ECOLOGY AND BIOLOGY OF IN BRAZIL

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ECOLOGY AND BIOLOGY OF IN BRAZIL José Roberto P. Parra Mariuxi Lorena Gomez Torres Dori Edson Nava Paulo Eduardo Branco Paiva USDA, APHIS International Workshop on Tamarixia species McAllen, TX, Feb. 2-4, 2010 Depto. de Entomologia e Acarologia Esalq/USP, Brazil

Diaphorina citri Kuwayama, 1908 USA - Texas (2001) Mexico (2002) Guadeloupe (1998) Venezuela (1999) Argentina (1997) Halbert & Nuñez (2004) USA - Florida + Caribbean (1998) Dominican Republic (2001) Brazil (1942) Puerto Rico (2002) Cuba (2001) (COSTA LIMA, 1942) (SILVA et al., 1968)

HOSTS Rutaceae 21 species (some of them incomplete development only egg laying) Murraya paniculata (Orange jessamine)

FRUITS WITH GREENING SYMPTOM Photos: P.T. Yamamoto

nymph adult LIFE CYCLE OF D. citri eggs nymph

Diaphorina citri Duration and viability of egg and nymphal stages at different hosts. 24ºC, RH: 70% and 14h photophase. Host Duration (days) Viability (%) Egg Nymph Egg Nymph Sex Ratio Rangpur lime 3.61a 14.0a 87.5a 82.4a 0.50a Orange jessamine 3.63a 14.1a 88.4a 88.8a 0.50a Sunki mandarin 3.57a 13.5a 89.8a 44.6b 0.47a Mean values followed by the same letter in the column are not different by Tukey test (P>0.05). NAVA et al. (2007)

Diaphorina citri Number of eggs 450 400 350 300 250 200 150 100 50 0 ab 265.1 Rangpur lime a 348.37 Orange jessamine b 166.22 Sunki mandarin Mean values followed by the same letter in the column are not different by Tukey test (P>0.05). Mean number of eggs of D. citri reared on different hosts. 24ºC, RH: 70% and 14h photophase. NAVA et al. (2007)

Diaphorina citri Mean duration for the egg and nymphal stages and biological cycle (eggadult) of D. citri reared on Rangpur lime at different temperatures. RH: 70% and 14h photophase. Temperature (ºC) 18 20 22 25 28 30 32 Egg 7.7 a 6.4 b 5.9 b 4.5 c 3.2 d 2.9 d 2.6 d Nymph days 35.8 a 24.5 b 23.8 b 12.6 c 12.2 c 9.4 c 9.4 c Biological cycle 43.5 a 30.9 b 29.6 b 17.1 c 15.4 cd 12.4 d 12.1 d NAVA et al. (2007)

Diaphorina citri Mean viability for the egg and nymphal stages and biological cycle (egg-adult) of D. citri reared on Rangpur lime at different temperatures. RH: 70% and 14h photophase. Temperature (ºC) 18 20 22 25 28 30 32 Egg 95.0 a 95.2 a 88.4 a 93.8 a 89.8 a 90.5 a 81.6 a Nymph % 70.7 a 70.0 a 72.5 a 74.0 a 77.5 a 73.8 a 15.0 b Biological cycle 69.9 a 66.6 a 64.1 a 69.4 a 69.5 a 66.8 a 12.2 b NAVA et al. (2007)

NATURAL ENEMIES Ectoparasitoid entomophages Endoparasitoid Predators Tamarixia radiata (Hym.: Eulophidae) Diaphorencyrtus aligarhensis (Hym.: Encyrtidae) Coccinelids and green lacewings

SUCCESSFUL INTRODUCTIONS OF T. radiata Dominica Guadeloupe 1999 (1,000 adults) St. Lucia Barbados Reunión Isles 1978 (4,600 adults) Etienne et al. (2001)

Tamarixia radiata polychromatic variation typical Highly similar at the molecular level (ITS1 and ITS2 markers).

adult Parasitization Emergence mummy Barretos 57.7% (67.2%) Pongai 36.5% (43.2%) Guarantã 39.3% (79.7%) Collected in Jaboticabal and Piracicaba counties, State of São Paulo, in 2006. Pederneiras 57.9% (64.5%) Ribeirão Bonito 80.0% (50.0%) Casa Branca 27.5% (78.5%) São Carlos 76.9% (77.1%) Botucatu 37.5% (62.5%) Itirapina 48.8% (79.2%) Torres et al. (2006)

PRODUCTION SYSTEM OF Phyllocnistis citrella AND Ageniaspis citricola Chagas et al. (2002)

BIOLOGICAL CYCLE Torres & Parra (in preparation)

Infestation Diaphorina citri Flushing egg 15-17 days Population maintenance Cutting the leaves young nymphs Adult releasing Rearing maintenance 24-48 hr Parasitization Tamarixia radiata 24-48 hr Parasitoid development 12-15 days parasitoid pupae Torres & Parra (in preparation)

Tamarixia radiata Mean duration of T. radiata reared on D. citri at different temperatures. RH: 70% and 14h photophase. Temperature (ºC) 18 20 22 25 28 30 32 Duration (days) 17.31 a 14.20 b 12.46 c 10.33 d 10.09 d 7.55 e 7.59 e Mean values followed by the same letter in the column are not different by Tukey test (P>0.05). Torres & Parra (in preparation)

Tamarixia radiata Fertility life table of T. radiata reared on D. citri at different temperatures. RH: 70% and 14h photophase. Temperature (ºC) 15 20 25 30 35 Ro 9.88 23.62 126.79 58.63 21.27 r m 0.1826 0.2531 0.3742 0.3378 0.2528 λ 1.2003 1.2880 1.4538 1.4019 1.2889 Torres & Parra (in preparation)

Tamarixia radiata 100 a Parasitization (%) 80 60 40 20 c 22.92 b 44.79 84.17 a 72.50 b 40.63 0 15 20 25 30 35 Temperature (ºC) Parasitization of D. citri by T. radiata at different temperatures during 24h. RH: 70% and 14h photophase. Torres & Parra (in preparation)

Tamarixia radiata Emergence (%) 100 80 60 40 20 b 45.83 b 49.66 a 86.49 a 88.41 a 78.81 0 15 20 25 30 35 Temperature (ºC) T. radiata emergence on D. citri at different temperatures. RH: 70% and 14h photophase. Torres & Parra (in preparation)

Tamarixia radiata adult feeding x parasitization (25 2ºC; 70±10%; photophase: 14h) Food Honey Honey + pollen Honey + yeast Nymphs Without food Parasitization (%) 32.50 b 63.64 a 22.86 b 37.50 b 19.44 b Torres & Parra (in preparation)

Tamarixia radiata biological development egg prepupa pupa close to emergency female adult male Torres & Parra (in preparation)

D. citri x T. radiata parasitization Parasitization (%) 100 80 60 40 20 (25 2ºC; 70±10%; photophase: 14h) b a 61.25 a 88.75 0 c c 13.13 1 2 3 4 5 Instars Torres & Parra (in preparation)

D. citri x T. radiata parasitization at different temperatures 35 c Temperature (ºC) 30 25 20 c b a 15 d 0 50 100 150 200 Parasitized nymphs (total) Torres & Parra (in preparation)

Tamarixia radiata parasitization in different varieties 2005-2007 Variety Hamlin Pêra Natal Valência Parasitization (%) 35.6 ± 11.5 19.2 ± 6.5 7.3 ± 5.9 8.6 ± 2.3 Paiva (2009)

Tamarixia radiata ab c 90% a a 70% RH b b 50% Parasitization (%) b c 30% Emergence (%) Parasitization and emergence of T. radiata at different RH. 25ºC and photophase of 14h. Torres & Parra (in preparation)

D. citri x T. radiata 4 th 5 th instars nymph reduction after release Araras, SP 100 Before release After release Nymphs reduction (%) 80 60 40 20 0 Control area Area A Area B Torres & Parra (in preparation)

D. citri x T. radiata parasitization after release Araras, SP Parasitization (%) 100 80 60 40 51.57 72.75 Area A Area B Control area 20 0 Before release 10.00 0.00 4.17 0.00 8 days after release 15 days after release Torres & Parra (in preparation)

D. citri x T. radiata 100 80 parasitization after release Cordeirópolis 100 80 (control) 60 60 40 40 20 20 0 Before releasing Releasing (1) Releasing (2) Releasing (3) 0 Before releasing Releasing (1) Releasing (2) Releasing (3) 100 80 Nymphs (4 th -5 th instar) Parasitization Limeira 100 80 (control) 60 60 40 40 20 20 0 Before releasing Releasing (1) Releasing (2) Releasing (3) 0 Before releasing Releasing (1) Releasing (2) Releasing (3) Torres & Parra (in preparation)

Tamarixia radiata and Wolbachia 60 Honey + pollen (W+) Honey + pollen + antibiotic (W-) a Parasitization (%) 40 20 a 30.29 b 19.80 46.52 b 41.26 0 Parasitization (%) Emergence (%) Torres, Cônsoli & Parra (in preparation)

Zoning of Diaphorina citri and Tamarixia radiata in the State of São Paulo, Brazil using Geographic Information System (GIS) D. citri TT = 13.5ºC K = 210.9 DD RH = 70 85% T. radiata TT = 7.1ºC K = 187.5 DD RH = 70% Development range 18 30ºC 25 30ºC

Tamarixia radiata cycles Diaphorina citri cycles Isothermal Map Torres & Parra (in preparation)

Relationship between D. citri and T. radiata life cycles in São Paulo state Region North Northeast Southwest Southeast D. citri : T. radiata 1 : 2.6-3.1 1 : 3.1-4.0 1 : 3.1-6.3 1 : 3.1-6.3 Torres & Parra (in preparation)

FINAL REMARKS The most important restriction is the spraying to control the vector; Then, it is very important to select pesticides (selective products); Selection of T. radiata strain; To increase the parasitoid population, release in alternative hosts; Scale up the parasitoid rearing system in order to release in problem areas; Validate the parasitoid and vector zoning.

Acknowledgments To CNPq, Fapesp and Fundecitrus for financial support