Migracion y dispersion de Anthonomus grandis (Coleoptera: Curculionidae) en America del Sur.
The <<cotton boll weevil>> Anthonomus grandis Boheman (Coleoptera: Curculionidae) (BW) is considered the most destructive cotton [Gossipium hirsutum L. (Malvaceae)] pest in America, due to its behavioural characteristics that allow migration and dispersal, its biological characteristics such as high reproductive capacity, multivoltine life cycle, and the fact that predation and parasitism by natural enemies provide poor control of its populations. From moderate numbers of overwintered adults the pest may develop into yield-damaging populations within the span of a single generation. Any insect species that exhibit these attributes has the potential of being a dangerous economic pest (Walker & Niles, 1971).
In the Northern and Southern American cotton growing areas, even though there are over 50 recorded beneficial species of predators and parasites that attack the BW, these do not effectively control the pest populations. The BW is also susceptible to protozoan and fungal pathogens, but effective control has not been achieved so far, primarily because the pathogens do not act fast enough (Bell, 1983). This fact is consistent with the concept that there are in principle, no effective control agents found in the habitat of newly introduced pests (Ables et al., 1983).
In South America, the BW has invaded Brazil, Paraguay, Argentina and Bolivia (dos Santos, 2000; Gomez et al., 2000; Cosenzo et al., 2001; Duran Parada, 2000). Cotton production in these countries is mainly represented by two opposite situations: large cotton fields of over 50 ha and farmers with less than 3 ha, where smallholders rely on cotton as a cash crop. Cotton-growing areas in Paraguay and Argentina are scattered among the region and represented mainly by smallholders. This fact makes the cotton pest complex situation quite different from the one in the US or in Australia, two countries with modern and technically advanced agricultural industries.
As shown by the US Boll Weevil Eradication Program (http:// permanent.access.gpo.gov/lps3025/ weevil.html), the only effective way thus far, to reduce BW populations to levels below economic significance is the use of intensive pheromone mass trapping, pin-head applications based on pheromone trapping, in-season insecticide applications and intensive <<diapause-control programs>>. Such an intensive, high input approach makes cotton growing unprofitable for small farmers. Moreover, insecticides pose a serious drawback on populations of beneficial organisms that regulate other cotton pests, such as Pectinophora sp. (Lepidoptera: Gelechiidae), and Heliothis sp. (Lepidoptera: Noctuidae). Therefore, the use of pesticides to manage the BW impacts the whole insect pest management of the crop, and augments production costs. Thus, the arrival of the boll weevil, has had severe social consequences because although damage by this insect pest has reduced yields and profits drastically (e.g. Paraguay), smallholders are not expected to abandon cotton in the short term, since historically there have been no other alternatives to cotton for a cash crop (Cosenzo et al., 2001).
The BW has been an issue of interest since the species first became known as a pest in USA in the early 1890's and considerable work has been published on the subject. However, in South America, the BW has only recently become a key pest, and many questions regarding its biology, dispersal and host relationships still remain unanswered in this singular South American-scenario.
Recent advances in the knowledge of the BW in the framework of a project titled Integrated Pest Management of the Cotton Boll Weevil in Argentina, Brazil and Paraguay (CFC-ICAC/04), present an opportunity to review the origin, dispersal, host relationships and natural enemies of the pest in South America (Stadler, 2001). The new discovery of the BW at the southern limit of the cotton cropping area in Argentina and the latest advances in the knowledge of the interaction between the BW and its host-plant as well as its feeding habits, offer an opportunity to understand the dispersal of the BW in Brazil, Paraguay, Argentina and Bolivia. Based on the knowledge obtained we present a review of the ecological and physiological factors that have made the dispersal and establishment of the BW in South America so successful, and discuss its implications.
Natural history of the cotton boll weevil
As described by West-Eberhard (2005), variability in responsiveness in an organism is due partly to genetic variation and partly to variations in the developmental plasticity of phenotype structure, physiology, and behaviour that arise during development and may be influenced by inputs from the environment, like temperature, photoperiod and food availability. Survival and reproduction of an individual strongly depend on its phenotypic plasticity (Caswell, 1983; Ishihara, 1999).
The phenotypic plasticity of the BW has been demonstrated by the high variability in time required by this species to develop from egg to adult even for eggs laid on the same day. This developmental time range may be as short as three days and as long as thirty six days for weevils developing in squares and up to fifty one days for weevils developing in bolls. Moreover, the BW is a multivoltine species with eight to ten generations during the normal season, and this is a critical attribute that makes it a dangerous economic pest (Coad, 1915; Horton & Ellis, 1997). Different authors report that spring-emerging BWs search for the nearest cotton plants (Cushman, 1911; Grossman, 1928) to feed on. Those weevils emerging before squares are available may feed on the terminals of cotton seedlings or on pollen from flowering plants near the cotton fields. The BW, however, needs cotton pollen to successfully mate, and oviposition does not occur until squares are present (Pierozzi Jr., 1985). After cotton square formation, BWs are attracted to cotton fields by plant volatiles. They respond to the host plant volatiles as well as to aggregation pheromones from other individuals present in the field (Tumlinson et al., 1969; White & Rummel, 1978). Later, they mate and lay eggs when squares reach approximately 0.6 mm in diameter. BW oviposition has been well described by several authors (Cushman, 1911; Hunter & Price, 1912; Bottrell, 1983). The BW female scouts the flower or fruit bud tapping it with her antennae before laying an egg. Upon selecting a suitable site the insect begins to bore a hole into it with its mouthparts, after pulling out a piece of the epidermis and lays an egg. Females prefer to oviposit on squares rather than on bolls (Isley, 1932; Habib & Fernandes, 1983) unless the squares are too big (Showler, 2004). Usually, females lay one egg per square but each female may lay about two hundred eggs during a ten to twelve day period. Eggs hatch in three to five days and newly emerged larvae feed within the squares for eight to ten days. The pupal stage lasts from five to seven days. Generation time from egg to egg averages about eighteen to twenty one days, depending on environmental conditions (Horton & Ellis, 1997). Toward the end of summer, most emerging adult weevils enter a <<pre-diapause>> state, where they don't mate and spend a great part of the time feeding to build up reserves for the winter. In semiarid regions (e.g. Rolling plains of Texas), adults generally spend the winter sheltered under leaf litter in wooded areas near cotton fields, in fence rows and grass banks surrounding cotton fields (Sterling & Adkisson, 1971). The BWs remain in these overwintering sites until temperatures become warmer and days lengthen (Horton & Ellis, 1997).
Cate & Skinner (1978) state that BWs are primarily pollen feeders and their populations can be sustained by pollen when cotton is unavailable. Work conducted in the northern hemisphere and in Paraguay and Brazil, has shown that the BW feeds on pollen from Malvaceae when reproductive hosts are lacking (Cross et al., 1975; Lukefahr et al., 1986; Marengo Lozada et a/., 1987). Diversification in foraging in the BW is a product of its phenotypic plasticity as part of the survival strategy in adults during periods when cotton is not available. It has been shown that the BW is a polyphagous species and feeds on pollen of other plants apart from Malvales in North and South America (Benedict eta/., 1991; Jones eta/., 1993). In Argentina and in Paraguay, adult BWs feed on native flora in the absence of cotton. This was shown by different authors studying BW populations from Formosa and Misiones (Argentina), where 37 pollen types were found in the digestive tract of trapped individuals. Pollen found belonged to Malvaceae, Compositae (Asteraceae), Solanaceae, Euphorbiaceae, Amaranthaceae, Leguminosae (Fabaceae), and Polygonaceae (Cuadrado & Garralla, 2000; Cuadrado, 2002). In the winter, pheromone trapped BWs showed pollen from different species of Solanaceae, Leguminosae, Malvaceae, and Compositae in their digestive tract (Cuadrado, 2002). Finally, Showler & Abrigo (2007) showed that adult BWs can be sustained on non pollen food sources from plant species common in the south tropics and Mesoamerica. These authors demonstrated that the BW is able to feed on endocarps of prickly pear, grapefruit and orange, and survive up to three and a half months. Moreover, BWs seem to have a higher survival rate during the winter in citrus orchards than in other habitats, and Showler (2006) calls these <<overwintering hot spots>> for the BW. Pollen as well as non pollen food sources other than cotton are called <<feeding hosts>> and do not induce reproduction. Nevertheless, feeding hosts allow the survival of weevils during the cotton-free months and represent an important energy supply for pre-diapausal, migratory and post-diapausal activities.
Recent findings present Hampea sp. (Malvaceae) as an original reproductive host for the BW. However the BW has adopted other reproductive hosts such as Gossypium hirsutum, Cienfuegosia sp. (Malvaceae) and a pantropical species of Hibiscus (Malvaceae), Hibiscus pernambucensis (Cate, 1996).
The tribe Gossypiae (Malvaceae) in America embraces four genera: Gossypium, Hampea, Thespesia and Cienfuegosia, and BWs have been observed on all them. Hampea occurs mainly in Mexico and Central America and south of the Amazon only the genus Cienfuegosia occurs wild and Thespesia populnea (L.) is often commercially grown. The BW's reproductive hosts in South America have not been experimentally determined so far, but according to Krapovickas (2000) the genus Cienfuegosia seems to be the most probable reproductive host for the BW and its geographic distribution in Argentina overlaps with the cotton-cultivated areas in this country. Cienfuegosia is endemic from the province of Chaco (Argentina) and Paraguay and it can be found up to latitudes of 33[degrees] S. Therefore, knowledge of the species and its possible role as alternative host for the BW is of great importance, especially considering that its blooming period extends from September to June in Paraguay, providing an alternative food source for the BW in the off season (Krapovickas, 2000).
The BW faces different seasonal challenges during its life cycle, such as absence of its reproductive host, harsh winter conditions, and shortening of daylight. Phenotypic plasticity allows the BW to adapt to adverse factors through migration, dormancy and seasonal phenotypic variation.
Cotton boll weevil dormancy
Dormancy is a genetically based arrestment in insect development through behavioral adaptation to a seasonally changing environment. Stimuli like food quality and abundance can influence dormancy through interaction with photoperiod and temperature (Dingle, 1972; Beck, 1980). Dormancy also allows synchronization of insect lifecycles interacting with development rates and determining patterns of voltinism (Tauber & Tauber, 1976). Quiescence and diapause are the two types of dormancy usually identified in insects although diapause shows several intermediate forms (Muller, 1970; Beck, 1980; Tauber et al., 1986).
Overwintering in the BW occurs in the adult stage, which may provide the greatest flexibility for location of, and movement within overwintering sites, as well as movement towards food and reproductive resources in spring.
The literature reports on BW diapause are diverse and in most cases, rather confusing (in Rankin et al., 1994). Most literature reports on BW diapause (Earle & Newston, 1964; Keeley et al., 1977; Wolfenbarger et al., 1978; Graham et al., 1979; Guerra et al., 1982; Braga Sobrino & Lukefahr, 1984; Rankin et al., 1994) match Muller's (1970) definition of oligopause: a <<facultative response to unpredictable exigencies on an irregular basis, induced by adverse environmental conditions>> and this particular response appears and ends with a delay relative to unfavourable conditions.
According to Muller's (1970) classification, some populations in the US as well as in north-eastern Brazil show an oligopause (Braga Sobrino & Lukefahr, 1984). On the other hand, the <<diapause syndrome>> described in the BW by Rankin et al. (1994), consists of a set of behavioural and physiological species-specific markers of pre-diapause, diapause and post-diapause processes to seasonal changes (Tauber et al., 1986).
Graham et al. (1979) suggest that the incidence of diapause in BW may vary considerably from year to year. Earle & Newston (1964) describe differences in BW diapause between individuals as a consequence of overwintering strategies other than diapause that occurs in response to an array of environmental factors or diet. Differences in responses to overwintering cues among insects of the same species from different geographical areas are common, and critical photoperiods for diapause induction often appear related to latitude (Tauber et al., 1986; Leather et al., 1993). For example, there are significant differences in BW diapause (Keeley et al., 1977; Wolfenbarger et al., 1976; Guerra et al., 1982), as well as in winter time reproduction (Showler, 2006) between subtropical and temperate environments. Guerra et al. (1982) reported that in the subtropical regions in the US, diapause is best distinguished by interruption of sexual functions, which is only temporary and can be easily altered through feeding on cotton flower buds.
The regulation of diapause in the BW is complex and dynamic. Both early and late life stages are sensitive to dynamic photoperiods and temperatures, individuals remain sensitive to these cues for different durations, and the cues have a cumulative effect on diapause induction over part or all of the life cycle (Wagner et al., 1999). This adaptation would provide the species with flexibility to allocate portions of its population to reproduction or diapause as conditions dictate during development.
Migration of the cotton boll weevil
Migration in insects is a persistent, directed movement dependent upon an inhibition of response to physiological stimuli (i.e. mating, food), that could eventually arrest movement Kennedy (1961). This definition has shown to be useful in distinguishing migratory and trivial flight in insects (Rankin et al., 1994). The BW, like other insect species, uses migration not only to escape from old habitats and/or adverse conditions but also for colonization and active exploitation of temporary habitats (Southwood, 1962).
Migration in the BW occurs in the fall, when the major portion of the BW population moves from cotton fields into a winter habitat relatively near the source field. According to Moody et al. (1993), the early progeny of these migrants will probably enhance the effective dispersal from the point of origin. These authors also consider the reproductive BWs dispersing from infested fields in the fall to play an indirect but major role in the establishment of overwintered adults in new areas. Showler (2006) reports that curculionids are not known to migrate between specific locations and that the long range movements of BWs are passive and accidental relying on wind currents. So, the BW might spread randomly to favorable and unfavorable habitats like plant seeds do. Early workers recognized that the BW did not rely totally on its flying ability to cover great distances because it is a slow flyer with a non-aerodynamic body design, reaching unassisted flight speeds of < 4,8 km h-1 (McKibben et al., 1988). For BWs lifted by convective currents to higher altitudes where wind velocities are greater, wind velocity and direction play primary roles in displacement as decisive factors determining the direction and distance travelled. Rainey (1977) highlighted the enormous survival rate of insects using kinetic energy of atmospheric circulation through downwind movement to locate and exploit ephemeral vegetation.
In South America, the BW tends to disperse during late summer and early fall matching the end of the cotton season, and favored by high wind speeds. The average highest wind speeds observed in Argentina, Brazil and Paraguay are from the NE and N directions and they can have a significant influence on BW dispersal from infested areas (Ravelo et al., 2001). As described by several authors (Gomez et al., 2000; Cosenzo et al., 2001), the highest BW trapping catches in Misiones were observed after cotton harvest, which is coincident with the massive migration of BW from southern Paraguay to NE Argentina (Misiones and Formosa provinces) in the fall (Gomez et al., 1996; dos Santos, 2000; Gomez et al., 2000). Young weevils emerged in the fall, will migrate after cotton harvest mainly as a result of food scarcity as shown by different authors in Brazil, Paraguay and Argentina (Gomez et al., 1996; Gomez et al., 2000; dos Santos, W. J., 2001; Cosenzo et al., 2001). On the other hand, spring-emerging early reproductive BWs will migrate in absence of reproductive hosts, and feed on feeding hosts until a reproductive host becomes available. Spring-emerging BWs reproduce after reaching the limits of their dispersal flight. During this phase, BWs could travel great distances (Rankin et al., 1994). Studies conducted by Rankin (1974) indicate that juvenile hormone (JH) controls the timing and coordination of flight and reproduction through its response to photoperiod, temperature and food quality in Oncopeltus fasciatus (Dallas) (Heteroptera: Lygaeidae). In this species, intermediate JH titers stimulate migratory behavior, allowing rapid colonization by young adults at their highest reproductive potential, maximizing the utilization of the new habitat. This phenomenon is termed <<oogenesis flight syndrome>> (Dingle, 1974). During starvation, JH titers continue to decline until the individual settles down to survive on its reserves to maximize the chance of finding a more favorable environment (Rankin & Riddiford, 1977). A similar efficient strategy is employed to some extent by other species as the (e.g.) Colorado potato beetle [Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae)] and the common cockchafer [Melolontha melolontha L. (Coleoptera: Melolonthidae)] (Stengel & Schubert, 1970). Very little is known about the reproductive physiology of the BW, oogenesis, or adult diapause in this species. However, in a study conducted by Taub-Montemayor et al. (1997) elevated levels of hemolymph juvenile hormone esterase (JHE) were found to be positively correlated with survival throughout the winter in South Texas population of weevils. According to these authors JH seems to control vitelogenesis in the pre-reproductive female weevil and high JHE levels are correlated with diapause onset and overwinter survival. Boll weevils with relatively large fat bodies and incompletely or partially developed ovaries show a tendency to make long duration flights (Rankin et al., 1994). This condition is typical of the <<oogenesis flight syndrome>> in which migration occurs prior to the onset of reproduction (Dingle, 1974).
Dispersal of the cotton boll weevil in Latin America
The BW may move more than 60 km in search of food or overwintering habitats. Johnson et al. (1975) recaptured marked BWs at distances ranging from 2 to 66 km from the release point and Guerra (1988) reported that several marked BWs were recovered at a flight distance of approximately 320 km. Other authors reported that an advance of approximately 80 km year -1 was normal for this insect as it spread north and eastward (Hunter & Coad, 1923). The BW dispersal stochastic models developed by McKibben et al. (1991), show that maximum dispersal distances can be greater than 100 km for some individuals of a migrant population.
In the USA, the BW was firstly found in Texas in 1892. In the subsequent thirty years, it infested the USA cotton belt and spread to Venezuela in 1949 and to Colombia in 1950 (Burke et al., 1986). The rapid expansion of the BW in the cotton growing areas in North and Central America and its high impact on the crop yield are an evidence of the fast dispersal rate and high reproductive capacity of this pest.
The Amazon was thought to be an adequate barrier that would restrain the BW from moving southwards. However, in February of 1983 the Department of Entomology of the Agricultural School in Piracaba-Sao Paulo reported the presence of the pest in cotton fields in Campinas Sao Paulo (Braga Sobrinho, 2000) (Fig. 1), although it is possible that the appearance of the BW in Brazil was due to an accidental introduction other than because of natural dispersal (dos Santos & Meneguim, 1996). In June 1983, probably disseminated through cottonseed trade, the BW infested the cotton growing areas of the northeast of Brazil (Paraiba and Pernambuco). In March 1985, 350 000 ha of cultivated cotton in the states of San Pablo, Paraiba, Pernambuco and Rio Grande do Norte were affected by the pest (dos Santos & Meneguim, 1996; Degrande, 1991). The first infestation in Parana was found in 1987. Less than five years later, the pest had infested more than 90% of the cotton producing area of the country. It was especially appalling for smallholders, who couldn't afford new technological advances to control the pest (Gomez et al., 2000).
The appearance of the BW in Brazil put Paraguay on the alert, where cotton is the main crop. Traps to monitor the pest were installed in Paraguay and as a measure to restrain the advance of the pest into the country, the entrance of cottonseeds from Brazil was banned and cotton cultivated with seeds coming from that country were destroyed. In spite of all these efforts, BWs were captured in pheromone traps for the first time in Paraguay in 1991, in the district of Saltos del Guayra (Gomez et al., 1996).
In 1993, the BW was reported in the province of Misiones (Fig. 1), restricted to non-cultivated areas. In June 1994, BWs were captured in San Ignacio de Loyola (Argentina), on the border with Paraguay, near cotton fields. At the same time BWs appeared in pheromone traps in the department of Pilcomayo and then Pilagas (Formosa province). In 1996, BWs were captured 60 km southwest of the cultivated area (Cosenzo etal., 2001), and finally in August 2006 BW was reported in Cte. Fernandez (Chaco), the main argentine cotton cropping area (http:// www.inta.gov.ar/saenzpe/actual/06/abril/ noticia1.htm) (Fig. 1). In 1999 the presence of the BW was reported in Bolivia, and it is suspected that it was introduced from Brazil (Duran Parada, 2000).
[FIGURE 1 OMITTED]
At present the occurrence of the BW in the Parana state (Brazil), not only constitutes a problem by reducing cotton profitability, but it also creates dispersal sources that move to Argentina. The pest has been restrained from the main cotton growing area in Argentina although sporadic re-infestations occur due to migrating insects from Paraguay (Cosenzo et al., 2001).
In Paraguay the BW affected approximately 95% of the cotton growing areas in 1996, migrating in a windward direction (NE) at a speed of 60 km a year (Gomez etal., 2000). There are three distinct BW infested areas in Paraguay (Fig. 2): the northern area where BW populations are high (A), the central area where pest populations are moderate to high (B) and the southern area (C), dispersal front of the BW, with intermediate levels of infestation (Gomez et al., 2000). As shown in the figure, BW dispersion has been precisely followed in Paraguay through trapping programs developed by the Ministry of Agriculture of this country (Gomez et al., 2000), demonstrating that the BW disperses downwind at a rate of 60 to 100 km in a year.
In an attempt to eradicate the BW from Argentina, and to prevent infestation of the main cotton cropping areas of the Chaco and Formosa provinces, the Argentine authorities decided to destroy all cotton planted in the province of Misiones (Fig. 1), close to the border of Paraguay and Brazil. Surprisingly, even when cotton was eradicated in the province of Misiones, trap captures established since 1996, show a trend of BW populations migrating upwind in northeast direction in the fall from Paraguay into Misiones and further into Corrientes province (Argentina) (Retzlaff, 1998), two provinces where citrus are among the main crops. Remarkably, the results of the Argentine BW trapping program show that the BWs' southwestern (downwind) migration in direction to the main Argentine cotton cropping area was always lower than expected (E. Cosenzo pers. comm.).
[FIGURE 2 OMITTED]
In South America, the BW tends to disperse during late summer and early fall matching the end of the cotton season, and is favored by high wind speeds. The average highest wind speeds observed in Argentina, Brazil and Paraguay are from the NE and N directions and they've had a significant influence on BW dispersal from infested areas (Ravelo et al., 2001). As described by several authors, the highest BW trapping catches where reached after cotton harvest, which is coincident with the massive migration of BWs from southern Paraguay to Argentina (Misiones and Formosa provinces) in the fall (Gomez et al., 1996; dos Santos, W. J., 2000; Gomez et al., 2000). The unusual behavior of upwind movement, over short distances, of large numbers of weevils from Paraguay into non-cotton areas into Misiones (Fig. 2) since 1996, can be understood under the light of ShowleCs (2006) work. This author showed that BWs survive better in citrus orchards than in other habitats during the winter and that such habitats are examples of overwintering <<hot spots>> in the sub-tropical Lower Rio Grande Valley of Texas. Cotton harvest in Paraguay (March, April) causes BWs to search for alternative food sources (Guerra, 1986), as well as for overwintering refuges. Also, cotton harvest overlaps with late citrus orchard ripening in Misiones and Corrientes (Argentina). Therefore, the atypical upwind (northeast) movement of weevils from harvested cotton fields in Paraguay observed since 1996, reinforces ShowleCs (2006) statement on the attractiveness of citrus orchards volatiles to the BW.
The BW invaded Brazil in 1983, from where it moved southwest and arrived in Paraguay in 1991, in Argentina in 1993 and finally in Bolivia in 1999. In August 2006, the BW reached the epicenter of the argentine cotton cropping area (27[degrees] S) (Fig. 1). Since its introduction in Sao Paulo in 1983, the BW has moved approximately 1400 km southwest. The remarkable upwind (North-East) movement of weevils from harvested cotton fields in Paraguay to Misiones-Argentina (Fig. 2), where no cotton is grown, suggests that BWs are attracted to citrus orchards volatiles and that such habitats are probably overwintering areas.
The variability in responsiveness of the BW to environmental factors is due partly to genetic variation and partly to variations in the developmental plasticity of phenotype structure that arise during individual development influenced by inputs from the environment, like temperature, photoperiod and food availability (West-Eberhard, 2005). Variability in responsiveness to environmental cues permits the BW to go through several overlapping generations during the cotton growing season, to develop in squares as well as in bolls, to adjust its developmental time from egg to adult to a broad time range, to migrate and disperse when the conditions are unfavorable, to feed on pollen from different botanical families as well as from non pollen food sources. External factors have a major developmental effect on the BW, which allows for variable life spans. Thanks to this, this insect is able to thrive in various environments differing in food availability and climate. These are all critical attributes that make the BW a great survivor, and a dangerous economic pest (Coad, 1915; Horton and Ellis, 1997).
Because the BW can profit in an opportunistic way from pollen of very different botanical families as well as from other plant structures like endocarps of prickly pear, grape fruit and oranges, BW migration routes seem to be independent of possible <<floristic corridors>> connecting different cotton cropping areas in South America. It remains necessary to determine if Cienfuegosia is a reproductive host for the BW experimentally in order to establish if BWs migrating great distances between cotton cropping sites, do reproduce on wild hosts or if they do so exclusively on cotton.
Determined efforts were made by various investigators to establish principles and techniques to control the BW. Experience has shown that no efficient biocontrol agents are available at the moment and total dependence on insecticides is a non effective and expensive form of BW control. Also, erradication technologies as those utilized in the US BW eradication program are not feasible in Paraguay and Argentina due to the large number of smallholders with less than 3 ha plots, distributed erratically in the forest, producing cotton as a cash crop, and based on rudimentary technology. In this scenario only an integration of cultural and chemical tactics will provide effective control. These cultural methods involve the management of overwintering habitat, stalk destruction, uniformly delayed cotton planting, early crop termination, the use of resistant cotton varieties and chemical control of diapausing BWs. The arrival of the BW to the epicenter of the argentine cotton cropping area in August 2006, reinforced the fact that the BW should finally be included in an integrated cotton pest management program jointly with other major cotton pests common in Argentina and Paraguay such as the pink boll worm [(Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae)], the boll worm complex (Spodoptera-Heliothis) and the leaf worm [Alabama argillacea (Hubner) (Lepidoptera: Noctuidae)].
After its introduction to Sao Paulo-Brazil in 1983, the BW has moved approximately 1400 km southwest reaching the centre of the Argentine cotton cropping area (27[degrees] S) in August 2006. From there, the BW has spread towards the southwest at an average of 61 km year-1 between Sao Paulo and Cte. Fernandez, Chaco-Argentina. The same speed was observed during the dispersal of the pest from the north to the south of Paraguay. However, the BW didn't move as fast as expected from SW Paraguay to the centre of the Argentine cotton cropping area (Cte. Fernandez-Chaco) between 1995 and 2006. It took the BW approximately ten years to move 250 km. This slower progress was probably the result of control measures in the framework of the BW eradication program developed by the Argentine government.
The arrival of the BW at the center of the Argentine cotton cropping area and the cotton cropping scenarios in Paraguay and Argentina reinforces the fact that the BW should finally be included in an integrated cotton pest management program jointly with other major cotton pests.
This work was supported by CONICET Grant No 001857/05. We thank to Dr. Marcelo F. Tognelli (IADIZA-CRICyT-CONICET) for his assistance in map referencing.
1. ABLES, J. R, J. L. GOODENOUGH & A. W. HARTSTACK. 1 983. Entomophagous arthropods. In: R. L. Ridgway, E. P. Lloyd & W. H. Cross (eds.), Cotton insect management with special reference to the boll weevil, USDA ARS Agr. Handbook, Misc. Publ. no. 589, pp. 103-127.
2. BECK, D. 1980. Insect Photoperiodism. Academic press Inc., New York.
3. BELL, M. R. 1983. Microbial Agents. In: R. L. Ridgway, E. P. Lloyd & W. H. Cross (eds.), Cotton insect management with special reference to the boll weevil, USDA ARS Agr. Handbook, Misc. Publ. no. 589, pp. 103-127.
4. BENEDICT, J. H., D. A. WLOFENBARGER, V. M. BRYANT JR. & M. GEOERGE. 1991. Pollen ingested by boll weevils (Coleoptera: Curculionidae) in southern Texas and northeast Mexico. J. Econ. Entomol. 84: 126-131.
5. BOTTRELL, D. G. 1983. The ecological basis of boll weevil (Anthonomus grandis Boheman) management. Agr. Ecosyst. and Envir. 10: 247-274.
6. BRAGA SOBRINHO, R. & M. J. LUKEFAHR. 1984. Ocurrencia de diapausa no picudo do algodoneiro Anthonomus grandis Boheman, na regiao nordeste do Brasil. In: Resumos IX Congreso Brasileiro de Entomologia, Londrina, Brasil. Sociedad Entomologica do Brasil: 19.
7. BRAGA SOBRINHO, R. 2000. Situacion y perspectivas para el control del picudo del algodonero. In: Workshop Proceedings III International Workshop on <<Integrated Pest Management of the Cotton Boll Weevil in Argentina, Brazil and Paraguay>>, 5-7 September 1999, Riberao Preto-Brazil, pp. 11-30.
8. BURKE, H. R., W. E. CLARK, J. R. CATE & P. A. FRYXELL. 1986. Origin and dispersal of the boll weevil. Bull. Entomol. Soc. Am. 32: 228-238.
9. CASWELL, H. 1983. Phenotypic plasticity in life-history traits: Demographic effects and evolutionary consequences. Am. Zool. 23:35-46.
10. CATE, J. R. & J. SKINNER. 1978. Fate and identification of pollen in the alimentary tract of the boll weevil (Anthonomusgrandis Boh.). Southwest. Entomol. 3: 263-265.
11. CATE, J. 1996. Strategies for management of the cotton boll weevil. In: Workshop Proceedings <<Integrated Pest Management of the Cotton Boll Weevil in Argentina, Brazil and Paraguay>>, 11-15 September 1995, Londrina, Brazil, pp. 10-17.
12. COAD, B. R. 1915. Relation of the Arizona wild cotton weevil to cotton plantings in the arid best. U.S. Dep. Agric. Bull. 233.
13. COSENZO, E., C. RAMIREZ & E. STEGER. 2001. Situacion del Programa Nacional de Prevencion y Erradicacion del Picudo del Algodonero (PNPEPA) y su proyeccion regional. In: Proceedings of the <<Cotton in the Southern Cone --Project on Integrated Pest Management of the Cotton Boll Weevil in Argentina, Brazil and Paraguay CFC/ICAC/04, PART 1, pp. 178-200.
14. CROSS, W. H., M. J. LUKEFAHR, P. A. FRYXELL, & H. L. BURKE. 1975. Host plants of the boll weevil. Environ. Entomol. 4: 19-26.
15. CUADRADO, G. A. & S. S. GARRALLA. 2000. Plantas Alimenticias Alternativas del Picudo del Algodonero (Anthonomus grandis Boh.) (Coleoptera: Curculionidae) en la Provincia de Formosa, Argentina. Analisis Palinologico del Tracto Digestivo. An. Soc. Entomol. Brasil 29: 245-255.
16. CUADRADO, G. A. 2002. Anthonomus grandis Boheman (Coleoptera: Curculionidae) en la zona central y sur oeste de Misiones, Argentina: Polen como fuente alimenticia y su relacion con el estado fisiologico en insectos adultos. Neotropical Entomol. 31(1): 121-132.
17. CUSHMAN, R. A. 1911. Studies in the biology of the boll weevil in the Mississippi Delta region of Louisiana. J. Econ. Entomol. 4: 432-448.
18. DEGRANDE, P. E. 1991. Aspectos biologicos do bicudo. In: Bicudo do algodoneiro: Manejo Integrado. UFMS/EMBRAPA-UEPAE Dourados, pp. 11-28.
19. DiNGlE, H. 1972. Migration strategies of insects. Science 175: 1327-1335.
20. DINGLE, H. 1974. Diapause in a migrant insect, the milkweed bug Oncopeltus fasciatus (Dallas) (Hemiptera: Lygaeidae). Oecologia 17: 1-10.
21. dos SANTOS, W. J. & A. M. MENEGUIM. 1996. Biologia, comportamento e dinamica populacional do bicudo do algodoneiro Anthonomus grandis Boh. In: Workshop Proceedings <<Integrated Pest Management of the Cotton Boll Weevil in Argentina, Brazil and Paraguay>>,11-15 September 1995, Londrina, Brazil, pp. 100-107.
22. dos SANTOS, W. J. 2000. Ocorrencia e distribucao do bicudo Anthonomus granais, em areas cultivadas com o algodoneiro. In: Workshop Proceedings III International Workshop on <<Integrated Pest Management of the Cotton Boll Weevil in Argentina, Brazil and Paraguay>>, 5-7 September 1999, Riberao Preto, Brazil, pp 79-86.
23. dos SANTOS, W. J. 2001. Manejo de insecticidas para o controle do bicudo. In: Proceedings of the <<Cotton in the Southern Cone--Project on Integrated Pest Management of the Cotton Boll Weevil in Argentina, Brazil and Paraguay CFC/ ICAC/04>>. Part 1, 26-28 June 2001, Fortaleza-Brazil>>, pp. 242-248.
24. DURAN PARADA, D. 2000. Situacion y programa de prevencion y erradicacion del picudo mexicano en Bolivia. In: Workshop Proceedings III International Workshop on <<Integrated Pest Management of the Cotton Boll Weevil in Argentina, Brazil and Paraguay>>, 5-7 September 1999, Riberao Preto, Brazil, pp. 135-137.
25. EARLE, N. W. & L. D. NEWSTON. 1964. Initiation of diapause in the boll weevil. J. Insect Physiol. 10: 131-139.
26. GOMEZ, V. A., D. PESSOLANI, & M. SANABRIA. 1996. Estudio preliminar de la fluctuacion del picudo Antononomus granais Boh. en el region de Chore, Dto. San Pedro. In: Workshop Proceedings <<Integrated Pest Management of the Cotton Boll Weevil in Argentina, Brazil and Paraguay>>, 11-15 September 1995, Londrina, Brazil, pp. 115-118.
27. GOMEZ, V. A., D. PESSOLANI, E. GOMEZ, & M. SANABRIA. 2000. Movimiento poblacional del picudo del algodonero en zonas del Paraguay. In: Workshop Proceedings III International Workshop on <<Integrated Pest Management of the Cotton Boll Weevil in Argentina, Brazil and Paraguay>>, 5-7 September 1999, Riberao Preto, Brazil, pp. 87-92.
28. GRAHAM, H. M., N. S. HERNANDEZ JR., J. R. LLANES & J. TAMAYO. 1 979. Seasonal incidence of diapause in boll weevil populations in the boll weevil in the Lower Rio Grande Valley of Texas. Southwest. Entomol. 4: 170-175.
29. GROSSMAN, E. F. 1928. Resumption of egg-laying by hibernated cotton boll weevils (Anthonomus grandis Boh.). Fla. Entomol. 12: 33-38.
30. GUERRA, A. A., R. D. GARCIA & J. A. TAMAYO. 1982. Physiological activity of the boll weevil during the fall and winter in subtropical areas of the Rio Grande Valley of Texas. J. Econ. Entomol. 75: 11-15.
31. GUERRA, A. A. 1986. Boll weevil movement: dispersal during and alter the cotton season in the Lower Rio Grande Valley of Texas. Southwest. Entomol. 11: 10-16.
32. HABIB, M. E. M. & W. D. FERNANDES. 1983. Anthonomus grandis Boheman (Curculionidae) ja esta na lavoura algodoneira do Brasil. Rev. Agric. 58: 74.
33. HORTON, D. L. & H. C. ELLIS. 1997. Weevils and Borers. In: Hudson, R. D. & D. B. Adams. 1997. A County Agent's Guide to Insects Important to Agriculture in Georgia. Entomology 97, RDH (1). Univ. of GA, Col. Ag. Env. Sci, Coop. Ext. Serv., Tifton, GA 31793. http://www.bugwood.org/ factsheets/acrobat/99001.pdf
34. HUNTER, W. D. & W. D. PRICE. 1912. The Mexican boll weevil: a summary of the investigations of this insect up to Dec. 31,1911. U.S. Senate Doc. No 305, 118 pp.
35. HUNTER, W. D. & B. R. COAD. 1923. The boll weevil problem. USDA Farmers Bull 1329: 2-3.
36. ISHIHARA, M. 1999. Adaptive phenotypic plasticity and Its difference between univoltine and multivoltine populations in a bruchid beetle, Kytorhinus sharpianus. Evolution. 53: 1979-1986.
37. ISLEY, D. 1932. Abundance of the boll weevil in relation of summer weather and to food. Arkansas Agr. Exp. Sta. Bull. 271: 54-55.
38. JOHNSON, W. L., W. H. CROSS, J. E. LEGGET, W. L. MCGOVERN, H. C. MITCHELL & E. B. MITCHELL. 1975. Dispersal of marked boll weevil: 1970-1973 studies. Ann. Entomol. Soc. Am. 68: 1018-1022.
39. JONES, R. W., J. R. CATE, E. MARTINEZ HERNANDEZ & E. SALGADO SOSA. 1993. Pollen feeding and survival of the boll weevil (Coleoptera: Curculionidae) of selected plant species in northeastern Mexico. Environ. Entomol. 22: 99-103.
40. KEELEY, L. L., D. S. MOODY, D. LYNN, R. L. JOINER & S. B. VINSON. 1977. Succinate-cytochrome c reductase activity and lipids in diapause and non diapause Anthonomus grandis from different latitudes. J. Insect Physiol. 23: 231-234.
41. KENNEDY, J. S. 1961. A turning point in the study of insect migration. Nature. 189: 785-791.
42. KRAPOVICKAS, A. 2000. El genero Cienfuegosia y el <<picudo del algodonero>> al sur del tropico, en Sudamerica. In: Workshop Proceedings III International Workshop on <<Integrated Pest Management of the Cotton Boll Weevil in Argentina, Brazil and Paraguay>>, 5-7 September 1999, Riberao Preto, Brazil, pp. 43.
43. LEATHER S. R., K. F. A. WALTERS & J. S. BALE. 1993. The ecology of insect overwintering. Cambridge University Press, Cambridge.
44. LUKEFAHR M. J., S. BARBOSA & R. BRAGA SOBRINO. 1986. Plantas hospedeiras do picudo com referencia especial a flora brasileira. In: Barbosa, S., Lukefahr M. J. & Braga Sobrino, R. O bicudo do algodoneiro. EMBRAPA--DDT/ Brasil, Doc no 4, pp. 275-285.
45. McKIBBEN, G. H., M. J. GRODOWITZ & E. J. VILLAVASO. 1988. Comparison of flight ability of native and two laboratory-reared strains of boll weevils (Coleoptera: Curculionidae) on a flight mill. Environ. Entomol. 17: 852-854.
46. McKIBBEN, G. H., J. L. WILLERS, J. W. SMITH & T. L. WAGNER. 1991. Stochastic model for studying boll weevil dispersal. Environ. Entomol. 20: 1327-1332.
47. MARENGO LOZADA, R. M., L. A. ALVAREZ & W. H. WHITHCOM. 1987. El picudo mejicano del algodonero (Anthonomus granais Boh.). El desafio para la produccion algodonera en el Paraguay. Ministerio de Agricultura y Ganaderia [Asuncion-Paraguay]. Misc. No 118.
48. MARENGO LOZADA, R. M., & W. H. WHITHCOM. 1993. Hospederas alternantes del picudo mejicano del algodonero (Anthonomus granais Boh.). Ministerio de Agricultura y Ganaderia [Asuncion-Paraguay].
49. MOODY, D. S., D. G. BOTTRELL & D. R. RUMMEL. 1993. Late season migration of the boll weevil in the Texas Rolling Plains. Southwest. Entomol. 18: 1-10.
50. MULLER H. J. 1970. Formen der Dormanz bei Insekten. Nova Acta Leopold. 35: 7-27.
51. PIEROZZI Jr. I. 1 985. Ecologia aplicada de Anthonomus grandis Boheman, 1843 (Coleoptera : Curculionidae), na regiao de Campinas, SP. Tese de Maestrado UNICAMP, Campinas, SP, Brazil.
52. RAINEY, R. C. 1977. Rainfall: scarce resource in <<opportunity country>>. Phil. Trans. R. Soc. (B), 278 : 439-455.
53. RANKIN, M. A. 1974. The hormonal control of flight in the milkweed bug, Oncopeltus fasciatus. In: Barton Browne, L. (ed.) Experimental analysis of insect behaviour. Springer, Berlin-Hidelberg-New York, pp. 317-328.
54. RANKIN, M. A. & L. M. RIDDIFORD. 1977. The hormonal control of migratory flight in Oncopeltus fasciatus: The effects of the corpus cardiacum, corpus allatum and starvation on migration and reproduction. Gen. and Com. Endocrinology 33: 309-321.
55. RANKIN, M. A., HAMPTON, E. N. & SUMMY, K. R. 1994. Investigations of the oogenesis-flight syndrome in Anthonomus grandis (Coleoptera: Curculionidae) using tethered flight tests. J. Insect Behav. 7(6): 795-810.
56. RAVELO, A. C., M. GRILLI & J. A. SANTA. 2001. Monitoreo del picudo del algodonero mediante utilizacion de informacion satelital y terrestre. In: Proceedings of the <<Cotton in the Southern Cone-Project on Integrated Pest Management of the Cotton Boll Weevil in Argentina, Brazil and Paraguay CFC/ICAC/04>>, PART 1, 26-28 June 2001, Fortaleza, Brazil, pp. 215-224.
57. RETZLAFF, V. E. 1998. Programa nacional de prevencion y erradicacion del picudo del algodonero en Argentina. In: Workshop Proceedings II International Workshop on <<Integrated Pest Management of the Cotton Boll Weevil in Argentina, Brazil and Paraguay>>, 3 December 1997, Pres. R. S. Pena, Chaco, Argentina, pp. 31-39.
58. RUMMEL, D. R., J. R. WHITE & G. R. PRUITT. 1978. A wild feeding host of the boll weevils in west Texas. Southwest. Entomol. 3: 171-175.
59. SHOWLER, A. T. 2004. Influence of cotton fruit stages as food sources on boll weevil (Coleoptera: Curculionidae) fecundity and oviposition. J. Econ. Entomol. 97: 1330-1334.
60. SHOWLER, A. T. 2006. Short-range dispersal and overwintering habitats of the Boll Wevils (Coleoptera : Curculionidae) during and after harvest in the Subtropics. J. Econ. Entomol. 99: 1152-1160.
61. SHOWLER, A. T. & V. ABRIGO. 2007. Common subtropical and tropical nonpollen food sources of the boll weevil (Coleoptera: Curculionidae). Environ. Entomol. 36(1): 99-104.
62. SOUTHWOOD, T. R. E. 1962. Migration of terrestrial arthropods in relation to habitat. Biol. Rev. 37: 171-214.
63. STADLER, T. 2001. Integrated Pest Management of the Cotton Boll Weevil in Argentina, Brazil and Paraguay CFC/ICAC/04. Techncial Paper No 16. Common Fund for Commodities.
64. STENGEL, M. & G. SCHUBERT. 1970. Role des corpora allata dans le comportement migrateur de la femelle de Melolontha melolontha L. (Coleoptera: Scarabeidae). C. R. Hebd. Seanc. Sci., Paris (D) 270: 181-184.
65. STERLING, W. L. & P. L. ADKISSON. 1971. Seasonal biology of the Boll Weevil in the high and rolling plains of Texas as compared with previous biological studies of this insect. TexasAgric. Exp. Stn. P-993: 12 pp.
66. TAUB-MONTEMAYOR, T. E., PALMER, J. O. & RANKIN., M. A. 1997. Endocrine regulation of reproduction and diapause in the Boll Weevil, Anthonomus grandis Boheman. Arch Insect Biochem. 35: 455-477.
67. TAUBER, M. J. & C. A. TAUBER. 1976. Insect seasonality: Diapause maintenance, termination, and postdiapause development. Annu. Rev. Entomol. 21: 81-107.
68. TAUBER, M. J., C. A. TAUBER & S. MASAKI. 1986. Seasonal adaptations of insects. Oxford University Press, Oxford.
69. TUMLINSON, J. H., D. D. HARDEE, R. C. GUELDNER, A. C. THOMPSON, P. A. HEDIN & J. P. MINYARD. 1969. Sex pheromones produced by male boll weevil: Isolation, identification and synthesis. Science. 166: 1010-1012.
70. WAGNER, T. R, VILLAVASO, E. J. & WILLERS, J. L.1999. Diapause in the Boll Weevil (Coleoptera: Curculionidae): Life stage sensitivity to environmental cues. Ann. Entomol. Soc. Am. 92: 396-402.
71. WALKER, J. K. Jr. & G. A. NILES. 1971. Population dynamics of the boll weevil and modified cotton types: Implications for pest management. Texas Agric. Exp. Sta. Bull. 1109: 21-24.
72. WEST-EBERHARD, M. J. 2005. Developmental plasticity and the origin of species differences, PNAS, May 3, 2005, vol. 102, Suppl. 1: 6543-6549.
73. WHITE, J. R. & D. R. RUMMEL. 1978. Emergence profile of overwintered boll weevils and entry into cotton. Environ. Entomol. 7: 7-14.
74. WOLFENBARGER, D. A., H. M. GRAHAM, R. D. PARKER & J. W. DAVIS. 1976. Seasonal patterns of boll weevil response to traps baited with grandlure in the lower Rio Grande Valley. Tex. Agric. Exp. Stn. Res. Monogr. 8: 20-25.
STADLER, Teodoro * and Micaela BUTELER **
* Laboratorio de Investigaciones y Servicios Ambientales Mendoza (LISAMEN) Centro Regional de Investigaciones Cientificas y Tecnologicas (CRICYT-CONICET) Av. Ruiz Leal S/N Parque General San Martin, CC. 131, M 5500 IRA, Mendoza, Argentina; e-mail: email@example.com
** Department of Land Resources and Environmental Sciences, Montana State University, 334 Leon Johnson Hall, Bozeman 59717, Montana, USA; e-mail: firstname.lastname@example.org