Elsevier

Virus Research

Volume 120, Issues 1–2, September 2006, Pages 1-16
Virus Research

Review
Protecting crops from non-persistently aphid-transmitted viruses: A review on the use of barrier plants as a management tool

https://doi.org/10.1016/j.virusres.2006.02.006Get rights and content

Abstract

Barrier plants are a management tool based on secondary plants used within or bordering a primary crop for the purpose of disease control. Aphid-transmitted viruses account for approximately 50% of the 600 known viruses with an invertebrate vector. Barrier plants may act as real natural sinks for non-persistent aphid-transmitted viruses and have proved in the past to be an effective crop management strategy to protect against virus infection. Increasing the knowledge on aphid host seeking and flying behaviour, and on how barrier plants may affect the behaviour of aphids and their natural enemies will allow further development of this environmentally-friendly habitat manipulation strategy. An ideal plant barrier should be a non-host for the virus and the vector, but appealing to aphid landing and attractive to their natural enemies and should allow sufficient residence time to allow aphid probing before taking-off occurs. In this review, we have addressed why aphids are manageable by barrier cropping, the mechanisms by which barrier plants affect the occurrence of non-persistently aphid-transmitted viruses and the limitations of using barrier plants as a virus control strategy. Finally, we have pointed out future directions of research that should be conducted to integrate barrier cropping with other disease management strategies, and optimise and extend the use of barrier plants as a strategy for managing aphid-transmitted virus diseases.

Introduction

Aphids are among the most serious agricultural insect pests. They cause major economic losses in several crops worldwide, directly because of their feeding and indirectly by inflicting plant impairments (e.g., viruses, phytoxemias). However, their population threshold level as virus vectors is much lower than it is for them as direct pests (Satapathy, 1998). Aphids are the most common vectors of plant viruses, and aphid-borne non-persistently transmitted viral diseases (ABNPV) are of greatest economic importance in several annual cropping systems (Tomlinson, 1987). About 50% of the approximately 600 viruses with invertebrate vectors are transmitted by aphids and most of the roughly 290 known aphid borne viruses are non-persistent (NPV) (Hull, 2002). Non-persistent viruses are transmitted non-specifically by a large number of aphid species after very brief probes (1–2 min), are lost readily after probing on a healthy plant and have a short retention time in the vector (few hours). Conversely, persistent viruses are transmitted specifically by few aphid species that feed and colonise the crop, are retained in the vector for many days and transmitted after long inoculation access periods (optimum 24–48 h). Semipersistent transmission shares some of the properties of non-persistent and persistently transmitted viruses (for more information see reviews by Plumb and Callow, 2002, Ng and Perry, 2004).

Current control strategies for aphids regularly rely upon pesticide applications. However, many aphid species have and continue to become resistant to various classes of chemical compounds (Furk and Hines, 1993, Perring et al., 1999, Nebeshima et al., 2003, Li and Han, 2004). Additionally, insecticides are largely ineffective in managing ABNPVs (Raccah, 1986, Howell, 1993, Perring et al., 1999). Furthermore, insecticides may contribute to the spread of virus transmission by inducing greater vector activity (Budnik et al., 1996). Therefore, the development of non-chemical management strategies for controlling aphid vectors of NPVs is warranted.

It is well known that flora diversification can result in reduced pest population (references in reviews by Andow, 1991, Hooks and Johnson, 2003). It has also been established that the number of alatae and apterae aphids found on primary crops are consistently less in vegetational diverse than monoculture habitats (Smith, 1969, Smith, 1976, Horn, 1981, Costello and Altieri, 1995, Hooks et al., 1998, Showler and Greenberg, 2003). Thus, it is equitable to suppose that if an aphid population is recurrently found at lower numbers on host plants in vegetationally diverse habitats, this will provisionally result in decrease incidences of ABNPV. Still, there are few published studies where secondary crops or plants have been specifically used to reduce the occurrence of ABNPV. Secondary plants used within or bordering a primary crop for the purpose of disease suppression are often referred to as barrier crops (Deol and Rataul, 1978). This approach belongs to the wide array of habitat manipulation strategies that aims at making crops less favourable for pests and more attractive to beneficial insects. Barrier cropping is a cultural technique that perfectly fits under the philosophy of “Ecological Engineering for Pest Management” recently reviewed by Gurr et al., 2004. Among those studies in which barrier plants were investigated, many showed that barrier cropping lessens the incidence and/or hinders the spread of aphid-borne non-persistent viruses (Fereres, 2000, several references therein). Despite the potential success of using barrier plants for vector management, this tactic has received limited research attention compared with other management strategies. For example, the use of inert material such as reflective mulches and row covers (Perring et al., 1989, Webb and Linda, 1992, Brown et al., 1993, Stapleton and Summers, 2002) and mineral oils (Vanderveken and Semal, 1966, Webb and Linda, 1993, Wang and Pirone, 1996, Asjes, 2000) have been extensively investigated and many growers are familiar with these traditional management practices. Barrier cropping can also become a recognized component of integrated disease management (IDM). Presently, greater dissemination of information on this tactic for viral disease management is needed so that the agricultural community becomes better acquainted with this cultural management tool.

It is not our goal to conduct a thorough review of barrier cropping. We aim by reviewing the literature to: (1) alert readers that plant diversification in the form of barrier plants should receive greater recognition as a tenable management tactic for reducing the occurrence and spread of ABNPV, (2) give a holistic account of the mechanisms most responsible for the rate of spread of NPVs in florally diverse habitats and (3) suggest future direction of barrier cropping research. For the sake of simplicity, any form of plant diversification (e.g., mixed cropping, cover crops, border plants, intercrops, trap crops, flower strips, organic mulch, etc.) used to protect a primary crop from insect transmitted viral diseases will be referred to as barrier cropping regardless of its layout, composition or how it impacts vector behaviour.

Section snippets

Limitations of current control strategies

Insecticidal control of aphids that transmit plant viruses in a non-persistent manner may not reliably prevent the spread of disease within the field (Thackray et al., 2000). This is presumably due to the very short acquisition and inoculation times involved (Perring et al., 1999). Aphids are capable of transmitting NPVs prior to obtaining a lethal insecticide dose (Gibson and Rice, 1989). In some instances, insecticides may increase, rather than suppress the spread of virus transmission by

Aphid behaviour

There are several aspects of aphid behaviour that conjecturally makes them manageable by barrier cropping; much of which centres around their visual host finding activities while in flight. For example, during flight, aphids respond strongly to visual stimuli (Kring, 1972) and locate host plants by contrasting the soil background with the green colour of plant foliage (Kennedy et al., 1959, Kennedy et al., 1961). Therefore, the greater the percentage of vegetative cover in a crop field, the

Virus-sink hypothesis

In several studies investigating the use of barrier plants to manage non-persistently transmitted viruses no attempts were made to determine the underlying causes of experimental findings. An exception involved studies conducted in Spain by Fereres (2000). Fereres used a combination of laboratory and field experiments to test the potential use of sorghum (Sorghum vulgare) and maize (Zea mays) as barriers to protect pepper (Capsicum annuum) plants against Potato virus Y (PVY) and CMV. He

Limitations of using barrier plants

The findings from several studies indicate that barrier cropping can be successfully used to significantly mitigate the severity of yield lost caused by non-persistently transmitted aphid-borne viruses (Table 1). Still there may be limitations to deploying this strategy under conditions of polycyclic disease spread or when trying to protect a perennial host crop. For example, eastern gamagrass, Tripsacum dactyloides is a perennial grain susceptible to infection by viruses such as Sugarcane

Incorporating barrier cropping with other disease management strategies

In this review, we focus our attention on one tool (i.e., barrier cropping) for mitigating yield constraints menaced by aphid carriers of NPVs. However, it has been suggested that understanding environmental influences on insect-borne viruses requires more than knowledge on the effects of individual tactics (Irwin et al., 2000). Indeed it is critical that multiple pest management tactics be examined concomitantly, so that the opportunity for successful vector suppression rises. In many

Future use of barrier cropping

Several field experiments (Table 1) have shown that barrier cropping can be successfully used to lessen the occurrence of insect transmitted diseases resulting in increased crop yields. In addition to their potential to reduce the severity of ABNPVs, barrier plants may help lower the occurrences of other insect transmitted plant pathogens. For example, Heathcote (1968) found that rows of mustard (Brassica juncea) or barley intercropped with sugar beet (Beta vulgaris could reduce the occurrence

Vector behaviour

One aim of the review was to bring to surface the techniques responsible for virus occurrences in barrier cropped habitats. The findings revealed may not unequivocally explain all mechanisms contributable to reduced virus spread in flora diverse habitats, but it provides some clarification on the crucial factors accountable for disease suppression. Still, most of the reasons cited for disease occurrences in Table 1 were based on the original authors’ opinion and in most instances the

Concluding remarks

This review has identified several studies showing that barrier cropping is a promising tactic for mitigating yield losses caused by ABNPVs. Despite the number of published “triumphs” on barrier cropping, most studies fail to scrutinize the underlying reasons for reduced virus spread. In many instances, readers have to make tentative assumptions or entrust suggestions made by the original authors on the causes of virus suppression. This review has recognized several possible mechanisms, which

Acknowledgements

The authors thank Rodrigo P.P. Almeida and two anonymous referees for helpful comments on earlier drafts. CRRH was supported by a Western Region IPM Grant (Project number 2004-05060).

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