Incidence of Listronotus bonariensis (Coleoptera: Curculionidae) in ryegrass pastures from southern Chile. New background

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1 Journal of Soil Science and Plant Nutrition, 2017, 17 (1), SHORT COMMUNICATION Incidence of Listronotus bonariensis (Coleoptera: Curculionidae) in ryegrass pastures from southern Chile. New background Leonardo Parra 1, 2,3*, Manuel Chacón-Fuentes 2,3, Marcelo Lizama 2,3 and Andrés Quiroz 2,3 1 Scientific and Technological Bioresource Nucleus, BIOREN-UFRO, Universidad de La Frontera, Temuco, Chile. 2 Laboratorio de Química Ecológica, Departamento de Ciencias Químicas y Recursos Naturales, Universidad de La Frontera, Temuco, Chile. 3 Centro de Investigación Biotecnológica Aplicada al Medio Ambiente (CIBAMA), Universidad de La Frontera, Av. Francisco Salazar 01145, Temuco, Chile. *Correponding author: leonardo.parra@ufrontera.cl Abstract The Argentine stem weevil, Listronotus bonariensis, is an important pest in pastures, especially ryegrass (Lolium sp.), compromising grassland persistence and productivity. Both, adult and specially larvae cause severe damage, action that generate the death of the tiller and reducing forage production. Chemical control has limited effectiveness in adult s insect and negative effects on the environmental and toxicity to pollinators when applied close to the flowering period is observed. Therefore, the main currently strategy is based on the use of cultivars of Lolium endophyte fungus-infected with Neothypodium genus. However, over a decade that there are no reports on the presence of this weevil in southern Chile. Hence, the aim of this research was report the actual incidence of L. bonariensis in ryegrass pastures. The results of two years of prospecting showed that this weevil is currently causing damage to the ryegrass pastures indicating that the effectiveness of species infected with the fungus must be evaluated. Keywords: Damage, distribution, immature stage, endophyte, weevil 91

2 92 Parra et al. 1. Introduction The Argentine stem weevil Listronotus bonariensis (Coleoptera: Curculionidae), a native species of South America, is an important pest in pastures, especially ryegrass (Lolium sp.), wheat and barley, because their attack occurs in two stages of development. Weevil larvae bore the stem and crowns compromising pasture persistence and productivity, while the adult stage can reduce seedling establishment by defoliation and cutting of the stems (Baker and Addison 2006; Barrat et al., 2016). In New Zealand this insect causes yield losses in a range between 5 and 30% in L. perenne and economic losses that reach the U.S. $ 138 million/ year (Prestidge et al., 1991). In the same country, the densities of L. bonariensis reach between 130, ,000/ha (Barratt et al., 2007). In Chile, the first record on the incidence of L. bonariensis was reported by Norambuena and Gerding (1985) on wheat and barley in the south of the country, detecting 27.9% and 7.1% attacked axes, respectively. Subsequently, Cisternas (2001) indicated that in Osorno (Región de Los Lagos) were determined losses of 44.4% dry matter production in L. multiflorum (ryegrass biannual) due to larval attack. The latest research on the subject determined that densities above or equal to 125 adults/m 2 are critical to the establishment of pasture (Cisternas and Villagra, 2003). Chemical control has limited effectiveness on adult s insect, and it is ineffective against the larvae that populate the tillers. Furthermore, organophosphate insecticides present risks on the environmental such as residual effect, exclusion period and toxicity on pollinators when applied close to the flowering period (Urrutia, 2005), reason for which there is growing interest in the search for new control alternatives (Tampe et al., 2016). In this sense, the main strategy used to control this weevil is based on the use of cultivars of Lolium and fescue (Festuca arundinacea) endophyte-infected with Neothypodium genus and they are resistant to feeding larvae and adults of L. bonariensis (Spiering et al., 2005; Moore et al., 2015). In general, Neotyphodium endophytes have been used as an effective tool for controlling grassland pest due offer protection against porina larvae Wiseana cervinata (Lepidoptera: Hepialidae), African black beetle Heteronychus arator (Coleoptera: Scarabaeidae) and L. bonariensis (Jensen and Popay, 2004; Vidal and Jaber, 2015). This topic has been studied extensively in New Zealand during the last decade by Popay et al., (2003). In this regard, an updated study in laboratory and field conditions, conducted with larvae of Costelytra zealandica (Coleoptera: Scarabaeidae), one of the largest subterranean pests in pastures of New Zealand, determined a negative relationship between the content of lolines in roots of fescue and consumption and weight gain by larvae (Patchett et al., 2011). This effect would be detrimental to the insect, and it would be induced by the same larva, which feed on the root triggering a defensive process of the plant, which would transport the alkaloid from the crown to the root (Patchett et al., 2008). Bryant et al., (2010) reported that lolines released by the endophyte Neotyphodium uncinatum present in Festuca pratensis, were effective in controlling Adoryphorus coulonii larvae (Coleoptera: Scarabaeidae) under laboratory conditions. In another interesting work, Karpyn et al., (2017) compiled information on the detrimental effect of certain strains of ryegrass endophytes on the survival and oviposition of African black beetle. The use of endophytes of the genus Neotyphodium that accumulate lolines or another alkaloid in the roots of plants and to reduce the growth, development and survival of subterranean insects would be a potential method for pest control in grasslands, which would have some advantages such as, effectiveness, low cost and no impact toxic to Journal of Soil Science and Plant Nutrition, 2017, 17 (1), 91-98

3 Incidence of Listronotus bonariensis (Coleoptera: Curculionidae) in ryegrass pastures 93 livestock grazing. In Chile, the research on fungal endophytes began in the early 90s. Although, researchers at the Instituto de Investigaciones Agropecuarias (INIA) conducted several studies and obtaining valuable results on the controlling effect of endophyte on L. bonariensis, its current research is outdated. The latest report dates from 2003, and corresponds to the compilation of the information related to the effect of the interaction of the Argentine stem weevil and species of the genus Lolium in milk and meat bovine production in southern Chile (Lanuza et al., 2003). Therefore, the aims of this research were to report the actual incidence of L. bonariensis and presence of endophytes in ryegrass pastures of southern Chile. 2. Materials and Methods The study was carried out on 12 pastures located between the regions of Bío-Bío and Los Lagos during the period and (Table 1). The prospection method used for determining the incidence of L. bonariensis was a variation of the methodology proposed by Alzugaray et al., (2010). At each selected site, 10 squares (0.3 x 0.3 m) were selected randomly per sampling unit (n=10) with 3 replicates each. All plants (100 tillers) were cut at ground level with a scalpel and stored in plastic bags and taken to the Laboratorio de Química Ecológica (LQE) of the Universidad de La Frontera. Table 1. Ryegrass pastures located in different areas of southern Chile during seasons and The evaluated samples correspond to the average of the two seasons. The presence of L. bonariensis was determined as following: a) through immature stages (direct) and b) by identifying specific damage on the plant (indirect). The presence and confirmation of immature stage (eggs and larvae) of L. bonariensis was evaluated under a stereoscopic microscope following the entomological keys by Artigas (1994), while that the incidence of the curculionid on the plant was evaluated through identification of damage on stems and leaves following a modification of the methodology proposed by Alarcón et al., (2010). The verification of the presence of endophytic fungi in tissue was checked by the method adapted by Dombrowski et al., (2006). Briefly, 100 tillers obtained from different ryegrass pastures were cut and the inner epidermis of a leaf sheath was peeled off and placed on a glass slide. Two drops of rose Bengal stain were applied to each sample. After 60 s the Journal of Soil Science and Plant Nutrition, (1), 91-98

4 94 Parra et al. samples will be covered with a cover slip. Finally, the microscopic examination (40X) was performed, identifying as positive those samples presenting typical fungal mycelium. The percentage infection will be determinate from rate of samples with endophyte and the sampled examined. 3. Results and Discussion Figure 1 shows a geographical distribution of L. bonariensis in different ryegrass pastures of southern Chile Figure 1. Geographical distribution of damage produced by Listronotus bonariensis in different ryegrass pastures in southern Chile. Symbology described in the figure indicates different degrees of attack of L. bonariensis in each zone evaluated during seasons and The presence of the insect was detected by: a) damage caused to the level of tillers base by the action larvae, b) foliar consumption by adults, and c) presence of oviposited eggs into the tissue of the sheath. Although differences in the degree of insect attack and number of pastures sampled by region are observed, it shows that this weevil is present in the four southern regions of the country being regions of La Araucanía and Los Lagos which had a higher presence of the insect. The results for the Región del Bío-Bío showed an lower damage than other regions evaluated (Figure 2). Cato zone presented a low level of damage (6.3%) similar to the localities of Chillán and Los Ángeles where there was no presence of individuals or damage by L. bonariensis. The above is because in those zones there are great surfaces of other crops that are hosts of L. bonariensis such as wheat, barley, oats and maize, therefore its presence and incidence in ryegrass is lower than other areas evaluated (Norambuena and Gerding, 1985). The results of the incidence of this insect prospected in the other regions indicated that the most intense attacks by L. bonariensis were found in Region de Los Lagos and in a less extent in regions of La Araucanía and Los Ríos, which is consistent with the report of Cisternas and Villagra (2003). The zones of Región de Los Lagos, Remehue, Osorno and Purranque had a similar pasture damage product of action of the L. bonariensis (33, 29 and 30%) (Figure 2). In addition, the average number of immature stages (eggs + larvae) for this region was 268.5/m 2, value that exceeds the limits established by Prestidge et al., (1985) and Cisternas and Villagra (2003), who reported 180 and 125 individuals/m 2 respectively, being these values critical for the survival of a pasture. Similar to the results obtained in Región de Los Lagos, in the Región de La Araucanía an average of immature stages/ m 2 was obtained, which would affect ryegrass pastures production. These results do not agree with Journal of Soil Science and Plant Nutrition, 2017, 17 (1), 91-98

5 Incidence of Listronotus bonariensis (Coleoptera: Curculionidae) in ryegrass pastures 95 Barrat et al., (2016) who indicated that the average of L. bonariensis individuals varies between 13-40/m 2 in New Zealand pastures. These same authors suggest that climatic conditions and its phenology are the main factors that affected fitness and performance of L. bonariensis. On the contrary in zones of Vilcún (Región de La Araucanía) and Remehue (Región de Los Lagos) an opposite effect to the rest of the areas evaluated. In both areas, it was observed that the damage produced by L. bonariensis is less than the amount of collected insects. Possibly this effect is related to the presence of endophytes that act inhibiting the action of the weevil. However, this should be evaluated in a future study. Based on the results of two years of prospecting, it is estimated that in the zones of greatest insect attack (Región de La Araucanía to Los Lagos), an average of 29.2 individuals/ m 2 produce about 30% damage. Moreover, it is inferred that the potential for the production of forage could be negatively affected because L. bonariensis remains present and damaging the ryegrass pastures of southern Chile. The microscopic analysis of ryegrass indicated that the highest incidence of endophyte fungus was found in the Maquehue zone (41%, Table 2). In this same area, there is a high damage produced by L. bonariensis (Figure 2) which would indicate that the no protection of the endophyte fungus to the plant, possibly due to loss of viability of the fungus. The above would be explained because as the age of forage seed increases the endophyte fungus loses its viability which possibly occurring with the pastures of the Maquehue zone (Wheatley et al., 2007; Hill and Roach, 2009). The rest of the areas presented an infection of the endophyte less than 30% (Table 2). Figure 2. Average damage and number of immature stages (eggs + larvae) of Listronotus bonariensis in different ryegrass pastures in southern Chile. Zones evaluated during seasons and The zone of Angol (Región de La Araucanía) was only evaluated in the season Journal of Soil Science and Plant Nutrition, (1), 91-98

6 96 Parra et al. Table 2. Percentage (%) of infection of endophyte fungus in ryegrass pastures in different areas of southern Chile during seasons and Conclusions In conclusion, this survey has revealed that the Argentine stem weevil, L. bonariensis, still affecting the ryegrass pastures of southern Chile regions. Probably the cause of the damage increase by L. bonariensis (>30%) is due to a lack controlling effect of endophytes fungi, therefore, new control strategies must be performed. Future studies should addressed to (1) prospect the presence of endophytic fungi in the ryegrass pastures evaluated and (2) search for new strains of endophytic fungi that could be more effective in controlling L. bonariensis. References Alarcón, D., Ortega, F., Perich, F., Pardo, F., Parra, L., Quiroz, A Relationship between radical infestation of Hylastinus obscurus (Marsham) and the yield of cultivars and experimental lines of red clover (Trifolium pratense L.). Journal of Soil Science and Plant Nutrition. 10, n Alzugaray, R., Ribero, A., Silva, H., Stewart, S., Castiglioni, E., Bartaburu, S., Martínez, J.J Prospección de agentes de mortalidad natural de áfidos en leguminosas forrajeras en Uruguay. Agrociencia. 14, Acknowledgements Financial support for this research was supplied by FONDECYT (Project ). Supported (partially) by Dirección de Investigación, Universidad de La Frontera. Artigas, J Entomología Económica: insectos de interés agrícola, forestal, médico y veterinario (nativos, introducidos y susceptibles de ser introducidos). Eds. Universidad de Concepción, Concepción, Chile. Journal of Soil Science and Plant Nutrition, 2017, 17 (1), 91-98

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