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PINK BOLLWORM Pectinophora gossypiella (Saunders) -- Lepidoptera,
Gelechiidae (Contacts) ----- CLICK on Photo to enlarge &
search for Subject Matter with Ctrl/F. GO TO ALL: Bio-Control Cases When
P. gossypiella invaded the lower Colorado Desert of Arizona
and California in 1978, within 10 years the following damages resulted: (1) total cotton area dropped from 79,942
ha. to 37,130 ha., (2) total value of cotton dropped from $245,812,807 to
$71,803,418, (3) insect control costs increased from $375.59/ha. to
$639.98/ha., and (4) whitefly populations increased exponentially with
pyrethroid insecticide use (Johnson et al. 1982) producing severe honeydew,
yield loss and disease symptoms in cotton and surrounding vegetables
(tomatoes, cucurbits, sugar beets and lettuce). Pectinophora is a numerically small genus but based on its
distribution and species richness, the center of endemicity appears to lie
along the coastal rim of Australia extending from southeast Queensland to
northern Western Australia. From
Australia pink bollworm probably taken by humans to Indonesia and then
further distributed to parts of Africa, India, Mexico and the United
States. Dispersal Pectinophora may have originated in Australia or in
neighboring islands to the northwest of the continent on a malvaceous plant
other than domesticated cotton.
Generally ignored in all discussions of pink bollworm movement is the
positional relationship of Indonesia.
This region seems geographically pivotal and important in
understanding pink bollworm movement.
Indonesia has not been an important cotton producing region and
therefore it has been largely ignored in an analysis of pink bollworm
problems. Nevertheless, movement of
pink bollworm into the Indonesian Archipelago from Northern Australia seems
obvious. The earliest record of pink
bollworm on Java dates from 1903 (Kalshover 1981). More recently, pink bollworm was observed on Bali, Lombok,
Flores and Timor; this would suggest that it is widespread in Indonesia (G.
Gordh, unpub. data). The
shift of pink bollworm from Australia to Indonesia seems probable in
that: (1) the movement could have
been affected by trade, probably by indigenous peoples (the Bugis or Makassar
of Sulawesi) before Dutch colonization or (2) pink bollworm naturally invaded
the islands of Indonesia at an earlier time in geological history
(Miocene-Pleistocene). Once on the
islands of Indonesia, pink bollworm was sustained on some of the numerous
species of malvaceous plants in that region.
Two host plants commonly used by pink bollworm, Hibiscus tiliaceus
and Thespesia populnea, are widespread in
Indonesia. In
this hypothetical scenario, subsequent trade between India and the Indonesian
Archipelago, probably during the Hindu expansion, moved pink bollworm into
India. In India, pink bollworm
remained at insignificant levels on endemic alternative host plants, such as Abutilon indicum, Hibiscus
spp., Thespesia populnea, etc. During this period of residence in India,
pink bollworm may have been transported to Africa by traders. When
American cotton was imported into India, pink bollworm quickly shifted
hosts. Movement to Egypt probably
occurred from India via transport of seed.
Movement elsewhere within Africa probably occurred from the spread of
pink bollworm in Tanzania northward into Kenya and thence along the coast
into Somalia. Movement to Brazil and
Mexico came through transport of infested seed originating in Egypt. Movement to Malaysia, China and Hawaii
came through transport of infested seed originating in India. Pink bollworm has been described from
India in 1843 and subsequently recovered in Hawaii (1901), East Africa
(1904), Malaysia and Burma (1906), Egypt (1907), Australia (1911), Mexico
(1911), Brazil (1913), Texas (1917), China (1918) and California (1965). Spread in Egypt
and the United
States The
history of pink bollworm in Egypt is tied to the production of cotton. During historical times cotton was woven
into fabric before it was cultivated in Egypt (Ballou 1919). Cotton production probably began in the
13th or 14th century. Production was
increased and the industry stimulated about 1820. Then cotton in Upper Egypt was produced as a perennial crop;
cotton in Lower Egypt was produced as an annual crop. The first cotton seeds used for commercial
plantings in Egypt were obtained from ornamental gardens near Cairo. This so-called Jumel cotton was cultivated
for many years as a three-year perennial.
Subsequently Sea Island cotton was imported from Georgia and Florida
in the United States, and Peruvian cotton was imported from brazil. During the latter half of the 19th century
Ashmuni and Mit Affifi were the common varieties produced. Pink
bollworm was first noted in spinning mills near Alexandria in 1906-07
(Pearson 1958). Willcocks (1916)
first detected pink bollworm in field plots during November-December
1910. The moth may have been present
in Egypt as early as 1903. Accounts
of pink bollworm in Egypt around 1879 have not been confirmed. That is the year in which the cotton worm,
Prodenia litura, was discovered in
Egypt. Records of pink bollworm in
Egypt around 1879 may refer to cotton worm.
Alternative host plants for pink bollworm in Egypt include Bamia, Hibiscus esculentus, teel, Hibiscus
cannabinus, and hollyhock, Althea rosea (Willcocks 1916).
The source of the infestation has been traced to badly ginned cotton
received from India (Willcocks 1916).
It was noted that Caravonica cotton seed had been introduced into
Egypt from Queensland, but no pink bollworms were detected. By 1912 pink bollworm was the most common
pest of cotton in Lower Egypt. Pink
bollworm was first intercepted in the United States at Hearne, Texas on
September 10, 1917 by Mr. Ivan Schiller (Hunter 1918). Infestations in Texas developed from
Mexican cotton seed taken to Texas for oil extraction. Subsequent infestations may have resulted
from bales of ginned cotton swept from the wharves of Galveston during
hurricanes of August 1915 (Hunter 1918).
Presumably the cotton bales washed ashore near cultivated cotton. Pink
bollworm was first detected on wild cotton in southern Florida during 1932,
but origin of the infestation cannot be documented. The pest was detected on cultivated cotton in northern Florida
and southern georgia at about the same time, and persisted until eradicated
during 1936. Pink bollworm persists
at very low levels on wild cotton in the Florida Keys (G. Gordh pers.
commun.). Pink
bollworm was first reported in California during 1965 (Legner & Medved 1979). Problems with this insect in the
southwestern United States since 1965 have centered in New Mexico, Arizona
and the California lower desert. More
substantial acreage of cotton growing in the Central Valley of California have
experienced sporadic infestations which are controlled by releases of sterile
pink bollworm males. Parasitoids During
the past 80 years, 160 species in 43 genera of parasitic Hymenoptera have
been collected with or reared from pink bollworm infested cotton (Gordh
1989). The genera Apanteles, Bracon, Brachymeria,
Chelonus and Elasmus among the parasitic
Hymenoptera contribute numerous species of potentially useful pink bollworm
parasitoids. Efforts to permanently
establish 14 imported parasitic Hymenoptera on the pink bollworm in the lower
Colorado Desert of California and Arizona during 1969-78 we thwarted by
widespread insecticide application, even though field reproduction of eight
species was recorded. Inundative
releases of parasitoids produced varying levels of pink bollworm reduction,
the best performance being attained with egg-larval parasitoids, Chelonus spp.
(Braconidae). A Chelonus sp. nr. curvimaculatus
(Cameron) obtained from the presumed native range of pink bollworm in northwestern
Australia was most effective, giving an adjusted 69.9% infested boll
reduction by August 24 at the equivalent release rate of 2,667 females/ha.
(Legner & Medved 1979). Extensive collections in northwestern Australia in 1991-92
revealed that Apanteles oenone and a Dirhinnus sp. were very active
on P. gossypiella (J.
Altmann, unpub. data). Nutritional
studies have been conducted by Legner & Thompson (1977) Insecticide
applications eventually eliminated attempts to biologically control pink
bollworm in the United States.
Insecticides represent the primary control measure which has been
successful in limiting damage of pink bollworm in commercial cotton. However, during more than 40 years of
application, insecticides have not solved the problem anywhere in the
world: each growing season finds pink
bollworm present and developing resistance to toxic compounds. Predators All
of the common predators in cotton fields are capable of feeding on pink
bollworm eggs and first instar larvae (Jackson 1980). Biological control programs were initiated
at the University of California during the late 1960's. Field work during this period focused on
survey of predators occurring naturally in the lower desert. Laboratory studies were summarized by
Orphanides et al. (1971); field
studies were summarized by Irwin et al. (1974). These studies show that several groups of arthropods attack
pink bollworm naturally, including mites, predaceous Dermaptera, Hemiptera,
Coleoptera and Neuroptera. The egg
stage is most vulnerable to attack by predators because it is relatively
exposed when compared to larvae and pupae.
Most predators lack morphological modification of the legs and
mouthparts necessary to penetrate bolls to feed on pink bollworm larvae. The dermapteran Labidura riparia
(Pallas) attacks all immature stages of pink bollworm including the pupa
(Orphanides et al. 1971). However,
the predator is not a dominant element in a predatory complex. Hemiptera are abundant in cotton in
southeastern California, and at least five species in five genera of
Hemiptera have been recovered from pink bollworm. Hemiptera seem to express the broadest range of attack, feeding
on eggs, larvae, cocooned larvae and probably pupae. Irwin et al. (1974) found that Nabis, Geocoris and Orius
all demonstrated effectiveness in field studies. Coleoptera are well represented with four species in four
genera attacking pink bollworm. Most
beetles focus on eggs and early instar larvae as prey. Chrysoperla
carnea (Stephens) is the
only neuropteran reported attacking pink bollworm in California, and seems to
prefer eggs and early instar larvae (Orphanides et al. 1971). There is little data about the consumption
of pink bollworm by predators under natural field conditions. The alfalfa/cotton ecosystems are
basically composed of eight genera of numerically important primary
consumers, six genera of predators and associated parasitoids and
hyperparasitoids in New Mexico (Gordon et al. 1986). A number of parasitoid species and most
predaceous arthropods are non host specific (Huffaker & Rabb 1984). Ehler & van den Bosch (1974) suggested
that most common predators in cotton fields are opportunists that switch
between primary consumer and other predaceous prey species depending on
availability. Although animal
populations may be associated for a number of reasons, predation is one of
them, and the measurement of interspecific association may be used to reduce
the total possible testable combinations (Smith 1980). Ellington (1988) analyzed 17
predator/primary consumer and predator/predator genera from 862 cotton
samples for co-occurrence from 1981-84 and 1987. There were 273 significant co-occurrences above three
(3-14). A switching parasitoid or
predator can stabilize an otherwise unstable host/parasitoid interaction
(Murdock 1969, Royama 1971). A
primary consumer like pink bollworm entering an ecosystem with a high
density, species rich arthropod complex, may experience a damped density
response. Arthropod Complexity in
Cotton The
cotton ecosystem is very complex. In
Arkansas about 600 species of predators representing 45 families of insects,
9 families of spiders and 4 families of mites may be associated with cotton
(Whitcomb & Bell 1964). In the
San Joaquin Valley, California, 300-350 arthropod species may be found in
cotton (van den Bosch & Hagen 1966).
This complex arthropod group may be composed of three trophic
levels: primary consumers,
parasitoids and hyperparasitoids and predators. Some 15-30 genera may be present in sufficiently high numbers
to warrant evaluation. Included in
this group are four superfamilies of minute, parasitic Hymenoptera which are
responsible for the biological control of many key phytophagous species and
are often unfortunately the first arthropods to be removed by insecticide
application because they have lower genetic variability and exhibit lower
detoxification capacities (Croft 1990).
Potential For Biological Control
The
gelechiid moth genus Pectinophora
contains three species: P. gossypiella (Saunders), P. scutigera
(Holdaway), and P. endema (Common). All three species occur in Australia: P.
gossypiella occurs in the
Northern Territory and Western Australia; P.
scutigera and P. endema occur in Queensland. Life
history data is provided by Fullaway (1909) and Busck (1917) for pink
bollworm in Hawaii. Similar
information is provided by Gough (1916, 1920) and Ballou (1918) for pink
bollworm in Egypt and Hunter (1918) and Loftin et al. (1921) for pink
bollworm in Mexico. Russo (1940)
provided an extensive description of anatomy for all stages of development,
based on studies in Somalia. Holdaway
(1926) discussed the bionomics and biology of spotted pink bollworm in
relation to pink bollworm. He
concluded that the spotted species was native to Queensland and that its
primary host plants were Hibiscus
tiliaceus and Thespesia populnea; commercial cotton was a secondary host. Common (1958) reviewed the species of Pectinophora associated with
cotton in Australia, described P.
endema from eastern
Australia, and provided a key to the species. All
species of Pectinophora are
potential pests because they feed upon the buds, flowers and seed capsules of
malvaceous plants. The list of
hostplants for pink bollworm is extensive and has been summarized by Li
(1936) and Noble (1969). Pectinophora gossypiella and P. scutigera are pests of cotton; P. endema
attacks hibiscus in Australia but not cotton. Pectinophora gossypiella became a commercial
problem because its larval stage frequently enters diapause while in seed
capsules, which enabled the pest to become widespread. In contrast the spotted bollworm does not
enter larval diapause within seed capsules and therefore has not become
widespread (Sloan 1946). In
Queensland P. scutigera is not an especially
important pest of cotton, but can cause damage to late maturing bolls and
reach more serious levels of infestation when cotton is grown near other host
plants. During
the past 80 years, 160 species in 43 genera of parasitic Hymenoptera have
been collected with or reared from pink bollworm infesting cotton (Gordh
1989), most of which are probably casual.
The Hymenoptera are divided into at least 13 superfamilies which
contain about 80 families and more than 100,000 identified species. Within this numerically large and
biologically diverse group, species which attack pink bollworm are restricted
to the superfamilies Ichneumonoidea, Chalcidoidea and Chrysidoidea. Although
several genera of ichneumonids have been reported attacking pink bollworm, no
group prevails. In contrast, the
genera Apanteles, Bracon and Chelonus among the Braconidae contribute numerous species
of parasitoids. Gordon Gordh (1992)
reported that only two genera of Trichogrammatidae have been taken from pink
bollworm eggs, but it is doubtful that these collections were actually from
that host. Trichogramma is cosmopolitan in distribution and presently
contains more than 12 species.
Biological information developed on the genus indicates that host
specificity is not common. Gordh
stated that the genus is substantially larger than presently recognized and
probably contains many species which potentially attack pink bollworm
eggs. The problem with this is that
true pink bollworm, P. gossypiella sequesters its eggs
under the calyx and other plant structures in a manner that is not generally
available to parasitoids in the Trichogrammatidae. The
genus Trichogrammatoidea has
generally been ignored in biological control work. This genus contains about 30 species and is predominantly
Indo-Australian in distribution. A
few records exist for the new world, but these probably represent expansions
of the natural geographical distribution by species transported in
commerce. Most recently two species
have been recovered from Pectinophora
scutigera in Queensland,
Australia, which deposits its eggs in an exposed position on host plants. Gordon Gordh reported that they also
readily attack P. gossypiella (G. Gordh, unpub.
data), but this information is undoubtedly wholly from data secured in
confinement cages in the laboratory, where indeed trichogrammatids are easily
mass cultured (J. Altmann & E. F. Legner, personal observations). History of Biological
Control Effort Biological
control efforts were undertaken in Egypt during 1928-35, with the
introduction of Bracon mellitor (Say) from Hawaii, Bracon kirkpatricki (Wilkinson) from Kenya and the Sudan, and Bracon lefroyi (Dudgeon & Geough) from India (Kamal
1951). No practical results were
reported although the latter species became established. In
the United States importations to Texas during 1932-35 were made of Bracon brevicornis (Wesmael) from Europe, and B. mellitor from Hawaii.
Chelonus blackburni (Cameron) from
Hawaii and Exeristes roborator F. from Egypt. Additional strains of these species as
well as B. nigrorufum (Cushman) and Chelonus pectinophorae (Cushman), were made from Korea during
1937-44. Although large numbers were
released, they were not established.
Failure to do so was attributed to concurrent heavy insecticide usage. Final attempts to establish parasitoids
from India were made in 1953-55. Bracon brevicornis, B.
gelechiae (Ashmead), Chelonus heliope (Gupta), and Apanteles
angaleti (Muesebeck)
importations also failed, reportedly due to intensive pesticide treatment and
low winter temperatures (McGough & Noble 1955, 1957; Noble 1969, Noble
& Hunt 1937). Bracon kirkpatricki
and C. blackburni were introduced in southern Arizona during
1917-74, with only minor impact on P.
gossypiella being recorded
(Bryan et al. 1973, 1976; Fye & Jackson 1973). It is significant that most of these parasitoids were known from
other hosts than P. gossypiella, and that they were
colonized under unfavorable circumstances.
Therefore, when biological control efforts began in California in
1969, explorations were extended to acquire not only previously tested
species, but specific ones as well (Legner & Medved 1979). In
the biological control effort in California, parasitic Hymenoptera that were
successfully reared from P. gossypiella were obtained
during explorations in India, eastern Africa, southern Europe, Australia and
Hawaii. The parasitoids were cultured
from 5-20 founders and colonized in cotton fields infested with P. gossypiella in southeastern California and western
Arizona. The potato tuberworm, Phthorimaea operculella (Zeller) was used
for mass propagation, with no known deleterious effects on the biology of the
parasitoids (Legner & Thompson 1977).
Specific experiments were designed to measure the ability of a
particular parasitoid to permanently establish in cotton fields, and its
regulative impact on the pink bollworm population (Legner & Medved 1979). Eight out of 14 parasitic species
introduced in the area reproduced in the field, but no species was ever
recovered in the summer following the year of release, even though field
reproduction in the release year was often significant and overwintering
possibilities existed (Fye & Jackson 1973, Legner 1979). During
the year in which releases were made, parasitoid recovery was greatest in
autumn months following peaks in host abundance, which was probably due to a
combination of parasitoid reproduction and more favorable environmental
conditions for development in the cooler autumn period (Legner & Medved 1979). Significant regulative impact against P. gossypiella by several parasitic species was detected
(Legner & Medved 1979), but as no carry-over to the
second year was possible, compounded control with time was not
observable. It was concluded that in
the absence of widepread insecticide applications, annual early season
parasitoid releases over large areas of cotton might result in a drop of pink
bollworm density if continued for several years, with decreasing numbers of
parasitoids required for control in succeeding years as pink bollworm
densities drop through parasitization. A
lack of genetic heterogeneity in imported parasitoids also could have
restricted their influence especially as founder cultures never exceeded 20
individuals. A further search in the
presumed endemic range of pink bollworm in northwestern Australia and
southern Indonesia (Common 1958, Wilson 1972), might yield additional
effective species and strains.
However, a permanent self-perpetuating regulation may be difficult to
attain as natural restrictions on the early germination of cotton at the
higher latitudes in springtime may cause an asynchrony whereby emerging
overwintering parasitoids cannot find hosts upon which to develop
successfully (Legner 1979 ). A
search for natural enemies in the endemic range of P. gossypiella
in northwestern Australia was supported by the University of California in
1981-82 (Sands & Hill 1982), and US/AID in 1981-83. Two species of Elasmus (Westwood), E.
broomensis and E. bellicaput (Girault) were found. Elasmus broomensis was determined to be
a primary parasitoid and considered as a useful agent for biological control (Naumann
& Sands 1984). Additional species
found were Apanteles oenone Nixon and Chelonus sp. nr. curvimaculatus. As part of the survey, 21 species of
Lepidoptera including 5 Gelechiidae) were reared from the seed capsules of
Malvaceae. The possibility of
hyperparasitic activity by the Elasmus
was eliminated experimentally. Genetic Incorporation Into Cotton of Bacillus thuringiensis
Toxin The
gene for a larvicidal toxin produced by Bacillus thuringiensis was
incorporated into the genome of commercial cotton and an array of other plant
species that are grown commercially for food and fiber. The degree of pest control never reached
economically acceptable levels, and resistance of Lepidoptera to the toxin as
of 2017 has very high, as would be expected from any non-living killing
agent. The levels of control from
many previous widespread field applications of Bacillus thuringiensis
were never spectacular, so that the poor performance was not surprising. Additional
detail on biological / integrated control, biology of hosts natural enemies and pheromone disruption
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