Hymenopterous parasitoids of Dasiops (Diptera: Lonchaeidae) infesting cultivated Passiflora spp. (Passifloraceae) in Cundinamarca and Boyaca, Colombia Received for publication: 5 February, 2016. Accepted for publication: 30 June, 2016. Doi: 10.15446/agron.colomb.v34n2.55616 1 Department of Agronomy, Faculty of Agricultural Sciences, Universidad Nacional de Colombia. Bogota (Colombia). 2 Faculty of Engineering, Corporacion Universitaria Minuto de Dios (Uniminuto). Bogota (Colombia). msantamaria@uniminuto.edu 3 National Phytosanitary Laboratory Diagnosis, Tibaitata Research Center, Instituto Colombiano Agropecuario (ICA). Bogota (Colombia). Agronomía Colombiana 34(2), 200-208, 2016 Hymenopterous parasitoids of Dasiops (Diptera: Lonchaeidae) infesting cultivated Passiflora spp. (Passifloraceae) in Cundinamarca and Boyaca, Colombia Parasitoides himenópteros de Dasiops (Diptera: Lonchaeidae) que infestan Passiflora spp. (Passifloraceae) cultivadas en Cundinamarca y Boyacá, Colombia Maikol Santamaría1, 2, Everth Ebratt3, Angela Castro3, and Helena Luisa Brochero1 ABSTRACT RESUMEN Dasiops spp. are the most important pest in cultivated Passiflora plants. Larvae of these fruit f lies are herbivores, feeding on f lower buds and fruit of yellow passionfruit, sweet granadilla, banana passionfruit and purple passionfruit crops located in Cundinamarca and Boyaca, Colombia. Geographic distribu- tion, natural abundance and percentage of parasitoidism for every Dasiops species by each plant species were determined. Aganaspis pelleranoi (Hymenoptera: Figitidae) was found to be a parasitoid of D. inedulis (14.19-50.00%), infesting f lower buds of yellow passionfruit and fruit of sweet granadilla (7.41%). Microcrasis sp. (Hymenoptera: Braconidae) was found to be parasitizing both D. gracilis (0.83-3.13%) and D. inedulis (0.83%) in purple and yellow passionfruit. Trichopria sp. and Pentapria sp. (Hymenoptera: Diapriidae) were found to be parasitizing D. inedulis (40.00% and 4.17-20.00%, respectively) and D. gracilis (1.69-22.22% and 1.67-29.17%, respectively) in purple passion fruit. Dasiops caustonae was found to be infesting banana pas- sionfruit only in Boyaca, naturally parasitized by Pentapria sp. (11.11-33.33%). Because Pentapria sp. had a wide geographical distribution as an idiobiont of Dasiops spp. pupae, in all of the assessed cultivated Passif lora species, despite a high selection pressure by chemical control distributed at regular calendar intervals, it would be a crucial strategy in pest management control. Collecting fallen f lower buds and fruit infested by Dasiops spp. is important to truncate the life cycle of fruit f lies and allow emergence of parasitoids. This simple cultural strat- egy could have important implications in reducing production costs, increased crop yields and environmental care. Dasiops spp. son la plaga más importante de plantas cultivadas de Passif lora. Las larvas de estas moscas de la fruta consumen botón f loral y fruto de cultivos de maracuyá, granadilla, curuba y gulupa localizados en los departamentos de Cundinamarca y Boyacá en Colombia. Se determinó la distribución geográ- fica, abundancia natural y porcentaje de parasitoidismo para cada especie de Dasiops en cada especie de planta. Aganaspis pelleranoi (Hymenoptera: Figitidae) fue encontrada como parasitoide de D. inedulis (14,19-50,00%) que infestó botón f loral de maracuyá y fruto de granadilla (7,41%). Microcrasis sp. (Hymenoptera: Braconidae) fue encontrada como parasitoide de D. gracilis (0,83-3,13%) y D. inedulis (0.83%) en gulupa y maracuyá. Trichopria sp. y Pentapria sp. (Hymenoptera: Di- apriidae) fueron encontradas parasitando D. inedulis (40,00% y 4,17-20,00%, respectivamente) y D. gracilis (1,69-22,22% y 1,67-29,17%, respectivamente) en gulupa. D. caustonae fue encontrada infestando curuba únicamente en Boyacá y para- sitada naturalmente por Pentapria sp. (11,11-33,33%). Debido a que Pentapria sp. mostró amplia distribución geográfica como idiobionte de pupas de Dasiops spp., en todas las especies de Passif lora estudiadas, a pesar de la presión de selección por el control químico implementado tipo calendario, sería una estrategia crucial en el control de plagas. La recolección de botones f lorales y frutos infestados por Dasiops spp., es im- portante para cortar el ciclo de vida de las moscas de la fruta y permitir la emergencia de parasitoides. Esta simple estrategia cultural podría tener importantes implicaciones en la reduc- ción de costos de producción, el aumento de los rendimientos de los cultivos y el cuidado del ambiente. Key words: Hymenoptera, fruit f lies, Lonchaeidae biodiversity. Palabras clave: Hymenoptera, moscas de la fruta, Lonchaeidae, biodiversidad. markets are yellow passionfruit (Passif lora edulis f. f la- vicarpa Deg.), sweet granadilla (P. ligularis Juss.), purple passionfruit (P. edulis Sims and banana passionfruit (P. tri- partita var. mollissima Nielsen & Jorgensen) (MADR, 2015). Introduction The species of cultivated Passiflora that are the most wide- spread and important in the national and international http://dx.doi.org/10.15446/agron.colomb.v34n2.55616 201Santamaría, Ebratt, Castro, and Brochero: Hymenopterous parasitoids of Dasiops (Diptera: Lonchaeidae) infesting cultivated Passiflora spp. (Passifloraceae)... The f lies of the Dasiops Rondani (Diptera: Lonchaeidae) genus are the insect pests of major economic importance in cultivated Passif lora, due to the habit of the larvae consuming the internal structures of f lowers bud and fruit (Santamaria et al., 2014; Castro et al., 2012). They are responsible for causing production losses in excess of 50% (Castro et al., 2012). Different species of f lies of the Dasiops genus that infest cultivated Passif lora are currently recognized. Dasiops inedulis Steyskal infests f lower buds of purple passionfruit, sweet granadilla and yellow passionfruit. Specific infesta- tions exist regarding the vegetal species: D. yepezi Norrbom and McAlpine in sweet granadilla, D. gracilis Norrbom and McAlpine in purple passionfruit and D. caustonae Nor- rbom and McAlpine in banana passionfruit (Santamaría et al., 2014; Castro et al., 2012). To control Dasiops spp., most farmers implement con- ventional strategies based on the application of synthetic chemical insecticides on a calendar basis (Wyckhuys et al., 2012). However, this management has affected the sustain- ability of the crops and has deteriorated the biodiversity that provides ecosystem services such as biological control (CDB, 2010). The natural enemies of pest populations are crucial in the context of sustainable agriculture because it provides ben- efits at an economic, social and environmental level (Gliess- mann, 2006; Thomson and Hoffmann, 2010). Among their natural enemies, parasitoids of the Hymenoptera order are particularly significant due to the specificity they have for their hosts. For this reason, they have been used exten- sively for biological control (Heraty, 2009). The idea is to consider the parasitoids that act naturally because they constitute model systems that provide benefits for natural control (Ehler, 1994) and do not represent the irreversible problems of exotic introductions (Haye et al., 2005; Basso and Grille, 2009). The aim of this study was to determine the natural para- sitoid f lies of the Dasiops genus and the relationship with four plant species of economically interesting Passif lora to estimate the trophic association between parasitoid, host, plant and the percentages of natural parasitism in the departments of Cundinamarca and Boyaca in Colombia. Materials and methods Study sites Productive farms of passion fruit, purple passion fruit, sweet granadilla and banana passion fruit located in five municipalities of Cundinamarca and two municipalities of Boyaca were selected on records based on Dasiops spp., infestation. On each farm, samples were taken every 15 d for 17 months (Tab. 1). In all cases, the agronomic crop mana- gement was based on conventional chemical strategies. The geographical coordinates and altitude were determined by a global positioning system using GPS 40 Garmin device (Garmin, Schaff hausen, Switzerland). Recovery of natural parasitoids and their association with each crop and Dasiops species On each of the farms, 1 ha of the crop was selected to collect all f loral buds and fruit infested by Dasiops spp., in accor- dance to specific symptoms of each species (Santamaría et al., 2014). These plant structures were placed separately in 30x40x15 cm white plastic containers, covered with 1 cm of sifted soil obtained from the crop and labelled f lower bud traps (TB) or fruit traps (TF). Each trap was placed within the crop, 2 m from the edge in order to expose the larvae and pupae of the f lies to the natural parasitoids (Tab. 1). Every fortnight, the trap substrate was inspected to recover pupae of fruit f lies. These were washed with clean water to remove adhering soil and pathogens and placed indi- vidually into plastic jars (10 cm in diameter x 6 cm high) containing 2 mm of sterilized river substrate sand and covered by a mesh top. The samples were maintained under controlled laboratory conditions to recover parasitoids that emerged. The conditions had an average temperature of 18°C, average relative humidity of 60% and a photoperiod of 12 h light/12 h dark. The taxonomic identification of Dasiops species was based on morphological characters (Korytkowski, 2003) and Cheslavo Korytkowski from Panama University, as expert of this group, confirmed each one. Taxonomic classifica- tion of parasitoids was carried out based on morphological characteristics according to taxonomic keys and related scientific literature (Guimarães et al., 2003; Buffington and Ronquist, 2008; Sharkey and Wahl, 2006; Campos and Sharkey, 2006; Dix, 2009; Masner, 2006 a, b; Masner and García, 2002). Additionally, experts were consulted: Carlos Sarmiento of the Instituto de Ciencias Naturales Unal (In- stitute of Natural Sciences), Bogota ; Paul Hanson, Profes- sor at the Universidad de Costa Rica (University of Costa Rica) ; Marta Loiacono of the Museo de La Plata, Division Entomologia (La Plata Museum, Entomology Division), Argentina; and Valmir Antonio Costa of the Centro Ex- perimental do Instituto Biologico Heitor Penteado (Heitor Penteado Experimental Centre of the Biological Institute) Campinasm, Brazil. The levels of parasitoid presence were analyzed according to the mortality rate, which compared 202 Agron. Colomb. 34(2) 2016 TABLE 1. Number of traps for flower buds and fruit in accordance with the species of Passiflora spp. cultivated assessed in Cundinamarca and Boyaca departments in Colombia. Plant species Department Municipality Geographical coordinates Altitude (m a.s.l.) Life zones* Number of traps installed Number of flower per trap Number of fruits per trap Common and scientific name TB TF Yellow passionfruit P. edulis f. flavicarpa Cundinamarca Tena 4°40´07´́ N 966 LM-WP 1 1 10 38 74°21́ 24´́ W La Mesa 4°40´01́ ´N 845 LM-WP 5 0 77 0 74°31́ 26´́ W Subtotal yellow passionfruit (n) 6 1 87 38 Purple passionfruit P. edulis f. edulis Cundinamarca Fusagasuga 4°12 1́1́ ´N 1,932 PM-WP 1 4 6 311 74°12´38´́ W Tibacuy 4°21́ 11́ ´N 1,843 PM-WP 1 3 5 58 74°28 1́4´́ W Boyaca Buenavista 5°31́ 08´́ N 2,100 PM-PHP 0 5 0 109 73°57´06´́ W Subtotal purple passionfruit (n) 2 12 11 478 Sweet granadilla P. ligularis Cundinamarca San Bernardo 4°06´00´́ N 1,937 PM-WP 2 2 39 27 74°12´22´́ W Tena 4°40´07´́ N 1,781 PM-WP 1 1 21 12 74°21́ 24´́ W Boyaca Buenavista 5°31́ 08´́ N 2,030 PM-PHP 4 4 35 18 73°57´06´́ W Subtotal sweet granadilla (n) 7 7 95 57 Banana passionfruit P. tripartita var. molissima Boyaca Umbita 4°40´07´́ N 2,709 PM-PHP 0 5 0 59 74°21́ 24´́ W Subtotal banana passionfruit (n) 0 5 0 59 Total 15 25 193 632 Life zones: premontane wet forest (PM-WP), lower montane wet forest (LM-WP), premontane per-humid forest (PM-PHP) (Holdridge, 1967). the number of parasitoids with the number of adult f lies of the Dasiops genus. Results and discussion Parasitoids belonging to Braconidae, Diapriidae and Figitidae Hymenoptera families were recorded (Tab. 2). All of these are endoparasitoids of the Diptera immature stages (Fernández and Sharkey, 2006). Aganaspis pelleranoi (Bretes, 1924) (Hymenoptera: Figitidae) was found to be a parasitoid of pupae of D. yepezi and D. inedulis (Fig. 1A); parasitoids of pupae of D. inedulis and D. gracilis were found Microcrasis sp. Fischer, 1975 (Hymenoptera: Braconidae) (Fig. 1B), Trichopria sp. Ashmead, 1893 (Hymenoptera: Diapriidae) (Fig. 1C) and Pentapria sp. Kieffer, 1905 (Hy- menoptera: Diapriidae) (Fig. 1D). Pentapria sp., were found parasitizing D. caustonae in banana passionfruit. A. pelleranoi was the first recorded instance of this species as a parasitoid of the genus Dasiops Rondani. This parasit- oid emerged from pupae of D. inedulis and D. yepezi which infested f lower buds of all Passif lora species evaluated and fruits of sweet granadilla, respectively (Tab. 2). However, A. pelleranoi is recognized as a koinobiont, endoparasitoid of larva and emerges in pupa, solitary, native to the Neotropics (Ovruski et al., 2000) parasitizing flies of the genus Neosilba (Diptera: Lonchaeidae) (Diaz and Gallardo, 2001) and, in several species of the genus Anastrepha (Nunes et al., 2012). The adult female is a forager; enters fruits infested by f lies, seeks and detects larvae of the host through tactile explora- tion with antennae and tarsi, although it can be guided by chemical signals of plants (Guimarães and Zucchi, 2004; Aluja et al., 2009). Parasitism of D. yepezi could occur when larvae fall down from fruits to pupate on soil or pushing up from fallen f lower buds by D. inedulis infestation. 203Santamaría, Ebratt, Castro, and Brochero: Hymenopterous parasitoids of Dasiops (Diptera: Lonchaeidae) infesting cultivated Passiflora spp. (Passifloraceae)... TABLE 2. Geographic distribution and abundance of natural parasitoids of the genus Dasiops flies in Cundinamarca and Boyaca departments in Colombia. Parasitoid species Family Type of parasitoid Number of parasitoids Host Cultivated passionflowers species Passionflower structure affected by Dasiops spp. Geographic distribution Life zone (Holdridge, 1967) ♀ ♂ Mun. Dep. Aganaspis pelleranoi Figitidae Koinobiont larva-pupa 2 Dasiops yepezi Sweet granadilla Fruit Ten Cu PM-WP 1 Dasiops inedulis Sweet granadilla Flower bud Ten Cu PM-WP 5 2 Yellow passionfruit Flower bud LM Cu LM-WP Total 8 2 Microcrasis sp. Braconidae Koinobiont larva-pupa 6 Dasiops gracilis Purple passionfruit Fruit Fus Cu PM-WP 1 Dasiops inedulis Yellow passionfruit Flower bud LM Cu LM-WP Total 7 Trichopria sp. Diapriidae Idiobiont pupa 1 1 Dasiops gracilis Yellow passionfruit Fruit Ten Cu LM-WP 4 2 Purple passionfruit Fruit Fus Cu PM-WP 1 Bue By PM-PHP 1 1 Dasiops inedulis Purple passionfruit Flower bud Fus Cu PM-WP Total 7 4 Pentapria sp. Diapriidae Koinobiont larva-pupa 2 Dasiops gracilis Yellow passionfruit Fruit Ten Cu LM-WP 37 8 Purple passionfruit Fruit Fus Cu PM-WP 1 2 Bue By PM-PHP 1 Dasiops inedulis Sweet granadilla Flower bud Ten Cu PM-WP 1 Purple passionfruit Flower bud Fus Cu PM-WP 1 Sweet granadilla Flower bud SB Cu PM-WP 1 2 Dasiops caustonae Banana passionfruit Fruit Umb By PM-PHP Total 42 14 Total Parasitoids 64 20 Ten. Tena; LM: La Mesa; Fus: Fusagasuga; SB: San Bernardo; Bue: Buenavista; Umb: Umbita; Cu: Cundinamarca; By: Boyaca. FIGURE 1. Natural parasitoids of the genus Dasiops flies. A, A. pelleranoi male; B, Microcrasis sp. female; C, Trichopria sp. female; D, Pentapria sp. male. A. pelleranoi presented variable percentage of parasitism in accordance to Dasiops species and cultivated passionf lower species (Tab. 3). In D. inedulis infesting yellow passion fruit crops in La Mesa municipality, we registered 50 to 14% of parasitoidism, while just 4.17% was observed in the municipality of Tena (Tab. 3). In D. yepezi, as pest of sweet granadilla fruits, 4.2% parasitoidism was recorded. Sweet granadilla crops where this parasitoid was registered were characterized by having woodland in the periphery and f lowering weeds within the growing area, characteristics that are advantageous for parasitoid populations, as they provide shelter and food (Hajek, 2004). Agro-ecosystems with greater diversity encourage the presence and activity of the parasitoid as observed on Anastrepha spp. where 204 Agron. Colomb. 34(2) 2016 there was found an increase of 89.9% in shaded coffee productive systems (Souza et al., 2005). In this context, the results found in this study are important because, if A. pelleranoi can be found from Mexico to Argentina (Nunes et al., 2012), acting as generalist and oviposits regardless of the species of f ly or host plant (Sivinski et al., 1997), this species could be found in other regions that produce sweet granadilla and passion fruit with infestations of D. inedulis and D. yepezi evaluated by Castro et al., (2012). As a koino- biont, allowing Dasiops to feed on plants during larvae TABLE 3. Percentage of parasitoidism by species of Dasiops and cultivated Passiflora in Cundinamarca and Boyaca departments in Colombia. Parasitoid species Host Cultivated Passiflora Structure Geographic distribution Number of pupas of Dasiops spp. Number of Dasiops spp. flies emerged Number of parasitoids Percentage of parasitoids per sampling Aganaspis pelleranoi Dasiops yepezi Gr F Ten Cu 27 25 2 7.41 Dasiops inedulis Gr B Ten Cu 24 23 1 4.17 Dasiops inedulis Ma B LM Cu 6 3 3 50.00 11 9 2 18.18 6 5 1 16.67 7 6 1 14.29 Mean 18.45 ± 14.95 Microcrasis sp. Dasiops gracilis Gu F Fus Cu 160 155 5 3.13 120 119 1 0.83 Dasiops inedulis Ma B LM Cu 120 119 1 0.83 Mean 1.60 ± 1.08 Trichopria sp. Dasiops gracilis Ma F Ten Cu 9 7 2 22.22 Gu F Fus Cu 24 23 1 4.17 160 155 5 3.13 Bue By 59 58 1 1.69 Dasiops inedulis Gu B Fus Cu 5 3 2 40 Mean 14.24 ± 14.90 Pentapria sp. Dasiops gracilis Ma F Ten Cu 9 7 2 22.22 Gu F Fus Cu 24 22 2 29.17 120 113 7 5 160 154 6 18.75 120 90 30 1.67 Bue By 8 7 1 12.5 9 8 1 11.11 59 58 1 1.69 Dasiops inedulis Gu B Fus Cu 5 4 1 20 Gr B SB Cu 17 16 1 5.88 Ten Cu 24 23 1 4.17 Dasiops caustonae Cu F Umb By 3 2 1 33.33 9 8 1 11.11 4 3 1 25 Mean 14.40 ± 10.05 Ma, maracuya (passion fruit); Gr, granadilla (sweet granadilla); Gu, gulupa (purple passion fruit); Cu, curuba (banana passion fruit); B, flower bud; F: fruit; Ten, Tena; LM, La Mesa; Fus, Fusagasuga; SB, San Bernardo; Bue, Buenavista; Umb, Umbita; Cu, Cundinamarca; By, Boyaca. stage, it is not a promising as biocontrol agent. However, A. pelleranoi is contributing to control of natural population of Dasiops inedulis and D. yepezi in Tena and La Mesa in the Cundinamarca Department, one of the more important areas to produce passion fruit crops. Microcrasis sp., emerging from D. gracilis infested purple passion fruit and D. inedulis infested f lower buds of pas- sion fruit, is the first record as parasitoids of Dasiops spp. Because of seven putative species of Microcrasis being 205Santamaría, Ebratt, Castro, and Brochero: Hymenopterous parasitoids of Dasiops (Diptera: Lonchaeidae) infesting cultivated Passiflora spp. (Passifloraceae)... registered in Colombia (Dix, 2009), D. gracilis and D. inedu- lis have been listed in several municipalities of Antioquia, Tolima, Meta, Huila, Caldas, Quindío, Risaralda and Valle del Cauca, where these crops are settled; the geographical distribution of these wasps should be wider (Castro et al., 2012). Microcrasis spp., are endoparasitoids koinobiont (larva-pupa) of Tephritidae fruit f lies (Núñez et al., 2009), solitaries (Dix, 2009) and, endemic from the Neotropics (Wharton, 1997). Over three evaluations, the percentage of parasitism of Mi- crocrasis sp., on D. inedulis was low (0.83%), where, as in D. gracilis. it was affecting purple passion fruit crops (3.13%) (Tab. 3). Parasitoids of the genus Microcrasis, are better suited to humid agro-ecosystems associated with plants that provide shade (Núñez et al., 2009), then it is possible that this kind of monoculture is not the best refuge for adults of this species (Speight et al., 2008) or, competence with other parasitoids, as A. pelleranoi occupying the same niche, is affecting the efficiency of Microcrasis as parasitoid of D. inedulis (Hajek, 2004). Male and female of Trichopria spp., emerging from D. gracilis as pest as fruits of yellow and purple passion fruit and from D. inedulis as pest of f lower buds of purple pas- sion fruit, (Tab. 2) constitute the first record of wasps of this genus as parasitoids of Dasiops spp. Eleven specimens, nine emerged from the pupae of D. gracilis and two from D. inedulis, representing seven females and four males with a sex ratio of 1:0.57, were obtained. These wasps, recognized as parasitoids of Diptera, particularly in Tephritidae species (Souza-Filho et al., 2007), have broad distribution derived by parthenogenesis (Harms and Grodowitz, 2011). Trichopria sp. had inconsistent percentages of parasitoid- ism (Tab. 3). Parasitoidism of 40% was recorded for D. inedulis in purple passion fruit while on D. gracilis, it ranged between 1.69% and 4.17 on purple passion fruit and 22% in yellow passion fruit (Tab. 3). This parasitoid is a gregarious idiobiont parasitoid infesting pupae of sev- eral species of Diptera (García and Corseuil, 2004). In this study, every specimen obtained emerged from a Dasiops spp. pupa, possibly because of the high availability of hosts in the environment and the size of the pupae (Basso and Grille, 2009). However, the population dynamic of this parasitoid, endemic to the Neotropics, could be affected by the introduction of non-native (exotic) Diptera hosts (Monteiro and Prado, 2000), by high rainfall and by the variable population of native hosts. Although Pentapria sp. have been registered parasitizing D. inedulis of sweet granadilla crops (Santos et al., 2009), we are presenting first records as parasitoids of D. gracilis and D. inedulis in yellow and purple passion fruit of D. caustonae in banana passionfruit and, of D. inedulis infest- ing f lower buds of purple passion fruit (Tab. 2). Forty- two females and fourteen males were found, representing a sex ratio of 1:0.33, characterizing the most abundant natural population of parasitoid found in five of the six municipali- ties evaluated in this study. Pentapria inhabits ecosystems of high mountains, cloud forests and tundra in Neotropics and Nearctic regions (Masner and García, 2002) and, it has been registered in Colombia between 150 to 3,660 m a.s.l. (Arias-Penna, 2003). However, information on the biology, habits and rates of parasitism by this species is unknown (Masner, 2006b). Levels of parasitism of Pentapria sp. varied across three species of f lies in the four crops. The highest percentage of parasitoidism was recorded in banana passionfruit, with 33.3% for D. caustonae infesting fruits. For D. gracilis, a pest of purple passion fruit fruits, the percentage or parasitism ranged 1.67 to 29.17%. However, as parasitoid of pest af- fecting f lower buds in Passif lora, maximum parasitoidism recorded was 5.88% in sweet granadilla and 20% in purple passion fruit (Tab. 3). Pentapria sp., unlike A. pelleranoi, Microcrasis sp. and Trichopria sp., was found in all four cul- tivated species of Passif lora, from which it can be inferred that this is the most recurrent and abundant parasitoid of f lies of the genus Dasiops. D. inedulis has a broad distribution as it affects f lower buds from sweet granadilla, yellow and purple passion fruit crops, occupying several life zones (Castro et al., 2012) in accordance to the Holdridge classification (Hold- ridge, 1967). For this pest, all families of the parasitoids (Aganaspis pelleranoi, Microcrasis sp., Trichopria sp., and Pentapria sp.) registered in this study, were found at- tacking D. inedulis. Additionally, there are more species acting as natural enemies to this fruit f ly, as Basalys sp. (Hymenoptera: Diapriidae), Pachycrepoideus. vindem- miae (Rondani) (Hymenoptera: Pteromalidae), Aspilota sp. (Hymenoptera: Braconidae), Bracon sp. (Hymenoptera: Braconidae), Orgilus sp. (Hymenoptera: Braconidae) and Opius sp. (Hymenoptera: Braconidae) (Santos et al., 2009; Chacón and Rojas, 1984; Ambrecht, 1985; Aguiar-Menezes et al., 2004). Coupled with cultural practices that promote the establishment of parasitoids in Passif lora crops, an integrated crop management can be established to further address D. inedulis, f loral species causing early abortion affecting crop yields (Santamaría et al., 2014). It is clear that the abundance of the host, characteristics of each production system (i.e stringing/wiring; density) 206 Agron. Colomb. 34(2) 2016 but particularly, characteristics of the environment where crops are established, determine the abundance of natural enemies as parasitoids (Núñez et al., 2009; García and Corseuil, 2004). Additionally, the natural population of parasitoids, but particularly microparasitoids as belonging to Braconidae family, are affected by abiotic conditions as rainfall limiting their efficacy to localize their host (Núñez et al., 2009; Hance et al., 2007). In this context, landscape management, promoting shelter and foraging sites for adult parasitoids is crucial to maintaining the natural populations of the natural enemies associated with crop production systems (Straub et al., 2008; Landis et al., 2000). Pentapria sp., showed wide geographical distribution as an idiobiont of pupae of Dasiops spp., in all of the assessed cultivated Passif lora species , despite the high pressure of selection by chemical control distributed at regular calendar intervals. This species has an important value as biocontrol of fruit f lies in Passif lora crops; however, more studies are required to define its potential implementation. Collecting fallen f lower buds and fruits infested by Dasiops spp. is important to truncate the life cycle of fruit f lies and allow emergence of parasitoids. This simple cultural strat- egy could have important implications in reducing produc- tion costs, increased crop yields and environmental care. Acknowledgments This study was financed by the Universidad Nacional de Colombia (National University of Colombia) Bogota cam- pus, the Research Fund of the Faculty of Agronomy and the main campus of the Corporacion Universitaria Minuto de Dios (Minute of God Corporation University) and the Faculty of Engineering. Technical; scientific and logistical support were provided by the Instituto Colombiano Agro- pecuario ICA (Colombian Agricultural Institute) through the project “Adjustment, validation, and transfer of phytosa- nitary management technologies of the lonchaeid f ly - Dasiops spp. (Diptera: Lonchaeidae), in Passif lora crops in Colombia” ASOHOFRUCOL code TR-1305. Sincere thanks are given to the following academics: Carlos Sarmiento, Professor at the Instituto de Ciencias Naturales Unal (Institute of Natural Sciences) - Bogotá, Paul Hanson, Professor at the Uni- versidad de Costa Rica (University of Costa Rica), Marta Loiácono, of the Museo de La Plata, División Entomología (La Plata Museum, Entomology Division)- Argentina and Dr. Valmir Antonio Costa, of the Centro Experimental do Instituto Biológico Rodovia Heitor Penteado (Experimental Centre of the Rodovia Heitor Penteado Biological Institute) Campinas - Brazil. We give special thanks to the Passif lora growers and cultivators who are the reason for this study. In memory of the scientific contributions of Professor Cheslavo Korytkowski. Many thanks to Rosie Holmes at Lincoln University, Christchurch, New Zealand for her contribution to the English translation of this manuscript. Literature cited Aguiar-Menezes, E., R. Nascimento, and F. Menezes. 2004. 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