Preferred name: Listronotus bonariensis
Authority: (Kuschel)
Taxonomic position: Animalia: Arthropoda: Hexapoda: Insecta: Coleoptera: Curculionidae: Cyclominae
Other scientific names: Hyperodes bonariensis (Kuschel), Hyperodes griseus (Hustache), Neobagous setosus (Hustache)
Common names in English: Argentine stem weevil, wheat stem weevil
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EPPO Categorization: A1 list
EU Categorization: A1 Quarantine pest (Annex II A)
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EPPO Code: HYROBO

Listronotus bonariensis mainly attacks Lolium spp., but also many other pasture grasses. Maize is a significant host, and L. bonariensis has been recorded infesting important cereal crops (barley, oats, wheat). Adult damage and even larval feeding have been recorded incidentally in brassica crops established immediately after pastures, with significant loss of seedlings due to adult feeding. However, there is no evidence L. bonariensis can complete development in plant species other than grasses (Poaceae).

Laboratory assays have shown L. bonariensis adults feed and readily oviposit on the C4 grasses, Andropogon gerardii, Digitaria sanguinalis, Panicum coloratum, Panicum virgatum and Pennisetum clandestinum. 

Host list: Agrostis capillaris, Anthoxanthum aristatum, Avena sativa, Brassica napus, Brassica rapa, Bromus, Dactylis glomerata, Digitaria sanguinalis, Festuca rubra, Holcus lanatus, Hordeum vulgare, Lolium arundinaceum, Lolium multiflorum, Lolium perenne, Medicago sativa, Paspalum dilatatum, Phalaris aquatica, Phleum pratense, Pisum sativum, Poa annua, Poa pratensis, Poa trivialis, Secale cereale, Trifolium repens, Triticum aestivum, Zea mays

L. bonariensis originates in South America and has spread across the Pacific to Oceania.

South America: Argentina, Bolivia, Brazil (Rio Grande do Sul), Chile, Uruguay
Oceania: Australia (New South Wales, South Australia, Tasmania, Victoria, Western Australia), New Zealand

The biology of L. bonariensis has been extensively studied in New Zealand (Barker et al., 1988, Barker, 2013, Goldson, 1981, Goldson & Emberson, 1981, Goldson et al., 2001, Goldson et al., 1998, Goldson et al., 1999, Barker, 1988, Barker, 1989, May, 1961, Barker & Pottinger, 1986, Kalvelage, 1999). 

In New Zealand L. bonariensis has two main generations a year, and often a partial third generation in warmer localities/seasons. L. bonariensis adults overwinter in the grass sward and enter oligopause at the autumnal equinox. They gradually become reproductive over winter, leading to an oviposition period in late winter and early spring. Larval development in spring lasts 50-66 days and summer adults emerge 7-15 days after pupation. This adult generation peaks in early summer and is reproductively active over summer. Some of their progeny can mature and oviposit prior to atrophy of reproductive organs and overwintering, giving rise to a third generation. Later emerging adults do not become reproductive before overwintering. The generations can overlap as the adults may live for many months. 

During summer, adult activity is mainly nocturnal, peaking at dusk, whereas in winter activity is predominantly during the day. Adult feeding intensity increases linearly with temperature, between approximate lower and upper thresholds of 5°C and 42°C. Adults prefer to feed on leaf tissue between veins on the upper surface with the lower leaf cuticle often left intact. 

The sex ratio is 1:1 in laboratory-reared populations. Laboratory studies have shown that fecundity ranges from around 25 to over 380 eggs per female. Grasses are the preferred oviposition host and eggs are usually inserted in the pseudostem under the top layer of the leaf sheaths. Normally one to three but occasionally up to six eggs are laid at each oviposition event. The duration of egg development varies from 10 to 20 days in full summer to over 30 days in spring. 

When the plants are in vegetative growth, the neonate larvae tunnel into the tillers and feed downwards into the crown, with only one surviving in each tiller. If a larva kills a tiller before it is ready to pupate, it transfers to an adjacent one. In addition, around 30% of larvae, particularly later instars, may be found in pasture thatch, and under irrigation the proportion living outside host plants may be significantly higher. During and after flowering, or in stolonating grasses, neonate larvae may enter the stems near nodes. There are four larval instars. Immediately prior to pupation the larvae chew exit holes in the tillers, drop to the ground and form smooth-walled spherical cells 5-6 mm below the soil surface in which pupation occurs. 

The estimated degree-day (DD) requirements and threshold temperatures to complete development of the egg, larval, prepupal, pupal, and egg to adult stages are 83, 189, 40, 172, and 454 degree days heat accumulation, above threshold temperatures of 9.9, 9.2, 13.0, 11.0, and 10.7°C, respectively.

Adult dispersal by flight is highly variable both within and between seasons and with locality. Predisposing conditions for flight have been found to be temperatures are >19°C, relative humidity <81% and windspeed <10.8 km/h. In New Zealand, flight does not occur in the colder winter months and is more common on the drier lowland eastern regions than higher altitude or more humid regions.

Natural enemies

In South America, L. bonariensis is parasitized by: Patasson atomarius (Hymenoptera: Mymaridae), egg parasitoid; Heterospilus spp. (Hymenoptera: Braconidae), larval parasitoid; and Microctonus hyperodae (Hymenoptera: Braconidae), an adult parasitoid (Lloyd, 1966). The latter was successfully introduced into New Zealand in the 1990s (Goldson et al., 1998, Barker & Addison, 2006). The most prevalent pathogens in New Zealand L. bonariensis adult populations are Microsporidium itiiti Malone (Microsporida) and Beauveria bassiana (Balsamo) Vuillemin (Clavicipitaceae)(Barker et al., 1989). Linyphiid spiders are considered likely to be significant predators (Vink & Kean, 2013) in New-Zealand and elsewhere.

Symptoms

Adult feeding on leaves produces narrow rectangular holes in the leaf blades, giving a windowed appearance. Adults produce fibrous frass deposits on the leaves. 

Larval feeding in vegetative and flowering tillers may result in external brown discoloration adjacent to where larvae have fed. Damaged tillers always contain a burrow which contains fine granular frass and often the larva. Vegetative tillers die slowly outward from the innermost rolled leaf; the leaves withering, yellowing, then turning brown. On flowering stems, the tunneling near the nodes can result in premature ripening, reduced seed formation and stem breakage. Larvae always leave a round exit hole (1-1.5 mm diameter) at the base of the tiller when they move to pupate in the soil. Larval damage in pastures is most noticeable in dry summers when tiller replacement is inhibited. Whole plants may die.

Morphology

Eggs

Elongate, rounded at the ends and oval or round in cross-section. Length varies from 0.75-1 mm and width from 0.2-0.3 mm. When laid, eggs are yellowish-white but become dark olive green over 1-2 days.

Larva

Legless, cream to creamy-white with light to dark-brown head capsule and whitish-yellow elongated body tapering slightly to the posterior. The latter is sparsely covered with hairs. When fully grown, larvae are 5-6 mm long.

Pupa

Cream to light-brown or lemon coloured.

Adult

Colour variable from light grey-brown to dark-brown or black. Elongate (3 mm long), compact and hard bodied. Pronounced snout and three white stripes on the thorax. The body is covered with brown and white scales and numerous hairs which tend to hold dust (Ferro, 1976). They feign death when disturbed.

Detection and inspection methods

In pasture and grasslands, the simplest method of detecting L. bonariensis is vacuum sampling for adults with a modified blower-vac (McNeill & van Koten, 2020). If samples suspected to harbor adults (e.g. suction or seed) are placed in closed containers at ambient temperatures, adults will collect around the lid and on damp paper towels placed on the surface on the container contents. Sticky traps can be used to trap adults but only a proportion of each generation develops flight muscles and the predisposing conditions for flight may be limited (Goldson et al., 1999). 

EPPO Standard PM 3/78 recommends inspecting consignment of seed and grain of cereals and verifying the absence of adults.

The pest can disperse itself locally by flight. International movement would most probably be as contaminant of seeds of pasture grasses (L. bonariensis was introduced into Australia as adults with ryegrass seed (Chadwick 1963)), and possibly with other host seeds (cereals, horticultural plants) and grain. Bedding and fodder for live animal exports, especially those transported by air, may also pose a risk if the plant material is disposed of near an area with host plants. Larvae and pupae could also be dispersed with rooted plants of host species, but most recorded host species are not traded as rooted plants. EFSA (2018) reports 4 interceptions in the EU on seed and 1 on plants of Cortaderia sp. (pampa grass). Pupae could be introduced in soil.

Economic impact

The economic impact of L. bonariensis to New Zealand’s pastoral industry, and the research on which the analysis was based, is summarized by Ferguson et al. (2019). The high migratory potential of the adults means that pastures of any age can harbour large infestations. Adults and larvae are oligophagous, feeding on most gramineous plants. They can severely damage pastures, particularly ryegrasses (Lolium spp.). Generally, the generation emerging in summer is most damaging. In the early 1980s, Epichloë fungal endophyte infection, while causing ryegrass staggers in livestock, was found to protect its perennial ryegrass host from L. bonariensis damage (Prestidge et al., 1982, di Menna et al., 2012). This discovery led to the introduction of new, less harmful strains of the fungus, several of which have been commercialized for ryegrasses, tall fescue (Schedonorus phoenix), meadow fescue (Festuca pratensis) and Festulolium (meadow fescue x ryegrass). The endophytes may provide protection against other pasture pests and efficacy against the various pest species varies with endophyte strain, grass species and cultivar. The new endophyte strains are now used by most New Zealand farmers (Johnson et al., 2013).

Comparisons between endophyte-free and ryegrass infected with endophytes provide a useful measure of the impact of L. bonariensis. There is good correlation between percentage of tillers damaged by larvae and ryegrass yield: for example, at a trial site 60% tiller damage in endophyte-free ryegrass was associated with a yield close to 60% of the yield endophyte-protected ryegrass (Popay et al., 1999). In dry summers, vulnerable grasses may die allowing ingress of weeds. 

Newly sown pastures and gramineous crops are particularly vulnerable to L. bonariensis when established by direct drilling and minimal cultivation techniques from infested pasture. The residual adult and larval populations can survive in the turf after herbicide application and migrate onto the new seedlings as they emerge. Grasses are not fully protected by the endophyte for the first 4–6 weeks after germination (Ferguson et al., 2019). Severe damage has been reported to establishing maize (Hughes & Gaynor, 1984) and wheat, barley and oats crops (Cromey et al., 1980). Establishing forage brassica (Upritchard & Park, 1976, Kelsey, 1958) and pea (McNeill et al., 2020) crops are also vulnerable. 

L. bonariensis has been shown to be a significant pest of ryegrass in South America (Parra et al., 2017), as well as cereals and maize in Argentina, especially when following ryegrass pasture (Simón & Golik, 2018).

Control

Insecticide-treated seed is the most effective way to protect seedlings when establishing crops or pasture. Once established, L. bonariensis is difficult to control with insecticides as adults can rapidly re-infest from nearby and the larvae live within the plant. 

Some pasture grass species can be protected with Epichloë fungal endophyte infection and a range of commercial cultivars are now available with a choice of endophyte. Epichloë–infected seed is commercially sold in Europe (Krauss et al., 2020).

A small parasitic wasp, Microctonus hyperodae, was introduced to New Zealand from South America in 1990 as a biological control agent and rapidly established throughout the country. It attacks the adult weevil, rendering it sterile immediately and killing it when the parasitoid larvae emerges to pupate.

Phytosanitary risk

Pasture grasses such as L. perenne and L. multiflorum, as well as other hosts such as wheat and maize, are widely grown across the EPPO region. As L. bonariensis occurs in areas with similar climate to part of the EPPO region and host plants are present, it is likely to establish in the region if it was introduced. In the EPPO region, L. bonariensis has considerable potential to cause damage to pasture grasses and could possibly also affect cereals.

Seeds and grains of relevant host plants should come from pest-free areas. Seed and grain lots can also be sampled prior to export to guarantee pest freedom. Adult L. bonariensis are susceptible to fumigants typically used to disinfect shipping containers containing pest-infested seeds and grains.

Barker GM & Addison PJ (2006) Early impact of endoparasitoid Microctonus hyperodae (Hymenoptera: Braconidae) after its establishment in Listronotus bonariensis (Coleoptera: Curculionidae) populations of northern New Zealand pastures. Journal of Economic Entomology 99, 273-287.

Barker GM & Pottinger RP (1986) Diel activity of the adult Argentine stem weevil. New Zealand Journal of Zoology 13, 199-202.

Barker GM (1988) Effect of temperature on development and survival of Argentine stem weevil (Listronotus bonariensis) immature stages. New Zealand Journal of Zoology 15, 387-390.

Barker GM (1989) Functional anatomy of the reproductive system of Listronotus bonariensis (Kuschel). New Zealand Entomologist 12, 34-42.

Barker GM (2013) Biology of the introduced biocontrol agent Microctonus hyperodae (Hymenoptera: Braconidae) and its host Listronotus bonariensis (Coleoptera: Curculionidae) in Northern New Zealand. Environmental Entomology 42, 902-914.

Barker GM , Pottinger RP & Addison PJ (1989) Population dynamics of the Argentine stem weevil (Listronotus bonariensis) in pastures of Waikato, New Zealand. Agriculture, Ecosystems and Environment 26, 79-115.

Barker GM, Prestidge RA & Pottinger RP (1988) Reproductive phenology of Listronotus bonariensis (Kuschel) (Coleoptera:Curculionidae) in northern New Zealand pastures. Bulletin of Entomological Research 78, 659-668.

Chadwick CE (1963) Occurrence of the Argentine stem weevil in New South Wales. Australian Journal of Science 26, 91-92.

Cromey MG, Grbavac N & Sheridan JE (1980) Diseases and pests of cereals in the Wairarapa - a six year study. Proceedings of the thirty-third New Zealand Weed and Pest Control Conference 33, 254-257.

di Menna ME, Finch SC, Popay AJ & Smith BL (2012) A review of the Neotyphodium lolii/Lolium perenne symbiosis and its associated effects on animal and plant health, with particular emphasis on ryegrass staggers. New Zealand Veterinary Journal 60, 315-328.

EFSA (2018) Panel on Plant Health (PLH), Jeger M, Bragard C, Caffier D, Candresse T, Chatzivassiliou E, Dehnen-Schmutz K, Gilioli G, Gregoire J-C, Jaques Miret JA, Navarro MN, Niere B, Parnell S, Potting R, Rafoss T, Rossi V, Urek G, Van Bruggen A, Van der Werf W, West J, Winter S, Gardi C, Bergeretti F and MacLeod A, 2018. Scientific Opinion on the pest categorisation of Listronotus bonariensis. EFSA Journal 16(1), 5101, 23 pp. https://doi.org/10.2903/j.efsa.2018.5101

EPPO (2016) Standard PM 3/78 (1) Consignment inspection of seed and grain of cereals. EPPO Bulletin 46(1), 49–57. Also available from https://gd.eppo.int/standards/PM3/

Ferguson CM, Barratt BIP, Bell N, Goldson SL, S. Hardwick, Jackson M, Jackson TB, Phillips CB, Popay AJ, Rennie G, Sinclair S, Townsend R & Wilson M (2019) Quantifying the economic cost of invertebrate pests to New Zealand’s pastoral industry. New Zealand Journal of Agricultural Research 62, 255-315.

Goldson SL & Emberson RM (1981) Reproductive morphology of the Argentine stem weevil, Hyperodes bonariensis (Coleoptera: Curculionidae). New Zealand Journal of Zoology 8, 67-77.

Goldson SL (1981) Reproductive diapause in the Argentine stem weevil, Listronotus bonariensis, (Kuschel) (Coleoptera: Curculionidae), in New Zealand. Bulletin of Entomological Research 71, 275-287.

Goldson SL, McNeill MR, Proffitt JR & Baird DB (2001) Seasonal variation in larval-instar head-capsule sizes of Argentine stem weevil, Listronotus bonariensis (Kuschel) (Coleoptera: Curculionidae). Australian Journal of Entomology 40, 371-375.

Goldson SL, Proffitt JR & Baird DB (1998) The bionomics of Listronotus bonariensis (Coleoptera: Curculionidae) in Canterbury, New Zealand. Bulletin of Entomological Research 88, 415-423.

Goldson SL, Proffitt JR & Baird DB (1999) Listronotus bonariensis (Coleoptera: Curculionidae) flight in Canterbury, New Zealand. Bulletin of Entomological Research 89, 423-431.

Goldson SL,Proffitt JR & Baird DB (1998) Establishment and phenology of the parasitoid Microctonus hyperodae (Hymenoptera: Braconidae) in New Zealand. Environmental Entomology 27, 1386-1392.

Hughes KA & Gaynor DL (1984) Comparison of Argentine stem weevil and slug damage in maize direct-drilled into pasture or following winter oats. New Zealand Journal of Experimental Agriculture 12, 47-53.

Johnson LJ, De Bonth ACM, Briggs LR, Caradus JR, Finch SC, Fleetwood DJ, Fletcher LR, Hume DE, Johnson RD, Popay AJ, Tapper BA, Simpson WR, Voisey CR & Card SD (2013) The exploitation of epichloae endophytes for agricultural benefit. Fungal Diversity 60, 171–188.

Kalvelage H (1999) Effect of temperature on development of Listronotus bonariensis (Kuschel) (Coleoptera: Curculionidae) on Lolium perenne (L.) (Gramineae: Festucoidae). In Department of Ecology. Lincoln University.

Kelsey JM (1958) Damage in ryegrasses by Hyperodes griseus Hust. New Zealand Journal of Agricultural Research 1, 790-795.

Lloyd DC (1966) Surveys for Natural Enemies of Hyperodes bonariensis Kuschel in South America. Commonwealth Institute of Biological Control, South American Station.

May BM (1961) The Argentine stem weevil Hyperodes bonariensis Kuschel on pasture in Auckland. New Zealand Journal of Agricultural Research 4, 289-297.

McNeill MR & van Koten C (2020) Sampling to determine density of arthropods in intensively grazed grasslands. Journal of Applied Entomology 144, 519-533.

McNeill MR, Scott RE & Richards NK (2020) A novel association between the grass pest Argentine stem weevil (Coleoptera: Curculionidae) and peas. New Zealand Journal of Crop and Horticultural Science 48, 183-189.

Parra L, Chacón-Fuentes M, Lizama M & Quiroz A ( (2017) Incidence of Listronotus bonariensis (Coleoptera: Curculionidae) in ryegrass pastures from southern Chile. Journal of Soil Science and Plant Nutrition 17, 91-98.

Popay AJ, Hume DE, Baltus JG, Latch GCM, Tapper BA, Lyons TB, Cooper BM, Pennell CG, Eerens JPJ & Marshall SL (1999) Field performance of perennial ryegrass (Lolium perenne) infected with toxin free fungal endophytes (Neotyphodium spp.). In Proceedings Ryegrass Endophyte: An Essential New Zealand Symbiosis Symposium’. Grassland Research and Practice Series No. 7., pp. 113–122. New Zealand Grassland Association: Palmerston North, New Zealand, Napier, New Zealand.

Prestidge RA, Pottinger RP & Barker GM (1982) An association of Lolium endophyte with ryegrass resistance to Argentine stem weevil. Proceedings of the New Zealand Weed and Pest Control Conference 35, 119-122.

Simón MR & Golik SI (2018) Cereales de verano. Editorial de la Universidad Nacional de La Plata, La Plata. https://doi.org/10.35537/10915/68613 [accessed on 18 November 2020]

Upritchard EA & Park OL (1976) Control of insects in seedling field brassicas with phorate granules. In Proceedings of the Twenty Ninth New Zealand Weed and Pest Control Conference, pp. 193-196. Times Commercial Printers, Christchurch, New Zealand.

Vink CJ & Kean JM (2013) PCR gut analysis reveals that Tenuiphantes tenuis (Araneae: Linyphiidae) is a potentially significant predator of Argentine stem weevil, Listronotus bonariensis (Coleoptera: Curculionidae), in New Zealand pastures. New Zealand Journal of Zoology 40, 304-313.

This datasheet was extensively revised in 2021 by Pip Gerard (AgResearch, New Zealand). Her valuable contribution is gratefully acknowledged.

EPPO (2024) Listronotus bonariensis. EPPO datasheets on pests recommended for regulation. https://gd.eppo.int (accessed 2024-11-19)

This datasheet was first published in the EPPO Bulletin in 1989 and revised in the two editions of 'Quarantine Pests for Europe' in 1992 and 1997, as well as in 2021. It is now maintained in an electronic format in the EPPO Global Database. The sections on 'Identity', ‘Hosts’, and 'Geographical distribution' are automatically updated from the database. For other sections, the date of last revision is indicated on the right.

CABI/EPPO (1992/1997) Quarantine Pests for Europe (1^st and 2^nd edition). CABI, Wallingford (GB).

EPPO (1989) EPPO data sheet on quarantine organisms no 168: Listronotus bonariensis. EPPO Bulletin 19(4), 689-694. https://doi.org/10.1111/j.1365-2338.1989.tb01161.x