Temporal Occurrence of Plusiinae on Soybean in the Mississippi River Delta

Home , Plusiinae, Rachiplusia, Rachiplusia ou, Trichoplusia

Journal of Economic Entomology, 114(2), 2021, 723–727 doi: 10.1093/jee/toaa308 Advance Access Publication Date: 13 January 2021 Field and Forage Crops Research

K. Clint Allen,1, Nathan S. Little, and Omaththage P. Perera

USDA-ARS, Southern Insect Management Research Unit, 141 Experiment Station Road, Stoneville, MS 38776 and 1Corresponding author, e-mail: [email protected] Downloaded from https://academic.oup.com/jee/article/114/2/723/6092645 by guest on 01 October 2021 Subject Editor: Dominic Reisig

Received 8 September 2020; Editorial decision 3 December 2020

Abstract The subfamily Plusiinae of the moth family Noctuidae is made up 400 species worldwide. Two species of the subfamily, the soybean looper, Chrysodeixis includens (Walker), and the cabbage looper, Trichoplusia ni (Hübner) (Lepidoptera: Noctuidae), are important defoliating insect pests of various field crops and have been the subject of previous Plusiinae surveys in the Southern U.S. Soybean fields were sampled in the Mississippi Delta from 2010 to 2012 to determine the temporal occurrence of various Plusiinae species on soybean. As in previous surveys, C. includens was the most common Plusiinae species in soybean during the 3-yr survey, especially in late season collections (July–September). Rachiplusia ou (Guenée) (Lepidoptera: Noctuidae) was the predominant species observed in early season collections (May–early July). Populations of R. ou during the first sample dates during 2010 were much higher than those observed during the other years of the survey. Only three collected larvae successfully developed into T. ni adults, one each collected during May, June, and July. Although R. ou was not commonly reported in previous studies on soybean, it occurred in low numbers during June and July during the 3-yr study. The temporal occurrence and species composition followed a pre- dictable pattern in all 3 yr of the study.

Key words: Chrysodeixis includens, Trichoplusia ni, Rachiplusia ou, soybean

Plusiinae is a subfamily of the moth family Noctuidae comprised T. ni and C. includens were found on cotton, Gossypium hirsutum of approximately 400 described species worldwide and 76 spe- L. (Malvales: Malvaceae), soybean, Glycine max (L.) (Fabales: cies found in America north of Mexico (LaFontaine and Poole Fabaceae), crucifers (Brassicaceae), peanut (Fabales: Fabaceae), 1991). Adults have a characteristic silver stigma on their forewings, Arachis hypogaea L., sweet potato, Ipomoea batatas (L.) (Solanales: whereas larvae can generally be distinguished from other members Convolvulaceae), and tomato, Solanum lycopersicum L. (Solanoles: of Noctuidae by biordinal crochets with the first two pairs of prolegs Solanaceae). Trichoplusia ni was the predominant species found on missing or vestigial (LaFontaine and Poole 1991). Although larvae cotton and crucifers. Chrysodeixis includens was found in large num- have been described as possessing two pairs of abdominal prolegs, bers in some collections from cotton and was the predominant spe- there is an additional pair on the last abdominal segment (anal cies on soybeans, peanuts, and sweet potatoes (Hensley et al. 1964). prolegs) to make a total of three pairs (Herzog 1980). The larvae are In Louisiana surveys, more than 80% of the loopers collected from commonly referred to as ‘loopers’ and are important pests of vege- cotton were T. ni, whereas more than 90% of the loopers collected table and field crops (Hensley et al. 1964). Two of the most notable from soybean were C. includens (Hensley et al. 1964). In both studies, species within Plusiinae, which are pests of agronomic crops, are the another looper species, Rachiplusia ou (Guenée) (Lepidoptera: cabbage looper, Trichoplusia ni (Hübner), and the soybean looper, Noctuidae), was collected in the spring months on various clovers, Chrysodeixis includens (Walker) (Lepidoptera: Noctuidae). Trifolium spp. (Hensley et al. 1964, Canerday and Arant 1966). During the 1960s and 1970s, surveys were conducted in some In North Carolina, T. ni and C. includens were the only Plusiinae states in the southern United States to determine the species compos- species collected from tobacco, Nicotiana tobacum L. (Solanaceae: ition of Plusiinae on several cultivated crops due to their increased Solanaceae), with T. ni being the most common species early in the occurrence (Hensley et al. 1964, Canerday and Arant 1966, Elsey season. Chrysodeixis includens was seldom found until September, and Rabb 1967). Before these studies, populations of loopers on field which also corresponded to increased populations on soybean crops were generally assumed to be cabbage looper (Hensley et al. (Elsey and Rabb 1967). In the Lower Rio Grande Valley of Texas, 1964, Canerday and Arant 1966). In Alabama, mixed populations of both T. ni and C. includens populations were found throughout

Published by Oxford University Press on behalf of Entomological Society of America 2021. 723 This work is written by (a) US Government employee(s) and is in the public domain in the US. 724 Journal of Economic Entomology, 2021, Vol. 114, No. 2 the year, with peak population of C. includens occurring during natural sunlight through a laboratory window. Caterpillars that sur- August. Trichoplusia ni was collected from 28 host plants, whereas vived to the adult stage were frozen and either pinned or identified C. includens were collected from 22 different host plants (Harding in cups to species based on characteristics described in LaFontaine 1976). In northern Florida, overall populations of T. ni were greater and Poole (1991). than populations of C. includens. Trichoplusia ni had a strong Soybean fields were sampled from the last week of May until preference for cabbage, Brassica oleracea var. capitata L., and col- September. Within a particular year, two to three soybean fields were lards, Brassica oleracea var. viridis L. (Brassicales: Brassicaceae) sampled within a County on a weekly basis. During 2010, fields were whereas C. includens were the predominant species on soybean sampled in Madison and Washington Counties, MS, and Desha County, (Martin et al. 1976). AR. During 2011, soybean fields were sampled in Holmes, Sunflower Other studies followed that examined the species composition and Washington Counties, MS and Desha County, AR. During 2012, of loopers particularly on soybean. During 1982–1983, Beach and soybean fields located in Coahoma, Holmes, Tunica, Warren, and Todd (1987) found 98% of the looper populations in Georgia on Washington Counties, MS and Desha County, AR, were sampled. soybean were C. includens during July–September. The few T. ni Looper densities and species composition, based on collected individ- that were collected occurred earlier in the season and a single spe- uals surviving to adult, were recorded throughout the growing season. Downloaded from https://academic.oup.com/jee/article/114/2/723/6092645 by guest on 01 October 2021 cimen of R. ou was collected during July. Beach and Todd (1986) Additionally, in 2010 and 2011, the thoracic leg color of loopers were also noted that higher densities of C. includens were found in soy- recorded as either ‘green’ or ‘black’. For sample dates where at least bean fields with cotton fields nearby compared with soybean fields 10 loopers were collected and the leg color recorded from individual with no cotton in the near vicinity. In Mississippi, Jost and Pitre fields, correlation analysis was used to examine relationships between (2002) found mixed populations of T. ni and C. includens larvae in leg color and looper density during 2010 and 2011 and for both years cotton and soybean, with more T. ni larvae found in cotton and more combined using PROC CORR (SAS Institute 2014). C. includens in soybean. Much has changed regarding the cropping landscape in the Southern United States since the previous Plusiinae surveys were Results conducted. Due to the introduction of transgenic crops and the chan- 2010 ging crop mixes, we conducted a 3-yr survey to examine potential Of the 3,083 Plusiinae larvae collected, 966 developed into moths differences in the Plusiinae composition on soybean compared with and were identified (Table 1). During the last week of May, higher many of the studies that were reported 40–50 yr ago. An increased densities of R. ou were encountered than at any other week during understanding of the temporal occurrence of looper species can aid the 3 yr of the survey. The last R. ou was collected on 8 July, whereas in making appropriate management decisions for their control. The the first C. includens was collected on 24 June (Fig. 1). A single larva objective of this study was to examine patterns in the occurrence of developed into a T. ni adult, and this was collected on 21 May. various looper species on soybean in the Mississippi Delta.

2 011 Materials and Methods Densities of Plusiinae larvae were lower than those observed in From 2010 to 2012, soybean fields in the Mississippi Delta were 2010. Of the 774 larvae collected, 306 successfully developed and sampled to examine the diversity and abundance of arthropods emerged as moths (Table 1). Populations were low during most of using a 38-cm-diameter sweep net. On each sample date, at least the soybean growing season and then peaked during the first 2 wk six sets of 25 sweeps were used to estimate the number of caterpil- of September (Fig. 1). Rachiplusia ou larvae were collected in low lars and those with three sets of abdominal prolegs (one pair on the numbers from 24 May through 27 July. Larvae of C. includens were last abdominal segment and two additional pairs) were recorded as collected from 7 July through the end of sampling on 22 September. ‘loopers’. Either all or a subset of caterpillars (depending on density) There were no T. ni larvae that were collected and successfully were collected and placed singly in 20-ml plastic cups filled with a reared to adults. wheat germ-based artificial diet (Shaver and Raulston 1971, Blanco et al. 2009) and cups capped with a cardboard lid. Cups were la- 2012 beled by location and sample date and transported back to the la- In total, 1,124 Plusiinae larvae were collected during 2012 and boratory. Caterpillars were reared in the laboratory at ~24°C using 570 survived to the adult stage and were identified (Table 1).

Table 1. Plusiinae species collected from soybean fields in the Mississippi Delta from 2010 to 2012

May June July Aug. Sept. Total

2010 Chrysodeixis includens 0 1 64 689 21 775 Rachiplusia ou 171 15 4 0 0 190 Trichoplusia ni 1 0 0 0 0 1 2011 Chrysodeixis includens 0 0 9 133 121 263 Rachiplusia ou 1 29 13 0 0 43 Trichoplusia ni 0 0 0 0 0 0 2012 Chrysodeixis includens 0 0 221 321 — 542 Rachiplusia ou 7 6 13 0 — 26 Trichoplusia ni 0 1 1 0 — 2 Journal of Economic Entomology, 2021, Vol. 114, No. 2 725 Downloaded from https://academic.oup.com/jee/article/114/2/723/6092645 by guest on 01 October 2021

Fig. 1. Plusiinae larvae collected in soybean fields in the Mississippi Delta from 2010 to 2012.

Fig. 2. Species composition of Plusiinae larvae collected from soybean fields in the Mississippi Delta from 2010 to 2012.

Rachiplusia ou were collected from 16 May through 26 July, relationship (r = 0.1544; n = 13; P = 0.6146) between black leg color whereas C. includens were collected from 2 July through the last and looper density in the fields examined. During 2011, an additional sample date of 29 August. Two T. ni larvae survived and emerged as 13 field collections from 1 August through 13 September were used moths. These were collected on 15 June and 2 July from the same to examine the relationship between field densities and presence of field in Sunflower Co., MS (Fig. 2). black thoracic legs. Looper densities ranged from 2 to 45.6 loopers per 100 sweeps (Fig. 3). A significant positive relationship between looper density and individuals possessing black thoracic legs was ob- Thoracic Leg Color and Density served during 2011 (r = 0.7053; n = 13; P = 0.0071). For both years Since soybean loopers can exhibit both black and green thoracic legs, combined (2010–2011), a positive, but not significant relationship the leg color of collected soybean loopers was recorded and matched was observed (r = 0.2253; n = 26; P = 0.2685). to densities from sweep net samples within a given field during 2010 and 2011 (Fig. 3). During 2010, over a 3-wk period, from 10 August through 31 August, 13 different individual field collections were exam- Discussion ined for the percentage of soybean loopers possessing black legs and Previous papers have examined the species of Plusiinae inhabiting the sampled densities of loopers in those fields. Densities ranged from crop hosts in the southern United States (Hensley et al. 1964; 2.7 to 136 loopers per 100 sweep net samples (Fig. 3). For 2010, cor- Canerday and Arant 1966; Elsey and Rabb 1967; Burleigh 1972; relation analysis revealed that there was a positive but nonsignificant Beach and Todd 1986, 1987; Jost and Pitre 2002). In soybean, many 726 Journal of Economic Entomology, 2021, Vol. 114, No. 2 Downloaded from https://academic.oup.com/jee/article/114/2/723/6092645 by guest on 01 October 2021

Fig. 3. Proportion of loopers with black thoracic legs at various sampling densities in soybean fields in the Mississippi Delta during 2010–2011. of these studies examined species during later parts of the growing were C. includens. Populations of T. ni were more prevalent on soy- season and may have missed low populations of early season bean in these studies compared with only three T. ni larvae collected loopers, especially R. ou that were found in this study. During the from soybean and reared to adults in the current study. Besides first year of the survey, high populations of R. ou were observed random cyclical fluctuations in the occurrence of populations of during the first two sample dates when soybeans had first started T. ni, which may represent the differences between the studies, blooming and these were the highest populations encountered. changes in the agricultural landscape may also explain decreased Consistently low populations of R. ou were collected during May numbers of T. ni on soybean. One of the most notable differences is through the middle of July in all 3 yr of the study. Previous studies the introduction of cotton varieties expressing insecticidal proteins on the biology of R. ou detailed the survival and developmental from the soil bacterium, Bacillus thuringiensis (Berliner). Since Bt time of this insect in the laboratory (Mitchell 1966, Canerday and cotton varieties were grown on the vast percentage of cotton acres in Arant 1967), but little information is available regarding its biology the present study area and it had not yet been introduced when the and development on field crops. Previous surveys have noted its previous studies were conducted, it potentially impacts more recent presence early in the year on crimson clover, Trifolium incarnatum T. ni populations occurring on soybean. This is especially true for L. (Fabales: Fabaceae) (Hensley et al. 1964, Canerday and Arant T. ni that use cotton to increase populations that move to soybean 1966). Other recorded host plants include nasturtium, Trapaeolum later in the growing season. spp., cosmos, Cosmos spp., and wormseed, Dysphania anthelmintica There has been some confusion with regards to the identification (L.) (Caryophyllales: Chenopodiaceae) (Crumb 1956, Eichlin and of C. includens and T. ni based on the thoracic leg color of larvae. Cunningham 1969). Rachiplusia ou has been recorded as a pest of Hensley et al. (1964) noted that soybean loopers had often been spearmint, Mentha spicata L., and peppermint, Mentha xpiperita referred to as ‘the black legged looper’ and they observed that leg L. (Lamiales: Lamiaceae), in Indiana (Gould 1960). It has also been coloration in the progeny of a single female was variable. Jost and reported on the field crops tobacco (Crumb 1956), wheat, Triticum Pitre (1998) examined thoracic leg colors of soybean and cabbage aestivum L. (Cyperales: Poaceae) (Eichlin and Cunningham 1969), loopers for potential use in species identification from a few fields a single specimen collected on cotton (Hensley et al. 1964), and in Mississippi. They described this technique as unreliable for field one collected on soybean in Georgia during July (Beach and Todd identification but observed that the black coloration of thoracic legs 1987). Jones and Duckworth (2017) also reference unpublished in soybean loopers appeared to be more prevalent at higher densities. data on its presence on cotton and soybean. Most information pub- In the current study, we observed a positive relationship in 1 of 2 lished regarding R. ou are related to the pathogenicity of a nuclear yr (2011) with respect to soybean looper densities and proportion polyhedrosis virus isolated from this insect to other lepidopteran of larvae exhibiting black thoracic legs. During 2010, a relatively insect pests (i.e., Paschke and Sweet 1966, Lewis and Adams 1979). high density compared with other sampling points (136 larvae/100 Previous examinations of Plusiinae on cotton and soybean in the sweeps) resulted in only approximately 29% of the looper collected Southern United States have reported mixed populations of T. ni and population with black thoracic legs (Fig. 3). Other variables such C. includens (Hensley et al. 1964, Canerday and Arant 1966, Jost as age of the collected population or other abiotic factors may play and Pitre 2002). In both studies, the majority of Plusiinae caterpillars a role in the green versus black pigmentation present in soybean collected from cotton were T. ni and those collected from soybean looper larvae. Journal of Economic Entomology, 2021, Vol. 114, No. 2 727

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