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Introduction
The bud midge Prodiplosis longifila Gagné (Diptera: Cecidomyiidae) is a severe pest mainly of Solanaceae crops in South America, causing economic losses in potato (Solanum tuberosum L.) in Peru (Kroschel, Mujica, Alcazar, Canedo & Zegarra, 2012) and tomato (Solanum lycopersicum L.) in Ecuador (Valarezo, Cañarte, Arias, Proaño, Navarrete, Garzón, Jines, Cuadros, Porro, Linzán & Chávez, 2003) and Colombia (Hernández et al., 2015). Besides Solanaceae crops, P. longifila causes losses to asparagus (Asparagus officinalis L.) (Asparagaceae) crops in Peru (Goldsmith, Castillo & Clarke-Harris, 2013) and to flower buds of Tahiti lime (Citrus x latifolia Tanaka ex Q. Jiménez) (Rutaceae) orchards in the United States (Florida) (Peña, Duncan & Torres, 1990). Recently, it was reported feeding on floral buds of Tahiti lime in Colombia (Hernandez, Guzman, Martínez, Manzano & Selvaraj, 2015). Because of severity of its damage on traded fruits such as tomatoes, P. longifila was included recently in European and Mediterranean Plant Protection Organization alert list (European and Mediterranean Plant Protection Organization, EPPO; https://gd.eppo.int/taxon/ PRDILO). In addition, P. longifila, other cecidomyiid species belonging to genus Dasineura can cause economic losses to several crops around the world such as Dasineura mali K. on apple Malus pumila Mill. (Rosaceae) (Hall, Amarawardana, Cross, Francke, Boddum & Hillbur, 2012) and Dasineura oxycoccana (Johnson) on cultivated blueberries Vaccinium corymbosum L. (Ericaceae) (Sampson, Rinehart, Liburd, Stringer & Spiers, 2006). Prodiplosis floricola Felt feeds on floral buds of Spiraea salicifolia L. (Rosaceae) and Clematis sp. (Ranunculaceae) in the United States (Gagné & Jaschhof, 2014) and it causes economic damage to Caryocar brasiliense Cambess. (Caryocaraceae)in Brazil (Gagné & Jaschhof, 2014). Recently P. floricola was reported feeding on Tahiti lime floral structures in Colombia (Duque-Gamboa, 2017. In Press.).
P. longifila larvae feed on leaf buds, flowers and immature tomato fruits and on flowers and flower buds of Tahiti lime (Peña, Duncan & Torres, 1990; Hernandez et al., 2015) and consumes the epidermis tissue of asparagus shoots (Goldsmith, Castillo & Clarke-Harris, 2013). Control of P. longifila on different crops include adult mass trapping using light and color traps (Goldsmith, Castillo & Clarke-Harris, 2013), physical control with high pressure water to remove adults (Goldsmith, Castillo & Clarke-Harris, 2013) but chemical spray is the principal control method used (Valarezo et al., 2003; Kroschel et al., 2012). In relation to biological control several natural predators have been reported (Valarezo et al., 2003; Goldsmith, Castillo & Clarke-Harris, 2013).
Taxonomic studies on native parasitoids attacking P. longifila have been largely neglected. Unidentified Synopeas species have been reported to act as natural enemies of P. longifila on tomato (Valarezo et al., 2003), Tahiti lime (Peña, Duncan & Torres, 1990) and asparagus (Goldsmith, Castillo & Clarke-Harris, 2013).
Synopeas females are shiny micro wasps (1-2 mm) characterized by having cylindrical antennae and by lacking wing veins (Buhl, 1997). They are koinobiont endoparasitoids of eggs and early larval stages of Cecidomyiidae (Austin, Johnson & Dowton, 2005). Adult wasps emerge during the prepupal or pupal stage of the host (Masner & Arias-Penna, 2006). Biological information is limited (Abram, Haye, Mason, Cappuccino, Boivin & Kuhlmann, 2012; Sampson et al., 2006).
Because of the economic impact of P. longifila, the aim of this study was to survey parasitized P. longifila (and other cecidomyiid species) on bell pepper (Capsicum annuum L.), chili pepper ( Capsicum frutescens L.), tomato and Tahiti lime in Colombia, to quantify and reveal the taxonomic identity of emerging parasitoid species.
Materials and methods
Cecidomyiidae
To determine the presence of Cecidomyiidae (and its parasitoids), plantations of bell pepper, chili pepper, Tahiti lime and tomato were sampled in the departments of Antioquia, Boyacá, Caldas, Cauca, Cundinamarca, Huila, Nariño, Quindío, Risaralda, Santander and Valle del Cauca in Colombia (Figure 1).
Figure 1 Map of Colombia showing tritrophic interactions in sampled sites. The superior and inferior circumference segments correspond to plant host and insect host respectively. The central point corresponds to parasitoid species.
Plant structures containing Cecidomyiidae were collected from each crop. For tomato, leaves, flowers and fruit were collected; for Tahiti lime, flower buds were collected; and for bell pepper and chili pepper, immature fruits were collected. Every sample location was georeferenced by using a Global Positioning System (GPS; GPSmap 60CSx, Garmin), and the presence/absence of Cecidomyiidae was determined. Plant structures containing larvae were removed and placed in plastic containers (20 x 10 x 5 cm) along with wet napkins to avoid desiccation. Containers were transported to the Laboratory of Entomology and Acarology of the Universidad Nacional de Colombia, Palmira campus and placed into growth chambers (Panasonic MLR-351) under controlled conditions [23°C and 75% relative humidity (RH)]. Adults of the pest species were identified microscopically according to Gagné (1994).
Parasitoids
The Cecidomyiidae larvae that did not develop to adults and showed symptoms of being parasitized (pale green color in the middle section of the larvae and translucent pupae, Figure 2), were retained in controlled-environment chamber until emergence of their parasitoids. Emerged parasitoids were placed in 75% alcohol for one hour, and then maintained refrigerated at -10°C for three days. They were then pinned with micro-entomological pins. Morphospecies were classified using dichotomous keys for family (Masner & Arias-Penna, 2006) and species (Buhl, 2011). A representative specimen of each species was photographed with a camera and attached to a compound stereoscope (SMZ-445), and several pictures of each specimen were taken from different perspectives.
Figure 2 Symptoms of immature stages of Prodiplosis longifila parasitized: a: initial symptom on a parasitized larva, b: parasitoid development on pupae and c: parasitoid emergence. Magnification 35x.
Multifocal compositions were created using the software CombineZP (http://www.hadleyweb. pwp.blueyonder.co.uk/). Parasitoid taxonomic identification was carried out by P. Buhl. Specimens were deposited in the Entomological Museum of the Universidad Nacional de Colombia, Palmira (CEUNP).
Parasitoid searching behavior
For Tahiti lime orchards, a photographic record was obtained (Panasonic Lumix DMC-LX5), and the behavior of Synopeas aff. curvicauda on the flower buds was observed.
Data Analysis
Assuming a similar sampling effort by each crop batch and based on the presence of Prodiplosis spp. in all crops, the abundance of recovered parasitoids by host crop was obtained and parasitoid preference for a host crop was determined using X 2 analysis (null hypothesis of parasitoid equal preference). Due to the fact that some parasitoid species were not recovered from certain crops (values = zero) the Yates' continuity correction for X 2 was used (Daya, 2001).
Results
From 168 batches of crops located between 739 and 2973 m.a.s.l. in the Andes and interandean valleys, the larvae of Cecidomyiidae were found on chili pepper, Tahiti lime, bell pepper and tomato; however, they were not found on asparagus or potato. The presence of P. longifila (on tomato, bell pepper and Tahiti lime), Prodiplosis floricola (on Tahiti lime) and Dasineura sp. (on chili pepper and bell pepper) was confirmed. Examination of 157 parasitoid specimens grown in the laboratory yielded four identified species: Synopeas varipes Harrington (1900) (Figure 3 a,b), Synopeas reticulatifronsBuhl (2011), (Figure 3 c,d), Synopeas aff. longiventre Ashmead (1893) (Figure 3f) and Synopeas aff. curvicauda Foster (1856) (Figure 3e) (Table 1). Parasitoids appeared 15 days after Cecidomyiidae in plantations in which farmer had stopped using insecticides.
Figure 3 Parasitoid wasp species found: Synopeas varipes: female (a.), male (b.); Synopeas reticulatifrons: female (c), male (d); Synopeas aff. longiventre: female (f); Synopeas aff. curvicauda: female (e).
Table 1 Number of parasitoids recovered from Prodiplosis spp. larvae collected in bell pepper, Tahiti lime and tomato crops.
Synopeas varipes Harrington, 1990
Examined material
Colombia, Huila; 4♂♂, 3♀♀; El Agrado, La Yagilda, 2°14'4.5''N, 75°43'56.0"W, 784 m.a.s.l.; 13.II.2013; Prodiplosis (P. longifila and/or P. floricola) larvae collected from Citrus x latifolia in growth chambers coll. L. Miguel Hernández, Yoan Camilo Guzmán, Maria R. Manzano (Museum CEUNP); Huila; 2♂♂, 2♀♀; Garzón, La Junga, 2°14'4.5''N, 75°43'56.0'W, 784 m.a.s.l.; 14.II.2013; Prodiplosis (P. longifila and/or P. floricola) larvae collected from Citrus x latifolia in growth chambers, coll. L. Miguel Hernández, Yoan Camilo Guzmán, Maria R. Manzano (Museum CEUNP). Huila; 1♂, 1♀; Garzón, La Galda, 2°9'38.8''N, 75°43.0'56'W, 784 m.a.s.l.; 14.II.2013; Prodiplosis (P. longifila and/or P. floricola) larvae collected from Citrus x latifolia in growth chambers, coll. L. Miguel Hernández, Yoan Camilo Guzmán, Maria R. Manzano (Museum CEUNP). Santander; 4♂♂, 599; Lebrija, La Laguna, 7°5'57.5'' N, 73°12'54.6'W, 1098 m.a.s.l.; 12.VI.2012; P. longifila and/or Dasineura sp. larvae collected from Capsicum annuum in growth chambers; L. Miguel Hernández, Yoan Camilo Guzmán, Maria R. Manzano (Museum CEUNP). Valle del Cauca; 27♂♂, 17♀♀; Universidad Nacional de Colombia, Palmira campus, 3°30'42.6''N, 76°18'20.8"W, 998 m.a.s.l.; 3.VI.2012; P. longifila larvae collected from S. lycopersicum in growth chambers, coll. L. Miguel Hernández, Yoan Camilo Guzmán, Maria R. Manzano (CEUNP). Valle del Cauca; 6♂♂, 4♀♀; Zarzal, Las Lajas, 4°24'41.2''N, 76°3'20.6'W, 974 m.a.s.l.; 1.II.,2014; Prodiplosis (P. longifila and/or P. floricola.) larvae collected from Citrus x latifolia in growth chambers, coll, L. Miguel Hernández, Yoan Camilo Guzmán, Maria R. Manzano (Museum CEUNP). Valle del Cauca; 1♂, 3♀♀; Candelaria, Experimental Center of Universidad Nacional de Colombia, Palmira campus (also named CEUNP), 3°24'27.1''N, 76°25'6.9'W, 971 m.a.s.l.; 24.IV.,2012; P. longifila larvae collected from S. lycopersicum in growth chambers, coll. L. Miguel Hernández, Yoan Camilo Guzmán, Maria R. Manzano (Museum CEUNP). Antioquia; 299; Támesis, San Isidro, 5°41'9.2''N, 75°41'25.2"W, 1162 m.a.s.l.; 2.V.2013; Prodiplosis (P. longifila and/or P. floricola) larvae collected from Citrus x latifolia in growth chambers; coll. L. Miguel Hernández, Yoan Camilo Guzmán, Maria R. Manzano (Museum CEUNP).
A total of 82 specimens of Synopeas varipes were collected on tomato (48 specimens), Tahiti lime (25 specimens) and bell pepper (9 specimens). Abdomen of the female of the species Synopeas varipes is characterized by the terminal segments forming a deflected tail and the presence of a small sharp scutellar spine. Male can be distinguished by the shape of the abdomen and antennae (Figures 3 a, b, 5a-e). Synopeas. varipes was found in every plantation except chili pepper plantations, and it was especially abundant on Tahiti lime (42 specimens), where it was found together with S. aff. curvicauda on flower buds (Figure 5). Eighty-three specimens of this species were found in all of the plantations. Adults are black and microscopically perforated and have a pale scape. Scutellum has a small sharp spine; the sides of the basal part of the abdomen are hairy and silver in color; legs are brown with yellowish tibia and tarsus; second sternite is clearly convex, and the last is perforated. In males, the last sternite is shorter than the second sternite. The maximum length of the body is 1.1 mm, and head is uniform and clearly perforated (Buhl, 2011).
- e. Synopeas varipes: a. antenna ♀; b. scutellar spine; c. abdomen ♂ (lateral view); d. abdomen ♀ (lateral view); e. abdomen ♂ (dorsal view); f. - i. Synopeas aff. longiventre: f. antenna ♀; g. scutellar spine; h. abdomen ♀; i. abdomen ♂; j. - n. Synopeas reticulatifrons: j. antenna ♂; k. antenna ♀; l. scutellar spine; m. abdomen ♀ (dorsal view); n. abdomen ♀ (lateral view); o. - q. Synopeas aff. curvicauda: o. antenna ♀; p. scutellar spine; and q. abdomen ♀. Scale = 1.00 mm.
Figure 5 Diagram showing the observed parasitoids
Synopeas aff. longiventre Ashmead, 1893
Examined material
Colombia, Santander; 4♂♂, 2♀♀; Lebrija, La Laguna, 7°5'57.5''N 73°12'54.6"W, 1098 m.a.s.l.; 12.VI.2012; Dasineura sp. and/or P. longifila larvae collected from C. annuum in growth chambers, coll. L. Miguel Hernández, Yoan Camilo Guzmán, Maria R. Manzano (Museum CEUNP). Cauca; 1♂; Cajibio, La Viuda, 2°33'33.7''N, 76°34'39.8'W, 1763 m.a.s.l; 5.IV,2013; P. longifila larvae collected from S. lycopersicum in growth chambers, coll. L. Miguel Hernández, Yoan Camilo Guzmán, Maria R. Manzano (Museum CEUNP). Valle del Cauca; 1♂; Roldanillo, Santa Rita, 04°28'04.0''N, 76°07.0'18.1'W, 939 m.a.s.l; 7.IX,2012; Dasineura sp. larvae collected from C. frutescens in growth chambers, coll. L. Miguel Hernández, Yoan Camilo Guzmán, Maria R. Manzano (Museum CEUNP).
A total of 8 specimens of this species were collected on tomato (1 specimen), bell pepper (6 specimens) and chili pepper (1 specimen). The identity of S. aff. longiventre should be elucidated in order to determine whether thus is a new species because it is similar to S. longiventre. Female of S. aff. longiventre has an abdomen that is twice as long as thorax and partially compressed when observed dorsally, and scutellum has a very small spine (Figures 3f, 5f-i). The antennae have 10 segments (Figure 5f), which are covered by filaments in males.
Synopeas reticulatifrons Buhl, 2002
Examined material
Colombia, Valle del Cauca; 18♂♂, 22♂♂; National University of Colombia, Palmira campus, 3°30'42.6''N, 76°18'20.8''W, 998 m.a.s.l.; 3.VII.2012, P. longifila larvae collected from S. lycopersicum in growth chambers, coll. L. Miguel Hernández, Yoan Camilo Guzmán, Maria R. Manzano (Museum CEUNP). Valle del Cauca; 3♂♂, 1♀; Candelaria, Experimental Center of the National University of Colombia, Palmira campus (Museum ECNUP), 3°24'27.1''N, 76°25'06.9''W, 971 m.a.s.l.; 16.IV.2012; P. longifila larvae collected from S. lycopersicum in growth chambers; coll. L. Miguel Hernández, Yoan Camilo Guzmán, Maria R. Manzano (Museum CEUNP). Huila; 2♂♂, 1♀; Garzon, La Galda, 2°14'4.5''N, 75°43'56.0'W, 784 m.a.s.l.; 13.II.2013, Prodiplosis (P. longifila and/or P. floricola) larvae collected from C. x latifolia in growth chambers; L. Miguel Hernandez, Yoan Camilo Guzman, Maria R. Manzano (Museum CEUNP). Huila; 1♂, 1♀; Garzon, La Junga, 2°14'4.5''N, 75°43'56.0'W, 784 m.a.s.l.; 13.II.2013, Prodiplosis (P. longifila and/or P. floricola) larvae collected from C. x latifolia in growth chambers; L. Miguel Hernandez, Yoan Camilo Guzman, Maria R. Manzano (Museum CEUNP). Antioquia; 1♂; Marinilla, 06°09'54.4''N, 075°20'05.3''W, 2178 m.a.s.l.; 29.II.2013, P. longifila larvae collected from S. lycopersicum in growth chambers; coll. L. Miguel Hernandez, Yoan Camilo Guzman, Maria R. Manzano (Museum CEUNP).
A total of 50 specimens of this species were collected on tomato (45 specimens) and Tahiti lime (5 specimens). Adults are black in color, the abdomen is almost as long as the head and thorax combined and slightly wider than the thorax; and the scutellar spine is longer than the propodeum and has a translucent end (Figures 3 c,d; 5 l-n). The males of this species are differentiated from the females by their antennae: the apical segments of males are longer than they are wide (Figure 5j, k).
Synopeas aff. curvicauda Forster, 1856
Examined material
Colombia, Valle del Cuaca; 5 ♀♀; Palmira, Corporación Colombiana de Investigación Agropecuaria (CORPOICA), 3°30'45.7''N, 76°18'53.1"W, 1006 m.a.s.l.; 16.V.2012; directly collected from flower buds of Tahiti lime trees, coll. L. Miguel Hernández, Yoan Camilo Guzmán, Maria R. Manzano (CEUNP). Valle del Cauca; 3♂♂, 5♀♀; Zarzal, Las Lajas, 4°24'41.2''N, 7603'20.6"W', 974 m.a.s.l.; 14.II.2014; Prodiplosis (P. longifila and/or P. floricola) larvae collected from growth chambers; coll, L. Miguel Hernández, Yoan Camilo Guzmán, Maria R. Manzano (Museum CEUNP). Huila; 2♂♂, 1♂; Garzón, La Junga, 2°9'38.8''N, 75°39'36.8'W, 739 m.a.s.l.; 14.II.2013; Prodiplosis (P. longifila and/or Prodiplosis floricola) larvae collected from C. x latifolia in growth chambers, coll. L. Miguel Hernández, Yoan Camilo Guzmán, Maria R. Manzano (Museum CEUNP). Antioquia; 1♂; Tamesis, San Isidro, 5°42'09.0''N, 75°40'24.8'W, 845 m.a.s.l.; 2.V.2013, Prodiplosis (P. longifila and/or P. floricola) larvae collected from Citrus x latifolia in growth chambers; coll. L. Miguel Hernández, Yoan Camilo Guzmán, Maria R. Manzano (CEUNP).
A total of 17 specimens of this species were collected on Tahiti lime. It is important to confirm whether Synopeas aff. curvicauda is new because it is similar to S. curvicauda (but with shorter basal flagellar segments in the female). This species was observed only on Tahiti lime (16 specimens) where both P. longifila and P. floricola were found. However, it is unknown if both P. longifila and P. floricola are parasitized by Synopeas aff. curvicauda Forster. The adults are black with uniformly perforated head (Figure 3e); female abdomen is 1.6 times longer than the head and thorax combined but narrower than the thorax (Figure 3e). Antennae and scutellar spine are shown in Figures 3, 5. The main feature of the abdomen is its comma shape (Figures 3e, 5o-q).
Parasitoid searching behavior
In Tahiti lime orchards, Synopeas aff. curvicauda wasps were observed walking on flower buds using their antennae to locate the small space formed in the flower bud corolla to place the ovipositor and lay eggs (Figure 4).
Parasitoid-plant association
Numbers of parasitoids recovered from Prodiplosis species collected on different host plants are presented in Table 1. Parasitoid species were not equally found on all host plants (X 2 (continuity) = 93.11, df = 6, P < 0.05). Synopeas varipes and S. reticulatifrons were the most abundant species (84.6% of total recovered parasitoids) and they were associated mainly to tomato. On Tahiti lime three parasitoid species were found (30.1% of total recovered parasitoids) and Synopeas aff. curvicauda was found only on this crop (10.9% of total recovered parasitoids).
Discussion
In this study, four Synopeas species (Synopeas aff. curvicauda Synopeas aff. longiventre, S. reticulatifrons and Synopeas. varipes) were collected from three different host species of Cecidomyiidae (Prodiplosis longifila, P. floricola and Dasineura sp.) living on three commercial species of Solanaceae (tomato, chili pepper and bell pepper) and on Tahiti lime. In the New World information about Synopeas-host interaction is not complete.
On one hand Synopeas hosts have not been identified. Several Synopeas species have been described in temperate areas (Buhl, 1997; Buhl, 2011; MacGown & Evans, 2003) and a few in tropical areas such as Panama, Brazil and Costa Rica (Buhl, 2011) but mostly with unknown hosts. Because of the small size of cecidomyiid larvae which makes it difficult to separate species, it was not possible to clarify if Synopeas aff. curvicauda parasitizes both P. longifila and P. floricola. Molecular tools may be useful to improve these results (Hrcek, Miller, Quicke & Smith, 2011). On the other hand, the Synopeas species that regulate P. longifila in Peru, Ecuador (Valarezo et al., 2003) and in USA (Peña, Duncan & Torres, 1990) remain unidentified.
In general, members of the superfamily Platygastroidea rarely parasitize a wide range of hosts (Austin, Johnson & Dowton, 2005). Abram et al. (2012), presented a complete revision of the species of Cecidomyiidae that are considered crop pests and confirmed a low specificity between Synopeas and their Cecidomyiidae hosts. For example, species such as Synopeas myles (Walker) is able to parasitize five Cecidomyiidae species of the genera Contarinia and Dasineura (Abram et al., 2012). Similarly, S. varipes, found in the present study parasitizes P. longifila in tomato, Dasineura sp. on chili pepper and the P. longifila - P. floricola complex on Tahiti lime. Moreover, S. varipes is also a parasitoid of D. mali on apples (Buhl, 1997). Although our study did not test parasitoid attraction some hypothesis may explain our results.
Firstly, Prodiplosis and Dasineura feed on plant tissue by scraping the epidermal tissues of plant structures using piercing-sucking mouthparts (Gagné, 1994) and this damage could induce volatile production which can be detected by parasitoids. For Brassicaceae species it was found that volatile emissions are very similar when plant are damaged by different herbivores and parasitoids cannot detect these differences (Gols & Harvey, 2009). For example our results show that S. aff. curvicauda was found only on Tahiti lime where P. longifila and P. floricola coexist in the same flower bud (Duque-Gamboa, 2017. In Press.) and probably producing similar attractive volatiles.
Synopeas curvicauda parasitizes Contarinia solani (Rübsaamen) on Solanum dulcamara L. blossoms and is probably attracted by its odors. Our field observations showed that Synopeas aff. curvicauda flew to Tahiti lime flower buds to detect and parasitize Prodiplosis larvae. Citrus blossoms produce volatile compounds such as linalool, β-myrcene, a-myrcene, limonene, (E)-ocimene, methyl anthranilate and indole, which are most likely involved in attracting other insects, such as pollinator bees (Jabalpurwala, Smoot & Rouseff, 2009) . Females of Synopeas aff. curvicauda were observed on Tahiti lime orchards on flower buds while using their antennae repeatedly to locate the upper orifice before they began laying their eggs. The detection of chemical information by Platygastroidea appears to be conducted by one or two multiporous gustatory sensilla located in the lower part of the antennal clavus (Austin, Johnson & Dowton, 2005).
Our results revealed three Synopeas species (Synopeas aff. longiventre,S. reticulatifrons, and S. varipes) with potential as biological control agents of P. longifila on tomato given the threat of this pest for tomato trade. These species merit biological and behavioral studies before being selected for augmentative biological control programs (Van-Lenteren & Manzaroli, 1999) as they are key species to be studied for developing conservative biological control, an approach suggested for Dasineura brassicae on Brassicae in Europe including some Platygastridae species (Ulber, Williams, Klukowski, Luik & Nilsson, 2010) . The value of biological control of Synopeas species against P. longifila was noted for Tahiti lime in the USA (Goldsmith, Castillo & Clarke-Harris, 2013) and Synopeas sp. was reared and released in asparagus in Peru to control P. longifila. Parasitoids are more specific than other biological control agents and therefore have restricted host ranges, which is an advantage to implement biological control programs (Van-Lenteren & Manzaroli, 1999). The finding and taxonomic identification of Synopeas species in the present study open a new opportunity to explore their potential to be used in IPM programs in order to reduce the high input of pesticides against P. longifila in the tropics (Valarezo et al., 2003; Kroschel et al., 2012). It is unknown if P. longifila or P. floricola cause economic damage to Tahiti lime orchards in Colombia (Hernandez et al., 2015; Duque-Gamboa, 2017) and if that is the case, the results of the present study indicate that Synopeas aff. curvicauda would be the parasitoid species to be further investigated.
Conclusion
Four species of parasitoids (S. varipes, Synopeas aff. longiventre, S. reticulatifrons and Synopeas aff. curvicauda) were found associated with three cecidomyiid species (Prodiplosis longifila, Prodiplosis floricola and Dasineura sp.) in four crops (chili pepper, bell pepper, Tahiti lime and tomato) conforming a complex of plant-herbivore-parasitoid interactions. Parasitoid species were not equally found in all host plants (X 2 (continuity) = 93.11, df = 6, P < 0.05) and they were more abundant on tomato crops and Tahiti lime orchards. Synopeas varipes and S. reticulatifrons were the most abundant species (84.6% of total recovered parasitoids). Synopeas aff. curvicauda was the only parasitoid species found on Tahiti lime.
