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1 March 2011 Egg Parasitoids Attacking Cactoblastis cactorum (Lepidoptera: Pyralidae) in North Florida
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Abstract

Interest in the natural enemies of Cactoblastis cactorum (Berg) has increased since the moth was found in Florida in 1989. Previous surveys for natural enemies in Argentina identified egg parasitoids in the family Trichogrammatidae as potentially important control agents of C. cactorum. A study was conducted in north Florida to identify and to assess occurrence of egg parasitoids attacking this invasive moth in its new homeland. Surveys undertaken at 6 locations in north Florida from Jul 2008 to Dec 2009 revealed that eggsticks of C. cactorum were attacked by egg parasitoids from the Trichogramma genus: T. pretiosum Riley, T. fuentesi Torre, and an additional unidentified Trichogramma species belonging to the T. pretiosum group. In order to assess the importance of these egg parasitoids, the fate of individual C. cactorum eggsticks was determined during weekly visits to each site. This assessment showed that the combined level of parasitism of C. cactorum eggsticks was very low with less than 0.2% of host eggs attacked at any one of the 6 sites. While parasitoids attacked smaller eggsticks, there was no correlation between the numbers of eggs in an eggstick attacked with increasing number of eggs/eggstick. Comparing the mean number of eggs/eggstick, there was no difference between the 3 flight periods of C. cactorum, but there was a difference between the 6 sites. Based on these results, the use of Trichogramma wasps as an inundative biological control agent, complementary to the Sterile Insect Technique application, is discussed.

The cactus moth, Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae), is often cited as the perfect example of a successful weed biological control agent (Moran & Zimmermann 1984). In 1925, the cactus moth was introduced from its native Argentina into Australia to control prickly pear cactus, Opuntia spp., which had originally been brought into Australia for commercial purposes (Dodd 1940; Mann 1970). The cactus had become invasive and made large tracts of rangeland unfit for grazing cattle. Within a few years after the introduction of C. cactorum into Australia, US $6 million worth of rangeland was restored, equivalent to more than US $60 million in today's dollars (Dodd 1940; Williamson 2009). Based on these promising results, C. cactorum was imported from Australia to South Africa, Mauritius, and Hawaii to manage other non-native and invasive Opuntia spp. (Moran & Zimmermann 1984). In 1957, C. cactorum was introduced into several Caribbean islands (Nevis, Montserrat, and Antigua) to control non-native as well as native Opuntia spp. (Simmonds & Bennett 1966). Unfortunately, the implementing agencies did not fully consider the potentially injurious environmental impacts of C. cactorum if this insect were to move to neighboring countries where some species of Opuntia are important native species and some are commercially important (Stiling et al. 2004).

The first record of C. cactorum in the U.S. was from Bahia Honda Key, Florida, in Oct 1989 (Dickel 1991). It is uncertain how the moth arrived in Florida, but several interceptions of Caribbean ornamental Opuntia spp. infested with C. cactorum were found at ports of entry in south Florida during the 1980s and 1990s (Pemberton 1995; Zimmermann et al. 2001; Stiling 2002; Simonsen et al. 2008). Since its appearance in Florida, C. cactorum has become a threat to native Opuntia spp. in North America. Current management options include the use of Pherocon 1-C Wing traps (Trécé Incorporated, Salinas, CA) baited with a 3-component synthetic sex lure (Suterra, LLC, Bend, OR) to identify the presence of the moth, coupled with removal of infested plants to reduce C. cactorum populations (Bloem et al. 2005; Hight & Carpenter 2009). Complementary to the detection, monitoring, and removal efforts, implementation of the Sterile Insect Technique (SIT) is being used to slow the geographic expansion of C. cactorum in the U.S. (Hight et al. 2002; Bloem et al. 2005; Bloem et al. 2007). In Mexico, localized invasions of C. cactorum on 2 islands were eradicated in 2008 with a program of pheromone traps, host removal, and SIT (NAPPO 2006; NAPPO 2008; NAPPO 2009).

Bennett & Habeck (1995) suggested biological control as an additional control option that should be considered for C. cactorum. Pemberton & Cordo (2001) reported that several larval and pupal parasitoids attacked the cactus moth in South America, including species of Hymenoptera (Braconidae, Chalcidae, and Ichneumonidae), and 1 Diptera (Tachinidae). They also reported on 2 chalcid species (Brachymeria ovata (Say) and B. pedalis Cresson) and 1 unidentified egg parasitoid from the family Trichogrammatidae attacking C. cactorum in Florida. Logarzo et al. (2008) found the larval parasitoid Apanteles alexanderi Brethes (Hymenoptera: Braconidae) and the egg parasitoid Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae) attacking C. cactorum in Argentina.

Trichogrammatid egg parasitoids have been used successfully for inundative biological control against major lepidopteran pests such as corn borers, sugarcane borers, and cotton bollworm (Li-Ying 1994; van Lenteren 2000). Egg parasitoids are easy to rear in mass quantity in laboratory conditions and to release over wide areas. Biological control can be used to complement and synergize the application of SIT (Gurr & Kvedaras 2010). Recent studies showed that the combination of both techniques was more efficient in controlling pest population of the codling moth, Cydia pomonella (L.) (Bloem et al. 1998). Synergistic interactions between SIT and fruit fly biological control with parasitoids increased the suppression of pest fruit flies, even leading to eradication (Sivinski 1996; Rendon et al. 2006). SIT and biological control have been successfully combined to combat several lepidopteran pests, including C. pomonella (Bloem et al. 1998) and painted apple moth, Orgyia anartoides (Walker) (Suckling et al. 2007). Radiation doses for sterilizing C. cactoblastis adults have been determined to produce partially sterile but more fit males which, when mated with wild females, generate sterile offspring (Carpenter et al. 2005). The combination of egg parasitoid releases and SIT has the advantage that parasitoids manage high pest densities, while SIT works best at low pest densities. In addition, release of sterile insects provides an egg resource for egg parasitoids increasing the ratio of natural enemies to adult hosts. Egg parasitoids and sterile insects have the characteristic of being self dispersing and consequently are able to cover wide areas (Sivinski 1996).

We conducted field surveys in order to identify egg parasitoids already established in North Florida that attack C. cactorum. Cactoblastis cactorum adults have 3 annual flight periods in north Florida (Apr–May, Jul–Aug, and Oct–Nov) (Hight et al. 2005; Hight & Carpenter 2009). We report on the distribution, seasonality, and parasitism parameters of the Trichogramma species attacking C. cactorum in northern Florida. The number of eggs/eggstick was compared between different flight periods and sites to assess host egg resource for egg parasitoids. The effect of C. cactorum eggstick size on level of parasitism was evaluated by comparing number of eggs from parasitized versus un-parasitized eggsticks. These data will be beneficial in promoting discussions on possible implementation of biological control for the cactus moth and, in particular, assessing the potential of an inundative biological control program against C. cactorum in North America.

MATERIALS AND METHODS

Field surveys were carried out at 6 locations (Fig. 1) in north Florida from Jul 2008 to Dec 2009. The selection of study sites was based on existing records of infestations from the literature, personal observations from preliminary surveys, and information provided by experts. Female C. cactorum place their eggs end to end to form a chain that looks like a short “stick”, and the egg mass is referred to as an eggstick. Although no extensive field surveys were conducted from May to Jul 2008 at St. Marks and St. George Island, eggsticks with eggs that appeared parasitized were collected and held in laboratory conditions until parasitoids emerged. At survey locations, 20 to 30 healthy Opuntia spp. plants were chosen with no to minor feeding damage by cactus moth larvae and an average of at least 50 pads per plant. During weekly visits throughout all 3 flight periods, any new eggstick was identified by plant, pad, and its general location on the plant so the eggstick could be found during subsequent checks. A mark was made on the plant at the base of the eggstick with a felt tip pen and a red tape “flag” affixed to an insect pin placed near the eggstick to aid in finding the eggstick. The flag was labeled with a unique number to identify each eggstick. The oviposition preferences of C. cactorum females on host plants were recorded by classifying the attachment of the eggstick to either a glochid at an areole, to a spine, or on the fruit. Observations on plant habitat and host eggstick distribution within the surveyed site and within the selected plant were collected to provide additional information on the host finding behavior of egg parasitoids. The number of eggs per eggstick was determined either by a direct count or by a correlated estimate of eggstick length to egg number (2.62 ± 0.013 eggs/mm). The ratio of eggstick length to egg number was calculated in this study by counting the number of eggs in a segment of eggstick, replicated on 20 eggsticks. Eggstick length was estimated in situ by placing a plastic string next to the eggstick and cutting a piece of equivalent length. The length of the piece of string was then measured to the nearest 0.01 mm with a metric micrometer. Measurements of eggsticks were obtained so that the number of eggs per eggstick could be estimated if the eggstick was lost before it could be collected and directly counted. The fate of each eggstick was determined by making weekly visits to each site to evaluate the status of previously tagged eggsticks. The fate of each eggstick was categorized as follows: eggstick lost; predated (visible chewing damage) eggs in the eggstick versus non predated eggs; or parasitized eggs in the eggstick (black eggs formed before C. cactorum larvae successfully developed). Eggsticks were collected if they were damaged during evaluation or measurement, eggs of the eggstick had hatched, or eggs appeared predated or parasitized. Eggsticks with viable eggs were collected and held in small plastic cups (30 mL) under laboratory conditions (25 ± 1 C°, 16:8 L:D and 40–60% RH) to record hatch rate. Eggsticks with parasitized eggs were collected and monitored in the laboratory to determine the emergence rate, number of eggs/eggstick attacked by parasitoids, number of parasitoids emerging per parasitized egg, and to ascertain the identity of the parasitoids. Parasitoid specimens were submitted to R. Stouthamer, Department of Entomology, University of California, Riverside, for molecular identification. The sequencing of ribosomal DNA Internal Transcribed Spacer 2 (ITS 2) was used to identify the different species of egg parasitoids.

Fig. 1.

Locations and their coordinates surveyed for egg parasitoids of Cactoblastis cactorum in North Florida.

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Data Analysis

The numbers of eggs/eggstick at different flight periods for each surveyed location and the average number of eggs/eggstick at each site were log transformed before analyses to satisfy the assumptions of the analysis of variance. One way analysis of variance (PROC GLM) was applied to the log transformed data and the separation of means was made with the least significant difference (LSD) test. Comparison of number of eggs/eggstick that was parasitized versus number of eggs/eggstick not parasitized was also evaluated with a one-way analysis of variance (PROC GLM). Since only a few eggsticks with parasitized eggs were collected in this study (see text below), comparisons between eggsticks with parasitized eggs were made against the same number of randomly selected eggsticks with un-parasitized eggs. Variation between the number of eggs for parasitized eggsticks and the number of eggs for the randomly selected un-parasitized eggsticks was analyzed by a folded F test (Davis 2007). Because the variances in numbers of eggs for eggsticks with parasitism and number of eggs in eggsticks without parasitism were not significantly different, means of these 2 groups were compared with a two-sample t-test. A Pearson's Correlation Coefficient (r) was calculated to determine whether the numbers of eggs parasitized were dependent on the number of eggs/eggstick. The SAS Statistical Software Version 9.2 (SAS Institute, Cary North Carolina) was used to perform the statistical analyses. Estimates of central tendencies were reported as mean ± standard error of mean.

RESULTS AND DISCUSSION

Although host plant species of Opuntia stricta (Haworth) Haworth, O. humifusa (Rafinesque) Rafinesque, and O. ficus-indica (L.) P. Miller varied among the different geographic regions surveyed, the oviposition preferences of C. cactorum females was similar on the various species (Table 1). In this study, parasitized eggsticks of C. cactorum appeared mostly on the areole/glochid structure of the pads (Table 1).

Altogether, 1,527 eggsticks with 91,013 C. cactorum eggs, not including 344 eggsticks missing from the field or lost during collection, were tagged on plants of Opuntia spp. (Table 2). Of all the eggsticks checked, 62% were collected on Okaloosa Island and had a mean of 59 (+/- 1.83) eggs/eggstick. The proportion of eggsticks examined in the laboratory as percentage of all eggsticks surveyed at the 6 field sites ranged from 53 to 100%, except for summer 2008 at St. George Island and St. Marks National Wildlife Refuge (NWR) in which only 30% and 24%, respectively, of the monitored eggsticks were examined (Table 2). The majority of the eggsticks from these 2 locations for this flight period were recorded as lost (Table 2). The cause for this high number of lost eggsticks is not clear. Several biotic and abiotic factors could have contributed to the high number of lost eggsticks. During summer 2008, 23% of eggsticks examined from St. Marks had eggs that were preyed upon compared with less than 3% in other locations. Although not directly observed at St. George Island or St. Marks, substantial predation of C. cactorum eggs by ants has been recorded in South Africa (Robertson 1984). Because the plants surveyed at St. Marks were located within 100 m of the waters of the Gulf of Mexico, strong winds characteristic of coastal regions could have knocked eggsticks off the plants. All other study sites were along the Gulf Coast; in none of them were the plants as close to the water as at St. Marks. In addition, heavy rainfall may have separated the eggsticks from plants, but we do not have any data on the severity of the rain storms at different study sites. Cactoblastis cactorum life table studies in Argentina (Logarzo et al. 2009) and South Africa (Robertson & Hoffmann 1989) identified rain and wind as major factors contributing to mortality of eggs.

Surveyed sites and oviposition periods were analyzed to evaluate their influence on number of eggs/eggstick. Eggsticks were collected for multiple oviposition periods at 3 sites (St. George Island, St. Marks, and Okaloosa Island) (Table 2). The numbers of eggs/eggsticks for the different oviposition periods were not significantly different for St. George Island (F = 1.84, df = 1, P = 0.18), St. Marks (F = 93.86, df = 3, P = 0.07), or Okaloosa Island (F = 0.22, df = 3, P = 0.88). Because the numbers of eggs/eggstick for multiple oviposition periods were not different, eggsticks from all flight periods were pooled to calculate the means for those sites (St. George Island (62 ± 2.8), St. Marks (53 ± 2.8), and Okaloosa Island (59 ± 1.8)). The pooled eggsticks were used to compare the number of eggs/eggstick between all 6 sites and significant differences were found (F = 11.44, df = 5, P < 0.0001) (Table 2).

Female C. cactorum laid similar numbers of eggs/eggstick for each of the 3 oviposition periods but not at all 6 survey sites along the Florida panhandle. The longest eggsticks were observed at St. George Island, Pensacola Beach, and Okaloosa Island (Table 2). Significantly smaller eggsticks were recorded at St. Marks and Mexico Beach (Table 2). Panacea had significantly smaller number of eggs/eggstick than all other sites (Table 2). The cause of differences between eggsticks at the various sites was unclear. Studies in South Africa identified differences in total fecundity of C. cactorum due to host plant species, the flight period when eggs were laid, and the temperature during oviposition (Robertson 1989). We did not distinguish eggsticks collected from different host plants (Table 1). While South African female C. cactorum had significantly higher fecundity during the summer flight (Robertson 1989), our study did not show any difference in number eggs/eggstick between flight periods in north Florida. Cactoblastis cactorum has a tendency to oviposit on plants with high nitrogen (Myers et al. 1981; Robertson 1987), but we have no direct measurements of plant quality at our sites.

Comparing the number of eggs/eggstick for eggsticks that were parasitized (38 ± 13.7) (Table 3) against un-parasitized eggsticks (61 ± 13.1) revealed a significant difference (pooled t test = 3.14, df = 12, P = 0.0085). Although the number of eggs/eggstick was highly variable, the variation of the number of eggs/eggstick for parasitized versus the randomly selected un-parasitized group was similar (folded F test = 1.10, df = 6, P = 0.91), suggesting that the difference found between the two groups was not driven by unequal or extreme variation. However, there was not a significant correlation between the number of eggs/eggstick and number of eggs parasitized by Trichogramma spp. (n = 7, r = -0.16, P = 0.74). Therefore, while female Trichogramma spp. parasitized eggsticks with fewer eggs, they did not parasitize more eggs as the number of eggs in an eggstick increased. The average number of eggs parasitized in an eggstick was 9 (±5.8).

TABLE 1.

SITES SURVEYED IN NORTH FLORIDA FOR TRICHOGRAMMA EGG PARASITOIDS OF CACTOBLASTIS CACTORUM EGGSTICKS ON OPUNTIA SP. AND ADDITIONAL INFORMATION ON MOTH OVIPOSITION PREFERENCE.

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TABLE 2.

NUMBER OF CACTOBLASTIS CACTORUM EGGSTICKS COLLECTED, LOST IN THE FIELD, EXAMINED IN THE LABORATORY, AND MEAN NUMBER OF EGGS PER EGGSTICK ± SE AT DIFFERENT SITES IN NORTH FLORIDA FOR DIFFERENT OVIPOSITION PERIODS.

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TABLE 3.

LOCATION AND DATE PARASITIZED CACTOBLASTIS CACTORUM EGGSTICK WAS COLLECTED, IDENTITY OF PARASITOID SPECIES, NUMBER OF EGGS PER EGGSTICK, NUMBER OF PARASITIZED EGGS, NUMBER OF PARASITOIDS EMERGED, FEMALE RATIO, AND PARASITISM LEVEL OF EGG PARASITOIDS ATTACKING C. CACTORUM IN NORTH FLORIDA.

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Ten eggsticks were found parasitized at 3 of the 6 sites surveyed (Pensacola Beach, St. Marks, and Okaloosa Island). Five of the parasitized eggsticks were found at Okaloosa Island. Parasitized eggsticks were found during all 3 oviposition periods of C. cactorum females: the spring flight (St. Marks and Pensacola Beach), summer flight (Pensacola Beach), and fall flight (Okaloosa Island). Of the 496 eggs in the 10 parasitized eggsticks, a total of 89 eggs (or 18%) were parasitized, resulting in the emergence of 181 adult parasitoids with a sex ratio of 70% (±14) females (Table 3). The level of parasitism by Trichogramma spp., relative to the total number of eggs examined during the different flight periods for each site, was less than 0.2% of total C. cactorum eggs collected (Table 3). We did not observe any parasitized eggsticks at St. George Island, Mexico Beach, or Panacea.

Two species of Trichogramma were reared from C. cactorum eggsticks in north Florida (Table 3) and identified by differences in IST2 sequences. Trichogramma pretiosum was collected at St. Marks, Pensacola Beach, and Okaloosa Island, while T. fuentesi Torre was recovered only from Okaloosa Island. It was not possible to identify 2 collections of Trichogramma spp. from Okaloosa Island; one because a good molecular sequence could not be obtained and for the other the sequence was not in the database and possibly represents a new species in the T. pretiosum group (R. Stouthamer, UC—Riverside, personnel communication).

More than 15 million ha of agriculture and forestry worldwide are treated annually with Trichogramma egg parasitoids (van Lenteren 2000). Trichogrammatid wasps have been used successfully in inundative release programs against lepidopteran pests in greenhouses and crop production worldwide (Smith 1996). Inundative releases of Trichogramma spp. have been implemented in Florida to control major lepidopteran pests of collards, cabbages, soybeans, bell peppers, tomatoes, corn, and tobacco production (Martin et al. 1976). Trichogramma pretiosum is commonly found in the Western hemisphere. This Trichogramma species has been released commercially against major lepidopteran pests such as cotton leafworm (Alabama argillacea) (Hübner), corn earworm (Helicoverpa zea) (Boddie), tomato pinworm (Keiferia lycopersicella) (Walshingham), sugarcane borers (Diatraea spp.), and cabbage looper (Trichoplusia ni) (Hübner) (Pinto et al. 1986; Hassan 1993; Li-Ying 1994; Monje et al. 1999). Trichogramma fuentesi have been recorded in countries in South America (Argentina, Columbia, Mexico, Peru, and Venezuela) and in the U.S. (Alabama, California, Florida, Louisiana, New Jersey, South Carolina and Texas) (Fry 1989, Pinto 1999). Its primary hosts are species from the Noctuidae family such as H. zea and Heliothis virescens (F.) and from the Pyralidae family such as Diatrea saccharalis (F.), Ephestia kuehniella Zeller, and Ostrinia nubilalis (Hübner) (Fry 1989; Wilson & Durant 1991; Pintureau et al. 1999; Querino & Zucchi 2003). Trichogramma parasitoids also are widely used for pest control in orchards (Olkowski & Zang 1990). The observed low incidence of the wasps in natural areas might be explained by unfavorable environmental factors or natural plant chemicals (Smith 1996; Romeis et al. 1997, 1999). However, contrary to other natural enemies, Trichogramma can be easily and cheaply mass-reared for the implementation of an inundative biological control program.

The potential for inundative releases of Trichogramma spp. as a strategy against C. cactorum is currently being investigated with sustainable laboratory colonies of T. fuentesi originating from field collected insects reared from parasitized C. cactorum eggsticks. Biological characteristics (sex ratio, egg load, and longevity) and different behavioral mechanisms (influence of parasitoid age, density, and host age on parasitism) involved in host finding of T. fuentesi reared on C. cactorum eggs are being evaluated. The inundative releases of Trichogramma wasps could be integrated in the current pest management system based on SIT applications during the 3 flight periods by building Trichogramma populations. This field survey was useful in identifying a potential inundative biological control agent that could be integrated within a pest management strategy against C. cactorum.

ACKNOWLEDGMENTS

We thank Shalom Benton (FAMU) for field collection and laboratory assistance and Chris Albanese, Michael Getman, and John Mass (USDA-ARS-CMAVE, Tallahassee) for field assistance. We thank Stuart Reitz (USDA-ARS-CMAVE, Tallahassee, FL) and Jim Nation (University of Florida) for comments on earlier drafts of this manuscript. This work is funded under the FAMU-USDA APHIS Cooperative Agreement, 07-10-8100-0755-CA. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture.

REFERENCES CITED

1.

F. D. Bennett , and D. H. Habeck 1995. Cactoblastis cactorum: A successful weed control agent in the Caribbean, now a pest in Florida? pp. 21–26 In E. S. Delfosse and R. R. Scott [eds.], Proc. VIIIth Intl. Symp. Biol. Control Weeds. 2–7 February 1992, Canterbury, New Zealand.  Google Scholar

2.

K. Bloem , S. Bloem , J. Carpenter , S. Hight , J. Floyd , and H. Zimmermann 2007. Don't let cacto blast US—Development of a bi-national plan to stop the spread of the cactus moth Cactoblastis cactorum in North America, pp. 337–344 In M. J. B. Vreysen , A. S. Robinson , and J. Hendrichs [eds.], Area-Wide Control of Insects Pests: From Research to Field Implementation. Springer, Dordrecht, The Netherlands.  Google Scholar

3.

S. Bloem , K. Bloem , and A. L. Knight 1998. Oviposition by sterile codling moths, Cydia pomonella (Lepidoptera: Tortricidae) and control of wild populations with combined releases of sterile moths and egg parasitoids. J. Entomol. Soc. British Columbia 95: 99–109. Google Scholar

4.

S. Bloem , S. D. Hight , J. E. Carpenter , and K. A. Bloem 2005. Development of the most effective trap to monitor the geographical expansion of the cactus moth Cactoblastis cactorum (Lepidoptera: Pyralidae). Florida Entomol. 88: 300–306. Google Scholar

5.

J. E. Carpenter , S. Bloem , and F. Maree 2005. Inherited sterility in insects, pp. 39–68 In V. A. Dyck , J. Hendricks , and A. S. Robinson , [eds.], Sterile Insect Technique, Principles and Practice in Area Wide Integrated Pest Management, IAEA. Springer, Dordrecht.  Google Scholar

6.

J. B. Davis 2007. Inference on the means and variances from two independent populations, pp. 281–284 In Statistics using SAS® Enterprise Guide, Cary, NC: SAS Institute Inc.  Google Scholar

7.

T. S. Dickel 1991. Cactoblastis cactorum in Florida (Lepidoptera: Pyralidae: Phycitinae). Trop. Lepidoptera 2: 117–118. Google Scholar

8.

A. P. Dodd 1940. The Biological Campaign Against Prickly Pear. Commonwealth Prickly Pear Board, Brisbane, Australia. 177 pp. Google Scholar

9.

J. M. Fry 1989. Natural enemy databank, 1987, pp. 118–119 In A Catalogue of Natural Enemies of Arthropods Derived from Records in the CIBC Natural Enemy Databank, CAB International, Wallingford, Oxford, UK.  Google Scholar

10.

G. M. Gurr , and O. L. Kvedaras 2010. Synergizing biological control: Scope for sterile insect technique, induced plant defenses and cultural techniques to enhance natural enemy impact. Biol. Control 52: 198–207. Google Scholar

11.

S. A. Hassan 1993. The mass rearing and utilization of Trichogramma to control lepidopterous pests: achievements and outlooks. Pestic. Sci. 37: 387–391. Google Scholar

12.

S. D. Hight , and J. E. Carpenter 2009. Flight phenology of male Cactoblastis cactorum (Lepidoptera: Pyralidae) at different latitudes in the southeastern United States. Florida Entomol. 92: 208–216. Google Scholar

13.

S. D. Hight , J. E. Carpenter , K A. Bloem , S. Bloem , R. W. Pemberton , and P. Stiling 2002. Expanding geographical range of Cactoblastis cactorum (Lepidoptera: Pyralidae) in North America. Florida. Entomol. 85: 527–529. Google Scholar

14.

S. D. Hight , J. E. Carpenter , S. Bloem , and K. A. Bloem 2005. Developing a sterile insect release program for Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae): Effective overflooding ratios and release-recapture field studies. Environ. Entomol. 34: 850–856.  Google Scholar

15.

L. Li-Ying 1994. Worldwide use of Trichogramma for biological control on different crops: A survey, pp. 37–53 In E. Wajnberg , S. A. Hassan [eds.], Biological Control with Egg Parasitoids, CAB International, Wallingford.  Google Scholar

16.

G. Logarzo , L. Varone , and J. Briano 2008. Cactus Moth, In Annual Report 2008 South American Biological Control Laboratory, United States Department of Agriculture, Agricultural Research Service, USDA-ARS, Hurlingham, Argentina. [Online]  http://www.usda-sabcl.org/projects/AnnualReport2008PartLCACTUSMOTH.pdf. Google Scholar

17.

G. Logarzo , L. Varone , and J. Briano 2009. Cactus Moth, In Annual Report 2009 South American Biological Control Laboratory, United States Department of Agriculture, Agricultural Research Service, USDA-ARS, Hurlingham, Argentina. [Online]  http://www.ars.usda.gov/SP2UserFiles/Place/02110000/CompleteAnnualReport2009.pdfGoogle Scholar

18.

J. Mann 1970. Cacti Naturalized in Australia and Their Control. Department of Lands, Queensland, Australia. Google Scholar

19.

P. B. Martin , P. D. Lingren , G. L. Green , and R. L. Ridgway 1976. Parasitization of two species of Plusiinae and Heliotis spp. after releases of Trichogramma pretiosum in seven crops. Environ. Entomol. 5: 991–995. Google Scholar

20.

J. C. Monje , C. P. W. Zebitz , and B. Ohnesorge 1999. Host and host age preference of Trichogramma galloi and T. pretiosum (Hymenoptera: Trichogrammatidae) reared on different hosts. J. Econ. Entomol. 92: 97–103. Google Scholar

21.

V. C. Moran , and H. G. Zimmermann 1984. The biological control of cactus weeds: Achievements and prospects. Biocontrol News and Infor 5: 297–320. Google Scholar

22.

J. H. Myers , J. Monro , and N. Murray 1981. Egg clumping, host plant selection, and population regulation in Cactoblastis cactorum (Lepidoptera). Oecolgia 51: 7–13. Google Scholar

23.

Nappo (North American Plant Protection Organization). 2006. Official Pest Reports: Detection of an outbreak of cactus moth (Cactoblastis cactorum) in Isla Mujeres, Quintana Roo, Mexico. [Online]  www.pestalert.org Google Scholar

24.

Nappo (North American Plant Protection Organization). 2008. Official Pest Reports: Eradication of cactus moth (Cactoblastis cactorum Berg) out-break in Isla Mujeres, Quintana Roo, Mexico. [Online]  www.pestalert.org Google Scholar

25.

Nappo (North American Plant Protection Organization). 2009. Official Pest Reports: Detection and eradication of a cactus moth (Cactoblastis cactorum Berg) outbreak in Isla Contoy, municipality of Isla Mujeres, Quintana Roo, Mexico. [Online]  www.pestalert.org Google Scholar

26.

W. Olkowski , and A. Zhang 1990. Trichogramma modern day frontier in biological control. IPM Practitioner 12: 1–15. Google Scholar

27.

R. W. Pemberton 1995. Cactoblastis cactorum (Lepidoptera: Pyralidae) in the United States, an immigrant biological control agent or an introduction of the nursery industry? American Entomol. 41: 230–232. Google Scholar

28.

R. W. Pemberton , and H. Cordo 2001. Potential and risk of biological control of Cactoblastis cactorum (Lepidoptera: Pyralidae) in North America. Florida Entomol. 84: 513–526. Google Scholar

29.

J. D. Pinto , E. R. Oatman , and G. R. Platner 1986. Trichogramma pretiosum and a new cryptic species occurring sympatrically in Southwestern North America (Hymenoptera: Trichogrammatidae). Ann. Entomol. Soc. America 79: 1019–1028. Google Scholar

30.

J. D. Pinto 1999, Systematics of the North American species of Trichogramma Westwood (Hymenoptera: Trichogrammatidae). Mem. Entomol. Soc. Washington 22: 140.  Google Scholar

31.

B. Pintureau , S. Petinon , and C. Nardon 1999. Possible function of substances excreted by Trichogramma and darkening of their hosts. Bull. Soc. Zool. France 124: 261–269. Google Scholar

32.

R. B. Querino , and R. A. Zucchi 2003. New species of Trichogramma Westwood (Hymenoptera: Trichogrammatidae) associated with lepidopterous eggs in Brazil. Zootaxa 163: 1–10. Google Scholar

33.

P. Rendon , J. Sivinski , T. Holler , K. Bloem , M. Lopez , A. Martinez , and M. Aluja 2006. The effects of sterile males and two braconid parasitoids, Fopius arisanus (Sonan) and Diachasmimorpha krausii (Fullaway) (Hymenoptera), on caged populations of Mediterranean fruit flies, Ceratitis capitata (Wied.) (Diptera: Tephritidae) at various sites in Guatemala. Biol. Control 36: 224–231. Google Scholar

34.

H. G. Robertson 1984. Egg predation by ants as a partial explanation of the difference in performance of Cactoblastis cactorum on cactus weeds in South Africa and Australia, pp. 83–88 In E. S. Delfosse [ed.], Proc. VI Symp. Biol. Contr. Weeds. 19–25 August 1984, Vancouver, Canada.  Google Scholar

35.

H. G. Robertson 1987. Oviposition site selection in Cactoblastis cactorum (Lepidoptera): constraints and compromises. Oecologia 73: 601–608. Google Scholar

36.

H. G. Robertson 1989. Seasonal temperature effects on fecundity of Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae): differences between South Africa and Australia. J. Entomol. Soc. South Africa 52: 71–80. Google Scholar

37.

H. G. Robertson , and J. H. Hoffmann 1989. Mortality and life-tables of Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae) compared on two host-plant species. Bull. Entomol. Res. 79: 7–17. Google Scholar

38.

J. T. Romeis , G. Shanower , and P. W. Zebitz 1997. Volatile plant infochemicals mediate plant preference of Trichogramma chilonis. J. Chem. Ecol. 23: 2455–2465. Google Scholar

39.

J. T. Romeis , G. Shanower , and P. W. Zebitz 1999. Trichogramma egg parasitism of Helicoverpa armigera on pigeonpea and sorghum in southern India. Entomol. Exp. Appl. 90: 69–81.  Google Scholar

40.

F. J. Simmonds , and F. D. Bennett 1966. Biological control of Opuntia spp. by Cactoblastis cactorum in the Leeward Islands (West Indies). Entomophaga 11: 183–189. Google Scholar

41.

T. J. Simonsen , R. L. Brown , and F. A. Sperling 2008. Tracing an invasion: Phylogeographical of Cactoblatis cactorum (Lepidoptera: Pyralidae) in the United States based on Mitochondrial DNA. Entomol. Soc. America 101: 899–905. Google Scholar

42.

J. M. Sivinski 1996. The past and potential of biological control of fruit flies, pp. 369–377 In J. B. A. McPheron and G. J. Steck [eds.], Fruit Fly Pests, A World Assessment of their Biology and Management. St. Lucie Press, Delray Beach, FL.  Google Scholar

43.

S. M. Smith 1996. Biological control with Trichogramma advances, successes, and potential of their use. Annu. Rev. Entomol. 41: 375–406. Google Scholar

44.

P. D. Stiling 2002. Potential non-target effects of a biological control agent, prickly pear moth, Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae), in North America, and possible management actions. Biol. Invasions 4: 273–281. Google Scholar

45.

P. D. Stiling , D. Moon , and D. Gordon 2004. Endangered cactus restoration: Mitigating the non-target effects of biological control agent (Cactoblastis cactorum) in Florida. Rest. Ecol. 12: 605–610. Google Scholar

46.

D. M. Suckling , A. M. Barrington , A. Chhagan , A. E. A. Stephens , G. M. Burnip , J. G. Charles , and S. L. Wee 2007. Eradication of the Australian painted apple moth Teia anartoides in New Zealand: trapping, inherited sterility, and male competitiveness, pp. 603–615 In M. J. B. Vreysen , A. S. Robinson and J. Hendrichs [eds.], Area-Wide Control of Insect Pests. Springer, Dordrecht, The Netherlands.  Google Scholar

47.

J. C. Van Lenteren 2000. Success in biological control of arthropods by augmentation of natural enemies, pp. 77–103 In G. Gurr and S. Wratten [eds.], Biological Control: Measures of Success. Kluwer Academic Publishers, Hingham, USA.  Google Scholar

48.

S. H. Williamson 2009. Six ways to compute the relative value of a U.S. dollar amount, 1970 to present. [Online]  http://www.measuringworth.com/uscompareGoogle Scholar

49.

J. A. Wilson Jr., and J. A. Durant 1991, Parasites of the European corn borer (Lepidoptera; Pyralidae) in South Carolina, USA. J. Agr. Entomol. 8: 109–116.  Google Scholar

50.

H. G. Zimmermann , V. C. Moran , and J. H. Hoffmann 2001. The renowned cactus moth, Cactoblastis cactorum (Lepidoptera: Pyralidae): Its natural history and threat to native Opuntia floras in Mexico and the United States of America. Florida Entomol. 84: 543–551. Google Scholar
Oulimathe Paraiso, Stephen D. Hight, Moses T. K. Kairo, and Stephanie Bloem "Egg Parasitoids Attacking Cactoblastis cactorum (Lepidoptera: Pyralidae) in North Florida," Florida Entomologist 94(1), 81-90, (1 March 2011). https://doi.org/10.1653/024.094.0111
Published: 1 March 2011
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