First records of parasitoids attacking the Asian citrus psyllid in Ecuador

Portalanza, Diego E.; Sanchez, Luis; Plúas, Marjorie; Felix, Imelda; Costa, Valmir A.; Dias-Pini, Nivia da Silva; Ferreira-Stafanous, Sheryl; Gómez-Torres, Mariuxi L.

doi:10.1016/j.rbe.2017.02.002

ABSTRACT

First records of parasitoids attacking the Asian citrus psyllid in Ecuador. The objective of the current study was to investigate the presence of natural enemies of Diaphorina citri (Hemiptera: Liviidae) (the Asian citrus psyllid) in Ecuador. Incidence of parasitoid Diaphorencyrtus aligarhensis (Hymenoptera: Encyrtidae) was assessed between November 2015 and March 2016, in Letamendi, Febres-Cordero and Tarqui, urban districts of Guayaquil. Highest incidence of parasitism occurred in those regions and seasons of the year with the highest temperatures commensurate with increase of citrus plant shoots. Similar to their host, these parasitoids appear to have established in Ecuador by accident, and were not the result of purposeful introduction. This fortuitous introduction is a potentially helpful tool in controlling the Asian citrus psyllid, and potentially Huanglongbing.

Keywords: Diaphorencyrtus aligarhensis; Diaphorina citri; Endoparasitoid; Huanglongbing; Tamarixia radiata

Diaphorina citri Kuwayama (Hemiptera: Liviidae) is distributed throughout Southeast Asia, India, Saudi Arabia, Mauritius and Reunion islands, Brazil, Uruguay (EPPO, 2014), Colombia (Moncayo-Donoso et al., 2014), Ecuador (Cornejo and Chica, 2014), U.S. (Sétamou et al., 2008), Argentina, Venezuela, Mexico and in some countries of the Caribbean and Central America (EPPO, 2014; SENASICA, 2012).

Among D. citri cataloged hosts there are 25 genera in the family Rutaceae, primarily Citropsis, Citrus and Murraya (Ikeda and Ashihara, 2008). Due to their distribution and biological characteristics it is the most important vector of huanglongbing (HLB) or greening, the main citrus disease worldwide (Bove, 2006; Wang and Trivedi, 2013).

Transmission of pathogens by arthropods is a serious problem for agriculture. In order to address these agricultural problems and to maintain the quality of agro-ecosystems, biological control tactics are being used to reduce the pest. The idiobiont ectoparasitoid Tamarixia radiata (Waterston) (Hymenoptera: Eulophidae) and the arrhenotokous endoparasitoid Diaphorencyrtus aligarhensis (Shaffee, Alam and Agarwal) (Hymenoptera: Encyrtidae) have been used in programs of classical biological control to the population of D. citri in different regions of the world (Gómez-Torres et al., 2006; Parra et al., 2007).

Tamarixia radiata is the main agent of biological control of D. citri. This parasitoid has high efficiency of parasitism and a great capacity for dispersal, establishment, and field adaptation. Thus, the success of T. radiata releases for biological control of D. citri, and consequently the HLB, was reported in the Reunion, Mauritius and Guadeloupe islands (Étienne et al., 2001), Taiwan (Chien et al., 1991) and in USA (Hall et al., 2008).

Diaphorencyrtus aligarhensis preferentially parasitizes second and third instar D. citri (Sule et al., 2014). In addition to parasitization, females can kill D. citri nymphs via host feeding (Rohrig et al., 2011). D. aligarhensis has been used against D. citri in various citrus-growing regions including Taiwan, Reunion Island, Saudi Arabia, and Florida (Rohrig et al., 2012). Florida populations of D. aligarhensis, sourced from Taiwan and China, have failed to establish, despite repeated release efforts (Rohrig et al., 2012; Bistline-East et al., 2015).

Despite the presence of D. citri being reported in Ecuador since 2014 (Cornejo and Chica, 2014), so far no parasitoid populations have been detected which might help to keep balance of this pest. Within this context, the aim of this study was to survey the population of D. citri in Ecuadorian regions where it has been reported, and determine variations among pest populations in different seasons and consequently identify the parasitoids associated with this psyllid.

Diaphorina citri population's assessment in urban and rural areas of Guayas province:

To identify D. citri's associated parasitoids, samples were taken in urban districts in the city of Guayaquil: Ximena (2° 13' 35" S-79° 53' 45" W), Febres-Cordero (2° 11' 45" S-79° 54' 54" W), Urdaneta (2° 12' 08" S-79° 54' 20" W), Rocafuerte (2° 11' 16" S-79° 52' 44" W), Tarqui (2° 09' 52" S-79° 56' 14" W), Chongon (2° 16' 56" S-80°11' 08" W), Letamendi (2° 12' 15" S-79° 54' 12" W), and other cities of Guayas province: El Empalme (0° 56' 32" S-79° 37' 49" W), Balzar (1° 17' 36" S-79° 52' 49" W), Colimes (1° 32' 22" S-79° 58' 25" W), Santa Lucía (1° 41' 30" S-79° 59' 14" W), Pedro Carbo (1° 48' 58" S-80° 18' 22" W), Daule (1° 51' 26" S-79° 52' 08" W), Alfredo Baquerizo Moreno (1° 55' 24" S-79° 32' 31" W), Milagro (2° 09' 01" S-79° 35' 48" W), Naranjal (2° 40' 41" S-79° 38' 24" W), Balao (2° 53' 38" S-79° 41' 12" W) between April 2013 and April 2016 at every 15 days (Fig. 1).

Fig. 1
Diaphorina citri surveys between April 2013 and 2016. Points represent monitored areas in Guayas province, Ecuador. The lower box represents where the province is located.

In each case, a collection was taken from ten branches with buds from thirty plants showing nymphs of D. citri. The collection was made by following a protocol previously defined and with reference established by Gómez-Torres et al. (2006), samples were taken very carefully using secateurs being careful not to disturb the insects present in each stratum until packaging for transport.

The collected twigs were placed in paper bags (30 cm × 15 cm), properly labeled, and conditioned at 22 ± 3 °C in a Waeco^® electric Cooler box model CarFridge (17.5 cm × 31 cm × 31 cm) where they were transported to the laboratory and immediately transferred to acrylic cages (35 cm × 45 cm × 35 cm). Then, they were deposited on properly sterilized plastic trays containing a moistened filter paper sheet. For proper conservation of the collected material, the laboratory was maintained at 25 ± 1° C, relative humidity of 80 ± 10% and a 12 h photo phase.

Every 24 h, the acrylic cages containing the nymphs were observed for the extraction of emerged parasitoids, which were dried in a critical point dryer (Leica CPD 030) and double-mounted on points. Parasitoid identification was done according to Noyes (1980) and Hayat (1981) for genus and to Shafee et al. (1975) for species. The percentage of emergence was 78.05. The specimens were deposited at Coleção de Insetos Entomófagos Oscar Monte (Instituto Biológico, Campinas, São Paulo, Brazil). Parasitoids collected emerged on nymphs of D. citri were identified as D. aligarhensis. Female and male specimens of Tamarixia radiata were also recorded.

Images of the identified material taken under the stereoscopic microscope and scanning electron microscope (SEM) were examined by Dr. John S. Noyes (Natural History Museum, London, UK), who confirmed the identification.

With these initial studies in Ecuador, the various collections demonstrated the natural presence of parasitoids D. aligarhensis and T. radiata in Letamendi, Febres-Cordero and Tarqui, urban districts of Guayaquil (Fig. 2). Thus, population variations of the pest and the parasitoid may occur at different times of the year, depending on the region and the management. The absence of natural enemies, in some localities, could be directly related to the indiscriminate application of chemicals used to control insects and mites, as well as D. citri.

Fig. 2
Letamendi, Febres Cordero and Tarqui (triangles), Guayaquil city urban districts where Diaphorencyrtus aligarhensis was detected. The lower box represents where the city is located.

Establishment of this parasitoid in other countries of South America has not been reported. Similar to D. citri, the endoparasitoid D. aligarhensis appears to have established in Ecuador accidentally, and were not the result of purposeful introduction. It is not unusual for this parasitoid to be discovered in non-release locations in Hawaii (Matsunaga, 2014).

This work fits within the objectives of the national plan of well living of Ecuador (Sumak Kawsay) 2012-2017 Article 7 "To guarantee the rights of nature and to promote environmental sustainability". With this record the possibility of adopting a new tactic for sustainable management of D. citri and thus maintain an ecological balance that allows sustainable and economically fair agriculture opens.

Acknowledgements

To Dr. John S. Noyes (Natural History Museum, London, UK), for the help on the identification of Diaphorencyrtus aligarhensis. To the "Instituto Nacional de Ciência e Tecnologia dos Hymenoptera Parasitoides da Região Sudeste Brasileira (INCT-Hympar Sudeste)", for financial support to one of the authors (VAC). To Eng. Javier Contreras (AGROCALIDAD) for technical support.

We express heartfelt thanks to Javier Ponce, Ministro de Agricultura, Ganadería, Acuacultura y Pesca del Ecuador for their support in creating the Red de Expertos en Protección Vegetal (MAGAP-REPV).

References

Bistline-East, A., Pandey, R., Kececi, M., Hoddle, M., 2015. Host range testing of Diaphorencyrtus aligarhensis (Hymenoptera: Encyrtidae) for use in classical biological control of Diaphorina citri (Hemiptera: Liviidae) in California. J. Econ. Entomol. 108, 940-950.
Bove, J.M., 2006. Huanglongbing: a destructive, newly-emerging, century-old disease of citrus. J. Plant Pathol. 88, 7-37.
Chien, C.C., Chu, Y.I., Ku, S.C., 1991. Biological control of citrus psyllid, Diaphorina citri in Taiwan. II. Evaluation of Tamarixia radiata and Diaphorencyrtus diaphorinae for the control of Diaphorina citri Chin. J. Entomol. 11, 25-38.
Cornejo, J.F., Chica, E.J., 2014. First record of Diaphorina citri (Hemiptera: Psyllidae) in Ecuador infesting urban citrus and orange jasmine trees. J. Insect Sci. 14, 1-1.
Étienne, J., Quilici, S., Marinal, D., Franck, A., 2001. Biological control of Diaphorina citri (Hemiptera: Psyllidae) in Guadeloupe by imported Tamarixia radiata (Hymenoptera: Eulophidae). Fruits 56, 307-315.
EPPO, 2014. Available at: https://www.eppo.int/QUARANTINE/data_sheets/insects/DIAACI_ds.pdf (accessed 21.04.16).
» https://www.eppo.int/QUARANTINE/data_sheets/insects/DIAACI_ds.pdf
Gómez-Torres, M.L., Nava, D., Gravena, S., Costa, V.A., Parra, J.R.P., 2006. Registro de Tamarixia radiata (Waterston) (Hymenoptera: Eulophidae) em Diaphorina citri Kuwayama Hemiptera: Psyllidae) em São Paulo. Rev. Agric. 81, 112-117.
Hall, D.G., Hentz, M.G., Adair, R.C., 2008. Population ecology and phenology of Diaphorina citri (Hemiptera: Psyllidae) in two Florida citrus groves. Environ. Entomol. 37, 914-924.
Hayat, M., 1981. Taxonomic notes on Indian Encyrtidae (Hym.: Chalcidoidea). II. J. Nat. Hist. 15, 17-29.
Ikeda, K., Ashihara, W., 2008. Preference of adult Asian citrus psyllid, Diaphorina citri (Homoptera: Psyllidae) for Murraya paniculata and Citrus unshiu Jpn. J. Appl. Entomol. Zool. 52, 27-30.
Matsunaga, J.N., 2014. First records of parasitoids attacking the Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae), in Hawaii. Proc. Hawaii. Entomol. Soc. 46, 41-43.
Moncayo-Donoso, M.A., Almanza-Pinzón, M.I., Caicedo-Vallejo, A.M., Muñoz-Flores, J.E., Montoya-Lerma, J., Carabalí-Muñoz, A., 2014. Diversidad genética de Diaphorina citri en cultivos cítricos del Valle del Cauca y Quindío. Biotecnol. Sect. Agropecu. Agroind. 12, 106-114.
Noyes, J.S., 1980. A review of the genera of Neotropical Encyrtidae (Hymenoptera: Chalcidoidea). Bull. Br. Mus. 41, 107-253.
Parra, J.R.P., Gómez-Torres, M.L., Paiva, P.E.B., 2007. Efeciência do parasitóide Tamarixia radiata para o controle do psilídeo Diaphorina citri em São Paulo. Citric. Atual. 61, 18-19.
Rohrig, E.A., Hall, D.G., Qureshi, J.A., Stansly, P.A., 2012. Field release in Florida of Diaphorencyrtus aligarhensis (Hymenoptera: Encyrtidae), an endoparasitoid of Diaphorina citri (Homoptera: Psyllidae), from mainland China. Fla. Entomol. 95, 479-481.
Rohrig, E., Shirk, P.D., Hall, D.G., Stansly, P.A., 2011. Larval development of Diaphorencyrtus aligarhensis (Hymenoptera: Encyrtidae), an endoparasitoid of Diaphorina citri (Hemiptera: Psyllidae). Ann. Entomol. Soc. Am. 104, 50-58.
SENASICA, 2012. Available at: http://www.pestalert.org (accessed 21.04.16).
» http://www.pestalert.org
Sétamou, M., Flores, D., French, J.V., Hall, D.G., 2008. Dispersion patterns and samplings plans for Diaphorina citri (Hemiptera: Psyllidae) in citrus. J. Econ. Entomol. 101, 1478-1487.
Shafee, S.A., Alam, M., Agarwal, M.M., 1975. Taxonomic Survey of Encyrtid Parasites (Hymenoptera: Encyrtidae) in India, vol. 10. Aligarh Muslim UniversityPublications (Zoological Series) on Indian Insect Types, pp. 1-125.
Sule, H., Muhamad, R., Omar, D., Hee, A.K.W., 2014. Parasitism rate, host stage preference and functional response of Tamarixia radiata on Diaphorina citri Int. J. Agric. Biol. 16, 783-788.
Wang, N., Trivedi, P., 2013. Citrus huanglongbing: a newly relevant disease presents unprecedented challenges. Phytopathology 103, 652-663.

Publication Dates

Publication in this collection
Apr-Jun 2017

History

Received
26 May 2016
Accepted
19 Feb 2017

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial No Derivative License, which permits unrestricted non-commercial use, distribution, and reproduction in any medium provided the original work is properly cited and the work is not changed in any way.

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[2] Bove, J.M., 2006. Huanglongbing: a destructive, newly-emerging, century-old disease of citrus. J. Plant Pathol. 88, 7-37.

[3] Chien, C.C., Chu, Y.I., Ku, S.C., 1991. Biological control of citrus psyllid, Diaphorina citri in Taiwan. II. Evaluation of Tamarixia radiata and Diaphorencyrtus diaphorinae for the control of Diaphorina citri Chin. J. Entomol. 11, 25-38.

[4] Cornejo, J.F., Chica, E.J., 2014. First record of Diaphorina citri (Hemiptera: Psyllidae) in Ecuador infesting urban citrus and orange jasmine trees. J. Insect Sci. 14, 1-1.

[5] Étienne, J., Quilici, S., Marinal, D., Franck, A., 2001. Biological control of Diaphorina citri (Hemiptera: Psyllidae) in Guadeloupe by imported Tamarixia radiata (Hymenoptera: Eulophidae). Fruits 56, 307-315.

[6] EPPO, 2014. Available at: https://www.eppo.int/QUARANTINE/data_sheets/insects/DIAACI_ds.pdf (accessed 21.04.16).
» https://www.eppo.int/QUARANTINE/data_sheets/insects/DIAACI_ds.pdf

[7] Gómez-Torres, M.L., Nava, D., Gravena, S., Costa, V.A., Parra, J.R.P., 2006. Registro de Tamarixia radiata (Waterston) (Hymenoptera: Eulophidae) em Diaphorina citri Kuwayama Hemiptera: Psyllidae) em São Paulo. Rev. Agric. 81, 112-117.

[8] Hall, D.G., Hentz, M.G., Adair, R.C., 2008. Population ecology and phenology of Diaphorina citri (Hemiptera: Psyllidae) in two Florida citrus groves. Environ. Entomol. 37, 914-924.

[9] Hayat, M., 1981. Taxonomic notes on Indian Encyrtidae (Hym.: Chalcidoidea). II. J. Nat. Hist. 15, 17-29.

[10] Ikeda, K., Ashihara, W., 2008. Preference of adult Asian citrus psyllid, Diaphorina citri (Homoptera: Psyllidae) for Murraya paniculata and Citrus unshiu Jpn. J. Appl. Entomol. Zool. 52, 27-30.

[11] Matsunaga, J.N., 2014. First records of parasitoids attacking the Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae), in Hawaii. Proc. Hawaii. Entomol. Soc. 46, 41-43.

[12] Moncayo-Donoso, M.A., Almanza-Pinzón, M.I., Caicedo-Vallejo, A.M., Muñoz-Flores, J.E., Montoya-Lerma, J., Carabalí-Muñoz, A., 2014. Diversidad genética de Diaphorina citri en cultivos cítricos del Valle del Cauca y Quindío. Biotecnol. Sect. Agropecu. Agroind. 12, 106-114.

[13] Noyes, J.S., 1980. A review of the genera of Neotropical Encyrtidae (Hymenoptera: Chalcidoidea). Bull. Br. Mus. 41, 107-253.

[14] Parra, J.R.P., Gómez-Torres, M.L., Paiva, P.E.B., 2007. Efeciência do parasitóide Tamarixia radiata para o controle do psilídeo Diaphorina citri em São Paulo. Citric. Atual. 61, 18-19.

[15] Rohrig, E.A., Hall, D.G., Qureshi, J.A., Stansly, P.A., 2012. Field release in Florida of Diaphorencyrtus aligarhensis (Hymenoptera: Encyrtidae), an endoparasitoid of Diaphorina citri (Homoptera: Psyllidae), from mainland China. Fla. Entomol. 95, 479-481.

[16] Rohrig, E., Shirk, P.D., Hall, D.G., Stansly, P.A., 2011. Larval development of Diaphorencyrtus aligarhensis (Hymenoptera: Encyrtidae), an endoparasitoid of Diaphorina citri (Hemiptera: Psyllidae). Ann. Entomol. Soc. Am. 104, 50-58.

[17] SENASICA, 2012. Available at: http://www.pestalert.org (accessed 21.04.16).
» http://www.pestalert.org

[18] Sétamou, M., Flores, D., French, J.V., Hall, D.G., 2008. Dispersion patterns and samplings plans for Diaphorina citri (Hemiptera: Psyllidae) in citrus. J. Econ. Entomol. 101, 1478-1487.

[19] Shafee, S.A., Alam, M., Agarwal, M.M., 1975. Taxonomic Survey of Encyrtid Parasites (Hymenoptera: Encyrtidae) in India, vol. 10. Aligarh Muslim UniversityPublications (Zoological Series) on Indian Insect Types, pp. 1-125.

[20] Sule, H., Muhamad, R., Omar, D., Hee, A.K.W., 2014. Parasitism rate, host stage preference and functional response of Tamarixia radiata on Diaphorina citri Int. J. Agric. Biol. 16, 783-788.

[21] Wang, N., Trivedi, P., 2013. Citrus huanglongbing: a newly relevant disease presents unprecedented challenges. Phytopathology 103, 652-663.