Novel strategies for aphid control using naturally occurring fungi

Abstract

A four-year project was undertaken to provide information on the epidemiology of the aphid-pathogenic fungus Pandora (= Erynia) neoaphidis which would facilitate its practical exploitation for microbial control of aphids in field crops. In particular we focused on the potential for managing field margins as reservoirs of P. neoaphidis in agroecosystems.

During field studies conducted between 2000 and 2003, six new P. neoaphidis isolates were collected from primrose, pea and nettle aphids and included for evaluation in laboratory assays. Aphids on grasses such as Yorkshire fog, legumes (e.g. bird's-foot trefoil, clover) and stinging nettle, amongst others, were identified as beneficial sources of P. neoaphidis within agroecosystems. At an experimental field margin on Rothamsted Farm, the largest aphid and fungus densities were recorded in 2001, but numbers were generally small in all other years. In bean and wheat crops, conidia of P. neoaphidis were mostly found within 2 m of artificial release points but could be detected 12 m away. Pest aphids placed within 2 m of fungal sources became infected. Trials in polytunnels demonstrated that pest aphids on crop plants could be infected by spores carried downwind from infected aphids on non-crop plants such as nettles.

The overall ranking for laboratory susceptibility of pest and non-pest aphids to P. neoaphidis was: Acyrthosiphon pisum > Aphis fabae, Microlophium carnosum, Metopolophium dirhodum, Myzus persicae, Uroleucon jaceae > Sitobion avenae > Brevicoryne brassicae, Rhopalosiphum padi. Isolates originally collected from non-pest aphids were able to infect pest aphids. There were no significant effects of host plant or cultivar (including a transgenic wheat cultivar expressing snowdrop lectin) on susceptibility of A. pisum, M. dirhodum or M. persicae to P. neoaphidis. Therefore, the host plant on which an aphid is feeding is unlikely to affect the performance of P. neoaphidis. Genotypes of M. persicae with high levels of esterase-based insecticide resistance were more resistant to fungal infection than insecticide-susceptible genotypes.

Species-specific molecular primers were developed for P. neoaphidis and the morphologically similar species P. kondoiensis. Intra-specific variation among P. neoaphidis isolates was quantified using ERIC, ISSR and RAPD PCR-based DNA fingerprint analyses. Three groups, or clusters, of P. neoaphidis isolates were established. Potential cluster- and isolate-specific diagnostic markers were identified and evaluated but require further development. Molecular studies supported laboratory bioassays which indicated free movement of P. neoaphidis isolates between different aphid species was possible. The optimal temperatures for growth of most P. neoaphidis isolates were between 18 and 22°C. Some isolates also grew reasonably well at 10-15°C. At recommended rates, chlorothalonil, dichlofluanid, fenhexamid, prochloraz and carbendazim completely inhibited germination of conidia of P. neoaphidis. Mycelial growth of one isolate, originally from nettle aphid, was less affected by the fungicide azoxystrobin compared with three isolates from pest aphids.

In summary, the project has provided substantial field and laboratory data on the factors influencing the epidemiology of P. neoaphidis in patchy aphid populations in fragmented agricultural landscapes. Both molecular and biological attributes of fungal isolates suggest free movement of isolates between different aphid hosts in the field. Field margin plants with potential as reservoirs have been identified and cross transmission and dispersal of the fungus between aphid species occurring in margins and crops was demonstrated. This underpins the exploitation of field margins as reservoirs of P. neoaphidis for pest aphid control.