First record of damage to Salix viminalis L. by Ostrinia furnacalis (Guenée) (Lepidoptera: Crambidae)

Abstract

The Asian corn borer, Ostrinia furnacalis (Guenée) (Lepidoptera: Crambidae), is one of the most harmful pests of many crops in Asia and Australia. This paper reports for the first time its occurrence and damage on basket willow (Salix viminalis L.). The finding allows us to alert farmers and institutions for further tracking its establishment and spread in monoculture and polyculture systems involving the basket willow in China and other countries.

Keywords:

• Salix viminalis
• Ostrinia furnacalis
• COI gene
• New host plant
• DNA barcoding

1. Introduction

The Asian corn borer, Ostrinia furnacalis (Guenée) (Lepidoptera: Crambidae), mostly known as a major pest of maize (Calcagno et al., 2017), is distributed throughout Asia and Australia (Yuan et al., 2013). The larvae feed on more than 70 other plant species (Table 1; Wang et al., 2018; Yuan et al., 2015), including some important food and non-food crops such as sorghum, millet, and cotton (Afidchao et al., 2009; 2013; Yuan et al., 2015). Colonization of O. furnacalis could also occur on woody plants, although only three species (i.e., Populus euramevicana; Malus pumila; Camellia sinensis; see, Table 1) have been recorded to date (Yuan et al., 2015).

Table 1. Host plant species of O. furnacalis (Yuan et al., 2015)

Family (Number)	Species
Herbaceous plants
Amaranthaceae (1)	Amaranthus viridis L.
Asteraceae (18)	Xanthium sibiricum Patrin ex Widder, Artemisia argyi Lévl. et Van., Artemisia selengensis Turcz. ex Bess., Artemisia scoparia Waldst. et Kit., Carduus nutans L., Artemisia integrifolia L., Cirsium arvense (L.) Scop., Sonchus brachyotus DC., Neopallasia pectinata (Pall.) Poljak., Dendranthema morifolium (Ramat.) Tzvel., Bidens biternata (Lour.) Merr. et Sherff., Helianthus annuus L., Bidens tripartite L., Tripolium vulgare Nees., Cirsium arvense var. integrifolium., Ambrosia trifida L., Artemisia annua L., Ambrosia artemisiifolia L.
Malvaceae (3)	Alcea rosea Linnaeus., Abutilon theophrasti Medicus, Gossypium herbaceum L.
Euphorbiaceae (1)	Ricinus communis L.
Leguminosae (7)	Pisum sativum L., Vignaangularis (Willd.) Ohwi et Ohashi., Vigna radiate (Linn.) Wilczek., Glycine max (L.) Merr., Vicia faba L., Phaseolus vulgaris L., Vigna unguiculata (Linn.) Walp.
Poaceae (13)	Triticum aestivum L., Echinochloa crusgalli (L.) Beauv., Setaria viridis (L.) Beauv., Imperata cylindrical (Linn.) Beauv., Coix lacroyma-jobi L., Avena sativa L., Zea mays L., Sorghum bicolor (L.) Moench, Setariaitalic L., Panicum miliaceum L., Oryza sativa L., Sorghumsudanense (Piper) Stapf., Saccharum L., Phragmites australis (Cav.) Trin. ex Steud.
Passifloraceae (1)	Passiflora coerulea L.
Polygonaceae (3)	Fagopyrum esculentum Moench., Rumex patientia L., Polygonum lapathifolium L.
Chenopodiaceae (1)	Chenopodium album L., Beta vulgaris L.
Ranunculaceae (1)	Paeonia lactiflora Pall.
Moraceae (3)	Humulus scandens (Lour.) Merr., Cannabis sativa L., Humulus lupulus L.
Zingiberaceae (1)	Zingiber officinale Roscoe.
Rutaceae (2)	Citrus maxima Merr., Citrus medica L.
Solanaceae (5)	Capsicum annuum L., Solanum melongena L., Lycopersicon esculentum Mill., Capsicum annuum L. var. grossum (Willd.) Sendtn., Solanum tuberosum L.
Cucurbitaceae (2)	Cucumis sativus L., Cucumis melo L.
Dioscoreaceae (1)	Dioscorea esculenta (Lour.) Burkill.
Labiatae (2)	Elsholtzia blanda Benth., Spinacia oleracea Nakai.
Brassicaceae (1)	Brassica oleracea L.
Woody plants
Rosaceae (1)	Malus pumila Mill.
Theaceae (1)	Camellia sinensis (L.) Kuntze.
Salicaceae (2)	Populus euramevicana cv. “I-214”., Salix viminalis L.

The basket willow (Salix viminalis L.), a vigorous and fast-growing shrub willow, is widely distributed in Europe and Asia. It has been used for phytoremediation in sites contaminated by heavy metals and cultured commercially for biofuel industry due to its rapid growth yielding high biomass (Mleczek et al., 2010). The leaves are also used in sericulture for raising larvae of Chinese oak silkworm (Antherea pernyi Guérin-Méneville). In October 2021, local farmers in Heilongjiang Province, China, observed a new lepidoptera species with the larvae severely damaging S. viminalis. In this study, by DNA-barcoding and phylogenetic analysis, the pest was identified as O. furnacalis. To the best of our knowledge, this is the first report on the likelihood of O. furnacalis being a pest on S. viminalis, thus highlighting the necessity to establish monitoring and management plans in S. viminalis-growing regions prior to economic loss.

2. Material and methods

2.1. Sample collection

The larvae observed to affect S. viminalis were collected by hand from Nongjiang farm, Heilongjiang Province (47° 68′ 02.08″ N, 133° 13′ 57.00″ E; Sampling date: 21 October 2021). These insect samples were sent to Shenyang Agricultural University for species identification. At the collection site, rice has long been planted since 1988. To raise Chinese oak silkworm, the farmer planted the cutting of S. viminalis in Spring, 2021.

2.2. Molecular species identification

Four larvae as biological replicates were used for DNA extraction, PCR amplification and sequencing. Total DNA was extracted from each sample replicate with traditional phenol/chloroform method. The primers C1-J1483 (5-’GGTCAACAAATCATAAAGATATTGG-3’) and C1-N2194 (5’-TAAACTTCAGGGTGACCAAAAAATCA-3’; Simon et al., 2006) were used for PCR amplification for the target mitochondrial COI gene fragment as the DNA barcode. The PCR product was detected by 1% agarose gel electrophoresis, purified and directly sequenced based on Sanger sequencing method with the PCR primers. A BLAST search was conducted in GenBank to determine the closest sequence match. Sequence data were aligned using MAFFT (https://mafft.cbrc.jp/alignment; Katoh et al., 2019). A phylogenetic tree, where the sequences were selected from different genus of Crambidae family in NCBI, was constructed by using the neighbor-joining method with MEGA X software (Kumar et al., 2018). The inferred phylogeny was tested by a bootstrap analysis with 1000 replicates.

3. Results

The insect pest severely damaged S. viminalis with up to 40% damage ratio as estimated by the local farmers. When sampling in the field we observed that the larvae infest the plant species as a stem borer. Early instar of the larvae tunneled into the stems and the resulting hollow stem are prone to break. As shown in Figure 1, the early-instar larva (about 13–14 mm long) has two pairs of ventral feet and crawls like an inchworm. It also has a reddish-brown head, a brown body and a small number of bristles.

Figure 1. The damage of O. furnacalis to S. viminalis described in this study. (a) Damaged one year old stem of S. viminalis. (b) Tunneling holes by O. furnacalis. (c) Larva of O. furnacalis.

The 658 bp sequence from the COI-barcoding has been deposited in GenBank with accession no. MZ883095. By BLASTN search against the database of GenBank, the COI gene sequences from four specimens all identified a 100% identity to that of O. furnacalis voucher II-8 (accession no. MN720679), but a 98.2% identity to that of European corn borer Ostrinia nubilalis Hübner voucher ECFR01 (accession no. EU128660; Figure 2). The phylogenetic analysis indicated that the sequences from the specimen and O. furnacalis Voucher II-8 were grouped into a single clade, and they were separated from all other species of Crambidae insects (Figure 3).

Figure 2. Alignment of COI sequences of four specimens with O. furnacalis voucher II-8 (accession no. MN720679) and O. nubilalis voucher ECFR01 (accession no. EU128660). Numbers at the right indicate nucleotide positions. Identical nucleotides are represented by a dot.

Figure 3. Phylogenetic tree based on COI sequences. The COI sequences of selected species was analyzed using a neighbor-joining method implemented in MEGA X. The selected species and GenBank accession numbers of their COI gene sequences: Cnaphalocrocis patnalis (MK566597); Achyra nudalis (HQ991414); Torulisquama obliquilinealis (MF053615); Hahncappsia cochissensis (HQ977670); Anania perlucidalis (KX044481); Ostrinia furnacalis voucher II-8 (MN720679); Ostrinia nubilalis voucher ECFR01 (EU128660). The sequence obtained in this study is circled.

4. Discussion

The Asian corn borer (O. furnacalis), first described in 1854, has had an expanding distribution range since the end of last century, and is now widely endemic to Asia Pacific regions such as China, Japan, and Australia (Yuan et al., 2013, 2015). The occurrence, biology, and behavior of the species has been studied in China since 1977 (Yuan et al., 2015; Zhou et al., 1995).

Nowadays, the distribution of this pest in China ranges from Northern to Southern regions, with infestation on many economically important crops including Zea mays, Oryza sativa, Sorghum bicolor, Glycine max (Wei & Chen, 2020), and have many researches on how to prevent and control this pest, such as ginsenosides (Liu et al., 2019), Trichogramma (Wang et al., 2022) and Bacillus thuringiensis (Liu et al., 2016). The pest exhibited a strong freeze tolerance in cold regions that supports its devastating performance in maize that is grown in Heilongjiang, the northernmost province of China (He et al., 2005). Other than maize, O. furnacalis is also a concern in the production of Sorghum bicolor, Setaria italica, and Saccharum offinarum in the Heilongjiang Province.

The willows (genus Salix) are comprised of hundreds of species, distributed throughout the world, but mostly in the northern hemisphere (Argus, 1986). They are suitable for use in prevention of leaching of hazardous wastes in evapotranspirative plantations, phytoremediation of contaminated soils, treatment wetlands and urban and agricultural catchment runoff systems or even to prevent erosion (Frédette et al., 2019). The moth Earias clorana L. has previously been considered to be monophagous, ingesting only plants in the genus Salix (Wiatrowska et al., 2018) and the Phratora vulgatissima females adult preferred S. viminalis for feeding and oviposition (Austel et al., 2014). However, no information is reported about O. furnacalis host in the S. viminalis. O. furnacalis, which was identified based on the COI sequence, damaging S. viminalis was reported for the first time. The larva was first found in Heilongjiang Province in 2021. We should be alert to the spread and destruction of this insect and urge entomologists to be aware of this new potential threat.

Here, using a collection of behavioral, morphological, and molecular identification, we confirmed the colonization of O. furnacalis on the basket willow S. viminalis, potentially woody plant being the host of the pest. Because rice is also a host plant of O. furnacalis, we conjectured that the larvae of O. furnacalis found in S. viminalis originated from the pest population on rice that were grown before the planting of S. viminals into the polycultural system. The host preference, population dynamics, and resulting damaging levels need to be assessed in the future. We hope that entomologists are aware of this new potential threat and monitor the occurrence in S. viminalis-growing regions using various approaches (Deng et al., 2022; Park et al., 2017).

Acknowledgements

We thank Prof. Li Qin of Shenyang Agricultural University for their helpful advice.

Disclosure statement

No potential conflict of interest was reported by the authors.

Additional information

Funding

This work was supported by grants from the National Natural Science Foundation of China grant 31972617 to (Y.Q. L.) and the China Agriculture Research System of MOF and MARA grant CARS-18 (to Y.Q. L.), and Natural Science Foundation of Liaoning Province grant 2022-MS-259 (to H.W.).