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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil Recommendations by Technical Advisors March 2010 1 Recommendations regarding Derogations to use alpha- Cypermethrin, Deltamethrin, Fenitrothion, Fipronil and Sulfluramid in FSC Certified Forests in Brazil Richard Isenring, Lars Neumeister September 2009, amended in March 2010 Contents 1. Scope 2. Recommendations I. Control of Leaf-Cutting Ants 1.1 Demonstrated Need for Insecticide Use 1.2 Risk Mitigation for Insecticide Use 1.3 Alternatives for Control of Leaf-Cutting Ants 1.4 Stakeholder Opinions on Insecticide Use 1.5 Conclusions II. Coleopteran Defoliating Insects (Costalimaita ferruginea) III. Lepidopteran Defoliating Insects (Thyrinteina arnobia) IV. Termites (Preventive Treatment) Annex I Studies on Herbivory of Leaf-Cutting Ants Annex II Research and Bibliography on Leaf-Cutting Ants Annex III Toxicologic and Environmental Properties of Active Ingredients Technical Advisors to the FSC Pesticides Committee Lars Neumeister (Dipl. Ing. Land Usage & Nature Protection) Fürstenwerder, Germany. Email: [email protected] , Website: www.pestizidexperte.de Richard Isenring (M.Sc. in Chemistry, MGU Certificate / Environmental Studies) Basel, Switzerland. Email: [email protected]

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Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors

March 2010 1

Recommendations regarding Derogations to use alpha-Cypermethrin, Deltamethrin, Fenitrothion, Fipronil and Sulfluramid in FSC Certified Forests in Brazil

Richard Isenring, Lars Neumeister

September 2009, amended in March 2010

Contents

1. Scope

2. Recommendations

I. Control of Leaf-Cutting Ants 1.1 Demonstrated Need for Insecticide Use

1.2 Risk Mitigation for Insecticide Use

1.3 Alternatives for Control of Leaf-Cutting Ants

1.4 Stakeholder Opinions on Insecticide Use

1.5 Conclusions

II. Coleopteran Defoliating Insects (Costalimaita ferruginea)

III. Lepidopteran Defoliating Insects (Thyrinteina arnobia)

IV. Termites (Preventive Treatment)

Annex I Studies on Herbivory of Leaf-Cutting Ants

Annex II Research and Bibliography on Leaf-Cutting Ants

Annex III Toxicologic and Environmental Properties of Active Ingredients

Technical Advisors to the FSC Pesticides Committee

Lars Neumeister (Dipl. Ing. Land Usage & Nature Protection)

Fürstenwerder, Germany. Email: [email protected], Website: www.pestizidexperte.de

Richard Isenring (M.Sc. in Chemistry, MGU Certificate / Environmental Studies)

Basel, Switzerland. Email: [email protected]

Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors

March 2010 2

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 leaf-

cutting 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)

A.W. Faber-Castell S.A. SCS-FM/COC-00081P Fipronil

* (dispersible granules) Sulfluramid (granular baits)

Adami S/A. Madeiras, South Brazil SW-FM/COC – 002665

Deltamethrin (dust)

Fipronil (granular baits)

Sulfluramid (granular baits)

Agro-Florestal Motrisa Ltda., South Brazil SW-FM/COC-1808 Sulfluramid (granular baits)

Amapá Florestal e Celulose Ltda – Amcel SCS-FM/COC-000114P Fenitrothion (liquid)

Sulfluramid (granular baits)

Amata S/A. – Unidade Castanhal, Pará Candidate FMO (SW) Sulfluramid (granular baits)

Aracruz Celulose S/A Candidate FMO

(undefined CB)

Deltamethrin (liquid)

Fipronil (dispersible granules)

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)

ARAUPEL S/A (com COC serraria) SW-FM/COC-180

Deltamethrin (liquid)

Fipronil (dispersible granules)

Sulfluramid (granular baits)

ArcelorMittal Energética Jequitinhonha

Ltda (formerly Acesita Energética Ltda.) SGS-FM/COC-004161

alpha-Cypermethrin (liquid)

Deltamethrin (dust)

Deltamethrin (liquid)

Fipronil (dispersible granules)

Sulfluramid (granular baits)

ArcelorMittal Florestas Ltda. (formerly CAF Santa Bárbara Ltda.)

SGS-FM/COC-1943

alpha-Cypermethrin (liquid)

Deltamethrin (dust)

Deltamethrin (liquid)

Fenitrothion (liquid)

Fipronil (dispersible granules)

Sulfluramid (granular baits)

Battistella Florestal, Unidade Lages, S. BR Candidate FMO (SW) Sulfluramid (granular baits)

*Application withdrawn in 2009

Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors

March 2010 3

Battistella Florestal, Unidade Rio Negrinho,

South Brazil (formerly Mobasa, South BR) SW-FM/COC-1070

Fipronil (granular baits)

Sulfluramid (granular baits)

Caceres Florestal S.A. SCS-FM/COC-091P Sulfluramid (granular baits)

CAXUANA Reflorestamento S/A (com

COC serraria) SW-FM/COC-215

Deltamethrin (dust)

Fenitrothion (liquid)

Fipronil (dispersible granules)

Sulfluramid (granular baits)

Celulose Irani S/A., South Brazil Candidate FMO (SW)

Deltamethrin (dust)

Fipronil (dispersible granules)

Sulfluramid (granular baits)

Cenibra – Celulose Nipo-Brasileira S.A. SGS-FM/COC-2167

Deltamethrin (liquid)

Fipronil (dispersible granules)

Sulfluramid (granular baits)

Conpacel – Consórcio Paulista de Papel e

Celulose (formerly Ripasa S.A. Celulose e

Papel)

SCS-FM/COC-00076P

alpha-Cypermethrin (liquid)

Deltamethrin (liquid)

Fenitrothion (liquid)

Fipronil (dispersible granules)

Sulfluramid (granular baits)

Duratex S.A. SCS-FM/COC-00029P

alpha-Cypermethrin (liquid)

Deltamethrin (dust)

Deltamethrin (liquid)

Fenitrothion (liquid)

Fipronil (dispersible granules)

Sulfluramid (granular baits)

Eucatex S.A. Ind. E Com. SCS-FM/COC-00040P

alpha-Cypermethrin (liquid)

Deltamethrin (liquid)

Fipronil (dispersible granules)

Sulfluramid (granular baits)

Florestal Vale do Corisco, Ltda. SCS-FM/COC-00038P Deltamethrin (dust)

Sulfluramid (granular baits)

Floresteca Agro Florestal Ltda. SGS-FM/COC-0079

Deltamethrin (dust)

Deltamethrin (liquid)

Sulfluramid (granular baits)

Flosul Indústria e Comercio de Madeiras

Ltda., South Brazil SW-FM/COC-087 Sulfluramid (granular baits)

Grim – Grupo de Reflorestadores do Imbaú,

South Brazil SW-FM/COC-1820 Sulflurarnid (granular baits)

Jari Celulose S.A. SCS-FM/COC-00077P

Deltamethrin (liquid)

Fenitrothion

Sulfluramid (granular baits)

José Ailton Thomaz, Bahia (south) Candidate FMO

(undefined CB)

Deltamethrin (dust)

Deltamethrin (liquid)

Fipronil (dispersible granules)

Sulfluramid (granular baits)

Juliana Florestal Ltda., South Brazil SW-FM/COC-130 Sulfluramid (granular baits)

Jurandir de Souza Boa Morte, Bahia (south) Candidate FMO

(undefined CB)

Deltamethrin (dust)

Deltamethrin (liquid)

Fipronil (dispersible granules)

Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors

March 2010 4

Sulfluramid (granular baits)

KLABIN S/A - ANGATUBA Candidate FMO (SW)

Deltamethrin (dust)

Deltamethrin (liquid)

Fenitrothion (liquid)

Fipronil (dispersible granules)

Sulfluramid (granular baits)

KLABIN S/A - PARANÁ (com PFNM) SW-FM/COC-NTFP

038

Deltamethrin (dust)

Deltamethrin (liquid)

Fenitrothion

Fipronil (dispersible granules)

Sulfluramid (granular baits)

KLABIN S/A - SANTA CATARINA (com

COC serraria) SW-FM/COC-1301

Deltamethrin (dust)

Deltamethrin (liquid)

Fenitrothion (liquid)

Fipronil (dispersible granules)

Sulfluramid (granular baits)

Lwarcel Celulose e Papel Ltda. SCS-FM/COC-0093P

alpha-Cypermethrin (liquid)

Deltamethrin (dust)

Deltamethrin (liquid)

Fenitrothion (liquid)

Fipronil (dispersible granules)

Sulfluramid (granular baits)

Madecal Agro-Industrial Ltda, South Brazil SW-FM/COC-000205 Fipronil (granular baits)

Sulfluramid (granular baits)

Madepar Indústria e Comércio de Madeiras

Ltda., South Brazil SCS-FM/COC-00048P

Fipronil (granular baits)

Sulfluramid (granular baits)

MASISA do Brasil Ltda. SW-FM/COC-1531

Deltamethrin (dust)

Deltamethrin (liquid)

Sulfluramid (granular baits)

Norske Skog Florestal Ltda. Candidate FMO (SCS) Deltamethrin (dust)

Sulfluramid (granular baits)

Ouro Verde Agrosilvopastoril Ltda. Candidate FMO (CB?) Sulfluramid (granular baits)

Plantar S.A. SCS-FM/COC-00057P

Deltamethrin (dust)

Deltamethrin (liquid)

Fenitrothion (liquid)

Fipronil (dispersible granules)

Sulfluramid (granular baits)

Reflorestadora Sincol Ltda., South Brazil SW-FM/COC-001135

Deltamethrin (dust)

Fipronil (granular baits)

Sulfluramid (granular baits)

Renova Floresta Ltda., South Brazil SW-FM/COC-1777 Fipronil (granular baits)

Sulfluramid (granular baits)

SATIPEL Florestal SW-FM/COC-1409

Deltamethrin (dust)

Deltamethrin (liquid)

Fipronil (dispersible granules)

Sulfluramid (granular baits)

Seiva S/A, South Brazil SW-FM/COC-003580 Fipronil (granular baits)

Sulfluramid (granular baits)

Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors

March 2010 5

Seta S/A - Sociedade Extrativa de Tanino

de Acácia, South Brazil SW-FM/COC-1274 Sulfluramid (granular baits)

Sguario Florestal S.A. SGS-FM/COC-2745

Deltamethrin (dust)

Fenitrothion (liquid)

Sulfluramid (granular baits)

Souza Cruz- S/A, South Brazil SCS-FM/COC-00116P Fipronil (granular baits)

Sulfluramid (granular baits)

SUZANO Papel e Celulose S/A - Unidade

Mucuri SW-FM/COC-1377

alpha-Cypermethrin (liquid)

Deltamethrin (dust)

Deltamethrin (liquid)

Fipronil (dispersible granules)

Sulfluramid (granular baits)

SUZANO Papel e Celulose S/A - Unidade

Suzano SW-FM/COC-2093

alpha-Cypermethrin (liquid)

Deltamethrin (dust)

Deltamethrin (liquid)

Fipronil (dispersible granules)

Sulfluramid (granular baits)

Tanagro S.A. SGS-FM/COC-1664 Deltamethrin (liquid)

Sulfluramid (granular baits)

Timbó Empreendimentos Florestais Ltda. SCS-FM/00065P Sulfluramid (granular baits)

Vanda Almeida Mattos, Bahia (south) Candidate FMO (SW)

Deltamethrin (dust)

Deltamethrin (liquid)

Fipronil (dispersible granules)

Sulfluramid (granular baits)

Votorantim Celulose e Papel, Ltda. (VCP) SCS-FM/COC-00085P

alpha-Cypermethrin (liquid)

Deltamethrin (liquid)

Fipronil (dispersible granules)

Sulfluramid (granular baits)

Certifier Contact Forest management reports

SGS do Brasil Ltda – Qualifor Program São Paulo, Brazil

Website: www.br.sgs.com/pt_br/fsc__qualifor

Ms P. Azambuja

[email protected] http://www.forestry.sgs.com/fore

st-management-reports.htm

Scientific Certification Systems – SCS

Emeryville, CA, USA

Website: www.scscertified.com

Ms V. Shimoyama vanilda.shimoyama@brturbo.

com.br

www.scscertified.com/nrc/forest_

certclients.php#southamerica

Rainforest Alliance SmartWood Program – Imaflora. Programa de Certificação

Florestal. São Paulo, Brazil

Website: ww2.imaflora.org

Mr R. Camargo Cardoso

[email protected]

www.rainforest-

alliance.org/forestry/public_docu

ments_country.cfm?country=3

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

Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors

March 2010 6

Table 2. Insecticides rated as ‘highly hazardous’ under FSC indicators (thresholds)

Active ingredient Indicator Acute toxicity

(LD50) Aquatic toxicity

(LC50) Octanol-water parti-

tion coefficient (Kow) Persistence

(half life)

Cypermethrin x x

alpha-Cypermethrin x x x x

Deltamethrin x x x

Fenitrothion x

Fipronil x x

Sulfluramid 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

Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors

March 2010 7

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 beta-

eudesmol;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 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 4 E.g. extract of Ateleia glazioviana, Canavalia ensiformis, Centrosema brasilianum, Citrus sinensis, Helietta

puberula, Hymenaea courbaril, Ipomea batata, Manihot esculenta, Myroxylon peruiferum, Pilocarpus grandi-

florus, Piper cenocladum, Raulinoa echinata, Ricinus communis, Sesamum indicum, or Trichillia glauca. 5 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

Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors

March 2010 8

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 alpha-

cypermethrin 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 nucleopoly-

hedroviruses (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.

Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors

March 2010 9

E. The technical advisors recommend the certificate holders who applied for a derogation for deltame-

thrin (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 Pereira L.G.P. A Lagarta-Parda, Thyrinteina arnobia, principal lepidóptero desfolhador da cultura do

Eucalipto. CETEC 2007. http://sbrtv1.ibict.br/upload/dossies/sbrt-dossie219.pdf 7 Branco EF. Aspectos econômicos do controle de Thyrinteina arnobia (...) com Bacillus thuringiensis (Berliner)

em povoamentos de Eucalyptus spp. Lab. de Proteção Forestal 1995. http://floresta.ufpr.br/~lpf/outras02.html 8 Dos Santos A. Plano de amostragem e nível de dano econômico de cupins subterrâneos (Isoptera) em plantios

de eucalipto. Doutorado em andamento, UFLA. http://buscatextual.cnpq.br/buscatextual/visualizacv.jsp?id=K4704676U6

Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors

March 2010 10

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

10 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)

Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors

March 2010 11

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, leaf-

cutting 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

Thomas JC. Formigas cortadeiras: instruções básicas para o controle. EMATER-PR, Curitiba 1990 13

Forti L.C., y Boaretto M.A.C. Formigas cortadeiras: Biologia, ecologia, danos e controle. UNESP 1997 14

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 15

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.

Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors

March 2010 12

· 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 Florida Cooperative Extension Service (FCES). Insecticides used in the urban environment: Mode of action.

Florida 1997. http://edis.ifas.ufl.edu/IN077 18

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

Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors

March 2010 13

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 grass-

cutting 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

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 21

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/0-

0/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

Oliveira M. Valuable wood. Pesquisa FAPESP 115, 2005. http://www.revistapesquisa.fapesp.br/?art=1561&bd=1&pg=1&lg=en 25

Anjos N., et al. Árvores e formigas cortadeiras (Hymenoptera: Formicidae) em Viçosa, Minas Gerais. Revista

Trópica 1(2): 11-16, 2008. http://www.uni-

lueneburg.de/umanagement/csm/content/naoek/downloads/downloads_publikationen/Anjos_et_al_2008_Revista_Tropica.pdf

Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors

March 2010 14

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 leaf-

cutting 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

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) 27

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 28

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): 107-

113, 1995. http://www.informaworld.com/smpp/content~db=all~content=a905708940 29

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 Perfluoro-

octano. Ginebra 2007. http://chm.pops.int/Portals/0/Repository/poprc3/UNEP-POPS-POPRC.3-20.Spanish.PDF (sp)

Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors

March 2010 15

1.2 Risk Mitigation for Insecticide Use

1.2.1 Legislation for Occupational Safety in Brazil (General Aspects)

Certified companies confirmed that they adhere to the national legislation on occupational safety and

have established operational procedures to mitigate risks of pesticides, including the use of appropriate

personal protective equipment by forest workers. Authorities periodically inspect if companies comply

with national regulations for protection of workers. In Brazil, forest plantations are required to maintain

a distance of 30 m from rivers. National legislation for chemical safety and guidelines are listed below.

Regulations for Occupational Safety and Risk Mitigation in Brazil Ministério do Trabalho e Emprego: Norma Regulamentadora de Segurança e Saúde no Trabalho na

Agricultura, Pecuária, Silvicultura, Exploração Florestal e Aqüicultura – NR 31. 2005. http://www.mte.gov.br/legislacao/normas_regulamentadoras/nr_31.pdf

NR 31 – Manual de Aplicação. 2005. http://www.higieneocupacional.com.br/download/nr31-cna.zip

NPR 4 – Equipamento de Proteção Individual. http://www.mte.gov.br/legislacao/normas_regulamentadoras/nr_rural_04.asp

NPR 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

Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors

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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

Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors

March 2010 17

(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

Toxicity Class* in Brazil /

WHO Class (active ingredient)

Sulfluramid

Mirex-S; Dinagro-S S: 8-10 g per m

2 nest

Formulated product (in Brazil): IV

WHO class III „Slightly hazardous‟

Q: 10-12 g per nest

Fluramim S: 6-10 g per m

2 nest

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

Fipronil Blitz S: 10 g per m

2 nest

Q: 5 g per nest

Formulated product (in Brazil): IV

WHO class II „Moderately hazardous‟

Isca Formicida Landrin Q: 8-10 g per nest

Formulated product (in Brazil): III

WHO class II „Moderately hazardous‟ Chlorpyrifos

Isca Formicida Pyrinex

(Isca Formicida Pyrineus) S: 5-10 g per m

2 nest

Isca Formicida Atta-Fós S: 10 g per m2 nest

Diflubenzuron Isca Formilin (BASF; not

listed in Anvisa register) S: 10 g per m

2 nest

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/

Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors

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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

Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors

March 2010 19

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 metabo-

lites 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 perfluoro-

octane 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 perflurooctane-

sulfonic 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/BF9B2067-

FDB0-49B0-9543-8EEA03A415FD/1651/2004Abstracts.pdf 37

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 38

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

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 41

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) 42

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 43

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 44

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 45

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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March 2010 20

the metabolite PFOS accumulated in various organs, mainly in the liver (US EPA 2001).46

Increased

levels of PFOA or PFOS in blood were linked to a higher risk of thyroid disease (Melzer et al 2010).

4. Sulfluramid is in WHO class III („Slightly hazardous‟), is moderately to highly toxic to fish, and

moderately to highly toxic to bird species (see annex III). Toxicity of sulfluramid and its primary

metabolite, PFOA, is based on the same mechanism. In animals, PFOA was several times more

toxic (Schnellmann et al 1990).47

The main metabolite of sulfluramide, PFOS, is immunotoxic in

rats and similar effects are likely in humans (DeWitt et al 2009).48

A risk assessment for sulfluramid

concluded that in the medium term less toxic methods of ant control can and should substitute

sulfluramid in Brazil (Porto & Milanez 2009).49

5. Water and also blood and fat from rats were analysed in areas where sulfluramid had been applied.

Sensitivity of chemical analysis was limited: the detection limit for sulfluramide in blood and fat was

13.6 part per billion (ppb = micrograms per litre) and for PFOA it was 187 ppb (less sensitive). In

water, the detection limit for sulfluramid was 0.027 ppb, while for PFOA it was 0.37 ppb (BioAgri

1997).50

To monitor influx of sulfluramid and its metabolites to the environment and gradual accu-

mulation in wildlife, up-to-date technology for chemical analysis with a high sensitivity is needed. 6. In animal tissue, metabolites PFOA and perfluorooctanesulfonate (= perfluorooctanesulfonic acid

salt PFOS) are now commonly detected (Giesy & Kannan 2002).51

PFOA and volatile precursors of

perfluorinated chemicals are transported through the atmosphere or sea over large distances and are

later metabolized to PFOS in animals (Stock et al 2007; Martin et al 2006).52

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 US Environmental Protection Agency (EPA). Sulflramid: Human health risk assessment for sulfluramid.

Washington DC 2001. http://www.epa.gov/opp00001/foia/reviews/128992/128992-053.pdf Melzer D., et al. Association betweens perfluoroctanoic acid (PFOA) and thyroid disease in the NHANES

study. Environmental Health Perspectives Online 20 January, 2010. http://dx.doi.org/10.1289/ehp.0901584 47

Schnellmann RG, and Randall O M. Perflurooctane sulfonamide: a structurally novel uncoupler of oxidative

phosphorylation. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1016(3): 344-348, 1990. (quoted in

Key et al 1997). http://dx.doi.org/10.1016/0005-2728(90)90167-3 48

DeWitt J.C., et al. Immunotoxicity of perfluorooctanoic acid and perfluorooctane sulfonate and the role of

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 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) 50

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) 51

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 52

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

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 54

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 55

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 56

Souza D.J. Cortadeiras sob ameaça. Revista Ciência Hoje 222, 2002. http://cienciahoje.uol.com.br/4148 57

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

EFTRN: EC funding for research in the tropics/subtropics. www.etfrn.org/ETFRN/resource/frames/linkfund.html 59

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 60

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 Meta-

rhizium 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/ 61

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 rubropi-

losa seven days after application of 10 g/m2 and 50 g/m

2, 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

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/ 63

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 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 65

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 66

Lopez E., and Orduz S. Metarhizium anisopliae and Trichoderma viride for control of nests of the fungus-

growing ant, Atta cephalotes. Biological Control 27(2), 2003. http://dx.doi.org/10.1016/S1049-9644(03)00005-7 67

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/ 68

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 non-

toxic 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

“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/list-

kieselgur_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) 71

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 72

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 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 74

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 75

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,

Cazal C.M., et al. Isolation of xanthyletin, an inhibitor of ants‟ symbiotic fungus, by high-speed counter-

current chromatography, J. of Chromatography A 1216(19), 2009 http://dx.doi.org/10.1016/j.chroma.2009.02.066 76

Magalhães C.P., et al. Biochemical basis of the toxicity of manipueira (…) to nematodes and insects. Phyto-

chemical Analysis 11(1), 2000. http://www3.interscience.wiley.com/journal/70001198/abstract?CRETRY=1&SRETRY=0 Sebrae (2008): O aproveitamento sustentável da manipueira. http://www.rts.org.br/noticias/destaque-

2/arquivos/cartilha.pdf; SBPC: Mandioca, a última fronteira? http://www.jornaldaciencia.org.br/Detalhe.jsp?id=27482

Farias A.R.N., et al. Manipueira e plantas armadilhas no controle de formigas cortadeiras na cultura da

mandioca. 2007. http://www.infobibos.com/Artigos/2007_4/manipueira/index.htm 77

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 77

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 78

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 79

Marinho et al. Beta-eudesmol induced aggression in the leaf cutting ant Atta sexdens rubropilosa. Entomo-

logia 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

Hughes WO, et al. Field evaluation of potential of alarm pheromone compounds to enhance baits for control

of grass-cutting ants (Hymenoptera: Formicidae). Journal of Economic Entomology 95(3), 537-543, 2002. http://www.bioone.org/doi/abs/10.1603/0022-0493%282002%29095%5B0537%3AFEOPOA%5D2.0.CO%3B2

81 The Pherobase. Semiochemicals of Atta species. http://www.pherobase.com/database/genus/genus-Atta.php

Semiochemicals of Acromyrmex species. http://www.pherobase.com/database/genus/genus-Acromyrmex.php 82

Delabie J.H.C., and Jahyny B. A mirmecosfera animal: relações de dependência entre formigas e outros

animais. Revista O Biológico 69(supl.), 2007. http://www.biologico.sp.gov.br/docs/bio/suplementos/v69_supl_2/p7-12.pdf

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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): 682-

684, 1998., http://www3.interscience.wiley.com/journal/119102866/abstract 84

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 85

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 86

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 87

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 88

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

Leaf-

cutting ants are still often controlled with chlorpyrifos (Lorsban® powder). Methods to control ants

were compared in Colombia, including use of lime, lime mixed with chlorpyrifos (6:1), and manual

collection of ant queens. An effective method favored by farmers was lime mixed with decreasing

amounts of chlorpyrifos (requiring 3-7 repeat applications). Pure lime (requiring 9-10 applications) was

cheaper. Chemical methods reduced the number of active ant holes by over 80%. Although most

farmers used chlorpyrifos on ants (pouring it around ant holes or pumping it into nests), ant control failed, due to ineffective application and lacking coordination (Munk Ravnborg et al 2000).

92

Cypermethrin paste (6.7% a.i.) is used specifically for control of Atta capiguaira (ANVISA 2009).

Hydramethylnon resulted in 50% mortality in Atta sexdens rubropilosa, propoxur (Blattanex®) caused

less than 40% mortality and chlorpyrifos less than 20% (Coll 2003).21

In the USA, hydramethylnon is

used in baits for controlling the Texas leaf-cutting ant (TAE (no year)).23

Piperonyl compounds had high mortality (up to 82%) in Atta sexdens (Victor et al 2001, see annex II).

Rotenone is a botanical insecticide made from root extracts of timbó (Derris species) (Fang & Casida

1999).93

The powder (e.g. Rotenat pó) is used for ant control in organic agriculture (Santiago 2004).

89

Nagamoto N.S., Forti L.C., and Raetano C.G. Evaluation of the adequacy of diflubenzuron and dechlorane in

toxic baits for leaf-cutting ants (Hymenoptera: Formicidae) based on formicidal activity. Journal of Pesticide

Science 80: 9-13, 2007. http://dx.doi.org/10.1007/s10340-006-0143-8 90

Forti LC. Approach on the ants‟ biology, screening and desirable features of active ingredients and insect

growth regulators for control of leaf-cutting ants. UNESP, Botucatu, São Paulo 2008. http://chm.pops.int/Portals/0/Repository/addinfo_2008/UNEP-POPS-POPRC-SUB-F08-PFOS-LEAF6.English.pdf

91 Zanuncio J.C., et al. Control of Atta laevigata (Hymenoptera: Formicidae), with Landrin-F bait, in areas

previously covered with Eucalyptus. Ciencia Rural 29(4): 1999. http://www.scielo.br/pdf/cr/v29n4/a01v29n4.pdf 92

Munk Ravnborg H., et al. Collective action in ant control. CAPRi Working Paper 7. CGIAR, Washington DC

2000. http://www.capri.cgiar.org/wp/capriwp07.asp, http://www.capri.cgiar.org/pdf/CAPRIWP07.pdf 93 Fang N., and Casida J.E. Cubé resin insecticide: Identification and biological activity of 29 rotenoid constitu-

ents. Journal of Agricultural Food and Chemistry 47(5), 1999. http://pubs.acs.org/doi/abs/10.1021/jf981188x

Santiago J.P., and Guimarães V. Formigas cortadeiras: possibilidades de controle. AAO, São Paulo 2004. http://www.aao.org.br/dicas3.asp

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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

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 94

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 clear-

cuts). 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 uneven-

aged 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.

Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors

March 2010 31

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

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 98

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 99

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 100

Imaflora. Consulta Pública. 2007. http://ww2.imaflora.org/index.cfm?fuseaction=content&IDassunto=4&IDsubAssunto=53 101

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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research institutions (Brazilian Agricultural Research Corporation - Embrapa), associations of forest

plantations (Associação Brasileira de Produtores de Florestas Plantadas - Abraflor, Minas Gerais Silvi-

culture Association / Associação Mineira de Silvicultura AMS, Sociedade Brasileira de Silvicultura

SBS). The individual certificate holders consulted representatives of workers and subcontracted staff

(National Union of Workers CUT), regional government authorities, non-governmental organizations

(for social welfare or environmental protection), neighbours and representatives of local communities. Regional non-governmental organizations consulted include Fundação ABC / Agricultural Research &

Development, Adecav, Biodiversitas Foundation, Centro de Ação Voluntária / Center for Voluntary

Action, Centro Cultural do Vale do Jequitinhonha, Comissão Pastoral da Terra CPT / Pastoral Land

Commission, Conservação Internacional, Instituto de Conservação Ambiental / Nature Conservancy,

Instituto de Desenvolvimento Sustentável e Energias Renováveis IDER / Institute of Sustainable

Development and Energy, Instituto Socioambiental ISA, Macon Lodge, Mandalla Agency, O Boticario,

Raízes da Terra, and Serviço Nacional de Aprendizagem Rural / National Office for Rural Education.

A large proportion of the contacted stakeholders responded, and the majority of these were supportive.

Non-supportive answers will be replied to after a final decision of FSC-IC on derogation applications.

For sulfluramid, out of 3839 stakeholders who were consulted, 3447 responded. Of these, 3395 were

supportive and 52 (1.5%) did not support use of sulfluramid in forest management. According to the

applicant, non-supportive answers can be classified as follows: 71% without justification; 17% based

on technical or environmental aspects; 7% with unfounded justification; 5% based on toxicity aspects.

Table 4. Stakeholder Opinions on Use of ‘Highly Hazardous’ Insecticides

Stakeholders who responded to consultation

Number contacted / Number of responses

Opinion on derogation for ‘highly hazardous’ insecticide Supportive / Non-supportive

alpha-Cypermethrin, liquid

(Fendona): 950 / 944 931 / 13 (non-supportive A: 33%, B: 13%, C: 13%, D: 40%)

Deltamethrin, liquid (Decis): 3197 / 2968 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): 3462 / 2978 2916 / 62 (non-supportive A: 77%, B: 12%, C: 4%, D: 8%)

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: 3839 / 3447 3395 / 52 (A: 71% 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 prohi-

bited under the Stockholm Convention (CONSEA 2009).102

This reflects concerns about the hazardous

102

CONSEA. Letter from Mr R.F. Maluf, president of CONSEA, to the President of Brazil, April 29, 2009. http://www.planalto.gov.br/consea/static/agenda/Plenarias2009/090429/EM_003_impactos%20da%20sulfluramida.pdf

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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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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.

Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors

March 2010 35

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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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 alpha-

cypermethrin) 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 Control with

active ingredient

Area treated 2006; 2007;

2008 (certificate no.) Latin name Common

name Order: family

Adeloneivaia

subangulata

lagarta-da-

acacia

Lepidoptera:

Saturniidae deltamethrin

283; 182.6; 782.5 ha

(SGS-1664)

Bonagota cronaodes lagarta enrola-

deira da maçã

Lepidoptera:

Tortricidae deltamethrin

17; 17; 17 ha (nursery)

(SGS-4161)

Colaspis species Coleoptera:

Chrysomelidae not controlled

Costalimaita

ferruginea

besouro-

amarelo /

yellow beetle

Coleoptera:

Chrysomelidae

α-cypermethrin 3035.4; 0; 0 ha (SGS-

1943)

deltamethrin

300; 500; 0 ha (SCS-85P)

89; 58.7; 159.8 ha (SGS-

2167)

0.4; 1.5; 0.3 ha (SCS-40P)

13466.2; 13466.2; 13466.2

ha (nursery) (SCS-93P)

Eupseudosoma

aberrans, E. involuta

lagarta-

cachorrhinho

Lepidoptera:

Arctiidae not controlled

Euselasia apisaon lagarta-

euselasia

Lepidoptera:

Riodinidade not controlled

Glena bipennaria

Glena unipennaria

Lepidoptera:

Notodontidae not controlled

Lampetis

drummondi besouro cai-cai

Coleoptera:

Buprestidae not controlled

Melanolophia sp. Lepidoptera:

Geometridae B. thuringiensis 0; 0; 120 ha (SCS-76P)

Metaxyonycha

angustata

besouro

quarto-pintas

Coleoptera:

Chrysomelidae not controlled

Nystalea nyseus Lepidoptera:

Notodontidae not controlled

Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors

March 2010 37

Psorocampa

denticulata

Lepidoptera:

Lymantriidae not controlled

Sarsina violascens cariposa-

violácea

Coleoptera:

Chrysomelidae not controlled

Sternocolaspis

quatuordecimcostata

Coleoptera:

Chrysomelidae not controlled

Thyrinteina arnobia

lagarta-parda

do eucalipto /

eucalyptus

brown looper

Lepidoptera:

Geometridae

deltamethrin

857.6; 4643.5; 0 ha (SGS-

1943)

0; 0; 11 ha (SCS-76P)

18.5; 0; 1780.5 (SCS-77P)

B.thuring 0.5 l/ha +

α-cyperm 0.15 l/ha

857.6; 4643.5; 0 ha (SGS-

1943)

B. thuringiensis 251; 0; 7191.2 ha (SCS-

77P)

Costalimaita ferru-

ginea, other beetles

T. arnobia

Melanolophia sp.

besouro-

amarelo

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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March 2010 38

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

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 108 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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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

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) 110

Van Driesche R., et al. Control of pests and weeds by natural enemies. Blackwell Publ., Oxford, UK 2008 111

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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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. Cole-

opteran 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

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 113

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.2005.09.005 114

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 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 117

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) 118

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

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 120

Machado A.L. Estudos biologicos e comportamentais de Migdolus fryanus (Westwood, 1863) (Coleoptera:

vesperidae) e sua interação com nematoides entomopatogenicos, e outros agentes de mortalidade. Tese de

Doutorado, Unicamp 2006. http://libdigi.unicamp.br/document/?code=vtls000378083 121 Goettel M.S., et al. Entomopathogenic fungi and their role in regulation of insect populations. In: Gilbert L.I.,

et al. Comprehensive molecular insect science: Control. Vol. 6, pp. 361-405. Elsevier Publ., Amsterdam 2005 122 Souza R.M. Feromônios do besour-amarelo, Costalimaita ferruginea. Projeto de Doutorado.

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 inter-

planted 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

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 124

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 125

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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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 m

3/ha

for 100 % defoliation (Oda & Berti Filho 1978).127

Damage from lepidopteran defoliators in E. saligna

126

Freitas S. de. Efeito do desfolhamento na produção de Eucalyptus grandis Hiil ex Maiden (Myrtaceae)

visando avaliar os danos causados por insetos desfolhadores. Tese de Doutorado, ESALQ/USP 1988 127

Oda S., y Berti Filho E. Incrementos anual volumétrico de Eucalyptus saligna sm. em áreas com diferentes

níveis de infestações de lagartas de Thyrinteina arnobia (…). IPEF 17: 27-31, 1978.

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(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: SGS-

1943). 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

Van Driesche R., et al. Control of pests and weeds by natural enemies. Blackwell Publ., Oxford, UK 2008 130

Bressan D.A., y Santos H.R. Controle de lagartas de Adeloneivaia subangulata (…) com Bacillus

thuringiensis Berliner (1911) em condições de laboratório. Revista Florestas, 1985. http://ojs.c3sl.ufpr.br/ojs2/index.php/floresta/article/viewFile/6365/4565

(see also: http://ojs.c3sl.ufpr.br/ojs2/index.php/floresta/article/view/6360/4560)

Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors

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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 132

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/glfc-

bacillus-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.,

Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors

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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

et al. Comprehensive molecular insect science: control. Vol. 6, pp. 361-405. Elsevier Publ., Amsterdam 2005

136 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 137 Organic Materials Review Institute (OMRI). Spinosad. 2002. http://www.omri.org/spinosad_final.pdf 138

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)

Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors

March 2010 49

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 (Lepidop-

tera: 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 …)

Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors

March 2010 50

(…). 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

Galon J.A. (Bayer). Fórum nacional sobre carvão vegetal. 2008. http://painelflorestal.com.br/upload/bayer.pdf Wilcken C.F., Raetano C.G. Eficiência do inseticida fipronil no controle de cupins subterrâneos (Isoptera) em

eucalipto. Abstracts of XV Congresso Brasileiro de Entomologia, p. 547. Caxambu, Brazil 1995 141

Peralta R.C.G., et al. Wood consumption rates of forest species by subterranean termites (Isoptera) under

field conditions. Revista Árvore 28(2): 283-289, 2004. http://www.scielo.br/pdf/rarv/v28n2/20993.pdf

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4.3 Risk Mitigation for Use of Fipronil: See 1.2.1 (p. 14 above)

4.4 Stakeholder Opinions on Use of Fipronil: See 1.4 (pp. 29-31 above)

4.5 Alternatives for Direct Control of Termite Colonies (Cornitermes / Syntermes species)

Current practices of preventively treating eucalypt seedlings with fipronil have the great advantage of

reducing the amount of insecticide entering the environment to a very low level. This reduces the risk

to non-target organisms (such as natural enemies of termites) significantly, compared to direct chemical

control of termite nests. Preventive treatment of seedlings prior to planting should be the predominant

or only method of termite control. Stored wood is also often treated with preservatives such as borates.

In situations where termite colonies might be targeted directly (to control or eliminate a whole colony,

e.g. if termites are attacking buildings), biological agents should be used preferentially. Besides direct

application of an insecticide (e.g. in baits), several methods have a potential to control termite colonies.

Promising alternatives include pathogenic fungi. Alternative methods for direct termite control might

be used in exceptional situations where a certain termite colony is targeted. As preventive treatment of

seedlings protects these very effectively, direct control of termite colonies is usually not necessary.

Abamectin qualifies as „highly hazardous‟ under FSC criteria. Abamectin and fipronil were equally

effective for termite control. One application of abamectin (as a liquid concentrate) or of fipronil

(granules) both resulted in 100% mortality of Cornitermes cumulans (Valerio et al 1998).142

However,

fipronil achieved only 50% mortality in Syntermes species.

Borax preserves wood against attack by termites, especially when combined with smaller amounts of

copper hydroxide (Lebow et al 2005).143

In Brazil, borax is registered as a wood preservative (Anvisa

2009). Borate salts are applied to wood in various ways (UA 2006).144

Borax also acts as an insecticide.

When applied in baits, borax effectively controls termites and cockroaches (Quarles 2003).145

Botanical extracts from several plants were toxic to termites (Coptotermes gestroi) in laboratory tests,

e.g. extract of Ocimum basilicum / manjerição caused 12% mortality (Reis et al 2008).146

Combinations

142

Valerio JR et al. Controle químico e mecânico de cupins de montículo (Isoptera: Termitidae) em pastagens.

Anais da Sociedade Entomológica do Brasil 27(1), 125-131, 1998. http://dx.doi.org/10.1590/S0301-

80591998000100016 143

Lebow et al. Resistance of borax-copper treated wood in aboveground exposure to attack by subterranean

Formosan termites. US Forest Service 2005. http://www.fpl.fs.fed.us/documnts/fplrn/fpl_rn295.pdf 144

University of Arkansas (UA). Termite and other structural pest control. Little Rock, Arkansas, 2006. http://www.aragriculture.org/pesticides/training/manuals/AG1155/default.htm

145 Quarles W. IPM for termites – Termite baits. The IPM Practitioner 25(1-2), 2003. http://www.birc.org/JanFeb2003.pdf

146 Reis F.C., et al. Avaliação de produtos naturais no controle de Coptotermes gestroi (Isoptera: Rhinotermiti-

tidae) . Revista O Biológico 70(supl. 1), 2008. http://www.biologico.sp.gov.br/docs/bio/suplementos/v70_supl/37.pdf

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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 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 149

Börne H. Pflanzenkrankheiten und Planzenschutz [Plant diseases and plant protection]. Stuttgart 1981 150

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 151

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 soon-

cheon 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

Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors

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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-sp-

beauveria-bassiana/efeito-trichoderma-sp-beauveria-bassiana.shtml 162

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 163

Schmidt L., Meke G. Tree species resistant to termites. 2008. http://en.sl.life.ku.dk/upload/technical_briefs_5.2008.pdf 164

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 165

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 166

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 compa-

nies 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 m

2 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 m

2 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 Ghazoul J. Plant-animal interactions in forest ecosystems. In: Burley et al. Encyclopedia of forest science.

Volume 1, pp. 57-62. Elsevier Publ., Oxford 2004 170

Herz H., Beyschlag W., and Hölldobler B. Herbivory rate of leaf-cutting ants in a tropical moist forest in

Panama at the population and ecosystem scales. Biotropica 39(4): 482-488, 2007. http://www.blackwell-

synergy.com/doi/full/10.1111/j.1744-7429.2007.00284.x 171

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 172

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=0006-

3606%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 leaf-

cutting 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

clearing of mature forest in Brazilian Amazonia. Studies on Neoptropical Fauna and Environment 30(2): 107-

113, 1995. http://www.informaworld.com/smpp/content~db=all~content=a905708940 174

Florin W., et al. The effects of temperature, light, and nutrient conditions on the foraging of leaf-cutter ants

(Atta cephalotes) in forested and disturbed areas. In: Villalobos E., et al (eds). Summer Program on Tropical

Ecology, pp. 73-82, 2002. http://www.ots.duke.edu/en/education/pdfs/usap/coursebooks/te02.pdf 175

Mendes F.E.S., et al. Efeito da pressão de ataque de Atta sexdens na estrutura da vegetação em áreas de

sucessão secundária no médio Rio Doce. VI Congresso de Ecologia do Brasil, Fortaleza, 2003. pp. 234-236. http://seb-ecologia.org.br/anais/11.pdf

176 Cornelius J.P., et al. Swietenia (American Mahogany). In: Burley et al. Encyclopedia of forest science.

Volume 3, pp. 1720-1728. Elsevier Publ., Oxford 2004 177

Caffarini P., et al. Impacto del estrés hídrico y la procedencia de Eucalyptus globulus Labill. Sobre el

comportamiento de herbivoría de Acromyrmex lundi Guérin. Idesia 24(1), 2006. http://dx.doi.org/10.4067/S0718-34292006000100002

178 Meyer S.T., et al. Selecting the drought stressed: effects of plant stress on intraspecific and within-plant

herbivory patterns of the leaf-cutting ant Atta colombica. Functional Ecology 20(6), 2006. http://www3.interscience.wiley.com/journal/118572728/abstract?CRETRY=1&SRETRY=0

179 Meyer S.T. Ecosystem engineering in fragmented forests: Edge-mediated hyper-abundance of leaf-cutting

ants and resulting impacts on forest structure, microclimate and regeneration. 2008. http://kluedo.ub.uni-

kl.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 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 182

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%2F0012-

9658%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.1744-

7429.2007.00285.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 (Sousa-

Souto et al 2007).190

185

Majer J.D., and Recher H.F. Are eucalypts Brazil's friend or foe? An entomological viewpoint. Anais da

Sociedade Entomológica do Brasil 28(2): 185-200, 1999. http://www.scielo.br/pdf/aseb/v28n2/v28n2a01.pdf

Nair K.S. Pest outbreaks in tropical forest plantations: Is there a greater risk for exotic tree species? CIFOR,

Jakarta, Indonesia 2001. http://www.cifor.cgiar.org/publications/pdf_files/Books/Nair.pdf 186

Evans J. Bioenergy plantations – Experience and prospects: Worldwide experience with high yield forest

plantations. Biomass and Bioenergy 13(4-5): 187-191, 1997. http://dx.doi.org/10.1016/S0961-9534(97)10007-1 187

Rao M. Variation in leaf-cutter ant (Atta spp.) densities in forest isolates: the potential role of predation.

Journal of Tropical Ecology 16: 209-225, 2000. http://www.journals.cambridge.org/action/displayAbstract?fromPage=online&aid=35257

188 Vasconcelos H.L., and Cherrett J.M. Leaf-cutting ants and early forest regeneration in Central Amazonia:

effects of herbivory on tree seedling establishment. Journal of Tropical Ecology 13(3): 357-370, 1997. http://links.jstor.org/sici?sici=0266-4674(199705)13%3A3%3C357%3ALAAEFR%3E2.0.CO%3B2-K#abstract

189 Sternberg et al. Plants use macronutrients accumulated in leaf-cutting ant nests. Proceedings of the Royal

Society B 274: 315–321, 2007. http://penguin.bio.miami.edu/leo/PDF%20articles/atta.pdf 190

Sousa-Souto L., et al. Leaf-cutting ants, seasonal burning and nutrient distribution in Cerrado vegetation.

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

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/0 192

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)00183-4 193

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.uni-

lueneburg.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. http://www.scielo.br/pdf/aseb/v26n1/v26n1a29.pdf

Associação Brasileira Técnica de Celulose e Papel (ABTCP). Pinus Letter 3, 2008. http://www.celso-

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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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51-70, 2008. http://www.scielo.br/pdf/aa/v38n1/v38n1a07.pdf

Baer B., et al.Examination of the immune responses of males and workers of the leaf-cutting ant Acromyrmex

echinatior and the effect of infection. Insectes Sociaux 52(3), 1995. 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.blackwell-

synergy.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. http://www.ipef.br/publicacoes/curso_formigas_cortadeiras/cap10.pdf

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Barata G. Avanços no conhecimento não impedem dificuldades no controle das cortadeiras. Notícias do Brasil

61(3), 2009. http://cienciaecultura.bvs.br/pdf/cic/v61n3/a03v61n3.pdf

Barbieri R.F. Fluxo de corante e inseticida entre operárias de formigas cortadeiras. Revista O Biológico 69(supl.

2): 375-377, 2007. http://www.biologico.sp.gov.br/docs/bio/suplementos/v69_supl_2/p375-377.pdf

Barbosa V.S., et al. Influência da herbivoria de formigas cortadeiras no successo reprodutivo de espécies

vegetais de Floresta Atlântica. 2007. http://www.seb-ecologia.org.br/viiiceb/pdf/1679.pdf

Barbosa V.S. Efeito da fragmentação florestal na taxa de parasitismo de fungos associados ao jardim da formiga

cortadeira, Atta laevigata. Tese de Doutorado, UFPE 2004. http://www.bdtd.ufpe.br/tedeSimplificado//tde_busca/arquivo.php?codArquivo=377

Bellotti A.C., et al. Biological control in the Neotropics: A selective review with emphasis on cassava. Second

Internat. Symposium on Biological Control of Arthropods 2005. http://www.bugwood.org/arthropod2005/vol1/5a.pdf

Berti Filho E. Controle biológico e entomologia florestal. IPEF Boletim Informativo 5(14): 5-16, 1977. http://www.ipef.br/publicacoes/boletim_informativo/bolinf14.pdf

Bianchi-Santos M., et al. Efeito do ácido oléico sobre o metabolismo de operárias da formiga cortadeira Atta

sexdens rubropilosa. XXV Congr. Brasil. de Zool, resumo 536, 2006. http://www.unb.br/ib/zoo/CBZ/resumos/Insecta.pdf

Bieber A.G.D., et al. Recrutamento de plântulas sobre ninhos inativos da formiga cortadeira Atta cephalotes na

Floresta Atlântica Nordestina. Revista O Biológico 69(supl. 2): 329-333. 2007. http://www.biologico.sp.gov.br/docs/bio/suplementos/v69_supl_2/p329-333.pdf

Bizi R.M. Microrganismos Endofíticos. Laboratório de Proteção Florestal. http://floresta.ufpr.br/~lpf/contbio02.html

Boaretto et al. Response of the grass-cutting ant Atta capiguara Gonçalves, 1944 (Hymenoptera:

Formicidae) to sugars and artificial sweeteners. Scientia Agricola 60(3): 505-509 2003. http://www.fca.unesp.br/lisp/artigos/Boaretto%20et%20al%202003%20-%20sugars.pdf

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2000. http://www.uesb.br/entomologia/cortadeiras.htm, (1997): http://www.ipef.br/publicacoes/stecnica/nr30/cap3.pdf

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sexdens. 32a Reunião Anual de Sociedade Brasileira de Química 2009. http://sec.sbq.org.br/cdrom/32ra/resumos/T1819-1.pdf

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Bragança M.A.L., et al. Parasitismo por Neodohrniphora spp. Malloch (Diptera, Phoridae) em operárias de Atta

sexdens rubropilosa Forel (Hymenoptera, Formicidae). Revista Brasileira de Entomologia 52(2): 300-302, 2008. http://www.scielo.br/pdf/rbent/v52n2/a11v52n2.pdf

Bragança M.A.L., et al. Influência do tamanho das operárias de Atta sexdens rubropilosa (Hym.: Formicidae)

sobre a razão sexual e tamanho do parasitóide Neodohrniphora tonhascai (Diptera: Phoridae). Revista O

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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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Bragança M.A.L., et al. Parasitism characteristics of two phorid fly species in relation to their host, the leaf-

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phorid Neodohrniphora sp. Entomol. Exp. et Appl. 89(3), 1998. http://www.springerlink.com/content/r132129321872422/

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64, 2008. http://www.scielo.cl/pdf/idesia/v26n1/art08.pdf

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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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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

Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors

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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): 157-

160, 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. Cypermethrin, alpha-Cypermethrin, and zeta-Cypermethrin

2. Deltamethrin

3. Fenitrothion

4. Fipronil

5. 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

194

(PM): Tomlin C. The Pesticide Manual. 14th edition, British Crop Protection Council 2006

195 Khambay B. Pyrethroid insecticides. Pesticide Outlook 13: 49-54, 2002. 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 environ-

ment (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) „Cypermethrin‟: BCF = 1204, the calculated bioaccumulation

197

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/ 198

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 Treatment of severe poisoning with pyrethroids (such as Cypermethrin) is

difficult (Ray 2000).202

Chronic effects following an incident of systemic

199

(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 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 201

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 (Muller-

Mohnssen 1999).203

2. Deltamethrin

Active ingredient Deltamethrin (CAS no. 52918-63-5)

Chemical class Pyrethroid (a synthetic derivative of pyrethrum)

Use type 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

International Agency for Research on Cancer (IARC), Overall Evaluations of Carcinogenicity to Humans,

Lyon 2007, http://monographs.iarc.fr/ENG/Classification/crthalllist.php 205

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 206

US Environmental Protection Agency (EPA). Reregistration Eligibility Decision for Fenitrothion.

Washington DC. 2006. http://www.epa.gov/pesticides/reregistration/REDs/fenitrothion_red.pdf US EPA. Reregistration Eligibility Decision (RED) Fenitrothion. Washington DC 1995. http://www.epa.gov/pesticides/reregistration/REDs/0445.pdf

US EPA. Fenitrothion Facts. Washington DC 2000. http://www.epa.gov/oppsrrd1/REDs/factsheets/0445tredfact.pdf

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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 bioaccu-

mulate 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

PAN North America (PANNA). Pesticides Database (search for chemical name). http://www.pesticideinfo.org 208

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. Environ-

mental 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 Sulfluramid (CAS no. 4151-50-2)

Chemical class Fluorinated sulfonamide

Chemical name N-ethylperfluoro-octan-1-sulfonamide

Other names Ethyl perfluorooctylsulphonamide, GX-071 (HB), GX-439

Use type Insecticide with stomach action (Footprint 2009)

Usage 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 Kamrin A. Pesticide profiles: Toxicity, environmental impact, and fate. Boca Raton, Florida 1997

210 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

Insecticides for Control of Pest Insects in FSC Certified Forests in Brazil – Recommendations by Technical Advisors

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Metabolites Perfluorooctanesulfonamide, perfluorooctanesulfonic acid (perfluorooctane-

sulfonate) (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

Technology 31(9): 2445-2454, 1997. http://www.stanford.edu/group/evpilot/pdf/es961007c%202.pdf (p. 2450) 212

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) 213

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%2F1551-

5028%282003%29022%3C0196%3ABATDOP%3E2.0.CO%3B2 214

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 215

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.

Additional Publications on Sulfluramid, Metabolites, and Perfluorinated Compounds

Allsopp M., et al. Perfluorinated chemicals: an emerging concern. Greenpeace Research Laboratories, University

of Exeter, UK 2005. http://greenpeace.to/publications/perfluorinated_chemicals_2005.pdf

Arrendale R.F., et al. Determination of GX 071 and its major metabolite in rat blood by cold on-column injection

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