NOTA CIENTÍFICA

¹ Systematic Entomology Laboratory, United States Department of Agriculture, Animal and Plant Inspection Service, Plant Protection and Quarantine, (USDA/ APHIS/PPQ). Beltsville, MD, EE.UU.
² Laboratorio de Entomología, Centro de Investigación Palmira, Corporación Colombiana de Investigación Agropecuaria (Corpoica). Palmira (Colombia).
³ Jardín Botánico de San Andrés, Universidad Nacional de Colombia, San Andrés Isla (Colombia).
⁴ Departamento Ciencias Agronómicas, Facultad de Ciencias Agrarias, Universidad Nacional de Colombia. Medellín.

Fecha recibido: 05/10/2012. Fecha aprobado: 05/12/2012

ABSTRACT

Here we report for the first time the presence of Anagyrus kamali Moursi and Gyranusoidea indica Shafee, Alam and Agarwal (Hymenoptera: Encyrtidae), parasitoids of the pink hibiscus mealybug (PHM), Maconellicoccus hirsutus (Green) (Hemiptera: Pseudococcidae), on San Andres Island, Colombia. Brief notes are provided to allow differentiation of the two parasitoid species.

Keywords: natural enemies, biological control, morphology, new distribution record

RESUMEN

Se reporta por primera vez la presencia de Anagyrus kamali Moursi y Gyranusoidea indica Shafee, Alam y Agarwal (Hymenoptera: Encyrtidae), parasitoides de la cochinilla rosada del hibisco (CRH), Maconellicoccus hirsutus (Green) (Hemiptera: Pseudococcidae) en la Isla de San Andrés, Colombia. Se proveen notas breves para diferenciar las dos especies de parasitoides.

Palabras clave: enemigos naturales, control biológico, morfología, nuevos registros de distribución

Introduction

The pink hibiscus mealybug (PHM), Maconellicoccus hirsutus (Green) (Hemiptera: Pseudococcidae) (Figure 1), is now widespread throughout the Caribbean islands. The taxonomy of mealybugs is based on the morphology as seen on slide-mounted specimens studied under a compound microscope. Maconellicoccus hirsutus has 9-segmented antennae, cerarii usually numbering 4–6 pairs (only on posterior abdominal segments), a circulus, and oral rim tubular ducts on both dorsum and venter (Kawai, 1980; Williams, 2004; Williams and Watson, 1988). It has a huge host range and occurs in all of the zoogeographic regions of the world (Ben-Dov et al., 2013). On mainland Colombia, M. hirsutus was originally reported from the Departments of Atlántico, Cesar, Guajira and Magdalena (Kondo et al., 2008). In the Department of "San Andres, Providencia and Santa Catalina", it was first reported in 2010 on the island of Providencia (ICA, 2010). More recently it was reported on San Andres Island where it is common on Hibiscus spp. and Malvaviscus arboreus (Kondo et al., 2012).

Despite the vicinity of San Andres to Central America, the PHM was likely introduced to San Andres from mainland Colombia on ornamental plants because of the constant trade between the island and mainland Colombia (Kondo et al., 2012). High populations of the PHM can result in prolific production of honeydew, subsequently causing sooty mold growth, and heavy populations may cause host- plant wilting; the mealybug injects a toxic saliva during feeding, which can cause a characteristic symptom known as bunchy top in hibiscus (Hodges and Hodges, 2006).

The control of the PHM is the most recent example of a successful classical biological control program. Williams (1996) indicated that the key parasitoid of the PHM is Anagyrus kamali Moursi (Hymenoptera: Encyrtidae), a species that is likely of Asian origin. Reddy et al. (2009) reported that on the Marianna Islands, A. kamali, Allotropa sp. nr. mecrida (Walker) (Hymenoptera: Platygasteridae) and Cryptolaemus montrouzieri Mulsant (Coleoptera: Coccinellidae) have successfully suppressed populations of the PHM below the economic threshold. According to Chong (2009), the combination of natural enemies, namely, the mealybug destroyer C. montrouzieri and the parasitoids A. kamali and Gyranusoidea indica Shafee, Alam and Agarwal (Hymenoptera: Encyrtidae), significantly reduced the initial populations of M. hirsutus and maintained subsequent populations under damaging levels in the Caribbean and the USA. The parasitoid rearing program at the Division of Plant Industry in Gainesville, Florida, USA, recently ended as the parasitoids now are well established in that state (A.J. Fox, personal communication, apud Kondo et al., 2012). Anagyrus kamali is such an efficient parasitoid on Puerto Rico, that mass rearing is no longer necessary because the wasp is now well established there (J.C. Rodrigues, personal communication, apud Kondo et al., 2012). In Egypt, the encyrtid A. kamali is known to provide good control (Williams, 1986).

Anagyrus kamali has been recorded for various scale insects, namely: Coccus hesperidum L. (Coccidae), Ferrisia virgata (Cockerell), Ferrisia sp., M. hirsutus, Trabutina serpentina (Green), Nipaecoccus viridis (Newstead), Nipaecoccus sp., Phenacoccus hirsutus Granara de Willink, Formicococcus robustus (Ezzat and McConnell), Planococcus citri (Risso), P. halli Ezzat and McConnell, and Pseudococcus sp. (Pseudococcidae) (Noyes, 2012). However, A. kamali appears to be specialized on the PHM. Sagarra et al. (2001) conducted susceptibility, preference and suitability tests on eight mealybug species, namely, Dysmicoccus brevipes (Cockerell), M. hirsutus, Nipaecoccus nipae (Maskell), P. citri, P. halli, Leptococcus neotropicus (Williams and Granara de Willink), Pseudococcus elisae Borchsenius, Puto barberi (Cockerell), and Saccharicoccus sacchari (Cockerell), and determined that of the nine studied species, M. hirsutus was the only suitable mealybug host. According to the Chalcidoidea database (Noyes, 2012), A. kamali is widespread and has been reported from the Antilles, Bangladesh, Belize, Caribbean (including West Indies), Egypt, Grenada, Hawaii, India, Indonesia, Jordan, Montserrat, Pakistan, Peoples' Republic of China, Puerto Rico, Saint Lucia, Sri Lanka, St. Christopher (Kitts) and Nevis, Trinidad and Tobago, and the US Virgin Islands.

We also reared Gyranusoidea indica from PHM on San Andres Island. This species was described from India and has been introduced into Australia, Egypt, Guyana, Trinidad, various Caribbean countries (Noyes, 2012), and California, USA (Goolsby et al., 2002). Gyranusoidea indica has been recorded as a parasitoid of M. hirsutus (Meyerdirk and Warkentin, 1999; Abd-Rabou, 2001), F. virgata (Cockerell) (Abd-Rabou, 2001), N. viridis (Newstead) (Sharaf and Meyerdirk, 1987) and Pseudococcus longispinus (Targioni Tozzetti) (Abd-Rabou, 2001).

Materials and methods

The mealybug host was identified as M. hirsutus by GE and TK using the taxonomic keys by Kawai (1980), Williams (2004), and Williams and Watson (1988). Scale insect hosts of A. kamali listed in the Chalcidoidea database (Noyes, 2012) included some older names and synonyms, thus, the currently accepted names listed in the scale insect database ScaleNet (Ben-Dov et al., 2013) were used in the introduction section above.

Samples of encyrtid parasitoids were reared from the PHM feeding on twigs of Hibiscus rosa-sinensis L. (Malvaceae) by MFMA. The encyrtid parasitoids were identified as A. kamali and G. indica by GE using the original descriptions (Moursi, 1948; Shafee et al., 1975) and additional comments by Noyes (1980) and Michaud and Evans (2000). Studied material is deposited at the United States National Museum of Natural History, Beltsville, Maryland, USA (USNM). Other material studied and collected by MSG was identified by JAQ to the genus level using the keys by Gibson et al. (1997) and Noyes (1980), and is deposited at the Museo Entomológico Francisco Luis Gallego, Universidad Nacional de Colombia, Sede Medellín, Medellín, Colombia (MEFLG).

Studied material

Anagyrus kamali Moursi. Colombia: San Andres Island: 12°32'10.3''N, 81°42'30.1''W, 5 m, 08.ix.2011, coll. Maria Fernanda Maya, ex Maconellicoccus hirsutus on Hibiscus rosa-sinensis L. (Malvaceae), 1 female and 1 male on microscope slide (USNM). Gyranusoidea indica Shafee, Alam and Agarwal. Colombia: San Andres Island: 12°32'10.3''N, 81°42'30.1''W, 5 m, 08.ix.2011, coll. Maria Fernanda Maya, ex M. hirsutus on H. rosa-sinensis L. (Malvaceae), 1 female on microscope slide (USNM).

Other studied material

Anagyrus sp. (likely A. kamali Moursi). 12°32'10.3''N, 81°42'30.1''W, 5 m, 19.ix.2012, coll. Marcela Silva Gómez, ex M. hirsutus (on H. rosa-sinensis L. (Malvaceae), 60 females and 19 males in vial (MEFLG); 12°32'14.7''N, 81°42'39.6''W, 42 m, 23.ix.2012, coll. Marcela Silva Gómez, ex M. hirsutus on Guazuma ulmifolia (Malvaceae), 11 females and 13 males in vial (MEFLG); 12°34'59.1''N, 81°41'23.7''W, 2 m, 13.x.2012, coll. Marcela Silva Gómez, ex M. hirsutus (on Cordia sebestena (Boraginaceae), 1 female in vial (MEFLG).

RESULTS AND DISCUSSION

Anagyrus kamali is superficially similar to G. indica, but can be distinguished by having the postmarginal vein of the forewing short, less than 0.5x as long as the stigmal vein (Figure 2A); frons dark brown, flagellum yellow with first segment dark brown in the female (Figure 2B), and the male with a dark spot at the apex of the antennal club. In G. indica, the postmarginal vein of the forewing is long, about 2x as long as the stigmal vein (Figure 2C); frons orangish, flagellum light brown in the female (Figure 2D); the male lacks the dark spot at the apex of the antennal club. In addition, most Anagyrus species can be separated from Gyranusoidea species by having conspicuous, moderately dense white setae on the face and irregular sculpture on the frontovertex, whereas Gyranusoidea species have pale setae on the face, but never conspicuous, and regular, polygonal sculpture on the frontovertex. For other differences, also see Montes-Rodríguez (2012).

The two parasitoids were recently reported in two municipalities in the Department of Norte de Santander, in mainland Colombia, on M. hirsutus infested shoots of H. rosa-sinensis (Montes-Rodríguez, 2012). According to Montes-Rodríguez (2012), A. kamali and G. indica probably came to Colombia by crossing the border from Venezuela, since the two parasitoids have been produced commercially and released by individuals and personnel from state-owned institutions in that country as a mean of biological control of the PHM (Cermeli et al., 2002). In Venezuela, the two parasitoids have been released in Zulia and Táchira, states that are located along the border with Colombia (Torres et al., 2007, apud Montes-Rodríguez, 2012).

The PHM generally becomes a pest when introduced into a new environment, and that was the case when first introduced onto the island of Providencia (ICA, 2010). However, on San Andres Island the PHM is not a serious pest, probably because the encyrtid parasitoids A. kamali and G. indica and other natural enemies are keeping it under control. The two parasitoids were probably introduced to San Andres from mainland Colombia along with M. hirsutus.

Acknowledgements

The authors thank the Colombian Ministry of Agriculture and Rural Development (MADR) that funded the short-term research project: "Distribución y determinación de los niveles de daño de la cochinilla acanalada Crypticerya multicicatrices en la isla de San Andrés y búsqueda preliminar de enemigos naturales en el Valle del Cauca"; and the Government of San Andrés, Providencia y Santa Catalina, that funded the project: "Convenio Interadministrativo de Cooperación Técnica para Montaje de Laboratorio de Investigación Científica No. 058 de 2011, entre la Gobernación Departamental y la Universidad Nacional de Colombia Sede Caribe". Many thanks also to John Jairo Alarcon from the Instituto Colombiano Agropecuario (ICA) for kindly sending the material studied to the USNM for identification. Especial thanks to Penny Gullan (The Australian National University, Canberra, Australia), Dr. M. Bora Kaydan (çukurova Üniversity, Adana, Turkey) and to anonymous reviewers for useful comments that helped improved the content of the manuscript.

BIBLIOGRAPHIC REFERENCES

Abd-Rabou S. 2001. Parasitoids attack mealybugs (Homoptera: Coccoidea: Pseudococcidae) in Egypt. Egypt J Agric Res 79(4):1355-1376.         [ Links ]

Ben-Dov Y, Miller DR, Gibson GAP. 2013. ScaleNet: a database of the scale insects of the world. In: http://www.sel.barc.usda.gov/scalenet/scalenet.htm; accessed: October, 2012.         [ Links ]

Cermeli M, Morales VP, Godoy F, Romero R, Cárdenas O. 2002. Presencia de la cochinilla rosada de la cayena Maconellicoccus hirsutus (Green) (Hemiptera: Pseudococcidae) en Venezuela. Entomotropica 17(1):103-105.         [ Links ]

Gibson GAP, Hubner JT, Woolley JB. 1997. Annotated keys to the Genera of Nearctic Chalcidoidea (Hymenoptera). Ottawa, Canada: NCR Research Press.         [ Links ]

Goolsby JA, Kirk AA, Meyerdirk DE. 2002. Seasonal phenology and natural enemies of Maconellicoccus hirsutus (Hemiptera: Pseudococcidae) in Australia. Fla Entomol 85(3): 494-498.         [ Links ]

Hodges A, Hodges G. 2006. Pink hibiscus mealybug identification (on line). Plant Health Progress, http://www.plantmanagementnetwork.org/sub/php/diagnosticguide/2006/hibiscus/mealybug.pdf; accessed: October, 2012.         [ Links ]

ICA, Instituto Colombiano Agropecuario. 2010. Plan para el manejo y mitigación del riesgo ocasionado por la cochinilla rosada (Maconellicocus hirsutus) y la chinche acanalada (Crypticerya multicicatrices) en las islas de San Andrés y Providencia. San Andrés, Colombia: Subgerencia de protección vegetal dirección técnica de epidemiologia y vigilancia fitosanitaria.         [ Links ]

Kawai S. 1980. Scale insects of Japan in colors. (in Japanese). Tokyo: National Agricultural Education Association.         [ Links ]

Kondo T, Ramos-Portilla AA, Vergara-Navarro EV. 2008. Updated list of mealybugs and putoids from Colombia (Hemiptera: Pseudococcidae and Putoidae). Bol Mus Ent Univ Valle 9(1):29-53.         [ Links ]

Kondo T, Gullan P, Ramos Portilla AA. 2012. Report of new invasive scale insects (Hemiptera: Coccoidea), Crypticerya multicicatrices Kondo and Unruh (Monophlebidae) and Maconellicoccus hirsutus (Green) (Pseudococcidae), on the islands of San Andres and Providencia, Colombia, with an updated taxonomic key to iceryine scale insects of South America. Insecta Mundi 0265:1-17.         [ Links ]

Meyerdirk, DE, Warkentin RW. 1999. Non-target impact of exotic natural enemies released on Maconellicoccus hirsutus Green in St. Kitts, West Indies. IOBC/WPRS Bulletin 22(2):49-50.         [ Links ]

Michaud JP, Evans GA. 2000. Current status of pink hibiscus mealybug in Puerto Rico including a key to parasitoid species. Fla Entomol 83(1):97-101.         [ Links ]

Montes-Rodríguez JM. 2012. Primer registro de parasitoides de la cochinilla rosada del hibisco, Maconellicoccus hirsutus (Hemiptera: Pseudococcidae), en Colombia [First record of parasitoids of the pink hibiscus mealybug, Maconellicoccus hirsutus (Hemiptera: Pseudococcidae), in Colombia]. Rev Colomb Entomol 38(2):274-275.         [ Links ]

Moursi AA. 1948. Contributions to the knowledge of the natural enemies of mealybugs. 1. Description of two new species of Anagyrus (Hymenoptera : Encyrtidae). Bull Soc Fouad Ier d'Entomol 32:9-16.         [ Links ]

Noyes JS. 1980. A review of the genera of Neotropical Encyrtidae (Hymenoptera: Chalcidoidea). Bull Brit Mus Nat Hist (Bot) 41:197-198.         [ Links ]

Noyes JS. 2012. Universal Chalcidoidea Database. In: http://www.nhm. ac.uk/chalcidoids; accessed: October, 2012.         [ Links ]

Sagarra LA, Vincent C, Stewart RK. 2001. Suitability of nine mealybug species (Homoptera: Pseudococcidae) as hosts for the parasitoid Anagyrus kamali (Hymenoptera: Encyrtidae). Fla Entomol 84(1):112-116.         [ Links ]

Sharaf NW, Meyerdirk DE. 1987. A review on the biology, ecology and control of Nipaecoccus viridis (Homoptera: Pseudococcidae). Misc Publ Entomol Soc Am 66:1-18.         [ Links ]

Shafee SA, Alam M, Agarwal MM. 1975. Taxonomic survey of encyrtid parasites (Hymenoptera: Encyrtidae) in India. Aligarh Muslim University Publication, Zoological Series on Indian Insect Types 10: 22-23.         [ Links ]

Torres BS, Fernández I, Laya M, Soto M. 2007. Resultados del proyecto fitosanitario de prevención y control de la cochinilla rosada Maconellicoccus hirsutus Green, durante el período 2006 - 2007. Entomotropica 22(2):122.         [ Links ]

Williams DJ. 1986. The identity and distribution of the genus Maconellicoccus Ezzat (Hemiptera: Pseudococcidae) in Africa. Bull Entomol Res 76 (2):351-357.         [ Links ]

Williams DJ. 1996. A brief account of the hibiscus mealybug Maconellicoccus hirsutus (Hemiptera: Pseudococcidae), a pest of agriculture and horticulture, with descriptions of two related species from southern Asia. Bull Entomol Res 86:617-628.         [ Links ]

Williams DJ. 2004. Mealybugs of Southern Asia. The Natural History Museum, Kuala Lumpur: Southdene SDN, BHD.         [ Links ]

Williams DJ, Watson GW. 1988. The scale insects of the tropical South Pacific Region. The mealybugs (Pseudococcidae). London: CAB International Institute of Entomology.         [ Links ]