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Review

Interaction of Cultural, Biological, and Varietal Controls for Management of Stalk Borers in Louisiana Sugarcane

by
Thomas E. Reagan
* and
Megan M. Mulcahy
*
Department of Entomology, Louisiana State University AgCenter, Baton Rouge, LA 70803, USA
*
Authors to whom correspondence should be addressed.
Insects 2019, 10(9), 305; https://doi.org/10.3390/insects10090305
Submission received: 31 July 2019 / Revised: 10 September 2019 / Accepted: 11 September 2019 / Published: 19 September 2019
(This article belongs to the Special Issue Ecology and Pest Management of Sugarcane Insects)

Abstract

:
Diatraea saccharalis F is considered the most important pest of sugarcane in the United States. This article focuses on the history of pest management as it relates to the control of this stem borer in Louisiana sugarcane, and how control practices have become more in tune with integrated pest management paradigms. Various pest management strategies are employed against D. saccharalis and the interactions between each of these provide farmers with the tools needed to curb damaging infestations. However, the invasion of the Mexican rice borer, Eoreuma loftini (Dyar), and other confounding environmental factors have presented farmers, consultants, and researchers with new pest management challenges. We address these challenges and provide an overview of ongoing developments, particularly in the Louisiana sugarcane pest management program.

1. Introduction

The sugarcane borer, Diatraea saccharalis F (Lepidoptera: Crambidae), is native to the West Indies, as well as Central and South America. It was introduced into Louisiana in the 1850s due to the continued importation of sugarcane for production in the state [1]. Since its introduction, D. saccharalis has long been regarded as the most damaging insect pest on the crop. Adults of D. saccharalis are drab beige in color and have an inverted v-pattern of dots on their wings [2]. Female moths oviposit in clusters on the leaves of sugarcane plants and other grasses. Once the eggs hatch, neonate larvae migrate to and feed within leaf sheaths [3]. After about 10 days, the larvae bore into sugarcane stalks, where they continue to develop through several molts. The larvae then pupate within expanded feeding tunnels inside the sugarcane stalk and eventually emerge as adult moths. In mature plants, damage from the borers cause the tops of the sugarcane to weaken or die, leading to lodging during heavy infestations. In young plants, D. saccharalis feeding can kill the leaves within the whorl, resulting in a condition known as dead tops, or “dead heart”. Ultimately, sugar production per hectare is reduced by approximately 0.61% for every 1% of sugarcane internodes bored. Severe infestations can cause yield losses of over 20% in affected fields [4].
This review follows the history of D. saccharalis management in Louisiana and the ways in which it has changed to align with new integrated pest management outlooks. The review also looks at how the management of D. saccharalis influences the management of other stem-boring pests within the area and how it has affected sugar production in the region.

2. A Brief History of Stalk Borer Management in Louisiana

Well before the use of modern pesticides, pest management in the early 1900s emphasized the robust use of common-sense cultural practices for managing this insect in sugarcane. Some recommended cultural control tactics included improvement of field hygiene practices, burning of sugarcane before harvest, manipulation of planting dates, and strategic flooding of fields [5]. One of the most important D. saccharalis management tactics at the time was to have all sugarcane growers in Louisiana plant non-insect-infested seed cane [6]. Growers were encouraged to submerge sugarcane in hot water to kill borer larvae prior to planting and to manually remove severely damaged plants during the early growing season [7].
An increase in the availability and affordability of insecticides in the 1940s and early 1950s shifted focus away from cultural control practices, which were typically considered labor intensive [2]. Initially, inorganic cryolite and the botanical ryania were applied to sugarcane to reduce D. saccharalis infestations. However, these insecticides provided less than 50% control [8]. As such, they were later replaced, in the mid-to-late 1950s, by organic chlorines or chlorinated hydrocarbons, such as endrin [9]. This class of insecticide was far more effective, with Louisiana Agricultural Experiment Station and USDA-ARS station scientists demonstrating extreme efficiency with both foliar sprays and granules [10]. Unfortunately, the widespread use of these insecticides had unanticipated problems that were felt in sugarcane and other cropping systems. Insect populations were being subjected to repetitive applications of a single class of insecticide, leading to extreme selective pressure [11]. This resulted in the evolution of resistance to pesticides in several pest species. Insecticide resistance against endrin and endosulfan was eventually reported in populations of D. saccharalis in Louisiana [12]. In the late 1950s, it also became increasingly apparent that the massive, global use of pesticides was having severe ecological impacts [13,14]. For example, organochlorine pesticides were shown to negatively impact many organisms, including nontarget insects, birds, fish, and snakes, besides numerous other vertebrate and invertebrate species [15].
The concept of integrated pest management (IPM) was developed in response to a mounting record of insecticide failures and to mitigate environmental disasters [14]. Integrated pest management itself can be loosely defined as a decision-making process based on a thorough knowledge of the pest and its tritrophic and environmental interactions [13,16]. It is concerned with using multiple pest management tactics in conjunction with threshold models for the control of insect pests or diseases in agricultural crops [13,16]. The main purpose of IPM is to prevent economically damaging outbreaks of pests and decrease pesticide resistance while also reducing the risks to human health and the environment by reducing the use of chemical insecticides, herbicides, and fungicides on crops [17]. The development of the pest management program against D. saccharalis exemplifies the switch from the indiscriminate use of insecticides to the use of integrated control methods. This includes a return to cultural control tactics and greater emphasis being placed on sustainable pest management strategies, such as varietal resistance, biological control, and green chemistries.

3. Host Plant Resistance in Sugarcane Cultivars

Recognition of possible stalk borer resistance in sugarcane was cited as early as 1902 by Stubbs and Morgan [18]. The development of sugarcane varieties, with improved host plant resistance against the sugarcane stalk borer, undoubtedly occurred prior to the development of modern insecticides. However, the mechanisms of resistance were poorly understood [2]. Studies by Coburn and Hensley (1972) [19] compared larval survival and establishment of D. saccharalis on resistant (NCO 310) and susceptible (CP 44-101) cultivars. In this study, appression of the sugarcane leaf sheath was shown to have an effect on the boring behavior of the sugarcane borer. In the resistant cultivar (NCO 310), natural boring by D. saccharalis occurred in the fifth leaf sheath down from the whorl. In contrast to this, boring in the susceptible cultivar (CP 44-101) typically occurred in the top first or second leaf sheath, which were open (not appressed). The benefits of leaf sheath appression were tested by physically tying leaf sheaths of CP 44-101 closed while simultaneously prying the upper sheaths of NCO 310 open [19]. They found reverse mortality, with more survival in NCO 310 and less in the manually “closed” CP 44-101. Other applied entomologists have cited various characteristics in sugarcane which are correlated to borer resistance in the crop, including narrow leaves, high fiber content, light stalk color, heavy wax coating, leaf shedding, thin stalks, longleaf spindles, erect leaves, high vigor, juice content, low leaf senescence, and attractiveness to egg-laying moths [20,21,22].
Additionally, early research conducted by Mathies and Charpentier (1969) [23] suggested that rind hardness may confer resistance to sugarcane borers due to its negative effects on the survival of neonate larva. This was followed up by studies that confirmed the benefits of rind hardness in reducing the prevalence of D. saccharalis infestations with the use of a durometer (penetrometer) [24]. These results were expanded upon in Reagan and Martin (1982) [25]. They were able to assess eight common cultivars at the time, as well as nine experimental station cultivars, dividing the level of resistance into four groupings. This included the traditional method of evaluating cultivar resistance using percentage of bored internodes, in addition to determining the distinct number of adult emergence holes [26]. These measures are still used as an assessment tool today to monitor D. saccharalis injury and infestation levels. Rind hardness and fiber content remain important tools in the development of resistant cultivars to combat D. saccharalis [27].
In addition to extensive work conducted against D. saccharalis [20], studies looking at resistance to the invasive borer Eoreuma loftini (Dyar) (Lepidoptera: Crambidae) were initiated in 2001 [28] and continued by Wilson (2011) [21] and Wilson et al. (2015) [29]. E. loftini (the Mexican rice borer) is another stalk borer invading sugarcane in Louisiana. Its behavior and habits are very similar to those of Chilo saccariphagus Bojer (Lepidoptera: Crambidae) and Eldana saccharina Walker (Lepidoptera: Pyralidae) [30,31]. Mechanisms used to manage these pests have been well researched in Southern Africa and may be incorporated into the Louisiana sugarcane pest management strategy through collaboration in the future. For instance, the South African cultivars N21 and N24 were found to be resistant to both E. saccharina and E. loftini, whereas N27 was susceptible [22]. Of the South African cultivars, N21 has excellent drought tolerance [32]. Evidence demonstrates that, like E. saccharina, the Mexican rice borer responds favorably to water stress in sugarcane plants [31]. Drought promotes outbreaks of phytophagous insects due to elevated plant nutrient levels (especially nitrogen), reductions in the plants ability to defend itself, and lastly, through the creation of improved temperature niches in the physical environment, allowing for increases in survivability and developmental rate [33,34,35]. Thus, tolerance to water stress within sugarcane varieties can be used successfully within sugarcane cultivars to manage stem borer populations during adverse climatic conditions. Resistant cultivars, such as N21 and N24, also hinder stalk penetration by borer larvae, which are therefore more exposed to predation, parasitism, and insecticide applications (since they are largely protected once inside the stalk) [32]. This is particularly true of E. loftini larvae, which typically pack their feeding tunnels tightly with excrement, thus isolating them from external control measures [36]. Reduced penetration as a means of host plant resistance can therefore be used in conjunction with IPM tools such as biocontrol and judicious insecticide use to control stem-boring pests in sugarcane [37]. The tunnels of D. saccharalis are wider and more open, thus allowing improved management through arthropod predation and parasitoids [38]. However, this pest can still be difficult to control once inside the stalk. Research is currently assessing the resistance of various cultivars, both local and foreign, to identify unique resistant germplasms for the development of commercial cultivars that are able to reduce infestations of both D. saccharalis and E. loftini pest populations in Louisiana [22].
Furthermore, annual assessments of stalk borers (D. saccharalis and E. loftini) in four or five replication experiments have been conducted over a 10–12-year period at the LSU AgCenter and the USDA-ARS at Houma, Louisiana, United States to evaluate new cultivars. These are similar to those conducted by Reagan and Martin (1982) [25]. Each annual program starts out with at least 100 seed lines [22,39]. In addition to the measurements previously mentioned for monitoring stem borer infestations, a sequential plan for the sugarcane borer was developed for minimizing and streamlining sampling time in the field [40]. Currently, the following varieties are available and recommended to growers for resistance to stem borers in Louisiana: L 99-226, L 01-299, and HoCP 04-838 [41]. Of the recommended varieties for the 2019 growing season in Louisiana, L 01-283 and Ho 12-615 are considered mildly resistant to the sugarcane borer. A further five of the recommended commercial varieties (HoCP 96-540, HoCP 00-950, HoCP 09-805, L 11-183, and L 12-201) are susceptible to damage from D. saccharalis [41].

4. Development of Sustainable Insecticides for Use in Louisiana Sugarcane

Organophosphates (acetylcholinesterase inhibitors), such as azinphos-methyl and monocrotophos, replaced the organochloride (GABA-gated channel blocker) endrin after that insecticide was banned. However, monocrotophos had problems with resistance in the Lower Rio Grande Valley [42,43]. After suspension and restriction of azinphos-methyl (loss of label in 1995 for fish kills), these insecticide control methods were finally replaced by the insect growth regulator tebufenozide [42,44]. The first ever evaluation for D. saccharalis control by tebufenozide occurred in 1993 [45]. Now, more than 80% of all the tebufenozide insecticide produced in the United States is applied to Louisiana sugarcane annually. This insecticide is considered to be narrow range and minimum risk [40,46]. It is a molting accelerator compound which affects larval growth in some lepidopterous insects, particularly those in the families Pyralidae and Crambidae [46]. Unlike most insecticides, which rapidly kill insects a few hours after exposure, tebufenozide acts only during the molt, when insects shed their exterior cuticle. Larvae exposed soon after the molt show no chemical effects for several days until after the next molt [47,48]. In addition, tebufenozide was one of the few insecticides developed at the time which did not suppress nontarget crickets, beneficial spiders, and other selected arthropods [49]. This is in contrast to the insecticide lambda-cyhalothrin, which is a broad-spectrum pyrethroid (sodium channel modulator) that is effective against D. saccharalis and several nontargeted secondary pests [42], including the West Indian canefly, Saccharosydne saccharivora Westwood (Hemiptera: Fulgoridae), and yellow sugarcane aphid, Sipha flava Forbes (Hemiptera: Aphididae). Although this made pyrethroid insecticides, such as lambda-cyhalothrin, a useful tool for farmers, they have since begun to be phased out due to their negative impacts on beneficial arthropods in the agroecosystem, pest resurgence (especially in aphid populations), and insecticide resistance problems [50,51].
In sugarcane biological control studies, stem borer parasitoids that were exposed to sugarcane leaves from insecticide-treated field plots showed very low levels of mortality to tebufenozide [49]. As such, tebufenozide use in sugarcane allowed for increased predation and parasitism of D. saccharalis to such an extent that insecticide applications on sugarcane were reduced from three applications a year to just half an application per year. This resulted in tebufenozide receiving the presidential Green Chemistry Challenge Award for insecticide discovery research in 1998 from the president of the United States and the Federal Environmental Protection Agency [46].
Other research programs have also assessed the potential for using different economic injury thresholds for managing D. saccharalis with insecticides, together with susceptible and resistant commercial cultivars. Posey et al. (2006) [39] conducted a two-year study to assess this integrated approach. In this four-replication test, susceptible cultivars (LCP 85-384 and Ho CP 91-555) exceeded 40% bored internodes in untreated plots. However, when treated with tebufenozide, damage levels in susceptible cultivars did not differ significantly from the levels attained in resistant cultivars. Furthermore, a higher threshold level could be used (10% bored internodes vs. 5% bored internodes) with tebufenozide, without compromising the level of control.
Due to its efficacy, Louisiana experienced widespread use of tebufenozide, which represented 90% of all the foliar applications of insecticides in sugarcane during the 2007 growing season alone [52]. This increased concerns regarding the potential for the development of resistance against the chemistry in populations of D. saccharalis, which has been an on-going problem in Louisiana sugarcane pest management [51]. In 2008, researchers selected for resistance to tebufenozide in laboratory-reared D. saccharalis. They obtained a 27.1-fold increase in LC50 after 12 generations of the pest were subjected to selection with tebufenozide [53]. Thus, insecticide resistance management strategies were highlighted as being necessary to preserve D. saccharalis control tactics for the Louisiana sugarcane industry [51].
Fortunately, success with tebufenozide paved the way for the development and introduction of other selective, sustainable insecticide chemistries. Recent studies have demonstrated the effectiveness of a chitin inhibitor (novaluron) for D. saccharalis control [38]. Like tebufenozide, novaluron has no measurable impact on nontarget arthropods and can be used in conjunction with biocontrol strategies. Two diamide insecticides, namely, chlorantraniliprole and flubendiamide, are also extremely effective for the management of lepidopteran stem borers [38,54]. These insecticides attack insect ryanodine receptors and are active against other lepidopteran pests too [54,55]. Fortunately, their high-level selectivity means that nontarget organisms are relatively safe if they are exposed to the diamides [56]. While these insecticides are labeled for use in Louisiana sugarcane, studies comparing these insecticides with industry standards for D. saccharalis and E. loftini are ongoing [38]. However, the effectiveness of these insecticides, together with on-going tebufenozide use, have the potential to provide farmers with multiple pest management options to better control stem borer infestations and to curb the likelihood of insecticide resistance through reduced selective pressure.
Scouting by farmers and other stakeholders is an important tool that can improve the application of insecticides in a manner that promotes IPM for the control of D. saccharalis in Lousiana. Farmers, extension officers, and consultants scout for D. saccharalis from mid-June to September by looking for larval feeding scars on leaf sheaths and by looking for larvae, as well as entrance and exit holes near internodes and along the stalk [57]. Effective monitoring of this pest allows farmers to spray insecticides on sugarcane only when the borers are present at damaging levels. The economic injury level for D. saccharalis is 6–12% internodes bored (depending on the variety selected), at which point action should be taken and insecticides applied [4]. This avoids unnecessary chemical applications and can reduce costs, environmental contamination, and insecticide resistance. However, scouting for D. saccharalis is time consuming, laborious, and by the time farmers can see the effects of stem borer damage, it is too late to treat fields [40]. Although alternative scouting methods, such as black light and pheromone traps, have been assessed in the past [58], correlating trap catches with larval infestations and crop damage is difficult for many stem borer species [59]. Therefore, Louisiana is reliant on manual scouting techniques for D. saccharalis [60]. Due to differences in mating behavior and response to trap design, there has been some success using pheromone traps to monitor E. loftini populations. Capture of 20 moths per trap per week roughly corresponds to the action threshold for this species in sugarcane [60]. The use of pheromone traps has also been useful in detecting populations of E. loftini and for monitoring its invasion into new sugarcane growing regions [38]. Therefore, the efficacy of pheromone traps for stem borer scouting should continue to be researched and improved upon, as well as the use of moth sex pheromones for mating disruption [61].

5. The Role of Biological Control and Adverse Weather Conditions in Borer Management

The movement towards more environmentally aware pest management practices can be seen relatively early on in the southeastern United States, with a shift in paradigms regarding the Federal and State USDA-APHIS red imported fire ant, Solenopsis invicta Buren (Hymenoptera: Formicidae), eradication program [62]. When interviewed by Rachel Carson (1962) [63], the Head of the Louisiana State University Entomology Department Dr. L.D. Newsom stated that “the imported fire ant eradication program had thus far been a failure”. He went on to say that the infestation had increased in Louisiana since the program was initiated. The failures of such programs eventually led to an abandonment of eradication as a pest management solution, with focus shifting to more localized control tactics [64]. In the case of S. invicta, the cancellation of the EPA’s mirex eradication program revealed that in many agricultural areas, the fire ant eradication program had negative effects on crop yields [64,65,66]. Not only did mirex decrease populations of beneficial natural predators, such as spiders, carabids, and staphylinids, but S. invicta were also shown to have a positive impact on crop production through predation of D. saccharalis larvae [65,66,67]. Additionally, tick populations decreased in areas where imported S. invicta had just begun invading northwest Louisiana. This led to reductions in tularemia (rabbit fever) and other tick-borne diseases in human populations due to S. invicta predation [68]. This highlighted the benefits of S. invicta in Louisiana and the benefits of preserving natural predator and parasitoid populations within sugarcane fields.
Depending on the particular borer attacking sugarcane, biological control via predation has a substantial impact [69]. Although biological control using indigenous and exotic parasitoid wasps and flies has had some success in Florida and the Lower Rio Grande Valley in Texas [43,70], it has been less effective in other regions of the United States [71]. Predation on parasitoids in Louisiana can be severe, thereby reducing the ability of parasitoids to establish and maintain pressure on sugarcane borer populations [72]. The more temperate climate in Louisiana and parasitoid inability to locate hosts in young sugarcane are likely affecting the success of parasitoids such as Cotesia flavipes Cameron (Hymenoptera: Braconidae) [73]. Entomopathogens, such as Beauveria bassiana Balsamo (Hypocreales: Cordycipitaceae), are unable to curb D. saccharalis populations under field conditions [74,75], and although Bacillus thuringiensis Berliner reportedly decreases D. saccharalis damage by up to 75%, it has yet to be adopted for commercial production [31,76]. Biological control of E. loftini is even more problematic due to its cryptic behavior inside the sugarcane stalk [77].
Another hurdle for successful biological control in Louisiana is the prevalence of heavy rains, tropical storms, and other adverse weather conditions. A 4-treatment, 12-replication large-area study was conducted in numerous places within St. Mary, Iberia, and Vermilion parishes in southcentral Louisiana to assess the impact of Hurricane Rita on biological control [78]. This storm surge affected large areas of the state, including sugarcane production regions. Both flooded and nonflooded areas were tested for efficacy of natural biological control in plant and ratoon commercial sugarcane [78]. The study showed that sugarcane in flooded areas experienced a rise in yield losses of between US$1.9 million and US$2.6 million due to increases in pest infestations after the hurricane. The primary entomological role of the hurricane was its impact on biological control, mainly through a reduction in arthropod predation. A significant 2.8-fold reduction in numbers of the predators was observed in impacted fields. Even with a significant 2.4-fold increase in the average number of insecticide applications (for D. saccharalis management) in formerly flooded fields, sugarcane growers still incurred substantially higher losses as a result of pest injury [78]. The effects of adverse weather on agriculture and pest populations is of growing concern and should continue to be monitored, as the likelihood of extreme weather events in the region is expected to become more frequent due to warmer waters in the Gulf of Mexico and similar issues related to ongoing global climate change [79,80]. This is especially true since climate change alone is expected to improve conditions for insect pests, thereby increasing the risk of pest outbreaks in sugarcane cropping systems [81].

6. Recommended Cultural Control Practices

In the past, a large number of cultural controls were recommended to farmers for the management of D. saccharalis in Louisiana sugarcane [82]. Some of these cultural control practices have since been discontinued due to a lack of labor and higher input costs [3]. These include hot water treatments of seed cane, removal of postharvest trash, and targeted manual destruction of damaged plants in the spring [3]. Another formerly common cultural control method was the preharvest burning of sugarcane, which was used throughout the world as a means of reducing in-field pest populations [83]. Preharvest burning had the added benefit of removing extraneous leaf materials, making the sugarcane easier to cut and process [31,83]. However, postharvest sucrose deterioration in sugarcane stalks, loss of soil organic matter, and the negative environmental and health effects caused by sugarcane burning emissions have resulted in pressure on farmers to adopt “green cane harvesting” [84,85]. Thus, preharvest burning can no longer be relied upon to reduce pest numbers. Fortunately, some studies have demonstrated the benefits of unburnt residues and trash blankets on stem borer predators, such as S. invicta [84,86].
Current cultural control practices that are used in Louisiana to manage D. saccharalis populations include (1) planting noninfested seed cane; (2) reducing overwintering larvae by plowing stubble postharvest; and (3) maintaining crop residues, trash, and broken stalks in fields over winter, so that remaining larvae are killed by low temperatures [57]. Furthermore, maize (Zea mays L. (Poales: Poaceae)) acts as a suitable host plant for D. saccharalis [40,87]. Therefore, farmers are advised to plant susceptible maize cultivars as far from sugarcane as possible to decrease midsummer migrations of the moth from senescing cornfields [57]. Finally, planting date may also have an effect on D. saccharalis populations in sugarcane, with early planted sugarcane being susceptible to increased infestations [88]. Planting date manipulation may also be a useful tool for managing E. loftini infestations, however management of this borer would likely improve with early planting [71]. This pest responds well to water-stressed plants, high nutrient content, and availability of cryptic oviposition sites. Therefore, improved water management, judicious nitrogen application, and removal of sugarcane trash are some cultural methods that can be used against E. loftini [31]. Of course, this may clash with recommendations to retain plant residues and trash in order to curb D. saccharalis numbers. This highlights the need to consider pest interactions in the sugarcane agroecosystem and to manage both stem borer species as a pest complex.

7. Conclusions

In conclusion, it is evident that D. saccharalis has had a great impact on sugarcane research and production techniques in the region for many years. The Louisiana sugarcane industry exemplifies the move towards more sustainable, economically viable, and environmentally sound farming practices. The evolution of D. saccharalis management techniques underscores the trend towards integrated pest management, with the focus shifting from the prescripted use of insecticides to a more holistic system that includes the use of biological control and varietal management. This has the added benefit of reducing input costs and conserving important ecological processes that will continue to aid in the management of this pest. Farmers now have a diverse set of tools with which to control D. saccharalis. The invasion of E. loftini has presented new challenges to the Louisiana sugarcane industry; however, novel research avenues and management practices are being pursued and developed to address this challenge in a way that enhances and complements the existing insect pest management program in sugarcane.

Author Contributions

T.E.R., funding, visualization, outline, and content contribution. M.M.M., literature review, writing, formatting, and editing.

Funding

This review was funded by the entomology program that is managed by T.E.R., under USDA(NIFA) grant no. 12166495.

Acknowledgments

The authors would like to acknowledge the LSU AgCenter and LSU Entomology Department. We would also like to thank Ph.D. student Forest Huval for his assistance during the compilation of this review article as well as Blake Wilson for his valuable advice. Thank you to M. Stout, T. Schowalter, R. Diaz, and D. Swale for their internal reviews, as well as the unknown external reviewers. This manuscript is published with permission of the LAES with manuscript no. 2019-234-34109.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Bessin, R.T.; Reagan, T.E. Fecundity of sugarcane borer (Lepidoptera: Pyralidae), as affected by larval development on Gramineous host plants. Environ. Entomol. 1990, 19, 635–639. [Google Scholar] [CrossRef]
  2. Dyar, H.G.; Heinrich, C. The American moths of the genus Diatraea and allies. Proc. U. S. Natl. Mus. 1927, 71, 1–48. [Google Scholar] [CrossRef]
  3. Hensley, S.D. Management of sugarcane borer populations in Louisiana, a decade of change. Entomophaga 1971, 16, 133–146. [Google Scholar] [CrossRef]
  4. White, W.H.; Viator, R.P.; Dufrene, E.O.; Dalley, C.D.; Richard, E.P., Jr.; Tew, T.L. Re-evaluation of sugarcane borer (Lepidoptera: Crambidae) bioeconomics in Louisiana. Crop Prot. 2008, 27, 1256–1261. [Google Scholar] [CrossRef]
  5. Holloway, T.E.; Haley, W.E.; Loftin, U.C.; Heinrich, C. The sugar-cane borer in the United States. USDA Tech. Bull. 1928, 41, 77. [Google Scholar]
  6. Frazier, D.S. Fire in The Cane Field; State House Press: Abilene, TX, USA, 1962; p. 384. [Google Scholar]
  7. Holloway, T.E.; Haley, W.E. Suggestions for the Control of the Sugar-Cane Moth Borer; CAB International: New York, NY, USA, 1924; p. 3. [Google Scholar]
  8. Hensley, S.D.; McCormick, W.J.; Long, W.H.; Concienne, E.J. Field tests with new insecticides for control of the sugarcane borer in Louisiana in 1959. J. Econ. Entomol. 1961, 54, 1153–1154. [Google Scholar] [CrossRef]
  9. Long, W.H.; Concienne, E.J.; Hensley, S.D.; McCormick, W.J.; Newsom, L.D. Control of the sugarcane borer with insecticides. J. Econ. Entomol. 1964, 52, 821–824. [Google Scholar] [CrossRef]
  10. Hensley, S.D.; McCormick, W.J. Granular versus spray formulations of endrin for control of the sugarcane borer in Louisiana. J. Econ. Entomol. 1964, 57, 219–220. [Google Scholar] [CrossRef]
  11. Peshin, R.; Pimentel, D. Integrated Pest Management; Springer: Dordrecht, The Netherlands, 2014; pp. 65–97. [Google Scholar]
  12. Yadav, R.P.; Anderson, H.L.; Long, W.H. Sugarcane borer resistance to insecticides. J. Econ. Entomol. 1965, 58, 1122–1124. [Google Scholar] [CrossRef]
  13. Kogan, M. Integrated pest management: Historical perspectives and contemporary developments. Ann. Rev. Entomol. 1998, 43, 243–270. [Google Scholar] [CrossRef]
  14. Kogan, M.; Bajwa, W.I. Integrated pest management: A global reality? Anais Soc. Entomol. Bras. 1999, 28, 1–25. [Google Scholar] [CrossRef]
  15. Van den Bosch, R. The Pesticide Conspiracy; University of California Press: Berkeley, CA, USA, 1978. [Google Scholar]
  16. Ehler, L.E. Integrated pest management (IPM): Definition, historical development and implementation, and the other IPM. Pest Manag. Sci. 2006, 62, 787–789. [Google Scholar] [CrossRef] [PubMed]
  17. Prokopy, R.J. Two decades of bottom-up, ecologically based pest management in a small commercial apple orchard in Massachusetts. Agric. Ecosyst. Environ. 2003, 94, 299–309. [Google Scholar] [CrossRef]
  18. Stubbs, W.C.; Morgan, H.A. Cane borer Diatraea saccharalis. La. Agric. Exp. Sta. Bull. 1902, 2, 888–927. [Google Scholar]
  19. Coburn, G.E.; Hensley, S.D. Differential survival of Diatraea saccharalis (F.) larvae on 2 varieties of sugarcane. Proc. Int. Soc. Sugarcane Technol. 1972, 14, 440–444. [Google Scholar]
  20. Long, W.H.; Hensley, S.D. Insect pests of sugar cane. Ann. Rev. Entomol. 1972, 17, 149–176. [Google Scholar] [CrossRef]
  21. Wilson, B.E. Advanced Management of the Mexican Rice Borer (Eoreuma loftini) in Sugarcane. Master’s Thesis, Louisiana State University, Baton Rouge, LA, USA, May 2011. [Google Scholar]
  22. Reagan, T.E.; Akbar, W.; Beuzelin, J.M. Identifying sugarcane varieties resistance to borers and aphids. La. Agric. 2008, 51, 18–19. [Google Scholar]
  23. Charpentier, L.J.; Mathes, R. Cultural practices in relation to stalk moth borer infestations in sugar cane. In Pests of Sugar Cane; Williams, J.R., Metcalfe, J.R., Mungomery, R.W., Mathes, R., Eds.; Elsevier: Amsterdam, The Netherlands, 1969; pp. 163–164. [Google Scholar]
  24. Martin, F.A.; Richard, C.A.; Hensley, S.D. Host resistance to Diatraea saccharalis (F.): Relationship of sugarcane internode hardness to larval damage. Environ. Entomol. 1975, 4, 687–688. [Google Scholar] [CrossRef]
  25. Reagan, T.E.; Martin, F.A. Plant resistance: A key management tool for control of the sugarcane borer in Louisiana. In Proceedings of the Inter-American Sugar Cane Seminar: Varieties and Breeding, Miami, FL, USA, 3–6 October 1982; Volume 3, pp. 13–22. [Google Scholar]
  26. Bessin, R.T.; Reagan, T.E.; Moser, E.B. Integration of control tactics for management of the sugarcane borer (Lepidoptera: Pyralidae) in Louisiana sugarcane. J. Econ. Entomol. 1990, 83, 1563–1569. [Google Scholar] [CrossRef]
  27. White, W.H.; Tew, T.L.; Richard, E.P., Jr. Association of sugarcane pith, rind hardness, and fiber with resistance to the sugarcane borer. J. Am. Soc. Sugarcane Technol. 2006, 26, 87–100. [Google Scholar]
  28. Reay-Jones, F.P.F.; Way, M.O.; Sètamou, M.; Legendre, B.L.; Reagan, T.E. Resistance to the Mexican rice borer (Lepidoptera: Crambidae) among Louisiana and Texas sugarcane cultivars. J. Econ. Entomol. 2003, 96, 1929–1934. [Google Scholar] [CrossRef] [PubMed]
  29. Wilson, B.E.; Vanweelden, M.T.; Beuzelin, J.M.; Reagan, T.E.; Way, M.O.; White, W.H.; Showler, A.T. A relative resistance ratio for evaluation of Mexican rice borer (Lepidoptera: Crambidae) susceptibility among sugarcane cultivars. J. Econ. Entomol. 2015, 108, 1363–1370. [Google Scholar] [CrossRef] [PubMed]
  30. Conlong, D.E.; Sweet, P.; Piwalo, J. Resistance of southern African varieties of sugarcane to Chilo sacchariphagus (Lepidoptera: Crambidae) in Mozambique, and development of a non-destructive field resistance rating system. Proc. South Afr. Sugarcane Technol. Assoc. 2004, 78, 297–306. [Google Scholar]
  31. Showler, A.T. Selected abiotic and biotic environmental stress factors affecting two economically important sugarcane stalk boring pests in the United States. Agronomy 2016, 6, 10. [Google Scholar] [CrossRef]
  32. Kvedaras, O.L.; Byrne, M.J.; Coombes, N.E.; Keeping, M.G. Influence of plant silicon and sugarcane cultivar on mandibular wear in the stalk borer Eldana saccharina. Agric. For. Entomol. 2009, 11, 301–306. [Google Scholar] [CrossRef]
  33. Rhoades, D.F. Herbivore population dynamics and plant chemistry. In Variable Plants and Herbivores in Natural and Managed Systems; Denno, R.F., McClure, M.S., Eds.; Academic Press: New York, NY, USA, 1983; pp. 155–220. [Google Scholar]
  34. White, T.C.R. The abundance of invertebrate herbivores in relation to the availability of nitrogen in stressed food plants. Oecologia 1984, 63, 90–105. [Google Scholar] [CrossRef] [PubMed]
  35. Atkinson, P.R.; Nuss, K.J. Associations between host-plant nitrogen and infestations of the sugarcane borer, Eldana saccharina Walker (Lepidoptera: Pyralidae). Bull. Entomol. Res. 1989, 79, 489–506. [Google Scholar] [CrossRef]
  36. Hummel, N.; Reagan, T.E.; Pollet, D.; Akbar, W.; Beuzelin, J.M.; Carlton, C.; Saichuk, J.; Hardy, T.; Way, M.O. Mexican Rice Borer, Eoreuma Loftini (Dyar); Louisiana State University AgCenter: Baton Rouge, LA, USA, 2008; p. 3098. [Google Scholar]
  37. Showler, A.T.; Reagan, T.E. Mexican rice borer, Eoreuma loftini (Dyar) (Lepidoptera: Crambidae): Range expansion, biology, ecology, control tactics, and new resistance factors in United States sugarcane. Am. Entomol. 2017, 63, 36–51. [Google Scholar] [CrossRef]
  38. Wilson, B.E.; VanWeelden, M.T.; Beuzelin, J.M.; Reagan, T.E.; Prado, J.A. Efficacy of insect growth regulators and diamide insecticides for control of stem borers (Lepidoptera: Crambidae) in sugarcane. J. Econ. Entomol. 2017, 110, 453–463. [Google Scholar] [CrossRef] [PubMed]
  39. Posey, F.R.; White, W.H.; Reay-Jones, F.F.; Gravois, K.; Salassi, M.E.; Leonard, B.R.; Reagan, T.E. Sugarcane borer (Lepidoptera: Crambidae) management threshold assessment on four sugarcane cultivars. J. Econ. Entomol. 2006, 99, 966–971. [Google Scholar] [CrossRef]
  40. Schexnayder, H.P., Jr.; Reagan, T.E.; Ring, D.R. Sampling for the sugarcane borer (Lepidoptera: Crambidae) on sugarcane in Louisiana. J. Econ. Entomol. 2001, 94, 766–771. [Google Scholar] [CrossRef] [PubMed]
  41. Waguespack, H. Cane Talk. Sugar Bull. 2019, 97, 11–12. [Google Scholar]
  42. Reagan, T.E.; Posey, F.R. A potential stalk borer insecticide management program that enhances biological control. Proc. Int. Soc. Sugar Cane Technol. 2001, 24, 370–373. [Google Scholar]
  43. Reagan, T.E.; Hensley, S.D.; Huffman, F.R.; Fuchs, T.W. Response to insecticides of the sugarcane borer in Louisiana and Texas. J. Econ. Entomol. 1979, 72, 94–96. [Google Scholar] [CrossRef]
  44. Southwick, L.M.; Willis, G.H.; Reagan, T.E.; Rodriguez, L.M. Residues in runoff and on leaves of azinphosmethyl and esfenvalerate applied to sugarcane. Environ. Entomol. 1995, 24, 1013–1017. [Google Scholar] [CrossRef]
  45. Rodriguez, L.M.; Ostheimer, E.A.; Reagan, T.E.; White, W.H. Small plot insecticide trials, 1993. Arthropod Manag. Tests 1994, 19, 278–279. [Google Scholar] [CrossRef]
  46. Regan, T.E.; Gravois, K. Search for a narrow range, minimum-risk insecticide for sugarcane borer control. La. Agric. 2016, 68, 1415. [Google Scholar]
  47. Rodriguez, L.M.; Reagan, T.E.; Ottea, J.A. Susceptibility of the sugarcane borer, Diatraea saccharalis (Lepidoptera: Crambidae) to tebufenozide. J. Econ. Entomol. 2001, 94, 1464–1470. [Google Scholar] [CrossRef]
  48. Rodriguez, L.M.; Ottea, J.A.; Reagan, T.E. Selection, egg viability, and fecundity of the Sugarcane Borer (Lepidoptera: Cambridae) with tebufenozide. J. Econ. Entomol. 2001, 94, 1553–1557. [Google Scholar] [CrossRef]
  49. Reagan, T.E.; Rodriguez, L.M.; Ostheimer, E.A.; Woolwine, A.E.; White, W.H. Comparison of insecticide effects on a braconid parasitoid, Cotesia chilonis, in sugarcane, 1996. Arthropod Manag. Tests 1997, 22, 321. [Google Scholar]
  50. Desneux, N.; Pham-Delègue, M.; Kaiser, L. Effects of sub-lethal and lethal doses of lambda-cyhalothrin on oviposition experience and host-searching behaviour of a parasitic wasp. Aphidius ervi. Pest Manag. Sci. 2004, 60, 381–389. [Google Scholar] [CrossRef] [PubMed]
  51. Beuzelin, J.M.; Akbar, W.; Mészáros, A.; Reay-Jones, F.R.F.; Reagan, T.E. Field assessment of novaluron for sugarcane borer, Diatraea saccharalis (F.) (Lepidoptera: Crambidae), management in Louisiana sugarcane. Crop Prot. 2010, 29, 1168–1176. [Google Scholar] [CrossRef]
  52. Pollet, D.K. Insecticide applications for 2007. In Sugarcane Research Annual Progress Report 2007; LSU AgCenter: Baton Rouge, LA, USA, 2008; p. 137. [Google Scholar]
  53. Akbar, W.; Ottea, J.A.; Beuzelin, J.M.; Reagan, T.E.; Huang, F. Selection and life history traits of tebufenozide-resistant sugarcane borer (Lepidoptera: Crambidae). J. Econ. Entomol. 2008, 101, 1903–1910. [Google Scholar] [CrossRef] [PubMed]
  54. Hardke, J.T.; Temple, J.H.; Leonard, B.R.; Jackson, R.E. Laboratory toxicity and field efficacy of selected insecticides against the fall armyworm (Lepidoptera: Noctuidae). Fla. Entomol. 2011, 94, 272–278. [Google Scholar] [CrossRef]
  55. Lahm, G.P.; Cordova, D.; Barry, J.D. New and selective ryanodine receptor activators for insect control. Bioorg. Med. Chem. 2009, 17, 4127–4133. [Google Scholar] [CrossRef] [PubMed]
  56. Tohnishi, M.; Nakao, H.; Furuya, T.; Seo, A.; Kodama, H.; Tsubata, K.; Fujioka, S.; Kodama, H.; Hirooka, T.; Mishimatsu, T. Flubendiamide, a novel insecticide highly active against lepidopterous insect pests. J. Pestic. Sci. 2005, 30, 304–360. [Google Scholar] [CrossRef]
  57. Gravois, K.; Viator, S.; Reagan, T.E.; Beuzelin, J.M.; Griffin, J.L.; Tubana, B.S.; Hoy, J.W. Sugarcane Production Handbook; Louisiana State University AgCenter: Baton Rouge, LA, USA, 2014; pp. 79–83. [Google Scholar]
  58. Hammond, A.M.; Hensley, S.D. The sugarcane borer sex attractant. Entomophaga 1971, 16, 159–164. [Google Scholar] [CrossRef]
  59. Campion, D.G.; Nesbitt, B.F. The utilisation of sex pheromones for the control of stemborers. Int. J. Trop. Insect Sci. 1983, 4, 191–197. [Google Scholar] [CrossRef]
  60. Wilson, B.E.; Showler, A.T.; Reagan, T.E.; Beuzelin, J.M. Improved chemical control for the Mexican rice borer (Lepidoptera: Crambidae) in sugarcane: Larval exposure, a novel scouting method, and efficacy of a single aerial insecticide application. Field Forage Crops 2012, 105, 1998–2006. [Google Scholar] [CrossRef]
  61. Spurgeon, D.W.; Raulston, J.R.; Lingren, P.D.; Gillespie, J.M. Mating disruption of Mexican rice borers (Lepidoptera: Pyralidae) in lower Rio Grande valley sugarcane. J. Econ. Entomol. 1997, 90, 223–234. [Google Scholar] [CrossRef]
  62. Sauer, R.J.; Reagan, T.E.; Collins, H.L.; Allen, G.; Campt, D.; Canerday, T.D.; LaRocca, G.; Lofgren, C.; Shankland, D.L.; Trestle, M.; et al. Imported fire ant management strategies—Panel 6. In Proceedings of the Symposium on the Red Imported Fire Ant, Atlanta, GA, USA, 7–10 June 1982; EPA/USDA (APHIS): Atlanta, GA, USA, 1982; pp. 91–110. [Google Scholar]
  63. Carson, R. Silent Spring; Haugthtion Mifflin: New York, NY, USA, 1962; p. 377. [Google Scholar]
  64. Tschinkel, W.R. The Fire Ants; Harvard University Press: Cambridge, MA, USA, 2006; pp. 59–60. [Google Scholar]
  65. Reagan, T.E.; Coburn, G.; Hensley, S.D. Effects of mirex on the arthropod fauna of a Louisiana sugarcane field. Environ. Entomol. 1972, 1, 588–591. [Google Scholar] [CrossRef]
  66. Reagan, T.E. Beneficial aspects of the imported fire ant: A field ecology approach. In Fire Ants and Leaf-Cutting Ants, Biology and Management; Lofgren, C., Van der Meer, R.K., Eds.; Westview: Boulder, CO, USA, 1986; pp. 58–71. [Google Scholar]
  67. Fuller, B.W.; Reagan, T.E. Comparative predation of the sugarcane borer (Lepidoptera: Pyralidae) on sweet sorghum and sugarcane. J. Econ. Entomol. 1988, 81, 713–717. [Google Scholar] [CrossRef]
  68. Jemal, A.; Hugh-Jones, M. A review of the red imported fire ant (Solenopsis invicta Buren) and its impacts on plant, animal, and human health. Prev. Vet. Med. 1993, 17, 19–32. [Google Scholar] [CrossRef]
  69. Meagher, R.L., Jr.; Smith, J.W., Jr.; Browning, H.W.; Saldana, R.R. Sugarcane stemborers and their parasites in southern Texas. Environ. Entomol. 1998, 27, 759–766. [Google Scholar] [CrossRef]
  70. Hall, D.G.; Nuessly, G.S.; Gilbert, R.A. Sugarcane Borer in Florida; University of Florida: Gainsville, FL, USA, 2007; pp. 1–6. [Google Scholar]
  71. Showler, A.T.; Reagan, T.E. Ecology and tactics for control of three sugarcane stalk-boring species in the Western Hemisphere and Africa. In Sugarcane: Production and Uses; Goncalves, J.F., Correia, K.D., Eds.; Nova: Hauppauge, NY, USA, 2012; pp. 1–15. [Google Scholar]
  72. White, W.H. Movement and establishment of sugarcane borer (Lepidoptera: Pyralidae) larvae on resistant and susceptible sugarcane. Fla. Entomol. 1993, 76, 465–473. [Google Scholar] [CrossRef]
  73. White, W.H.; Reagan, T.E.; Smith, J.W.; Salazar, J.A. Refuge releases of Cotesia flavipes (Hymenoptera: Braconidae) into the Louisiana sugarcane ecosystem. Environ. Entomol. 2004, 33, 627–632. [Google Scholar] [CrossRef]
  74. Alves, S.B.; Risco, S.H.; Neto, R.M. Pathogenicity of nine isolates of Metarhizium anisopliae (Metsch.) Sorok. To Diatraea saccharalis (Fabr.). J. Appl. Entomol. 1984, 97, 403–406. [Google Scholar] [CrossRef]
  75. Legaspi, B.C., Jr.; Legaspi, J.C.; Lauziere, I.; Jones, W.A.; Saldana, R.R. Jalisco fly as a parasitoid of the Mexican rice borer on different host plants. Southwest. Entomol. 2000, 25, 77–79. [Google Scholar]
  76. Rosas-Garcia, N.M. Laboratory and field tests of spray-dried and granular formulations of a Bacillus thuringiensis strain with insecticidal activity against the sugarcane borer. Pest Manag. Sci. 2006, 62, 855–861. [Google Scholar] [CrossRef]
  77. Beuzelin, J.M.; Wilson, B.E.; VanWeelden, M.T.; Mészáros, A.; Way, M.O.; Stout, M.J.; Reagan, T.E. Biology and management of the Mexican Rice Borer (Lepidoptera: Crambidae) in rice in the United States. J. Integr. Pest Manag. 2016, 7, 1–10. [Google Scholar] [CrossRef]
  78. Beuzelin, J.M.; Reagan, T.E.; Akbar, W.; Cormier, H.J.; Flanagan, J.W.; Blouin, D.C. Impact of Hurricane Rita storm surge on sugarcane borer (Lepidoptera: Crambidae) management in Louisiana. J. Econ. Entomol. 2009, 102, 1054–1061. [Google Scholar] [CrossRef] [PubMed]
  79. Bilskie, M.V. Coastal Flood Risk in a Changing Climate Along the Northern Gulf of Mexico. Master’s Thesis, Louisiana State University, Baton Rouge, LA, USA, 2016. [Google Scholar]
  80. Van der Wiel, K.; Kapnick, S.B.; van Oldenborgh, G.J.; Whan, K.; Philip, S.; Vecchi, G.A.; Singh, R.K.; Arrighi, J.; Cullen, H. Rapid attribution of the August 2016 flood-inducing extreme precipitation in south Louisiana to climate change. Hyddol. Earth Syst. Sci. 2017, 21, 897–921. [Google Scholar] [CrossRef] [Green Version]
  81. Goebel, F.; Nikpay, A. Integrated pest management in sugarcane cropping systems. In Integrated Pest Management in Tropical Regions; Rapisarda, S., Massimino Cocuzza, G.E., Eds.; CAB International: Boston, MA, USA, 2017; pp. 113–129. [Google Scholar]
  82. Dugas, A.L. Recommendations for the control of the sugarcane borer in Louisiana. Sugarcane Bull. 1956, 34, 191–192. [Google Scholar]
  83. Ma, S.; Karkee, M.; Scharf, P.A.; Zhang, Q. Sugarcane harvester technology: A critical overview. Appl. Eng. Agric. 2014, 30, 727–739. [Google Scholar]
  84. White, W.H.; Viator, R.P.; White, P.M. Effect of post-harvest residue and methods of residue removal on ground inhabiting arthropod predators in sugarcane. J. Am. Soc. Sugar Cane Technol. 2011, 31, 39–50. [Google Scholar]
  85. Meyer, E.; Norris, C.P.; Jacquin, E.; Richard, C.; Scandaliaris, J. Burnt versus green cane harvesting: Agricultural engineering challenges. Proc. Int. Soc. Sugarcane Technol. 2005, 25, 294–303. [Google Scholar]
  86. Ali, A.D.; Hudnall, W.H.; Reagan, T.E. Effects of soil types and cultural practices on the fire ant, Solenopsis invicta, in sugarcane. Agric. Ecosyst. Environ. 1986, 18, 63–71. [Google Scholar] [CrossRef]
  87. Flynn, J.L.; Reagan, T.E.; Ogunwolu, W. Establishment and damage of the sugarcane borer (Lepidoptera: Pyralidae) in corn as influenced by plant development. J. Econ. Entomol. 1984, 77, 691–697. [Google Scholar] [CrossRef]
  88. Beuzelin, J.M.; Akbar, W.; Mészárosa, A.; Reay-Jones, F.P.F.; Reagan, T.E. Sugarcane planting date impact on fall and spring sugarcane borer (Lepidoptera: Crambidae) infestations. Crop Prot. 2011, 29, 1168–1176. [Google Scholar] [CrossRef]

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Reagan, T.E.; Mulcahy, M.M. Interaction of Cultural, Biological, and Varietal Controls for Management of Stalk Borers in Louisiana Sugarcane. Insects 2019, 10, 305. https://doi.org/10.3390/insects10090305

AMA Style

Reagan TE, Mulcahy MM. Interaction of Cultural, Biological, and Varietal Controls for Management of Stalk Borers in Louisiana Sugarcane. Insects. 2019; 10(9):305. https://doi.org/10.3390/insects10090305

Chicago/Turabian Style

Reagan, Thomas E., and Megan M. Mulcahy. 2019. "Interaction of Cultural, Biological, and Varietal Controls for Management of Stalk Borers in Louisiana Sugarcane" Insects 10, no. 9: 305. https://doi.org/10.3390/insects10090305

APA Style

Reagan, T. E., & Mulcahy, M. M. (2019). Interaction of Cultural, Biological, and Varietal Controls for Management of Stalk Borers in Louisiana Sugarcane. Insects, 10(9), 305. https://doi.org/10.3390/insects10090305

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