The Mediterranean Fruit Fly (Diptera: Tephritidae), a Key Pest of Citrus in Egypt
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Journal of Integrated Pest Management, (2021) 12(1): 28; 1–10
https://doi.org/10.1093/jipm/pmab025
Profile
The Mediterranean Fruit Fly (Diptera: Tephritidae), a Key
Pest of Citrus in Egypt
Mahfouz M. M. Abd-Elgawad1,
Plant Pathology Department, Agricultural and Biological Research Division, National Research Centre, El-behooth Street, Dokki
12622, Giza, Egypt and 1Corresponding author, e-mail: mahfouzian2000@yahoo.com
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Subject Editor: Erin Hodgson
Received 2 May 2021; Editorial decision 13 July 2021
Abstract
The Mediterranean fruit fly (Mediterranean fruit fly), Ceratitis capitata (Wiedemann), is a key pest of citrus fruit
(Sapindales: Rutaceae), and can infect over 300 other economically important fruit-bearing plant species globally.
The Mediterranean fruit fly moves to different hosts continuously and has 8–10 overlapping generations a year in
Egypt. The female lays the eggs under the fruit peel and hatched larvae use anterior mouth hooks to vigorously
feed on fruit flesh until they reach the third and last instar. As tens of eggs are often deposited in a single spot,
the fruit becomes juicy and inedible. Larval infection and feeding also facilitate the entry of fungi and microbes
that can rot the fruit. Infestation of citrus orchards can result in significant annual losses in crop size and quality.
As a quarantine pest with high reproductive potential and dispersive ability, the Mediterranean fruit fly is difficult
to manage and poses a major threat to Egyptian citrus export because of concerns over infection or pesticide
residues. This review discusses the current state of research on Mediterranean fruit fly biology and ecology as well
as host fruit production practices from the standpoint of pest management. Integrated pest management programs
consisting of regulatory, cultural, chemical, genetic, and biological control methods that are currently the most
effective strategies for Mediterranean fruit fly control are also described.
Key words: citrus, pest, Mediterranean fruit fly, control
As the name suggests, the Mediterranean fruit fly Ceratitis capitata agricultural practices, especially those related to the control of this
(Wiedemann) infests and reproduces on plants in the Mediterranean pest species.
basin, which includes parts of three continents (Asia, Africa, and
Europe). However, its spread extends further: the Mediterranean
fruit fly is a key pest of major fruit crops in many mild temperate, Life Cycle and Biology
subtropical, and tropical regions (Sciarretta et al. 2018) including Ceratitis capitata is a holometabolous insect. The eggs are 1 mm
countries in Central America and Caribbean, Australia, Africa, Asia, in length, slender and smooth, slightly curved, and shiny white in
Europe, and South America (Thomas et al. 2019). Its distribution has appearance. They are usually deposited just under the rind or skin
also expanded over time to new and previously uninfested areas, and surface of the host fruit as it begins to ripen, which may cause dis-
infection of other crops such as tomato (Solanum lycopersicum L.), figuration that reduces its commercial value. The ovipositor of a fe-
pepper (Capsicum annuum L.), and eggplant (Solanum melongena male is about 1.2 mm long (Thomas et al. 2019). As females tend
L.) have been reported. The Mediterranean fruit fly is known to in- to deposit the eggs in an area of the fruit that is scratched or where
fect the fruit of more than 300 plant species and thus ranks highly the skin is already broken, several females may use the same or a
as a globally destructive pest that is responsible for annual losses of nearby spot. About 1–30 eggs are laid at one time, but the number
over two billion U.S. dollars (USD) (Malavasi 2014). In Egypt, the can be as high as 300 in a cavity in the fruit skin that is 1–2 mm deep
Mediterranean fruit fly is the main pest not only of citrus but also (Fig. 1). A female lays 100–500 eggs during her lifetime in Egypt
of many other deciduous and permanent fruit trees. The Egyptian (Abd-Elsalam 1993), but as many as 800 (22 per day) have been
Ministry of Agriculture (MOA) has reported infestation of a var- reported elsewhere (Thomas et al. 2019). Females die as soon as ovi-
iety of economically important hosts including grapefruit (28.13%), position ceases. Unripe or semi-ripe fruits are favored by the female
guava (27.1%), apricot (24.41%), peach (23.22%), fig (8.67%), for oviposition. Larval mortality is higher in riper fruit than unripe
orange (7%), and mango (6%) (Lysandrou 2009). These percent- fruit, and thus increases the proportions of unhatched or dead eggs
ages may differ from one year to the next depending on the annual and larval mortality. The eggs usually develop under the rind as the
spread of C. capitata and variations in environmental factors and fruit ripens, with the area around the puncture site or the infected
© The Author(s) 2021. Published by Oxford University Press on behalf of Entomological Society of America.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), 1
which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
2 Journal of Integrated Pest Management, 2021, Vol. 12, No. 1
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Fig. 1. Four stages in the life cycle of the Mediterranean fruit fly.
spot changing color and texture depending on the plant species and
degree of ripeness of the fruit (Fig. 2); in orange, the color often
becomes reddish or greenish-yellow; in peaches, the puncture point Fig. 2. Different host species of the Mediterranean fruit fly according to fruit
becomes gummy; mandarins become black at the infection site; and ripening periods throughout the year. The ripening periods of different fruits
a dark scar forms on the surface of infected apricot or fig. The time grown in Egypt overlap, such that the Mediterranean fruit fly can reproduce
until egg hatching varies by geographic location and is mainly in- all year round.
fluenced by temperature. In Egypt, eggs hatch after 10–15 d in au-
tumn and spring but after just 2–3 d in the summer; a longer time is
required in winter depending on the ambient temperature. Females minimum of 19 d at 20.6°C–21.7°C (Back and Pemberton 1915). On
may even refrain from laying eggs at temperatures below 16°C. In the contrary, at relatively high temperatures, larvae may pupate and
other regions, eggs hatch after 1.5–3 d in warm weather but the egg eclose earlier than usual. In Egypt, the duration of the pupal stage
stage is also prolonged at low temperatures. is about 8 d in the summer, 15–20 d in spring and autumn, and 30
Larvae (maggots) are whitish-yellow and may serve as a model d in winter (Abd-Elsalam 1993). Notwithstanding the accelerating
for other fruit fly species in terms of their feeding and development. effect of high temperatures on life cycle duration, C. capitata has
Larvae have an elongated form with a narrow anterior end that has a lower temperature threshold than the peach fruit fly, Bactrocera
a slight ventral curve, and a flattened caudal end (Fig. 1). The mouth zonata (Saunders), with lower survival rates of immature stages at
has anterior hooks and the spiracles are located anteriorly on the 35°C and 40°C (Elnagar et al. 2010).
dorsal edge of the straight tubule row, which comprises 7–11 tu- Adults exit the puparium in large numbers early in the morning
bules (Thomas et al. 2019). First instars feed on the fruit flesh while on warm days but emerge more sporadically at cool temperatures.
tunneling and roaming inside the fruit, which ultimately becomes a The adults are somewhat smaller (4–5 mm in length) than that of
juicy and inedible tissue mass. Larval feeding facilitates the entry of the house fly (Musca domestica L.), but the head is almost equal
fungi and microbes into the fruit. The infested fruit rots and if the to or slightly larger. After eclosion, adults are sexually immature;
infestation spreads throughout the orchard, a large percentage of males attain sexual maturity and mate 4–5 d after emerging from the
fruits will drop. Larvae continue to feed on the fruit until they reach puparium, whereas females are ready to copulate 6–8 d after eclo-
the third and last instar (about 7–9 mm in length), at which point sion at 24.4°C–25. 6°C. Mating can take place at any time of day.
they exit the fruit to pupate in the soil at a depth of 5–15 cm or else Oviposition may occur just 4–5 d after eclosion in hot weather but
at any other convenient location. at 10 d after emergence from the puparium at lower temperatures
Temperature impacts the duration of the larval and pupal stages. (20°C–22.2°C) (Thomas et al. 2019).
The former—which includes three instars—may be as short as 6–10 Winds help adult Medflies travel longer distances. The front mot-
d at 25°C–26.1°C (Thomas et al. 2019). In Egypt, the larval stage tled wings are wide with colored (yellowish, brownish, and black)
is about 10–14 d in the summer but 2–3 wk in the spring and au- markings and a broad brownish-yellow strip across the medial re-
tumn. The duration of each stage is also influenced by the type and gion. Adults have a yellow body marked with different colors (white,
condition of the host fruit. Development time is generally longer in blue, brown, and black). In general, half of adults die within the first
citrus fruits, particularly lemon and lime; larvae need 14–26 d to 2 mo after eclosion, but the proportion is higher in the absence of
reach maturity in a ripe susceptible lemon compared to 10–15 d in food and water; in some cases, flies die within 4–5 d after eclosion,
a green peach. Fully-grown larvae are almost white and about 8 mm before laying any eggs. With sufficient food (plant sap, honeydew,
in length (Abd-Elsalam 1993), and often exit the fruit in large num- or fruit) and favorable conditions (mild weather with adequate tem-
bers at or just after dawn to pupate. The pupa is 4–4.3 mm in length perature, available host and water, and absence of natural enemies
and has a barrel shape and brownish, yellowish, or dark reddish and adverse agricultural practices), adult flies can live for over 6
color. Pupae can withstand adverse conditions such as extremes in mo. The lifespan of C. capitata is greatly affected by food scarcity;
temperature and absence or shortage of food and water. However, in Egypt, adults usually live about 1.5–5 mo when adequate food
nonadult stages cannot develop at or below 10°C. The duration of sources are available, with 8–10 overlapping generations a year
the pupal stage is 6–13 d at 24.4°C–26.1°C, which is extended to a (Abd-Elsalam 1993). C. capitata populations in Egypt showed 2–4
Journal of Integrated Pest Management, 2021, Vol. 12, No. 1 3
peaks in seasonal abundance (Ghanim 2017) corresponding to the As a polyphagous species that infects a variety of hosts, the man-
ripening period of different host fruits including citrus. For example, agement of C. capitata has great economic importance. The damage
large C. capitata populations were reported in Upper Egypt between caused by the Mediterranean fruit fly to citrus fruit in Egypt includes
August and December that had been growing between January loss of quality, fruit dropping, and low yield (Ibrahim and Khalif
and July (Hashem et al. 2001). On the other hand, the smallest 1997). The Mediterranean fruit fly is also a vector for fruit-rotting
C. capitata populations were recorded in winter or when there were fungi (Cayol et al. 1994) and is especially damaging to citrus and
few host fruits in Lower Egypt and the Nile Delta region, where peach in Mediterranean countries (CABI/EPPO 1997). In addition to
temperatures are lower than in Upper Egypt. A comparison of lower mandarin, three major varieties of orange—i.e., Navel, Valencia, and
temperature thresholds (T0) and degree days (DDs; i.e., the tempera- Baladi—are the citrus plants most affected by C. capitata in Egypt.
ture required for development) between C. capitata and B. zonata in Host preference and the extent of damage caused by C. capitata
an Egyptian guava orchard revealed that the former developed more are mainly dictated by the chemical and physical characteristics of
rapidly than the latter at 20°C and 25°C, whereas the overall rates the fruit (e.g., fruit size, exocarp hardness, plant species, and chem-
of development were similar between the two species at 30°C and ical composition) as well as habitat (geographic area) and environ-
35°C (Bayoumy et al. 2020). The peach fruit fly was more sensitive mental factors (e.g., weather) (Abd-Elsalam 1993, Ekesi et al. 2016).
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to cold than the Mediterranean fruit fly, with a higher T0; moreover, Thus, fruit species or cultivars are not all equally susceptible to the
B. zonata had higher survival rates at 30°C than C. capitata, which Mediterranean fruit fly.
could be attributable to its tropical adaptation. The two species re- The Mediterranean fruit fly is one of the most serious pests of
quired 616 and 424 DD, respectively, for a complete generation. The fruit trees and other plants, which has serious socioeconomic con-
peak activity periods of Mediterranean fruit fly can potentially be sequences in Egypt. With the low cost of labor and production, the
exploited by pest control measures in infested orchards. close proximity of export markets, early fruiting season, and climate
and soil conditions that are favorable for high yields of good-quality
fruit, Egypt is among the top citrus producers and exporters in the
world (Omar and Tate 2018, Abd-Elgawad 2020a). Moreover, as
Host Plants and Economic Importance the economic crisis associated with coronavirus disease of 2019
The global hosts of Mediterranean fruit fly were recently categor- (COVID-19) continues, the value of citrus has increased as a result of
ized according to their economic rank and geographic distribution affordable local availability; and the export of citrus has brought sig-
(Thomas et al. 2019, CABI 2020). The most economically signifi- nificant revenue of foreign currency. The latter is not only important
cant and preferred C. capitata hosts in Egypt are citrus (Citrus at the state level, but also supports employment (e.g., through
sinensis (L.) Osbeck) of various varieties including orange (e.g., packing facilities). As such, there has been a continuous expansion
Valencia, Baladi, Navel, Sweet orange, Shamooti, and Hamlin); of citriculture to newly reclaimed areas of Egypt (Abd-Elgawad et al.
mandarin orange (Citrus reticulata Blanco); Mediterranean man- 2016). Egypt exports citrus fruit to 98 countries and the demand is
darin (Citrus deliciosa Ten.); sour orange (Citrus aurantium L.); increasing. The top 10 export destinations are Russia, United Arab
lemon [Citrus limon (L.) Osbeck], except for the Baladi variety; Emirates, The Netherlands, Saudi Arabia, China, Ukraine, United
lime [Citrus aurantifolia (Christm.) Swingle]; sweet lime (Citrus Kingdom, India, Bangladesh, and Malaysia (Wally and Akingbe
limetta Risso); Meyer lemon (Citrus meyeri Yu. Tanaka); citron 2019). Japan and Brazil have recently begun importing oranges pro-
(Citrus medica L.); Star Ruby Red grapefruit (Citrus paradise duced in Egypt (Anonymous 2020). Exports to Russia have lately
Macfady); tangerine (Citrus tangerine Tanaka); calamondin increased by about 12% (Wally and Akingbe 2019) although in the
[Citrus microcarpa (Bunge) Wijnands]; calamansi (Citrus mitis past, Egyptian citrus fruits were banned from entry into Russia be-
Blanco); Kumquat (Citrus japonica Thunb.); grape (Vitis vinifera cause of fruit fly larvae-infected oranges (Hamza and Beillard 2012).
L.), peach (Prunus persica L.); mango (Mangifera indica L.); guava The ban was lifted after Egypt adopted cold treatment of exported
(Psidium guajava L.); apricot [Prunus armeniaca L. (Armeniaca oranges as a pest control measure (Hamza 2014). Since then, cold
vulgaris Lam.)]; pear (Pyrus communis L.); apple (Malus treatment training for Egyptian inspectors and exporters has become
domestica Borkh); plum (Prunus salicina L.); fig (Ficus carica L.); standard operating procedure. Other countries such as Morocco
and pomegranate (Punica granatum L.). In addition to the fruit, have also been affected by quarantines related to C. capitata-
C. capitata larvae may also feed on the buds and stems, seed- infected citrus (Anonymous 2016). Market dynamics and free trade
lings, saplings, and succulent tap roots of host plants (Weeks et al. have placed increasing pressure on pest control. In the case of bans,
2020). After burrowing into and spoiling the fruit flesh, larvae action plans are usually established that involve additional measures
exit and leave behind a large hole that can serve as an entry point to control the pest or repair other types of damage (e.g., political)
for fungi and bacteria that cause the fruit to rot. Infected ripe to resume exports. Egypt benefited from a Russian ban of Turkish
fruits usually have a deformed water-soaked appearance and de- oranges in 2015–2016 (Omar and Tate 2018). The Fruit Fly Control
graded quality, and often drop from the tree (Weeks et al. 2020). project and quarantine regulations for quality control of exported
The Mediterranean fruit fly can also transmit the fungi Penicilium citrus have been implemented in Egypt with the aim of controlling
digitatum and Penicilium italicum via egg deposition, which in- fruit fly infestations (Hamza and Beillard 2012). Under the quality
variably increases the number of fallen fruit (Lysandrou 2009). assurance plan for the production of citrus for export, sound citrus
There are approximately 0.65 million hectares of fruit crops pest management practices have become a prerequisite for any grove
yielding 12 million tons of fruit yearly in Egypt; C. capitata and certified for export production. Chemical treatment threshold levels
B. zonata cause damage to 2.5 million tons of these fruits annually have been reduced to 0.5 female or 1 male trap−1 day−1 (Rachid and
(Abou-Saddam 2021). The infestation rates of fruit fly species may be Ahmed 2018). These levels of Mediterranean fruit fly catches are
as high as 30–40% in Egypt, with an annual loss of 177 million USD defined for some trapping systems (Manrakhan 2016) to determine
(Mahmoud et al. 2017). Additional expenses are incurred because of the appropriate method and intensity of pest control; they should be
the various insecticides that are used for Mediterranean fruit fly con- similarly applied to various baits and lure-based trapping systems.
trol such as triazophos, imidacloprid, dipterex, and neem products. This can inform decision-making in C. capitata control programs
4 Journal of Integrated Pest Management, 2021, Vol. 12, No. 1
of citrus, and can also provide guidance to farmers producing other Mating compatibility among C. capitata populations from dif-
susceptible fruits. ferent regions worldwide has been investigated (Cayol et al. 2002),
and courtship behaviors have been reported (Yuval and Hendrichs
2000). Interestingly, exposing C. capitata males to the odor of or-
ange may enhance their mating with females (Shelly et al. 2006).
Ecology and Effect of Environmental
Moreover, male C. capitata fed a high-protein diet showed higher
Factors on the Development and Survival of
sexual activity (Yuval et al. 2007), although this effect varied ac-
C. capitata cording to environmental conditions and fly genotype.
Ceratitis capitata is endemic to sub-Saharan Africa but has occa-
sionally spread to other countries (CABI 2020). Nonetheless, the
Egyptian and European Mediterranean fruit fly populations have Management of C. capitata in Egypt
similar mitochondrial (mt)DNA haplotypes (Gasparich et al. 1997), Regulatory, Cultural, and Sanitary Methods
suggesting the European population originated from Egypt or vice
From the regulatory standpoint, growers are obligated to collectively
versa (which is more likely) in the 1800s. An examination of mtDNA
control C. capitata infestation in the event that the pest has spread at
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haplotypes revealed that West Africa is the probable source of both
the district or governorate level in Egypt. Chemical sprays as the sole
populations (CABI 2020). The Mediterranean fruit fly has adapted
means of C. capitata control are prohibited to avoid environmental
well to various ecologic settings (Harris 1977) including urban and
pollution; an integrated pest management (IPM) approach is manda-
cultivated areas, but it can also occur in stable forests and currently
tory (Anonymous 2018). With C. capitata prevalent in many regions
inhabits different areas with diverse host plant species. Its broad host
in Egypt, preventing its spread to uninfested zones in the country is
profile is attributable to its capacity to utilize nearly all fleshy fruit
critical, and infected or susceptible fruits from affected areas should
types as a food source for larval growth and reproduction.
not be transferred to these zones. Joint action across regions and
The Mediterranean fruit fly tends to conform to the characteris-
countries is becoming increasingly important for Mediterranean
tics of citrus growing areas. The life cycle of C. capitata is lengthened
fruit fly control.
or shortened according to factors such as temperature and host avail-
Rigorous postharvest treatment (e.g., hot or cold treatment,
ability. Although its development time generally depends on ecologic
insecticide dipping, and fumigation) should be applied before re-
factors, the temperature is a key driver of growth at each life stage.
locating the fruits. Citrus groves may be flooded immediately fol-
In general, a higher temperature leads to more rapid development.
lowing fruit harvest after first flooding neighboring groves of infested
In temperate and warm regions such as Egypt, C. capitata actively
mango and guava or mixed with citrus trees, as long as this treat-
reproduces year-round. The upper range of temperatures for its de-
ment does not conflict with other horticultural recommendations.
velopment is 30°C–33°C; the rate of development is reduced at tem-
Flooding can kill larvae and pupae in the soil and limit the spread
peratures above 35°C (Shoukry and Hafez 1979). Low humidity may
of C. capitata to nearby hosts (Anonymous 2018). Planting a single
also adversely affect Mediterranean fruit fly egg and larval stages,
fruit tree species per grove is preferred so that the date of infection
but this may only occur in laboratory assays as low humidity seldom
can be determined and control measures implemented in a timely
occurs in cultivated fields in Egypt (Shoukry and Hafez 1979). On
manner. It is best to avoid cultivating pome and stone fruit trees
the contrary, regions with harsh climates may limit Mediterranean
within the range of citrus groves so as not to facilitate the transmis-
fruit fly survival and reproduction. For instance, its northward mi-
sion of C. capitata from one plant species to another. Mediterranean
gration to Northern Europe is likely blocked by the cold winters
fruit fly-infected fruits—whether on trees or the ground—should be
in that region. The lowest temperature at which C. capitata larvae
collected and promptly destroyed in a way that ensures the complete
could still develop was determined as 10.2°C (Duyck and Quilici
disposal of the insect larvae that they harbor (by incineration or by
2002). Female oviposition ceases at temperatures below 15.5°C and
exposing plastic bags containing infected fruits to direct sunlight).
fly development does not occur below 10°C (Thomas et al. 2019).
Wrapping fruit in the paper as a physical barrier against infection
However, the activity of adult Medflies is greatly reduced or abol-
by C. capitata is a good practice that must be implemented before
ished at temperatures above 30°C; therefore, C. capitata migrates to
the fruit is contaminated. Citrus varieties that can resist infection
regions with lower temperatures (Cayol 1996). Without behavioral
such as Baladi lemon should be preferentially planted in areas of
thermoregulation, the temperature range for coordinated adult mo-
known C. capitata infestation. Tillage of heavily infested orchards is
bility is 42.4°C–43.0°C. The lowest and highest temperatures that
recommended to expose pupae to radiation from the sun or to nat-
are tolerated by C. capitata vary according to feeding status, age
ural predators. Such regulatory, cultural, and sanitary methods are
(Nyamukondiwa and Terblanche 2009), and the long- and short-
increasingly required to prevent the transfer of Mediterranean fruit
term thermal record of its different life stages (Nyamukondiwa and
fly to areas free of infestation or reduce infestation levels in general.
Terblanche 2010, Weldon et al. 2011, Nyamukondiwa et al. 2013).
Given the recent bans of Egyptian citrus by a few importing coun-
Population size depends not only on host availability and specific
tries because of Mediterranean fruit fly infection or pesticide res-
ecologic factors but also on seasonal factors; the size normally in-
idues, these control strategies will help to ensure that Egypt remains
creases in the spring when early ripening fruit is available in orchards.
competitive with other exporting countries.
In Egypt, the Mediterranean fruit fly moves between different hosts
throughout the year (Fig. 2)—i.e., apricot in May and June, peach
from April until the end of August, pear from July to October, guava Chemical Control
from July to November, and citrus fruit from September to May In many countries, field control of C. capitata adults involves
(Ibrahim and Khalif 1997). The larvae feed and develop on many spraying plants with insecticides (often organophosphates, pyreth-
deciduous, subtropical, and tropical fruits as well as some vegetables. roids, and spinosad) mixed with protein baits (Martinez-Ferrer et al.
Infection of various hosts underlies the overlapping generation times 2012, Rachid and Ahmed 2018, CABI 2020) or spraying the soil to
of C. capitata, but also aggravates its losses; a lack of fruit for 3–4 mo kill fallen larvae and pupae (Stark and Vargas 2009). Medflies may
reduces the population size to a minimum. be attracted to trapping systems that release ammonia and trimedlureJournal of Integrated Pest Management, 2021, Vol. 12, No. 1 5
[1,1-dimethylethyl 4(or 5)-chloro-2-methylcyclohexanecarboxylate], et al. 2020). Spinosad has been applied during the harvest period
which achieve chemosterilization by inhibiting insect growth and as the preharvest interval is relatively short (Rachid and Ahmed
reducing the viability of eggs laid by exposed females or females 2018). A spinosad-based fruit fly bait (GF-120 NF Naturalyte; Dow
that have mated with exposed males (Smith 2020). Another simple AgroSciences, Indianapolis, IN, USA) was proposed as a safe alter-
method known as biofeeding involves attracting flies to a yellow native to Malathion-based baits in Egypt (Mahmoud et al. 2017).
suspended carton or device with sticky bait containing spinosad; GF-120 consists of 0.02% spinosad and 99.8% inert ingredients
the flies are attracted to the bait but are unable to escape and die. such as sugar, water, and attractants. The recommended rate of ap-
This device remains active for a few months and is appropriate for plication for tephritid fruit flies is 1–3 ounce per tree (24–85 g/tree)
organic farms. mixed with water for spot spraying. GF-120 is more effective when
A few insecticides are recommended for use in Egypt but partial combined with other control measures such as male annihilation,
spray application is mandated by the Egyptian MOA (Anonymous biocontrol agents (BCAs), mass trapping, and field sanitation (Vargas
2018). Unlike the previously used approach of covering whole crops, et al. 2008, Mahmoud et al. 2017).
partial spraying uses a volume of insecticide solution as low as 50 ml Other compounds—especially kaolin—were shown to be
per tree to reduce the adverse environmental and economic conse- more effective against C. capitata with much better safety pro-
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quences of excessive chemical insecticide application (Mahmoud files than traditional insecticides (e.g., Malathion) in Egypt (Abd-
et al. 2017). This method attracts C. capitata males and females via Elgawad et al. 2012) and elsewhere (Mazor and Erez 2004, Braham
a food attractant [e.g., a specific dose of insecticide plus 250 cm3 et al. 2007). Hydrophilic kaolin, which mainly contains kaolinite
of a food attractant such as Buminal (Buminal GmbH, Herrsching [Al2(OH)2 Si2O5], is used commercially against several insect pests
am Ammersee, Germany), supplemented with water to 20 liter]. and diseases (Glenn and Puterka 2005) at a dose of 5 kg/ 100 liter
Pheromone traps are also recommended as a prerequisite (Fig. 3). At water (Lo Verde et al. 2011). This wettable powder (WP) must be
least one trap per 5 acres is used to detect and estimate C. capitata homogeneously mixed in water before spraying to ensure uniform
population size; the number and intensity of chemical spray (e.g., fruit coverage and full protection from flies. Deterrence of ovipos-
for every or every other tree line per bed) is scheduled based on this ition, repellence, and reduced survival of insects were noted on
size. In combination with chemical pesticides, traps are suspended plants and fruits coated with hydrophobic particle films of kaolin
in shady areas where an infestation is expected to occur about 15 d (Glenn and Puterka 2005). Kaolin conferred greater protection of
before the start of the fruit maturation stage, and are checked and citrus fruit from C. capitata fly infections and was effective over a
refurnished periodically. Many growers add 2 liter Buminal and 0. 5 longer-term than Malathion and spinosad (Braham et al. 2007), and
liter Malathion (Malatox 57% EC; Santa Cruz Biotechnology, Santa may thus be a valid alternative to the insecticides that are currently
Cruz, CA, USA) to water in a 20-liter backpack sprayer to coat tree applied in citrus orchards.
trunks without contaminating the fruit. Citrus trees are normally
sprayed twice: before the fruits show color (around mid-September)
and 3 wk later (Anonymous 2018). As an integrative control strategy, Trap Optimization and Aims
killing strips (pieces of twisted burlap about 20 cm in length and Eco-friendly control strategies for C. capitata typically involve baits
10 cm in diameter stuffed into a bag) can also be suspended from and lure-based trapping systems. Chemicals used as host or food
tree branches in the shade away from the fruits (Fig. 3). The bags are baits or aggregation and sex pheromone lure in traps that are de-
immersed in the spray solution and fully saturated before use and signed for specific goals are continually being improved to offer
must be re-wetted when required. Partial spraying and killing strips longer-lasting protection and greater safety (IAEA 2003, Ekesi et al.
both employ the so-called attract-and-kill approach with insecticide 2016, Gazia 2020). For instance, the three-component BioLure
and bait, respectively. (Suterra, Bend, OR, USA) attracts C. capitata females, whereas the
Spinosad, a naturally derived insect control chemical, has become enriched ginger root oil products PheroLure (Insect Science, Tzaneen,
a popular choice for the control of Mediterranean fruit fly popula- South Africa) and zingerone [4-(4-hydroxy-3-methoxyphenyl)-
tions because of its short persistence in the environment; the com- 2-butanone] are more effective in luring males (Broughton and
pound degrades rapidly 3–7 d after application with little residue, Rahman 2016, Manrakhan et al. 2017). Cyantraniliprole (100 g/liter
although significant toxicity was also reported after 10 d (Pinheiro in a suspoemulsion) may be as effective and safe as Malathion, which
Fig. 3. Different trap designs that can impact trap efficacy and lure volatilization. 1) Killing strips; 2) Nadal trap; 3) Steiner trap; 4) McPhil trap; 5) Tephri trap; and
6) yellow device.6 Journal of Integrated Pest Management, 2021, Vol. 12, No. 1
has toxic residues and can induce the development of resistance in a male attractant (IAEA 2003). Lures and traps should suit the in-
insects (Grout et al. 2018). Trap–bait matching can also enhance tended purpose, whether this be survey, control, or eradication.
C. capitata capture. The McPhail trap uses protein baits to attract Seasonal fluctuations of C. capitata populations are an important
both sexes, while the Steiner and Jackson traps are usually used with consideration for maximizing trap efficiency. Males are usually abun-
kerosene and trimedlure, respectively, to attract males. Food baits dant in early spring, while more females are trapped in late summer
combined with fruit juices, protein or hydrolyzed protein solutions, or early fall or when host fruits of a plant variety in a specific area
or fermenting sugar solutions are often used to capture adult fruit have ripened. In Egypt, most common citrus fruit varieties ripen in
flies but tend to attract more females than males (Ekesi et al. 2016). September–December (Navel orange, Succari orange, and Fairchild
The efficacy of control measures is evaluated by the number of in- mandarin), December–March (Baladi orange, Common mandarin,
fected and fallen fruits and the number of flies captured in traps. Blood orange, Shamooti, and Hamlin), and March–June (Valencia
Traps are used for fruit fly surveys and control and eradi- orange) (Fig. 2). Using separate lures for males or females just before
cation operations. In surveys, detection determines whether the and during these periods increases the success rate of pest control
Mediterranean fruit fly exists in a given area; delimiting defines measures. Applying similar strategies to adjacent fruit-bearing plant
the boundaries of a region considered to be free from or infested by species can also improve Mediterranean fruit fly control efficiency.
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the pest; and monitoring records traits of C. capitata populations Growers can use local trap types or techniques for easier handling
such as relative abundance and seasonal fluctuations (IAEA 2003). and lower cost. The Gazia trap (Gazia 2020) is a cost-effective trap
Surveys may examine the lure or attractant or trap efficiency, the for collecting a relatively small number of fruit flies for scientific
effectiveness of targeted programs, presence of fruit flies and host research (e.g., to increase laboratory strains of C. capitata). Other
species, climate-related and seasonal fluctuations in Mediterranean simple and inexpensive techniques may be applied to repel Medflies
fruit fly populations, and topography. For surveys of C. capitata in in cases of light orchard infestation; some growers use 500 ml
groves, both sex pheromone and food attractants may be used sep- Malathion in 5 liter water to fill several large cups or containers with
arately to determine the male:female ratio. Traps containing methyl relatively wide mouths, which are suspended on citrus tree branches
eugenol (ME) are distributed 25 m apart in the grove, while those to repel the flies.
containing trimethylamine (TMA) are placed 50 m apart (MOA
2020). Trap densities may be lower when sampling to detect im- Outside of Orchards
mature stages and increased 10 fold from the monitoring to the Dry food traps should be uniformly and permanently placed 20
delimiting stage (IAEA 2003). m apart inside fruit storage wards as long as they harbor semiripe
Control or eradication programs should integrate measures or ripe fruits. The expiration date of the food attractant should be
other than traps (Ekesi et al. 2016, Thomas et al. 2019). For con- monitored, with replacement after 40–50 d in winter (from October
trol programs, the threshold for initiating a spraying regimen is to February) and 30–40 d in summer (from March to September).
seven adults per trap per week. About 8–12 sex lure-based traps and Separate sex pheromone traps for males of the peach fly and
12–20 food-based traps per acre are used in Egypt depending on the Mediterranean fruit fly must be placed in each fruit storage ward in
biological and ecologic conditions of the region. When citrus trees the middle of the fruit hold in the shade at a height of 3 m with space
are intercropped with or adjacent to guava trees, the upper limits on all sides. The trap should be cleaned whenever the attractant or
of these ranges are used. Trap and spray control methods should pheromone is replaced. The condition of fruits in the place of dis-
start with guava trees because of their long and early fruiting season. play (e.g., fruit market) should be monitored to ensure that there
These measures vary depending on whether citrus is the main or a is no evidence of fruit fly infection; if an infection is suspected, the
marginal crop because of differences in infestation risk levels and place should be cleaned immediately and any potentially contamin-
control program goals. During the application of control measures ated fruits should be correctly disposed of. Spraying any chemical
in orchards, Medflies may migrate to urban areas or fruit markets insecticide on the displayed products and in surrounding areas is
to avoid the chemicals; hence, trap densities may be higher in these prohibited.
locations than in orchards. The judicious use of traps should not be
based solely on their numbers in an orchard, but also on their place- Sterile Male Technique and Self-Limiting Technology
ment (e.g., at the borders to catch invading flies), the infection status Projects have been ongoing in Egypt and elsewhere that utilize sterile
of the crop to be defended, and Mediterranean fruit fly population insect technique (SIT) as an autocidal Mediterranean fruit fly con-
density. trol method. Males are sterilized with cobalt and then released; fe-
To prevent insects from escaping, traps must be appropriately males that mate with these males lay unfertilized eggs, leading to a
designed with sticky material or insecticide. Alternatively, liquid bait gradual decline in the population. Cost-effective mass-rearing and
solutions (e.g., of proteins) may be effective in retaining the flies. irradiation systems for application of the SIT within the context of
Protein solution is mixed with 1.5–2 g borax to delay the decay of IPM enabled local suppression, prevention, and eradication of the
the seized flies. In synthetic lures, attracted males are retained in solu- Mediterranean fruit fly (Elaini et al. 2020). There are several pre-
tion by a surfactant, while a parapheromone trap may also capture a requisites to achieving good results: the targeted Mediterranean fruit
small number of females. Male-attracting traps use 2,2-dichlorovinyl fly population should be restricted and ecologically confined, and
dimethyl phosphate with TMA for C. capitata and Malathion with females should ideally mate just once during their lifetime. A draw-
ME for B. zonata. Food or host odors can be employed to capture back of the SIT is that sterile males have shorter lifespans and are
females. Parapheromone traps are more effective than liquid bait less competitive in terms of mating than normal males (Rachid and
in areas with a low population density of C. capitata, as the latter Ahmed 2018).
can capture high numbers of nontarget insects. The combination of Manipulating a self-limiting gene to disrupt insects’ normal
TMA, ammonium acetate, and putrescine yields a highly attractive development and prevent reproduction is a promising method for
lure for C. capitata females; it is also more specific than liquid protein pest control. Mating between males that have been sterilized by ir-
baits and can detect females at lower field levels than trimethyllysine, radiation and normal females produces no viable female offspring.Journal of Integrated Pest Management, 2021, Vol. 12, No. 1 7
Weekly release of such males was shown to eliminate Mediterranean C. capitata third-instar larvae (Bazman et al. 2008, Gazit et al. 2010,
fruit fly populations (Leftwich et al. 2014). However, to achieve suc- Abd-Elgawad et al. 2012, Rohde et al. 2020). For instance, mature
cessful pest control with the SIT or by self-limiting genetic manipu- C. capitata larvae were most susceptible to EPN infection during
lation, cost-effective mass rearing methods and efficient generation the first 4 hr after their emergence from the food source for pu-
of a male-only release group are required. Optimal rearing condi- pation, whereas soil moisture levels of 3–20% and temperatures of
tions for the Mediterranean fruit fly are currently being investigated: 22°C–41°C did not adversely affect EPN activity (Gazit et al. 2010).
the pupal density leading to the highest C. capitata egg yield was Steinernema riobrave Texas was superior to 11 other EPN strains in
14,000–18,000 pupae per cage, whereas an embryo density of 1.25– inducing >80% mortality in the final C. capitata larval stage under
2.0 ml/kg larval diet maximized the generation of male-only pupae varying environmental conditions (Gazit et al. 2010). On the other
(Elaini et al. 2020). hand, a Turkish isolate of Steinernema weiseri Mrácek, Sturhan,
and Reid induced 100% mortality in C. capitata larvae (Bazman
Biological Control et al. 2008). Three EPNs—i.e., Steinernema feltiae, Heterorhabditis
Egyptian farmers are accustomed to raising poultry in fruit groves bacteriophora, and Heterorhabditis megidis, S. feltiae—achieved the
without disturbing human-friendly birds such as hornbill (Ocyceros best performance in controlling C. capitata (Medina et al. 2008).
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griseus) and hoopoe (Upupa africana) that feed on Medflies, espe- Fewer C. capitata adults emerged from Mediterranean fruit fly
cially in their subterranean stages (fallen or last instar larvae and prepupae-infested soil treated with the nematodes S. riobrave or
pupae). Members of the order Coleoptera and some ant species also H. bacteriophora than from untreated sterilized or natural soil (Abd-
prey on Mediterranean fruit fly at these stages. In Egypt, the earwig Elgawad et al. 2012).
Labidura riparia as well as spiders attack Mediterranean fruit fly The above results indicate that some EPNs such as the Turkish
pupae in the soil and under fallen infested fruits. isolate of S. weiseri (Bazman et al. 2008) and S. riobrave Texas
The rate of parasitism of the Mediterranean fruit fly was re- (Gazit et al. 2010) have the potential to kill C. capitata larvae as
ported as ≤ 9% (El-Husseini et al. 2018), but hymenopteran para- soon as they fall to the ground for pupation or even after they pu-
sitoids are considered more effective among other BCAs within this pate (Abd-Elgawad et al. 2012). Thus, their field application under
rate. One study investigating the biocontrol potential of five para- the fruit tree canopy (before adult emergence) under the appropriate
sitoid species including three that are native to Africa (Tetrastichus conditions of temperature and moisture is a promising IPM strategy.
giffardii Silvestri, Psyttalia cosyrae Wilkinson, and Psyttalia In accordance with this attract-and-kill approach, EPN application
concolor Szépligeti) and two exotic species (Fopius arisanus Sonan by a trap tree method similar to that used against the plum curculio
and Diachasmimorpha longicaudata Ashmead) against C. capitata Conotrachelus nenuphar (Herbst.) (Coleoptera: Curculionidae)
and other fruit fly species found that the Mediterranean fruit fly may be effective against C. capitata (Shapiro-Ilan et al. 2013). In
was highly targeted by P. concolor based on the number of para- this novel approach, branches of several perimeter-row trees are
sitized C. capitata eggs or larvae, and moderately targeted by the baited with synergistic lures; this results in the aggregation of adult
other four species (Mohamed et al. 2017). P. concolor attacks many C. capitata on the trees, which can then be specifically targeted with
tephritids on various cultivated and wild plants, but its only natural insecticide (Leskey et al. 2008). A suitable EPN strain or species is
hosts are C. capitata and the olive fruit fly Bactrocera oleae Rossi then sprayed onto the soil under the trap tree canopy to control
(Pinheiro et al. 2020). the ground-dwelling stages of the flies. Conditions of temperature
A variety of entomopathogenic nematodes (EPNs) and fungi and soil moisture that are favorable for the selected EPN strain or
(EPF) were shown to be promising agents for Mediterranean fruit species should be ensured (Bazman et al. 2008, Gazit et al. 2010,
fly control, especially under laboratory conditions (Hallouti et al. Rohde et al. 2010, 2020) to optimize EPN efficacy and persistence
2020; Rohde et al. 2010, 2020). EPN isolates were more effective in after application. An iterative approach to predicting and improving
inducing mortality in larvae and adults than in pupae (CABI 2020). these parameters has been proposed that involves the timed release
Larvae are particularly susceptible to infection by EPNs from the of EPNs followed by spatial modeling of their fates (Abd-Elgawad
time they leave the fruit until they enter the soil (Gazit et al. 2010). 2017). Early release models can guide subsequent applications by
Different EPN species can infect and kill C. capitata larvae and providing insight into which aspects of the EPN and environment
pupae without significantly altering their appearance (Fig. 4). The are the strongest drivers of efficacy and persistence. The window of
variable EPN-induced mortality rates across studies may be attribut- opportunity for nematodes to attack C. capitata larvae in the soil
able to differences in the virulence of EPN strains or species, foraging should be identified and targeted to establish short-term equilib-
strategy of EPN-infective juveniles, EPN application method rium of EPN–host dynamics. This is especially important as a few
and rate, environmental conditions, and density and condition of Mediterranean fruit fly larvae that were susceptible to EPNs (Abd-
Elgawad et al. 2012) were found in Egypt infecting fallen mango
(Abd-Elgawad 2014) and citrus (Abd-Elgawad 2020b) fruits in nat-
urally EPN-infested soil. Additional research is needed to evaluate
the actions of EPNs so that effective IPM programs for C. capitata
can be developed.
Various EPF have also been tested against C. capitata.
Beauveria bassiana was capable of infecting and killing
C. capitata larvae, pupae, and adults over different courses
of exposure (Chergui et al. 2020). Metarhizium anisopliae and
B. bassiana were more lethal to Mediterranean fruit fly than
Paecilomyces lilacinus (Soliman et al. 2020) but in another study,
Fig. 4. C. capitata larvae and pupae infected with different EPN species. B. bassiana was generally ineffective against C. capitata (Medina
H. bacteriophora (Hb), H. indica (Hi), Steinernema carpocapsae (Sc), and et al. 2008), possibly because the median lethal time depends on
Steinernema glaseri (Sg). the fungal isolate that is used. The results obtained from these8 Journal of Integrated Pest Management, 2021, Vol. 12, No. 1
laboratory bioassays require validation under more realistic field frequency and dosage of chemical pesticides. Diflubenzuron signifi-
conditions. Additionally, indigenous fungus strains are likely to cantly reduced the emergence of the parasitoid P. concolor used as
be superior for controlling C. capitata (Hallouti et al. 2020). It is a BCA from 44.2% to 3.3% when C. capitata larvae were fed at
essential to identify and establish the optimal conditions and ap- 0.02 and 0.2 g active ingredient (ai) per kg diet, respectively; the
plication strategies to achieve maximum C. capitata control with reduction was only from 43.9% to 40.1% when fenoxycarb was
entomopathogens. used at 5 and 50 g ai/kg diet, respectively (González et al. 1998).
Like microbial pesticides, many botanical agents such as most Negative interactions can also occur between BCAs: the emer-
plant extracts and oils are a safe alternative to chemicals. Essential gence of P. concolor was decreased from 27.3% to 0.0% with the
oils can be toxic to the pest or may act as oviposition deterrents, application of azadirachtin—a compound derived from neem tree
stimulants, repellents, or attractants that enhance mating of sterile (Azadirachta indica A. Juss)—at 0.015 and 0.15 g ai/kg diet, respect-
male C. capitata. The essential oils of Baccharis dracunculifolia ively (González et al. 1998). Some lure-based Mediterranean fruit fly
and Pinus elliottii induced mortality in 100% of C. capitata pupae traps can attract and kill beneficial parasitoids, but spinosad does
(Oviedo et al. 2018). not harm these BCAs in nature (Smith 2020). Moreover, P. concolor
females were moderately injured when exposed to fresh residues
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of the fungicides tebuconazole, penconazole, and difenoconazole,
Considerations for IPM but there was no injury when these fungicides were used to treat
P. concolor-parasitized C. capitata pupae (Jacas and Viñuela 1994).
Traps can be used to assess the efficacy of the abovementioned con-
Melaleuca alternifolia (Myrtaceae) essential oil is more toxic to
trol methods. Setting threshold levels for fruit flies in various lure-
C. capitata than to its parasitoid P. concolor (Benelli et al. 2013).
based trapping systems is critical in different citrus-producing areas
The lethal and sublethal effects of biopesticides, insecticides, herbi-
within a region to guide growers on the control strategies needed to
cides, and fungicides on BCAs and related bioactive compounds that
achieve C. capitata-free orchards. Pest control measures should thus
may be used against citrus pests and pathogens must be clearly deter-
be implemented on a case-by-case basis. For instance, C. capitata
mined to develop comprehensive IPM strategies. While biopesticides
was completely eradicated in Carnarvon, Western Australia through
and herbicides were shown to have relatively few adverse effects on
sequential steps. In phase one, 70 traps were set according to the
P. concolor reproductive parameters and mortality, pyrethroids and
seasonal abundance of wild Mediterranean fruit fly; then in phase
organophosphates are highly toxic insecticides, and a few fungicides
two, 7.5 million sterile male flies obtained via the SIT were released
are also known to be damaging to P. concolor (Pinheiro et al. 2020).
per week. As this was insufficient to reduce the wild Mediterranean
Comprehensive IPM may be achieved by increasing agroeco-
fruit fly population, the number was increased to 12 million a week
system resilience and stakeholder input (Barrera 2020). In Egypt, the
in combination with the application of chemical control agents in
capacities of the government and private sector, extension services,
phases three and four. Only the latter was halted in phase five when
growers, and other stakeholders with respect to fruit fly control
wild fly levels were undetectable. This strategy of releasing sterile
should be cooperatively enhanced. Strict quarantine regulations with
males was continued for three virtual fly generations (October
proper devices and equipment (e.g., taxonomic tools and expertise,
1984–January 1985); successful eradication was declared when
traps, and lures) should be adopted, and fruit fly maps should be
there was a complete absence of wild flies or larvae during this
distributed to assist in the detection and identification of different
period (Fisher et al. 1985).
species. Each case of infestation must be controlled according to
There are three major types of interaction between biologicals
the prevailing biological and environmental conditions, given the
and chemicals used against a pest: 1) positive (additive or syner-
possibility of interactions between the different control methods.
gistic), in which control is greater with a combination of agents than
Ultimately, combining 2 or more compatible methods in holistic IPM
is expected from the addition of the individual agents; 2) neutral,
programs is an effective strategy to rid citrus fruit of pesticide res-
where the BCA is compatible with but does not add value to the
idues, pests, and diseases.
chemical used alone (i.e., no significant or consistent change in con-
trol when both are used together); and 3) negative (Mediterranean
fruit fly control and BCA are less effective). An obvious example of
Acknowledgments
a positive interaction is the suppression of C. capitata larval infec-
tion of Navel oranges by separate applications of S. riobrave and This article was supported in part by the U.S.–Egypt Project Cycle 17 (no.
172) entitled “Preparing and evaluating IPM tactics for increasing strawberry
commercial kaolin WP; maximal pest control was achieved when
and citrus production”; and the NRC In-house Project No. 12050105 entitled
both agents were used simultaneously in laboratory and field tests
“Pesticide alternatives against soil-borne pathogens and pests attacking eco-
in Egypt (Abd-Elgawad et al. 2012). Thus, for partial spray appli-
nomically important solanaceous crops”. Thanks to Ibrahim Shehata, Mostafa
cation, pesticides with potentially additive or synergistic effects Hammam, and Ahmed Mahfouz for help in preparing some of the presented
should be selected to circumvent health hazards and the develop- figures.
ment of resistance in pests (Abd-Elgawad and Askary 2018). In this
context, EPN species or isolates (Fig. 4) with varying degrees of
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