Additional records of Entomophthora aphidis and E. planchoniana from aphids in New Zealand

Abstract

The place of Entomophthora spp. in natural control of aphids in New Zealand was noted by Lowe (1973), who stated that the incidence of these pathogens in economically important aphids is not normally sufficient to control high-density populations. Nevertheless, it has been considered desirable to determine the species of fungi present, and to record the aphid species attacked and their host plants. Some such records were given by Hall et al. (1976), who also listed earlier references. The additional records tabulated below are from collections made at Christchurch by Lowe, unless otherwise indicated. Determinations of the two species of Entomophthora were by Hall, and of host plants by Botany Division, Department of Scientific and Industrial Research, Lincoln.     

The survival of Entomophthora spp. in mummified aphids at different temperatures and humidities

Entomophthora aphidis survived for at least 32 weeks at 0°C and 20 or 50% RH and E. thaxteriana for at least 16 weeks at 10°C and 20 or 50% RH in mummified infected pea aphids, Acyrthosiphon pisum. The fungi produced infective conidia when the aphids were moistened. This probably explains the survival of Entomophthora species infecting aphids during short periods when the weather is unsuitable for conidial discharge and host infection.     

Entomophthora species infecting pea aphis

• 1 Three species of Entomophthora infected the pea aphis, Acyrthosiphon pisum, on lucerne at Rothamsted Experimental Station, Harpenden, Hertfordshire, between 1967 and 1972 and caused a maximum mortality of 83% in July 1968.
• 2 E.thaxteriana, the commonest species, occurred each year and frequently infected aphids during cool weather in spring and autumn. E.aphidis and E.planchoniana were absent in some years and were most common during warm weather in midsummer.
• 3 The incidence of infection by the three species was correlated with the density of conidia in the air above the crop, host density and rainfall, but not with any other weather factor considered.
• 4 Infection at any time was much more closely related to environmental factors during the preceding 12 than 3 days. The regressions, however, were weak and the relative importance of different environmental factors for the spread of infection can probably only be determined under controlled conditions in the laboratory.

     

The effect of introducing the aphid-pathogenic fungus Erynia neoaphidis into populations of cereal aphids

The aphid-pathogenic fungus Erynia neoaphidis, as dried fungus-infected aphids, was applied to caged plots of winter wheat infested with cereal aphids at two sites, one in Hertfordshire and the other in Hampshire, in 1983. In each trial, the fungus became established in the aphid populations in the treated plots even though conditions were drier than average and therefore sub-optimal for fungus spread. Treatment applied in the third week of June increased the proportion of infected aphids more than that applied two weeks later at one site, and the early application was the only treatment to have an obvious effect at the other. In spite of the observed effect of treatments on the proportion of infected aphids, the fungus failed to reduce the numbers of aphids relative to those in untreated plots, chiefly because in these plots many aphids were killed by fungi of the same species as that introduced and other related species from natural sources. Artificial introduction of E. neoaphidis acts too slowly and unpredictably to be likely to form a practical alternative to conventional insecticides for cereal aphid control.     

Infection of Sentinel Cotton Aphids (Homoptera: Aphididae) by Aerial Conidia ofNeozygites fresenii(Entomophthorales: Neozygitaceae)

Uninfected adultAphis gossypii(Homoptera: Aphididae) apterae (sentinel aphids) on cotton leaves were exposed for 8 h to the air over a commercial cotton field in Louisiana during the night of 1–2 July 1995. At 0015 h there were 90,437 primary conidia/m³air of the fungusNeozygites fresenii(Entomophthorales: Neozygitaceae) at the midfield position as determined from Rotorod samples. Forty-eight percent (n = 106) of the sentinel aphids exposed for 8 h at midfield were infected by aerial conidia ofN. fresenii.Exposure of sentinel aphids outside the cotton field, at 10 and 100 m downwind and 10 m upwind, resulted in 34.8% (n = 131), 24.0% (n = 129), and 17.4% (n = 146) infected aphids, respectively. These data demonstrate that wind-dispersed aerial conidia ofN. freseniiare infective and rapidly and efficiently disperse the pathogen throughout aphid populations within and between fields.     

Selection of an Isolate of the Insect Pathogenic Fungus Metarhizium anisopliae Virulent to the Lettuce Root Aphid, Pemphigus bursarius

The virulence of hyphomycete entomopathogenic fungi was measured in laboratory bioassays against the lettuce root aphid, Pemphigus bursarius, a serious pest of field lettuce grown in the UK. Of 25 isolates of fungi examined, only one isolate, Metarhizium anisopliae 391.93, killed lettuce root aphids consistently. This fungus was isolated originally from the closely related saltmarsh aphid, P. trehernei. The median lethal concentration of conidia at 10 days post6- 1 inoculation estimated from five independent bioassays was 2.45 × 10⁶ conidia ml^-1. The fungus had no significant effect on the mean number of offspring/aphid produced, but it sporulated 6 profusely on host cadavers, producing approximately 4 × 10⁶ conidia/cadaver 14 days after treatment, and diseased aphids died attached to plant roots. It thus has the potential to spread through densely packed colonies of P. bursarius feeding on the roots of susceptible or partially resistant plants.     

Observations on the Occurrence of Entomophthorales Infecting Aphids (Aphidoidea) in Slovakia

The species spectrum of entomophthoralean fungi parasiting aphids was investigated in Slovakia. The surveys focused on aphid fauna occupying both agricultural crops and vegetation at non-crop sites. During the surveys, 15 different entomophthoralean species were identified from 66 aphid species. Of these 15 fungal species, eight had not previously been recorded in Slovakia and one species, Erynia erinacea (Ben-Ze’ev et Kenneth) Remaudière et Hennebert, had not been recorded previously in Central Europe. New hosts for some parasitic fungi were also recorded. The occurrence of fungal infection and the fungal species spectrum varied with sampling period and sampling area. In general, the fungi were observed parasiting aphid populations from April until November. Pandora neoaphidis (Remaudière et Hennebert) Humber was the predominant fungal pathogen and could effectively reduce aphid populations. Entomophthora planchoniana Cornu and Conidiobolus obscurus (Hall et Dunn) Remaudière et Keller were also common pathogens of aphids, but without an epizootic potential. On the other hand, Neozygites fresenii (Nowakowski) Remaudière et Keller had a strong tendency to establish epizootics in dense aphid colonies, especially in those of the black bean aphid. Other entomophthoralean species observed in the country were considered to be minor aphid pathogens on account of their low occurrence, lower specificity to aphids, or high specificity to a single aphid species. This is the first detailed report to date on the occurrence of Entomophthorales in Slovakia.     

Growth, development and consumption by four syrphid species associated with the lettuce aphid, Nasonovia ribisnigri, in California

The lettuce aphid, Nasonovia ribisnigri Mosley, was accidentally introduced into California from Europe during the late 1990s and soon became an economic pest of Romaine lettuce along California’s central coast region. Indigenous syrphid larvae attack the lettuce aphid and are believed to be effective in the management of this invasive pest, although there have been no studies on the capacity of the syrphid larvae to kill and consume lettuce aphids. We focused on four syrphid species commonly found in central coast lettuce fields: Allograpta obliqua (Say), Eupeodes fumipennis (Thomson), Sphaerophoria sulphuripes (Thomson), and Toxomerus marginatus (Say). Laboratory feeding experiments were conducted to estimate the development times of all juvenile stages, the daily growth rate of larvae, the number of third instar aphids killed, the aphid biomass killed, and the aphid biomass consumed as measures of predator performance. Results show that during larval development E. fumipennis killed the most third-instar aphids (507 aphids, 88 mg biomass killed) and reached the largest size, followed by A. obliqua (228 aphids, 39 mg killed), S. sulphuripes (194 aphids, 31 mg killed) and T. marginatus (132 aphids, 20 mg killed). Body size alone did not account for species differences in per-capita larval consumption rates. This information is discussed in relation to the predation potential of syrphids through the short cropping cycle of lettuce, and the choice of plant species to use for floral resource provisioning to enhance the activity of syrphids needed for effective management of lettuce aphids in California’s central coast fields.     

Improving secondary pick up of insect fungal pathogen conidia by manipulating host behaviour

It is often assumed that efficient application of a mycoinsecticide involves hitting the target pest insect directly with a lethal dose of conidia. However, secondary pick‐up of conidia from surrounding vegetation may be a more important source of inoculum. We have investigated ways of increasing conidia acquisition by enhancing host movement. The aphid alarm pheromone, E‐β‐farnesene, significantly increased mortality among peach potato aphids. Myzus persicae Sulzer, that were exposed for 24 h to discs of green pepper leaf sprayed with conidia of Verticillium lecanii (Zimmerman) Viegas then transferred to fresh untreated discs to allow disease development. A more practical approach to increasing conidia pick‐up appears to be the use of sub‐lethal doses of the chloronicotinyl insecticide imidacloprid. One percent of the recommended dose, applied systemically, dramatically increased aphid movement; quantified by image analysis of videotaped aphid behaviour. This resulted in greater mortality from mycosis in experiments where aphids were exposed to insecticide‐treated leaf discs that had been sprayed with fungal conidia. A comparison with results from an experiment where conidia were sprayed directly onto aphids which were feeding on insecticide‐infused pepper discs established that synergy was due to an indirect effect of the insecticide, i.e. through increased movement, rather than a direct effect viz. predisposition of insecticide‐weakened insects to disease.     

Infection of cereal aphids by the fungus Entomophthora

Three species of Entomophthora killed many Metopolophium dirhodum, M. festucae and Sitobion avenae on wheat at Harpenden, Hertfordshire, in 1971. Rainfall was low and aphid numbers were small in May and there was no Entomophthora infection. E. planchoniana first infected M. dirhodum early in June and the percentage of each aphid species infected increased during and after heavier rain in the first 2 weeks of June. M. dirhodum and S. avenae were most often infected by E. planchoniana, and the less common M. festucae mostly by E. aphidis and E. thaxteriana. Relative frequencies of E. aphidis and E. thaxteriana were largest before, and of E. planchoniana after, mid-July. The largest percentages infected were 53% of M. dirhodum and 30% of S. avenae during the second half of July and 60% of M. festucae in late June. The percentages of old nymphs and apterous adults that were infected were similar and only about half those of infected alatae.     

Entomophthora pyriformis,sp. n., entomophthorale parasite de puceron

Summary A new species ofEntomophthora found in France on Aphids is described as new under the nameE, pyriformis. It is distinguished by the following characters: multinucleate, pear-shaped conidia, with large papilla; small resting spores; short, more or less branched hyphal bodies. A key of determination is given for the Aphid parasiteEntomophthora species with more or less spherical conidia.      

The relationship between conidial dose,moulting and insect developmental stage on the susceptibility of cotton aphid,Aphis gossypii,to conidia of Lecanicillium attenuatum,an entomopathogenic fungus

The cotton aphid is one of the most serious pests of greenhouse vegetable crops worldwide. It is difficult to control because field populations usually include simultaneously several insect developmental stages. The current research evaluated an isolate (CS625) of Lecanicillium attenuatum, a fungal pathogen of aphids, as to its virulence against different developmental stages of cotton aphid, Aphis gossypii. The influence on mortality of several other factors also was examined: (a) insect moulting, (b) the number of conidia attached to insect cuticles and (c) germination rates of conidia on cuticles of aphids at various developmental stages. Mortality of cotton aphids treated with L. attenuatum conidia varied according to the developmental stage of the host, i.e. the LT_50s with third-instar nymphs and adults was shorter than with first-instar nymphs. The number of spores attached to the surface of first-instar nymphs was approximately one-half of that on third-instar nymphs and adults. Also, the level of spore germination on the surface of first-instar nymphs was lower than on the surface of other stages of the aphid. After moulting, the numbers of conidia attached to new insect cuticles were less than on exuviae. These results suggest that early nymphal stages of cotton aphids may escape fungal disease due, at least in part, to a combination of three factors: low numbers of conidia attached to their cuticles; low levels of conidial germination and rapid ecdyses, which removed conidia before their germ tubes penetrated the host hemolymph.     

Occurrence and distribution of entomophthoralean fungi infecting aphids in mainland China

Seventeen species of entomophthoralean fungi infecting 15 species of aphids have been reported from mainland China. They belong to seven genera: Batkoa, Conidiobolus, Entomophthora, Neozygites, Pandora, Tarichium and Zoophthora. C. thromboides, E. planchoniana, N. fresenii and P. neoaphidis have the widest distributions covering five regions with the exception of the south-west. Tarichium atrospermum and Z. canadensis were only reported in the eastern region and P. echinospora only in the mid-southern region. Pandora neoaphidis, the most common species, occurred in many aphid populations. Species belonging to the genus Conidiobolus frequently appeared in the warm summer season, however, disease incidence was lower compared to the genus Pandora.     

The role of the perennial stinging nettle, Urtica dioica, as a reservoir of beneficial natural enemies

A wide range of natural enemies, including predators, parasites and entomophagous fungi were observed to feed on the stinging nettle aphid, Microlophium carnosum, populations of which increased rapidly in late April and early May. Patches of stinging nettles thus served as an important alternate feeding site for some beneficial natural enemies before pest aphids appeared on cultivated plants. Anthocoridae, Miridae and Coccinellidae were the most abundant specific predators sampled on nettles; only the Coccinellidae appeared to disperse over a defined period to other habitats. The hymenopterous parasites Aphidius ervi and Ephedrus lacertosus parasitized up to 10% of M. carnosum populations in June: two species of the fungus Entomophthora occurred spasmodically. Cutting patches of nettles in May or June had the most striking effect on the species and numbers of Coccinellidae. Cutting in mid-June might increase the numbers and impact of natural enemies on nearby pest infestations.     

A description of the life cycle of Entomophthora sp. in the two-spotted spider mite

Entomophthora sp. killed its host, Tetranychus urticae, in 3.38 days at 25°C and in 11.02 days at 15°C. Development of hyphal bodies within the mite was studied with a light microscope, and a scanning electron microscope was used to examine spore development and structure. A comparison of this fungus with other mite-infecting fungi revealed that it is more closely related to E. floridana than to E. tetranychi, and should be called Entomophthora sp. near floridana until a more detailed study of E. floridana can be made.     

First survey on ecological host range of aphid pathogenic fungi (Phylum Entomophthoromycota) in Tunisia

Summary. The natural occurrence of fungal pathogens of aphids and their ecological host range was investigated in Tunisia from 2009 to 2012. The survey focused on aphid infesting different crops and weeds and included 10 different aphid species. Samples were collected from eight agricultural crops sites belonging to three different bioclimatic zones. Four pathogens from the phylum Entomophthoromycota were found to occur naturally in Tunisian ecosystems: Pandora neoaphidis (Entomophthorales: Entomophthoraceae), Entomophthora planchoniana (Entomophthorales: Entomophthoraceae), Conidiobolus obscurus (Entomophthorales: Ancylistaceae) and Neozygites fresenii (Neozygitales: Neozygitaceae). The occurrence of entomophthoralean fungi depended on the sampling area, the bioclimatic zone, and aphid species. P. neoaphidis and E. planchoniana were the predominant pathogens infecting a wide range of aphid species whereas C. obscurus and N. fresenii were sporadically present on a limited number of aphid species. This study is the first survey on ecological host range of entomophthoralean fungi in Tunisia, and the first documentation of C. obscurus and N. fresenii to occur in Tunisia and Maghreb Region.     

Natural occurrence of entomophthoroid fungi (Entomophthoromycota) of aphids (Hemiptera: Aphididae) on cereal crops in Argentina

The spectrum of entomophthoroid fungal species parasitising aphids on cereal crops and a study of the phenology and prevalence of these pathogens were investigated in Argentina. The studies were conducted at six different sites cultivated with crops of Triticum aestivum (wheat), Avena sativa (oats) and Sorghum bicolor (sorghum) during two consecutive years. Entomopathogenic fungi from the new phylum Entomophthoromycota were recorded from six aphid species on cereals in Argentina: Rhopalosiphum maidis, Rhopalosiphum padi, Rhopalosiphum rufiabdominalis, Schizaphis graminum, Sitobion avenae and Sipha maydis. Three species of entomophthoroid fungi were found infecting these aphid species: Pandora neoaphidis, Zoophthora radicans (Entomophthorales: Entomophthoraceae) and Neozygites fresenii (Neozygitales: Neozygitaceae). Entomophthoroid fungal infections occurred mostly in autumn–winter seasons (March–August), and coincided with periods of high relative humidity and comparatively low temperatures. This study represents the first base‐line characterisation of entomophthoroid fungi infecting aphids on cereal crops in Argentina.     

Influence of <Emphasis Type="Italic">Lecanicillium attenuatum</Emphasis> on the development and reproduction of the cotton aphid, <Emphasis Type="Italic">Aphis gossypii</Emphasis>

The activity of entomopathogens on insect pests has been investigated for many species but the influence of entomopathogenic fungi on factors other than mortality relating to population increase has not been frequently studied. The influence of Lecanicillium attenuatum CS625 (=Verticillium lecanii CS625) on development and reproduction of cotton aphid (Aphis gossypii) was investigated. A conidia suspension of the isolate was applied onto first instar nymphs. Increased spore concentration did not significantly affect each nymphal stage, total nymphal period, pre-reproductive period and the age of first larviposition. A significant dose effect on reduction of life span, reproductive period and fecundity was observed in 1st and 3rd instars after spore application. When conidia were applied to 1st instars, life span was significantly reduced to 10.8 and 8.4 days at 1 × 10⁴ and 1 × 10⁸ conidia/ml, respectively from 12.2 days in the control. During the life span, total fecundity was 41 ± 7.3, 26 ± 0.8 and 22 ± 5.7 nymphs per female at 1 × 10⁴, 1 × 10⁶ and 1 × 10⁸ conidia/ml, respectively compared with 51 ± 2.0 nymphs per untreated female. Reproduction period was also significantly shortened with increasing spore concentration. Application of spores to 3rd instars showed a similar trend. However, daily fecundity of individual aphids was not affected by spore dose. It was concluded that the isolate of L. attenuatum is able to affect populations of cotton aphid by reducing life span and total fecundity as well as by killing the aphids directly.     

Microcosm studies on intraguild predation between female erigonid spiders and lacewing larvae and influence of single versus multiple predators on cereal aphids

Abstract: Intraguild predation between female erigonid spiders [Erigone atra (Blackwall) and Oedothorax apicatus (Blackwall), Araneae, Erigonidae] and lacewing larvae (second instar larvae of Chrysoperla carnea (Stephens), Neuropt., Chrysopidae) and interaction effects of predator combinations on cereal aphids were investigated in a microcosm system under laboratory conditions. The microcosm experiments were run for 7 days and consisted of 15wheat seedlings, 15 Sitobion avenae (F) (Hom., Aphididae) as start population, plus a female spider or a lacewing larva or a combination of a spider plus a lacewing larva. The mortality rate of lacewing larvae was significantly increased by 44 and 31% due to intraguild predation by female spiders of E. atra and O. apicatus in comparison with lacewing larvae that were kept alone. The final aphid numbers in the microcosms were significantly reduced by all single predator treatments (spiders, lacewing larvae) and the predator combinations in comparison with controls without predators. The predation effect on aphid populations due to both spider species was similar and not statistically different. An additive effect of the predator combinations ‘spider plus surviving lacewing larva’ was found for both spider species resulting in reduced aphid numbers compared with the single predator treatments. When the lacewing larva was killed by an E. atra female the effects on aphids were non‐additive, but aphid numbers were not statistically increased compared with the lacewing larva treatment. When the lacewing larva was killed by an O. apicatus female, the effects of spider and C. carnea larva were additive on aphid numbers. In the presence of additional prey (fruit flies and Collembola) intraguild predation was not found and E. atra females had no significant effect on the survival of lacewing larvae. In addition, E. atra females had no significant effect on aphid numbers in the presence of fruit flies and Collembola, but in combination with a lacewing larva that survived, a significantly greater reduction of the aphid population was observed compared with the lacewing larva treatment. The body mass of lacewing larvae at the end of the experiment was not statistically influenced by the presence or absence of an E. atra female.     

Introduced ants reduce interaction diversity in a multi‐species,ant–aphid mutualism

Mutualisms contribute in fundamental ways to the origin, maintenance and organization of biological diversity. Introduced species commonly participate in mutualisms, but how this phenomenon affects patterns of interactions among native mutualists remains incompletely understood. Here we examine how networks of interactions among aphid‐tending ants, ant‐tended aphids, and aphid‐attacking parasitoid wasps differ between 12 spatially paired riparian study sites with and without the introduced Argentine ant Linepithema humile in southern California. To resolve challenges in species identification, we used DNA barcoding to identify aphids and screen for parasitoid wasps (developing inside their aphid hosts) from 170 aphid aggregations sampled on arroyo willow Salix lasiolepis. Compared to uninvaded sites, invaded sites supported significantly fewer species of aphid‐tending ants and ant‐tended aphids. At invaded sites, for example, we found only two species of ant‐tended aphids, which were exclusively tended by L. humile, whereas at uninvaded sites we found 20 unique ant–aphid interactions involving eight species of ant‐tended aphids and nine species of aphid‐tending ants. Ant–aphid linkage density was thus significantly lower at invaded sites compared to uninvaded sites. We detected aphid parasitoids in 14% (28/198) of all aphid aggregations. Although the level of parasitism did not differ between invaded and uninvaded sites, more species of wasps were detected within uninvaded sites compared to invaded sites. These results provide a striking example of how the assimilation of introduced species into multi‐species mutualisms can reduce interaction diversity with potential consequences for species persistence.