Journal of Economic Entomology, 113(3), 2020, 1158–1175

doi: 10.1093/jee/toaa026
Advance Access Publication Date: 4 March 2020
Commodity Treatment and Quarantine Entomology Research

Nonhost Status of Commercial Sweet Granadilla

(Passiflora ligularis) in Peru to Ceratitis capitata (Diptera:
Tephritidae) and Anastrepha fraterculus
Orlando S. Dolores,1 Javier M. Layme, and Carlos C. Huaynate
Servicio Nacional de Sanidad Agraria (SENASA), La Molina 1915, La MOlina, Lima 15024, Peru and 1Corresponding author, e-mail:
[email protected]

Subject Editor: Lisa Neven

Received 30 May 2019; Editorial decision 29 January 2020

Abstract
The host status of sweet granadilla (Passifflora ligularis Juss.) to Ceratitis capitata (Wiedemann) and
Anastrepha fraterculus (Wiedemann) in Peru was determined. Experiments were conducted in Pasco (Peru)
in four different orchards, over 2 yr (2016 and 2017), two orchards per year. Choice (granadilla plus natural
host) and no-choice foraging behavior trials were conducted using sleeves under field conditions, and forced
infestation was examined in laboratory cages, with five females per fruit. The development time of C. capitata
was determined, and the oviposition behavior of C. capitata and A. fraterculus was examined. Three fruit ma-
turity stages of intact (n = 1,320) and punctured (n = 1,320) granadilla fruits were examined. Adult C. capitata
(n = 4,418) and A. fraterculus (n = 2,484) were trapped in the orchards, and commercial granadilla fruits
(n = 1,940) sampled and dissected. Fruit fly infestation was not found in any intact granadilla fruits. Larvae
and pupae were found inside punctured granadilla only in fruits broken after 20 d, and adults only emerged
when those pupae were removed from the fruit. Ceratitis capitata development time was longer in punctured
granadilla than that in host fruit. In the oviposition test, A. fraterculus and C. capitata did not lay eggs in intact
granadilla, and C. capitata laid eggs in punctured fruits but larvae were not found. Because of the resistance
mechanisms of the pericarp, commercial fruits of Passiflora ligularis are not a natural host of C. capitata and
A. fraterculus in Peru.

Key words: Granadilla, Anastrepha, Ceratitis, Tephritidae, host status

Passiflora ligularis Juss. is commonly known as sweet granadilla Castillo and Ortiz (2011) sampled fruit in Oxapampa (Pasco,
or yellow passion fruit, and is native to Peru (Chóez et al. 2015). Peru), and infestations of Ceratitis capitata (Wiedemann) and
Passiflora is the genus of greatest economic importance in the family Anastrepha fraterculus (Wiedemann) were not found in sweet gran-
Passifloraceae with approximately 530 species distributed in the new adilla fruits, but fruits were infested by Dasiops sp. and Neosilva
world (Ulmer and MacDougal 2004). The main passion fruit pro- sp. (both in the family Lonchaeidae). However, information on the
ducers are found in South America, primarily in Brazil, Colombia, condition of the fruits (i.e., maturity stage, presence of damages,
Peru, and Ecuador. Commercial passion fruit crops are also found in whether from a plant or fallen on the ground) was not provided. In
Australia, Hawaii (United States), India, New Guinea, Kenya, South addition, these authors related the infestation to the larvae found
Africa, Sri Lanka, and Costa Rica. In Peru, sweet granadilla is culti- but not to emerged adults. They also noted that flies of the genus
vated primarily in highland valleys and jungles, such as those found Dasiops oviposit on and infest flowers and fruits of sweet granadilla
in the Pasco, Cajamarca, La Libertad, and Piura departments, whose Passiflora ligularis; however, larvae remained inside fruits and only
commercial areas are considered the largest in the country. left them after fruits fell to the ground. This behavior suggests that
Korytkowski (2001) in a review of the genus Anastrepha in Lonchaeidae larvae are not capable of leaving the fruits for pupation
Peru and linked some of the recorded species with passion fruit and have to wait for the fruit pericarp to break naturally to exit,
by noting that A. chiclayae Greene had been bred from Passiflora. which demonstrates that the pericarp is the fruit cover that provides
Furthermore, A. curitis Stone, is mentioned in connection with mechanical resistance to the fruit and thereby prevents larvae from
Passiflora quadrangularis L. and the fruits of Passiflora sp. Similarly, leaving.
the author states that Passiflora quadrangularis is a host of In Hawaii, Liquido et al. (1990) collected Passiflora ligularis fruits
A. pseudoparalella Loew. from the plant and those fallen on ground and found infestation

© The Author(s) 2020. Published by Oxford University Press on behalf of Entomological Society of America. 1158
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Journal of Economic Entomology, 2020, Vol. 113, No. 3 1159

by C. capitata, but the maturity level and fruit conditions were not pectin isolates (13.6%) of high esterification (79%) with the highest
indicated. viscosity (3.41 dl g−1) was found in the mesocarp fraction. The mois-
In Venezuela, Carrero et al. (2000) reported A. pallidipennis ture contents were also low at 4.5, 6.1, 6.0, and 4.3% for the exo-
Greene from damaged fruits of ‘parchita maracuya’ (Passiflora edulis carp, mesocarp, endocarp, and pericarp, respectively.
f. sp. flavicarpa Sims) for the first time. In the laboratory, adults Chóez et al. (2015) complemented the information on chem-
were obtained from naturally infested fruits. When fruits that re- ical composition and found 22 chemical compounds associated
mained attached to plants were collected and moved to laboratory, with essential oils in the shell of granadilla P. ligularis in Ecuador.
the examination revealed larvae with typical dipteran characteristics, Approximately 34% of the chemical compounds corresponded to
and when they completed their development to adult fruit flies, the squalene, which according to Ahmed et al. (2018), has toxic and
genus Anastrepha was identified. repellent effects against phytophagous insects and mites. This result
In Colombia, Rengifo et al. (2011) conducted a host status study suggests that squalene prevents females from laying eggs, in addition
for the fruit fly C. capitata in purple passion fruit P. edulis f. edulis. to the hardness and thickness of the pericarp. Therefore, squalene
The authors did not find larvae or emerged adults from 976 fruits could be the first instance of chemical resistance identified in gran-
manually harvested or from 623 fruits fallen on the ground. Under adilla fruits against tephritid fruit flies.
laboratory conditions, forced infestation experiments with punc- Because this background information does not conclusively state the
tured and intact fruits were conducted with C. capitata to determine host status of commercial granadilla fruits to tephritid fruit flies in Peru,
the acceptability of different maturity stages and the physiological a demonstration of the nonhost status of commercial sweet granadilla
suitability of different stages of fruit development. For intact fruits, P. ligularis fruits to C. capitata and A. fraterculus under the specific con-
C. capitata females oviposited exclusively in fruits with a zero level ditions of sweet granadilla production areas, as well as identifying the
of maturation (Maturity index 18.4; ICONTEC 1997), with 41.67% resistance mechanisms that might be involved, is important.
of fruits accepted for oviposition at a rate of 183.1 ± 33.8 eggs per
fruit. However, oviposition was not reported for fruits with mat-
uration levels of 2 and 4 (maturity index 26.0 and 32; ICONTEC Materials and Methods
1997). In punctured fruits, C. capitata laid 84,410 and 84,250 eggs The information on materials and methods applied and/or used
inside fruits with maturation levels of 0 and 2, respectively, but the in this study was obtained from Cowley et al. (1992), Aluja et al.
emergence of C. capitata adults did not occur at any level of ma- (2004), Aluja and Mangan (2007), North American Plant Protection
turity. Based on these laboratory tests, the authors concluded that Organization NAPPO (2005), and International Standard for
purple passion fruit was not a host to C. capitata. Phytosanitary Measures-ISPM standard #37. Although the preferred
In Colombia, Wyckhuys et al. (2012) determined the compos- name for P. ligularis is sweet granadilla (CABI 2018), only granadilla
ition and seasonal dynamics of the Diptera species complex asso- is used this research paper.
ciated with three passion fruit crops (P. edulis f. edulis, P. edulis
f. flavicarpa, and P. ligularis). The research was conducted from 2008
to 2010 by trapping in passion fruit commercial orchards. Fifty-five Experimental Locations
flies of the Tephritidae were found, with 37 individuals obtained The research area was in Oxapampa (409 km from Lima City),
from P. ligularis fruits and 18 from those of P. edulis f. edulis. Among which is one of the provinces of the Pasco department that is geo-
the tephritid flies in P. ligularis orchards, 86% were A. fraterculus, graphically limited by Huanuco (north), Lima (west), Junin (south),
3% were A. obliqua Macquart, 5% were A. striata, and 5% were and Ucayali (east). Oxapampa is the highest granadilla production
A. grandis Macquart. The tephritid flies captured in P. edulis f. edulis area in Peru with approximately 2,000 ha. The predominant produc-
orchards included A. fraterculus (95%) and A. striata (5%). tion scale is small-farmer based (based on area in accordance with
Cowley et al. (1992) adopted the fruit fly host definition for quar- references provided by the Food and Agriculture Organization of the
antine situations: ‘Any fruit or vegetable in which fruit fly oviposit United Nations-FAO 2017).
under field conditions, the eggs hatch into larvae, and the larvae ac- The climate in Oxapampa is characterized by medium rainfall
quire sufficient sustenance to form viable pupae from which adults levels (1,000–1,500 mm), temperature ranging from 18 to 25°C,
emerge and are capable of reproduction’. These authors also ex- and Relative Humidity between 70 and 90%. Weather data were
pressed that adult fruit flies should be obtained by rearing from in- obtained from the Oxapampa Meteorological Station that be-
fested, unsprayed hosts (i.e., wild rather than laboratory-bred flies longs to Servicio Nacional de Meteorologia e Hidrologia del Peru
should be used). Because flies derived from wild populations often - SENAMHI (meteorological national authority).
fail to mate or oviposit, a laboratory-breeding colony can be used. Sweet passion fruit plants in Oxapampa study orchards were 3
However, a breeding colony should be supplemented with the add- yr old and grafted on passion fruit rootstock. Said orchards are sur-
ition of wild flies every 2 yr to maintain genetic similarity between rounded by coffee, guava, citrus, among other crops. Four experi-
the laboratory colony and the wild population. With the supplemen- mental orchards were used: two in Huancabamba sector, Laturachi
tation of laboratory colonies with wild flies, situations are avoided subsector (Boronda and Ortiz orchards), and two in Chorobamba
in which laboratory flies develop different ovipositional preferences. sector, San Martin subsector (Espinoza and Asconoa orchards). The
Canteri et al. (2010) examined the chemical structure and com- Ortiz (10°22′34.25″ S, 75°34′33.89″ W; 2093 m a. s. l.) and Espinoza
position of the pericarp of granadilla fruit sand note that the most (10°35′46.62″ S, 75°29′3.64″ W; 1933 m a. s. l.) orchards were used
abundant component of pericarp and its fractions (epicarp or exo- in 2016; whereas the Boronda (10°22′12.44″ S, 75°35′10.45″ W;
carp, mesocarp, and endocarp) is total dietary fiber (48–65%), with 2227 m a. s. l.) and Asconoa (10°36′4.47″ S, 75°29′18.51″ W; 1897
61, 66, 48, and 65% fiber for the exocarp, mesocarp, endocarp, and m a. s. l.) orchards were used in 2017.
pericarp, respectively. In addition, the xylose content was relatively Importantly, during the execution of the field experiments and at
high at 133.4, 31.8, and 15.9 mg g−1 for the exocarp, mesocarp, and least 1 mo before they began, insecticides (including oils) were not
endocarp, respectively. Other monosaccharides and polysaccharides sprayed over the lots under study. Therefore, control measures other
were also found. The authors also stated that the highest content of than pesticides were implemented to solve specific pest problems.
1160 Journal of Economic Entomology, 2020, Vol. 113, No. 3

Species of Tephritidae and Sources of Insects were not rotten were dissected to remove immature stages (larvae or
Adults of C. capitata and A. fraterculus of wild origin (few gener- pupae) that had not left the fruits.
ations under captivity and host fruits as the larval diet) were used in Once removed from fruit, the pupae were placed in small plastic
this study. The colony was collected from the study area, both species containers to recover adults. After emergence and once their wings
of fruit flies were reared for at least fifth filial generation [ISPM 37 reached complete coloration (2–3 d), the recovered adults were
(2017)]. The adult fruit flies were recovered from field-collected host placed in small plastic containers containing 70% alcohol and iden-
fruits, such as mango Mangifera indica L. (Anacardiaceae) and guava tified to species.
Psidium guajaba L. (Myrtaceae) for A. fraterculus and peach Prunus
persica L. (Rosaceae) and coffee Coffea arabica L. (Rubiaceae) for Granadilla Fruit Sampling at the Experimental
C. capitata. These fruits were maintained at 26 ± 2°C and 65 ± 5% Orchards
RH in boxes with pupation media (we used sand instead of ver- To determine whether granadilla fruits could be infested by natural
miculite) according to the procedure described by Aluja (2004). The populations of fruit flies in each experimental orchard during har-
emerged adults were placed in 40 × 40 cm Plexiglas cage with water vest (Within April and November), 50 commercial fruits were ran-
and food (3:1 mixture of sugar and hydrolyzed protein). The adults domly harvested every 15 d and transported to the laboratory using
were mass-reared in room conditions at 26 ± 2°C and 65 ± 5% RH, Tecnopor boxes, which were labeled by orchard name, sampling
with a 12:12 (L:D) h photoperiod. date, trap code, number of fruits, and name of collector. At the la-
boratory, 50% of the fruits were cut immediately and searched for
Trapping C. capitata and Anastrepha spp. Adults in eggs and larvae, whereas the other 50% were placed individually in
Experimental Granadilla Orchards maturation boxes and subsequently dissected after 15 d to search
To corroborate the occurrence of tephritid species, a trapping system for fruit fly larvae and pupae. A 15-d period before dissecting the
was implemented in the experimental granadilla orchards. The fruits was considered an appropriate length of time for fly devel-
system was set up according to the SENASA Phytosanitary Programs opment in fruits that had been exposed to naturally occurring fruit
and Fruit Fly Section (SMFPF 2006). McPhail traps were baited with flies. The sampled and dissected fruits and recovered adults were
Torula yeast pellets (Coltec Comercializadora Agrotecnologica S.A., recorded.
Guatemala; Lot Number P155-715), 4 of which were dissolved in
250 ml of water with 5% of Borax as a lure for capturing adult Granadilla Fruit Maturity Stages
Anastrepha spp. and C. capitata. The traps were rebaited on a To determine the fruit maturity stage, the ICONTEC (1997) Norma
weekly basis. The McPhail traps were hung from granadilla plant Tecnica Colombiana 4101 Fruta fresca. Granadilla. Specifications
branches, and all flies captured were put in 50 cm3 vials with 70% were used as a reference, and only the three maturity stages of green
alcohol. (Fig. 1A), green-yellow (Fig. 1B), and yellow (Fig. 1C) were con-
In Huancabamba sector, 7 km from Oxapampa, 3 and 11 McPhail sidered in the study. The physical attribute (color) was the primary
traps were installed in San Martin and La Florida subsectors, re- attribute, but chemical characteristics such as total soluble solids
spectively. In Chorobamba sector, 24 km from Oxapampa, 7, 10, (TSS, °Brix), acidity (A, %), and maturity index (MI) were also
and 6 McPhail traps were installed in Ancahuachanan, Lanturachi, evaluated. The fruit maturity index (MI), according to ICONTEC
and Mallapampa subsectors, respectively. (1997), is a measure of the balance between sweetness and acidity,
The traps were placed inside and around the experimental and the following formula was applied: MI = TSS/Acidity.
orchards at the rate of 1 trap per each 20 ha, which is equiva-
lent to 5 traps per km2 (=100 ha). The following parameters were Forced Infestation Trials Using Sleeves Under Field
recorded: 1) total number of hectares under trapping; 2) total
Conditions
number of traps; and 3) FTD (fruit flies/trap/day). All traps were
This research was conducted in two experimental orchards during
georeferenced using GPS (Global Positioning System) and were
the 2-yr study period. Organza-made sleeves (0.5 m in diameter
checked by SENASA personnel specialized in fruit fly trapping
and 1 m in length) were used to enclose granadilla fruit-bearing
management, following procedures in the National fruit fly detec-
branches (Fig. 1D). In this experiment, the three maturity stages
tion system manual (SENASA 2010).
(green, green-yellow, and yellow) were tested (Every sleeve con-
The information accumulated during 1 yr and 8 mo was used to
tained only one maturity stage). Each sleeve-enclosed branch con-
determine the fruit fly population levels during this study.
tained five fruits. The age of the flies varied between 7 and 12 d
(C. capitata) and 12 and 17 d (A. fraterculus). In each sleeve, sexu-
Infestation-Level Assessment for A. fraterculus and ally mature male and female fruit flies were released at a rate of
C. capitata in Natural Hosts Located in Perimeter five couples per fruit (Fig. 1E). These flies remained in the sleeve for
and Interior Portions of Experimental Orchards four consecutive days with water and food (standard protein-sugar
To define the potential sources of fruit fly infestation that reached mixture in a solid state).
the experimental orchards, the fruits of all species of plant hosts and The fruit flies were released under two experimental fruit condi-
weeds with fleshy fruits that were growing either inside or outside tions: Choice (CH) and No-Choice (NCH). The treatments were in-
of the experimental orchard perimeters, plus those found in sur- tact (CH-intact and NCH-intact) and punctured (CH-puncture and
rounding native and wild vegetation, were sampled during the 2-yr NCH-puncture) fruits. The NCH experiment used five granadilla
study. Granadilla fruits that fell to the ground from each orchard fruits naturally hanging from the plant. The CH experiment used
were also included as noncommercial fruit, and any damage either five granadilla fruits naturally hanging and five natural host fruits
mechanical or that produced by external feeders was recorded. (peach for C. capitata and mango for A. fraterculus), artificially
The sampled fruits were labeled and taken to the laboratory. The hung from the plant with a 5 cm distance between a granadilla fruit
samples were weighed and placed in maturation boxes, with bot- and a host fruit. In addition, five natural host fruits alone artificially
toms containing sand to facilitate pupation. After 10 d, all fruits that hung within a sleeve and were used as the control.
Journal of Economic Entomology, 2020, Vol. 113, No. 3 1161

A B C

D E

G
G

F H

Fig. 1. Maturity stages of granadilla fruits: (A) Green stage; (B) Green-yellow stage; and (C) Yellow stage. Sleeves enclosing branches of green granadilla fruits
with host fruits for the Choice test (D) and yellow (mature) granadilla fruits for the No-choice test (E); granadilla fruit being punctured for experimental test (F);
Three maturity stages of granadilla fruits (G); and cages under laboratory conditions (H).

To ensure that fruit flies/fruit proportion did not change during bore) (Fig. 1F) and as deep as 10 mm. To determine whether host
the experiment, the sleeves were checked every morning, and an- fruits had been previously infested, 40 fruits per lot and per fruit
other fly of the same species, age, and sex replaced each dead fly. species were placed into plastic bins or boxes (60 cm length ×
A total of 375 sleeves were used in the entire study. For tests 50 cm width × 10 cm depth) to allow the eventual development of
with granadilla in 2016, 60 sleeves for C. capitata were set up in fruit fly larvae.
the Huancabamba sector. In 2017, 120 sleeves were installed for All tests were performed with only wild fruit fly females. After
A. fraterculus in the Huancabamba sector, 60 sleeves for C. capitata a 4-d exposure period, all fruits were removed, taken to laboratory,
in the Chorobamba sector, and 60 sleeves for C. capitata in the and individually weighed. The conditions were recorded when an
Huancabamba sector. Additionally, 75 sleeves (15 sleeves for each infestation occurred.
fruit fly species, experimental year, and place) were established for After some time, when fruits started to rot, all larvae possible
natural host fruits. were expected to leave the fruits. Therefore, host fruits were dis-
For the punctured CH and NCH tests, each granadilla fruit sected on day 10 after exposure. Because no larvae left granadilla
was punctured the day the trial began. The surface of each fruit fruits 20 d after exposure, fruits were also dissected on day 20 to
was punctured 10 times by inserting a needle (Steel-made, 0.5-mm observe their inner parts.
1162 Journal of Economic Entomology, 2020, Vol. 113, No. 3

Because breaking the pericarp (shell) to open the fruits was an to demonstrate the role of the shell (pericarp) as a barrier resistance
artificial intervention, the statistical analyses were conducted and the mechanism against fruit flies. Therefore, the following two experi-
results discussed for two different scenarios: one scenario was for the ments were conducted with fruit fly species that achieved infestation
data gathered until day 20 without opening the fruits, and the other on punctured granadilla fruits.
scenario was for data gathered after opening the fruit on day 20.
Following Calzada (1982), the statistical analysis was based on a Fruit Fly Developmental Period in Two Different
completely randomized block design (CRBD) with the data square- Maturity Stages of Punctured Granadilla Fruit
root transformed for normality required by ANOVA, which was fol- The purpose of this test was to compare the development time for
lowed by Student’s t-tests and Tukey’s tests. The following variables the fruit fly species that achieved infestation on two different ma-
were analyzed: infestation percentage, number of larvae and pupae, turity stages (yellow-green and yellow) of punctured fruit with that
number of adults emerged, and percentage of adult emergence with of flies on natural hosts.
respect to larvae and pupae. To facilitate infestation, recently harvested granadilla fruits were
taken to laboratory and punctured (10 holes per fruit) as deep as
Granadilla Fruits Exposed to Female Fruit Flies 10 mm. The fruits were then placed individually in cages and ex-
Under Laboratory Conditions posed for 2 h to 5- to 10-d-old C. capitata gravid females. The rate
This research was conducted in the laboratory during the 2-yr study of 10 female fruit flies per fruit was selected to obtain approximately
period. Cages (0.5 m in diameter and 1 m in length) were used for this 100 eggs per fruit. The same procedure was performed to obtain in-
experiment in which granadilla and host fruits (Cherimoya in 2016 festation in the natural host fruit (peach).
and peach in 2017 for C. capitata, and mango for A. fraterculus), At the end of the exposure, the fruits were weighed and placed in
were placed. The three maturity stages (green, green-yellow, and maturation boxes. Then, after 0, 12, 24, 36, 48, 60, 72, 96, 120, 144,
yellow) were used (Fig. 1G), and five fruits were placed per box in 192, 240, 288, 336, 384, 480, 576, 720, 864, and 1,008 h, a group
which sexually mature male and female fruit flies were released at of fruits was dissected. The number of eggs, larvae (first, second, and
a rate of five couples per fruit. The flies remained in these boxes third instars), and pupae were counted.
(Fig. 1H) for four consecutive days with water and food. The gran- The eggs recovered from the punctured granadilla and natural
adilla fruits were harvested the day that the test began. host fruits during the evaluation were placed in hatching dishes (10-
To ensure that the fruit flies/fruit proportion did not change mm diameter, plastic Petri dishes containing absorbent wet cloth
during the experiment, the boxes were checked every morning, and and two pieces of black cardboard on which the eggs were placed).
another fly of the same species, age, and sex replaced each dead fly The dishes were kept in a clean place for 4 d. Then, the number of
encountered. emerged larvae was counted. This evaluation was used to determine
The fruit flies were released under 2 experimental fruit condi- the hatching percentage of eggs recovered from granadilla and nat-
tions: Choice (CH) and No-Choice (NCH). The treatments were in- ural host fruits. Larvae, pupae, and adults were also counted; larval
tact (CH-intact and NCH-intact) and punctured (CH-puncture and instars were identified as first, second, and/or third.
NCH-puncture) fruits. The NCH experiment used five granadilla According to Calzada (1982), statistical analyses of untrans-
fruits hung inside cages. The CH experiment used five granadilla formed data and data transformed by natural logarithm were per-
fruits and five natural host fruits hung inside a cage with a 5 cm formed to calculate the mean development times for egg, larva (first,
distance between a granadilla fruit and a host fruit. The fruit fly rate second, and third instars), and pupa stages. With oviposition the be-
was five couples per granadilla or host fruit. ginning, each developmental stage received a ‘number of days’ with a
A total of 180 cages were used. For C. capitata, 36 cages were 50% value to calculate the cumulative percentage. The weight mean
used in 2016 and again in 2017. Two experiments were conducted of the developmental time was calculated, and the developmental
in 2017 with A. fraterculus, with 36 cages used for each experiment. rate for each immature stage was estimated following a quadratic
In addition, 36 cages were used for natural host fruits (nine cages for regression. The following data were obtained for each fruit, which
each fruit fly species and experimental year). were recorded and statistically processed: 1) number of recovered
At 8:00 a.m., 10- to 20-day-old C. capitata and 18- to 20-day-old eggs, 2) number of live larvae, 3) number of pupae recovered, and
A. fraterculus sexually mature adults were released inside cages ac- 4) number of adults.
cording to treatments. The laboratory conditions were 26 ± 2°C and
65 ± 5% RH, with a 12-h photoperiod; these conditions remained Oviposition Behavior of C. capitata and
throughout the assay. A. fraterculus in Field Sleeves
The granadilla and natural host fruits were removed after 96 h of To determine the preference level for granadilla and natural host
exposure and weighed individually on a digital balance (0.001 g pre- fruits exposed to 5- to 10-d-old C. capitata and 12- to 16-d-old
cision), and the weights were recorded and each fruit was encoded. A. fraterculus gravid females, an oviposition behavior test using
Following Calzada (1982), the statistical analysis was based on sleeves was conducted under field conditions between July and
a CRBD with the data square-root transformed for ANOVA, which August 2017. Three granadilla fruit maturity stages were used
was followed by Student’s t-tests and Tukey’s tests. The following (green, green-yellow, and yellow), and the fruits were enclosed in-
variables were analyzed: infestation percentage, number of larvae side organza sleeves (1 and 0.5 m in length and width, respectively).
and pupae, number of adults emerged, and percentage of adult emer- Observations were recorded during the hours of highest activity,
gence with respect to larvae and pupae. from 9:00 a.m. to 12:00 p.m. for C. capitata and from 10:00 a.m.
to 3:00 p.m. for A. fraterculus; therefore, the 1-day evaluation cor-
Additional Experiments for Fruit Fly Species That responded to 3 and 5 h for C. capitata and A. fraterculus, respect-
Achieved Infestation on Punctured Granadilla ively. An evaluator was responsible for observing and recording the
The granadilla fruits were punctured to facilitate infestation by following behavioral parameters for one field sleeve: 1) number of
breaking through the shell of fruits. These punctured fruits helped visits to fruits; 2) oviposition attempts: ovipositor insertion without
Journal of Economic Entomology, 2020, Vol. 113, No. 3 1163

aculeus dragging; and 3) successful oviposition: ovipositor insertion any pupae that remained without adult emergence were maintained
and subsequent aculeus dragging. for an additional month.
Each sleeve enclosed five fruits and included water and food. Five All recovered adults from granadilla fruits were put into bins or
granadilla fruits and five natural host fruits were placed separately vials containing 70% alcohol. The adults were identified by properly
for each fruit fly species for the NCH test, and five granadilla fruits trained SENASA personnel from Oxapampa. The experiments in-
and five natural host fruits were placed together for each fruit fly cluded host fruits that represented the controls, and these fruits were
species for the CH test. At the beginning of the test, sexually ma- taken to laboratory and kept in the same facilities in which gran-
ture females were released at a 1:1 ratio (one fruit fly female per adilla fruits were maintained, including applying control measures to
fruit). The fruit flies remained in the sleeve during the evaluation, prevent cross-contamination by Drosophila flies. The fruit flies from
and a 5 cm distance separated a granadilla fruit and a host fruit. the colonies used in the assays, as well as the emerged flies of infested
A total of 90 sleeves were used in the entire study. For the tests fruits, were stored in small plastic containers with 70% alcohol to
involving granadilla, 36 sleeves were set up for C. capitata and 36 maintain voucher specimens, which could eventually be required to
for A. fraterculus. In addition, 18 sleeves (nine per each fruit fly spe- corroborate the fruit fly taxon (family, genera, and/or species) or to
cies) were established for the natural host fruits. provide other types of information.
For the punctured treatments within CH or NCH experiments,
each granadilla fruit was punctured on the day the test began. Ten
punctures were randomly distributed on the fruit surface and were Confidence Levels
made by inserting a needle as deep as 10 mm. According to Follet and Henneessey (2007), sample size and confi-
To determine that the natural host fruits had not been infested dence levels would be significantly higher if the number of eggs laid
previously, 10% of these fruits were placed in maturation boxes by adult flies is estimated and used in calculations. To apply this
(60 × 50 × 10 cm in length, width, and depth, respectively). When statement, we included theoretical calculations of Confidence Levels
fruit fly adults were not recovered from the fruits in these boxes, the using the formula suggested: C = 1 – (1 – pu)n; where C is the level
absence of previous infestation was confirmed. of confidence, pu is the acceptable level of survivorship and n is the
All tests used wild females. After completion of the test, all fruits number of test insects, eggs in this case.
were removed and taken to laboratory to be analyzed as previously The confidence level was calculated for each fruit fly species by
explained. using the number of female fruit flies (12,480 of C. capitata and
Statistical descriptive and inferential evaluations were performed 2,490 of A. fraterculus), which were used during the study periods
(Calzada 1982). The experiments were executed with type of fruit, and the number of eggs that such females may lay in optimal con-
field sleeve, fruit fly species, granadilla, and host fruit (peach and ditions (this is understood as if the target fruit would not have re-
mango) for the 2017 harvest season. Three response variables were sistance and as if puncturing would not have made). To do so, it
analyzed: NUMVISIT (number of visits), NUMINTOVI (number of was used the average number of eggs laid by females per day that
oviposition attempts), and OVIPOEXI (number of successful ovipos- corresponds to 25.2 for A. fraterculus (Malavasi and Zucchi, 2000)
itions). The descriptive evaluation used previously gathered data re- and 20 for C. capitata (De Graaf 2009).
garding behavioral parameter per fruit fly species.
For the inferential evaluation, three maturity types of granadilla
fruits were used for both fruit fly species: green, green-yellow, and Results
yellow. Following Calzada (1982), statistical analysis was based on Records of Meteorological Parameters in the
a CRBD with data square-root transformed for ANOVA, which was Experimental Zones During the 2016 and 2017
followed by Student’s t-tests and Tukey’s tests. Before using CRBD,
Seasons
the data were grouped by fruit fly species, experimental period,
During the 2016–2017 seasons, the mean ambient temperature in
and type of fruit maturity. The following variables were compared:
the granadilla production zones (Oxapampa, Pasco, Peru) varied
1) number of visits to fruits; 2) number of oviposition attempts;
from 17 to 20°C, the relative humidity varied from 80 to 94%, and
3) number of successful ovipositions; 4) number of recovered larvae;
the rainfall varied from 20 to 400 mm.
5) number of recovered pupae; and 6) number of emerged adults.

Recovery of Fruit Fly Adults Fruit Fly Population Densities in the Experimental
The granadilla fruits from forced infestation experiments in both Orchards and their Surroundings for the 2016 and
the field and laboratory were individually placed in 1.25-liter small 2017 Seasons Based on a Trapping System
plastic containers, with the bottom containing a sand layer as the pu- As shown in Fig. 2, fruit fly numbers fluctuated and peaks occurred
pation medium. The containers were tightly covered with a mesh lid from May to October, which is the fruiting season of many fruit
(organza cloth) to avoid the escape of fruit fly larvae, to prevent the species, providing good conditions for fruit fly reproduction. During
possible entrance of other insects such as Drosophila flies that could this period, the fly density at population peaks varied between 0.2
contaminate the sample, and to permit gas exchange. The containers and 1.6 flies per trap per day (FTD). The peaks with the highest FTD
were placed on wood/metal shelves (at various levels) in a room at values occurred when rainfall and relative humidity were relatively
26 ± 1°C and 70 ± 10% RH. low, and the lowest FTD values always coincided with the rainy
After 20 d for C. capitata and 25 d for A. fraterculus, the con- season (January through March).
tainers were inspected for larvae and pupae. All fruits were dissected The trapped fruit fly adults confirmed the natural occurrence of
to remove any larvae that had not left the fruit for pupation, and the A. fraterculus and C. capitata in Chorobamba and Huancabamba
sand was checked for pupae. When present, larvae and pupae were sectors and their corresponding subsectors. The total numbers of
counted and maintained in sand inside plastic containers (250 ml) to trapped A. fraterculus and C. capitata adults were 2,484 (1,306
recover adults. After 15 d, the plastic containers were inspected daily males and 1,178 females) and 4,418 (1,142 males and 3,276 fe-
to count and determine the sex of emerged adults. After this period, males), respectively.
1164 Journal of Economic Entomology, 2020, Vol. 113, No. 3

Fig. 2. Monthly values of flies per trap per day (FTD) for adult A. fraterculus (A) and adult C. capitata (B) captured in McPhail traps in granadilla production
sectors and subsectors in 2016 and 2017. Oxapampa, Pasco, Peru.

Infestation-Level Assessment for A. fraterculus and higher (34–71, and most values were between 50 and 62) than that
C. capitata in Natural Hosts in Perimeter and Interior of previous publications, as shown in Table 3. The high levels of MI
Portions of Experimental Orchards were explained by the high Brix values and low acidity levels for
To comply with the study protocol, the natural infestation of host fruits with the surface mostly yellow.
fruit was required to demonstrate the natural occurrence of fruit The fruits were harvested with quantitative attributes also de-
flies. These data for potential host fruits are shown in Table 1. termined, such as the weight (121.21 ± 0.31 gr.) and maturity index
A total of 8,490 fruits representing the fruits of 30 species were (56.01 ± 0.8%), with levels/values for both parameters. In spite of
collected by SENASA fruit fly inspectors, which were evaluated in the commercial attributes found for granadilla fruits, fruit fly imma-
the SENASA laboratory in Oxapampa (Pasco). One thousand three ture stages (eggs, larvae, or pupae) were not found.
hundred nine granadilla fruits were collected that could not be used
commercially because the fruits were damaged and showed cracking Choice and No-choice Foraging Behaviors Using
and/or sunburn. These fruits were picked either from a plant or from Sleeves Under Field Conditions
the ground (fallen). Although these noncommercial granadilla fruits First Evaluation: The Granadilla Epicarp Remained Unbroken
were vulnerable because of injuries, naturally occurring fruit flies (Intact) Until Day 20
did not infest them. By contrast, under the same natural soil and In all field sleeve tests involving intact fruit, both A. fraterculus and
environmental conditions, host fruits generated fruit fly adults. In C. capitata were unable to oviposit in the fruits through the epicarp,
addition, Anastrepha spp. and C. capitata infested 16 natural host based on testing of all fruit maturity stages (green, green-yellow, and
fruit species in the granadilla production areas. yellow). The infestations in host fruit species (control) confirmed
that the female fruit flies used in the experiments were gravid and in
Granadilla Fruit Sampling at the Experimental an optimal condition for effective oviposition behavior. The resist-
Orchards ance of the epicarp is fully discussed in the corresponding section of
A total of 1,940 commercial granadilla fruits were collected, 450 this article (Fig. 3).
fruits in 2016 and 1,490 fruits in 2017. To determine the MI, 190 Vargas et al. (2000) notes that C. capitata eggs hatch within
fruits were evaluated. Based on the dissection of 970 fruits (50% of 2–4 d and that larvae feed for another 6–11 d (at 13–35°C); there-
the total) on the day of sampling and the other 970 fruits after 20 d fore, third instar larvae take 6.3–10.2 d to leave the fruits. Similarly,
in suitable containers, fruit fly eggs, larvae, or pupae were not found. Malavasi and Zucchi (2000) determined that A. fraterculus eggs
These results demonstrated that naturally occurring fruit flies could hatch in 2.3–10.3 d at 15–30°C, and the larvae development take
not infest the granadilla fruits and are shown in Table 2. 11–34.5 d at 15–30°C; therefore, third instar larvae take 13.6–17.2
According to the ICONTEC (1997), the MI should vary between d to leave the fruits. The statistical comparisons between the treat-
19.9 and 35.4. The range of MI values for Peruvian granadilla was ments are shown in Tables 3 and 4.
Journal of Economic Entomology, 2020, Vol. 113, No. 3 1165

Table 1. Infestation ratios for Anastrepha spp. and C. capitata in natural host fruits from granadilla production areas in Chorobamba and
Huancabamba sectors in 2016 and 2017; Oxapampa, Pasco, Peru

Weight

Scientific name Common name Botanical family (Sum kg ± SEM) Fruit fly Species No of emerged individual

Annona cherimola Mill. Cherimoya Annonaceae 1.29 ± 0.11

Capsicum frutescens L. Pepper Solanaceae 2.59 ± 0.01
Capsicum pubescens Ruiz & Pav Rocoto pepper Solanaceae 5.28 ± 0.01
Capsicum sp. Paprika pepper Solanaceae 0.02 ± 0.00
Carica papaya L. Papaya Caricaceae 7.87 ± 0.09
Citrus aurantium L. Bitter orange Rutaceae 2.87 ± 0.04
Citrus jambhiri Lush. Rough lemon Rutaceae 12.15 ± 0.02 A. fraterculus 83
C. capitata 10
Citrus limetta Risso Sweet lemon Rutaceae 1.46 ± 0.02 A. fraterculus 8
Citrus limettioides Tanaka Sweet lime Rutaceae 10.22 ± 0.02 A. fraterculus 89
Citrus limonia Risso Rangpur Rutaceae 58.4 ± 0.02 A. fraterculus 151
C. capitata 51
Citrus reticulata Blanco Mandarin orange Rutaceae 1.51 ± 0.01 A. fraterculus 66
Citrus sinensis (L.) Osbeck Orange Rutaceae 34.92 ± 0.02 A. fraterculus 276
C. capitata 54
Citrus X paradisi Macfad Grapefruit Rutaceae 3.59 ± 0.02 A. fraterculus 4
Citrus X tangelo J. W. Ingram & H. E. Moore Tangelo Rutaceae 0.70 ± 0.06 A. fraterculus 9
Coffea arabica L. Coffee Rubiaceae 12.39 ± 0.02 C. capitata 616
Cucurbita máxima Duchesne ex Lam. Squash Cucurbitaceae 10.49 ± 0.29 A. grandis 41
Cucurbita pepo L. Pumpkin Cucurbitaceae 2.80 ± 0.12
Cyclantera pedata (L.) Shrader Stuffing cucumber Cucurbitaceae 17.16 ± 0.01
Eriobotrya japónica (Thunb.) Lindl. Loquat Rosaceae 1.05 ± 0.02 A. fraterculus 13
Eugenia uniflora L. Surinam cherry Myrtaceae 1.92 ± 0.01 A. fraterculus 60
Inga sp. Inga Fabaceae 13.30 ± 0.01 A. distincta 68
Juglans regia L. Walnut Juglandaceae 10.91 ± 0.02 A. schultzi 298
Lucuma obovata Lucuma Sapotaceae 1.50 ± 0.02
Passiflora ligularis Juss. Sweet granadilla Passifloraceae 115.64 ± 0.01
Persea americana Mill. Avocado Lauraceae 7.02 ± 0.05
Physalis peruviana L. Goldenberry Solanaceae 1.18 ± 0.00
Prunus pérsica (L.) Batsch Peach Rosaceae 5.02 ± 0.01 C. capitata 503
Psidium guajaba L. Guava Myrtaceae 46.96 ± 0.00 A. fraterculus 63
A. ornata 206
A. striata 1,415
Solanum betaceum Cav. Tamarillo Solanaceae 1.86 ± 0.03
Solanum quitoense Lam Naranjillo Solanaceae 1.34 ± 0.07

Based on this information, without opening the fruit or breaking exposed to 1,500 gravid females. After 20 d, granadilla fruits were
the epicarp, during the 20 d after intact and punctured granadilla dissected, and no infestation of intact granadilla fruits was observed.
were exposed to fruit flies, no larvae emerged from and no pupae For C. capitata, three trials were conducted between 2016 and 2017,
were found outside these fruits. By contrast, larvae and pupae were and 150 green, 150 green-yellow, and 150 yellow granadilla fruit
found outside host fruits in high numbers. The host fruits started were exposed to 2,250 gravid females. Fruit fly infestation was not
to decompose much earlier than the granadilla fruits because of the observed in any maturity stage.
high infestation and therefore were opened 10 d after exposure. The natural host fruits used as controls were successfully infested.
Mango was used for A. fraterculus. In the choice test, 150 fruits were
Second Evaluation: The Granadilla Epicarp was Broken on exposed, and 81 (54%) were infested, from which 888 adults emerged
Day 20 (76% emergence) from 1,098 larvae and pupae. In the no-choice test,
Results From Intact Granadilla Fruits. of the 150 fruits exposed, 79 (52%) fruits were infested, from which
In all field sleeve tests involving intact fruit, both A. fraterculus and 555 adults emerged (79% emergence) from 699 larvae and pupae.
C. capitata were unable to oviposit through the epicarp of all fruit Peach was the host fruit exposed to C. capitata. In the choice test, 225
maturity stages (green, green-yellow, and yellow). The infestation in fruits were exposed, and 165 (73%) were infested, from which 4,098
host fruit species (control) confirmed that the female fruit flies were adults emerged (62%) from 6,599 larvae and pupae. In the no-choice
gravid and in optimal condition for effective oviposition behavior. test, 158 (70%) fruits were exposed and infested, from which 4,883
To determine whether fruit flies completed the cycle inside of fruits, (62%) adults emerged from 7,934 larvae and pupae.
granadilla fruits were opened 20 d after exposure to female fruit
flies, and no larvae and pupae were found inside or outside intact Results From Punctured Granadilla Fruits.
granadilla fruits. In punctured fruits, the results were different when the granadilla
In 2017, two trials were conducted for A. fraterculus. A total fruits were opened 20 d after exposure to fruit fly females. Some
of 300 intact granadilla fruits (100 fruits per maturity stage) were larvae and pupae were found inside the punctured granadilla.
1166 Journal of Economic Entomology, 2020, Vol. 113, No. 3

Anastrepha fraterculus did not infest the 100 green fruits that

No. of fruit fly immature stages

were exposed. For the green-yellow fruits, five fruits were infested
of the 100 (5% infestation) that were exposed, with 32 larvae and
pupae recovered from which 12 adults emerged (38% emergence).
For the yellow fruits, 34 fruits were infested of the 100 (34% infest-

0
0

0
0
0
ation) that were exposed, with 309 larvae and pupae recovered from
which 89 adults emerged (29% emergence). The performance of
C. capitata was different. This fruit fly species was able to oviposit in
the punctures of 52 green fruits of the 150 exposed (35%), with 527
larvae and pupae recovered from which 76 adults emerged (14%
emergence). For the green-yellow fruits, 114 fruits were infested
of the 150 exposed (75%), with 1,762 larvae and pupae recovered
from which 274 adults emerged (16% emergence). For the yellow
43.47 ± 3.31
52.00 ± 1.57

59.38 ± 1.15
57.20 ± 1.05
56.01 ± 0.8
fruits, 100 fruits were infested of the 150 exposed (67%), with 1,456
MI

larvae and pupae recovered from which 342 adults emerged (81%
emergence). See Table 5.
A greater proportion of natural host fruits were infested than
that of granadilla. For A. fraterculus in the choice test, 73 mango
Fruit maturity evaluation (X ± SEM)

fruits were infested of the 150 (49% infestation), with 907 larvae
and pupae recovered from which 673 adults emerged (74% emer-
0.34 ± 0.04
0.26 ± 0.01

0.25 ± 0.00
0.28 ± 0.01
0.27 ± 0.01
% Acidity

gence). For C. capitata, 138 peach fruits were infested of the 225
fruits exposed (61% infestation), with 3,256 larvae and pupae re-
covered from which 2,500 adults emerged (77% emergence).

Granadilla Fruits Artificially Exposed to Female Fruit

Table 2. Granadilla fruits sampled from the production in Chorobamba and Huancabamba sectors in 2016 and 2017

Flies Under Laboratory Cage Conditions

12.35 ± 0.46
13.35 ± 0.26

14.67 ± 0.19
15.34 ± 0.16
14.57 ± 0.13

This experiment was also conducted using the two evaluations, the
% TSS

first one simulated natural conditions before cutting the fruit after
20 d of having been exposed to fruit flies, verifying the presence of
larvae and pupae outside fruits and/or in the sand. The second one
was performed after cutting such fruits after 20 d of having been
exposed to fruit flies, verifying the presence of larvae and pupae in-
20
20

70
80
190

side fruits.
N

First Evaluation: Granadilla Epicarp Remained Unbroken Until

Day 20
Weight (g) (X±SEM)

Based on the life cycle information provided by Vargas et al.

116.65 ± 1.00
114.52 ± 0.89

123.79 ± 0.50
122.07 ± 0.46
121.21 ± 0.31

(2000) and Malavasi and Zucchi (2000) for both C. capitata and
A. fraterculus, fruits were not opened for 20 d after intact and punc-
tured granadilla were exposed to fruit flies. No larvae emerged and
Oxapampa, Pasco, Peru. TSS = total soluble solids and MI = maturity index.

no pupae were found outside the fruits, which was in contrast to

high-intensity infestation in host fruits.
In all laboratory cage tests involving intact fruit, both
A. fraterculus and C. capitata were unable to oviposit in these
fruits through the epicarp, at any of the fruit maturity stages (green,
No. of fruits collected

green-yellow, and yellow) that were subjected to forced infestation

in experimental cages in the laboratory. The infestation in host fruit
species (control) confirmed that the female fruit flies used in these
1,940
250
200

700
790

experiments were gravid and in optimal condition for effective ovi-

position behavior.

Second Evaluation for Intact Granadilla Epicarp was Broken on

Day 20 (Cage-Lab)
Two trials were conducted in 2017, and a total of 900 gravid females
Huancabamba Sector

Huancabamba Sector

of A. fraterculus were exposed to 90 intact granadilla fruits (30 fruits

Chorobamba Sector

Chorobamba Sector
Sampling during 2016

Sampling during 2017

per maturity stage). After the dissection of fruits, no infestation of in-

tact granadilla fruits was observed in any maturity stage. Two trials
were conducted for C. capitata between 2016 and 2017. A total of
Sample year

900 gravid females were exposed to 60 green, 60 green-yellow, and

TOTAL:

60 yellow granadilla fruits, and infestation was not observed at any

maturity stage.
Journal of Economic Entomology, 2020, Vol. 113, No. 3 1167

Table 3. Results from ANOVA (DF-treatment, DF-Replicate, F-value, P-value) and Tukey’s comparison of means for C. capitata larvae and
pupae observed outside fruits (granadilla and host) 20 d after exposure to fruit flies without opening granadilla fruits

A) C. capitata in Chorobamba sector-2016

Variable Yellow Green-Yellow Green

DF-Treatment 6 6 6
DF-Replicate 4 4 4
F-value 8.61 7.52 6.71
P-value 0 0 0

Treatments Mean Group Mean Group Mean Group

NCh-host 1.6833 A 1.17 AB 1.529 A

Ch-pun-host 1.4367 AB 1.144 AB 0.669 AB
Ch-intac-host 2.5046 A 2.073 A 1.223 A
NCh-pun-gran 0 B 0 B 0 B
Ch-pun-gran 0 B 0 B 0 B
NCh-intac-gran 0 B 0 B 0 B
Ch-intac-gran 0 B 0 B 0 B

B) C. capitata in Chorobamba sector-2017

Variable Yellow Green-Yellow Green

DF-Treatment 6 6 6
DF-Replicate 4 4 4
F-value 184.99 106.21 68.83
P-value 0 0 0

Treatments Mean Group Mean Group Mean Group

NCh-host 7.0127 A 4.642 A 6.517 A

Ch-pun-host 4.39262 B 2.327 B 4.019 B
Ch-intac-host 6.85385 A 4.74 A 4.556 B
NCh-pun-gran 0 C 0 C 0 C
Ch-pun-gran 0 C 0 C 0 C
NCh-intac-gran 0 C 0 C 0 C
Ch-intac-gran 0 C 0 C 0 C

C) C. capitata in Huacabamba sector-2017

Variable Yellow Green-Yellow Green

DF-Treatment 6 6 6
DF-Replicate 4 4 4
F-value 149.78 50.78 17.53
P-value 0 0 0

Treatments Mean Group Mean Group Mean Group

NCh-host 5.18333 B 4.564 A 3.711 A

Ch-pun-host 4.76478 B 3.062 B 2.966 A
Ch-intac-host 6.95943 A 4.429 A 2.812 A
NCh-pun-gran 0 C 0 C 0 B
Ch-pun-gran 0 C 0 C 0 B
NCh-intac-gran 0 C 0 C 0 B
Ch-intac-gran 0 C 0 C 0 B

Results correspond with the field sleeve test with three maturity stages of granadilla in Oxapampa, Pasco, Peru. DF = degrees of freedom. Names of treatments are
as follows: Ch-intac-gran = Choice-intact granadilla; Ch-intac-host = Choice-intact host; Ch-pun-gran = Choice-punctured granadilla; Ch-pun-host = Choice-punctured
host; NCh-host = No-Choice host; NCh-intac-gran = No-Choice intact granadilla; and NCh-pun-gran = No-Choice punctured granadilla. Oxapampa, Pasco, Peru, 2017.

By contrast, the natural host fruits used as a control were success- 8,181 larvae and pupae from which 5,997 adults emerged. In the
fully infested. Mango was used as the natural host for A. fraterculus. no-choice test, 30 fruits were exposed and infested, and 3,902 larvae
In the choice test, 90 fruits were exposed, and 57 were infested, and pupae were recovered from which 2,453 adults emerged.
with the recovery of 1,098 larvae and pupae from which 888 adults
emerged. In the no-choice test, 30 fruits were exposed, and 27 were Second Evaluation for Punctured Granadilla Epicarp was
infested, with the recovery of 581 larvae and pupae from which 428 Broken on Day 20 (Cage-Lab)
adults emerged. Anastrepha fraterculus infested 10 (17%) green fruits of the 60
The host fruits exposed to C. capitata were cherimoya in the exposed, and 64 larvae and pupae were recovered from which 12
2016 trial and peach in the 2017 trial. In the choice experiment, adults emerged. For green-yellow fruits, 11 (18%) were infested of
90 fruits were exposed, and 87 were infested, with the recovery of the 60 exposed, with the recovery of 658 larvae and pupae from
1168 Journal of Economic Entomology, 2020, Vol. 113, No. 3

Fig. 3. Average number of larvae and pupae of C. capitata (A) and A. fraterculus (B) recovered after 20 d without opening granadilla fruits from sleeve field tests
in 2016 and 2017. Treatments are as follows: Intac-gran = Intact granadilla; Intac-host = Intact host; Pun-gran = Punctured granadilla; Pun-host = Punctured host;
Host = only host. Oxapampa, Pasco, Peru.

which 20 adults emerged. For yellow fruits, 28 (47%) were infested For C. capitata, 26 (43%) of 60 green fruits were infested, with
of the 60 exposed, and 360 larvae and pupae were recovered from the recovery of 153 larvae and pupae from which 21 adults emerged.
which 143 adults emerged. In the green-yellow maturity category, 39 fruits (65%) of the 60
Journal of Economic Entomology, 2020, Vol. 113, No. 3 1169

Table 4. Results from ANOVA (DF- degrees of freedom for treatments, DF-degrees of freedom for replicates, F-value, P-value) and Tukey’s
comparison of means for A. fraterculus larvae and pupae observed outside fruits (granadilla and host) 20 d after exposure to fruit flies
without opening granadilla fruits

A) A. fraterculus in Huancabamba sector-2017-1

Variable Yellow Green-Yellow Green

DF-Treatment 6 6 6
DF-Replicate 4 4 4
F-value 15.63 16.85 12.96
P-value 0.000 0.000 0.000

Treatments Mean Group Mean Group Mean Group

NCh-host 1.89942 A 1.811 A 1.349 A

Ch-pun-host 1.83213 A 1.333 A 2.271 A
Ch-intac-host 1.61808 A 1.056 A 1.789 A
NCh-pun-gran 0 B 0 B 0 B
Ch-pun-gran 0 B 0 B 0 B
NCh-intac-gran 0 B 0 B 0 B
Ch-intac-gran 0 B 0 B 0 B

B) A. fraterculus in Huancabamba sector-2017-2

Variable Yellow Green-Yellow Green

DF-Treatment 6 6 6
DF-Replicate 4 4 4
F-value 15.06 8.77 13.57
P-value 0.000 0.000 0.000

Treatments Mean Group Mean Group Mean Group

NCh-host 1.27365 A 1.247 A 1.421 A

Ch-pun-host 1.10776 A 0.944 A 1.507 A
Ch-intac-host 1.80393 A 0.951 A 1.482 A
NCh-pun-gran 0 B 0 B 0 B
Ch-pun-gran 0 B 0 B 0 B
NCh-intac-gran 0 B 0 B 0 B
Ch-intac-gran 0 B 0 B 0 B

Results correspond with the field sleeve test with three maturity stages of granadilla in Oxapampa, Pasco, Peru. DF = degrees of freedom. Names of treatments
are as follows: Ch-intac-gran = Choice-intact granadilla; Ch-intac-host = Choice-intact host; Ch-pun-gran = Choice-punctured granadilla; Ch-pun-host = Choice-
punctured host; NCh-host = No-Choice host; NCh-intac-gran = No-Choice intact granadilla; and NCh-pun-gran = No-Choice punctured granadilla. Oxapampa,
Pasco, Peru, 2017.

fruits exposed were infested, with the recovery of 1,093 larvae and For third-instar larvae, 50% entered this larval instar after 20 d,
pupae from which 149 adults emerged. In the yellow maturity cat- which was a couple of days later than the third instars in the host
egory, 54 (90%) of the 60 fruits exposed were infested, with the fruit. In addition, this larval instar was observed for over 36 d. The
recovery of 1,650 larvae and pupae from which 146 adults emerged. development of pupae inside green-yellow granadilla was longer
The natural host fruits used for choice tests involving A. fraterculus than that in the host fruit, with 50% of pupae appearing after 36 d,
were infested at a greater proportion than that of granadilla fruits. which was 15 d later than the appearance in the host. In addition,
A total of 69 (77%) of the 90 mango fruits were infested, with the re- pupae were recovered for over 42 d. Adult emergence was not ob-
covery of 1,459 larvae and pupae from which 1,186 adults emerged served from yellow and green-yellow granadilla fruits, in contrast to
(81% emergence). For the host fruit of C. capitata, of the 90 fruits host fruits, which showed adult emergence.
exposed, 89 (99%) were infested, and 6,317 larvae and pupae were The resistance of granadilla fruit against the fruit fly C. capitata
recovered, from which 4,523 adults emerged (72% emergence). was demonstrated again, because adults did not emerge from punc-
tured granadilla fruits that were infested, at either green-yellow or
Fruit Fly Developmental Period Test in Two Stages of yellow maturity levels. As previously observed, the ready-to-pupate
Granadilla Fruit Maturity larvae could not leave the fruits and were forced to pupate inside.
The results obtained for green-yellow (Fig. 4A) and yellow (Fig. 4B) These pupae eventually died inside.
granadilla fruits were similar. Fifty percent of the eggs remained until The development times for the eggs, larvae, and pupae of
1.5 d after being placed on the granadilla fruit, which was a result C. capitata were similar between green-yellow and yellow granadilla
similar to that of the host fruit. For the first-instar larvae, 50% ap- fruits. However, compared with the host fruit (peach), eggs, larvae,
peared after 5 d, which was 1 d later than the appearance in the host and pupae needed longer to develop in granadilla fruits. Based on the
fruit. For the second larval instar, 50% appeared after 12 d, which increase in development time of larval instars I, II, and III and the
was 2 d later than the appearance in the host fruit (Fig. 4C). In add- absence of recovered adults, punctured granadilla was not a good
ition, this larval stage was observed over 24 d. host for this fruit fly species.
1170 Journal of Economic Entomology, 2020, Vol. 113, No. 3

Table 5. Number of fruits infested, adults emerged per fruit, and number of larvae and pupae recovered when granadilla fruits were dis-
sected 20 d after exposure to fruit fly females of A. fraterculus and C. capitata in field sleeve tests in 2016 and 2017; Oxapampa, Pasco, Peru

A. fraterculus C. capitata

No. of fruits in- Larvae and pupae Adults emerged (mean ± No. of fruits in- Larvae and pupae Adults emerged
Treatments fested (mean ± SEM) SEM) fested (mean ± SEM) (mean ± SEM)

Yellow
Ch-intac-gran 0 0 0 0 0 0
Ch-intac-host 31 8.35 ± 1.08 6.32 ± 0.83 63 48.32 ± 4.4 24.59 ± 2.46
Ch-pun-gran 23 7.00 ± 0.95 5.13 ± 0.99 53 13.25 ± 3.20 12.19 ± 3.22
Ch-pun-host 24 12.04 ± 4.00 10.71 ± 3.88 53 25.92 ± 2.16 19.92 ± 1.67
NCh-host 27 9.48 ± 1.16 8.50 ± 1.15 55 58.85 ± 5.77 27.53 ± 2.73
NCh-intac-gran 0 0 0 0 0 0
NCh-pun-gran 11 13.45 ± 5.23 9.60 ± 4.81 47 16.04 ± 2.54 6.39 ± 1.02
Green-Yellow
Ch-intac-gran 0 0 0 0 0 0
Ch-intac-host 23 5.26 ± 0.66 4.00 ± 0.5 59 28.12 ± 2.88 22.12 ± 2.74
Ch-pun-gran 0 0 0 65 15.98 ± 1.79 5.85 ± 1.01
Ch-pun-host 22 8.23 ± 1.90 5.19 ± 0.62 41 14.66 ± 1.68 12.85 ± 1.43
NCh-host 26 9.23 ± 0.92 8.25 ± 0.85 52 30.54 ± 3.45 24.69 ± 3.05
NCh-intac-gran 0 0 0 0 0 0
NCh-pun-gran 5 6.40 ± 3.11 4.00 ± 1.18 49 14.76 ± 2.29 3.68 ± 0.69
Green
Ch-intac-gran 0 0 0 0 0 0
Ch-intac-host 27 10.63 ± 1.67 8.54 ± 1.45 43 44.09 ± 5.77 30.14 ± 3.61
Ch-pun-gran 0 0 0 33 13.42 ± 2.89 6.17 ± 1.69
Ch-pun-host 27 16.19 ± 4.99 13.04 ± 4.93 44 29.11 ± 3.34 23.10 ± 2.40
NCh-host 26 7.81 ± 0.93 6.12 ± 0.82 51 60.96 ± 6.43 40.88 ± 5.00
NCh-intac-gran 0 0 0 0 0 0
NCh-pun-gran 0 0 0 19 4.42 ± 0.86 1.00 ± 0.00

Names of treatments are as follows: NCh-host: No-Choice host; Ch-pun-host: Choice-punctured host; Ch-intac-host: Choice-intact host; NCh-pun-gran:
No-Choice punctured granadilla; Ch-pun-gran: Choice-punctured granadilla; NCh-intac-gran: No-Choice intact granadilla; and Ch-intac-gran: Choice-intact
granadilla. Maturity stages: Yellow = fully ripened; Green-Yellow = in the process of ripening; Green = unripe but ready to start color change.

According to Fig. 4A, when the development in yellow gran- than that in the host fruit, with 50% of the larvae appearing after
adilla fruit and the host fruit (peach) was compared, the egg period day 5, which was 1 d later than the appearance in the host fruit. In
in yellow granadilla fruits was similar to that in the host, with 50% addition, instar I larvae were observed until day 14. The develop-
of the eggs remaining until 1.5 d after being placed on the fruits. ment of larvae II in green-yellow granadilla was also longer than
For larval instar I, the development in yellow granadilla fruits was that in the host fruit, with 50% of the larvae appearing after day 10,
longer than that in the host fruit, with 50% of the larvae appearing which was 2 d later than the appearance in the host fruit. In add-
after day 5, which was 1 d later than the appearance in host fruit. In ition, instar II larvae were observed until day 24. The development
addition, the larvae at stage I were observed until day 12. For larval of larvae III in green-yellow granadilla fruits continued to be longer
instar II, the development in yellow granadilla fruits was also longer than that in the host fruit, with 50% of the larvae appearing after
than that in the host fruit, with 50% of the larvae appearing after day 14, which was 2 d later than the appearance in the host fruit.
day 12, which was 6 d later than the appearance in host fruit. In In addition, instar III larvae were observed until day 36. The devel-
addition, the larvae at stage II were observed until day 16. For larval opment of pupae in green-yellow granadilla fruits was longer than
instar III, the development in yellow granadilla fruits continued to be that in the host fruit, with 50% of the pupae appearing after day
longer than that in the host fruit, with 50% of the larvae appearing 35, which was 15 d later than the appearance in the host fruit. In
after day 20, which was 10 d later than the appearance in host fruit. addition, pupae were observed up to day 42. For the green-yellow
In addition, the larvae at stage III were observed until day 30. For granadilla fruits, no adult emergence was observed, because the
pupae, the development in yellow granadilla fruits was longer than hardness of the pericarp did not allow larvae to leave for pupation.
that in the host fruit, with 50% of the pupae appearing after day
35, which was 20 d later than the appearance in the host fruit. In
addition, pupae were observed up to day 42. For adults, no emer- Oviposition Behavior of C. capitata and
gence was observed from granadilla fruits, because the hardness of A. fraterculus Under Field Conditions Using Sleeves
the pericarp prevented larvae from leaving for pupation. Results corresponding to A. fraterculus can be found in Fig. 5A
According to Fig. 4B, when the development in green-yellow (Choice) and 5B (No-Choice), and for C. capitata in Fig. 5C (Choice)
granadilla fruit and the host fruit (peach) was compared, the egg and 5D (No-Choice). In all cases, intact and punctured green, green-
period in the green-yellow granadilla fruits was similar to that of yellow, and yellow granadilla fruits are included.
the yellow granadilla and to that of the host fruit, with 50% of the Anastrepha fraterculus females could not lay eggs in intact or punc-
eggs remaining until 1.5 d after being placed on the fruits. The de- tured green, green-yellow, and yellow granadilla fruits, in both choice
velopment of larvae I in green-yellow granadilla fruits was longer and no-choice tests. Although C. capitata could not lay eggs in intact
Journal of Economic Entomology, 2020, Vol. 113, No. 3 1171

general, rainfall can affect insect populations when drops of water

make direct contact with insects and create good conditions for the
progress of entomopathogens; however, some insects have evolved
strategies to survive rainfall, including initiating activities following
rainfall during the day, which is observed in the diurnal behavior
of fruit flies. Variation was observed in the weather, particularly in
rainfall, and the variation was a good indicator of the experimental
replicate years 2016 and 2017. These differences in meteorological
conditions between years helped to explain the overall results.
It is worth mentioning that C. capitata had a higher usage of
punctured fruits since it laid eggs in 53.7% of such punctured fruits,
comparing to A. fraterculus that laid eggs in just 15.4% of those
punctured fruits. In contrast, usage of intact fruit was similar be-
tween these two fruit fly species since none of them could lay eggs on
the hard skin of granadilla fruits.
Based on the trapping system and the fluctuations in fruit fly
populations, the high capture of fruit fly males in McPhail traps
was most likely explained by the feeding lure Torula and the phero-
mone produced by captured females before being trapped. The total
number of trapped, naturally occurring C. capitata adults was almost
double the total number of A. fraterculus adults in the Oxapampa
experimental area. Moreover, the male:female ratios were 1:0.9 and
1:2.8 for A. fraterculus and C. capitata, respectively. The predomin-
ance of the naturally occurring Mediterranean fruit fly C. capitata
may be of value for the aims of the study because of the high import-
ance for quarantine.
The availability of host fruit was an important factor affecting
fruit fly population fluctuations throughout the experimental
periods. Similar to the months of the year when harvestable or com-
mercial host fruit is available, most of the host fruit species had fruit
available from May to October, when the fruit fly (A. fraterculus and
C. capitata) populations peaked (from trapping system) during both
2016 and 2017 seasons. The highest FTD values were in 2016 for
C. capitata (above 1.6), and this level could have been related to an
increase in the number of host fruits available because of the rain-
fall amounts during January–March 2016, which were the highest
during the entire experimental period from 2016 to 2017.
For clarity, the sleeve and cage experiments were interpreted
using the two evaluations. In the first evaluation, intact and punc-
tured granadilla fruits were not opened for 20 d after exposure to
fruits flies. Larvae and pupae were not found outside either intact
or punctured granadilla, whereas many larvae and pupae were re-
Fig. 4. Development period of C. capitata immature stages in yellow (A) and
corded outside other host fruits. The punctured fruits had larvae
green-yellow (B) granadilla fruits, as well as in host fruit (C) in 2017. The arrows
indicate the accumulated probability for each fruit fly instar (first-, second-, and and pupae inside, because the third-instar larvae could not leave the
third-instar larvae) and stage (egg, larva, and pupa). Oxapampa, Pasco, Peru. fruits for pupation as they did on host fruit. However, the second
evaluation also suggests that when the epicarp is broken, artificial
infestation can occur. Notably, fruits with a broken epicarp do not
granadilla fruits, eggs were successfully laid in a few punctured green- have commercial value and therefore are not exported, preventing
yellow (Choice and No Choice) and yellow granadillas; however, the potential passive dispersion of fruit flies. After 20 d, larvae and
emerging larvae were not observed. By contrast, oviposition was suc- pupae were not found inside or outside intact granadilla fruits, but
cessful in host fruits (control) and resulted in larvae, pupae, and adults. some larvae and pupae were found remaining inside punctured
These results confirmed that the hardness of the epicarp is a resistance granadilla fruits. Thus, both evaluations demonstrated the epicarp
mechanism against fruit flies in intact granadilla fruits, regardless of the of granadilla fruit is an effective barrier in preventing fruit fly infest-
maturity stage. Corresponding ANOVA is shown in Table 6. ation and movement.
The larvae that developed from artificial oviposition performed
by female fruit flies through the needle holes could not leave punc-
Discussion tured granadilla fruits, and therefore, unusual pupation occurred in-
The ranges of temperature and relative humidity recorded in the side those fruits. This internal pupation occurred only in some of the
experimental zones during 2016 and 2017 were optimal for the punctured granadilla fruits that were exposed to fruit fly females.
granadilla crop and for fruit fly development. The discussion on The intact granadilla fruits remained completely free from fruit fly
rainfall (mm) is focused on the rainfall that occurred in December– eggs and, therefore, also from larvae and pupae. This result suggests
March and the ‘dry’ season that occurred in April–November. The that the pericarp is a resistance mechanism, which is discussed in
‘dry’ season was when rainfall occurred but at reduced volumes. In more detail as follows.
1172 Journal of Economic Entomology, 2020, Vol. 113, No. 3

Fig. 5. Average visits, oviposition attempts, and successful ovipositions of A. fraterculus (A and B) and C. capitata (C and D) females for three maturity stages of
granadilla fruits (green, green-yellow, and yellow) under Choice (A and C) and No-Choice (B and D) conditions involving intact and punctured granadilla fruits
and natural host fruits.

Liquido et al. (1990) report 1.84 C. capitata flies/kilo of sampled Moreover, in addition to the difficulty caused by the paper-like
granadilla fruits in Hawaii; however, said authors do not mention and dry texture and the absence of free water in these layers, the
the fruit condition nor the maturity degree. In addition, according to hardness, explained by the very low water content and the high level
their methodology, fruits were collected from trees and those fallen of fiber and pectin, might also hinder the movement of hatched larvae
on the ground. In contrast, we did not report C. capitata infestation (first instar). The paper-like and dry texture should be considered an-
from the granadilla fruits collected from trees and from those fallen other type of mechanical resistance against first and second instar
on the ground. larvae and most likely caused abrasions to the relatively thin cuticle
When fruits were punctured, juice emerged from some of the of the larvae. Some of these larvae were found dead within mesocarp
punctures and may explain why some eggs deposited in the needles and endocarp layers.
holes hatched and some larvae developed and pupated inside fruits. Anastrepha fraterculus used the punctures to lay eggs but only in
The juice from the puncture would have provided moisture for the green-yellow and yellow fruits, indicating that green fruits were not
eggs and first instar larvae. The punctures without juice would have preferred even with holes available. The holes alone did not guar-
resulted in dry conditions for eggs and therefore affected their incu- antee a completely successful A. fraterculus infestation because of
bation period. The eggs surrounded by dry tissue of the mesocarp the low percentage of larvae turning into pupae and pupae turning
may have died or the incubation period may have been extended. If into adults. Because fruit flies are not usually attracted to green
extended, the larvae that hatched may have been weakened or with fruits, this non-preference for green fruits would not be considered
poor growth, which may have complemented the subsequent and as a form of resistance; however, the slowed development in green-
direct mechanical resistance on larvae and pupae. The slower egg yellow and yellow fruits may involve the resistance mechanisms pre-
development in granadilla than that in host fruit could be explained viously addressed.
by the stress of a dry environment for eggs. Similarly, in the experiment examining the development of
The failure of larvae to leave and the forced pupation inside punc- C. capitata, the development time for eggs, larvae, and pupae was
tured granadilla fruits indicated the barrier also worked from the in- longer in granadilla fruit than that in host fruit. Although the MI
side. The ready-to-pupate third-instar larvae were not been able to of granadilla fruits was relatively high, the MI depends solely upon
perforate the endocarp, which is a paper-like, thick, hard, and dry Brix degree and acidity; therefore, other factors may have also been
tissue that the mouthparts of larvae cannot break, and were forced important. Generally, development time in insects is expanded when
to pupate inside the fruits. Thus, when pupae were found in the pulp, conditions in a given fruit are not optimal, which can include certain
the conclusion was that larvae could not perforate the endocarp. chemical compounds that may affect the regular development. To
However, other pupae were found within the mesocarp and complete the larval stage, the larvae must have eaten the arils of the
endocarp, which indicated that the related larvae could perforate the pulp, which may have slowed development compared with that in
endocarp but never the mesocarp and the epicarp. The inability to the host fruit. In addition, because pupae are directly formed from
break through was likely related to the absence of free water in these larvae, they also showed slower development. Therefore, pupal de-
layers, which increased the difficulties for larval movements. velopment time depended not only on the pupal environment but
Table 6. ANOVA (df = degrees of freedom) and Tukey’s comparison of means for oviposition behavior of A. fraterculus and C. capitata involving fruits of granadilla at different stages of maturity
(yellow, green-yellow, and green); Oxapampa, Pasco, Perú

Anastrepha fraterculus

Yellow Green-Yellow Green

Variable NUMVISIT NUMINTOVI OVIPOEXI NUMVISIT NUMINTOVI OVIPOEXI NUMVISIT NUMINTOVI OVIPOEXI

Gl-Treatment 6 6 6 6 6 6 6 6 6
Gl-Replicate 2 2 2 2 2 2 2 2 2
F-value 2.460 0.540 0.820 2.500 2.050 0.850 0.730 1.320 1.890
P-value 0.029 0.773 0.554 0.027 0.066 0.534 0.672 0.256 0.090

Treatments Mean Group Mean Group Mean Group Mean Group Mean Group Mean Group Mean Group Mean Group Mean Group

NCh-host 1.279 A 0.067 A 0.067 A 0.610 A 0.067 AB 0.067 A 1.221 A 0.133 A 0.200 A
Ch-pun-host 0.683 0.067 A 0.000 A 0.777 A 0.067 AB 0.067 A 0.893 A 0.200 A 0.067 A
Ch-intac-host 0.494 B 0.067 A 0.067 A 0.714 A 0.000 B 0.000 A 0.913 A 0.228 A 0.067 A
NCh-pun-gran 0.843 AB 0.000 A 0.000 A 1.273 A 0.161 AB 0.000 A 0.828 A 0.067 A 0.000 A
Journal of Economic Entomology, 2020, Vol. 113, No. 3

Ch-pun-gran 0.533 AB 0.133 A 0.000 A 1.480 A 0.492 A 0.000 A 1.120 A 0.200 A 0.000 A
NCh-intac-gran 0.808 AB 0.000 A 0.000 A 0.589 A 0.200 AB 0.000 A 0.793 A 0.000 A 0.000 A
Ch-intac-gran 0.479 B 0.094 A 0.000 A 0.973 A 0.267 AB 0.000 A 0.810 A 0.000 A 0.000 A

Ceratitis capitata

Variable Yellow Green-Yellow Green

NUMVISIT NUMINTOVI OVIPOEXI NUMVISIT NUMINTOVI OVIPOEXI NUMVISIT NUMINTOVI OVIPOEXI

Gl-Treatment 6 6 6 6 6 6 6 6 6
Gl-Replicate 2 2 2 2 2 2 2 2 2
F-value 1.270 3.360 0.940 6.050 3.910 1.340 1.240 0.830 1.000
P-value 0.277 0.005 0.469 0.000 0.002 0.247 0.293 0.546 0.430

Treatments Mean Group Mean Group Mean Group Mean Group Mean Group Mean Group Mean Group Mean Group Mean Group

NCh-host 1.203 A 0.504 A 0.200 A 1.714 A 0.780 A 0.200 A 0.483 A 0.000 A 0.000 A
Ch-pun-host 0.948 A 0.133 AB 0.133 A 0.876 BCD 0.067 B 0.200 A 0.249 A 0.000 A 0.000 A
Ch-intac-host 0.732 A 0.067 B 0.067 A 0.780 0.550 AB 0.255 A 0.133 A 0.000 A 0.067 A
NCh-pun-gran 0.686 A 0.200 AB 0.067 A 0.934 BC 0.315 AB 0.133 A 0.571 A 0.000 A 0.000 A
Ch-pun-gran 0.759 A 0.161 AB 0.094 A 1.488 ABC 0.389 AB 0.067 A 0.459 A 0.094 A 0.000 A
NCh-intac-gran 0.725 A 0.000 B 0.000 A 1.522 AB 0.161 B 0.000 A 0.476 A 0.067 A 0.000 A
Ch-intac-gran 0.868 A 0.000 B 0.000 A 0.828 CD 0.000 B 0.000 A 0.561 A 0.000 A 0.000 A

Maturity stages: Yellow: fully ripened; Green-Yellow = in the process of ripening; and Green = immature but ready to initiate color changes. Oviposition behavior: NUMVIST: number of visits; NUMINTOVI: number of
oviposition attempts; and OVIPOEXI: successful ovipositions. The names of the treatments are as follows: NCh-host: No-Choice host; Ch-pun-host: Choice-punctured host; Ch-intac-host: Choice-intact host; NCh-pun-gran:
No-Choice punctured granadilla; Ch-pun-gran: Choice-punctured granadilla; NCh-intac-gran: No-Choice intact granadilla; and Ch-intac-gran: Choice-intact granadilla.
1173
1174 Journal of Economic Entomology, 2020, Vol. 113, No. 3

also on the food quality and medium that were associated with the and Pasco for the logistic support, as well as to the SENASA Fruit Fly
larvae. To explain the slowed development, granadilla pulp aril may program for kindly providing trapping data. Finally, we thank very
also have resistance mechanisms against fruit flies; e.g., the pulp much Programa Nacional de Innovación para la Competitividad y
aril has a glue-like or mucilage-like substance that could cover the Productividad (INNOVATE-PERU) for kindly having provided the
spiracles, affecting respiration in larvae and pupae, or render move- financial support that rendered possible the development of this
ment of larvae difficult in the pulp. Such a combined effect would study.
slow fruit fly development compared with that in host fruits, such as
mango or peach. In addition, dead larvae and pupae were observed
inside the pulp of granadilla fruits. References Cited
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Central (2019), fruit fly host species such as peach, mango, and oviposition of essential oil of Gardenia jasminoides and its four major
citrus contain an average of 86% of water content while granadilla chemical components against whiteflies and mites. Sci. Rep. 8: 9375.
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