A New Detection of the Invasive Mexican Rice Borer (Lepidoptera: Crambidae) From Georgia in the United States Based on Morphological and Molecular ...
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Journal of Integrated Pest Management, (2022) 13(1): 17; 1–5 https://doi.org/10.1093/jipm/pmac014 Brief Communication A New Detection of the Invasive Mexican Rice Borer (Lepidoptera: Crambidae) From Georgia in the United States Based on Morphological and Molecular Data Ilgoo Kang,1 Blake Wilson,2,4, Blake Carter,3 and Rodrigo Diaz1 1 Department of Entomology, Louisiana State University Agricultural Center, 404 Life Sciences Building, Baton Rouge, LA, USA, 2 Louisiana State University AgCenter, Sugar Research Station, Saint Gabriel, LA, USA, 3University of Georgia Extension Service, Downloaded from https://academic.oup.com/jipm/article/13/1/17/6590884 by guest on 16 June 2022 Effingham County, Rincon, GA, USA, and 4Corresponding author, e-mail: bwilson@agcenter.lsu.edu Subject Editor: Thomas Kuhar Received 7 February 2022; Editorial decision 12 March 2022 Abstract The Mexican rice borer, Eoreuma loftini (Dyar), is an invasive herbivore that attacks many gramineous host plants. The species is an economic pest of several grass crops in North America including sugarcane (Saccharum spp.), rice (Oryza sativa), corn (Zea mays), and sorghum (Sorghum bicolor).The species was first detected in the United States in 1980 and has since expanded its range eastward along the Gulf Coast reaching Louisiana in 2008. A disjointed introduction was detected in Florida in 2012, though range expansion of this population within the state has been limited. Most recently, a separate introduction was detected along the Atlantic coast of Georgia near the South Carolina border (32.19884° N, 81.35894° W). Larvae were collected from sugarcane in 2020 and 2021 and identified as E. loftini.The identification was confirmed with genetic analysis showing >99% similarity with most mitochondrial cytochrome c oxidase subunit 1 (COI) sequences of known E. loftini. This is the furthest north and east of any established population in North America. Potential routes of introduction and impacts to crop production along the U.S. Atlantic Coast are discussed. Key words: Eoreuma loftini, invasive species, range expansion, Saccharum spp., sugarcane The Mexican rice borer, Eoreuma loftini (Dyar) (Fig. 1), is an in- 1984; Fig. 2). Initial detection of E. loftini in the Rio Grande Valley vasive crop pest that has been expanding its range northward and of Texas occurred in 1980 after numerous interceptions of larvae eastward into the United States. The species is an economic threat to in plant material at U.S. ports of entry. While establishment in the production of grass crops including sugarcane (Saccharum spp.), rice region is often attributed to introduction of infested plant material, (Oryza sativa), corn (Zea mays), and sorghum (Sorghum bicolor). evidence suggests the expansion may have occurred unaided. The Invasion of E. loftini may also have ecological consequences as the species was known to be present in the Mexican border states of stem borer also attacks a broad range of non-crop grasses. The first Nuevo Leon and Tamaulipas in the late 1970s, and many of the record of E. loftini in the U.S. state of Georgia is reported herein. border interceptions occurred from plant material that originated within a few km of the U.S. border (Johnson 1984). Further, the initial detection in Texas occurred when severe larval infestations Monitoring and Spread of E. loftini Along the were observed in sugarcane, suggesting that populations were likely Gulf Coast building in the area for some time prior to discovery. The native range of E. loftini is thought to be western Mexico north Following its initial detection in Hidalgo County, Texas, E. loftini to Arizona and southern California where its presence was noted in expanded its range in a northeastern direction at an average rate association with sugarcane (Dyar 1917, Morill 1925), rice, and nu- of 23.0 km/year, reaching the westernmost edge of the Texas rice merous non-crop grasses (Osborn and Phillips 1946). Although the production area in 1989 (Browning 1989, Reay-Jones et al. 2007). crops that serve as hosts have not been produced in this region for Development of pheromone traps capable of detecting male E. loftini decades, museum specimens reared from larvae collected from non- even at low population densities in the early 1990s greatly improved crop hosts indicate the species remains present in the region (Univ. monitoring efforts (Shaver et al. 1990, 1991). Range expansion con- Cal. Riverside, Entomol. Res. Mus., personal communication). The tinued with the leading edge of the invasion moving approximately species is thought to have spread to eastern Mexico in the 1960s and 16.5 km/year from 2000 to 2005 (Reay-Jones et al. 2007) reaching 1970s following the expansion of sugarcane to the region (Johnson Louisiana in 2008 (Hummel et al. 2010). The eastward spread © The Author(s) 2022. Published by Oxford University Press on behalf of Entomological Society of America. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), 1 which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
2 Journal of Integrated Pest Management, 2022, Vol. 13, No. 1 through southwestern Louisiana from 2008 to 2015 occurred at a rate of 17.9 km/year (Wilson et al. 2015, 2017a). By 2020, the insect had spread to 16 parishes in Louisiana with expansion continuing predictably into key crop-producing regions of the state (Wilson and Huval 2020). Thus, monitoring efforts indicate that range expan- sion in the Unites States occurred at consistent rates, presumably unaided, for 40 years. The first evidence of disjunct range expansion occurred in 2012 when E. loftini was detected in a light trap in Levy County in central Florida (Hayden 2012). The source of this population and mech- anism of spread is unknown, but the establishment in Florida ap- pears to have been the result of a single isolated introduction. Initial distribution and population density in Florida were relatively limited indicating the detection occurred not long after establishment. The population has since begun to expand towards the southeast, though Downloaded from https://academic.oup.com/jipm/article/13/1/17/6590884 by guest on 16 June 2022 this expansion has occurred at slower rates than those observed in Texas and Louisiana (VanWeelden et al. 2019). Pheromone trap detections were reported from Marion County (2013), Citrus and Sumter Counties (2014), and Lake County (2019). Expansion in Florida has remained slow. No northward spread has been detected since 2014, and expansion southward was only 14 km from 2015 to 2019 (J. Beuzelin, personal communication). Currently, E. loftini is not an economic pest in Florida as the established population re- mains more than 160 km away from areas of commercial production of susceptible grass crops. However, expansion into the Everglades Agricultural Area where sugarcane, rice, and sweet corn are widely cultivated could have large economic impacts (Fig. 3). No active monitoring programs are currently conducted outside Fig. 1. Mexican rice borer, Eoreuma loftini (Dyar) (Lepidoptera: Crambidae), of Louisiana and Florida. Expansion northward and westward in larva feeding in a sugarcane stalk (top) and adult on a leaf (bottom). Texas may be occurring simultaneously with eastward expansion Fig. 2. Geographical range expansion of E. loftini in North America. Records compiled from (Johnson 1984, Browning 1989, Reay-Jones et al. 2007, and Wilson et al. 2015, 2017a).
Journal of Integrated Pest Management, 2022, Vol. 13, No. 1 3 Downloaded from https://academic.oup.com/jipm/article/13/1/17/6590884 by guest on 16 June 2022 Fig. 3. Eoreuma loftini detection site in the U.S. state of Georgia, 2020 and 2021. into Louisiana. Monitoring in adjacent states in the southeastern were from S. halepense and P. urvillei, both of which are considered United States for potential human-aided introductions is not cur- invasive pests in the southern United States (Beuzelin et al. 2011). rently conducted, but may be warranted if spread continues Population declines of other crambid stem borers have been reported unpredictably. following establishment of E. loftini in parts of Mexico (Rodriguez- del-Bosque et al. 2011), although these declines may have resulted from changes in natural enemy communities rather than competitive Eoreuma loftini Ecological and displacement. While ecological impacts following establishment of Economic Impacts E. loftini are thought to be minimal in most regions, more research Eoreuma loftini is a polyphagous stem borer which attacks nu- into this area is needed. merous crop and non-crop grasses in the family Poaceae (Beuzelin et al. 2016a, Showler 2019). Crop hosts include corn (Zea mays), Establishment in Georgia sugarcane (Saccharum spp.), rice (Oryza sativa), and sorghum (Sorghum bicolor) in decreasing order of host preference (Showler Initial alert of potential detection of E. loftini in Georgia occurred et al. 2012). Detections have also been reported from wheat as the result of a post to a social media group for producers of (Triticum aestivum) in Texas, though its pest status in the crop is sugarcane syrup in the southeastern United States. Photos showed unknown. Key non-crop grass hosts include johnsongrass (Sorghum larvae with great resemblance to E. loftini along with larval injury halepense), vaseygrass (Paspalum urvillei), brome (Bromus spp.), and consistent with that caused by the species to sugarcane in Louisiana others (Beuzelin et al. 2011, 2013, 2016a). Many other grass species and Texas (B. E. Wilson, personal observation). Contact was made have also been reported as hosts, with early reports suggesting any with the private citizen making the initial post who confirmed her lo- grass species with sufficient stem size to support larvae feeding could cation in Effingham County, Georgia, USA and agreed to assist with be attacked (Van Zwaluwenburg 1926, Beuzelin et al. 2016a). specimen collection. Six larvae and one pupa were collected from the Economic impacts result from damaging infestations that can sugarcane patch on 1 December 2020, stored in alcohol, and shipped occur in crop hosts. Yield loss of up to 15% has been reported from to the Louisiana State University Department of Entomology (Baton unmitigated infestations in rice in Louisiana and Texas (Reay-Jones Rouge, LA). et al. 2007, Wilson et al. 2021). Losses in sugarcane have been re- We confirmed the first distribution record of E. loftini from Georgia, ported to be 15–25% (Wilson et al. 2012, Showler and Reagan USA based on both morphological and molecular data. In morphological 2017). Economic impacts to corn and sorghum are less well studied, analysis conducted in 2021, each specimen was examined under a micro- but plant death has been reported to result from extensive internal scope. Larvae of E. loftini were distinguished from other crambid larvae feeding in plants of both crops (Showler et al. 2012). by the presence of a single subventral seta on the meso- and metathorax Ecological impacts of E. loftini in non-crop habitats have not (Beuzelin et al. 2016a). Additional photos from the same field were pro- been well-studied. The species is known to utilize native and inva- vided in September of 2021 and also determined to be E. loftini. To iden- sive grasses along the U.S. Gulf Coast, particularly during winter tify the specimens using molecular method, a 658bp fragment of the when crop hosts are not available (Beuzelin et al. 2011, 2013). While mitochondrial cytochrome c oxidase subunit I gene (COI) of each insect the species has been found in densities of >3 larvae/m2 in non-crop was targeted and amplified using a primer set, LepF1 and LepR1, devel- habitats in invaded regions, these populations are not likely to be oped by. DNA was extracted from larval and pupal specimens using the sufficient to alter plant communities. Further, the primary grasses DNeasy Blood and Tissue Kit (QIAGEN, Hilden, Germany) and amp- from which E. loftini was recovered in non-crop habitats of Texas lified by polymerase chain reactions (PCR). PCR volumes were 25 µl
4 Journal of Integrated Pest Management, 2022, Vol. 13, No. 1 containing 12.5 µl of DreamTaq Green PCR Master Mix (2X) (Thermo The mode of introduction of E. loftini into Georgia is unknown, Scientific), 1–2 µl of template genomic DNA, 9.5 µl of ddH2O, and 1.0 µl though the apparent disjunct expansion suggests that human-aided of each primer at 5–10 µM. PCR conditions were 95°C for 3 min; 5 movement is a likely cause. Movement of infested plant material is initial cycles of 95°C for 30 s, 45°C for 30 s, 72°C for 1 min; 35 cycles the primary mode of introduction for invasive herbivores (Hulme of 95°C for 30 s, 51°C for 30 s and 72°C for 1 min; and a final ex- 2009). Although the initial detection occurred in sugarcane, this does tension at 72°C for 7 min. Crude PCR products were visualized on a not necessarily implicate movement of sugarcane in the spread to 1.8–2.0% agarose gels to confirm the success of amplification sent to the Georgia. Infestations of E. loftini in sugarcane in Florida have not LSU genomics facility. PCR products were initially cleaned by a EtOH been reported, so transportation of sugarcane from the region would precipitation clean-up method developed by the facility and sequenced not likely have contributed to the spread. Infested sugarcane imports on the 3130xl Genetic Analyzers (Applied Biosystems) using the BigDye could have come from the much more distant sources in western Terminator v1.1 chemistry (Applied Biosystems). DNA assembly and Louisiana or the Rio Grande Valley of Texas, but transportation of sequence editing were conducted using Geneious Prime 2019.2 (https:// sugarcane more than 1,000 km seems unlikely with closer sources www.geneious.com). The obtained sequences were compared with COI available. Further, the species may have been present in Georgia for sequences of E. loftini deposited in the GenBank database of the National several years, infesting many of the suitable weedy grass hosts before Center for Biotechnology Information (NCBI) using the Basic Local detection in crop plants. Movement of grass materials such as hay or Downloaded from https://academic.oup.com/jipm/article/13/1/17/6590884 by guest on 16 June 2022 Alignment Search Tool (BLAST). other forages for livestock feed is one possible means of transportation. Using BLAST, we confirmed that all the newly obtained COI Florida is a major producer of hay forage with more than 100,000 ha sequences were ~99% (Paspalum spp.) which are the known hosts of E. loftini (Chambliss matched with seven deposited sequences obtained from specimens et al. 2006, Beuzelin et al. 2016a). While most of this hay is sold as collected in Texas (Weslaco, Hidalgo), Louisiana (Baton Rouge), livestock fodder within Florida, it can generally be transported out of Florida, northwestern Mexico (Los Mochis, Sinaola), and >~97% state without restriction (USDA APHIS 2021). Unfortunately, deter- matched with three deposited sequences obtained from specimens mination of the mode of introduction with any degree of certainty is collected in the south-central region of Mexico (Zacatepec, Morelos). not possible. Future studies could, however, identify the source popu- The molecular data indicate the E. loftini population introduced to lation through genetic analyses and comparisons to known popula- Georgia is closely related with U.S. populations and the population tions from Texas, Louisiana, Florida, and Mexico. from northwestern Mexico. Additionally, we confirmed that utilizing Economic impacts to crop production in Georgia and surrounding COI barcoding helps quick and accurate identification of E. loftini. states are possible in coming years. Georgia currently produces ap- Because COI barcodes obtained from E. loftini collected in proximately 190,000 ha of corn and 90,000 ha of wheat with com- Louisiana and Texas are not available on the GenBank yet, it is not parable production of both crops in nearby South Carolina (USDA possible to determine the potential origins of the population intro- NASS 2021). More than >80% of the corn hectares in Georgia are duced into Georgia. planted with insecticidal Bacillus thuringiensis (Bt) varieties (Buntin This detection represents a significant range expansion appearing 2021). Transgenic Bt corn varieties that are effective against other corn to result from a new introduction. The extent of the established range stalk borers should also minimize losses from E. loftini (Showler et al. in Georgia remains unknown. Pheromone trap monitoring programs 2013, Beuzelin et al. 2016b). Increased economic losses are likely to should be established following the methods of Wilson et al. (2015, occur to non-Bt refuge corn in regions where E. loftini becomes estab- 2016, 2017a, 2017b) to delineate the extent of the invaded range in lished, however (Showler et al. 2012). The prevalence of irrigation in Georgia and possibly South Carolina. Georgia corn production may limit E. loftini infestations as the pest is The location of the Effingham County detection is approxi- exacerbated in drought conditions (Reay-Jones et al. 2008, Showler mately 400 km (250 miles) north of the closest known population and Castro 2010). Approximately, 90% of field corn is irrigated in in Sumter County, Florida. Effingham county lies north of the 32nd the Coastal Plain region surrounding the E. loftini detection site in parallel, approximately 130 km north of the northern most loca- Effingham County (Bryant 2021). Sweet corn and sugarcane grown tion in Louisiana where the species is known to occur (Wilson and for syrup production will also be at risk of infestation, but these crops Huval 2020). This indicates that the species may be capable of col- are not produced on a commercial farm scale in Georgia. onizing more temperate regions than other sugarcane stem borers such as the sugarcane borer, Diatraea saccharalis (F.). Indeed, the cold tolerance of E. loftini populations in Mexico was found to be Acknowledgments greater than both D. saccharalis and the neotropical corn stalk borer, We express gratitude to citizen scientists for their willingness to assist in Diatraea lineolata (Walker) (Rodriguez-del-Bosque et al. 1995). specimen collection. Additional thanks are in order to Randy Richard for pro- Based on its current known distribution, it is likely the species is cap- viding the initial alert. This work was funded in part by the USDA NIFA Foun- able of inhabiting the southern latitudes of Mississippi and Alabama. dational Grant 1027792, USDA Hatch funds, and the American Sugarcane Assuming these regions are suitable for E. loftini establishment, their League. This publication is approved by the Louisiana State University Agri- colonization in coming years is likely. The rate of expansion during cultural Center (LSU-MS-2022-270-36697). biological invasions generally increases with increasing size and number of source populations (O’Reilly-Nugent et al. 2016). With References Cited expansion in the southeastern United States now probable on three Beuzelin, J. M., A. Mészáros, T. E. Reagan, L. T. Wilson, M. O. Way, invasion fronts (Louisiana, Florida, and Georgia), continued estab- D. C. Blouin, and A. T. Showler. 2011. Seasonal infestations of two stem lishment throughout the region appears plausible. More research borers (Lepidoptera: Crambidae) in non-crop grasses of Gulf Coast rice into E. loftini cold tolerance and potential invasive range models agroecosystems. Environ. Entomol. 40: 1036–1050. including climatic data are needed to determine the extent of the Beuzelin, J. M., L. T. Wilson, A. T. Showler, A. Mészáros, B. E. Wilson, species possible spread in the southeastern United States. M. O. Way, and T. E. Reagan. 2013. Oviposition and larval development
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