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Identification & Distribution

Feeding by Brachycaudus helichrysi in spring induces pseudogall formation on their host Prunus, with the leaves rolling up tightly perpendicular to their mid-rib and laterally (see first picture below). The adult aptera of Brachycaudus helichrysi (see second picture below) is variable in colour, ranging from yellow to green to pink to white, often shiny with a slight wax dusting. Their antennae are shorter than the body with dusky tips. The dorsum of the abdomen is without a black shield. Their siphunculi are pale, tapered and short - 0.8-2.0 times the length of the cauda. The cauda is pale, short and blunt. The body length of Brachycaudus helichrysi apterae is 0.9 - 2.0mm.

The alate Brachycaudus helichrysi (see third picture above) has a dark dorsal abdominal patch, with 13-46 secondary rhinaria on the third antennal segment and 0-18 on the fourth.

The micrographs below show dorso-lateral views of an adult Brachycaudus helichrysi aptera and an alate vivipara, both in alcohol.

The clarified slide mounts below are of adult viviparous female Brachycaudus helichrysi from their primary host : wingless, and winged.

Micrographs of clarified mounts by permission of Roger Blackman, copyright AWP all rights reserved.

The leaf-curling plum aphid host alternates between various plum (Prunus) species (especially domestic plum and blackthorn, Prunus spinosa) and a wide range of Asteraceae such as asters, chrysanthemums, yarrow and groundsel. Brachycaudus helichrysi populations on red clover (Trifolium pratense) have been called var warei, but are not thought sufficiently distinct to warrant subspecific status. Anholocyclic populations occur in warmer regions and in glasshouses, and are sometimes found on new growth of various trees. This aphid is a serious pest on fruit trees and sunflowers. The distribution of Brachycaudus helichrysi sensu lato is cosmopolitan, but recent molecular studies have shown they comprise at least three sibling species which evolved in geographically isolated populations.

 

Biology & Ecology

Molecular identity

Molecular studies have now revealed that populations identified as Brachycaudus helichrysi throughout the world comprise several forms that are sufficiently distinct to be regarded as sibling species, genetically isolated from each other (Pifaretti et al. 2012 2013). Host alternation to Prunus domestica and related species only occurs in one of these forms (H1), in regions with a continental climate. The second form (H2) is mainly anholocyclic, and is mostly absent from the coldest regions, but has been shown to have a sexual phase on peach (Prunus persica) in northern India. Mixed populations of the two forms often occur on herbaceous hosts, and no clear differences in host preference on herbaceous plants between these two forms have so far been detected. Popkin et al. (2017) carried out further studies on the phylogeography of Brachycaudus helichrysi. Using a combination of DNA markers on a set of specimens sampled worldwide, they confirmed the existence of two main lineages (H1 and H2), with differing life cycles. They further characterized a third lineage (H3), restricted to East Asia, which is associated with apricot trees and Prunus species that are endemic to this region. The divergence of the lineages postdates the speciation of associated Prunus species but precedes their domestication. Their results suggest that, in Brachycaudus helichrysi, the differentiation between host-specific lineages initially started in geographically isolated populations, which subsequently each adapted to local Prunus species.

Life cycle

Bell (1983) carried out laboratory studies in Northern Ireland in 1977-80 on the life-history of Brachycaudus helichrysi. The life-cycle differed in several respects from those previously reported for geographically distinct populations, especially with respect to the timing of egg hatch. Body length and antennal segment measurements of the adult stages on sloe (Prunus spinosa), the most important overwintering food-plant of the aphid in the province, and red clover (Trifolium pratense), a summer food-plant, correlated well with published dimensions for the species.

Madsen & Bailey (1958) reviewed the biology of the leaf curl plum aphid in Northern California. Although the aphid has a very extensive host range, in California it is closely associated with plum. It overwinters as an egg located between or behind the buds. The eggs hatch about the petal fall stage of the plums, and the stem mothers give rise to small green apterous forms which tightly curl the leaves (see picture below). The aphids continue to reproduce within the curled leaves, infesting new growth until early June. At that time, alates are produced which leave the plums for an unknown alternate host. In late fall, alates return to the plums and give rise to small brown oviparae which mate and lay the overwintering eggs.

Talhouk (1972) described the life cycles of aphids infesting almond trees in the Lebanon. One species is Brachycaudus helichrysi, which is holocyclic, with winter eggs hatching in mid-March, apterous fundatrices and fundatrigeniae are present until mid-June and alates from mid-May. Most of the alates migrate to summer food-plants (mainly Prunus species) and the few remaining on almond after May are destroyed by predators and parasites. Feeding by this species results in leaf curling, growth stunting and irregular curvature of almond twigs. Brachycaudus helichrysi produces abundant honeydew and is well attended by ants (see picture below).

The other aphid species is Pterochloroides persicae which reproduces parthenogenetically on the bark of almond throughout the year on the warmer western side of Lebanon. In the east, which is dryer and cooler, with freezing temperatures in winter, sexual females and males appear in October-November, winter eggs are laid from late October to mid-January and hatch between mid-January and mid-March, and adult fundatrices are present from mid-April, fundatrigeniae until early May and alates in June-July, these latter migrating to other almond trees or to peach; colonies at this time are small with individuals widely scattered. This species does not depend on attendance by ants for survival as it can eject its honeydew efficiently, but ants are often present collecting existing honeydew deposits. Pterochloroides persicae has few predators and apparently no parasites in the Lebanon.

Natural enemies

Arora et al. (2009) looked at the population dynamics of leaf curling aphid, Brachycaudus helichrysi and its natural enemies in India. Both humidity and temperature were found to be positively correlated with population build up of the pest. Nymphs produced in the last week of November overwintered in the axils and bases of dormant buds of peach tree. The coccinellids Coccinella septempunctata, Leis dimidiata and Coelophora sauzeti, and the syrphids Ischiodon scutellaris, Paragus serratus and Paragus tibialis were recorded as aphidophagous predators and Diaeretiella rapae and an Aphidius species as parasitoids of the pest.

Verma & Chowdhuri (1975) observed Coccinella septempunctata feeding on Brachycaudus helichrysi on peach at Mashobra, Himachal Pradesh, India. Subsequent jar tests in the laboratory showed that one coccinellid adult ate an average of 42, 49 and 46 aphids/day at various set temperatures and humidities.

 

Other aphids on same host

Brachycaudus helichrysi has been recorded from 29 Prunus species.

 

Damage and control

Damage

Brachycaudus helichrysi is a little unusual amongst aphids in that it can be a major aphid pest on both its primary host (plum, peach, almonds) and its secondary hosts (various members of the Asteraceae). On plum the fundatrices and their offspring cause severe curling of the foliage.

On the secondary host the toxic effect of its saliva causes crinkling of the foliage. It is also harmful to artichoke capitula (the immature composite inflorescences, 'heads', or 'buds'). It colonizes the underside of leaves, leads to blemishes on the bracts, induces hardening and reddening of those bracts which leads in turn to the formation of appearance of a waxy film. The species transmits some viruses that depend on the non-persistent (noncirculative) mode, such as cucumber mosaic virus (CMV).

Lerin & Badenhausser (1995) looked at the influence of the Brachycaudus helichrysi on stem diameter and seed yield of sunflower (Helianthus annuus) in Europe. Yield losses were assessed in open field conditions and natural infestations over a 3-year period in Central West France. Stem diameter at harvest was used as a covariate to take account of variation in plant vigour, as neither its relationship with seed yield nor its mean value was affected by aphid infestation. It was found that yield losses occurred when aphid populations exceeded 100 per plant at the budding stage. No yield loss was observed when populations were less than 100 aphids per plant at the budding stage, and then decreased. This gave growers ample time to monitor populations and treat crops.

Chemical control

Madsen & Bailey (1958) reviewed the control of the leaf curl plum aphid in Northern California. In 1953, the aphid caused considerable damage to plums in the foothill areas of California. Oil-dinitro treatments were effective in controlling the overwintering eggs, but injured some plum varieties. Oil-phosphate sprays at the delayed dormant stage also controlled the eggs and did not injure the trees. With the exception of Thimet, no phosphate tested gave control of the aphids once they were within the curled leaves.

Considerable efforts have been made in India to find the optimal chemical control strategy to control damaging Brachycaudus helichrysi populations of peach. The progeny of the overwintering fundatrix suck sap from the developing leaves and floral buds sometimes resulting in the complete failure of the crop. Kapoor et al. (1989) conducted field studies in Haryana, India, to determine the most effective time for spraying insecticides against the aphids Brachycaudus helichrysi and Myzus persicae on peach. Both 0.025% oxydemeton-methyl and 0.03% dimethoate resulted in a significant reduction in aphid numbers compared with an untreated control. Sprays given before and after flowering resulted in more fruits/branch and fewer aphids/branch than sprays given after flowering only. Chandel et al. (2000) described the insecticidal management of Brachycaudus helichrysi in the mid-hills of Himachal Pradesh. Control experiments revealed that of three systemic insecticides, namely oxydemeton-methyl (0.025%), dimethoate (0.03%), and phosphamidon (0.025 and 0.04%), sprayed on peach at different times, oxydemeton-methyl at pink bud stage gave the best results. Pink bud stage was found to be the critical stage for spraying as during this period natural enemies of the aphid were least active. However a higher economic return came from the use of phosphamidon.

There then followed a series of trials in peach orchards using the (then) new neonicitinoid insecticides against Brachycaudus helichrysi. Singh et al. (2003) found that spraying of imidacloprid 0.007% was the most effective treatment, closely followed by carbosulfan and thiamethoxam (in 2000) and carbosulfan, koranda and methyl demeton (in 2001). Mishra & Zafer (2005), working in Uttaranchal, found that 17.8% Imidacloprid gave the highest yield and increase in yield compared to six other insecticides and the control. Imidacloprid also gave the lowest leaf curl aphid incidence. More recently Sharma (2010) showed that imidacloprid (0.008%), thiamethoxam (0.006 and 0.008%) and acetamiprid (0.008%) were significantly more effective against nymphs and adults of Brachycaudus helichrysi in all the combinations of treatments. No population was recorded 5 days after application compared to untreated control (19.4 aphids/leaf). Dimethoate at all doses was less effective.

In China Chen ZhaoLuan et al. (2006) found that that Brachycaudus helichrysi and Rhopalosiphum nymphaeae were the dominant species which seriously attacked the plum trees they examined. Brachycaudus helichrysi mainly attacks young leaves and shoots, making the young leaves curled and deformed. Rhopalosiphum nymphaeae usually attacks the back surfaces of young leaves and the young shoots, covering them with a white powdery substance. It was shown that the best insecticides for control of these aphids were a 2000x dilution of 10% imidacloprid wettable powder, or a 2500x dilution of 1.8% abamectin.

Biological Control

Hall & Burges (1979) carried out laboratory and glasshouse tests in the UK in 1972-77 on the control of aphids on chrysanthemum plants with the fungus Verticillium lecanii (=Lecanicillium lecanii, a commercially-marketed entomopathogenic fungus). In small glasshouses, aqueous sprays of fungal spores eliminated small populations of Brachycaudus helichrysi in the vegetative tips of plants, but not when they were in an exposed position on mature flower buds. Control of another aphid species, Macrosiphoniella sanborni, was however variable, and usually commercially unsatisfactory. In contrast, in both small and large glasshouses, sparse populations of Myzus persicae, the major aphid pest, were successfully and consistently controlled, sometimes spectacularly. It was thought that a combination of species-characteristic feeding-site preferences on the exposed parts of plants, where microclimate humidity was probably low, and the relative immobility of Macrosiphoniella sanborni and Brachycaudus helichrysi explained why these aphids were more difficult to control than Myzus persicae. However, it should be possible to control satisfactorily all aphid species in large commercial glasshouses where humidity might be higher than in the small experimental glasshouses. A single spray was sufficient to introduce infection that controlled the aphids for the duration of the crop.

Integrated Control

Epstein et al. (2000) describes the changes in the management of Brachycaudus helichrysi in California. In the 1970s and 1980s the integrated pest management program for almonds, nectarines, peaches, plums and prunes was to apply an organophosphate insecticide (e.g. diazinon), generally with oil, during the winter dormant season. This effectively controlled several different pest species, including Brachycaudus helichrysi. In the early 1970s this was viewed as environmentally sound, because one application in the dormant season potentially replaced multiple applications during the growing season. There were fewer adverse effects on beneficial insects, less exposure to field workers and no exposure of fruit to potential residues. However, there was organophosphate contamination of surface waters as a result of the organophosphate being washed off the orchards during winter rainstorms. Pressure on producers to reduce organophosphate use resulted in a modest decrease concomitant with an increase in dormant season pyrethroid application. There was also an increase in the 'monitor and treat only when pests are present' approach to control, at least for some of the pest species.

Hartfield & Campbell (1996) proposed the use of the selective insecticide pirimicarb for integrated pest management of plum aphids in UK orchards. Control measures used at that time for plum aphids in the UK involved tar oil winter washes and broad-spectrum insecticide sprays, both of which were damaging to natural enemy populations. In the absence of natural enemies, populations of pesticide-resistant Phorodon humuli increase unchecked. The effects of pirimicarb, a selective insecticide, on aphids and their natural enemies were assessed in plum orchard trials. The results confirmed the effectiveness of pirimicarb against spring populations of Brachycaudus helichrysi and showed no damaging effects on polyphagous predators. With these predator populations intact, the mid- to late-season populations of Phorodon humuli were heavily preyed upon and remained below economic thresholds. The selectivity of pirimicarb has made it a valuable component of an integrated pest management programme for plum aphids.

Acknowledgements

We especially thank Robin & Rosie Lloyd, The Long House Garden, for their kind assistance and permission to sample. Many thanks also to Roger Blackman for images of his clarified slide mounts.

We have made provisional identifications from high resolution photos of living specimens, along with host plant identity. In the great majority of cases, identifications have been confirmed by microscopic examination of preserved specimens. We have used the keys and species accounts of Blackman & Eastop (1994) and Blackman & Eastop (2006) supplemented with Blackman (1974), Stroyan (1977), Stroyan (1984), Blackman & Eastop (1984), Heie (1980-1995), Dixon & Thieme (2007) and Blackman (2010). We fully acknowledge these authors as the source for the (summarized) taxonomic information we have presented. Any errors in identification or information are ours alone, and we would be very grateful for any corrections. For assistance on the terms used for aphid morphology we suggest the figure provided by Blackman & Eastop (2006).

Useful weblinks

References

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