nests, recording control operations (location of treated sites, type/amount of bait used on
individual forest units, record-keeping in a database), safe storage of products, and periodic training of
workers to improve qualification and health. More progressive companies apply insecticide baits only
in the first year of establishment, use bait dispensers, have longer rotation intervals (up to 20 years),
monitor residues of insecticides in the environment (by analyzing water samples etc), improve the
efficiency of bait application by optimizing/reducing amounts (one company aims at 20% reduced
amounts within two years), and/or surround plantations with native forest in a wider zone than the
minimum of 30 m (source: Appendix B-I to applications).
In other regions of Brazil, many or most certificate holders have implemented the following measures
to mitigate the risks of formicides/insecticides: monitoring ant infestation in planted areas by sampling
and evaluating damage levels and density of ant nests in forest transects, classifying infestation level
31
Laranjeiro A.J. Manejo integrado de formigas cortadeiras na Aracruz Cellulose. IPEF, Piracicaba 1994.
http://www.ipef.br/publicacoes/curso_formigas_cortadeiras/cap07.pdf
32
Sousa N.J. Avaliação do uso de três tipos de porta-iscas no controle de formigas cortadeiras em áreas
preparadas para implantação de povoamentos de Pinus taeda L. Laboratório de Proteção Florestal 1996.
http://floresta.ufpr.br/~lpf/pragas01.html#p3
33
Pereira L.G.P. Estratégias de controle de formigas cortadeiras. CETEC 2007.
http://sbrtv1.ibict.br/upload/dossies/sbrt-dossie96.pdf?PHPSESSID=8097c61ce57048fc7d4ca763687fc962 (p. 14)
34
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
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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
(nil, low, medium, or high), selecting control methods and dosage, controlling active nests in nurseries
[viveiros] and planted forest units where nest density exceeds a critical level (defined as area covered
with nests per hectare) and where there is a risk of economic damage, and limiting application of baits
to dry periods (source: Appendix 4 to applications). One company monitors water quality of streams
(no residues of sulfluramid have been detected).
In Brazil, sulfluramid (formulated as granular baits) is categorised in toxicity class IV (Pouco tóxico /
„Low toxicity‟). This reflects the low content (0.3%) of sulfluramide in baits. Baits for use in domestic
gardens contain 0.01% sulfluramid (e.g. Grão Verde FS; Sulflurex-S). The World Health Organization
categorises the active ingredient sulfluramid in WHO class III: „Slightly hazardous‟ (WHO 2006).35
Table 3. Granular Insecticide Baits (Isca Formicida) in Brazil
Active
Ingredient
Commercial Name
Recommended Dose
S: 8-10 g per m2 nest
Q: 10-12 g per nest
S: 6-10 g per m2 nest
Fluramim
Q: 10-30 g per nest
Formic. Granul. Dinagro-S S: 6-10 g per m2 nest
Formic. Granul. Pikapau-S S: 6-10 g per m2 nest
Isca Formic. Attamex-S
S: 6-10 g per m2 nest
Isca Tamanduá Bandeira-S S: 6-10 g per m2 nest
S: 10 g per m2 nest
Blitz
Q: 5 g per nest
Isca Formicida Landrin
Q: 8-10 g per nest
Isca Formicida Pyrinex
S: 5-10 g per m2 nest
(Isca Formicida Pyrineus)
Isca Formicida Atta-Fós
S: 10 g per m2 nest
Toxicity Class* in Brazil /
WHO Class (active ingredient)
Mirex-S; Dinagro-S
Sulfluramid
Fipronil
Chlorpyrifos
Isca Formilin (BASF; not
Diflubenzuron
listed in Anvisa register)
2
S: 10 g per m nest
Formulated product (in Brazil): IV
WHO class III „Slightly hazardous‟
Formulated product (in Brazil): IV
WHO class II „Moderately hazardous‟
Formulated product (in Brazil): III
WHO class II „Moderately hazardous‟
Formulated product (in Brazil): IV
WHO class U „Unlikely to present
acute hazard in normal use‟
S = Sauba (Atta species); Q = Quenquém (Acromyrmex species).
*
Toxicicity Class: I - Extremamente tóxico; II - Altamente tóxico; III - Medianamente tóxico; IV - Pouco tóxico
(Note: WHO classification refers to the active ingredient. The toxicity class of a formulated product may differ.)
References: Botton 2007; Pereira 2007; Anvisa 2009
35
World Health Organization. The WHO recommended classification of pesticides by hazard 2004. Geneva
2005, amended in 2006. http://www.who.int/ipcs/publications/pesticides_hazard/en/
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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
Hojas de Seguridad / Safety Data Sheets for Formicide Use
Attamex-S (Unibras). http://www.unibras.net.br/site/images/online/arquivo_atta_mex_s_jardinagem_rev.pdf
Blitz (Basf). http://www.agro.basf.com.br/UI/Produtos.aspx?CodProduto=10&CodTipoProduto=1
Dinagro-S (Dinagro Agropecúaria). http://container2.netsite.com.br/dinagro/arquivos/486.doc
Fluramim (Milenia Agro). http://www.milenia.com.br/comum/arquivos/documentos/Fluramim%20-%20FISPQ.pdf
Formicida Isca Agripec (Nufarm / Agripec). http://www.nufarm.com.br/
Isca Form. Fortex (Biocarb). http://www.biocarbagroquimica.com.br/adm/fichas/20080208041807FISPQiscaformicidaFortex.pdf
Isca Formicida Landrin (Landrin).
http://www.landrin.com.br/fispqefichas/FICHA%20DE%20EMERG%CANCIA%20ISCA%20FORMICIDA%20LANDRIN.pdf
K-Othrine 2P (Bayer). http://www.bayercropscience.com.br/site/nossosprodutos/saudeambiental/DetalheDoProduto.fss?Produto=22
Mirex-S (Agroceres / Atta-Kill). http://www.mirex-s.com.br/pdf/ficha_tecnica_mirex-s_2.pdf
Pikapau-S (Produtos Químicos São Vicente). http://www.pikapau.com.br/produtos.asp?cat=3&prod=28
Sumifog 70 (Iharabras). http://www.ihara.com.br/sistemas/ficha_seg/doctos_pr/6100122.pdf
Tamanduá Bandeira-S (Grupo Bio Soja). http://www.biosoja.com.br/downloads/Boletim_7.pdf
1.2.3 Risk Mitigation for Use of Sulfluramid – Position of Technical Advisors
Ecological risks of sulfluramid baits: Large-scale use sufluramid may present a risk to non-target
animals (birds, mammals, amphibians, and reptiles) in the long term. This is due to several factors:
1. Forest plantations in South America cover large areas, often several 10'000 hectares. Sulfluramid is
usually applied during establishment (during years 1-3 after planting trees) at a rate of 8 g bait per
m2 of ant nest surface (near trails and entrance holes). Granular baits contain 0.3% of sulfluramid.
Total application rates of baits vary between 0.4 kg/ha and >3 kg/ha. In a survey, ants did not collect
14-43% of organic baits (Formicida Cocapec) (source: SGS-FM-1943). On average, ants left 28.4%
of baits. Assuming a total application rate of 1.2 kg/ha and similar percentage of leftover baits, the
average amount of sulfluramide (active ingredient) directly available to non-target animals (from
leftover baits) after one control operation is about 1 g per hectare. Although this amount seems low,
sulfluramid metabolites are gradually accumulating in living organisms and in the environment.
Some companies have reduced the total application rate to 0.4 kg/ha, but it appears that rates are
over 1.2 kg/ha in many places. In targeted use on specific sites, it seems plausible to assume that
baits might be applied to about 0.5% to 1% of total managed area. For example, if the total managed
area is 50'000 hectares, the treated area would be 250-500 ha. Based on a rate of 8 g bait per m2 nest
surface and 0.3% sulfluramid content, the amount of sulfluramid (active ingredient) applied during
establishment (years 1-3) to treated areas would be 60-120 kg (or 240 g per ha). One rotation cycle
on a Eucalyptus plantation takes 5-17 years (Couto et al 2004),36 or 11 years on average. During five
36
Couto L., et al. Eucalypt based agroforestry systems as an alternative to produce biomass for energy in Brazil.
In: IUFRO, IEA Bioenergy, SRWC: Biomass and Bioenergy Production for Economic and Environmental
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rotations (55 years on average), 300-600 kg of sulfluramid (active ingredient) would be applied to
treated areas. The amount per hectare seems low (especially if not targeted). But persistent metabolites of sulfluramid will continue to accumulate in the environment, particularly in living organisms.
In the whole of Brazil, an estimated 12'000 tons of insecticide baits are applied per year (Boaretto &
Forti 2000).37 Sulfluramid accounts for >95% of baits in Brazil (UNEP 2009).38 This corresponds to
34 tons of sulfluramid (active ingredient) entering the environment each year. Total production of
sulfluramid in Brazil is 30 tons per year (Cerqueira 2007).39
2. Sulfluramid is highly soluble in fats. It has a very large octanol-water partition coefficient logKOW
>6.8 (BCPC 2006/07). A value of logKOW 3.1 was also reported, and of 500 for the bioconcentration
factor (BCF), indicating moderate to high potential of sulfluramid to bioaccumulate (HSDB 2003).40
3. Fluorinated compounds can be significant contaminants in the environment. The combination of
persistence and biological activity is a cause for concern. Sulfluramid and its metabolite perfluorooctane sulfonamide (PFOA or DESFA) are both highly persistent (Key et al 1997).41 PFOA has an
extremely long half-life (slow degradation) compared to that of sulfluramid (Manning et al 1991).42
Practically no degradation of sulfluramid occurs beyond the metabolites PFOA and perflurooctanesulfonic acid (PFOS) (Key et al 1997). In the tissue or blood from rats exposed to sulfluramid for 56
days, PFOA was detected but it did not accumulate (Grossman et al 1992).43 In animals, sulfluramid
and PFOA are converted to PFOS (Xu et al 2004).44 PFOS has a high bioaccumulation potential, can
biomagnify (accumulate via food chain), is extremely persistent, and toxic (UNEP 2006).45 In rats,
Benefits. pp. 20-22. Conference 7-10 November, 2004. http://www.woodycrops.org/NR/rdonlyres/BF9B2067FDB0-49B0-9543-8EEA03A415FD/1651/2004Abstracts.pdf
37
38
Boaretto M.A., y Forti L.C. Perspectivas no controle de formigas cortadeiras. UNESP, Botucatu, São Paolo
2000. http://www.uesb.br/entomologia/cortadeiras.htm, (1997): http://www.ipef.br/publicacoes/stecnica/nr30/cap3.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.
http://www.pops.int/documents/meetings/poprc/submissions/AnnexF_2007/PFOS%20Brazil.doc
40
41
42
43
44
45
British Crop Protection Council (BCPC). The e-Pesticide Manual (electronic edition)., Hampshire, UK
2006/2007. http://www.pesticidemanual.com/
Hazardous Substance Database (HSDB) of the US National Library of Medicine (search for „sulfluramid‟).
(Data last updated in 2003). http://toxnet.nlm.nih.gov/cgi-bin/sis/search http://toxnet.nlm.nih.gov/cgi-bin/sis/htmlgen?HSDB
Key B.D., Howell R.D., and Criddle C.S. Fluorinated organics in the biosphere. Environmental Science and
Technology 31(9): 2445-2454, 1997. http://www.stanford.edu/group/evpilot/pdf/es961007c%202.pdf (see p. 2450)
Manning R.O., et al. Metabolism and disposition of sulfluramid, a unique polyfluorinated insecticide, in the
rat. Drug Metabolism and Disposition 19(1): 205-211, 1991. http://dmd.aspetjournals.org/cgi/content/abstract/19/1/205
Grossmann M.A., et al. Distribution and tissue elimination in rats during and after prolonged dietary exposure
to a highly fluorinated sulfonamide pesticide. Journal of Agriculture and Food Chemistry 40 (12): 2505–
2509, 1992. http://pubs.acs.org/doi/abs/10.1021/jf00024a033
Xu L., et al. Biotransformation of N-ethyl-N-(2-hydroxyethyl)perfluorooctanesulfonamide by rat liver
microsomes, cytosol, and slices and by expressed rat and human cytochromes P450. Chemical Research in
Toxicology 17(6), 2004. http://pubs.acs.org/doi/abs/10.1021/tx034222x
UNEP – POPs Review Committee. Risk profile on perfluorooctane sulfonate. Genevra 2006.
http://chm.pops.int/Portals/0/docs/from_old_website/documents/meetings/poprc/chem_review/PFOS/PFOS_RiskProfile_e.pdf (en)
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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 accumulation 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 Residues in fish, birds
http://chm.pops.int/Portals/0/docs/from_old_website/documents/meetings/poprc/chem_review/PFOS/PFOS_RiskProfile_s.pdf (sp)
46
47
48
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
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
DeWitt J.C., et al. Immunotoxicity of perfluorooctanoic acid and perfluorooctane sulfonate and the role of
peroxisome proliferator-activated receptor alpha. Critical Reviews in Toxicology 39(1), 2009.
http://www.informahealthcare.com/doi/abs/10.1080/10408440802209804?cookieSet=1&journalCode=txc
49
50
51
52
Porto M.F., y Milanez B. Documento técnico sobre os impactos da sulfluramida e de perfluorooctano (PFOS)
sobre a saúde humana e ambiental. Centro de Estudos da Saúde do Trabalhador e Ecologia Humana – Escola
Nacional de Saúde Pública Sérgio Arouca, Fundação Oswaldo Cruz. Abril 2009 (document available from
the authors: Dr M.F.S. Porto, http://buscatextual.cnpq.br/buscatextual/visualizacv.jsp?id=K4780497E1 )
BioAgri Laboratorios Ltda. Assesment of the environmental risk of sulfluramid-based ant baits in a forest
area. Project 01/97, Brazil 1997 (report incl. in derogation application from Veracel Celulose S.A, June 2007)
Giesy J.P., and Kannan K. Perfluorochemical surfactants in the environment. Environmental Science and
Technology 36 (7): 146A–152A, 2002. http://www.usask.ca/toxicology/jgiesy/pdf/feature%20article/FA-2.pdf
Stock N.L., et al. Perfluoroalkyl contaminants in the Canadian Arctic: Evidence of atmospheric transport and
local contamination. Environmental Science and Technology 41 (10): 3529–3536, 2007.
http://pubs.acs.org/doi/abs/10.1021/es062709x
Martin J.W., et al. Perfluoroalkyl contaminants in a food web from Lake Ontario. Environmental Science and
Technology 38 (20): 5379–5385, 2004. http://pubs.acs.org/doi/abs/10.1021/es049331s
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and mammals show that perfluoroalkylated sulfonates can bioaccumulate in marine and fresh-water
ecosystems (Houde et al 2006).53 Levels of PFOS measured in marine tucuxi dolphins from
Guanabara Bay, Brazil, were considered to be high enough to present a risk to the small population
concerned (Dorneles et al 2008).54 Besides being used as an insecticide, sulfluramid is also used as a
surfactant. But high levels of PFOS in dolphins off the Brasilian coast indicate that production of
sulfluramid on a large scale may be contributing significantly to global chemical contamination.
Measures to reduce risks from sulfluramid
Sulfluramid poses a risk to mammals (e.g. deer, rats), birds, amphibians, reptiles due to sulfluramid‟s
moderate potential for bioaccumulation, its moderate toxicity for mammals or high toxicity for birds,
and the high persistence of sulfluramid and its primary metabolite perflurooctane sulfonamide (PFOA).
Animals may be poisoned by consuming leftover baits or ants contaminated with sulfluramid. Over the
last years, several certificate holders (e.g. Jari Celulose, Veracel) have reduced the application rate of
sulfluramid baits to about 0.4 kg/ha. But this does not change the fact that PFOS, the main metabolite
of sulfluramid, is practically not metabolized and is accumulating in the environment and in organisms.
To reduce risks to non-target animals, sulfluramid baits should be applied predominantly or only during
the season and time of day when activity of leaf-cutting ants is at the highest level. Systematic (routine)
use of insecticides has negative impacts on non-target ant species such as leaf-litter ants – formigas de
serapilheira (Ramos et al 2003).55 These ants do not cut leaves but play an important role in forests.
Certain species of leaf-cutting ants such as Atta robusta are now close to extinction (Souza 2005).56
Bait dispensers (porta-iscas) or sachets (Mipis) should be used for sulfluramid application. This seems
feasible (Ukan 2008).57 If sulfluramid baits are applied directly (without using bait dispensers or Mipis)
on the major proportion of treated areas, evidence that this is necessary should be provided in audit
reports to the certifier (e.g. cost estimates for applying baits in dispensers or Mipis). Workers need to
follow use directions strictly and apply sulfluramid baits at the minimum recommended dose.
Sulfluramid should not be used in sensitive areas such as wildlife habitats or areas near nature reserves.
Certificate holders are recommended to define a quantitative reduction target (% reduction in the total
amount of sulfluramide active ingredient used per year) for the derogation period. As other insecticides
and a number of alternative methods are available for control of leaf-cutting ants, the aim should be to
reduce sulfluramid use by −100% within five years and to discontinue use after March 2015.
53
54
55
56
57
Houde M., et al. Biological monitoring of polyfluoroalkyl substances: A review. Environmental Science and
Technology 40 (11): 3463–3473, 2006. http://pubs.acs.org/doi/abs/10.1021/es052580b
Dorneles P.R., et al. High accumulation of perfluorooctane sulfonate (PFOS) in marine tucuxi dolphins
(Sotalia guianensis) from the Brazilian Coast. Environmental Science & Technology 42 (14): 5368–5373,
2008. http://pubs.acs.org/doi/abs/10.1021/es800702k
Ramos L.S., et al. Impacto de iscas formicidas granuladas sobre a mirmecofauna não-alvo em eucaliptais
(…). Neotropical Entomology 32(2): 231-237, 2003. http://www.scielo.br/pdf/ne/v32n2/17406.pdf
Souza D.J. Cortadeiras sob ameaça. Revista Ciência Hoje 222, 2002. http://cienciahoje.uol.com.br/4148
Ukan D. Avaliação qualitativa e quantitativa de micro-porta-iscas para o controle de formigas cortadeiras
(…). UFPR 2008. http://www.floresta.ufpr.br/pos-graduacao/defesas/pdf_ms/2008/d497_0701-M.pdf
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1.3 Alternatives for Control of Leaf-Cutting Ants
Several FSC certificate holders in Brazil are currently using or testing alternative methods for control
of leaf-cutting ants. Research institutions are developing alternatives. Development of alternatives is
best undertaken in collaboration with other certificate holders, scientific experts and PhD students at
universities, government agencies, and commercial enterprises. Funding is available from national
research programs and from international initiatives for sustainable development (ETFRN).58 Research
institutions and commercial companies are studying various alternatives for control of leaf-cutting ants.
In view of a possible prohibition, or restriction (more likely), of PFOS (precursor of sulfluramid) under
the Stockholm Convention, cost-effective alternative methods for ant control need to be developed.
Alternative chemicals which have been tested include organophosphates, carbamates, pyrethroids,
insect growth regulators (e.g. flufenoxuron), substances that inhibit reproduction (e.g. abamectin), and
other chemicals (such as hydramethylnon). It appears that in some cases, products labeled as „natural‟
were a fraud and had been adulterated with a synthetic insecticide. Several research groups are studying
the potential of plant extracts that are either directly toxic to ants or inhibit growth of symbiotic fungi.
Companies confirmed that they are committed to initiatives for developing/testing alternatives, support
experiments of research institutions financially, and provide technical teams and areas for field trials.
Ant control should be based on integrated pest management (IPM). To identify areas where ant control
is needed, a critical density of ant nests must be defined (maximum acceptable density for achieving
silvicultural objectives). Forest managers need to monitor nest density and damage regularly. Particular
attention may be warranted at the forest edge, in recently re-planted areas, and on sites with loose soil.
1.3.1 Combinations of Fungal / Bacterial Pathogens and Diatomaceous Earth
Pathogenic fungi have the potential to control leaf-cutting ants. In nests treated with Paecilomyces, a
pathogenic fungus, activity was significantly reduced (Varon Devia 2007).59 Beauveria bassiana and
Metarhizium anisopliae are pathogens of leaf-cutting ants. In lab tests on Atta sexdens, B. bassiana
infected a high proportion of workers (Diehl & Junqueira 2001).60 Mortality was lower in field tests
than in the laboratory. Defense of leaf-cutting ants (Acromyrmex species) against infection includes
hygiene, antibiotic secretion and immune system. Resistance to pathogenic fungi is based on genetic
diversity in a nest, and depends on the specific host-parasite interaction (Hughes & Boomsa 2004).61
58
59
60
61
EFTRN: EC funding for research in the tropics/subtropics. www.etfrn.org/ETFRN/resource/frames/linkfund.html
Varon Devia E.H. Distribution and foraging by the leaf-cutting ant, Atta cephalotus, in coffee plantations
with different types of management and landscape contexts, and alternatives to insecticides for its control
(Ph.D. thesis). CATIE 2007. http://orton.catie.ac.cr/REPDOC/A0976I/A0976I.PDF
Diehl E., and Junqeira L.K. Seasonal variations of metapleural secretion in the leaf-cutting ant Atta sexdens
piriventris (…), and lack of fungicide effect on Beauveria bassiana (…). Neotropical Entomology 30(4),
2001. http://www.scielo.br/pdf/ne/v30n4/a02v30n4.pdf
Busarello G.D. Avaliação da patogenicidade dos fungos entomopatogênicos Beauveria bassiana (…) e Metarhizium anisopliae (Metsch.) para o controle de Atta sexdens rubropilosa (…) em condições de laboratório,
UFGD 2008. http://www.ufgd.edu.br/fcba/mestrado-entomologia-conservacao-biodiversidade/dissertacoes-defendidas/
Hughes W.O.H., and Boomsma J.J. Diversity and disease resistance in leaf-cutting ant societies. Evolution
58(6): 1251-1260, 2004. http://www.jstor.org/stable/3449221
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In Atta sexdens rubripilosa, the fungus Metarhizium anisopliae caused significantly higher mortality
(64%) in combination with imidacloprid (Confidor®) due to increased susceptibility of ants (Santos et
al 2007).62 Combining pathogenic fungi with an insecticide such as fipronil or sulfluramid in baits may
enable reductions in the insecticide concentration (Forti et al 2007).63 The fungus Beauveria bassiana
appeared to be more effective for control of Acromyrmex species when it was directly applied to nests,
since attractiveness of baits varies seasonally (Diehl-Fleig & Silva 1994).64 In laboratory tests, Bacillus
thuringiensis isolated from Acromyrmex crassipinus and A. lundi caused 50-100% mortality (Pinto et al
2003).65 Other fungal ant pathogens include Enthomophthora, Hisurtella, Aschersonia and Nomuraea.
Metarhizium anisopliae, or M. anisopliae combined with Trichoderma viride, achieved 100% control
of Atta cephalotus in field tests; Trichoderma viride achieved 80% control (Lopez & Orduz 2003).66
Silva et al (2006) found that fungal pathogens Trichoderma harzianum and Escovopsis weberi inhibited
growth of symbiotic fungi by 75% and 68%, respectively.67 These findings show that using microbial
fungi is a possible strategy for control of leaf-cutting ants and merits further studies. The Instituto de
Pesquisas e Estudos Florestais will propose trials to evaluate the viability of this method.
Diatomaceous earth (terra diatomácea) caused 10.52% and 31.57% mortality in Atta sexdens rubropilosa seven days after application of 10 g/m2 and 50 g/m2, respectively (in powder formulation), while
sulfluramid caused 73.68% mortality (Ferreira Filho 2009).68 The author of this study concluded that
under field conditions diatomaceous earth did not control this ant species effectively. In another study,
when diatomaceous earth was combined with Thelohania solenopsae, a pathogenic fungus that infects
fire ants (Solenopsis species), mortality increased significantly (Brinkmann & Gardner 2001).69 More
field tests on diatomaceous earth are encouraged, especially in combination with a pathogenic fungus.
Such combinations could control ants effectively during periods of lower nest activity or in areas where
chemical control is no option or not desirable. Diatomaceous earth consists of fossilised diatoms and
62
63
Santos AV, et al. Selection of entomopathogenic fungi for use in combination with sub-lethal doses of
imidacloprid: perspectives for the control of the leaf-cutting ant Atta sexdens rubropilosa (…).
Mycopathologia 163: 233-240, 2007. http://www.springerlink.com/content/2hgm2q51025822l6/
Forti LC, et al. Dispersal of the delayed action insecticide sulfluramid in colonies of the leaf-cutting ant Atta
sexdens rubropilosa (Hymenoptera: Formicidae). Sociobiology 50(3), 2007.
http://www.fca.unesp.br/lisp/artigos/Dispersal%20Of%20the%20Delayed%20Action%20Insecticide%20Sulfluramid%2007.pdf
64
65
66
67
68
Diehl-Fleig E., and da Silva ME. Beauveria bassiana para controle das formigas cortadeiras do gênero
Acromyrmex. Piracicaba, IPEF 1994. http://www.ipef.br/publicacoes/curso_formigas_cortadeiras/cap02.pdf
Pinto L.M.N., et al. Pathogenicity of Bacillus thuringiensis isolated from two species of Acromyrmex (…).
Brazilian Journal of Biology 63(2): 301-306, 2003. http://www.scielo.br/pdf/bjb/v63n2/a15v63n2.pdf
Lopez E., and Orduz S. Metarhizium anisopliae and Trichoderma viride for control of nests of the fungusgrowing ant, Atta cephalotes. Biological Control 27(2), 2003. http://dx.doi.org/10.1016/S1049-9644(03)00005-7
Silva A., et al. Susceptibility of the ant-cultivated fungus Leucoagaricus gongylophorus (…) towards
microfungi. Mycopathologia 162(2): 115-119, 2006. http://www.springerlink.com/content/21p71w7135710k60/
Ferreiro Filho P.J. Eficiência da terra diatomácea no controle de formigas cortadeiras em florestas de
eucalipto. 13ª Reunião Técnica Programa de Proteçáo Florestal PROTEF, Bahia 2009.
http://www.ipef.br/eventos/2009/rtprotef13/RTProtef-Palestra_12.pdf
69
Brinkmann et al. Use of diatomaceous earth and entomopathogen combinations against the red fire imported
fire ant (...). Florida Entomologist 84(1): p. 740, 2001. http://www.fcla.edu/FlaEnt/fe84p740.pdf
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the main constituent is particulate silica (silicon dioxide). Purified forms contain up to 94% silica (these
can be identified by their CAS number, no. 61790-53-2). Diatomaceous earth has strong physi-sorptive
properties and absorbs lipids from the cuticle of arthropods, thereby desiccating the organism. It kills
arthropods also when ingested. A commercial product Perma-Guard Diatomaceous Earth® is registered
in the US for control of fire ants, grasshoppers, crickets and cockroaches. Diatomaceous earth is nontoxic and poses no risk to birds and mammals (it is applied directly onto animals against ectoparasites).
Diatomaceous earth can be classified as „harmless‟ according to criteria established by the European
Union if it contains less than 0.1% of particles of fine crystalline silica (with a diameter below 50 um)
(EC 2008).70 Diatomaceous earth is commercially registered for control of ants, crickets, cockroaches,
beetles and other insects (HTL 2006).71 In Brazil, diatomaceous earth is registered for use on insects in
rice, cereals and corn (Anvisa 2009; Bequisa 2009).72 Combinations of certain pathogenic fungi and
diatomaceous earth are possible alternatives for control of leaf-cutting ants with minimal or no toxicity.
1.3.2 Botanical Insecticides, Anti-fungal Agents, and Pheromones
Botanical insecticides are natural products derived from plants. Extracts of powdered sesame leaves
controlled lemon leafcutter ants (Atta sexdens rubropilosa) satisfactorily after 90 days, mortality was
>75% (Peres Filho & Dorval 2003).73 The authors encouraged more tests on the potential of sesame
powder for ant control. Extracts of Ateleia glazioviana („Timbó‟, marketed as Citromax®) controlled
Acromyrmex lundi very effectively, resulting in 95% mortality after 20 days (Cantarelli et al 2005).74
Extracts from the following plants were toxic to leaf-cutting ants or inhibited the symbiotic fungus:
Ateleia glazioviana / Timbó, Canavalia ensiformis, Centrosem brasilianum, Citrus sinensis, Helietta
puberula, Hymenaea courbaril / Jatoba, Ipomea batata, Manihot esculenta / manipueira, Myroxylon
peruiferum / cabreúva, Pilocarpus grandiflorus, Piper cenocladum, Raulinoa echinata, Ricinus
communis, and Sesamum indicum.75 E.g. manipueira is approved for ant control and is toxic to various
70
71
72
“The overall conclusion (…) it may be expected that kieselgur (diatomaceous earth) does not have any
harmful effects on human or animal health or on groundwater or any unacceptable influence on the
environment” (EC 2008). Source: European Commission (EC). Review report for the active substance
kieselgur (diatomaceous earth). Brussels, 2008. http://ec.europa.eu/food/plant/protection/evaluation/existactive/listkieselgur_en.pdf (Criteria for evaluation of kieselgur are defined in: European Commission (2007): Regulation
1095/2007/EC. http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2007:246:0019:0028:EN:PDF )
Headley Technologies Ltd. (HTL): MSDS: Insecolo®. 2002. http://www.hedleytech.com/msdsinsecolo.pdf;
(HTL 2006): http://pr-rp.pmra-arla.gc.ca/PR_SOL/pr_web.ve1?p_ukid=6946
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®. 2009. http://www.bequisa.com.br/produtos/?idLinha=1
73
74
75
Peres Filho O., and Dorval A. Effect of granulated formulations composed by chemical products and leaves
and seeds of sesame, Sesamum indicum, to control nests of Atta sexdens rubropilosa (…). Ciência Florestal
13(2): p. 6770, 2003. http://redalyc.uaemex.mx/redalyc/pdf/534/53413208.pdf
Cantarelli E.B., et al. Efeito de diferentes doses do formicida “Citromax” no controle de Acromyrmex lundi
(…). Ciência Florestal 15(3): 249-253, 2005. http://www.ufsm.br/cienciaflorestal/artigos/v15n3/A4V15N3.pdf
Carvalho T.A., et al. Atividade inseticida de Myroxylon peruiferum (cabreúva) frente às formigas cortadeiras
Atta sexdens (…). Anais de Eventos da UFSCar 4, 2008. http://ict2008.nit.ufscar.br/cic/uploads/C48/C48-001.pdf
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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,
76
77
77
78
79
Cazal C.M., et al. Isolation of xanthyletin, an inhibitor of ants‟ symbiotic fungus, by high-speed countercurrent chromatography, J. of Chromatography A 1216(19), 2009 http://dx.doi.org/10.1016/j.chroma.2009.02.066
Magalhães C.P., et al. Biochemical basis of the toxicity of manipueira (…) to nematodes and insects. Phytochemical 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/destaque2/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
mandioca. 2007. http://www.infobibos.com/Artigos/2007_4/manipueira/index.htm
Biavatti M.V., et al. Leaf-cutting ants toxicity of limonexic acid and degraded limonoids from Raulinoa
echinata (…). J. of the Brazil. Chemical Society 16(6b), 2005. http://www.scielo.br/pdf/jbchs/v16n6b/27348.pdf
Jackson C. Evolutionary aspects of ant-fungus interactions in leaf-cutting ants (research project). Ecological
Entomology, University of Southampton UK. http://www.sbs.soton.ac.uk/staff/cwj/cwj.php
Bigi MF, et al. Activity of Ricinus communis (Euphorbiaceae) and ricinine against the leaf-cutting ant Atta
sexdens rubropilosa (…) and the symbiotic fungus Leucoagaricus gongylophorus. Pest Management Science
60(9), 933-938, 2004. http://www3.interscience.wiley.com/cgi-bin/abstract/108561072/ABSTRACT?CRETRY=1&SRETRY=0
Marinho et al. Beta-eudesmol induced aggression in the leaf cutting ant Atta sexdens rubropilosa. Entomologia Experimentalis et Applicata 117(1), 2005. http://www3.interscience.wiley.com/journal/118684988/abstract,
http://esa.confex.com/esa/viewHandout.cgi?uploadid=140 (handout)
80
81
82
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
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
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
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beetles, flies, and other ants. Army ants (Nomamyrmex species) prey on young nests of Atta (Powell &
Clark 2004; Swartz 1998).83 Mass rearing of Canthon virens, a beetle that preys on young ant queens,
had limited success so far.
Certain phorid flies parasitise on Atta species. Phorid flies mostly prey on ant workers. But a phorid
parasitoid which preys on the reproductive caste could contribute to ant control (Bragança 2007).84
Combining a parasitic nematode (Steinernema carpocapsae) and insecticides (imidacloprid) increased
infectivity (Negrisoli 2005).85
1.3.4 Alternative Insecticides for Ant Control
Abamectin (or avermectin B1) has been tested on leaf-cutting ants. It is a fermentation product of a
soil bacterium and acts as an insecticide with contact and stomach action. Abamectin has been used to
control the queens of leaf-cutting ants Acromyrmex subterraneus. Porous paper impregnated with a
liquid solution of abamectin is applied. In colonies where queens were exposed to a 5% solution (50
mg abamectin per ml), foraging and leaf consumption were reduced and after 11 weeks colonies were
suppressed. Abamectin impaired the reproduction of ant queens (Antunes et al 2000).86 Abamectin is
degraded by light. Methods must be improved to deliver it effectively to ant queens. Due to high acute
toxicity (based on LD50 value), abamectin qualifies as „highly hazardous‟ pesticide under FSC criteria.
But most formulated products containing abamectin are of low toxicity to mammals (OSU 1994).87
Borax, an inorganic insecticide, controlled leaf-cutting ants (Atta cephalotes) more effectively than
sulfluramid in coffee plantations. Borax (disodium octaborate) caused the highest colony mortality
(four weeks with no activity, or 100%), while sulfluramid achieved 80% control (Varon Devia 2007).88
83
Powell S., and Clark E. Combat between large derived societies: A subterranean army ant established as a
predator of mature leaf-cutting ant colonies. Insectes Sociaux 51: 342–351, 2004.
http://www.springerlink.com/content/tg4a5cnk6ehf6l2x/
Swartz M.B. Predation on an Atta cephalotes colony by an army ant, Nomamyrmex esenbeckii. Biotropica 30(4): 682684, 1998., http://www3.interscience.wiley.com/journal/119102866/abstract
84
85
86
87
88
Bragança M.A.L. Perspectiva da contibuição de forídeos parasitóides no manejo de formigas cortadeiras.
Revista O Biológico 69(supl. 2), 2007. http://www.biologico.sp.gov.br/docs/bio/suplementos/v69_supl_2/p177-181.pdf
Negrisoli A.S. Jr. Avaliação de técnicas para estudo de compatibilidade de produtos fitossanitários com
nemtóides entomopatogênicos (…). M.Sc., UFLA. 2005. http://docentes.esalq.usp.br/sbn/ajuda/aldomario.pdf
Antunes E.C., Guedes R.N.C., Della Lucia T.M.C., and Serrão J.E. Sub-lethal effects of abamectin
suppressing colonies of the leaf-cutting ant Acromyrmex subterraneus subterraneus. Pest Management
Science 56(12), 1059-1064, 2000. http://www3.interscience.wiley.com/journal/75505141/abstract
Ohio State University (OSU). Extension Toxicology Network. Pesticide Information Profile: Abamectin.
New York 1994, http://pmep.cce.cornell.edu/profiles/extoxnet/24d-captan/abamectin-ext.html
Varon Devia E.H. Distribution and foraging by the leafcutting ant, Atta cephalotus, in coffee plantations with
different types of management and landscape contexts, and alternatives to insecticides for its control (Ph.D.
thesis). CATIE 2007. http://orton.catie.ac.cr/REPDOC/A0976I/A0976I.PDF
ANVISA: Relatório do Ingrediente Ativo: Produtos Formulados (Agrotóxicos):
– Bórax decahidratado. http://www4.anvisa.gov.br/AGROSIA/asp/frm_dados_ingrediente.asp?iVarAux=1&CodIng=558
– Octaborato dissódico. http://www4.anvisa.gov.br/AGROSIA/asp/frm_dados_ingrediente.asp?iVarAux=1&CodIng=1770
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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 Leafcutting 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
90
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
Science 80: 9-13, 2007. http://dx.doi.org/10.1007/s10340-006-0143-8
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
92
93
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
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
Fang N., and Casida J.E. Cubé resin insecticide: Identification and biological activity of 29 rotenoid constituents. 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
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Spinosad (spinosyn A) is derived from fermentation products of a soil microorganisam (actinomycete).
Spinosad is effective mainly by ingestion and to some extent by contact. Spinosad or other spinosyns
are active against Lepidoptera, Thysanoptera, Coleoptera, Isoptera, Hymenoptera, or other insect orders
(Salgado & Sparks 2005).94 Baits based on spinosad could be developed for ant control. Tests in the
laboratory and field are strongly encouraged. Spinsoad has a relatively low toxicity against beneficial
insects, especially predatory insects. It has a high level of selectivity for insect control. Toxixity of
spinosad to mammals, birds and aquatic species is relatively low when compared to other insecticides.
1.3.5 Mechanical / Cultural Control and Integrated Management of Leaf-cutting Ants
Mechanical control (ploughing or harrowing) partially destroys new nests of leaf-cutting ants. Since
minimum cultivation or no-tillage was introduced, conventional site cultivation is practiced less often.
Direct destruction of nests is limited to smaller areas and new nests of Atta species (up to four months
old). Mechanical control is more effective for controlling Acromyrmex as nests of this species are less
deep (Angels et al 1998).
Cultural control includes leaving understory vegetation which makes it more difficult for ant queens
to establish new nests. A vegetation cover helps to promote natural enemies of leaf-cutting ants. Trees
can be interplanted with plants that are toxic to ants. The deterrent effect of sesame (Sesamum Indicum)
was limited. Another strategy is to grow trap plants that divert ants from crop trees (Khan et al 2008).94
Various physical obstacles can prevent access of ants to trees, for example water (in containers around
seedling stems or in ditches). However, physical obstacles are viable only on small areas.
Integrated management of leaf-cutting ants
The FSC encourages integrated pest management (IPM). This entails that forest managers identify and
quantify pest problems. Monitoring pest organisms is a fundamental element of IPM (Wilcken 2008).95
Other elements of IPM are to consider the control options, most suitable type/s of remedial action, and
(if chemical control is selected) the most appropriate pesticide and method of application (accounting
for the risks). Integrated management of leaf-cutting ants requires that forest managers identify which
ant species cause major damage, and estimate how abundant these species are. A quantitative threshold
should be defined for damage (maximum acceptable losses of trees) and critical nest density (maximum
number of nests per hectare enabling silvicultural objectives to be met). This is essential for deciding if
ants need to be controlled, based on results of monitoring.
To locate areas where critical density of nests is exceeded, ant nests need to be monitored in managed
areas. Critical density depends on the forest age: it is lower for young forests as young trees are more
94
94
Salgado V.L., and Sparks T.C. The spinosyns: chemistry, biochemistry, modes of action, and resistance. In:
Gilbert L.I., et al. Comprehensive molecular insect science: Control. Vol. 6, pp. 137-173. Amsterdam 2005
Khan Z.R., et al. Chemical ecology and conservation biological control. Biological Control 45(2): 210-224,
2008. http://dx.doi.org/10.1016/j.biocontrol.2007.11.009
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vulnerable. Damage of trees caused by ants should be surveyed regularly, and defining a critical level
for tree damage may be helpful. Several alternative methods are available to control leaf-cutting ants.
Selected method/s should suit the local conditions, including ecological, climatic, silvicultural, and
economic factors (Laranjeiro & Louzada 2000).95
In integrated pest management, insecticides are only used when these cannot be avoided, the chemical/s
with the lowest hazard is selected, and the amount is limited to the minimum. Chemicals are generally
complemented with other methods of control, biological agents and preventive practices. To promote
natural enemies that prey on ants, plantations should be designed to maintain diversity of species and
habitat, structural complexity and ecosystem functionality, by restoring or conserving natural forests on
part of managed areas – „appropriate to the scale and intensity of the management activities and the risk
of negative impacts‟ (PyC del FSC, principio 6.2).11 For example, providing zones with native vegetation
around plantations (reforested areas) led to a reduction in the number of ant nests (Zanetti 2000).
Preventive silvicultural practices
Many pest problems – caused both by pest insects and weeds – are a direct consequence of intensive
management practices (relying on fast-growing exotic species in even-aged monocultures and clearcuts). Intensive forest management may exacerbate a previously localised pest problem. Clear-cutting
creates large areas of open spaces which leaf-cutting ants (Atta cephalotes) colonize (Jaffe & Vilela
1989).27 Nests of Acromyrmex and Atta species increased in number after clear-cuts (Vasconcelos &
Cherrett 1995).28
To reduce negative impacts on the diversity of habitats and species (including natural enemies of pest
organisms), companies should reduce the extent of clear-cutting. Less intensive harvest methods
prevent weed growth, thereby reducing or eliminating the need for herbicides, and can result in a lower
incidence of pest insects such as bark beetles. Preventive harvesting practices include, e.g., shelterwood
and mosaic cuts, sequential harvesting in continuous cover or closed canopy forestry (with unevenaged stands), and retention harvests (leaving individual shade/seed trees, or tree groups). In the long
term, these harvest methods and strip clear-cutting (Ocaña-Vidal 1992) or selective extraction of
groups (Bava & Bernal 2005) are more sustainable (adaptable to changing conditions) than clear-cuts.96
95
Laranjeiro A.J., and Louzada R.M. Manejo de formigas cortadeiras em florestas. Série Técnica IPEF 13(33):
115-124, 2000. http://www.ipef.br/publicacoes/stecnica/nr33/cap13.pdf
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.
http://www.fao.org/docrep/u6010e/u6010e06.htm#natural%20forest%20management%20with%20strip%20clear%20cutting
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Publications on integrated management of leaf-cutting ants / alternative control methods
Almeida A.F. Disseminando práticas de manejo ecológico de formigas cortadeiras no Sul da Bahia. Revista
Agriculturas 5(1), 2008. http://agriculturas.leisa.info/index.php?url=getblob.php&o_id=206560&a_id=211&a_seq=0
Cantarelli E.B., et al. Plano de amostragem de Acromyrmex spp. (Hymenoptera: Formicidae) em áreas de
pré-plantio de Pinus spp. Ciência Rural 36(2), 2006. http://www.scielo.br/pdf/cr/v36n2/a05v36n2.pdf
Nickele M.A. Ditribuição espacial, danos e planos de amostragem de Acromyrmex crassispinus (…). UFPR
2008. http://dspace.c3sl.ufpr.br:8080/dspace/bitstream/1884/16942/1/Disserta%C3%A7%C3%A3o%20Mariane%20A.%20Nickele.pdf
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
SBRT. Formigas cortadeiras. 2006. http://sbrtv1.ibict.br/upload/sbrt2647.pdf?PHPSESSID=6aa56910df57f5c60f1bee9de0deeaf0
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.
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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
In secondary forest, estimated herbivory rate of leaf-cutting ants Atta laevigata ranged from 5.7% (3%)
to 13%, and ants preferred young leaves (Vasconcelos 1999).97 Development of Pinus taeda trees cut
by ants in the first two years was significantly reduced (Cantarelli et al 2008).98 Control of ants should
focus on nurseries (viveiros) and areas with freshly planted tree seedlings or young trees, particularly in
the first 1-2 years after establishment. In older/mature trees, various types of herbivores generally tend
to prefer pioneer tree species. Preventive silvicultural practices include sowing a cover crop, planting
robust tree species that are well-adapted to local conditions, and limiting the extent of clear-felling.
Certificate holders are encouraged to cooperate with other forest companies and research institutions
(e.g. IPEF, Embrapa, etc) in developing a common initiative (plan) for the integrated management of
leaf-cutting ants. This could consist of recommended (or mandatory) procedures for monitoring ant
nests and/or tree damage, basic methods for identifying areas where critical nest density is exceeded (or
defining maximum acceptable damage), and criteria for selecting effective and environment-friendly
methods that are appropriate to local/regional conditions.
1.4 Stakeholder Opinions on Insecticide Use
1.4.1 Consultation of Stakeholders
Certificate holders consulted stakeholders at the national and regional scale. The Instituto de Pesquisa e
Estudos Florestais (Forestry Science Research Institute) posted derogation applications and a request
for comments online in September and November 2007 (IPEF 2007).99 This consultation addressed all
FSC certified companies and candidate companies. In addition, Imaflora posted derogation applications
on its website (Imaflora 2007).100 Very many stakeholders were contacted by letter or email. Copies of
original stakeholder comments (in print) were sent to FSC International. Imaflora compiled a sample of
stakeholders contacted by IPEF, and a sample of stakeholders contacted by FSC certificate holders.101
Consulted national stakeholders include the Ministry of Agriculture (MAPA), Ministry of Environment
(MME), Institute of Environment and Renewable Natural Resources (IBAMA), non-governmental
organizations (Associação Brasileira de Organizações Não-Governamentais - Abong / Brazilian
Association of NGOs, Greenpeace Brazil, SOS Mata Atlântica, WWF Brazil), Brazilian universities,
97
98
99
100
101
Vasconcelos H.L. Levels of leaf herbivory in Amazonian trees from different stages in forest regeration. Acta
Amazonica 29(4): 615-623, 1999. http://acta.inpa.gov.br/fasciculos/29-4/PDF/v29n4a12.pdf
Cantarelli E.B., et al. Quantificação das perdas no desenvolvivenmento de Pinus taeda após e ataque das
formigas cortadeiras. Ciência Florestal 18(1), 2008. http://redalyc.uaemex.mx/redalyc/pdf/534/53418104.pdf
Instituto de Pesquisa e Estudos Florestais (IPEF). Consulta Pública (website dated December 3, 2007,
accessed via Internet Archive). http://web.archive.org/web/20071111193247/www.ipef.br/pccf/consultapublica.asp
Imaflora. Consulta Pública. 2007. http://ww2.imaflora.org/index.cfm?fuseaction=content&IDassunto=4&IDsubAssunto=53
Sample of Stakeholders consulted by PCCF [Programa Cooperativo em Certificação Florestal] during the
Brazilian derogation process (2007). Document entitled: „Cosulted_stakeholders_Brazil_PCCF‟
Sample of Stakeholders consulted by EMF [Empreendimento de Manejo Florestal / Forest Management
Company] during the Brazilian derogation process (2007). Document: „Cosulted_stakeholders_Brazil_EMF‟
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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
research institutions (Brazilian Agricultural Research Corporation - Embrapa), associations of forest
plantations (Associação Brasileira de Produtores de Florestas Plantadas - Abraflor, Minas Gerais Silviculture 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 Opinion on derogation for ‘highly hazardous’ insecticide
Number contacted / Number of responses
Supportive / Non-supportive
alpha-Cypermethrin, liquid
(Fendona):
Deltamethrin, liquid (Decis):
950 / 944
3197 / 2968
931 / 13 (non-supportive A: 33%, B: 13%, C: 13%, D: 40%)
2900 / 68 (non-supportive A: 65%, B: 14%, C: 14%, D: 6%)
Deltamethrin, dust (K-Othrin): 2507 / 2240
2157 / 83 (non-supportive A: 72%, B: 7%, C: 8%, D: 12%)
Fipronil, dispersible granules
(Tuit Forest):
2916 / 62 (non-supportive A: 77%, B: 12%, C: 4%, D: 8%)
3462 / 2978
Fipronil, granular baits (Blitz): 1622 / 1414
1356 / 58 (non-supportive A: 72%, B: 9%, C: 14%, D: 5%)
Fenitrothion, liquid (Sumifog): 1838 / 1598
1563 / 35 (non-supportive A: 82%, B: 9%, C: 7%, D: 2%)
Sulfluramid, granular baits:
3395 / 52 (A: 71%
3839 / 3447
B: 7% C: 17% D: 5%)
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 prohibited 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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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
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
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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
1.5 Conclusions – Control of Leaf-Cutting Ants
1. Leaf-cutting ants – Atta / Acromyrmex species in particular – pose a problem in exotic plantations,
particularly during establishment. The level of infestation with ants and damage caused by herbivory
varies with tree species, tree age, site conditions, and silvicultural practices such as clear-felling. At
present, cost-effective non-chemical alternatives for control of leaf-cutting ants appear to be lacking.
However, complete control of ant nests in forests would probably cause new problems as these ants
perform important functions in the forest. Ants recycle nutrients in soil, aerate soil, and distribute
plant seeds. It is advisable to limit ant control to areas with unacceptably high densities of ant nests.
2. Based on acute toxixity, alphacypermethrin, deltamethrin, fenitrothion and fipronil are more toxic
(WHO class II „Moderately hazardous‟) than sulfluramid (WHO class III, „Slightly hazardous‟). But
sulfluramid and its primary metabolite perfluorooctane sulfonamide (PFOA or DESFA) are highly
persistent, have a (moderate) potential for bioaccumulation, and are moderately toxic to mammals,
or highly toxic to birds. PFOS, the main metabolite of sulfluramid, accumulates in mammals and is
toxic (US EPA 2001). In the long term, use of sulfluramid on a large-scale may present a risk to
mammals, birds, amphibians, and reptiles.
3. The aim should be to discontinue use of sulfluramide within five years. While sulfluramide is used,
it should be applied in bait dispensers (porta-iscas) or sachets (mipis), especially in sensitive areas.
Certificate holders applying sulfluramid baits directly (without dispensers/sachets) on the majority
of areas should provide evidence that this is necessary in audit reports to the certification body. Use
of baits must be limited to the minimum recommended dose. It is recommended to define reduction
targets (% reduction in amount (kg) of sulfluramide active ingredient used), e.g. −20% per year.
4. Certificate holders in Brazil consulted a very large number of stakeholders, both on a national and
regional scale. Between 944 and 3447 stakeholders responded and commented on the derogation
application/s for one or more „highly hazardous‟ insecticides. Between 13 and 83 stakeholders did
not support a derogation. Non-supportive responses ranged from 1.5% for sulfluramid to 4.3% for
fipronil in south Brazil. Organizations promoting sustainable production oppose use of sulfluramid.
Experts on public health concluded that sulfluramid should be replaced (Porto & Milanez 2009).49
The Ministry of Environment thinks that sulfluramid can gradually be substituted with alternatives.
5. Pathogenic fungi combined with B.t., diacetomaceous earth, plant extracts that are toxic to ants, or
anti-fungal agents (plant extracts or fungi which inhibit symbiotic fungi) may control leaf-cutting
ants more effectively. Combinations merit further studies. Pathogenic fungi can be combined with
spinosad, borax, rotenone, an insect growth regulator (chitin synthesis inhibitor), or imidacloprid.
Integrated pest management of leaf-cutting ants involves identifying which ant species causes most
damage, defining a critical nest density (maximum density for achieving silvicultural objectives),
monitoring nests, identifying areas with a critical nest density, and selecting ideal control method/s.
6. Certificate holders in Argentina and Brazil are using or testing alternatives for ant control. Some
also support studies at research institutions financially, and/or provide technical teams or areas for
field tests. The development of alternatives is best undertaken in collaboration with other certificate
holders, scientific experts and PhD students at universities, government agencies, and commercial
enterprises. Several universities and commercial enterprises are studying alternatives for ant control.
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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
7. A common initiative/plan for integrated management of leaf-cutting ants could include voluntary or
mandatory standards for monitoring ant nests and damage, identification of areas with critical nest
densities or unacceptably high damage levels, and selection of effective and environment-friendly
control methods appropriate for site conditions. Certificate holders are recommended to cooperate
with other companies and scientific experts (at universities) in developing IPM based ant control.
An initiative for integrated management of ants could include forest companies in Brasil who are not
FSC certified. E.g. national or regional forestry associations (Abraflor, AMS, SBS) might participate
in a national/regional initiative for integrated ant management.
II. Costalimaita ferruginea and other Coleopteran Defoliating Insects
2.1 Need for Deltamethrin and alpha-Cypermethrin to Control Costalimaita ferruginea and
other Coleopteran Defoliating Insects
The yellow beetle Costalimeita ferruginea damages young eucalyptus seedlings immediately after
planting (during the first month). The beetle causes holes in the leaves and feeds on the inner bark.
Defoliation at an early stage can proceed to complete loss of leaves. Most damage occurs during the
first 12 months in newly established plantations. Severe attacks can cause up to 50 % tree mortality.
Defoliage of over 75% can cause reductions in wood volume of 35.4% at the age of 12 months, or 28.5
% at 24 months (Mendes 1999).105 Attack at the age of 7 months increased mortality by 1.8-3.7 times at
harvest age (7 years). In E. grandis seedlings attacked by Costalimaita, the estimated mortality of trees
at 7 years age ranged from 6.4% to 13.1%, depending on the damage level in crown or tips (Pineaar &
Schiver 1981). Certificate holders state that insecticide use is the only way to protect eucalypt seedlings
at planting, as natural enemies (such as Trichogramma or parasitic wasp Anaphes nitens) do not control
Costalimaita effectively, due to its rapid appearance and short duration of attack. Similarly, pathogenic
fungi had limited effectiveness for controlling this beetle so far. Larvae develop in nearby fields of
sugarcane or pasture land, feeding on plant roots which adult beetles do not attack.
Certificate holders intend to use the following two pyrethroid insecticides for control of coleopteran
defoliators:
·Fendona 60 SC (liquid formulation): contains 6% alpha-cypermethrin (active ingredient)
Safety Data: Fendona 60 SC (Basf). http://www.basf.cl/asp-local/agro_prod_fichaweb.asp?prod_id=86
·Decis CE (liquid formulation): contains 2.5% deltamethrin (active ingredient)
Safety Data: Decis 25 CE (Bayer). http://www.bayercropscience.com.br/produtos/downloads/Decis25CE-REFL.pdf
105
Mendes J.E.P. Nível de dano e impacto do desfolhamento por Costalimaita ferruginea (…) em Eucalyptus
grandis Hill ex Maiden. Tese M.Sc., Universidade Federal de Viçosa, 1999
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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
From 43 certificate holders, 19 (or 44%) applied for a derogation for deltamethrin (liquid formulation)
to control coleopteran or lepidopteran defoliating insects. From 21 companies who provided additional
detailed information on the area affected by defoliators over the last three years, nine were affected by
Costalimaita ferruginea. Damage levels varied enormously between nurseries and young plantations.
In a large nursery, the % infested area of managed forests was 63.6% and the area where Costalimaita
was controlled amounted to 13'466.2 ha. In plantations, the % infested area ranged from 0.1% to 4.5%
(averaging 1.8%), the area where Costalimaita was controlled ranged from 184.6 ha to 3035.4 ha. From
9 companies with affected areas, only 3 companies used a chemical insecticide (deltamethrin or alphacypermethrin) to control Costalimaita. Other coleopteran defoliators were not controlled (see table 5).
Table 5. Control of Defoliating Insects in Eucalypt Plantations in Brazil
Lepidopteran / coleopteran defoliating insect species
Common
Latin name
Order: family
name
Adeloneivaia
lagarta-daLepidoptera:
subangulata
acacia
Saturniidae
lagarta enrola- Lepidoptera:
Bonagota cronaodes
deira da maçã
Tortricidae
Coleoptera:
Colaspis species
Chrysomelidae
Control with
active ingredient
deltamethrin
deltamethrin
Area treated 2006; 2007;
2008 (certificate no.)
283; 182.6; 782.5 ha
(SGS-1664)
17; 17; 17 ha (nursery)
(SGS-4161)
not controlled
α-cypermethrin
3035.4; 0; 0 ha (SGS1943)
300; 500; 0 ha (SCS-85P)
89; 58.7; 159.8 ha (SGS2167)
0.4; 1.5; 0.3 ha (SCS-40P)
13466.2; 13466.2; 13466.2
ha (nursery) (SCS-93P)
Costalimaita
ferruginea
besouroamarelo /
yellow beetle
Coleoptera:
Chrysomelidae
Eupseudosoma
aberrans, E. involuta
lagartacachorrhinho
Lepidoptera:
Arctiidae
not controlled
Euselasia apisaon
lagartaeuselasia
Lepidoptera:
Riodinidade
not controlled
Lepidoptera:
Notodontidae
not controlled
Glena bipennaria
Glena unipennaria
Lampetis
drummondi
besouro cai-cai
Melanolophia sp.
Metaxyonycha
angustata
Nystalea nyseus
March 2010
besouro
quarto-pintas
Coleoptera:
Buprestidae
Lepidoptera:
Geometridae
Coleoptera:
Chrysomelidae
Lepidoptera:
Notodontidae
deltamethrin
not controlled
B. thuringiensis
0; 0; 120 ha (SCS-76P)
not controlled
not controlled
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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
Psorocampa
denticulata
Sarsina violascens
cariposaviolácea
Sternocolaspis
quatuordecimcostata
Thyrinteina arnobia
lagarta-parda
do eucalipto /
eucalyptus
brown looper
Lepidoptera:
Lymantriidae
not controlled
Coleoptera:
Chrysomelidae
not controlled
Coleoptera:
Chrysomelidae
not controlled
Lepidoptera:
Geometridae
857.6; 4643.5; 0 ha (SGS1943)
0; 0; 11 ha (SCS-76P)
18.5; 0; 1780.5 (SCS-77P)
857.6; 4643.5; 0 ha (SGS1943)
251; 0; 7191.2 ha (SCS77P)
deltamethrin
B.thuring 0.5 l/ha +
α-cyperm 0.15 l/ha
B. thuringiensis
Costalimaita ferruginea, other beetles
T. arnobia
Melanolophia sp.
besouroamarelo
lagarta-parda
Coleoptera:
Chrysomelidae
Lepidoptera:
Geometridae
deltamethrin
184.6; 562.3; 484.5 ha
(SCS-57P)
2.2 Need for Deltamethrin and alpha-Cypermethrin to Control Costalimaita ferruginea and
other Coleopteran Defoliators – Position of Technical Advisors
Possible levels of damage in eucalypts caused by the yellow beetle Costalimaita ferruginea (or some
other coleopteran defoliators) seem to be more significant than damage from lepidopteran species. In
particular, losses were substantial in nurseries (viveiros). However, regular (annual) applications of a
pyrethroid (e.g. alpha-cypermethrin or deltamethrin) for controlling Costalimaita may be detrimental.
Information on estimated mortality of seedlings attacked by Costalimaita, depending on the damage,
was provided (Pineaar & Schiver 1981). But certificate holders did not include information on actual
levels of damage (type and severity) caused by Costalimaita. Thus actual losses cannot be estimated.
Depending on level of damage, 3-6% affected seedlings is the acceptable maxiumum (or less than 1%
if over 3/4 of the crown is damaged). Based on analysis of damage, it appears that plantations growing
wood for several purposes (multiprodutos de madeira) are protected from losses caused by defoliators
(Mendes 2004).106 But monitoring and recording attacks of defoliators in young eucalpyt plantations is
necessary to prevent damages and support forest management planning for integrated pest control.
Anjos and Majer (2003) recommended monitoring larvae of Costalimaita ferruginea periodically. In
almost 50% of cases when Costalimaita occurred in eucalypts, forest managers conducted chemical
control. The authors say that this proportion can be reduced to 10% if the beetle larvae are monitored,
and that insecticide use must be “limited to very intense infestations, new plantations, and where it is
106
Mendes J.E.P. Efeitos do ataque de Costalimaita ferruginea (…) sobre crescimento e produção de Eucalyptus
grandis Hill ex Maiden Tese de Doutorado, UFV 2004. ftp://ftp.bbt.ufv.br/teses/entomologia/2004/179924f.pdf
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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
justifiable, as as an economic, ecological, and social strategy” (Anjos & Majer 2003).107 Insecticides
kill the limited number of natural enemies, thereby enhancing numbers of pest insects. This can
necessitate another insecticide application if the first application was too early. Chemical control, if
conducted on a large scale or „routine‟ basis, is likely to exacerbate problems caused by Costalimaita in
the long term.
Besides being non-selective, regular use of pyrethroids increases the risk of resistance in pest insects.
Continued annual use in nurseries (viveiros), where Costamilaita causes particularly large damage, is
likely to result in reduced effectiveness of control with time. If the amount of insecticide is increased
further this may promote the development of tolerance or resistance in the targeted insect. In this case
the insecticide will be less effective for control of possible outbreaks (sudden, sporadic infestations).
In the large majority of plantations affected by Costalimaita, the proportion of infested areas was not
high enough to warrant chemical control. An exception to this is a large seedling nursery (viveiro). It
appears that Costalimaita is controlled annually on the whole area (13'466 ha) of the nursery. However,
„routine‟ use of acutely toxic, non-selective insecticides such as alpha-cypermethrin or deltamethrin is
not compatible with principles of integrated pest management (IPM). The FSC encourages certificate
holders to adopt IPM practices. In IPM, it is essential to monitor the occurrence of a pest organism and
levels of damage (FSC 2009).108 It appears that in this nursery this has not been done. Clearly, there is a
greater need for control of leaf-eating beetles (Chrysomelidae), including Costalimaita ferruginea, in
nurseries than in forest plantations due to preferences of beetles and greater susceptibility of seedlings.
However, it is not clear if control is needed on a regular (annual) basis as defoliator populations vary
strongly from year to year. No estimates of actual (recent) losses were provided. Anjos & Majer (2003)
pointed out that all plantations need to monitor leaf-eating beetles, and this will apply to nurseries also.
Less hazardous chemical alternatives are available for controlling lepidopteran defoliators, in particular
spinosad. Although it appears that this selective, low-toxicity insecticide is currently not registered in
Brazil, it could be used on the basis of a temporary special registration (RET). Spinsosad is registered
in many countries worldwide and effective against various lepidopteran and coleopteran insects. Other
chemical alternatives for control are insect growth regulators, e.g. flufenoxuron, teflubenzuron, etc.
These are far less hazardous to non-target species than pyrethroids. Due to high octanol-water partition
coefficients they qualify as „highly hazardous‟ under FSC criteria; their use would require a derogation.
Non-chemical alternatives for management of Costalimaita include monitoring, silvicultural practices
(leaving old tree stumps with sprouts as „traps‟, trap crops diverting beetles, reduced weed control), use
of biopesticides (combinations of B. thuringiensis and Beauveria bassiana, or a nucleopolyhedrovirus
NPV specific to coleopteran insects), and growing robust eucalypt species which are more tolerant to
beetles.
107
108
Anjos N., and Majer J.D. Leaf-eating beetles in Brazilian eucalypt plantations. School of Environmental
Biology Bull. 23, 2003. http://www.insecta.ufv.br/norivaldo/popups/projetos/abstract-leaf-eating-beetles-brazilian-eucalypt.htm
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
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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
NOTE: The FSC Principles and Criteria for Forest Stewardship are currently under revision. According
to the proposed new Principles and Criteria (draft), a derogation for pesticide use shall not be required
in nurseries (viveiros) under certain conditions. If the certificate holder („organization‟) “shows that it
operates an effective and secure integrated pest management system, chemicals that are on the FSC list
of prohibited chemicals, but are not listed as highly hazardous by WHO [= are not in WHO class Ia or
Ib] and are not prohibited by national laws, may be used in tree nurseries that are outside the limits of
the forest management unit, provided that strict security measures are documented, implemented and
verified by the certification body in each case” (FSC 2009, see proposed (revised) Principle 10.7).109
When the final version of new/revised FSC Principles and Criteria is approved, proposed amendments
become valid if they are included. In forest plantations, use of pesticides listed as „highly hazardous‟
by the FSC requires a derogation as the FSC Pesticides Policy (FSC-POL-30-001, 2005) and FSC
Pesticides Policy Guidance (FSC-GUI-30-001 V2-0, 2007) are valid under the revised P&C. If the
amendments above are adopted as proposed, a derogation shall not be required for use of ‘highly
hazardous’ pesticides in nurseries, provided that certificate holders fulfil the requirements above. As
the revision process is ongoing, additional conditions may be included in the final revised P&C (e.g.
restrictions for pesticides categorised by international organizations as a carcinogen or endocrine
disruptor, or additional measures required for preventing spray drift and run-off into surface waters).
2.3 Risk Mitigation for Deltamethrin and alpha-Cypermethrin: See 1.2.1 (p. 14 above)
2.4 Stakeholder Opinions on Use of Deltamethrin / alpha-Cypermethrin: See 1.4 (pp. 29-31)
2.5 Alternatives for Control of Costalimaita ferruginea and other Coleopteran Defoliators
Bacillus thuringiensis (B.t.) is a bacterial insecticide (biopesticide). Subspecies of B.t. control certain
types of pest insect effectively. Commercial products for control of lepidopteran defoliating insects are
usually based on Bacillus thuringiensis subspecies kurstaki, or Bacillus thuringiensis subspecies
aizawai (Van Driesche et al 2008).110 Using B. thuringiensis subspecies kurstaki is a suitable method
for controlling Thyrinteina arnobia if predatory and parasitic insects are to be preseserved. B.t. is
equally effective as insecticides (Pereira 2007).111 For the integrated management of Thyrinteina, its
occurrence and population densities need to be monitored. Biopesticides based on B. thuringiensis are
109
110
111
Principios y Criterios del FSC para el Manejo Forestal – Versión completa de la Versión 5-0 Borrador 2-0 de
los PyC del FSC (Principio propuesto 10.7; Criterios 6.6 y 6.7 original, p. 80), 2009 (This working document
is no longer online; see website on the review of FSC Principles and Criteria: http://www.fsc.org/pcreview.html)
Van Driesche R., et al. Control of pests and weeds by natural enemies. Blackwell Publ., Oxford, UK 2008
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
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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
only effective when applied to larval stages of pest insects at appropriate times. B.t. can be combined
with a chemical insecticide (Zanuncio et al 1992).112 But if applied in time B.t. is effective on its own.
A combination of Beauveria bassiana (strain GHA) and Bacillus thuringiensis subspecies tenebrionis
increased mortality of Colorodo beetle larvae (Coleoptera) synergistically (Wraight & Ramos 2005). 113
This approach of combining B.t. and Beauveria bassiana merits to be tested also on Costalimaita.
Botanical extracts can deter beetles from crop plants. Beetles attacked guava leaves siginificantly less
often when the leaves had been treated with extracts of Azadirachta indica (seeds), Mentha pulegium,
Chenopodium ambrosioides, Trichilia pallid, or Ruta graveolens (Baldin et al 2007).114
Decision-support systems help to select appropriate method/s of control and optimum timing. The
distribution and density (approximate numbers per ha) of Costalimaita needs to be monitored regularly.
A decision-support system has been developed for Chrysomelidae: Monitoring System for Leaf-Beetle
Control – CMB (Anjos & Majer 2003).107 Computer models facilitate evaluation of data (CFS 2009).115
Integrated management of Costalimaita involves monitoring development stage and numbers during
critical times of the year, e.g. when juvenile beetles migrate to the forest from surrounding areas. Coleopteran defoliators are monitored in November and December (Freitas et al 2002).116 The beetle stage
of Costalimaita ferruginea emerges from soil at the time of spring rain in October to November. About
five days after the first rainfall and up to weeks later, the critical time begins. In the state of São Paulo,
defoliation by Costalimaita occurs mainly between September and March. Damage to leaves can be
recognized by characteristic perforation. In guava, the critical level of damage (threshold for action) is
reached if the beetle or damage is present in 20% of plants. A preventive measure is to maintain a
vegetation cover on the ground which promotes the occurrence of natural enemies (Souza & Costa).117
Monitoring pest organisms is a fundamental element of integrated pest management (Wilcken 2008).118
112
113
114
Zanuncio J.C., et al. Eficiência de Bacillus thurringiensis e de deltametrina, em aplicação aérea, para o
controle de Thyrinteina arnobia Stoll, 1782 (Lepidóptera: Geometridae) em Eucaliptal no Pará. Acta
Amazonica 22(4), 1992. http://acta.inpa.gov.br/fasciculos/22-4/PDF/v22n4a01.pdf
Wraight S.P., and Ramos M.E. Synergistic interaction between Beauveria bassiana- and Bacillus
thuringiensis tenebrionis-based biopesticides applied against field populations of Colorado potato beetle
larvae. Journal of Invertebrate Pathology 90(3): 139-150, 2005. http://dx.doi.org/10.1016/j.jip.2005.09.005
Baldin E., et al. Atratividade e consumo de Costalimaita ferruginea por discos foliares de goibeira tratados
com extratos vegetais. X Simpósio de Controle Biológico, Junho 2007, Brasilia.
http://www.cenargen.embrapa.br/publica/trabalhos/doc250.pdf
115
E.g. see: Canadian Forest Service (CFS). BioSIM: Pest management planning decision support. 2009.
http://cfs.nrcan.gc.ca/factsheets/biosim
116
117
118
Freitas F.A., et al. Fauna de coleoptera coletada com armadilhas luminosas em plantio de Eucalyptus grandis
em Santa Bárbara, Minas Gerais. Revista Árvore 26(4), 2002. http://www.scielo.br/pdf/rarv/v26n4/a14v26n4.pdf
Souza M.F., and Costa V.A. Manejo integrado de pragas da goiabeira: Besouro-amarelo. 2007.
http://www.nutricaodeplantas.agr.br/site/ensino/pos/Palestras_William/Livrogoiaba_pdf/9_MIPpragas.pdf (pp. 16-17)
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
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Anjos and Majer (2003) concluded that an efficient system to monitor densities of chrysomelid beetles
and damage in eucalypt plantations is needed to locate the most highly infested areas, susceptible tree
species, etc. This is particularly important if agricultural crops are grown in the vicinity of plantations.
Larval stages of Costalimaita occur in agricultural areas and need to be monitored there. Integrated pest
management often combines different control methods and adapts these to suit the local conditions.
Insecticides are only used when they cannot be avoided; the least toxic product is used preferentially.
Neem tree extract (azadirachtin) is a very effective antifeedant (stopping attack of many insects) and it
acts as an insect growth regulator and sterilant in all insect species tested (Mordue et al 2005; see 2.7
below). Mulch of neem bark applied to the ground had a deterrent effect on Coptotermes species but
may not be effective against all species (Pearce 1997).
Nucleopolyhedroviruses (NPV): Nucleopolyhedroviruses (NPVs) can be cultured quite easily and are
used as bioinsecticides. They act specifically against the insect genus (or in some cases, family) of the
target/host insect from which they were isolated. NPVs have been isolated from Lepidoptera, Hymenoptera,
Diptera, Coleoptera, and other insect orders (Bonning 2005).119 Available products for control of other
coleopteran insects may be effective against Costalimeita. Research and field tests on NPVs specific to
Costalimaita are merited. This may present a feasible non-toxic, effective and highly selective alternative.
Parasitic nematodes have been tested on beetle species (Coleoptera). E.g. nematodes (Heterorhabditis
spp.) combined with Metarhizium ansiopliae and fipronil caused 80% mortality in Migdolus fryanus, a
beetle that attacks the roots of sugar cane (Machado 2006).120 Simlar combinations of a parasitic nematode
and pathogenic fungus may be effective for control of Costalimaita ferruginea.
Pathogenic fungi affect various species of host insect. Beetles (Coleoptera species) are prevalent hosts
of Metarhizium anisopliae. But individual strains of pathogenic fungi differ in specificity (Goettel et al
2005).121 Besides M. ansiopliae, other fungi meriting tests include Beauveria bassiana – especially a
combination of B. bassiana and B.thuringiensis – and Trichoderma species.
Pheromones: These naturally occurring chemicals are used to monitor pest insects or improve the
attractiveness of baits. Pheromones can be produced synthetically for use in beetle traps and baits. The
pheromones of Costalimaita are currently being studied (Souza 2009).122 Field trials are encouraged.
Reduced weeding: By reducing control of weeds to the minimum, part of the natural vegetation cover
(herbaceous plants and grasses) on the ground is retained. This attracts natural enemies of pest insects
119
120
121
122
Bonning B.C. Baculoviruses: Biology, biochemistry, and molecular biology. In: Gilbert L.I., et al (eds).
Comprehensive molecular insect science: Control. Volume 6, pp. 233-270. Elsevier Publ., Amsterdam 2005
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
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
Souza R.M. Feromônios do besour-amarelo, Costalimaita ferruginea. Projeto de Doutorado.
http://www.insecta.ufv.br/norivaldo/popups/projetos/rodolfo-projeto-doutorado.htm
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such as aphids. Natural enemies were present in spaces with weeds. Highest infestation of pest insects
occurred on areas where weeds were controlled completely using a herbicide. Retaining weeds partially
in the rows between trees (entrelinhas) resulted in increased growth of Pinus taeda (Oliveira 2003).123
Sowing a cover crop is also possible. This keeps competing weeds low while diversifying vegetation.
Leguminous plants grown as cover crop have an additional benefit of fertilizing soil by fixing nitrogen.
Spinosad (spinosyn A): These fermentation products derived from soil microorganisms are effective
against insects of different orders. Semi-synthetic derivatives termed spinosoids are available. Spinosad
and other spinosysns are active against Coleoptera species (Salgado & Sparks 2005).124 Spinosyns are
rather selective as they affect various beneficial insects relatively weakly, especially predatory insects
(Williams et al 2003, see 2.7 below). Field tests on the effectiveness of spinosad for controlling
Costalimaita are strongly encouraged.
Tolerant Eucalyptus species: Costalimaita does not favour about 8% of Eucalyptus species; „tolerant‟
species include E. camaldulensis, E. microcorys, and E. tereticornis. The beetle „favoured‟ 83% of
Eucalyptus species but only few species were „highly favoured‟ (Anjos & Majer 2003). In the medium
to long term, species of Eucalyptus can be selected and planted that are less favoured by Costalimaita
and which are less susceptible to attack from leaf-eating beetles.
Trap plants (stumps): A simple and highly effective method preventing damage from Costalimaita is
to leave sprouting tree stumps in plantations (over at least two months before the adult beetles appear).
Beetles prefer these sprouts to the seedlings planted among old tree stumps. They feed on sprouts („trap
plants‟) and are distracted from newly planted seedlings (Anjos & Majer 2003).107 The authors stated
that this method of control produced good results in all cases where beetle density was not high enough
to consume the foliage of sprouts on stumps. This method is also effective for managing jewel beetles.
Another possibility is to diversify structure of vegetation. „Trap hedges‟ grown from eucalyptus shoots
at the edge of managed ares (or between separate areas) will distract leaf-eating beetles from crop trees.
This would be particularly effective in in seedling nurseries and areas with newly planted young trees
Native plants and robust eucalyptus species which leaf-eating beetles attack preferentially can be interplanted between tree lines to distract beetles from seedlings. In Australia, this method has been used for
a long time. For example, damage to E. grandis caused by Anoplognathus chloropyrus (Scarabaeidae)
may be minimized by interplanting of E. dunnii which is a preferred food plant for A. chloropyrus and
which tolerates extensive defoliation for several successive years (Carne & Taylor 1978).125
123
124
125
Oliveira N.C. Efeitos de diferentes sistemas de manejo de plantas invasoras sobre o controle biologico e
incidência de Cinara atlantica (Hemiptera: Aphididae) em Pinus taeda e biologia de coccinelídeos
(Coleoptera). UNESP, 2003. http://www.ipef.br/servicos/teses/arquivos/oliveira,nc-m.pdf
Salgado V.L., and Sparks T.C. The spinosyns: chemistry, biochemistry, modes of action, and resistance. In:
Gilbert L.I., et al. Comprehensive molecular insect science: Control. Vol. 6, pp. 137-173. Amsterdam 2005
Carne P.B., and Taylor K.L. Insect pests. In: Hillis W.E., and Brown A.G. (eds). Eucalypts for wood
production. pp. 155-168. CSIRO, Adelaide, Australia 1978.
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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
molecular insect science: Control. Volume 6, pp. 117-135. Elsevier Publ., Amsterdam 2005
126
Principios y Criterios del FSC para el Manejo Forestal – Versión completa de la Versión 5-0 Borrador 2-0 de
los PyC del FSC (Principio propuesto 10.7; Criterios 6.6 y 6.7 original, p. 80), 2009 (This working document
is no longer online; see website on the review of FSC Principles and Criteria: http://www.fsc.org/pcreview.html)
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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
Nadai J., et al. Dimorfismo sexual em Lampetis spp. (Coleoptera: Buprestidae). Acta Biologica Leopoldensia
27(1), 2005. http://www.insecta.ufv.br/norivaldo/popups/buprestidae/janaina-dimorfismo%20sexual-lampetis%20spp-1.pdf
Oliveira N.C. Biologia de Gonipterus scutellatus em Eucalyptus spp. em diferentes temperaturas. Tese de
Doutorado, UNESP 2006. http://www.ipef.br/servicos/teses/arquivos/oliveira,nc-d.pdf
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,
1999. http://www.ingentaconnect.com/content/esa/jee/1999/00000092/00000006/art00007
UFV: Costalimaita ferruginea: Trabalhos. http://www.insecta.ufv.br/norivaldo/popups/introducao/costalimaita-trabalhos-ufv.htm
Williams T., et al. Is the naturally derived insecticide spinosad compatible with insect natural enemies?
Biocontrol Science and Technology 13(5), 2003. http://www.informaworld.com/smpp/content~db=all~content=a713993097
Young S.Y. Problems associated with the production and use of viral pesticides. Mem. Inst. Oswaldo Cruz
84(suppl. 3), 1989. http://www.scielo.br/pdf/mioc/v84s3/vol84%28fsup3%29_062-068.pdf
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 m3/ha
for 100 % defoliation (Oda & Berti Filho 1978).127 Damage from lepidopteran defoliators in E. saligna
126
127
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
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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(2.5-3.5 years old) caused reductions in annual increment of 40% (25.6 m3/ha) in the year after the
attack; total reductions amounted to 60% on average and caused tree mortality of ca. 6% (source: SGS1943). Caterpillars of Thyrinteina must be rapidly controlled due to a short cycle and high reproductive
potential. Companies monitor caterpillars of Thyrinteina through field inspections and sampling in the
affected areas (weighing excreta to assess development stage, and catching adult insects in light traps).
Based on monitoring results it is decided if biological and/or chemical methods are used for control.
The main method of control is using an insecticide in areas initially infested with caterpillars.
Several certificate holders give priority to the use of Bacillus thuringiensis (Dipel). B.t. is also used on
larger areas (over 5000 ha). To be effective, B.t. must reach larval stages of target insects, necessitating
application at the appropriate time. Selecting the time for application requires monitoring. If different
stages of larval development are present simultaneously this complicates correct timing of application.
According to Zanuncio et al (1994), deltamethrin has a low selectivity toward parasitoid flies and it
does not control Thyrinteina in the adult stage.128 Contrary to this finding, certificate holders stated:
“Biological control (Bacillus thuringiensis) will be implemented when the first infestations are detected during
plantation, generally with two applications; the first to reach the caterpillars and the second application carried
out between 10 and 15 days after the first, to control the recently hatched caterpillars;
Deltamethrin: is required in the case of overlapping generations, given that this chemical product is highly
efficient in all phases of the insect, i.e. from the egg to the adult, drastically reducing the pest population in the
area to be treated. (…) Deltamethrin will be required when the caterpillars reach maturity and no longer ingest
leaves. The control is carried out to interrupt the pest‟s life-cycle, avoiding an increase in population and
consequently in the area affected.”
Certificate holders intend to use the following product for controlling lepidopteran defoliators:
·Decis CE (liquid formulation): contains 2.5% deltamethrin (active ingredient)
Safety Data: Decis 25 CE (Bayer). http://www.bayercropscience.com.br/produtos/downloads/Decis25CE-REFL.pdf
From 7 companies with areas affected by Thyrinteina arnobia, 3 used an insecticide (deltamethrin) or
a biopesticide (B. thuringiensis) to control this lepidopteran defoliator. The % infested area of managed
forests ranged from 0.01% to 19.3% (averaging 3.9%), and the area where Thyrinteina was controlled
ranged from 11 ha to 10'782.5 ha. Regarding lepidopteran defoliators (caterpillars), some companies
said that they were aware of the potential damage in eucalypts but only monitored infestation level (by
inspecting trees visually) as the extent of defoliation was not high enough to cause economic losses.
Four companies were affected by other lepidopteran defoliating insects: Adeloneivaia subangulata,
Euselasia apisaon, Glena species, Lampetis drummondi, and Melanolophia species. But only one of
these species was controlled: Melanolophia species, using B. thuringiensis on 120 ha (see table 5 on
pp. 33-34 above).
128
Zanuncio J.C., et al. Eficiência da deltamentrina e da permetrina, em aplicação terrestre, contra os
lepidópteros Thyrinteina arnobia (Geometridae) e Nytalea nyseus (Notodontidae) no Trópico Úmido, Acta
Amazonica 24(4), 1994. http://acta.inpa.gov.br/fasciculos/24-4/PDF/v24n4a13.pdf
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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
130
Van Driesche R., et al. Control of pests and weeds by natural enemies. Blackwell Publ., Oxford, UK 2008
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)
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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
results. IT-based systems enable predictions about development of insect populations (CFS 2009).131
Remote sensing can be used to localise pest insects and optimize use of B.t. (Trivellato et al 2006).132
Integrated management of Thyrinteina or other lepidopteran defoliators involves monitoring the stage
of development and numbers during critical times of the year (before caterpillars enter the pupal stage).
Different methods can be combined, including preventive silvicultural practices (planting robust tree
species, retaining native vegetation on part of managed areas, reduced weeding, cover crops) and use of
biopesticides (B. thuringiensis and/or B. bassiana, or pathogenic fungi) or insecticides of low-toxicity.
Natural enemies: in Brazil, Podisus nigrispinus and Supputius cincticeps are predators of lepidopteran
defoliating insects, especially of eucalyptus brown looper Thyrinteina arnobia. Natural enemies can be
promoted by reducing weed control (retaining weeds between trees) and preserving natural forests on
part of the managed area (appropriate to scale of the plantation). Regulation of lepidopteran defoliators
(such as Euselasia apisaon) is enhanced where fragments of natural vegetation are present, e.g. through
increased predation parasitoid wasps (Murta el al 2008; Zanuncio et al 2009).133 Natural enemies of
lepidopteran insects can be mass-reared and released in infested areas.
Neem tree extract / azadirachtin has marked antifeedant activity in Lepidoptera (Mordue et al 1998).
Nucleopolyhedroviruses (NPV): Nucleopolyhedroviruses (NPV) are baculoviruses which affect certain
host insects. NPVs can be cultured quite easily and are used as bioinsecticides. They act specifically against
the insect genus (or in some cases, family) of the target/host insect from which they were isolated. NPVs
have been commercially used in forestry for a long time e.g, the virus-based product Gypchek for control
of gipsy moth (Lymantria dispar) (Thorpe et al 1999),134 or a product based on NPV specific to the pine
sawfly (Neodiprion lecontei) (CFS 2009).135 Available products for control of lepidopteran insects may
be effective against Thyrinteina. Research and tests on NPVs specific to Thyrinteina are metited. This may
present a feasible non-toxic, effective and highly selective alternative in the short to medium term.
Pathogenic fungi such as Beauveria bassiana and Metarhizium anisopliae are effective against a broad
range of host insects, including species of Lepidoptera, Diptera, Coleoptera, Hymenoptera, Homoptera.
Entomopathogenic fungi vary in the degree to which they infect only certain insect species, but a single
strain of pathogenic fungus rarely attacks both beneficial and pest species (Goettel et al 2005).135
131
E.g. see: CFS. BioSIM: Pest management planning decision support. http://cfs.nrcan.gc.ca/factsheets/biosim
Trivellato G.F., et al. Uso de sensoriamento remoto no monitoramento preciso de pragas em eucalipto. USP
2006. http://www.usp.br/siicusp/Resumos/14Siicusp/3996.pdf
133
Murta A.F. Efeitos de remanescentes de Mata Atlântica no controle biológico de Euselasia apisaon (…) por
Trichogramma maxacalii (…). Neotropical Entomology 37(2), 2008. http://www.scielo.br/pdf/ne/v37n2/a19v37n2.pdf
Zanuncio J.C., et al. Mortality of the defoliator Euselasia eucerus (Lepidoptera: Riodinidae) by biotic factors
in an Eucalyptus urophylla plantation in Minas Gerais State, Brazil. Anais da Academia Brasileira de
Ciências 81(1): 61-66, 2009. http://www.scielo.br/pdf/aabc/v81n1/a08v81n1.pdf
134
Thorpe K., et al. Aerial application of the viral enhancer blankophor BBH with reduced rates of Gypsy Moth
(…) nucleopolyhedrovirus. Biological Control 16, 1999. http://dx.doi.org/10.1006/bcon.1999.0758
135
Canadian Forest Service (CFS). Microbial control agents: Baculovisuses. http://cfs.nrcan.gc.ca/subsite/glfcbacillus-thuringiensis; Sylvar Technologies Inc. Baculovirus. http://www.sylvar.ca/content/13389
135
Goettel M.S., et al. Entomopathogenic fungi and their role in regulation of insect populations. In: Gilbert L.I.,
132
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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
Reduced weeding: By reducing control of weeds to the minimum, part of the natural vegetation cover
(herbaceous plants and grasses) on the ground is retained. This attracts natural enemies of pest insects.
Spinosad is a naturally occurring fermentation product derived from soil bacterium Saccharopolyspora
spinosa. Spinosad (spinosyn A) is used for controlling various pest insects on fruit or vegetable crops,
cotton, tree and vine crops and ornamentals on a global basis. Spinosad poses a relatively low hazard to
humans. It also presents a low hazard to fish, birds, and mammals (Harris & MacLean 1999).136 In
many countries, spinosad is authorized for use in organic agriculture (OMRI 2002; Racke 2006).137
2.6 Conclusions – Thyrinteina arnobia and other Lepidopteran Defoliators
1. On most plantations affected by eucalyptus brown looper Thyrinteina arnobia or other lepidopteran
defoliators, infestation level and damage was not sufficiently high to warrant chemical control, with
the exception of Melanolophia species. In 2008, a certificate holder controlled this insect on 120 ha
with Bacillus thuriengiensis.
2. Several alternatives are available for control of lepidopteran insects, including biopesticides based
on Bacillus thuringiensis (in particular B.t. subspecies kurstaki and B.t subspecies aizawai), use of
an IT decision-support system for evaluating monitoring data to optimize timing of B.t. applications,
nucleopolyhedroviruses (NPV) specific to lepidopteran insects, promotion of natural enemies (e.g.
birds or predatory insects) through reduced weeding (leaving part of the natural vegetation between
tree lines), restoration of natural forest on part of managed areas, and use of low-toxicity insecticides
such as spinosad or azadirachtin/neem (when development stage of pest insects limits use of B.t.).
3. In forest plantations with older trees, it appears feasible to control Thyrinteina arnobia and other
lepidopteran defoliators (caterpillars, in particular) by regular monitoring of insects (possibly also
outside managed areas), combining preventive silvicultural with biological methods of control, and,
in case of an outbreak/infestation, using a less hazardous insecticide such as spinosad. In nurseries
(viveiros), according to (proposed) revised FSC Principles and Criteria,138 a derogation for using a
„highly hazardous‟ pesticide shall not be required, providing that certain conditions are met.
2.7 Additional Publications on Thyrinteina arnobia and other Defoliators
Aguiar-Menezes E. de. Inseticidas botânicos: seus princípios ativos, modo de ação e uso agrícola. Embrapa
Agrobiologia 2005. http://www.cnpab.embrapa.br/publicacoes/download/doc205.pdf
Ambiental Tiétê. Manual técnico de plantio de eucalipto. http://www.sementesquality.com.br/manuais/Manual-Eucalipto.pdf
136
137
138
et al. Comprehensive molecular insect science: control. Vol. 6, pp. 361-405. Elsevier Publ., Amsterdam 2005
Harris & MacLean (1999): Spinosad: control of lepidopterous pests in vegetable brassicas. In: Proceedings of
the 52nd NZ Plant Protection Conference 1999, pp. 65-69. http://www.nzpps.org/journal/52/nzpp52_065.pdf
Organic Materials Review Institute (OMRI). Spinosad. 2002. http://www.omri.org/spinosad_final.pdf
Principios y Criterios del FSC para el Manejo Forestal – Versión completa de la Versión 5-0 Borrador 2-0 de
los PyC del FSC (Principio propuesto 10.7; Criterios 6.6 y 6.7 original, p. 80), 2009 (This working document
is no longer online; see website on the review of FSC Principles and Criteria: http://www.fsc.org/pcreview.html)
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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
Branco E.F. Aspectos econômicos do controle de Thyrinteina arnobia (…) com Bacillus thuringiensis (Berliner)
em povoamentos de Eucalyptus spp. Laboratório de Proteção Forestal 1995 http://floresta.ufpr.br/~lpf/outras02.html
Castro M.E.B., et al. Vírus isolado da lagarta do trigo tem potencial para controle da praga (Pseudaletia sp).
Embrapa 2007. http://www.embrapa.br/embrapa/imprensa/artigos/2007/artigo.2007-01-04.5743559910
Clemente A.T.C. Análise de populações de Lepidoptera em comunidades florestais de Araucaria angustifolia,
Eucalyptus grandis e Pinus taeda. Laboratório de Proteção Florestal. 1995. http://floresta.ufpr.br/~lpf/teses0114.html
Dal Pogetto M.H., et al. Controle de Thyrinteina arnobia (…) com micoinseticidas em condições de laboratório.
X Simpósio de Controle Biológico 2007. http://www.cenargen.embrapa.br/publica/trabalhos/doc250.pdf (p. 352)
Dias T.K., et al. Desenvolvimento do predador Tynacantha marginata alimentando com lagartos de Thyrinteina
arnobia. X Simpósio de Controle Biológico 2007. http://www.cenargen.embrapa.br/publica/trabalhos/doc250.pdf (p. 736)
Faria A.B.C., and Sousa N.J. Efeito residual em campo do imidacloprido no controle do pulgão-do-pinus
(Cinara spp.) (…), Scientia Agraria 8(3), 2007. http://ojs.c3sl.ufpr.br/ojs2/index.php/agraria/article/viewFile/9510/8011
Franz A.R. Efeito letal de Bacillus thuringiensis cepa 4412 (…) às lagartas de Spodoptera frugiperda (Lepidoptera: Noctuidae). Unisinos 2007. http://www.unisinos.br/mostra2007/trabalhos_publicados/docs/eixo2/02-007.pdf
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
Amazonica 38(1): 101-106, 2008. http://www.scielo.br/pdf/aa/v38n1/v38n1a11.pdf
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 …)
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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
(…). X Simpósio de Controle Biológico 2007. http://www.cenargen.embrapa.br/publica/trabalhos/doc250.pdf (p. 628)
Racke K.D. A reduced risk insecticide for organic agriculture: Spinosad case study. A.C.S. Symposium series
947, pp. 92-108, 2006. http://pubs.acs.org/doi/abs/10.1021/bk-2007-0947.ch007
Sapper Biermann A.C., et al. Ação de inseticidas botânicos sobre o consumo alimentar de Ascia monuste orseis
(Lepidoptera: Pieridae). UFSM 2009. http://www.cesumar.br/epcc2009/anais/pedro_krauspenhar_rosalino2.pdf
Sapper Biermann A.C. Bioatividade de inseticidas botânicos sobre Ascia monuste orseis (Lepidoptera: Pieridae).
UFSM 2009. http://cascavel.cpd.ufsm.br/tede/tde_busca/arquivo.php?codArquivo=2710
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
Neotropicales 17, 2005. http://web.catie.ac.cr/informacion/RMIP/rev75/BoletinPlagasForestales.pdf
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
141
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
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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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors
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/S030180591998000100016
143
144
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
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: Rhinotermititidae) . Revista O Biológico 70(supl. 1), 2008. http://www.biologico.sp.gov.br/docs/bio/suplementos/v70_supl/37.pdf
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of pathogenic fungi and botanical extracts could improve effectiveness. More tests are needed. Extract
of neem (Azadirachta indica) had toxic, antifeedant and deterrent effects on termites, although duration
of effect was limited (Grace & Yates 1992).147 Neem mulches also deterred Coptotermes species.
Chitin inhibitors may present a less hazardous chemical alternative. For example, six applications of
silafluofen (as a liquid) resulted in 30-40% mortality of termites Cornitermes cumulans (Mariconi et al
1994).148 For effective control, pest insects may need to absorb an insect growth regulator continuously
over a certain period (Börne 1981).149 This is likely to be more effective when applied in baits than in
direct use. E.g. chitin synthesis inhibitors generally act slowly. For controlling social insects such as
termites, slow action can be an advantage (Dhadialla et al 2005).150
Chitin synthesis inhibitors which are based on urea include, for example, chlorfluazuron, diafenthiuron,
diflubenzuron, flufenoxuron, hexaflumuron, lufenuron, noviflumuron, teflubenzuron and thidiazuron.
Although insect growth regulators generally have low toxicity and are relatively selective, they qualify
as „highly hazardous‟ under FSC criteria due to their high octanol-water partition coefficient which
indicates a certain potential for bioaccumulation.
Diatomaceous earth (terra diatomácea) is used as a wood preservative to prevent termite attacks in dry
wood elements in buildings. It consists mainly of silicon dioxide and acts as a desiccant, killing insects
by dehydration. Silica aerogel (silicon dioxide) is also used for wood protection but may not deter all
termite species (Grace & Yates 1999).151 Use of diatomaceous earth in baits combined with pathogenic
fungi merits further research (even partial dehydration of termites might weaken the immune defense).
Imidacloprid (Confidor®) applied as a liquid to nests of Cornitermes resulted in 78% mortality when
the funnel had a short tube and 96% mortality when the tube was longer (30 cm). Depth of application
was important for insecticide distribution in the nest and effectiveness of control (Fadini et al 2001).152
Although imidacloprid is WHO class II (“Moderately Hazardous”) like fipronil, it has a lower acute
toxicity and is not rated as „highly hazardous‟ under FSC criteria. Thus it might be used to substitute
fipronil. But imidacloprid has a high solubility in water and medium adsorption to soil (Tomlin 2006);
in soil it is moderately mobile and calculated leaching potential is high (Footprint 2007; see annex III).
147
Grace J.K., and Yates J.R. Behavioural effects of a neem insecticide on Coptotermes formosanus (Isoptera:
Rhinotermitidae). International Jounal of Pest Mangement 38(2), 1992.
http://www.informaworld.com/smpp/content~db=all~content=a905483315
148
149
150
151
Mariconi FAM et al. Ensaios de combate ao cupim de monte Cornitermes cumulans (Kollar, 1832) (Isoptera,
Termitidae). Scientia Agricola 51(3), 505-508, 1994. http://dx.doi.org/10.1590/S0103-90161994000300022
Börne H. Pflanzenkrankheiten und Planzenschutz [Plant diseases and plant protection]. Stuttgart 1981
Dhadialla T.S., et al. Insect growth- and development-disrupting insecticides. In: Gilbert L.I., et al (eds).
Comprehensive molecular insect science: Control. Vol. 6, pp. 55-115. Elsevier Publ., Amsterdam 2005
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
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Especially in areas with sandy soil, rainfall could lead to leaching of imidacloprid into groundwater.
Mechanical destruction of termite nests is a non-chemical alternative Use of a tractor-mounted drill
(„broca cupinzeira‟) resulted in 90-100% mortality in Cornitermes cumulans (Valerio et al 1998).142
Nematodes which parasitise on termites are possible biocontrol agents. The nematode Steinernema
carpocapsae was highly pathogenic to C. cumulans (Rosa et al 2008).153 The mobility and reproduction
rate of nematodes in termite nests appear to be a limiting factor. It was therefore recommended to use
synergistic effects by combining parasitic nematodes with Bacillus thuringiensis or with an insecticide
such as imidacloprid to increase susceptibility of termites to infection (Wang et al 2002). Combining
Steinernema carpocapsae with imidacloprid increased its infectivity (Negrisoli 2005).154
Pathogenic fungi such as Metarhizium anisopliae and Beauveria bassiana are promising biological
agents for termite control (Boyd et al 2002).155 Certain subspecies control specific pest insects more
effectively than others. For example, Metarhizium anisopliae strain ESF1 controls cockroaches and M.
anisopliae var. acridum (formerly M. flavoviride) is effective against migratory locusts or grasshoppers
(Magalhães et al 2000).156 While Metarhizium anisopliae appears to be an opportunistic pathogen of
termites, specific isolates were highly pathogenic (Milner et al 1998).157 Due to rapid sporulation (a
factor possibly contributing to high virulence), Metarhizium anisopliae may be better adapted to
overcome the defense of social insects (Sun et al 2002).158
A combination of Beauveria bassiana (strain GHA) and Bacillus thuringiensis (B.t.) subsp. tenebrionis
increased mortality of Colorodo beetle larvae (Coleoptera) synergistically (Wraight & Ramos 2005). 113
Growth of Beauveria bassiana may be slower at high temperatures. B.t. kills larvae at an early stage
and increases susceptibility of older larvae to B. bassiana (Kuepper 2009).159 The B.t. subspecies sooncheon and roskildiensis caused 100% mortality in termites Nasutitermes ehrhardti (Castilhos-Fortes
153
Rosa M.O.J., et al. Patogenicidade de Steinernema carpocapsae (Rhabditida: Steinernematidae) ao cupim de
montículo Cornitermes cumulans (Isoptera: Termitidae). Nematologia Brasileira 32(4), 2008.
http://docentes.esalq.usp.br/sbn/nbonline/ol%20324/260-269%20co.pdf
154
Wang C., et al. Laboratory evaluations of four entomopathogenic nematodes for control of subterranean
termites (…). Biological Control 31(2), 2002. http://www.rci.rutgers.edu/~insects/11-nematode.pdf
Negrisoli A.S. Jr. Avaliação de técnicas para estudo de compatibilidade de produtos fitossanitários com
nemtóides entomopatogênicos (…). M.Sc., UFLA. 2005. http://docentes.esalq.usp.br/sbn/ajuda/aldomario.pdf
155
Boyd et al. Environmental effects of currently used termiticides under Australian conditions. Queensland
2002. http://www.build.qld.gov.au/research/BrDocs/termiticides/termiticides_report.PDF
156
Magalhães et al. Field trial with the entomopathogenic fungus Metarhizium anisopliae var. acridum against
bands of the grasshopper Rhammatocerus schistocercoides in Brazil. Biocontrol Science and Technology 10,
427-441, 2000. http://www.informaworld.com/smpp/content~db=all~content=a713655539
157
Milner RJ, et al. Occurrence of Metarhizium anisopliae in nests and feeding sites of Australian termites.
Mycology Research 102 (2): 216-220, 1998. http://dx.doi.org/10.1017/S0953756297004735
158
Sun J, et al. Sporulation of Metarhizium anisopliae and Beauveria bassiana on Coptotermes formosanus and
in vitro. Journal of Invertebrate Pathology 81: 78-85, 2002. http://dx.doi.org/10.1016/S0022-2011(02)00152-0
159
Kuepper G. Colorado potato beetle: Organic control options: Biopesticides. National Center for Appropriate
Technology 2009. http://attra.ncat.org/attra-pub/coloradopotato.html#biopesticides
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2002).160 Thus combining fungal pathogens and B.thuringiensis seems promising for termite control.
But not all combinations are compatible. E.g. Trichoderma species affected growth of B. bassiana and
M. anisopliae when grown together simultaneously or within two days (Moino & Alves (no year)).161
Glucono delta-lactone (GDL) is a substance that could help to overpower the immune defence of
termites. GDL makes termites, locusts and cockroaches more susceptible to infections by bacteria and
fungi by blocking part of their immune defence. It renders these insects more vulnerable to microbial
pathogens by deactivating specific proteins incorporated in their nests (Bulmer et al 2009).162 Glucono
delta-lactone occurs naturally as a derivative of glucose. It is non-toxic to mammals, biodegradable and
inexpensive. GDL may increase the infectivity of pathogenic fungi. Combinations of pathogenic fungi
(M. anisopliae, B. bassiana or Aspergillus flavus) and glucono delta-lactone might reduce activity of
termites or provide effective control. (This might be desired exceptionally in areas with a high density
of C. bequaerti or S. molestus – in situations where preventive treatment was not effective or feasible).
Preventive silvicultural practices include, in the long term, growing tree species that are more robust.
E.g. Eucalyptus camaldulensis, E. deglupta, and E. microcorys are reported to be moderately to highly
resistant to termite attack (Schmidt & Meke 2008).163 In the short term, cultural practices favouring the
occurrence of termites can be avoided. Reduced tillage (less ploughing) prevents damage from termites
in seedlings. Non-tillage benefited natural enemies (predatory ant species Solenopsis and Pheidole) that
prey on termites (Lange et al 2008).164 Non-tillage can be combined with a cover crop (such as Mucuna
bracteata) to reduce competing vegetation. An alternative is to cover the ground with straw mulches.
Pyrethroids: Silafluofen has been used for controlling termites in the past. However, this insecticide
qualifies as „highly hazardous‟ due to its very high logKOW of 8.2 (Sanchez-Bayo 2004).165 In addition,
silafluofen is a reproductive toxin (rated as potential endocrine disruptor by the European Union).166
160
Castilhos-Fortes R., et al. Susceptibility of Nasutitermes ehrhardti (Isoptera: Termitidae) to Bacillus
thuringiensis subspecies. Brazilian Journal of Microbiology 33(3): 219-222, 2002.
http://www.scielo.br/pdf/bjm/v33n3/v33n3a06.pdf
161
Moino A., y Alves S.B. Efeito antagônico de Trichoderma sp. no desenvolvimento de Beauveria bassiana e
Metarhizium anisopliae Sorok. Monografías (no year). http://br.monografias.com/trabalhos/efeito-trichoderma-spbeauveria-bassiana/efeito-trichoderma-sp-beauveria-bassiana.shtml
162
163
164
165
166
Bulmer M.S, et al. Targeting an antimicrobial effector function in insect immunity as a pest control strategy.
PNAS 106(31): 12652-12657, 2009. http://www.pnas.org/content/106/31/12652.abstract
Trafton A. Blocking termites‟ defense mechanisms: Targeting immune system may offer sustainable pest
control method. MIT News June 8, 2009. http://web.mit.edu/newsoffice/2009/pest-0608.html
Schmidt L., Meke G. Tree species resistant to termites. 2008. http://en.sl.life.ku.dk/upload/technical_briefs_5.2008.pdf
Lange D., et al. Predacious activity of ants (…) in conventional and in no-till agriculture systems. Brazilian
Archives of Biology and Technology 51(6): 1199-1207, 2008. http://www.scielo.br/pdf/babt/v51n6/15.pdf
Sánchez-Bayo F. More realistic concentrations of agrochemicals for environmental risk assessments. Journal
of Pesticide Science 29: 130-133, 2004. http://www.jstage.jst.go.jp/article/jpestics/29/2/29_130/_article
European Commission. Endocrine Disrupting Substances (EDS) Database and Categorisation (database
downloadable from website). Brussels 2006. http://ec.europa.eu/environment/endocrine/strategy/short_en.htm
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4.6 Conclusions – Preventive Treatment of Seedlings with Fipronil
1. To prevent seedlings from attack by termites (Cornitermes bequaerti and Syntermes molestus), in
many areas these are treated with fipronil prior to planting. Preventive treatment of seedlings prior
to planting should be the predominant – or only – method of termite control. If termite colonies are
targeted directly (e.g. if termites attack buildings), biological agents should be used preferentially.
2. A common framework for integrated management of termites could include voluntary or mandatory
standards for monitoring termite nests and damage, identification of areas with critical nest densities
or unacceptably high damage levels, and selection of effective and environment-friendly methods
appropriate for site conditions. Certificate holders are recommended to cooperate with other companies and scientific experts at research institutions or universities in developing preventive practices
and IPM based methods of termite control (where this is needed to achieve silvicultural objectives).
4.7 Additional Publications on Termites
Almeida J.E.M., et al. Controle do cupim subterrâneo Heterotermes tenuis (Hagen) com iscas termitrap
impregnadas com inseticidas e associadas ao fungo entomopatogênico Beauveria bassiana (Bals.) Vuill. Anais
da Sociedade Entomológica do Brasil 27(4), 1998. http://dx.doi.org/10.1590/S0301-80591998000400017
Beringer J.S., et al. Efeito de Aspergillus e Beauveria bassiana cobre Cornitermes cumulans (Isoptera:
Termitidae). Unisinos 2007. http://www.unisinos.br/mostra2007/trabalhos_publicados/docs/eixo2/02-033.pdf
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
mark-release-recapture (Isoptera: Rhinotermitidae). Sociobiology 42(3), 2003.
http://www.csuchico.edu/biol/Sociobiology/volume/sociobiologyv42n32003.html#24
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
Entomology 30(2), 2001. http://www.scielo.br/pdf/ne/v30n2/a01v30n2.pdf
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Laboratório de Proteção Forestal. Cupins. http://floresta.ufpr.br/~lpf/pragas06.html
Leonardo A.M.C. Laboratório de Cupins, CEIS – UNESP. http://www.rc.unesp.br/ib/ceis/cupins.php
Moino A. Jr., Alves S.B. Efeito de imidacloprid e fipronil sobre Beauveria bassiana (Bals.) Vuill. e Metarhizium
anisopliae (Metsch.) Sorok. e no comportamento de limpeza de Heterotermes tenuis (Hagen). Anais da
Sociedade Entomológica do Brasil 27(4), 1998. http://dx.doi.org/10.1590/S0301-80591998000400014
OISAT. Termites control – Termitidae. 2005. http://www.oisat.org/downloads/AgroEcoTermite_control.doc
Passos E.M. dos. Patogenicidade de fungos do genero Isaria (Persoon) sobre Coptotermes gestroi (Wassmann)
(Isoptera: Rhinotermitidae) e aspectos imulógicos. Tese M.Sc., UFRPe 2009.
http://www.ppgea.ufrpe.br/novosite/files/dissertacoes/Eliana%20Maria%20dos%20Passos.pdf
Peralta R.C.G., et al. Wood consumption rates of forest species by subterranean termites (Isoptera) under field
conditions. Revista Árvore 28(2), 2004. http://dx.doi.org/10.1590/S0100-67622004000200015
Santos A. dos. Amostragem de cupins subterrâneos em plantios de eucalipto e persistência de resíduos de
fipronil em substrato de mudas e na calda inseticida. Tese, UFLA 2008.
http://biblioteca.universia.net/ficha.do?id=33823243
Santos M.N. Avaliações mensais de estacas de Pinus como isca-armadilhapara cupins subterrâneos em áreas de
composições florísticas distintas no jardim botânico do Rio de Janeiro e avaliação de extratos botânicos como
cupinicida. UFRRJ 2008. http://www.ufrrj.br/posgrad/PPFBA/paginas/docs_dissertacoes/2008MarcusNascimentoSantos.pdf
Sena J.M., et al. Assemblage of termites in a fragment of Cerrado on the coast of Paraíba State, Northeast Brazil
(Isoptera). Sociobiology 42(3), 2003. http://www.csuchico.edu/biol/Sociobiology/volume/sociobiologyv42n32003.html#19
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
subterranean termites (Isoptera: Rhinotermitidae). Sociobiology 42(3), 2003.
http://www.csuchico.edu/biol/Sociobiology/volume/sociobiologyv42n32003.html#7
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Annex I Studies on Herbivory of Leaf-cutting Ants
In Latin America, leaf-cutting ants (e.g. Atta cephalotes) are often a serious problem for farmers. But
quantitative data on the biomass consumption by leaf-cutting ants is lacking. In Panama, the amount of
leaves consumed by one colony of leaf-cutting ants (Atta colombica) in an old secondary forest was
determined. One ant colony harvested 13.2 tons of biomass (equivalent to 132 kg/ha) per year.
Consumption rates varied considerably between colonies. In the observed area, the proportion of
biomass consumed annually by ants was equivalent to 1.7% of the total leaf-area produced. The authors
concluded the results suggest that the impact of leaf-eating ants in natural tropical forests may be
considerably lower than previously assumed (Herz et al 2007).167
In a secondary forest in Panama, herbivory rates of leaf-cutting ants (Atta colombica) ranged from 9.0
m2 to 11.4 m2 per day (in the wet and dry season, respectively), but was highly variable on different
days. The total area of green leaves cut was 1'707 m2 and 3'855 m2 for two colonies. On average, total
dry weight of plant matter consumed was 370 kg in one year, of which 30% was non-green material
(Wirth et al 1997).168 Average consumption by small nests of Atta and Acromyrmex was estimated as
0.5-1.1 kg per year; foraging activity was higher if leaves contained less cellulose (Sousa-Souto 2007).
Elsewhere it is reported that one colony of leaf-cutting ants (Atta species) consumes 50-250 kg of dry
matter annually (Ghazoul 2004).169 Methods to determine consumption rates of leaf-cutting ants have
been refined (Herz & Beyschlag 2007).170 Herbivory is irregularly distributed and negligible in primary
forests. Removal of leaves by ants affects individual plants, especially those losing a high proportion of
leaves (Wirth et al 2003).171
In undisturbed rain forests of the Amazon, the maximum density of ant nests (Atta cephalotes) was
0.045 nests per hectare, while in managed forests nest densities were higher. The authors suggested that
the number of clearings is a limiting factor for colonization of new forest sites by these leaf-cutting ants
(Jaffe & Vilela 1989).172 After clearing mature forests, density of ant nests increased and prevalence of
different ant species changed (Vasconcelos & Cherrett 1995).173 In areas that have been cleared, the
167
Herz H., et al. Assessing herbivory rates of leaf-cutting ant (Atta colombica) colonies through short-term
refuse deposition counts. Biotropica 39(4): 476-481, 2007.
http://www3.interscience.wiley.com/journal/118501537/abstract
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
170
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
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.blackwellsynergy.com/doi/full/10.1111/j.1744-7429.2007.00284.x
171
172
Wirth R., Herz H., Ryel R.J., Beyschlag W., and Hölldobler. Herbivory of leaf-cutting ants: a case study on
Atta colombica in the tropical rainforest of Panama. Springer Publ., Berlin 2003
Jaffe K., and Vilela E. On nest densities of the leaf-cutting ant Atta cephalotes in tropical primary forest.
Biotropica 21(3): 234-236, 1989. http://links.jstor.org/sici?sici=00063606%28198909%2921%3A3%3C234%3AONDOTL%3E2.0.CO%3B2-C&size=LARGE&origin=JSTOR-enlargePage
173
Vasconcelos H.L., and Cherrett J.M. Changes in leaf-cutting ant populations (Formicidae: Attini) after the
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activity of leaf-cutting ants is higher than in forested areas (Florin 2002).174
Forests of native tree species offer limited resources to leaf-cutting ants which prevents infestations of
ants. In reforested areas, on the other hand, the low diversity of vegetation results in a large increase in
density of Atta sexdens (Mendes et al 2007).175 Leaf-cutting ants can severely attack plantations, e.g.
mahagoni (Swietenia) species, leading to reduced growth of young seedlings, forking or death. Where
insecticides are not available or too costly, attack may be minimized by inter-planting trees with other
species (or by planting species preferred by ants in adjacent areas) and by avoiding clean weeding
(Cornelius et al 2004).176 Eucalypt seedlings under stress of limited water were more attractive to leafcutting ants, resulting in increased preference for certain Eucalyptus species (Caffarini et al 2006).177
Where water resources are not too limited, a preventive alternative would be to grow tree species for
which ants have a smaller preference.
Ants are attracted to drought-stressed plants due to an increase in nutrient content in leaves with lower
water content (Meyer et al 2006).178 Foraging activity of leaf-cutting ants was studied in the Atlantic
Forest of Northeast Brazil which is highly fragmented. The density of nests of Atta cephalotes was ca.
8.5 times higher at the forest edge (up to 50 m inside the forest) than in the forest interior, where nest
density was low. With Atta sexdens, the density of nests was more uniformly distributed. A stable high
abundancy of nests was associated with the constant high availability of pioneer plants species which
the ants prefer. On average, herbivory rate (% removal of foliage) was four times higher at the forest
edge (36%) than in the forest interior (6%). Particularly Atta cephalotes altered forest structure by
opening gaps in the canopy and understory vegetation (Meyer 2008).179 Increased light availability was
accompanied by higher soil temperatures and lower water availability. The area affected by higher light
levels extended to about 4 m away from the nest edge. Survival of transplanted seedlings differed
strongly between habitat and tree species. In general, survival was high in the forest and low on nests
where it correlated strongly with seed size. Leaf-cutting ants might contribute to domination of pioneer
plant communities at forest edges. In the presence of ant nests, natural selection favoured plant species
174
175
clearing of mature forest in Brazilian Amazonia. Studies on Neoptropical Fauna and Environment 30(2): 107113, 1995. http://www.informaworld.com/smpp/content~db=all~content=a905708940
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
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
177
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
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.unikl.de/volltexte/2008/2286/pdf/Meyer2008EcoEnginForestEdgeKomprimiert.pdf
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which profit from increased light levels and which also are able to re-sprout (Meyer et al 2009).180
In fragmented natural forests, Atta species present a relatively frequent disturbance at an intermediate
level (among other types of disturbance), which probably can enhance separation of ecological niches.
While delaying forest succession, leaf-cutting ants are maintaining a higher diversity of plant species
(Wirth et al 2003).171 In natural rainforests, total defoliation of entire trees has never been reported.
Herbivory of leaf-cutting ants (Atta cephalotes) was determined in a monoculture of cassava (a food
preferred by ants) and three plant communities of increasing complexity and also composed of some
cassava. Before harvest, herbivory rate in the cassava monoculture was several times (to over ten
times) higher than in the other plant communities, and decreased with increasing complexity of
vegetation. Leaf consumption by ants represented 0.3% of total leaf area in the monoculture, and a
mean of 0.03% of total leaf area in three complex plant communities. Cassava was attacked most
heavily (per unit leaf area) in a successional plant community of introduced species, least heavily in
enriched successional vegetation, and at intermediate intensity in the monoculture. The ants preferred
woody to herbaceous species and introduced species to natural colonizers (Blanton & Ewel 1985).181
The leaf-cutting ants Atta cephalotes and A. colombica cut mature leaves selectively from 22-31% of
plant species present. Plants close to a nest had a higher probability of being attacked but were not
necessarily more strongly defoliated than other plants within 50-60 m of the nest. Consumption rates
decreased strongly for plants further than 60-80 m away from the nest (Rockwood 1976).182
Factors influencing leaf-cutting ants herbivory were studied in Brazil. Equally sized colonies of Atta
cephalotes located at the edge of an indigenous forest removed about twice as much leaf area than
interior colonies. At the forest edge, leaf area available to ants was clearly reduced. It appears that in
the edge zone of forests consumption by leaf-cutting ants is increased (Urbas et al 2007).183 These
findings indicate that fragmentation of forests may intensify problems with foraging ants.
In Costa Rica, a study found that nests of leaf-cutting ants located in partial shade consumed a larger
quantity of leaves than nests exposed to the sun. Ants preferred certain tree species to others. The
authors pointed out that tolerance of tree species toward pest attacks needs to be included in the
characterization of species‟ suitability for tropical plantations (Folgarait et al 1996).184
180
Meyer S.T., et al. Persisting hyper-abundance of leaf-cutting ants (Atta spp.) at the edge of an old Atlantic
forest fragment. Biotropica 1 (online publ.) 1-6, 2009.
http://www3.interscience.wiley.com/journal/122457478/abstract
181
182
Blanton C.M., and Ewel J.J. Leaf-cutting ant herbivory in successional and agricultural tropical ecosystems.
Ecology 66(3), 1985. http://links.jstor.org/sici?sici=0012-9658(198506)66:3%3C861:LAHISA%3E2.0.CO;2-X#abstract
Rockwood L.L. Plant selection and foraging patterns in two species of leaf-eating ants (Atta). Ecology 57(1):
48-61, 1976. http://www.esajournals.org/perlserv/?request=get-abstract&doi=10.1043%2F00129658%281976%29057%5B0048%3APSAFPI%5D2.0.CO%3B2
183
Urbas P., Araújo Jr. M.V., Leal I.R., and Wirth R. Cutting more from cut forests: Edge effects on foraging
and herbivory of leaf-cutting ants in Brazil. Biotropica 39(4): 489–495, 2007. http://dx.doi.org/10.1111/j.17447429.2007.00285.x, http://www.blackwell-synergy.com/doi/abs/10.1111/j.1744-7429.2007.00285.x
184
Folgarait P.J., et al. Leaf-cutting ant preferences for five native tropical plantation tree species growing under
different light conditions. Entomologia Experimentalis et Applicata 80(3): 521-530, 1996.
http://www.springerlink.com/content/j2878307585j86k4/
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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 (SousaSouto et al 2007).190
185
186
187
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
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
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
190
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
Sousa-Souto L., et al. Leaf-cutting ants, seasonal burning and nutrient distribution in Cerrado vegetation.
Austral Ecology 32(7): 758-765, 2007. http://www.blackwell-synergy.com/doi/abs/10.1111/j.1442-9993.2007.01756.x
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In a Costa Rican wet forest, phosphorus cycling by leaf-cutting ants (Atta colombica) was found to
result in a slightly higher input of energy than the energy consumed by ants as biomass (Lugo et al
1973).191 In the Amazon, in the soil under nests of leaf-cutting ants (Atta sexdens), nitrate levels were
higher than in soil that was not influenced by the presence of ant nests. The authors suggested that
nitrate may have diffused from soil beneath the nests to the surrounding soil (Verchot et al 2003).192
In the US, defoliation in pine plantations by the Texas leaf-cutting ant was localized but occurred
annually on sites with deep, sandy soil. From year to year, ant populations remain relatively stable
(USDA 2004).193
191
192
193
Lugo A.E., et al. The impact of the leaf cutter ant Atta colombica on the energy flow of a tropical wet forest.
Ecology 54(6): 1292-1301, 1973. http://www.jstor.org/view/00129658/di960233/96p0208y/0
Verchot et al. Leaf-cutting ant (Atta Sexdens) and nutrient cycling: deep soil inorganic nitrogen stocks,
mineralization, and nitrification in Eastern Amazonia. Soil Biology and Biochemistry 35(9): 1219-1222,
2003. http://dx.doi.org/10.1016/S0038-0717(03)00183-4
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
Fernandes, Joao Batista. UFSCAR – Produtos Naturais.
http://dgp.cnpq.br/buscaoperacional/detalhegrupo.jsp?grupo=0335106CJGECN1
Controle de Formigas. http://www.bv.fapesp.br/projetos-tematicos/1944/controle-formigas-cortadeiras-estudos-integrados/
Forti, Luiz Carlos. UFJF; UNESP. http://dgp.cnpq.br/buscaoperacional/detalhepesq.jsp?pesq=6187684824965648UNESP
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
Interesse Agrossilvicultural. http://www.inpa.gov.br/colecoes/colecoes2.php
Laboratório de Entomolgia e Fitopatologia, UENF. http://www.uenf.br/Uenf/Pages/CCTA/LEF/
Laboratório de Insetos Sociais-Praga, UNESP. http://www.fca.unesp.br/lisp/
Leite, Helia Garcia. UFV – Inventário, Mensuração e Manejo Florestal.
http://dgp.cnpq.br/buscaoperacional/detalhegrupo.jsp?grupo=033650272DP0J0
Link, Dionisio. UFSM – Entomologia; controle integrado. http://www.ufsm.br/dfs/professor/link/link.htm
Loeck, Alci Enimar. UFPEL – Formigas Cortadeiras.
http://dgp.cnpq.br/buscaoperacional/detalhegrupo.jsp?grupo=0045501JCB22SZ
Lopes, Juliane Floriane Santos. UFJF – Ecologia e Comportamento de Formigas.
http://dgp.cnpq.br/buscaoperacional/detalhegrupo.jsp?grupo=080420447FO0AH
Moreira, Aldenise Alves. UESB. http://dgp.cnpq.br/buscaoperacional/detalhepesq.jsp?pesq=0353071359502148
Oliveira, Nádia Cristina. UNESP, UFMT. http://dgp.cnpq.br/buscaoperacional/detalhepesq.jsp?pesq=3317779428214532
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
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Bibliography of Publications on Leaf-Cutting Ants and Alternative Control Methods
Almado R.P. Manejo de formigas cortadeiras na Arcelormittal florestas. Revista O Biológico 69(supl. 2): p. 133,
2007. http://www.biologico.sp.gov.br/docs/bio/suplementos/v69_supl_2/p133.pdf
Almeida J.E.M., y Batista A. Filho. Banco de micorganismos entomopatogênicos: Biodiversidade para o
controle microbiana de pragas. Biotecnologia Ciência & Desenvolvimento no 20, maio/junho 2001.
http://pessoal.utfpr.edu.br/marlenesoares/arquivos/banco_MO.pdf
Agroecologia em Rede. Banco de Pesquisas. http://www.agroecologiaemrede.org.br/banco_pesquisas.php
Aguiar-Menezes E. de. Inseticidas botânicos: seus princípios ativos, modo de ação e uso agrícola. Embrapa
Agrobiologia 2005. http://www.cnpab.embrapa.br/publicacoes/download/doc205.pdf
Anjos N., et al. Árvores e formigas cortadeiras (Hymenoptera: Formicidae) em Viçosa, Minas Gerais. Revista
Trópica 1(2): 11-16, 2008. http://www.unilueneburg.de/umanagement/csm/content/naoek/downloads/downloads_publikationen/Anjos_et_al_2008_Revista_Tropica.pdf
Antunes E.C., and Lucia T.M.C. Consumo foliar em Eucalyptus urophylla por Acromyrmex laticeps
nigrosetosus (…). Ciência e Agrotecnologia 23(1): 208-211, 1999. http://www.editora.ufla.br/revista/23_1/art28.pdf
Araújo M.S., et al. Efeito da queima da palhada de cana-de-açúcar sobre comunidade de formicídeos. Ecología
Austral 14(2): 191-200, 2004. http://www.scielo.org.ar/pdf/ecoaus/v14n2/v14n2a10.pdf
Araújo M.S., et al. Foraging activity of Acromyrmex laticeps nigrosetosus (…) in Eucalyptus stands. Acta
Scientiarum 24(5): 1321-124, 2002. http://www.periodicos.uem.br/ojs/index.php/ActaSciAgron/article/view/2370/1785
Araújo M.S., and Della Lucia T.M.C. Characterization of Acromyrmex laticeps nigrosetosus Forel nests in
Eucalyptus stands in Paraopeba, MG. Anais da Sociedade Entomológica do Brasil 26(1): 205-207, 1997.
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Associação Brasileira Técnica de Celulose e Papel (ABTCP). Pinus Letter 3, 2008. http://www.celsofoelkel.com.br/pinus_03.html#cinco
Augustin J.O., and Santod Lopes J.F. The best founding strategy: Atta sexdens (…). Revista O Biológico
69(supl. 2): 385-387, 2007. http://www.biologico.sp.gov.br/docs/bio/suplementos/v69_supl_2/p385-387.pdf
Azevedo C.P. Simulação de estratégias de manejo florestal na Amazônia com o uso do modelo SYMFOR.
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Baer B., et al.Examination of the immune responses of males and workers of the leaf-cutting ant Acromyrmex
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http://www.springerlink.com/content/qq06076546j66g43/
Ballari S.A., and Farji-Brener A.G. Refuse dumps of leaf-cutting ants as a deterrent for ant herbivory: does
refuse age matter? Entomologia Experimentalis et Applicata 121(3), 215–219, 2006. http://www.blackwellsynergy.com/doi/abs/10.1111/j.1570-8703.2006.00475.x
Bansho J.Y., et al. Controle de formigas cortadeiras na KFPC – PR. IPEF, 1994.
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Barata G. Avanços no conhecimento não impedem dificuldades no controle das cortadeiras. Notícias do Brasil
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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
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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.
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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
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sexdens rubropilosa Forel (Hymenoptera, Formicidae). Revista Brasileira de Entomologia 52(2): 300-302, 2008.
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Bragança M.A.L., et al. Influência do tamanho das operárias de Atta sexdens rubropilosa (Hym.: Formicidae)
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Bragança M.A.L., et al. First record of phorid parasitoids (Diptera: Phoridae) of the leaf-cutting ant Atta
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Tese Dout. UFGD 2008. http://www.ufgd.edu.br/fcba/mestrado-entomologia-conservacao-biodiversidade/dissertacoes-defendidas/
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hormiga cortadora Acromyrmex lundi (Guérin). UNSAM 2002.
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Caldeira M.A., et al. Distribuiçop espacial de sauveiros (Hymenoptera: Formicidae) em Eucaliptais. CERNE
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Camargo R.S., et al. Characterization of Acromyrmex subterraneus brunneus (…) young nests in a fragment of
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the Neotropical Forest. Revista Árvore 28(2), 2004. http://www.scielo.br/pdf/rarv/v28n2/20993.pdf
Cantarelli E.B. Silvicultura de precisão no monitoramento e controle de formigas cortadeiras em plantios de
Pinus. UFSM 2005. http://cascavel.cpd.ufsm.br/tede/tde_busca/arquivo.php?codArquivo=756
Cantarelli E.B. Referências bibliográficas. 2007. http://cascavel.cpd.ufsm.br/tede/tde_busca/arquivo.php?codArquivo=757
Carlos A.A., et al. Atratividade de diferentes polpas cítricas para Atta sexdens rubropilosa. Revista O Biológico
69(supl. 2): 369-370, 2007. http://www.biologico.sp.gov.br/docs/bio/suplementos/v69_supl_2/p369-370.pdf
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Zanetti R., et al. Eficiência de produtos termonebulígenos no controle de Atta laevigata (…) em plantio de
eucalipto. Ciência e Agrotecnologia 34(4), 2008. http://dx.doi.org/10.1590/S1413-70542008000400043
Zanetti R. Manejo integrado de formigas cortadeiras e cupins em áreas de eucalipto da Cenibra. UFLA 2007.
http://www.cenibra.com.br/pdf/LaudoFSC-Cenibra.pdf
Zanetti R. Monitoramento de formigas cortadeiras (Hym.: 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
Zanetti R. Manejo integrado de formigas cortadeiras. Manejo Integrado de Pragas Florestais, UFLA 2006.
http://www.den.ufla.br/Professores/Ronald/Disciplinas/Notas%20Aula/MIPFlorestas%20formigas.pdf
Zanetti R. Métodos de controle usados no MIP. Manejo Integrado de Pragas Florestais, UFLA 2006.
http://www.den.ufla.br/Professores/Ronald/Disciplinas/Notas%20Aula/MIPFlorestas%20controle.pdf
Zanetti R. Pragas de viveiros florestais. Manejo Integrado de Pragas Florestais, UFLA 2006.
http://www.den.ufla.br/Professores/Ronald/Disciplinas/Notas%20Aula/MIPFlorestas%20viveiros.pdf
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Zanetti R. Conceitos usados no MIP e componentes do MIP. Manejo Integrado de Pragas Florestais, UFLA
2006. http://www.den.ufla.br/Professores/Ronald/Disciplinas/Notas%20Aula/MIPFlorestas%20conceitos%20mip.pdf
Zanetti R. Amostragem de insetos em florestas. Manejo Integrado de Pragas Florestais, UFLA 2005.
http://www.den.ufla.br/Professores/Ronald/Disciplinas/Notas%20Aula/MIPFlorestas%20amostragem.pdf
Zanetti R, y Zanuncio J.C. Monitoramento de formigas cortadeiras em florestas cultivadas no Brasil. Plagas
Forestales Neotropicales 17, 2005. http://web.catie.ac.cr/informacion/RMIP/rev75/BoletinPlagasForestales.pdf
Zanetti R., et al. Level of Economic Damage for Leaf-Cutting Ants (Hymenoptera: Formicidae) in Eucalyptus
Plantations in Brazil. Sociobiology 42(2), 2003.
http://www.csuchico.edu/biol/Sociobiology/volume/sociobiologyv42n22003.html#18
Zanetti R., et al. Efeito da densidade e do tamanho de sauveiros sobre a produção de madeira em eucaliptais.
Anais da Sociedade Entomológica do Brasil 29(1), 2000. http://www.scielo.br/pdf/aseb/v29n1/v29n1a13.pdf
Zanetti R., et al. Influência da espécie cultivada e da vegetação nativa circundante na densidade de sauveiros em
eucaliptais. Pesquisa Agropecuária Brasileira 35(10), 2000. http://www.scielo.br/pdf/pab/v35n10/35n10a01.pdf
Zanuncio JC, da Cruz AP, Oliveira HN, Gomes FS. Controle de Acromyrmex laticeps nigrosetosus (…), em
Eucaliptal no Pará, com iscas granuladas com sulfuramida ou clorpirifós. Acta Amazonica 29(4), 1999.
http://acta.inpa.gov.br/fasciculos/29-4/PDF/v29n4a14.pdf
Zanuncio R, et al. Uso da isca granulada com sulfluramida 0,3 %, no controle de Atta sexdens rubropilosa Forel,
1908 (Hymenoptera: Formicidae). Revista 3(1), 1997. http://www.dcf.ufla.br/Cerne/revistav3n1-1997/SAUVA1.PDF
Zarzuela M.F.M. Utilização de entomoatógenos para o controle de formigas. Revista O Biológico 69(2): 157160, 2007. http://www.biologico.sp.gov.br/docs/bio/suplementos/v69_supl_2/p157-160.pdf
Zeh J.A., Zen A.D., and Zeh D.W. Dump material as an effective small-scale deterrent to herbivory by Atta
cephalotes. Biotropica 31 (2): 368–371, 1999. http://www.blackwell-synergy.com/doi/abs/10.1111/j.1744-7429.1999.tb00149.x
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Annex III Toxicologic and Environmental Properties of Active Ingredients
1.
2.
3.
4.
5.
Cypermethrin, alpha-Cypermethrin, and zeta-Cypermethrin
Deltamethrin
Fenitrothion
Fipronil
Sulfluramid
- Environmental Fate of Sulfluramid and its Metabolites
- Additional Publications on Sulfluramid, Metabolites, and Perfluorinated Compounds
1. Cypermethrin, alpha-Cypermethrin, and zeta-Cypermethrin
Active ingredient
alpha-Cypermethrin (CAS no. 67375-30-8), racemic (1:1) mixture of one R isomer
and one S isomer (source: Pesticide Manual (PM) 2006)194
Active ingredient „Cypermethrin‟, beta- or zeta-Cypermethrin (CAS no. 52315-07-8): „Cypermethrin‟
consists of 8 different isomers with the same chemical formula but with a different
molecular structure (Khambay 2002);195 purity is 90% (PM)
beta-Cypermethrin: reaction mixture containing two pairs of isomers (four isomers
in total) in ratio 2:3, technical purity is >95% and normally >97% (PM)
zeta-Cypermethrin: mixture enriched with certain isomers (PM); enriched in S
isomers (US EPA 2008)196
Chemical class
Pyrethroid (a synthetic derivative of pyrethrum)
Regulation (USA) „Cypermethrin‟ is a Restricted Use Pesticide (US EPA 2008)
Use type
Insecticide (liquid formulation), with contact and stomach action
Usage
Control of Coleoptera, Lepidoptera, and other pest insects (PM)
Acute toxicity
„Cypermethrin‟, alpha- and beta-Cypermethrin:
In WHO class II („Moderately hazardous‟)
In US EPA's Toxicity Category II (label reads „Warning‟) (US EPA 2008)
zeta-Cypermethrin: in WHO class Ib („Highly hazardous‟); the acute toxicity of
(PM): Tomlin C. The Pesticide Manual. 14th edition, British Crop Protection Council 2006
195
Khambay B. Pyrethroid insecticides. Pesticide Outlook 13: 49-54, 2002.
194
http://www.rsc.org/publishing/journals/PO/article.asp?doi=b202996k
196
US Environmental Protection Agency (EPA). Reregistration Eligibility Decision for Cypermethrin.
Washington D.C. 2008. http://www.epa.gov/oppsrrd1/REDs/cypermethrin_revised_red.pdf
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different forms of Cypermethrin varies with the isomers present (WHO 2006).197
EU classification alpha-Cypermethrin: Toxic if swallowed; irritating to respiratory system; harmful:
danger of serious damage to health by prolonged exposure if swallowed; Very toxic
to aquatic organisms, may cause long-term adverse effects in the aquatic environment (Source: European Chemicals Bureau (ECB) 2009).198
beta-Cypermethrin: Harmful by inhalation and if swallowed; irritating to respiratory
system; Very toxic to aquatic organisms, may cause long-term adverse effects in the
aquatic environment (ECB).
Aquatic toxicity
All forms of Cypermethrin are very highly toxic to fish. It is asserted that the toxic
effects are not observed under field conditions due to rapid loss from water (PM).
alpha-Cypermethrin: LC50 (96 h) 0.0028 mg/L for rainbow trout;
beta-Cypermethrin: 0.028 mg/L for carp, 0.015 mg/L for catfish;
zeta-Cypermethrin: 0.00069-0.0027 mg/L depending on species;
„Cypermethrin‟: 0.00069 mg/L for rainbow trout (PM).
Very highly toxic to daphnia, lethal concentration LC50 (48 h) ranges from 0.0001 to
0.0003 mg/L (PM).
Bird toxicity
Low toxicity to birds; alpha-Cypermethrin: Acute oral LD50 (dose per kg body
weight): >2025 mg/kg for bobwhite quail;
beta-Cypermethrin: 3515 mg of 5% formulation/kg for pheasants;
zeta-Cypermethrin: >10248 mg/kg for ducks;
„Cypermethrin‟: >2000 mg/kg for chickens (PM).
Ecotoxicity
The EPA‟s Levels of Concern (LOCs) are exceeded for aquatic organisms exposed
to Cypermethrin (e.g. through spray drift, run-off, etc). Acute LOCs are exceeded
for endangered species of small mammals feeding on grass and the chronic LOC is
also mostly exceeded (US EPA 2008).
Bee toxicity
Toxic to bees (PM); toxic to beneficial insects (US EPA 2008)
Bioconcentration Factor (BCF)
197
198
„Cypermethrin‟: BCF = 1204, the calculated bioaccumulation
World Health Organization. The WHO recommended classification of pesticides by hazard 2004. Geneva
2005, amended in 2006 (see note 9 on p. 7) http://www.who.int/ipcs/publications/pesticides_hazard/en/
European Chemicals Bureau (ECB), Directive 67/548/EEC on Classification & Labelling of Dangerous
Substances (search Annex I), Rome 2009, http://ecb.jrc.it/classification-labelling/search-classlab/
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potential is high (Footprint 2009);199
log(BCF) value is 2.89-2.92 for salmon (Mackay et al 2006)200
Octanol-water partition coefficient High, alpha-Cypermethrin: logKow 6.94;
beta-Cypermethrin: logKow 4.7;
„Cypermethrin‟: logKow 6.6 (PM)
Degradation half-life alpha-Cypermethrin: c. 13 weeks in loamy soil (PM); 35 days
(moderately persistent), range 14-112 days (Footprint 2009)
beta-Cypermethrin: 10 days (PM); zeta-Cypermethrin: 14-28 days
„Cypermethrin‟: 60 days (PM); 30 days (field) (Mackay et al 2006)
Water solubility
Low, alpha-Cypermethrin: 0.00397 mg/L at pH 7, 20°C (PM)
beta-Cypermethrin: 0.0934 mg/L at pH 7, 25°C (PM)
zeta-Cypermethrin: 0.045 mg/L at 25°C
„Cypermethrin‟: 0.004 mg/L at pH 7 (PM)
Soil sorption
Adsorbs strongly to soil; zeta-Cypermethrin: soil sorption coeffic. Koc > 11'542
„Cypermethrin‟: Koc > 26'492 (PM)
Cancer rating
„Cypermethrin‟, zeta-cypermethrin: Group C, „Possible Human Carcinogen‟ (US
EPA 2008; see footnote 16 above)
Endocrine disruption „Cypermethrin‟ is listed in Category 2 for endocrine disruption of the EU:
“Substances with potential evidence on endocrine disruption” (EC 2004)201
Acute poisonings
199
Treatment of severe poisoning with pyrethroids (such as Cypermethrin) is
difficult (Ray 2000).202 Chronic effects following an incident of systemic
(Footprint 2009): The FOOTPRINT Pesticides Properties Database. Database collated by the University of
Hertfordshire as part of the EU-funded FOOTPRINT project (search database for chemical), updated in 2009.
http://www.herts.ac.uk/aeru/footprint/en/
200
201
Mackay D, Shiu WY, and Ma KC, Handbook of physical-chemical properties and environmental fate for
organic chemicals, Volume 4, Boca Raton, Florida: CRC Press 2006
European Commission (EC). Commission Staff Working Document SEC(2004)1372 on the implementation
of the Community Strategy for Endocrine Disrupters – a range of substances suspected of interfering with the
hormone systems of humans and wildlife. Brussels 2004.
http://ec.europa.eu/environment/endocrine/documents/sec_2004_1372_en.htm
202
Ray DE, and Forshaw PJ, Pyrethroid insecticides: poisoning syndromes, synergies, and therapy, Journal of
Toxicology and Clinical Toxicology 38(2): 95-101, 2000,
http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=pubmed&dopt=Abstract&list_uids=10778904
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(acute) poisoning with pyrethroids frequently last more than two years (MullerMohnssen 1999).203
2. Deltamethrin
Active ingredient
Chemical class
Use type
Deltamethrin (CAS no. 52918-63-5)
Pyrethroid (a synthetic derivative of pyrethrum)
Insecticide (liquid formulation)
Acute toxicity
In WHO class II („Moderately hazardous‟) (WHO 2006)197
In US EPA's Toxicity Category II (label reads „Warning‟) (source: Pesticide
Manual (PM) 2006)194
EU classification
Toxic by inhalation and if swallowed; Very toxic to aquatic organisms, may
cause long-term adverse effects in the aquatic environment (European Chemicals
Bureau 2009)198
Aquatic toxicity
Very highly toxic to fish; Toxic to fish under laboratory conditions; not toxic to
fish under natural conditions; LC50 (96 h) 0.0014 mg/L for bluegill sunfish;
0.00091 mg/L for rainbow trout (PM)
Very highly toxic to daphnia, LC50 0.0035 mg/L (PM)
Bird toxicity
Low toxicity to birds, LD50 > 4640 mg/kg for mallard ducks (PM)
Bee toxicity
Toxic to bees, LD50 (oral) 0.079 μg per bee, (contact) 0.051 μg per bee (PM)
Bioconcentration Factor (BCF) BCF = 1400, threshold for concern, potential to bioaccumulate
(Footprint 2009)
logBCF = 2.62 for rainbow trout (Mackay et al 2006)200
Octanol-water partition coefficient High, logKow 4.6 (PM)
Degradation half-life
13 days, 21 days (field), non-persistent (Footprint 2009)199
Water solubility
Low, < 0.002 mg/L at 20°C (Mackay et al 2006)
Soil sorption coefficient
Strongly adsorption by soil colloids, Koc > 460‟000 (PM)
203
Muller-Mohnssen H, Chronic sequelae and irreversible injuries following acute pyrethroid intoxication,
Toxicology Letters 107(1-3): 161-176, 1999,
http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=pubmed&dopt=Abstract&list_uids=10414793
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Cancer rating
Unclassifiable (Group 3, IARC)204
Not likely (US EPA) (Pesticides Database, http://www.pesticideinfo.org)
Endocrine disruption
Listed in Category 1 for endocrine disruption of the EU:201 “At least one
study providing evidence of endocrine disruption in an intact organism”
Classified as endocrine disrupting chemical (Bila & Dezotti 2007).205
3. Fenitrothion
Active ingredient
Fenitrothion (CAS no. 122-14-5)
Chemical class
Organophosphate (organophosphorus ester)
Use type
Non-systemic insecticide/acaricide, with contact and stomach action;
acetylcholinesterase inhibitor (toxic to the nervous system) (PM)194
Usage
Control of a broad spectrum of insects in agriculture or forestry, including
cockroaches and locusts (PM)
Acute toxicity
In WHO class II („Moderately hazardous‟) (WHO 2006)197
In US EPA Toxicity Category II (label reads „Warning‟) (US EPA 1995; 2006)206
EU classification
Harmful if swallowed; Very toxic to aquatic organisms, may cause long-term
adverse effects in the aquatic environment (European Chemicals Bureau 2009)198
Aquatic toxicity
Moderately toxic to fish: LC50 (96 h) is 2.5 mg/L for bluegill sunfish; 1.3 mg/L for
rainbow trout (PM)
Very highly toxic to daphnia: EC50 (48 h) 0.0026 mg/L (PM)
Bird toxicity
Highly toxic to birds species: LD50 is 23.6 mg/kg for bobwhite quail; 1190 mg/kg
for mallard duck (PM); 2.3 mg/kg for pheasants (Footprint 2009)199
Bee toxicity
Toxic to bees; highly toxic to non-target arthropods (PM)
204
205
206
International Agency for Research on Cancer (IARC), Overall Evaluations of Carcinogenicity to Humans,
Lyon 2007, http://monographs.iarc.fr/ENG/Classification/crthalllist.php
Bila D.M., and Dezotti M. Desreguladores endócrinos no meio ambiente: efeitos e consequências. Química
Nova 30(3), 2007. http://quimicanova.sbq.org.br/qn/qnol/2007/vol30n3/26-RV06127.pdf
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
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Bioconcentration Factor (BCF)
BCF = 29, calculated potential to bioaccumulate is low (Footprint
2009)
Octanol-water partition coefficient High, logKow 3.43 (at 20°C) (PM)
Degradation half-life (soil) 12-28 days (upland), 4-20 days (under submerged conditions) (PM)
2.7 days, non-persistent (Footprint 2009)
Metabolites
3-methyl-4-nitrophenol (major metabolite); aminofenitrothion (submerged)
Degradation half-life (water) Relatively stable in water; hydrolysis half-life 84.3 days (at pH 7) (PM)
Water solubility
Low: 19 mg/L at 20°C (Footprint 2009)199
Soil sorption coefficient
Moderately mobile: KOC 322; low potential to leach (Footprint 2009)
Cancer rating
Group E – evidence of noncarcinogenicity for humans (US EPA 1995)206
Endocrine disruption
Listed in Category 1 for endocrine disruption of the EU:201 “At least one
study providing evidence of endocrine disruption in an intact organism”
4. Fipronil
Active ingredient
Fipronil (CAS no. 120068-37-3)
Chemical class
Phenylpyrazole
Use type
Insecticide with contact and stomach action (PM); GABA-gated chloride channel
antagonist (affects the nervous system) (Footprint 2009)
Usage
Control of a broad spectrum of insects; applied to foliage or soil, or used for seed
treatment (PM)
Acute toxicity
In WHO class II („Moderately hazardous‟) (WHO 2006)197
In US EPA Toxicity Category II (label reads „Warning‟) (source: PM)194
EU classification
Toxic by inhalation, in contact with skin and if swallowed; Toxic: danger of
serious damage to health by prolonged exposure if swallowed; Very toxic to
aquatic organisms, may cause long-term adverse effects in the aquatic
environment (European Chemicals Bureau 2009)198
Aquatic toxicity
Highly toxic to fish: LC50 (96 h) is 0.085 mg/L for bluegill sunfish; 0.248 mg/L
for rainbow trout; 0.43 mg/L for carp (PM)
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Moderately toxic to daphnia: LC50 is 0.19 mg/L for Daphnia magna; 3.8 mg/L
for D. carinata (PM)
Bird toxicity
Moderately toxic to highly toxic to bird species: LD50 is 11.3 mg/kg for bobwhite
quail; pheasant 31 mg/kg; partridge 34 mg/kg; > 2000 mg/kg mallard duck;
dietary LC50 (5 days) for bobwhite quail is 49 mg/kg diet; mallard duck > 5000
mg/kg diet (PM)
Low toxicity to bird species: LD50 is 4733 mg/kg (Footprint 2009)199
Bee toxicity
Highly toxic to bees, by contact and ingestion (PM)
Bioconcentration Factor (BCF)
BCF = 321, threshold for concern, calculated potential to bioaccumulate is moderate (Footprint 2009)
Octanol-water partition coefficient High: logKOW 4.0 (PM); logKOW 3.75 (Footprint 2009)
Degradation half-life 142 days (laboratory, 20°C, range: 32-346 days), 65 days (field, 5.6-135 days),
(soil)
persistent to moderately persistent (Footprint 2009)
Metabolites
Fipronil amide, fipronil sulfone, fipronil sulfide (Footprint 2009)
Degradation (water) Stable in water at pH 5 and pH 7, slowly hydrolysed at pH 9, hydrolysis half-life
28 days (PM)
Water solubility
Low: 1.9 mg/L (pH 5), 2.4 mg/L (pH 9) at 20°C (PM)19
Soil sorption coefficient
Low leaching potential: KOC 427-1248 ml/g (PM)
Slightly mobile: KOC 577 ml/g (Footprint 2009)
Cancer rating
Possible carcinogen (US EPA) (PANNA 2008)207
Endocrine disruption
Among substances classified as High Production Volume and/or
persistent and/or exposure expected in humans and wildlife, with
insufficient data (38 substances) (EC 2004)201
Suspected endocrine disruptor (Colborn et al 1996; Colborn et al 1993)208
207
208
PAN North America (PANNA). Pesticides Database (search for chemical name). http://www.pesticideinfo.org
Colborn T., et al. Our stolen future: Wide-spread pollutants with endocrine disrupting effects: Pesticide. New
York 1996. http://www.ourstolenfuture.org/Basics/chemlist.htm
Colborn T., et al. Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environmental Health Perspectives, 101: 378-384, 1993. http://www.ehponline.org/members/1993/101-5/colborn-full.html
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5. Sulfluramid
Active ingredient
Chemical class
Chemical name
Other names
Use type
Usage
Sulfluramid (CAS no. 4151-50-2)
Fluorinated sulfonamide
N-ethylperfluoro-octan-1-sulfonamide
Ethyl perfluorooctylsulphonamide, GX-071 (HB), GX-439
Insecticide with stomach action (Footprint 2009)
Control of ants and cockroaches (PM); termites (CDPR 2007)209
Acute toxicity
WHO class III („Slightly Hazardous‟) (WHO 2006)197
US EPA category III (label reads „Caution‟) (PM)194
Aquatic toxicity
Moderately toxic to highly toxic to fish, based on rating by Kamrin (1997)210
Lethal concentration LC50 (96 h) is 9.9 mg/L for rainbow trout, 7.99 mg/L
rainbow trout (PM); 9.92 mg/L for rainbow trout (renewal), 0.21 mg/L rainbow
trout (static), 0.189 mg/L fathead minnow (renewal) (PANNA 2008)207
Daphnia toxicity
LC50 (48h) 0.39 mg/L (PM)
Bird toxicity
Highly toxic to birds. Acute oral LD50 (dose per kg body weight): 45 mg/kg for
bobwhite quail; Dietary LC50 (8 days feeding study, dose per kg diet): 300 mg/kg
(ppm) for bobwhite quail, 165 ppm mallard duck (PM)
Bioconcentration Factor (BCF)
BCF = 500, threshold for concern (or risk); calculated potential for
bioaccumulation is moderate (Footprint 2009).
According to Franke et al (1994), a BCF of 500 indicates a high
potential for bioaccumulation in fish (HSDB 2003).210
(Exposure of fish to sulfluramid is expected to be generally very
low due to extremely low water solubility.)
Octanol-water partition coefficient Very high: logKOW > 6.8 (unionised) (BCPC 2006/2007)
High: logKOW 3.1 (Footprint 2009)
Degradation half-life (soil) Has not been shown to undergo further transformation; is converted to
highly recalcitrant/persistant perfluorooctanesulfonic acid (Key et al
1997).211
209
California Department of Pesticide Regulation (CDPR). Databases: Chemical ingredients.
http://www.cdpr.ca.gov/dprdatabase.htm
210
210
Kamrin A. Pesticide profiles: Toxicity, environmental impact, and fate. Boca Raton, Florida 1997
Franke C., et al. The assessment of bioaccumulation. Chemosphere 29(7): 1501-14, 1994.
http://dx.doi.org/10.1016/0045-6535(94)90281-X
211
Key B.D., Howell R.D., and Criddle C.S. Fluorinated organics in the biosphere. Environmental Science and
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Metabolites
Perfluorooctanesulfonamide, perfluorooctanesulfonic acid (perfluorooctanesulfonate) (Key et al 1997)
Main metabolite perfluorooctanesulfonate has a high potential to bioaccumulate:
bioconcentration factor BCF for bluegill sunfish is 2796 (3M 2002).212
BCF for rainbow trout is 2900-3100 (Martin et al 2003)213
Higher concentrations of PFOA and PFOS in blood serum were associated with a
higher prevalence of thyroid disease among the general adult population in the
USA (Melzer et al 2010, see additional publications below).
Water solubility
Insoluble (25°C) (PM); Very low: 0.0001 mg/L (at 20°C) (Footprint 2009)
Soil sorption coefficient Non-mobile: KOC 3'500'000 ml/g (Footprint 2009); immobile (class 1) in
brake/Quartz sand, purple latosol and medium dark red latosol, totally mobile
(class 5) in Quartz sand with low organic matter content (CENA (no year))214
Cancer rating
Not listed/reported
Endocrine disruption:- Sulfluramid: not listed/reported
- Perfluorooctanesulfonate: Suspected endocrine disruptor (Colborn et al
1996)215
212
213
Technology 31(9): 2445-2454, 1997. http://www.stanford.edu/group/evpilot/pdf/es961007c%202.pdf (p. 2450)
3M, 2002. Final report, perfluorooctanesulfonate, potassium salt (PFOS): A flow-through bioconcentration
test with bluegill (Lepomis macrochirus). Project Number 454A-134. Studyconducted for 3M. Wildlife
International Ltd., St. Paul, MN. (Reference quoted by UNEP 2006)
Martin J.W., et al. Bioconcentration and tissue distribution of perfluorinated acids in rainbow trout
(Oncorhynchus mykiss). Environmental Toxicology and Chemistry 22 (1): 196-204, 2003.
http://www.setacjournals.org/perlserv/?request=get-abstract&doi=10.1897%2F15515028%282003%29022%3C0196%3ABATDOP%3E2.0.CO%3B2
214
215
Centro de Energia Nuclear na Agricultura (CENA), Univ. SP. In: UNEP (2008): Toxicological summary for
sulfluramid. http://chm.pops.int/Portals/0/Repository/addinfo_2008/UNEP-POPS-POPRC-SUB-F08-PFOS-LEAF14.English.pdf
Colborn T., et al. Our stolen future: Wide-spread pollutants with endocrine disrupting effects: Other
compounds. New York 1996. http://www.ourstolenfuture.org/Basics/chemlist.htm
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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.
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