Differential performance and behavior of the corn leaf aphid, Rhopalosiphum maidis, on three species of the biomass crop miscanthus
Introduction
The need to substitute fossil fuels to reduce CO2 emissions and to ensure energy security has led to an increasing interest for perennial grasses as alternative sources of energy. Owing to its high yield potential and its good efficiency in carbon fixation and sequestration, the perennial rhizomatous C4-grass miscanthus has attracted much attention in Europe, the USA, and Japan (Lewandowski et al., 2003, Clifton-Brown et al., 2004, Stewart et al., 2009). The Miscanthus genus (Poaceae) comprises approximately 20 species originating from tropical to temperate areas of East-Asia (Numata, 1974, Clayton and Renvoize, 1986) and Africa (Hodkinson et al., 2002). The most interesting species for biomass production purposes is Miscanthus × giganteus, a vigorous sterile hybrid between M. sinensis and M. sacchariflorus (Zub and Brancourt-Hulmel, 2010). Miscanthus can be harvested annually from late autumn to early spring for 20–25 years (Lewandowski et al., 2003). Mean biomass yields range from 10 to 40 t ha−1 throughout Europe (Lewandowski et al., 2000) and field trials in the US showed that mean harvestable dry matter could range from 30 to 61 t ha−1 (Heaton et al., 2008). Nevertheless, the yield potential of M. × giganteus is limited in some climatic regions because of its poor frost tolerance and adaptation to water stress. Improvement programs of miscanthus are thus currently developed to identify key traits not only for biomass production but also for adaptation to a broad range of climate conditions. They mainly concern the species M. × giganteus, M. sinensis and M. sacchariflorus (e.g., Zub et al., 2011, Zub et al., 2012a).
The annual pesticide costs associated to the cultivation of M. × giganteus are predicted to be relatively modest due to its low susceptibility to diseases and pests (Lewandowski et al., 2003). However, several laboratory and field studies indicate that M × giganteus is a suitable host plant for some important pests of conventional cereal grain crops. Notably, two main insect pests of maize, the western corn rootworm, Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae), and the fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae), successfully develop on M. × giganteus (Prasifka et al., 2009, Spencer and Raghu, 2009, Gloyna et al., 2011). During an extensive field survey realized in the USA, large populations of the yellow sugarcane aphid, Sipha flava (Hemiptera: Aphididae), and the corn leaf aphid, Rhopalosiphum maidis (Hemiptera: Aphididae), were reported on M. × giganteus with apparent damage at least in youngest stands (Bradshaw et al., 2010). These studies suggest that insect pest flows are likely to occur between M. × giganteus crops and conventional cereal crops such as maize. Moreover, Jørgensen (2011) points out that another miscanthus species (i.e., M. sinensis) is not only grown for biomass but also for ornamental purposes. Due to its invasive characteristics, this miscanthus species has sometimes spread out of its growing areas. The main risks are therefore that these various miscanthus species could act as a refuge and/or reservoir for a number of insect pests possibly leading to increased damage in conventional crops (Jørgensen, 2011). According to Gloyna et al. (2011), the main strategies to control these potential pest problems would be the use of agrochemicals and breeding for improved resistance of miscanthus toward insect pests. The latter should receive a higher interest insofar as it fits into a context of sustainable agriculture. For instance, M. sacchariflorus, which is admittedly less productive in terms of biomass, provides a high resistance level against several major aphid pest species of common crops in Europe (Coulette et al., 2013) that could be used in such breeding programs.
This study aimed at investigating, through laboratory experiments, the colonization of three main miscanthus species (M. sinensis, M. sacchariflorus and the sterile hybrid M. × giganteus) by the corn leaf aphid, R. maidis. Our main objectives are to (1) identify agronomic risks linked to the ability of R. maidis to shift from its host plant to M. × giganteus, and (2) characterize the susceptibility levels of the three miscanthus species to R. maidis. This cosmopolitan aphid is indeed a significant pest of cereals such as barley, sorghum, and maize (Blackman and Eastop, 2007). Damage caused by R. maidis is currently restricted to tropical and warmer temperate regions where its anholocyclic populations can reach high densities (Blackman and Eastop, 2007). However, the abundance of R. maidis should increase in cooler regions in response to climate warming and intensified cereal cropping (Harrington, 2007), which should inevitably increase its pest status in these regions. We evaluated performance and plant penetration behavior of R. maidis on the three miscanthus species and barley. Miscanthus × giganteus being the only miscanthus species so far planted for biomass purposes, it was used as reference plant species for comparisons of performance and behavioral parameters in this study.
Section snippets
Insects
A laboratory colony of the aphid Rhopalosiphum maidis was initiated from a parthenogenetic aphid population. Aphids were reared on plants of winter barley (Hordeum vulgare var. Cervoise). Pots (90 mm × 90 mm × 70 mm) containing 25–30 barley plants were placed in ventilated Plexiglas® cages (240 mm × 110 mm × 360 mm) and maintained in a growth chamber under 20 ± 2 °C, 60 ± 5% relative humidity, and a 16:8 L:D light cycle.
Plants
Plantlets of the three miscanthus species, i.e., M. × giganteus (var. GigB, 2n = 3x = 57), M.
Comparison between the hybrid M. × giganteus and the reference host plant H. vulgare
Performance parameters were generally better on H. vulgare compared to M. × giganteus (Table 1). The pre-reproductive period duration was shorter (Mann–Whitney U test: U = 147, P = 0.003) and an increase of rm with a consecutive shorter DT (Mann–Whitney U test: U = 122, P = 0.008 for both parameters) was observed on H. vulgare. Also, when aphids were reared on H. vulgare, the nymphal survival rate (81%) was higher than on M. × giganteus (55%) (Fisher's exact test: P < 0.001).
Comparisons between the hybrid M. × giganteus and the parental species M. sinensis and M. sacchariflorus
The pre-reproductive period
Discussion
This study clearly showed that R. maidis was able to develop and reproduce on the three species belonging to the Miscanthus genus studied here. Consequently, R. maidis can be considered as a potential ‘colonizing aphid’ and the miscanthus species tested as potential reservoirs for this aphid species. Our results are in accordance with Huggett et al. (1999) who suggested that miscanthus crops, because of their perennial status, were likely to serve as intermediate hosts for R. maidis when wheat,
Acknowledgments
We would like to acknowledge the financial support from the Picardie region (research project MISCPIC). We also thank G. Labonne (UMR BGPI, Montpellier, France) for providing the R. maidis population. Andrew Roots is thanked for its critical reading of the manuscript especially concerning the English language.
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