Content uploaded by Takumasa Kondo
Author content
All content in this area was uploaded by Takumasa Kondo
Content may be subject to copyright.
48 Kondo et al., first report of Tamarixia radiata, a parasitoid of Diaphorina citri.
NOTA CIENTÍFICA
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.
LITERATURE CITED
Augier, L., G. Gastaminza, M. Lizondo, M. Argañaraz & E. Willink. 2006. Presencia de Diaphorina citri
(Hemiptera: Psyllidae) en el Noroeste Argentino (NOA). Revista de la Sociedad Entomológica Ar-
gentina 65 (3-4): 67-68.
Cermeli, M., P. Morales Valle, J. Perozo & F. Godoy. 2007. Distribución del psílido asiático de los cítricos
(Diaphorina citri Kuwayama (Hemiptera, Psyllidae) y presencia de Tamarixia radiata (Waterston)
(Hymenoptera, Eulophidae) en Venezuela. Entomotrópica. 22(3): 181-184.
Étienne, J. & B. Aubert. 1980. Biological control of psyllid vectors of greening disease on Reunion Island.
Pp. 118-121, in: Proceedings, 8th Conference of the International Organization of Citrus Virolo-
gists, 13-31 May 1979, Sidney, Australia. University of California Press, Riverside, CA.
Étienne, J., S. Quilici, D. Marival & A. Franck. 2001. Biological control of Diaphorina citri (Hemiptera:
Psyllidae) in Guadeloupe by imported Tamarixia radiata (Hymenoptera: Eulophidae). Fruits, 56:
307-315.
European and Mediterranean Plant Protection Organization (EPPO). 2005. Data Sheets on Quarantine Pests:
Diaphorina citri. http://www.eppo.org/QUARANTINE/insects/Diaphorina_citri/DIAACI_ds.pdf
(accessed on 3/01/2012).
Halbert, S. E. & K. L. Manjunath. 2004. Asian citrus psyllids (Sternorrhyncha: Psyllidae) and greening disea-
se of citrus: a literature review and assessment of risk in Florida. Florida Entomologist, 87: 330-
353.
Halbert, S. E. & C. A. Núñez. 2004. Distribution of the Asian citrus psyllid, Diaphorina citri Kuwayama
(Rhynchota: Psyllidae), in the Caribbean basin. Florida Entomologist, 87 (3): 401-402.
Hayat, M. & M. H. Shahi. 2004. Taxonomic notes on Indian Eulophidae (Hymenoptera: Chalcidoidea) - 1. On
the types of some Tetrastichinae. Oriental Insects, 38: 303-314.
Instituto Colombiano Agropecuario (ICA). 2010. Situación actual de HLB (Huanglonbing) y su vector el psi-
lido asiático de los cítricos (Diaphorina citri Kuwayama) en Colombia. Boletín epidemiológico.
LaSalle, J. 1994. North American genera of Tetrastichinae (Hymenoptera: Eulophidae). Journal of Natural
History, 28: 109-236.
Lizondo, M. J., G. Gastaminza, V. A. Costa, L. Augier, M. L. Gómez Torres, E. Willink & J. R. P. Parra.
2007. Records of Tamarixia radiata (Hymenoptera: Eulophidae) in Northwestern Argentina. Re-
vista Industrial y Agrícola de Tucumán, 84(1): 21-22.
Manjunath, K. L., S. E. Halbert, C. Ramadugu, S. Webb & R. F. Lee. 2008. Detection of ‘Candidatus Liberi-
bacter asiaticus’ in Diaphorina citri and its importance in the management of Citrus Huanglong-
bing in Florida. Phytopathology, 98(4): 387-396.
Mann, R. S. & L. L. Stelinski. 2010. An Asian citrus psyllid parasitoid, Tamarixia radiata (Waterston). Featu-
red Creatures. EENY-475. http://entnemdept.ifas. ufl.edu/creatures/beneficial/wasps/tamarixia_ ra-
diata.htm (accessed on 3/01/2012).
Michaud, J. P. 2004. Natural mortality of Asian citrus psyllid (Homoptera: Psyllidae) in Central Florida. Bio-
logical Control, 29(2): 260-269.
Noyes, J. S. 2011. Universal Chalcidoidea Database website. www.nhm.ac.uk/entomology/chalcidoids/index.
html (accessed on 4/01/2012).
Prinsloo, G. L. 1980. Annotated records of economically important Chalcidoidea (Hymenoptera) from South
Africa. I. Phytophylactica, 12: 159-163.
Rubio, T., M. Zambrano, A. Castro A., V. A. Costa & E. Ebratt 2011. Diaphorina citri Kuwayama y Tamari-
xia radiata (Waterson) en cultivos de cítricos de Cundinamarca, Colombia. Pp. 105, in: Abstracts
Boletín del Museo de Entomología de la Universidad del Valle 13(1): 48-51, 2012 51
of the XXXVIII Congreso de la Sociedad Colombiana de Entomología (SOCOLEN). July 27-29,
2011. Manizales, Colombia.
Villalobos, W., D. Hollis, C. Godoy & C. Rivera. 2005. First report of Diaphorina citri (Hemiptera: Psylli-
dae) in Costa Rica. Insecta Mundi, 19(3): 151-152.
Waterston, J. 1922. On the chalcid parasites of psyllids (Homoptera). Bulletin of Entomological Research, 13:
41-58.
Zuparko, R. L., D. L. De Queiroz & J. LaSalle. 2011. Two new species of Tamarixia (Hymenoptera: Eulop-
hidae) from Chile and Australia, established as biological control agents of invasive psyllids (He-
miptera: Calophyidae, Triozidae) in California. Zootaxa, 2921: 13-27.
Recibido enero 6, 2012, publicado julio 2012