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Spodoptera eridania (Lepidoptera: Noctuidae): first report on Amaranthus hybridus (Amaranthaceae) in Brazil

Abstract:

Background:

Amaranthus hybridus L. (Amaranthaceae) is an annual, dicotyledonous species that is considered one of the main weed infesting agricultural production systems. Some weeds species are considered host plants to insect pests, serving as “green bridges” for subsequent attacks on the main crop during the season, which can cause significant losses. Recording the occurrence of insects that can reach pest status is important for the deployment of mitigation measures against possible damage and economic losses to crops. The presence of Spodoptera eridania (Cramer) (Lepidoptera: Noctuidae) has not been previously registered in association with A. hybridus plants.

Objective:

Thus, the present study is the first report to describe the occurrence of S. eridania on A. hybridus in the municipality of Piracicaba, São Paulo, Brazil.

Methods:

Images of the larvae while feeding on A. hybrids were obtained using an Olympus® E-410 digital camera. The pictures were then sent to the Laboratory of Ecotoxicology and IPM (LEMIP) of the Department of Entomology of Lavras Federal University (UFLA) for species identification.

Results:

We observed S. eridania larvae larger than 7 cm feeding on the inflorescences and leaves of A. hybridus .

Conclusions:

This note reports the first occurrence of S. eridania larvae feeding on A. hybridus in the city of Piracicaba, SP, Brazil.

Keywords:
Invasive plant; Pest arthropod; Interaction; Infestation; Injury

In Brazil there is a complex of caterpillars of the genus Spodoptera that cause direct damage to many crops of economic importance, such as corn, cotton, and soybean ( Hoffmann-Campo et al., 1985Hoffmann-Campo CB, Oliveira EB, Moscardi F. [Soybean caterpillar mass rearing ( Anticarsia gemmatalis )]. Londrina: Empresa Brasileira de Pesquisa Agropecuária; 1985. Portuguese. ; Santos et al., 2005Santos KB, Meneguim AM, Neves PMOJ. [Biology of Spodoptera eridania (Cramer) (Lepidoptera: Noctuidae) in different hosts]. Neotrop Entomol. 2005;34(6):903-10. Portuguese. Available from: https://doi.org/10.1590/S1519-566X2005000600005
https://doi.org/10.1590/S1519-566X200500...
; Bueno et al., 2011Bueno RCOF, Bueno AF, Moscardi F, Parra JRP, Hoffmann-Campo CB. Lepidopteran larvae consumption of soybean foliage: basis for developing multiple-species economic thresholds for pest management decisions. Pest Manag Sc. 2011;67(2):170-4. Available from: https://doi.10.1002/ps.2047
https://doi.10.1002/ps.2047...
; Favetti et al., 2015Favetti BM, Butnariub AR, Foerster LA. Biology and reproductive capacity of Spodoptera eridania (Cramer) (Lepidoptera, Noctuidae) in different soybean cultivars. Rev Bras Entomol. 2015;59(2):89-95. Available from: https://doi.org/10.1016/j.rbe.2015.03.002
https://doi.org/10.1016/j.rbe.2015.03.00...
; Silva et al., 2017Silva DM, Bueno AF, Stecca CS, Andrade K, Neves PMOJ, Oliveira MCN. Biology of Spodoptera eridania and Spodoptera cosmioides (Lepidoptera: Noctuidae) on different host plants. Flo Entomol. 2017;100(4):752-60. Available from: https://doi.org/10.1653/024.100.0423
https://doi.org/10.1653/024.100.0423...
). The species Spodoptera eridania (Cramer) (Lepidoptera: Noctuidae) is often present in these crops and others attacking both vegetative and reproductive plant tissues ( Santos et al., 2005Santos KB, Meneguim AM, Neves PMOJ. [Biology of Spodoptera eridania (Cramer) (Lepidoptera: Noctuidae) in different hosts]. Neotrop Entomol. 2005;34(6):903-10. Portuguese. Available from: https://doi.org/10.1590/S1519-566X2005000600005
https://doi.org/10.1590/S1519-566X200500...
). The polyphagous habit of S. eridania contributes to considerable economic losses in agricultural host crops as it quickly adapts to different agroecosystems, being this lepidopterous considered one of the most polyphagous species ( Soo Hoo, Fraenkel, 1966Soo Hoo CF, Fraenkel G. The selection of food plants in a polyphagous insect, Prodenia eridania (Cramer). J Insect Physiol. 1966;2(6):693-709. http://doi.org/10.1016/0022-1910(66)90115-6
http://doi.org/10.1016/0022-1910(66)9011...
; Bortolotto et al., 2014Bortolotto OC, Silva GV, Bueno AF, Pomari A F, Martinelli S, Head GP et al. Development and reproduction of Spodoptera eridania (Lepidoptera: Noctuidae) and its egg parasitoid Telenomus remus (Hymenoptera: Platygastridae) on the genetically modified soybean (Bt) MON 87701 x MON 89788. Bull Entomol Res. 2014;104(6):724-30. Available from: https://doi.org/10.1017/S0007485314000546
https://doi.org/10.1017/S000748531400054...
).

Adult female S. eridania lays spherical eggs that are greenish when newly laid, with the embryonic period lasting on average four to six days. The larval period consists of six instars, and the larvae can reach 35 mm in length at the end of the phase; larvae are green or blackish-green with a light brown or reddish-brown head capsule. As larvae develop, they have a narrow dorsal white line and lateral stripes, with a yellowish or whitish stripe on each side of the body, which is interrupted by a dark spot on the first abdominal segment. A series of dark triangles may be present dorso-laterally along the body length. The larval stage can last from 14 to 20 days depending on abiotic factors, especially temperature. Larvae pupate in soil, and the pupae are brown, measuring 16 to 18 mm in length, and the pupal period lasts 11 to 13 days. The adult is a light-gray moth with wingspan of approximately 40 mm, with grayish or straw-yellow forewings with a black dot on the center, while the hind wings are whitish (Capinera, 2011; 2018Capinera JL. Common name: southern armyworm. Featured Creatures: Entomology & Nematology. 2018[access Jan 1, 2022]. Available from: http://entnemdept.ufl.edu/creatures/veg/leaf/southern_armyworm.htm
http://entnemdept.ufl.edu/creatures/veg/...
; Bragard et al., 2020Bragard C, Dehnen-Schmutz K, Di Serio F, Gonthier P, Jacques M, Jaques Miret JA et al. Pest categorisation of Spodoptera eridania . EFSA J. 2020;18(1):1-29. Available from: https://doi.org/10.2903/j.efsa.2020.5932
https://doi.org/10.2903/j.efsa.2020.5932...
).

The biotic potential and reproductive parameters of S. eridania were evaluated by Montezano et al. (2013)Montezano DG, Specht A, Sosa-Gómez DR, Roque-Specht VF, Barros NM. Biotic potential and reproductive parameters of Spodoptera eridania (Stoll) (Lepidoptera: Noctuidae) in the laboratory. Rev Bras Entomol. 2013;57(3):340-5. Available from: https://doi.org/10.1590/S0085-56262013005000026
https://doi.org/10.1590/S0085-5626201300...
in the laboratory, with an artificial diet adapted from Hoffmann-Campo et al. (1985)Hoffmann-Campo CB, Oliveira EB, Moscardi F. [Soybean caterpillar mass rearing ( Anticarsia gemmatalis )]. Londrina: Empresa Brasileira de Pesquisa Agropecuária; 1985. Portuguese. . At the conditions of 25 ± 1 °C, 70 ± 10% RH, and 14-h photophase, the longevity of females was on average 10.80 days, and 9.27 days for males. Pre- and post-oviposition, and oviposition periods were 2.07, 0.6, and 8.13 days, respectively. Mean female fecundity was 1,398 eggs, and the viability was 97.8%. Spodopera eridania showed high biotic potential, being estimated at 1.894 × 1025 individuals per female-1.year-1, which indicates a strong capacity to increase its population size in agricultural crops and to cause substantial economic losses.

Larvae of S. eridania are voracious, and the adults have high reproductive capacity. Larvae of S. eridania have polyphagous habit and can cause damage to crops by causing lesions in the reproductive structures and also by defoliating the plants ( Jesus et al., 2013Jesus FG, Sousa PV, Machado BR, Pereira AA, Alves GCS. [Development of Spodoptera eridania (Cramer) (Lepidoptera: Noctuidae) in different hosts]. Arq Inst Biol. 2013;80(4):430-5. Portuguese. Available from: https://doi.org/10.1590/S1808-16572013000400009
https://doi.org/10.1590/S1808-1657201300...
). Silva et al. (2017)Silva DM, Bueno AF, Stecca CS, Andrade K, Neves PMOJ, Oliveira MCN. Biology of Spodoptera eridania and Spodoptera cosmioides (Lepidoptera: Noctuidae) on different host plants. Flo Entomol. 2017;100(4):752-60. Available from: https://doi.org/10.1653/024.100.0423
https://doi.org/10.1653/024.100.0423...
demonstrated that soybean and cotton were more susceptible to the development and oviposition of S. eridania than wheat and corn. In addition, this insect species is able to develop on invasive weed plants, in which their presence during the off-season can act as “green bridge” as they provide food and shelter to the larvae.

Spodoptera eridania has been previously observed on invasive weed plants of the genus Amaranthus , family Amaranthaceae ( Montezano, 2014Montezano DG, Specht A, Sosa-Gomez DR, Roque-Specht VF, Barros NM. Immature stages of Spodoptera eridania (Lepidoptera: Noctuidae): developmental parameters and host plants. J Pest Sci. 2014;14(1):1-11. Available from: https://doi.10.1093/jisesa/ieu100
https://doi.10.1093/jisesa/ieu100...
). Larvae of S. eridania were collected from Amaranthus hybridus L. in Florida, along with emergences of the tachinid parasitoids, Winthemia rufopicta (Bigot), Eucelatori rubentis (Coquillett), and Lespensia sp. ( Tingle et al., 1978Tingle FC, Ashley TR, Mitchell ER. Parasites of Spodoptera exigua , S. eridania [Lep.: Noctuidae] and Herpetogramma bipunctalis [Lep.: Pyralidae] collected from Amaranthus hybridus in field corn. Entomophaga. 1978;23(4):343-7. Available from: http://doi.org/10.1007/BF02373051
http://doi.org/10.1007/BF02373051...
). Amaranthus viridis has been identified as a potential host for S. eridania because of its nutrient-rich composition ( Silva et al., 2017Silva DM, Bueno AF, Stecca CS, Andrade K, Neves PMOJ, Oliveira MCN. Biology of Spodoptera eridania and Spodoptera cosmioides (Lepidoptera: Noctuidae) on different host plants. Flo Entomol. 2017;100(4):752-60. Available from: https://doi.org/10.1653/024.100.0423
https://doi.org/10.1653/024.100.0423...
). Thereby, this condition can promote population growth and infestations of S. eridania in successive cultivated plants of economic importance, especially soybeans and cotton during the summer crop season ( Tingle et al., 1978Tingle FC, Ashley TR, Mitchell ER. Parasites of Spodoptera exigua , S. eridania [Lep.: Noctuidae] and Herpetogramma bipunctalis [Lep.: Pyralidae] collected from Amaranthus hybridus in field corn. Entomophaga. 1978;23(4):343-7. Available from: http://doi.org/10.1007/BF02373051
http://doi.org/10.1007/BF02373051...
; Santos et al., 2005Santos KB, Meneguim AM, Neves PMOJ. [Biology of Spodoptera eridania (Cramer) (Lepidoptera: Noctuidae) in different hosts]. Neotrop Entomol. 2005;34(6):903-10. Portuguese. Available from: https://doi.org/10.1590/S1519-566X2005000600005
https://doi.org/10.1590/S1519-566X200500...
). Considering the economic importance of S. eridania in agricultural systems, the present work records the first observation of this pest in A. hybridus in Brazil.

Larvae of S. eridania were observed feeding on A. hybridus plants in May 2021 inside the greenhouse, in the municipality of Piracicaba (22°42’30” S, 47°38’00” W, mean annual precipitation 190 mm, mean temperature 29 °C, 546 m altitude), state of São Paulo, Brazil. Images of the larvae while feeding on A. hybrids were obtained using an Olympus® E-410 digital camera. The pictures were then sent to the Laboratory of Ecotoxicology and IPM (LEMIP) of the Department of Entomology of Lavras Federal University (UFLA) for species identification.

Spodoptera eridania larvae of approximately 7 cm in length were naturally found infesting the upper part of A. hybridus plants at full bloom. The plants of A. hybrids were being cultivated in 540 pots filled commercial substrate in the greenhouse for other experimental purposes. Approximately 20 plants were attacked by on average three blackish-green larvae of S. eridania per plant ( Figure 1 ). Inside the greenhouse other family plants were cultivated side by side with A. hybridus , including soybean plants. After noticing the natural infestation, S. eridania larvae fed on inflorescences and leaves. Some of the A. hybridus plants were completely defoliated ( Figure 1 ) after 3 days of noticing the larvae infestation in the greenhouse.

Figure 1
(a,b,c) Spodoptera eridania larvae on Amaranthus hybridus plants, (d,e,f) larvae and symptoms of Spodoptera eridania attack on Amaranthus hybridu s plants

Spodoptera eridania has been mainly associated with soybean and cotton crops; however, its polyphagous behavior has contributed to its ability to quickly adapt to diverse agroecosystems as the larvae can feed on the leaves and reproductive structures of several plants species ( Silva et al., 2017Silva DM, Bueno AF, Stecca CS, Andrade K, Neves PMOJ, Oliveira MCN. Biology of Spodoptera eridania and Spodoptera cosmioides (Lepidoptera: Noctuidae) on different host plants. Flo Entomol. 2017;100(4):752-60. Available from: https://doi.org/10.1653/024.100.0423
https://doi.org/10.1653/024.100.0423...
). Its relatively short cycle allows this pest insect to produce many generations year round, and consequently have multiple and viable offspring. Larvae of S. eridania also present substantial movement between host plants ( Fanela et al., 2020Fanela TLM, Baldin ELL, Hunt TE, Faria RD. Baseline plant-to-plant larval movement of Spodoptera eridania in Bt and non-Bt soybean and its possible impacts on IRM. J Econ Entomo. 2020;113(4):1741-52. Available from: https://doi.org/10.1093/jee/toaa079
https://doi.org/10.1093/jee/toaa079...
), and their presence in agricultural production systems has been noted in the main soybean-producing regions in Brazil ( Souza et al., 2014Souza BHS, Costa EN, Silva AG, Boiça Júnior AL. [Bionomic aspects of Spodoptera eridania (Cramer): an expanding pest in soybean cultivation in the Brazilian Cerrado region]. EntomoBrasilis. 2014;7(2):75-80. Portuguese. Available from: https://doi.org/10.12741/ebrasilis.v7i2.381
https://doi.org/10.12741/ebrasilis.v7i2....
) due to the wide distribution of alternative food sources during the crop season as well as off-season ( Machado et al., 2020Machado EP, Rodrigues Junior GLS, Somavilla JC, Führ FM, Zago SL, Marques LH et al. Survival and development of Spodoptera eridania , Spodoptera cosmioides and Spodoptera albula (Lepidoptera: Noctuidae) on genetically-modified soybean expressing Cry1Ac and Cry1F proteins. Pest Manag Sci. 2020;76(12):4029-35. Available from: https://doi.10.1002/ps.5955
https://doi.10.1002/ps.5955...
).

The polyphagous habit of S. eridania benefits its growth and development, whereby under stress from food shortages, the larvae tend to attack other host plants, and may consume tender branches and inflorescences, perforate tissues, and even attack the roots of host plants ( Jesus et al., 2013Jesus FG, Sousa PV, Machado BR, Pereira AA, Alves GCS. [Development of Spodoptera eridania (Cramer) (Lepidoptera: Noctuidae) in different hosts]. Arq Inst Biol. 2013;80(4):430-5. Portuguese. Available from: https://doi.org/10.1590/S1808-16572013000400009
https://doi.org/10.1590/S1808-1657201300...
; Bragard et al., 2020Bragard C, Dehnen-Schmutz K, Di Serio F, Gonthier P, Jacques M, Jaques Miret JA et al. Pest categorisation of Spodoptera eridania . EFSA J. 2020;18(1):1-29. Available from: https://doi.org/10.2903/j.efsa.2020.5932
https://doi.org/10.2903/j.efsa.2020.5932...
). Among the plants most attacked by S. eridania larvae, those belonging to the families Amaranthaceae, Solanaceae, Fabaceae, and Poaceae predominate, not only because of the higher number of cultivated plants, but also for the large number of invasive species that can serve as primary food sources during the off-season when the main crop is not properly managed, before implementation or after harvest ( Bortoli et al., 2012Bortoli LC, Bertin A, Efrom CFS, Botton M. [Biology and fertility life table of Spodoptera eridania (Cramer) (Lepidoptera: Noctuidae) on strawberry and grapevine]. Rev Bras Frutic. 2012;34(4):1068-73. Portuguese. Available from: https://doi.org/10.1590/S0100-29452012000400013
https://doi.org/10.1590/S0100-2945201200...
; Montezano et al., 2014Montezano DG, Specht A, Sosa-Gomez DR, Roque-Specht VF, Barros NM. Immature stages of Spodoptera eridania (Lepidoptera: Noctuidae): developmental parameters and host plants. J Pest Sci. 2014;14(1):1-11. Available from: https://doi.10.1093/jisesa/ieu100
https://doi.10.1093/jisesa/ieu100...
).

Weeds of the genus Conyza are able to host S. eridania larvae and other lepidopteran pests in soybean crops in Brazil, and therefore should be properly managed to reduce the insect populations on the major crops ( Dalazen et al., 2016Dalazen G, Curioletti LE, Cagliari D, Stacke RF, Guedes JVC. Hairy fleabane as a source of major insect pests of soybean. Planta Daninha. 2016;34(3):403-9. Available from: https://doi.org/10.1590/S0100-83582016340300001
https://doi.org/10.1590/S0100-8358201634...
). When feeding during initial development, S. eridania larvae can assimilate nutrients from the host plants to meet their nutritional needs, allowing for normal development until adulthood ( Panizzi, Parra, 2009Panizzi AR, Parra JRP. [Bioecology and insect nutrition as a basis for integrated pest management]. In: Panizzi AR, Parra JRP, editors. [Insect bioecology and nutrition: basis for integrated pest management]. Londrina: Empresa Brasileira de Pesquisa Agropecuária; 2009. p. 1107-39. Portuguese. Available from: http://www.alice.cnptia.embrapa.br/alice/handle/doc/471523
http://www.alice.cnptia.embrapa.br/alice...
). Spodoptera eridania larvae showed shorter larval periods and higher pupal weights when fed on the invasive plant morning glory, Ipomoea grandifolia (Convolvulaceae), than soybean plants, therefore, this weed species can be considered as an alternative host plants for this pest ( Santos et al., 2005Santos KB, Meneguim AM, Neves PMOJ. [Biology of Spodoptera eridania (Cramer) (Lepidoptera: Noctuidae) in different hosts]. Neotrop Entomol. 2005;34(6):903-10. Portuguese. Available from: https://doi.org/10.1590/S1519-566X2005000600005
https://doi.org/10.1590/S1519-566X200500...
). These authors reported also the number of eggs per female laid on the leaves of soybean, cotton, and morning glory, which were high in all treatments, demonstrating that in addition to plants being an alternative food source, they are also suitable substrates for oviposition.

Clover, Trifolium repens (Fabaceae), is an invasive plant that presents suitable nutritional conditions for S. eridania larval growth and development. Female fertility was higher when S. eridania larvae were fed on leaves of clover compared to larvae that ingested plant tissues of peach and apple trees ( Silva et al., 2018Silva A, Baronio CA, Galzer ECW, Garcia MS, Botton M. Development and reprotuction of Spodoptera eridania on natural hosts and artificial diet. Braz J Biol. 2018;79(1):80-6. Available from: https://doi.org/10.1590/1519-6984.177219
https://doi.org/10.1590/1519-6984.177219...
). In another study, Jesus et al. (2013)Jesus FG, Sousa PV, Machado BR, Pereira AA, Alves GCS. [Development of Spodoptera eridania (Cramer) (Lepidoptera: Noctuidae) in different hosts]. Arq Inst Biol. 2013;80(4):430-5. Portuguese. Available from: https://doi.org/10.1590/S1808-16572013000400009
https://doi.org/10.1590/S1808-1657201300...
evaluated different host plants for the development of S. eridania and stated that Canavalia ensiformis was the most attractive to the larvae; however, plants of Raphanus sativus L. were the most consumed. Plants of R. sativus are weeds commonly found in soybean crops, which can host insect pests like S. eridania , in addition these plants can compete for light, nutrients, and space with the main crop, leading to lower yields ( Santos et al., 2005Santos KB, Meneguim AM, Neves PMOJ. [Biology of Spodoptera eridania (Cramer) (Lepidoptera: Noctuidae) in different hosts]. Neotrop Entomol. 2005;34(6):903-10. Portuguese. Available from: https://doi.org/10.1590/S1519-566X2005000600005
https://doi.org/10.1590/S1519-566X200500...
).

The genus Amaranthus has a great importance in agriculture as it includes a lot of species considered as weeds. It has been reported in recent studies difficulty in controlling A. hybridus due the resistance to glyphosate, the main herbicide used for its control ( García et al., 2020García MJ, Palma-Bautista C, Vazquez-Garcia JG, Rojano-Delgado AM, Osuna MD, Torra J et al. Multiple mutations in the EPSPS and ALS genes of Amaranthus hybridus underlie resistance to glyphosate and ALS inhibitors. Sci Rep. 2020;10(1):1-11. Available from: https://doi.org/10.1038/s41598-020-74430-0
https://doi.org/10.1038/s41598-020-74430...
; Resende et al., 2022Resende LS, Christoffoleti PJ, Netto AG, Presoto JC, Nicolai M, Maschietto EH et al. Glyphosate-resistant smooth-pigweed ( Amaranthus hybridus ) in Brazil. Adv Weed Sci. 2022;40(spe 2):1-6. Available from: https://doi.org/10.51694/AdvWeedSci/2022;40:Amaranthus005
https://doi.org/10.51694/AdvWeedSci/2022...
). Besides that, these plants can remain in crops becoming a green bridge for herbivorous insects that damage crops of interest reducing producer profit ( Moraes et al., 2020Moraes T, Silva AF, Leite NA, Karam D, Mendes SM. Survival and development of fall armyworm (Lepidoptera: Noctuidae) in weeds during the off-season. Florida Entomologist. 2020;103(2):288-92. Available from: https://doi.org/10.1653/024.103.0221
https://doi.org/10.1653/024.103.0221...
).

This study reports for the first time the natural occurrence of S. eridania larvae feeding on A. hybridus in the city of Piracicaba, SP, Brazil. This demonstrates that this invasive weed plant, which is difficult to eliminate in agricultural crops, can serve as “green bridge” to promote the growth and development of S. eridania . This can allow for the success of consecutive generations of the insect species and consequent attacks on major agricultural crop systems. Thus, preventive measures should be taken to control S. eridania by monitoring its population densities and investigating the existence of associated natural enemies. Furthermore, it is necessary to conduct studies under laboratory, greenhouse, and field conditions to evaluate the bioecological characteristics of S. eridania on A. hybridus plants to establish more effective management strategies for its control.

  • Funding
    This research was funded by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), grant number 142337/2020-0 and the article processing charge was funded by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

Acknowledgements

To Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for their support to this research.

References

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    » https://doi.org/10.1590/S0100-83582016340300001
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Edited by

Approved by:
Editor in Chief: Anderson Luis Nunes
Associate Editor: Silvia Fogliatto

Publication Dates

  • Publication in this collection
    01 July 2022
  • Date of issue
    2022

History

  • Received
    30 Mar 2022
  • Accepted
    23 May 2022
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