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FRUIT FLIES IN CALIFORNIA
Dr. E. F.
Legner, University of California, Riverside
The fruit flies of the family Tephritidae constitute a group of
agricultural pests of worldwide importance, as they attack a wide range of
fruits and vegetables. The most
important are the several species of Dacus and Ceratitis, which
occur in many countries of warm temperate and subtropical climates; Anastrepha,
an American genus occurring from Mexico and the West Indies through South
America; and Rhagoletis, with a more restricted host range, occurring in
the north temperate region. The
Mediterranean fruit fly, although eradicated periodically from the state of
Florida where it had
"peninsular" distribution, is presently firmly established in
southern Mexico where it is temporarily contained by a massive sterile-male and
parasite release effort by the U. S. Department of Agriculture. Eventually this species may move north
and pose a continuous threat along the
Mexican border. Another chronic threat
has been the permanently established population in the Hawaiian Islands, from
which periodic accidental invasions of California are thought to occur. Recently, Carey & Dowell (1989),
Greathead & Waage (1983), Gilstrap et al (1987), Wharton (1989) and Wong
& Ramadan (1990) have noted that further biological control efforts are
definitely justified against fruit flies.
The
Mediterranean fruit fly in particular has received a lot of attention in recent
times. It is a
major pest throughout the Mediterranean
region, portions of Africa, the Middle East, Central
and South
America, Mexico, and Hawaii, and has become established in Australia. In France, it
is able to persist from year to year only in
areas bordering the Mediterranean, yet survival is
reported in
Austria, where severe winters, with continuous frosts, can cause up to 90%
mortality
of the
pupae (Clausen 1978). Several studies
have investigated the potential economic of C.
capitata in California and elsewhere.
Details on this and various abatement tactics may be found
in UC/AID (1977) Galt & Albertson (1981),
Carey (1982, 1984), Gilmore (1983), Dowell (1983),
Schreibner (1983), Spitler & Couey
(1983), Williamson (1983), Krainaker et al. (1987) and Carter
(1990). Although parasitic insects have been
imported against it, all except one species were
obtained
from areas outside the fly's native range in central Africa. However, some reductions in
infestations are attributable to natural
enemy activity in the invaded areas, especially when parasitic
insects are mass released as biotic
insecticides (Wong & Ramadan 1990, Wong et al. 1990).
Some investigators
believe that the Medfly is already permanently established in California and
that unless the current eradication effort is greatly increased, it is just a
matter of time before it will spread throughout the state (Barinaga 1990). The Malathion baits currently in use against
may not be potent enough for fast eradication, as it is recognized that
Medflies will not eat the bait unless that is the only substance placed in
their cages (Citrograph 1990). Under
outdoor conditions they may prefer to seek out clean ripening fruit.
As it becomes
increasingly apparent that fruit flies pose continuous threats to California's
agriculture through periodic invasions of our borders, there is an urgent need
to consider the application of alternative methods to chemicals in eradication
and control programs. The implementation of effective biological controls at
the sources of an invasion as well as within the state boundaries where
breeding may occur, offers an environmentally sound, non-polluting
alternative. There is a need to (1)
develop and improve techniques for the search, procurement and evaluation of
natural enemies of fruit flies in their natural ranges (parasites, predators
and pathogens); (2) introduce and study
foreign natural enemies and evaluate their respective effectiveness under field
conditions in Hawaii, southern Mexico, and California; (3) develop a mass
production scheme for periodic releases of introduced natural enemies in
infested areas of California, and to observe their effectiveness under natural
conditions; and (4) build a culture bank of natural enemies for use in
conjunction with other eradication and control methods (e.g., sterile-male releases)
during periodic invasions of this pest and in anticipation of its possible
permanent establishment in the State of California.
The need for
investigation into the biological control of fruit flies in Hawaii, Mexico and
California is ever more important as it becomes recognized that insecticides,
although offering expedient and predictable results under certain conditions,
are often inadequate and at least perceived as dangerous, if not physically
dangerous to wildlife and humans alike.
As problems involving insecticidal residues and insect resistance to
chemicals continue to increase, many programs directed at the control of fruit
flies must ultimately be modified with increased dosages and costs to such an
extent that they invariably arouse the concern and ire of naturalist and
conservationist organizations. A case
in point is the fire ant eradication program.
By 1959 extensive damages to wildlife and domestic animals had
positively been attributed to the effects of several insecticides used in the
program (Clawson 1959). Fire ant
control was finally declared unsuccessful in 1960, and in some states, fire ant
numbers were actually reported to have increased since the eradication program
began (Byrd 1960, Cottam 1959).
Presently, a new effort to control fire ants is being attempted with
natural enemies imported from Brazil and Argentina.
Principal Fruit
Flies in California
Biological Control Efforts against Fruit Flies
The biological control efforts against fruit flies of the genus
Tephritidae have been extensive over the past half century, a thorough review
being given in Clausen (1987). However,
as it becomes increasingly apparent that the Mediterranean fruit fly, Ceratitis
capitata (Wiedemann), and Mexican fruit fly, Anastrepha ludens
(Loew) pose a continued threat to California's agriculture through periodic
invasions of our borders, there is an urgent need to consider the application
of alternative methods to chemicals in eradication and control programs. The
implementation of effective biological controls at the sources of an invasion
as well as within the state boundaries where breeding may occur, offers an
environmentally sound, non-polluting alternative. There is an urgent need to (1) search for, procure and initially
evaluate natural enemies of Mediterranean and Mexican fruit flies in their
natural ranges in central Africa and southern Mexico (parasites, predators and
pathogens); (2) introduce and study
foreign natural enemies in the adult stage, and evaluate their respective
effectiveness under field conditions in Hawaii, southern Mexico, and if
applicable, California; (3) attempt development of a mass production scheme of
resident California fruit flies (e.g., walnut husk fly) to serve as acceptable
hosts for Medfly natural enemies for use in laboratory study and periodic
colonization efforts in infested areas of California, and (4) to test the
feasibility of building a culture bank of Medfly and Mexican fruit fly natural
enemies on resident California fruit flies for use in conjunction with other
eradication and control methods (e.g., sterile-male releases, adult fly
baiting) during periodic invasions of these pests and in anticipation of their
possible permanent establishment in the State of California.
Specific Examples
Medfly. Cerititis capitata (Wiedemann)-- The Mediterranean
fruit fly was first described fin 1824 and was first noted as a pest in citrus in
1829 from shipments of oranges to England from the Azores. The fly spread throughout the world over the
next 100 years and was continually noted as a destructive pest wherever it was
found. The first program for the
biological control of the medfly was undertaken by the government of Western
Australia in 1902 with the engagement of George Compere to search for natural
enemies and to determine the aboriginal home of the medfly. Unfortunately Compere was never able to
ascertain the aboriginal home nor did he establish the parasites he collected
from India, Sri Lanka and Brazil in Western Australia.
The medfly invaded
Hawaii in 1910 and soon thereafter the Board of Commissioners hired Filipi
Silvestri to again search for natural enemies of this fly. It was determined by experts of the day that
collections should concentrate in Western Africa. Therefore, Silvestri traveled for eight months through West and
East Africa and South Africa. He found
only six specimens of the medfly on the entire journey, but reared many
parasitic insects from other fruit-infesting tephritids collected along the
way. He managed to establish four
species in Hawaii: Opius concolor
Szepligeti, Biosteres tryoni (Cameron), Coptera silvestrii
Kieffer and Dirhinus anthracina Walker. Two more missions over the next 30 years were sent out in hopes
of obtaining parasitic insects, but only Tetrastichus giffardianus
Silvestri and Biosteres fullawayi (Silvestri) were established.
Other biological
control programs were undertaken in several countries where the medfly was
firmly established, but these programs have not been well documented, and the
extent of control of any of the parasitic species is virtually unknown, the
notable exception being Hawaii. Even in
Hawaii control was never noteworthy and the medfly problem was finally
overshadowed by the introduction of Dacus dorsalis Hendel. For North America the answer to the medfly
invasions starting in 1929 was complete eradication by means of fruit stripping
and poisoned bait sprays.
The success of
these early and subsequent biological control programs against the medfly has
been variable (Gilstrap & Hart 1987, Wharton & Gilstrap 1983). In Hawaii, a cooperative biological control program
initiated in 1948 involved the release of 32 entomophagous species to combat
both medfly and the oriental fruit fly.
Three parasitic species, Biosteres longicaudatus
(Ashmead), B. vandenboschi (Fullaway), and B. oophilus
(Fullaway) became widespread and abundant (Bess et al. 1961). During 1966-1968, parasitization of the
medfly and the oriental fruit fly was high (ca. 70%); it was mainly due to the egg-pupal parasite, B. oophilus
(Haramoto & Bess 1970). During
1978-1981, Biosteres oophilus was still the predominant parasite
as it accounted for ca. 80% of the total parasitization. Occasionally the larval-pupal parasite, Biosteres
longicaudatus and B. tryoni (Cameron) achieved a
parasitization of 32 and 8%, respectively (Wong et al. 1984). Extensive fruit collections done between
1949-1985 showed that Jerusalem cherry, coffee and peach were among the most
important hosts of the medfly. These
fruits yielded more than 100 larvae/Kg of infested fruits (Liquido et al. 1990;
Nishida et al. 1985). The fruits that
yielded a high number of medfly larvae were elliptical or spherical and
yellowish or reddish. They had a
diameter of 1-7 cm and a weight of 1-30 grams.
Most of these hosts belonged to five plant families: Myrtaceae, Rutaceae, Rosaceae, Sapotaceae
and Solanaceae (Liquido et al. 1990).
In Costa Rica a
classical biological control program was initiated in 1955. During 1979-1980 parasitic insects were
collected from <10% of C. capitata populations. These were two introduced braconids, B.
longicaudatus and B. oophilus, and two indigenous
cynipids, Ganaspis carvalhoi (Dettmer) and Odontosema anastrephae
(Borgmeier) (Wharton et al. 1981). An
exploration for natural enemies of the medfly, conducted in West-Central Africa
during 1980-1982, showed that C. capitata occurred in low
frequency in coffee plantations in Cameroon.
Parasitization of tephritids in coffee by braconids ranged from 10-56%
(Steck et al. 1986). In Guatemala
infestation of C. capitata was serious in coffee and tangerine. The rest of the fruits were mainly infested
by Anastrepha spp. (Eskafi 1988,
1990). Parasitization rate of C.
capitata and Anastrepha spp. was low, ranging from 0.04 to
7.95%. The most common parasitic
species recovered from both flies were B. longicaudatus and Doryctobracon
crawfordi (Viereck) (Eskafi 1990).
The behavior of
the ectoparasite Muscidifurax raptor (Girault & Sanders) in
searching for the potential host C. capitata pupae was analyzed
under laboratory conditions. The searching
efficiency of M. raptor females decreased with increasing
density. The proportion of avoidance of
superparasitism was 0.615. The response
to a high parasite density was to increase the proportion of males in the
progeny, as males searching for mates interfered and decreased the searching
activity of the females (Podoler & Menzel 1977, 1979). The medfly was susceptible to the Mexican
strain of the nematode Steinernema feltiae. Emerging adults and pupae were not
susceptible to the nematode, but the third instars (prior to pupating in the
soil) suffered high mortalities (50-90%) when exposed to high nematode
concentrations (150,000 - 500,000 nematodes/cup) (Lindegren & Vail
1986). Field exposure of mature larvae
to a dose of 500 nematodes/cm2 yielded high mortality of C. capitata
(Lindegren et al. 1990). In addition to
the hymenopterous parasites and insect pathogenic nematodes, arthropod
predators such as ants could play an important role in reducing fruit fly
populations. Under laboratory conditions,
the Argentine ant, Iridomyrmex humilis (Mayr) caused 50%
mortality of medfly pupae after a 10 min. attack. However, ant predation could be important only in localized
areas; it is not adequate to regulate medfly populations (Wong et al. 1984).
Typically, the most effective natural
enemies of an insect occur in regions where the pest originated. The natural range of the Mediterranean
fruit fly is the sub-Saharan central African region, including the Island of
Madagascar. Although no information is
available from Madagascar, a number of promising natural enemies have been
discovered in Central Africa (Table 1; Bianchi & Krauss 1936, 1937;
Gilstrap & Hart 1987, Greathead 1976, Silvestri 1914, Steck et al. 1986,
van Zwaluwenburg 1936, 1937, Wharton, 1989, Wharton & Gilstrap 1983). However, because of technological
difficulties associated with transportation and culture, only two species attacking Ceratitis capitata
have been successfully translocated out of central Africa. A concentrated effort to locate natural
enemies there might yield the kind of species capable of regulating this pest
at low densities, as it has been known to be rare in that general region since
the early 1900's (Silvestri 1913). The
parasitic Hymenoptera are believed to be the most effective natural enemies of
fruit flies. At least six species of
fruit flies in the genus Ceratitis are known from central Africa, and
numerous parasitic Hymenoptera have been reported active on them at very low
host densities (Table 1, Silvestri 1913, Clausen 1978, F. Gilstrap, pers.
comm.). These have not been tested by
entomologists in California because the Mediterranean fruit fly has been
quarantined. Therefore, promising
species of natural enemies for Medfly might be found among these related
species. Also, there has been no
concentrated effort to locate disease organisms, such as viruses, bacteria and
fungi, which might prove invaluable in eradication campaigns.
Table
1. Known parasitic species attacking
fruit flies of the genus Ceratitis in
their natural range in Central Africa.
____________________________________________________________________________________________________________
Parasite
species Host stage attacked Parasite species Host stage attacked
____________________________________________________________________________________________________________
|
Biosteres caudatus Szepligeti larva |
Hedylus sp. larva |
|
Diachasma fullawayi Silvestri larva |
Galesus silvestrii Kieffer pupa |
|
Diachasmimorpha longicaudata
(Ashmead) larva |
Microbracon celer (Szepligeti) larva? |
|
Diachasmimorpha tryoni
(Cameron) larva |
Opius humilis Silvestri larva |
|
Dirhinus ehrhorni Silvestri pupa |
Opius inconsuetus
Silvestri larva |
|
Dirhinus giffardii Silvestri pupa |
Hedylus giffardii Silvestri larva? |
|
Ganaspis sp. larva? |
Opius n. sp. larva |
|
Halticoptera sp. larva? |
Spalangia afra Silvestri pupa |
|
Opius perproximus
Silvestri larva |
Tetrastichus dacicida Silvestri larva |
|
|
Tetrastichus giffardii Silvestri larva |
|
|
Tetrastichus oxyurus Silvestri larva |
|
|
Tetrastichus n. sp. larva |
|
|
|
_____________________________________________________________________________________
Mexican fruit
fly. Anastrepha
ludens (Loew)--Some of the natural enemies
of oriental and Mediterranean fruit flies have shown activity on Anastrepha
spp. in southern Mexico, and may be influential in partial biological control
of that species (Aluja et al. 1990).
However, there have been no formal attempts to obtain natural enemies
from other areas where different species of Anastrepha occur, such as
South America.
Two species of
parasitic insects are already proven and available as biotic insecticides
(augmentive releases) against Medfly.
These are Diachasmimorpha longicaudata and D. tryoni,
which have been used with some success in Mexico and Hawaii (USDA 1988, Wong et
al. 1990a,b). The use of these
parasites in lieu of Malathion during the establishment phase of specific
natural enemies from central Africa, would greatly aid their survival and while
providing some economic control of Medfly.
Misc. fruit flies--Several
species of Rhagoletis are very important pests of cultivated cherries in
North America and Europe, with some species having been considered as subjects
for biological control, despite the low economic threshold. Infestation rates of less than 0.2% are
currently required for commercial marketing of cherries in the United States. Four species of parasitic insects associated
with the Oriental fruit fly, Dacus dorsalis Hendel, were
introduced against such fruit flies.
These included Opius longicaudatus compensans
(Silv.), Opius longicaudatus farmosanus (Full.), Opius
oophilus Full., and Opius longicaudatus novacaledonicus
Full. These parasites were introduced
from Hawaii and released against Rhagoletis indifferens Cueran
and Rhagoletis fausta Osten Sak in Oregon and Washington in the
1950's (Clausen 1956b). However, none
became established probably because they all originated in tropical
regions. A parasite of R. cerasi,
the European cherry fruit fly, was imported against the eastern cherry fruit
fly, R. cingulata Loew during 1959-64 in New Jersey, without
successful establishment. Other species
including Biosteres sublaevis Wharton, Coptera occidentalis
and Phygadeuon wiesmanni are under investigation in California
and Oregon (Croft & AliNiazee 1999).