The passion flowers belong to genus Passiflora L. and are the most representative and abundant of the family Passifloraceae (Feuillet & McDougal 2007). Passion flowers include more than 500 described species and are distributed in tropical and sub-tropical areas around the world (Vanderplank 2000). Some species of this genus as Passiflora edulis f. flavicarpa Deneger (yellow passion fruit) and Passiflora edulis f. edulis Sims (purple passion fruit) are economically important worldwide (Martin & Nakasone 1994). Whereas, species as Passiflora ligularis Juss (sweet granadilla) and Passiflora quadrangularis L. (giant granadilla) are cultivated mainly in the Andean regions (Kluge 1998). In Peru, the purple passion fruit and sweet granadilla are the principal passion flowers cultivated, with an estimated production reaching 20000 tm in 5000 hectares and 50000 tm in 5800 hectares, respectively (Carrasco 2018, Ramos 2018). In this country, the province of Oxapampa (Pasco region) stands out as the main sweet granadilla producing area, with one third of the total national production (Mendieta 2015). Moreover, such province also has several favorable ecological conditions for the production of other passion flowers species.
Fruit flies (Diptera: Tephritidae) comprise a series of polyphagous species which cause damage in fruits and loss of export markets due to quarantine restrictions by fruit importing countries. In this family, the genus Anastrepha Schiner is the most diverse and economically important fruit fly species in the Neotropical region, including a large number of major fruit pests (Aluja 1994, Norrbom et al. 1999). In Peru, the main species associated with damage on cultivated host plants are Anastrepha fraterculus (Wiedemann), Anastrepha distincta Greene, Anastrepha obliqua (Macquart), Anastrepha serpentina (Wiedemann), Anastrepha striata (Schiner) and Anastrepha chiclayae (Greene) (Korytkowski 2001). However, reports of Anastrepha infesting passion flowers are not documented in Peru. Therefore, the aim of this study was to evaluate the presence of Anastrepha in fruits of passion flowers cultivated in Peru.
During September to December 2016 and January to August 2018 samples of ripe and unripe fruits from six species of passion flower was systematically collected in ten commercial orchards and in nearby areas in the understory, within province of Oxapampa (Table 1). The number of collected fruits flies varied according to the fructification season of each host species as well as fruit availability. In 2016, fruits were taken to Entomology Laboratory of Servicio Nacional de Sanidad Agraria (SENASA) of Oxapampa, while in 2018 the samples were taken to the Entomology Laboratory of Universidad Nacional Daniel Alcides Carrión (UNDAC). In these places, fruits were weighed and deposited for 48-96 h in trays containing sand and covered by organza voile. Puparia were placed on pots containing sand and closed with fabric for the emergence of adults. The adult flies of Tephritidae and Lonchaeidae were identified at species level using a stereomicoscope and biological microscope (Norrbom and McAlpine 1997, Zucchi 2000). Specimens were deposited in the collection of Fruit Fly Taxonomy Laboratory of Agrarian National Health Service (register in Sistema Integrado de Información de Mosca de la Fruta - SIIMF, SENASA), personal collection of P.C Strikis and the entomological collection of the UNDAC filial Oxapampa. In addition, samples of passion flowers were taken to Herbaria Oxapampa (Hoxa) for confirmation at the species level.
A total of 205 fruits (18.3 kg) of six passion flowers species were sampled, and we found three species that showed damage caused by frugivorous flies. Anastrepha pseudoparallela (Diptera: Tephritidae) caused infestation in unripe (8♂, 13♀) and ripe (7♂, 13♀) Passiflora ambigua fruits and P. quadrangularis unripe fruits (7♂, 2♀) (Table 1). In both cases, the larvae damaged the fruit by feeding the pulp stimulating rot and contamination with microorganisms owing to their excrements (Fig. 1A - B). Unripe and ripe fruits of P. ambigua were infested, while, these larvae bored until the mesocarp in high infestations (Fig. 1B). Passiflora quadrangularis evidenced damage caused by larvae only in unripe fruits; besides, the fruit skin showed oviposition puncture produced by female to lay eggs (Fig. 1C). Damages on P. ligularis were caused by Dasiops frieseni Norrbom & McAlpine (Diptera: Lonchaeidae) (16♂ ,19♀), evidenced by the wrinkling aspect in unripe fruits and pulp rot as the main trace (Fig. 1D) according to Salazar Mendoza et al. (2019). Nevertheless, P. alata, P. edulis f. edulis and P. edulis f. flavicarpa showed no evidence of larvae inside or any other damage caused by frugivorous flies.
Anastrepha pseudoparalella is considered endemic to the South America Tropics (Hernández-Ortiz & Aluja 1993) and was reported infesting Passiflora alata Dryand (sweet passion fruit) in the Southeastern of Brazil (Aguiar-Menezes 2004). In Peru, there is no documented damage caused by A. pseudoparallela in host plants, but only catch of adults in traps baited with hydrolyzed protein (Korytkowski & Peña 1968) are related. Species of Passifloraceae are commonly recognized for having cyanogenic compounds, flavonoids and phenolics in various parts of the plant (Dhawan et al. 2004) which are used as a mechanism of defense against the attack of insect herbivory (Lindroth & Batzli 1984, Freeman & Beattle 2008, War et al. 2012). The success in the larval development of A. pseudoparallela inside the fruits showed the ability of this species to tolerate such chemical defenses and indicated a high degree of specialization in some passion flowers (Stefani & Morgante 1996).
Species of genus Dasiops Rondani has been frequently associated to damage in fruits of Passiflora, and are considered important herbivore of passion flowers crops (Conpes 2008, Wyckhuys 2011). In Brazil, D. frieseni was reported infesting fruits of P. alata (Aguiar-Menezes et al. 2004) and P. edulis f. flavicarpa (Strikis et al. 2011).Galindo et al. (2014) found association and described the damage of Dasiops yepezi Steyskal, Dasiops gracilis Norrbom & McAlpine and Dasiops caustonae Norrbom & McAlpine in fruits of four passion flowers cultivated in Colombia: P. ligularis, P. mollissima, P. edulis f. edulis and P. edulis f. flavicarpa. On the other hand, Dasiops sp and D. frieseni were associated with fruit damage to P. ligularis in Peru (Salazar-Mendoza & Romero-Rivas 2016, Salazar-Mendoza et al. 2019). Through our study, we found that P. ligularis is not a host of fruit flies of the family Tephritidae.
Therefore, this is the first report of A. pseudoparallela infesting host fruits in Peru and the first time that a species of Tephritidae is associated to damage of passion flowers cultivated in Andean regions. More studies must be developed to understand the biology, ecology and behavior this species which could have important effects on some passion flowers production in this region.