Elsevier

Industrial Crops and Products

Volume 54, March 2014, Pages 135-141
Industrial Crops and Products

Differential performance and behavior of the corn leaf aphid, Rhopalosiphum maidis, on three species of the biomass crop miscanthus

https://doi.org/10.1016/j.indcrop.2014.01.018Get rights and content

Highlights

  • The corn leaf aphid Rhopalosiphum maidis is a potential pest of the promising bioenergy crop miscanthus.

  • We described the R. maidis colonization on three miscanthus species studied in Europe for biomass production.

  • M. sacchariflorus and M. sinensis were less suitable and acceptable host plants than M. × giganteus.

  • This methodology could be used to identify resistance traits to aphids in miscanthus.

Abstract

Miscanthus, a perennial C4-grass, is identified as a promising candidate for biomass production owing to its high yield potential under low nitrogen input and its low susceptibility to diseases and pests. However, some significant insect pests of conventional cereal grain crops such as the corn leaf aphid (Rhopalosiphum maidis) are able to develop on miscanthus. In the prospect of extensive planting of miscanthus for bioenergy, this may lead to the worsening of pest problems in the surrounding conventional crops. The aim of this study was to assess, through laboratory experiments, the ability of R. maidis to colonize three main miscanthus species studied in Europe for biomass production, i.e., Miscanthus × giganteus, M. sacchariflorus, and M. sinensis. In this purpose, comparative analyses of aphid's performance and plant penetration behavior were performed. Despite an altered plant penetration behavior on miscanthus, R. maidis was able to colonize (i.e., to develop and reproduce) the three miscanthus species tested and exhibited a behavior adapted to the transmission of both persistent and non-persistent phytoviruses. M. sacchariflorus and, to a lesser extent, M. sinensis were found less suitable and acceptable host plant for R. maidis than M. × giganteus. Results are discussed in terms of agronomic risks and implications for miscanthus improvement programs.

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.

References (42)

  • R.L. Blackman et al.

    Taxonomic issues

  • J.D. Bradshaw et al.

    First report of field populations of two potential aphid pests of the bioenergy crop Miscanthus × giganteus

    Folia Endocrinol.

    (2010)
  • D.G. Christian et al.

    First report of barley yellow dwarf luteovirus on Miscanthus in the United Kingdom

    Eur. J. Plant Pathol.

    (1994)
  • W.D. Clayton et al.

    Genera Graminum. Grasses of the world

    Kew Bull. Additional Ser.

    (1986)
  • J.C. Clifton-brown et al.

    Miscanthus biomass production for energy in Europe and its potential contribution to decreasing fossil fuel carbon emissions

    Glob. Change Biol.

    (2004)
  • Q. Coulette et al.

    Colonization of the biomass energy crop Miscanthus by the three aphid species, Aphis fabae, Myzus persicae, and Rhopalosiphum padi

    J. Econ. Entomol.

    (2013)
  • P.S. Curtis et al.

    Nitrogen and carbon dynamics in C3 and C4 estuarine marsh plants grown under elevated CO2 in situ

    Oecologia

    (1989)
  • P. Giordanengo

    DEMP 1.5.2, programme php pour calculer les paramètres démographiques (tables de survie)

    (2012)
  • P. Giordanengo

    EPG-Calc 5.1.2, programme php pour calculer les paramètres EPG

    (2012)
  • A. Givovich et al.

    Presence of a hydroxamic acid glucoside in wheat phloem sap, and its consequences for performance of Rhopalosiphum padi (L.) (Homoptera: Aphididae)

    J. Chem. Ecol.

    (1994)
  • K. Gloyna et al.

    Miscanthus, a host for larvae of a European population of Diabrotica v. virgifera

    J. Appl. Entomol.

    (2011)
  • Cited by (13)

    • Disentangling the ecotoxicological selectivity of clove essential oil against aphids and non-target ladybeetles

      2020, Science of the Total Environment
      Citation Excerpt :

      Curiously, despite its insecticide potential, clove essential oils have not been evaluated in agricultural scenarios involving aphids and their natural enemies such as ladybeetles. It becomes even more impressive when considering that crop fields infested with aphids such as Rhopalosiphum maidis F. (Hemiptera: Aphididae) can exhibit drastic yield reductions (up to 90%) due to these aphids' damage activities (e.g., viruses transmission, significant amounts of cell sap feeding and enormous quantities of sticky honeydew production) (Bing et al., 1991; Pointeau et al., 2014; Razmjou and Golizadeh, 2010; Van Emden and Harrington, 2017; Xie et al., 2014). The non-selective actions of aphid control tools (i.e., the synthetic compounds) also contribute to a reduction on yield (Amjad et al., 2018; Moscardini et al., 2015; Nawaz et al., 2017; Xiao et al., 2016; Yang et al., 2019).

    • Status of the bioenergy crop miscanthus as a potential reservoir for aphid pests

      2015, Industrial Crops and Products
      Citation Excerpt :

      However, the suitability of M. sacchariflorus to R. padi remained moderate as only three R. padi nymphs out of the 31 individuals tested reached the adult stage. In contrast, Pointeau et al. (2014) demonstrated that R. maidis was able to develop and reproduce and exhibited long phases of phloem sap ingestion on the three Miscanthus species (23–40% of the time over the duration of probing depending on the Miscanthus species). This could be explained by the fact that, contrary to R. padi, the corn leaf aphid R. maidis is also adapted to feed on C4-plants (Blackman and Eastop, 2000).

    • A new SAS program for behavioral analysis of electrical penetration graph data

      2015, Computers and Electronics in Agriculture
      Citation Excerpt :

      For example, the fifth event for insect 1 in cohort 1 was G, and this was the first G of three G events performed by this insect. Parameter versus variable: The early literature collectively calls the waveforms and derived values “parameters” (McLean and Kinsey, 1968) and this terminology continues to the present (Prado and Tjallingii, 1999, 2007; Walker and Backus, 2000; Giordanengo, 2014; Pointeau et al., 2014). However, recently, some authors have started using the term “response variable” or “variable” (Pelletier and Giguère, 2009; Serikawa et al., 2013; Tjallingii, 2014).

    • Insect vectors as drivers of plant virus emergence

      2015, Current Opinion in Virology
      Citation Excerpt :

      Under global warming, new vector species will migrate and colonize adapting to new regions with milder winters expanding vector-borne viruses. There are changes in agricultural practices itself, including the development of new biofuel crops, which are selected to increase biomass with the risk of becoming more susceptible to vectors or acting as an extensive monoculture reservoir of plant viruses [28]. This is the case of Arundo donax, considered as an invasive weed affecting water conservation in California, but recently approved as a biofuel crop.

    View all citing articles on Scopus
    View full text