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Biological Control in an overview Prof. Dr. José Roberto Postali Parra Departamento de Entomologia e Acarologia USP/ESALQ, , State of , Brazil UNIVERSITY OF SÃO PAULO Founded in 1934 Recognized as the best university in Latin America (Times Higher Education) Classified among 200 universities with best reputation worldwide / 50th in Life Science 28% of Brazilian scientific production 8 campi 89,000 students / 5,800 professors / Ribeirão Preto 16,000 employees São Carlos Pirassununga Lorena Piracicaba 246 undergraduate and 225 graduate São Paulo programs “LUIZ DE QUEIROZ” COLLEGE OF AGRICULTURE TODAY 13,568 degrees awarded 7 undergraduate programs 16 graduate programs 244 professors and 540 technical and administrative employees INSECT BIOLOGY LAB BRAZIL Leader in Latin America and in Tropical Agriculture

Its own technology In the last for Tropical years conditions

The transfer of technological packages Past from temperate areas were not well succeed Now Brazil is the leader in Tropical Agriculture with its own technology CULTIVATED AND AVAILABLE LAND AREAS PER COUNTRY FOR AGRICULTURE USE

450

400 350 Cultivated area 300 Agricultural area not cultivated 250

200

150

100

Area (million (million hectares) of Area 50

0

NEVES et al. (2005) On the other hand, the Brazilian Agriculture is perverse (wicked) for Biological Control implementation SUGARCANE FIELD BIODIVERSITY IN BRAZIL

NOT WELL- KNOWN

NOT WELL EXPLOITED BRAZILIAN AGRICULTURE 2012-2013 CROPS CULTIVATED AREA (x1000 ha) Cotton 887 Rice 2,409 Bean 3,065 Corn 15,627 Soybean 27,713 Sugarcane 8,500 Brazil 53,035

(pesticides) 1970 – 1980 DECADES

The grower has used Baculovirus anticarsia to control the Velvetbean Caterpillar, Anticarsia gemmatalis, in in soybean crop.

Moscardi F. 1999. Annual Review of Entomology, 44: 257-289. The beginning of studies in applied entomology in Brazil were significantly influenced by agrochemicals

Differently from other countries in Latin America that were influenced by American Universities FIRST IMPORTATION IN THE WORLD 1888

(Coleoptera: Coccinellidae)

Cottony Cushion Scale

(Hemiptera: Margarodidae) FIRST IMPORTATION IN BRAZIL 32 YEARS AFTER

Prospaltella berlesei (USA) (Hymenoptera: Aphelinidae)

Pseudaulacaspis pentagona (Hemiptera: Diaspididae) CHALLENGES FOR BIOLOGICAL CONTROL IMPLEMENTATION Grower culture; Pest survey; Poor extension service; Few privates companies producing natural enemies (of good quality); Availability of natural enemies for different crops; Transportation and storage logistic of natural enemies; Legislation of biological control; Releasing technologies (predation); Insecticides selectivity; Dynamic Agriculture; GMO areas. AVAILABILITY OF NATURAL ENEMIES FOR DIFFERENT CROPS 250

200

150 Species 100

50

0 1970 1975 1980 1985 1990 1995 2000 2007 2009 2011 van Lenteren (2012) NATURAL ENEMIES SPECIES AVAILABLE IN BRAZIL Cotesia flavipes x Diatraea Phytoseiulus longipes x saccharalis (parasitoid) Tetranychus urticae, Tetranychus evansi (predator)

Trichogramma galloi x Stratiolaelaps scimitus x Diatraea saccharalis Bradysia spp., Collembola, (parasitoid) soil acari, thrips (predator)

Trichogramma atopovirilia x Podisus nigrispinus x forest Spodoptera frugiperda defoliator caterpillar (predator) (parasitoid)

Trichogramma pretiosum x Orius insidiosus x thrips Spodoptera frugiperda, Tuta (predator) absoluta, Chrysodeixis includens (parasitoid)

Neoseiulus californicus x Cryptolaemus montrouzieri x Panonychus ulmi, Tetranychus scales (predator) urticae, Polyphagotarsonemus latus (predator) Phytoseiulus macropilis x Tetranychus urticae (predator) Parra (2010) TRANSPORTATION AND STORAGE LOGISTIC OF NATURAL ENEMIES Austria Hungary Romania Holland Lithuania Italy Poland

Czech Republic Estonia France Ireland Greece Belgium Ukraine Albania Bosnia Portugal Croatia Macedonia Spain Bulgaria Iceland United Kingdom Yugoslavia Germany Norway Latvia Finland Denmark Switzerland Belarus Sweden LEGISLATION OF BIOLOGICAL CONTROL

Associação Brasileira de Empresas de Controle Biológico (PRIVATE COMPANIES)

2007 RELEASING TECHNOLOGIES PREDATION DYNAMIC AGRICULTURE

Occupation of pasture and Cerrado areas Irrigated areas Crop succession No-tillage agriculture New varieties Invasive pests (Helicoverpa armigera) Insecticides utilization GMO areas (36 millions of hectares) TRAINED ENTOMOLOGISTS GRADUATED COURSE

until today

24% 25% biological control 2002 1998 2006 2006

1997

2011 2010 2006 2009 2008

2006 2000 1998 1986 BIOLOGICAL CONTROL IN BRAZIL EXAMPLES OF SUCCESS

decade

Neodusmetia sangwani (Hymenoptera: Encyrtidae)

Antonina graminis (Hemiptera: Pseudococcidae)

Exotic natural enemy introduced from Texas, USA, by Instituto Biológico

PASTURES BIOLOGICAL CONTROL IN BRAZIL EXAMPLES OF SUCCESS

decade parasitoids (Praon, Ephedrus, Aphidius) (Hymenoptera: Braconidae) wheat aphids (Hemiptera: Aphididae)

Exotic natural enemies introduced from different countries, by EMBRAPA-Wheat

WHEAT BIOLOGICAL CONTROL IN BRAZIL EXAMPLES OF SUCCESS

Ageniaspis citricola (Hymenoptera: Encyrtidae)

Phyllocnistis citrella (Lepidoptera: Gracillariidae)

Exotic natural enemy introduced from Gainesville, FL, USA, by ESALQ, EMBRAPA, GRAVENA and FUNDECITRUS

CITRUS A. citricola RELEASING AREAS (1) Colômbia (3) Novaes (1) Olímpia (2) (3) Altair (1) Monte Azul Pta (1) Orindiuva (1) Bebedouro (6) Pirangi (1) (1) (1) (1) Taquaral (3) Macedônia (1) Tabapuã (1) Taiaçú (1) Taiuva (1) (1) (2) Monte Alto (1) (1) Taquaritinga (4) Matão (4) Ubarana (2) Rincão (1) Adolfo (1) Mococa (1) Itápolis (7) Santa Lúcia (1) (3) Américo Brasiliense (1) Cafelândia (1) Casa Branca (2) (5) Lins (1) Aguaí (2) Getulina (1) Mogi-Guaçú (2) Pongai (1) Itirapina (1) Guarantã (1) (1) (2) Reginópolis (1) Eng. Coelho (2) Piraju (1) (1) Amparo (1) Itajú (1) Jaguariúna (1) Holambra (3) Tabatinga (2) Gavião Peixoto (4) Cordeirópolis (1) (1) (5) Brotas (4) Boa Esperança do Sul (4) Sarapuí (1) Piracicaba (1) Dourado (1) (1) Tatuí (1) Ribeirão Bonito (1) Buri (1) BIOLOGICAL CONTROL IN BRAZIL EXAMPLES OF SUCCESS

decade Trichogramma pretiosum (Hymenoptera: Trichogrammatidae)

Tuta absoluta (Lepidoptera: Gelechiidae)

Northeast part of Brazil, São Francisco Valley Exotic natural enemy introduced from Colombia, South America, by EMBRAPA

INDUSTRIAL TOMATO Haji et al. (2002) BIOLOGICAL CONTROL IN BRAZIL EXAMPLES OF SUCCESS

decade Trissolcus basalis Telenomus podisi (Hymenoptera: Platygastridae)

stink bugs (Hemiptera: Pentatomidae)

Native natural enemies reared by EMBRAPA-Soybean

SOYBEAN Corrêa-Ferreira (2002) Euschistus heros REARING There is a new dry artificial diet using lyophilized common bean and peanut seeds comparable to the natural diet for the neotropical brown stink bug.

Mendoza (2012) BIOLOGICAL CONTROL IN BRAZIL EXAMPLES OF SUCCESS

Diaphorina citri (Hemiptera: Liviidae)

Tamarixia radiata (Hymenoptera: Eulophidae)

Exotic natural enemy collected in Brazil in citrus groves by ESALQ and UNESP

CITRUS Gómez Torres et al. (2006) BIOLOGICAL CYCLE Tamarixia radiata MASS REARING Tamarixia radiata RELEASING AREAS STATE OF SÃO PAULO, BRAZIL

5.1x 49.5% 2.6x

Cajobi 86.2%

3.0x 3.4x Getulina Rincão 62.3% 53.3% Pirajuí 10.8x 7.9x Mogi Mirim 93.0% 51.5%

Tatuí 5.3x Regions HLB (%) 59.1% Center 73.5 North 28.2 2.5x 8.8 Northwest 69.6% West 47.4 Parasitization increase by T. radiata South 63.5 Reduction of D. citri population BIOLOGICAL CONTROL IN BRAZIL EXAMPLES OF SUCCESS

decade Diatraea saccharalis (Lepidoptera: Crambidae)

Cotesia flavipes (Hymenoptera: Braconidae)

Exotic natural enemy imported from Trinidad-Tobago and India/Pakistan by Planalsucar and ESALQ

SUGARCANE Botelho & Macedo (2002) BIOLOGICAL CONTROL IN BRAZIL Cotesia flavipes Sugarcane Borer infestation

1970´s decade in the State of São Paulo BIOLOGICAL CONTROL IN BRAZIL EXAMPLES OF SUCCESS Diatraea saccharalis decade (Lepidoptera: Crambidae)

Trichogramma galloi (Hymenoptera: Trichogrammatidae)

Native natural enemy from South America with a BC program developed by ESALQ

SUGARCANE Parra et al. (2010)

MASS REARED Trichogramma SPECIES IN BRAZIL

Zucchi, 1988 native species from South America sugarcane, corn

Riley, 1879 exotic species from North America tomato, corn, soybean

Oatman & Platner, 1983 exotic species from America corn TREATED AREA IN BRAZIL INSECTS

Cotesia flavipes

(sugarcane) Trichogramma galloi (sugarcane, corn) TREATED AREA IN BRAZIL PATHOGENS Metarhiziumcontrole biológico aplicado anisopliae (sugarcane) Trichoderma harzianum (soybean) Deladenus siricidicola (pinus) Baculovirus anticarsia (soybean) SUGARCANE AREA IN BRAZIL 8,5 MILLION HECTARES

Biological control Not treated

Parra et al. (2010) C. flavipes MASS PRODUCTION C. flavipes MASS PRODUCTION C. flavipes MASS PRODUCTION C. flavipes MASS PRODUCTION Trichogramma spp. MASS PRODUCTION

larvae rearing

trays with parasitized eggs Trichogramma spp. MASS PRODUCTION artificial diet Trichogramma spp. MASS PRODUCTION larval development

Factitious host - A. kuehniella Trichogramma spp. MASS PRODUCTION larval development Trichogramma spp. MASS PRODUCTION adult cages preparation Trichogramma spp. MASS PRODUCTION adult cages preparation Trichogramma spp. MASS PRODUCTION A. kuehniella emergence Trichogramma spp. MASS PRODUCTION adult cages preparation Trichogramma spp. MASS PRODUCTION adult cage

Factitious host - A. kuehniella Bottom cage Trichogramma spp. MASS PRODUCTION adult cages

Factitious host - A. kuehniella Trichogramma spp. MASS PRODUCTION egg collection Trichogramma spp. MASS PRODUCTION egg cleaning Trichogramma spp. MASS PRODUCTION A. kuehniella eggs Trichogramma spp. MASS PRODUCTION A. kuehniella eggs Trichogramma spp. MASS PRODUCTION UV chamber Trichogramma spp. MASS PRODUCTION Trichogramma card preparation Trichogramma spp. MASS PRODUCTION Trichogramma card preparation Trichogramma spp. MASS PRODUCTION Trichogramma card preparation Trichogramma spp. MASS PRODUCTION Trichogramma card preparation Trichogramma spp. MASS PRODUCTION parasitization

honey

Longevity (days) of T. pretiosum (25ºC) No food 1.3 ± 0.11 Honey 10% 2.4 ± 0.21 Pure honey 5.1 ± 0.65

Bleicher & Parra (1991) Trichogramma spp. MASS PRODUCTION Trichogramma spp. MASS PRODUCTION IN VITRO PRODUCTION OF Trichogramma IN BRAZIL

Cônsoli & Parra (1996) Biological Control 6: 401-406

Dias, Parra & Cônsoli (2010) Entomologia Experimentalis et Applicata 137: 126-131 POTENTIAL CROPS FOR BIOLOGICAL CONTROL UTILIZATION IN BRAZIL [email protected]