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First report of Tamarixia radiata (Waterston) (Hymenoptera: Eulophidae), a parasitoid of the asian citrus psyllid Diaphorina citri Kuwayama (Hemiptera: Psyllidae) in the state of Valle del Cauca, Colombia.

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Abstract

Here we report for the first time the presence of Tamarixia radiata (Waterston) (Hymenoptera: Eulophidae) parasitizing the Asian citrus psyllid Diaphorina citri Kuwayama (Hemiptera: Psyllidae) in three municipalities, i.e, Palmira, Sevilla and Zarzal, in the Department of Valle del Cauca, Colombia.
48 Kondo et al., first report of Tamarixia radiata, a parasitoid of Diaphorina citri.
NOTA CIENFICA
FIRST REPORT OF TAMARIXIA RADIATA (WATERSTON) (HYMENOPTERA: EULOPHIDAE), A
PARASITOID OF THE ASIAN CITRUS PSYLLID DIAPHORINA CITRI KUWAYAMA
(HEMIPTERA: PSYLLIDAE) IN THE DEPARTMENT OF VALLE DEL CAUCA, COLOMBIA
Takumasa Kondo, Edgar Mauricio Quintero Q.
Corporación Colombiana de Investigación Agropecuaria (CORPOICA), Centro de Investigación Palmira,
Colombia; correo electrónico: takumasa.kondo@gmail.com; emquinteroq@gmail.com
Mauricio Campuzano, Kris A. G. Wyckhuys
International Center for Tropical Agriculture CIAT, Recta Palmira-Cali, Cali, Valle del Cauca, Colombia;
correo electrónico: ngeniero.agropaisajes@gmail.com; kwyck2012@gmail.com
John Heraty
Department of Entomology, University of California, Riverside, C A, USA; correo electrónico:
john.heraty@ucr.edu
Figure 1. Tamarixia radiata (Waterston). A, emerging from Diaphorina citri nymph; B, male. Note plumose
antennae; C, female. Photos by E.M. Quintero.
Here we report for the first time the presence of
Tamarixia radiata (Waterston) (Hymenoptera:
Eulophidae) (Figure 1) parasitizing the Asian ci-
trus psyllid Diaphorina citri Kuwayama (Hemip-
tera: Psyllidae) in three municipalities, i.e, Palmi-
ra, Sevilla and Zarzal, in the Department of Valle
del Cauca, Colombia.
The Asian citrus psyllid D. citri is an economi-
cally important citrus pest in many citrus growing
regions of the world (Halbert & Manjunath 2004;
Manjunath et al. 2008). Diaphorina citri has a
wide distribution, recorded from Asia [Afghanis-
tan, Bangladesh, Cambodia (unconfirmed), China,
Hong Kong, India, Indonesia, Japan (Ryukyu Is-
lands), Lao, Macau, Malaysia, Myanmar, Nepal,
Pakistan, Philippines, Saudi Arabia, Singapore,
Sri Lanka, Taiwan, Thailand, Vietnam], Africa
[Mauritius, Réunion], the Caribbean [Bahamas,
Belize (from interception), Cayman Islands, Cuba,
Dominican Republic, Guadeloupe, Jamaica, Puer-
to Rico, and St. Thomas (from interception)],
Central America [Honduras (from interception)
and Mexico], South America [Argentina, Brazil,
Boletín del Museo de Entomología de la Universidad del Valle 13(1): 48-51, 2012 49
Colombia, Paraguay, Uruguay and Venezuela]
and North America [USA] (Augier et al. 2006,
Cermeli et al. 2007, EPPO 2005, Étienne et al.
2001, Halbert & Núñez 2004, ICA 2010, Villalo-
bos et al. 2005). Diaphorina citri was reported in
Colombia for the first time in 2007 and has been
recorded since from the Departments of Antio-
quia, Atlántico, Bolívar, Caldas, Cauca, Cesar,
Córdoba, Cundinamarca, Magdalena, Meta, Norte
de Santander, Quindío, Risaralda, Santander, Su-
cre, Tolima, and Valle del Cauca (ICA 2010).
The Asian citrus psyllid D. citri can cause direct
damage by sucking large amounts of sap, injecting
toxins that cause malformation of leaves and
shoots and by inducing sooty molds that grow on
its excreted honeydew (Michaud 2004). Moreo-
ver, D. citri is a vector of the phloem limited
gram-negative bacterium Candidatus Liberibacter
asiaticus, one of the pathogens that cause the de-
vastating citrus disease “Huanglongbing” (HLB)
or citrus greening disease (Halbert & Manjunath
2004).
Because of the importance of D. citri as a vector
of HLB, controlling this insect is a critical com-
ponent of disease prevention, containment and
management. In Reunion Island where D. citri has
been introduced, the psyllid has been controlled
successfully with the introduction of the ectopara-
sitoid T. radiata introduced from Pakistan (Étien-
ne & Aubert 1980).
Tamarixia radiata has been reported in Argentina,
Brazil, China, Guadeloupe, India, Indonesia, Ma-
laysia, Mauritius Mexico, Nepal, Pakistan, Philip-
pines, Puerto Rico, Réunion, Saudi Arabia, Tai-
wan, Thailand, USA (Florida and Texas), Vene-
zuela and Vietnam (Cermeli et al. 2007, Lizondo
et al. 2007, Mann & Stelinski 2010, Zuparko et al.
2011). In mid 2011, T. radiata was suspected to
parasitize D. citri in citrus orchards in the Colom-
bian State of Cundinamarca (Rubio et al. 2011),
but taxonomic confirmation is pending. This is the
first scientific report of T. radiata in Colombia.
Samples of parasitoids species of Diaphorina citri
were collected on the leaves of three Citrus spp.
(Rutaceae): Citrus reticulata Blanco, Citrus si-
nensis (L.) Osbeck cv. Salustiana and Citrus lati-
folia Tanaka. Specimens were identified as Tama-
rixia radiata (Waterston) by JH using the original
description (Waterston 1922) and additional
comments by Prinsloo (1980) and Hayat & Shahi
(2004). There are 47 described species of Tamari-
xia and only identification to regional faunas in
North America, Europe and India (Zuparko et al.
2011). Prior to the introduction of T. radiata, Ta-
marixia was not recorded from South America ot-
her than a casual record of some unplaced species
(LaSalle 1994). Tamarixia radiata can be distin-
guished by a combination of having the wing
speculum with sparse setae, the femora and tibia
usually completely yellow, at most slightly darke-
ned dorsally, the propodeal disc smooth and la-
cking carinae between the spiracle and median ca-
rina, and the abdomen dark laterally and dorso-
medially yellow (less pronounced and more ante-
rior in male). The male has a distinct ventral sense
organ located in the basal third of the scape (cf.
fig. 7, Waterston 1922) rather than being located
medially. Because of recent biological control ef-
forts, T. radiata is being spread in citrus-growing
regions worldwide (Michaud 2004, Noyes 2011,
Zuparko et al. 2011).
Material studied. Tamarixia radiata (Waterston).
Colombia: Valle del Cauca, Palmira, Corpoica
Research Station, 03°30'32"N, 76°19'12"W, 1015
m, 08.ix.2011, E.M. Quintero & T. Kondo, ex
Diaphorina citri Kuwayama (Hemiptera: Psylli-
dae) on Citrus reticulata Blanco (Rutaceae),
TK001 (5 females); same data except TK002 (1
male); TK003 (1 male); same data except on Ci-
trus sinensis (L.) Osbeck cv. Salustiana, TK004 (1
male), TK005 (1 male), TK006 (3 males), TK010
(5 females and 3 males). Colombia: Valle del
Cauca, Zarzal, finca Las Lajas, 04°25'33''N,
76°04'06''W, 914 m, 14.vii.2011, Mauricio
Campuzano, ex Diaphorina citri, on Citrus latifo-
lia Tanaka, CIAT-002 (1 male, no head and in
poor shape, indentity questionable); same data as
CIAT-002 except CIAT-003 (1 female); same da-
ta, except CIAT-004, 07.x.2011 (1 female). Co-
lombia: Valle del Cauca, Sevilla, vereda Altomi-
ra, finca Frutales Altomira, 04°21'59.05''N,
75°53'18''W, 1158 m, 06.x.2011, Mauricio
Campuzano, ex Diaphorina citri, on Citrus reticu-
lata, CIAT-005 (1 female). Colombia: Valle del
Cauca, Sevilla, vereda Altomira, finca El Danu-
bio, 04°20'29''N, 75°52'51''W, 1182 m,
02.xi.2011, Mauricio Campuzano, ex Diaphorina
citri, on Citrus reticulata, CIAT-006 (1 male). All
material deposited at the Department of Entomo-
logy, University of California, Riverside (UCRC).
Voucher specimens for material collected by
EMQ and TK are deposited at the Entomology co-
llection of Corpoica Palmira Research Station.
50 Kondo et al., first report of Tamarixia radiata, a parasitoid of Diaphorina citri.
ACKNOWLEDGEMENTS
The authors thank the Colombian Ministry of
Agriculture and Rural Development (MADR) that
funded the short-termed research project: “Plan de
contingencia para el manejo de Diaphorina citri
vector de HLB (enfermedad catastrófica de cítri-
cos) y caracterización de enemigos naturales”.
Many thanks to Juan Humberto Guarin for mana-
ging the funds for Corpoica. Part of the sampling
was carried out within the project “Agricultura
Específica por Sitio Compartiendo Experiencias
(AESCE)”, which is funded through Asohofrucol.
Funds of the latter project were managed by
CIAT.
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Recibido enero 6, 2012, publicado julio 2012
... En consecuencia, este himenóptero ha sido ampliamente estudiado y descrito en numerosos países como un efectivo agente de control biológico (ACB) de D. citri (Postali-Parra et al. 2016). En Colombia, Ebratt-Ravelo et al. (2011a) y Kondo et al. (2012) lo reportaron asociado al vector. En este manual se describen los pasos esenciales del proceso de cría masiva de T. radiata adaptados a las condiciones del Valle del Cauca, Colombia; se tomó como base el modelo de producción del parasitoide que se utiliza en México (Sánchez- González et al. 2015). ...
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... Los adultos de T. radiata son pequeñas avispas negras de 0,92 a 1,04 mm de largo, con los ojos bastante separados (figura 3a, b y c); la cabeza es un poco más ancha que larga y las alas son hialinas con venas amarillo pálido (Kondo et al. 2012). El dimorfismo sexual es evidente entre el macho (figura 3b) y la hembra adulta (figura 3c); los machos son ligeramente más pequeños que las hembras en cuanto a la longitud total y la extensión de las alas; el ovipositor de la hembra apenas sobresale del abdomen (figura 3c) (Waterston 1922). ...
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The Asian citrus psyllid, Diaphorina citri Kuwayama, was discovered in Florida in 1998. It can be one of the most serious pests of citrus if the pathogens that cause citrus greening disease (huanglongbing) are present. Citrus greening recently has been reported in Brazil by Fundecitrus, Brazil. The establishment of D. citri in Florida increases the possibility that the disease may become established. Diaphorina citri can be separated from about 13 other species of psyllids reported on citrus. The biology of D. citri makes it ideally suited to the Florida climate. Only two species, D. citri and Trioza erytreae (del Guercio), have been implicated in spread of citrus greening, a disease caused by highly fastidious phloem-inhabiting bacteria. The disease is characterized by blotchy mottle on the leaves, and misshapen, poorly colored off-tasting fruit. In areas where the disease is endemic, citrus trees may live for only 5-8 years and never bear usable fruit. The disease occurs throughout much of Asia and Africa south of the Sahara Desert, on several small islands in the Indian Ocean, and in the Saudi Arabian Peninsula. Transmission of citrus greening occurs primarily via infective citrus psyllids and grafting. It is transmissible experimentally through dodder and might be transmitted by seed from infected plants and transovarially in psyllid vectors. Citrus greening disease is restricted to Citrus and close citrus relatives because of the narrow host range of the psyllid vectors. Management of citrus greening disease is difficult and requires an integrated approach including use of clean stock, elimination of inoculum via voluntary and regulatory means, use of pesticides to control psyllid vectors in the citrus crop, and biological control of psyllid vectors in non-crop reservoirs. There is no place in the world where citrus greening disease occurs that it is under completely successful management. Eradication of citrus greening disease may be possible if it is detected early. Research is needed on rapid and robust diagnosis, disease epidemiology, and psyllid vector control.
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The Asian citrus psyllid, Diaphorina citri Kuwayama, was discovered in Florida in 1998. It can be one of the most serious pests of citrus if the pathogens that cause citrus greening disease (huanglongbing) are present. Citrus greening recently has been reported in Brazil by Fundecitrus, Brazil. The establishment of D. citri in Florida increases the possibility that the disease may become established. Diaphorina citri can be separated from about 13 other species of psyllids reported on citrus. The biology of D. citri makes it ideally suited to the Florida climate. Only two species, D. citri and Trioza erytreae (del Guercio), have been implicated in spread of citrus greening, a disease caused by highly fastidious phloem-inhabiting bacteria. The disease is characterized by blotchy mottle on the leaves, and misshapen, poorly colored off-tasting fruit. In areas where the disease is endemic, citrus trees may live for only 5-8 years and never bear usable fruit. The disease occurs throughout much of Asia and Africa south of the Sahara Desert, on several small islands in the Indian Ocean, and in the Saudi Arabian Peninsula. Transmission of citrus greening occurs primarily via infective citrus psyllids and grafting. It is transmissible experimentally through dodder and might be transmitted by seed from infected plants and transovarially in psyllid vectors. Citrus greening disease is restricted to Citrus and close citrus relatives because of the narrow host range of the psyllid vectors. Management of citrus greening disease is difficult and requires an integrated approach including use of clean stock, elimination of inoculum via voluntary and regulatory means, use of pesticides to control psyllid vectors in the citrus crop, and biological control of psyllid vectors in non-crop reservoirs. There is no place in the world where citrus greening disease occurs that it is under completely successful management. Eradication of citrus greening disease may be possible if it is detected early. Research is needed on rapid and robust diagnosis, disease epidemiology, and psyllid vector control.
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Asian citrus psyllid, Diaphorina citri Kuwayama (Rhynchota: Psyllidae), originally is from Asia but has been known in the Western Hemisphere for several decades. In 1998, it was discovered for the first time in the Caribbean Basin both in Guadeloupe and in Florida. Since then, it has spread widely among islands and adjacent mainland countries, including the Bahamas, the Cayman Islands, Jamaica, Dominican Republic, Cuba, Puerto Rico, Venezuela, Mexico, and Texas (USA). Additionally, there were interceptions of D. citri from St. Thomas and Belize. In Asia, D. citri primarily causes damage to citrus as a result of transmission of the pathogens that cause citrus greening disease. In July 2004, as this paper was going to press, citrus greening disease was reported in Brazil by Fundecitrus. This is the first credible report of the disease in the Western Hemisphere.
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