Macrosiphum euphorbiae (potato aphid)

Host-alternating populations of M. euphorbiae disperse through migratory flights in the spring and autumn. The spring migration takes aphids from the overwintering host-plant (Rosa spp.) to a wide range of secondary host-plants, including potato, tomato, lettuce and other cultivated plants. Non-host alternating populations can survive year-round on secondary hosts, especially in greenhouse and other indoor environments. Aphids can be carried on foliage in trade. There is little evidence to suggest that the geographical range of this aphid is currently expanding.

M. euphorbiae was first described by Thomas (1878), from specimens collected in Illinois, USA. Eastop and Hille Ris Lambers (1976) listed synonyms of M. euphorbiae.

M. euphorbiae is a relatively large aphid, with an elongated pear-shaped body. It has a variable body colour, usually being either a shade of yellowish-green or pinkish-red.Wingless adult females (apterae) are medium to large in size, being 1.7-3.6 mm long, and pear-shaped in appearance. The body colour is variable, usually a shade of light- but sometimes yellowish-green, or pink or magenta. The body is often rather shiny and the eyes are distinctly reddish. The antennae are six-segmented, with two to six secondary sensoria on the basal half of segment three. Antennae are usually only dark apically, but sometimes almost entirely dark. The legs, siphunculi (cornicles) and cauda (tail) are usually the same colour as the body, but siphunculi are often darker toward the apices. The legs are noticeably long. Siphunculi have a slight apical constriction with several rows of polygonal reticulation in the constricted areas, and are relatively long, being approximately 6 to 11 times as long as wide. The cauda is also relatively long, more than twice as long as wide, elongate, finger-shaped and with 8-10 lateral setae and 2-3 dorsal pre-apical setae (Blackman and Eastop, 2000; Stoetzel and Miller, 1998).Wingless immature forms are rather long-bodied and paler than adults, with a dark spinal stripe and a light dusting of whitish-grey wax. The dark stripe on the back is sometimes seen in adults.Winged adult females (alatae) are 1.7-3.4 mm long, although sometimes noticeably larger than apterae of the same population. The body colour varies from shades of green to pink. They have pale-green to yellow-brown thoracic lobes, with the antennae and siphunculi being darker than in the apterae. The hind wings have two characteristic oblique veins. The antennae are six-segmented, with ten to eighteen secondary sensoria on the basal third of the third segment. The central stripe on the back is much less distinct in winged forms (Stoetzel and Miller, 1998; Blackman and Eastop, 2000).The main distinguishing characteristics of M. euphorbiae are the length of the reticulated area on the siphunculi, the number of sensoria on the third antennal segment, and the tapering shape and presence of lateral hairs on the cauda (Palmer, 1952).

M. euphorbiae was originally a North American species, but is now virtually cosmopolitan. The distribution map includes records based on specimens of M. euphorbiae from the collection in the Natural History Museum, London, UK (NHM).

M. euphorbiae is native to North America, although it has been long established in Central and South America, Europe, Asia and Africa. It has more recently spread to countries in eastern Asia and Oceania.

In greenhouses, inspection procedures and the use of uninfected planting material can reduce infestation by M. euphorbiae.

Natural dispersal is the main means of spread for M. euphorbiae in field crops. A spring migration takes host-alternating populations from the primary host (Rosa spp.) to a wide range of secondary hosts, including potato, tomato and lettuce. Aphid populations can survive year-round in warm climates and in greenhouses, infesting crops late in the season. Aphids can potentially be dispersed on foliage, stems or fruits (especially with leaves attached) in trade.

The primary host of M. euphorbiae is Rosa spp., on which host-alternating populations breed sexually and overwinter. The aphid is highly polyphagous on secondary hosts, feeding on over 200 species in more than 20 plant families. It favours plants in the Solanaceae, especially potato and tomato (Blackman and Eastop, 2000). It is also common on aubergine, sweet potato, roses, lettuce, maize, sugarbeet and many other cultivated plants.

Keys to distinguish M. euphorbiae from other aphid species found on maize, peach, cotton and citrus in the USA were presented by Stoetzel and Miller (2001; 1998), Stoetzel et al. (1996) and Denmark (1990). M. euphorbiae is often found on the same host plants as Myzus persicae (green peach aphid), although M. euphorbiae is much larger than M. persicae and has a more elongated body shape.

GeneticsM. euphorbiae has a diploid chromosome number of 2n=10 (Blackman and Eastop, 2000). Raboudi et al. (2005) used polymorphic microsatellite loci to study population genetics. There are green and red biotypes of M. euphorbiae.Reproductive biologyM. euphorbiae is heteroecious and holocyclic (host-alternating and sexually reproducing) in North America, where it originates (Smith, 1919; Patch, 1925). The overwintering or primary host plants (on which eggs are laid) are wild and cultivated Rosa spp. (Blackman and Eastop, 2000). Shands et al. (1972) described the ecology of aphid populations on Rosa palustris, the most important overwintering host in Maine; while Sugimoto (1999) described sexual morphs overwintering on Rosa spp. in Washington State.The kinds of offspring produced by M. euphorbiae are influenced by daylength, parent type, genetic factors and temperature (MacGillivray and Anderson, 1964; Lamb and MacKay, 1997). The greatest proportion of apterous (wingless) were produced when daylength was greater than 13 hours and when parents were first 'generation' alatae, while the greatest proportion of alate (winged) viviparous females were produced when daylength was between 11 and 13 hours and when parents were apterous. The greatest proportion of oviparae (sexual females) was produced by second 'generation' alatae, while most males were produced by fourth 'generation' apterae (MacGillivray and Anderson, 1964).In host-alternating populations, eggs are laid that overwinter on the bark of Rosa. Eggs hatch from mid-April, into a generation of apterous females (fundatrices). Reproduction is then parthenogenetic until the production of sexual forms in the autumn. The offspring of the fundatrices feed on the new growth from rose buds. By the second generation, some alatae are produced, while most of the third generation is alatae. These are the spring migrants that locate the summer or secondary host plants, including potato. The spring migration is influenced by the time of egg hatching and the rate of aphid development and, in Maine, occurs anytime from late May to mid-June.In response to shorter daylengths, alatae are produced on the summer hosts (gynoparae) that will locate the winter host (Rosa spp.). The autumn migration is less spaced out than the spring migration; in Maine it occurs from 20 August 20 to 1 September (Shands et al., 1972). The gynoparae produce the sexual females or oviparae on the winter host. Winged males, also produced on the summer host, locate and mate with the oviparae (Shands et al., 1972).Males are attracted to sexual females by a sex pheromone that is released from the waving hind leg of 'calling' virgin females (Goldansaz and McNeil, 2003). The sex pheromone was identified as a mixture of (1R,4aS,7S,7aR)-nepetalactol and (4aS,7S,7aR)-nepetalactol in a ratio that varied with age from 4:1 to 2:1. In laboratory tests, males walked towards synthetic blends of the two components, in the ratios released by females, but did not respond to the individual components alone (Goldansaz et al., 2004).In Europe, and most other areas where M. euphorbiae is an exotic species, the life cycle is mainly anholocyclic with asexual reproductive on secondary hosts; although sexual morphs are sometimes produced in small numbers (Möller, 1971). Meier (1961) described the ecology of the aphid in Germany. In Europe, overwintering as eggs on Rosa spp. is rare, with aphids remaining mobile overwinter on weeds, on potato sprouts in storage or chitting houses, or on lettuce and other crops in greenhouses. In early May or June winged forms are produced that migrate to potatoes or other field crops. A second winged dispersal occurs in July if populations are high, while a smaller migration occurs in the autumn.The distinction between different life cycles in M. euphorbiae is less clear-cut, however, than for most aphid species. A degree of 'life cycle plasticity' and 'genotype plasticity' has been described. M. euphorbiae can remain on its primary host Rosa spp. throughout the year, eliminating the summer secondary host plants altogether (MacGillivray and Anderson, 1964). M. euphorbiae also deviates from the normal pattern seen in host-alternating aphids because apterous (wingless) females on secondary hosts are capable of producing mating females (oviparae) as well as winged females (gynoparae) and males. This enables M. euphorbiae to reproduce sexually on both primary and secondary hosts, although sexual reproduction on secondary hosts is much less common (Lamb and MacKay, 1997).Environmental requirementsThe fecundity of M. euphorbiae on potato under constant temperature regimes was described by Barlow (1962). An average of 221.24 'day-degrees' was required for complete development. The relation between temperature and development was linear between 5°C and 25°C; at 30°C all aphids died before reaching maturity. Survival declined with rising temperature, with fewer young produced at 25°C than at lower temperatures. This temperature response may partly explain the reported reductions in M. euphorbiae infestations during hot weather (Barlow, 1962). Temperature affects photoperiodic response in this aphid, modulating the photoperiodic response in warm or cool autumn conditions (Lamb and MacKay, 1997).MacGillivray and Anderson (1958) reported an average duration of development, from birth to production of first offspring, of 9.7 days for apterae and 10.6 days for alatae, on potato at 21.8°C; the average fecundity was 67.3 offspring per aphid for apterae and 64.1 for alatae. On pepper in Spain, at 10°C and a 14:8 light:dark cycle, the nymphal development period was around 20 days (Vasicek et al., 2001).AssociationsM. euphorbiae is sometimes attended by ants, for example, by Formica altipetens on Artemisia spp. in the USA (Ryti, 1992).

Parasites and hyperparasites of M. euphorbiae in North America were described by Shands et al. (1965) and Sullivan and van den Bosch (1971). Aphidius nigripes is the most common parasitoid attacking M. euphorbiae in eastern North America (Brodeur and McNeil, 1994). Karley et al. (2003) described natural enemies of M. euphorbiae in potato fields in the UK. Takada (2002) described parasitoids attacking M. euphorbiae on crops in greenhouses in Japan.

M. euphorbiae can be a major pest of potatoes, tomatoes and lettuce. It is a pest of both field crops and greenhouse-grown crops. High population levels of M. euphorbiae cause direct feeding damage. Aphids insert their stylets directly into a plant's phloem, and sometimes also the xylem. Large colonies of aphids can extract large amounts of nutrients from a plant. Leaves and stems can be distorted, with leaf roll or necrotic spots on leaves, whole plants can become stunted, and reductions in photosynthetic efficiency can result in significant yield losses. High infestations are particularly damaging during the period from 6 to 8 weeks before harvest. Aphids also secrete large amounts of honeydew, which promotes the development of sooty moulds on foliage and fruit. This cosmetic damage can significantly reduce the value of vegetable and fruit crops.

The effect of direct feeding damage by M. euphorbiae and Myzus persicae on the yield of commercial potato crops was evaluated in a series of field experiments in England and Wales between 1987 and 1992. Insecticides were used to manipulate aphid population densities in small plots. No consistent association was found between yield and aphid infestation level. The average density ranged from 1.5 to 25.7 aphids per compound leaf, and the maximum density ranged from 3.0 to 64.2 aphids per compound leaf (Parker, 2005).

M. euphorbiae is a vector of plant viruses within many crops, although transmission is usually in a non-persistent manner. Blackman and Eastop (2000) described the aphid as a vector of over 40 non-persistent viruses and five persistent viruses. The most important of these include Beet yellow net virus, Pea enation mosaic virus, Bean leaf roll virus, Zucchini yellow mosaic virus and Potato leaf roll virus (e.g., Hanafi et al, 1989; Singh et al., 1997). Chen et al. (1991) listed 67 plant viruses that M. euphorbiae is capable of transmitting. Other viruses transmitted include Beet mild yellowing virus, Beet chlorosis virus and Beet yellows virus in sugarbeet (e.g., Dewar et al., 2005; Kozlowska-Makulska et al., 2009), Sweet potato leaf speckling virus (e.g., Fuentes et al., 1996), Cucumber mosaic virus (e.g., Raccah et al., 1985; Gildow et al., 2008), Lettuce mosaic virus (e.g., Nebreda et al., 2004), Blackeye cowpea mosaic virus (e.g., Puttaraju et al., 2002) and Sugarcane mosaic virus (Yasmin et al., 2011).

The economic impact of M. euphorbiae in potato is mainly due to feeding on the foliage, but is also partly due to the transmission of plant viruses. When high aphid populations occur early in the season, the upper leaves of certain potato varieties roll upward (false leaf roll). This reduces photosynthetic efficiency and results in yield loss. Veen (1985) described leaf roll or top-roll symptoms induced on potato plants after infestation with M. euphorbiae; tuber yields of infested plants were reduced by 44% in comparison with controls. It was suggested that photosynthesis was inhibited by impaired phloem transport and the subsequent accumulation of carbohydrates in the leaves, and not by direct mechanical damage caused by the feeding aphid. Leaf roll due to aphid feeding occurs earlier in the season than the similar leaf roll symptoms caused by aphid-transmitted potato leaf roll virus. M. euphorbiae can spread Potato leaf roll virus within potato crops (MacKinnon, 1969). It also transmits Potato virus Y, in a non-persistent manner. However, M. euphorbiae is relatively unimportant as a vector of potato viruses in comparison to Myzus persicae (Singh and Boiteau, 1986; Blackman and Eastop, 2000).

Elnagar et al. (1996) reported substantial yield loss (tuber weight) in potatoes in Egypt due to M. euphorbiae transmitted Alfalfa mosaic virus and Potato virus Y (257.8 and 229.5 g/plant, respectively, compared to 763.2 g/plant for healthy plants).

M. euphorbiae can have adverse economic impacts on field-grown tomatoes (e.g., Tomescu and Negru, 2003), especially on staked fresh-market tomato production. Reduced profits in staked tomatoes were reported when aphids reached high densities, due to slightly lower yields and, more importantly, due to lower fruit quality caused by the indirect effects of aphids. These indirect effects included the attraction of stink bugs, which feed on both aphids and tomatoes, and the increased incidence of weather-related physiological disorders (e.g. sunscald and weathercheck) due to plant stunting (Walgenbach, 1997). M. euphorbiae is generally found on the terminal parts of tomato plants, where it occurs later in the season than Myzus persicae and other aphid species, causing it to be more damaging. Feeding damage by M. euphorbiae can also cause yield losses in field-grown lettuce (e.g. Steene et al., 2003).

M. euphorbiae can be a significant pest of crops in greenhouse. Populations can survive year-round in greenhouse environments. In lettuce crops, for example, populations of aphids can persist late into the autumn. Economic losses are due to yield loss, occasional virus spread, and especially to the presence of aphids, honeydew and sooty moulds that reduce the marketability of salad crops.

In Canada, M. euphorbiae is an important pest of flax. Peak populations occur during boll development, when the crop is especially sensitive to injury by aphids. Yield loss in flax was reported as 0.021 t/ha per aphid per plant for crops sampled at full bloom, and 0.008 t/ha per aphid per plant for crops sampled at the green boll stage (Wise et al., 1995).

M. euphorbiae is a significant pest of cultivated roses in greenhouses destined for sale as cut flowers, for mainly cosmetic reasons, and of roses grown as ornamentals in parks and gardens.

Chemical Control

M. euphorbiae is controlled on a range of crops by insecticides, including organophosphates, carbamates, pirimicarb and imidacloprid (a more recently introduced nicotinyl insecticide). On lettuce, for instance, it is mainly controlled by routine insecticide applications with organophosphates, carbamates or pyrethroids (Steene et al., 2003). Foster et al. (2002) reported resistance to organophosphate, carbamate, and pyrethroid insecticides in clones of M. euphorbiae collected in the UK. Acetylcholinesterase (AChE) is a primary target of many insecticides, including organophosphates and carbamates, and resistance to these insecticides is associated with the reduced sensitivity of AChE to inhibition. Resistance of M. euphorbiae to the carbamate pirimicarb was found to be associated with a one-point mutation in the gene encoding AChE. Diagnostic tests using PCR-RFLP based methods for detecting the presence of this mutation in individuals of M. euphorbiae in field populations are described (Raboudi et al., 2012).

Mineral oils have been used to control aphids and reduce the spread of non-persistent viruses. A laboratory study showed that the mineral oil Finavestan EMA can induce either probiotic effects or toxic effects in M. euphorbiae, depending on the mode of application and the concentration tested. These significance of these results for field use of mineral oils is discussed (Martoub et al., 2011).

In laboratory studies, essential oil of mentrasto (Ageratum conyzoides) has shown insecticidal activity against M. euphorbiae (Soares et al., 2011), while rosemary oil and ginger oil have shown a repellent effect (Hori, 1999). The repellency of various essential oils to the aphids Aphis gossypii, Myzus persicae and M. euphorbiae in pepper crops (Capsicum annuum) was evaluated in greenhouses. Treatments with garlic essential oil (Allium sativum) + soybean oil and Eucalyptus essential oil (E. globulus) + soybean oil were the most effective in repelling the aphids (Castresan et al., 2013).

Biological Control

Naturally occurring parasites and predators of M. euphorbiae are common, especially in the USA, and these can provide control. Parasite populations can be monitored by assessing the proportion of aphid mummies relative to unparasitized aphids. Spraying can disrupt natural enemies and should be avoided if a high proportion of mummies is present or if aphid populations are below damaging thresholds and predators appear to be asserting control. Major predators include coccinellids (ladybirds) larvae and adults, and syrphid and lacewing larvae.

In greenhouses, the release of parasites and Coccinellidae (e.g. Hippodamia and Harmonia species) can help control M. euphorbiae populations (e.g., Lieten, 1998). Entomopathogenic fungi, especially Verticillium lecanii, have also shown promise for the biological control of M. euphorbiae in greenhouses (Fournier and Brodeur, 1999). Pandora neoaphidis was the predominant entomopathogenic fungus affecting M. euphorbiae on lettuce in a study in the central Iberian Peninsula. It is suggested that conservation biological control is the best strategy for managing aphid pests in horticultural systems because of problems related to the isolation and artificial production of entomopathogenic fungi (Díaz et al., 2008).

Several parasitoids are used or have shown potential as biological control agents of M. euphorbiae. Aphelinus abdominalis, Aphidius ervi and Praon volucre are currently marketed against M. euphorbiae worldwide (Boivin et al., 2012), but the combined use of A. ervi and P. volucre is not recommended because of competition at the larval stage (Sidney et al., 2010). In commercial greenhouses of tomatoes in Albania, populations of aphids, including M. euphorbiae, were considerably reduced by introductions of the braconid Aphidius colemani and the cecidomyiid Aphidoletes aphidimyza (Çota Isufi, 2009). A. ervi is used commercially in the biological control of cereal and vegetable aphid pests, including M. euphorbiae (Ismaeil et al., 2013). Initial trials using a mixture of six different parasitoid species gave good control against M. euphorbiae on protected strawberry crops in the UK, without the need for pesticide treatment (Sampson et al., 2011).

A prototype of a computer-based decision aid (APHCON) has been developed to optimize the biological control of four aphid pests (Myzus persicae, Aulacorthum solani, M. euphorbiae and Aphis gossypii) occurring on greenhouse crops using eight commercially available natural enemies (Aphidius colemani, Aphidius ervi, Aphidius matricariae, Aphelinus abdominalis, Chrysoperla carnea, Episyrphus balteatus, Aphidoletes aphidimyza and Adalia bipunctata) (Hommes and Gebelein, 2005).

Host-Plant Resistance

Host-plant resistant to M. euphorbiae has been recorded in tomatoes (Musetti and Neal, 1997; Kohler and St Clair, 2005). A considerable difference in aphid feeding on different tomato varieties has been recorded, which has a genetic basis. A gene (Mi-1) in tomato confers resistance to nematodes and deters aphid feeding (Vos et al., 1998; Cooper et al., 2004; Goggin et al., 2004; Godzina et al., 2010). Its activity appears to increase in response to aphid feeding, via jasmonic acid and salicylic acid plant defence signalling pathways (Cooper and Goggin, 2005). It has been suggested that this resistance may no longer be as effective against pink forms of M. euphorbiae as it once was (UC IPM Online, 2005).

Various strategies and/or genes have been investigated for engineering the resistance of plants to aphids, but so far no aphid-resistant transgenic plants are commercially available. Before transgenic plants can be commercialized, their effects on both aphid infestations and the behaviour of their predators and parasitoids need to be fully evaluated (Yu et al., 2014). Local selection can also offer the possibility of developing innovative genetic strategies to increase resistance of tomato against aphids. Two tomato accessions from southern Italy (AN5 and AN7) lacking the tomato Mi gene but exhibiting high yield and quality traits have shown a significant reduction of M. euphorbiae fitness compared with a susceptible commercial variety and released larger amounts of specific volatile organic compounds that are attractive to the braconid Aphidius ervi (Digilio et al., 2010).

Reinink et al. (1995) described partial resistance in certain lettuce cultivars to M. euphorbiae. Lettuce accessions CGN16272 and CGN13361 have shown partial resistance and accession CGN13355 near complete resistance to M. euphorbiae (Cid et al., 2012).

Resistance of potato to the aphids M. euphorbiae and Myzus persicae can be improved by introgressing resistant traits from wild Solanum species into the potato germplasm. Accessions PI243340 and PI365324 of Solanum chomatophilum are resistant to M. euphorbiae (Pompon et al., 2010). In a laboratory study, the development time of M. euphorbiae on potato plants cv. Desirée GNA, which carries transgene-encoding agglutinin of snowdrop lectin (Galanthus nivalis), was more than 50% longer than that on the control (cv. Standard Desirée). No harmful effect of the transgenic plants on the non-target beneficial Aphidoletes aphidimyza were recorded (Hussein, 2005).

The use of transgenic plants expressing insecticidal Cry proteins derived from Bacillus thuringiensis (Bt) for toxicity against various lepidoteran and coleopteran pests is increasing worldwide (Yu et al., 2014). Field, greenhouse and laboratory studies have been carried out to assess the effect of these genetically modified plants on nontarget organisms including biological control agents (Romeis et al., 2006). In a laboratory study, the transgene Cry3AaBt-toxin in potato cv. Superior New Leaf had no effect on the developmental rate and fecundity of M. euphorbiae (Hussein, 2005). Another laboratory study showed that individuals of M. euphorbiae were smaller and fecundity was lower on genetically modified Bt potato plants expressing the CryIIIA toxin against Colorado potato beetle (Leptinotarsa decemlineata) than on non-transformed plants, although development time was the same on both (Ashouri, 2007). No adverse effects of transgenic-Bt tomato plants expressing the toxin Cry3Bb against Coleoptera were found on the biology of M. euphorbiae or its natural enemies, the mirid Macrolophus caliginosus and the braconid Aphidius ervi (Digilio et al., 2012).

Integrated Crop Management

The monitoring of M. euphorbiae populations, especially around 6 to 8 weeks before harvest, forms the basis for insecticide treatment decisions. Treatments may be necessary if natural enemy activity is low and aphid populations are increasing. Parker (1998) described a forecasting scheme to predict peak M. euphorbiae populations on potatoes. Monitoring can be carried out by direct aphid counts or the use of traps, e.g. sticky traps, vertical net traps, yellow water pan traps and green tile traps.

Integrated control measures for aphids, including M. euphorbiae, on protected crops include cultural control methods (weed removal, insect net around the greenhouse and in ventilation openings), use of insecticidal soap treatments during late spring, and the introduction of commercially available parasitoids (Çota Isufi, 2009). Fereres et al. (2003) showed that the use of ultraviolet-absorbing plastic films could reduce the spread of viruses by M. euphorbiae in lettuce, presumably by interfering with the behaviour of host-finding winged forms. Studies in central Spain have shown that covering tunnel-type greenhouses with ultraviolet-absorbing nets in combination with releases of Aphidius ervi could be an effective method of controlling M. euphorbiae on protected lettuce crops as part of an IPM programme (Sal et al., 2009; Legarrea et al., 2014). A field study in the UK showed that the presence of wildflower strips can lead to increased natural regulation of pest aphids during June and July plantings of outdoor lettuce crops (Skirvin et al., 2011).

Wittenborn and Olkowski (2000) assessed methods of monitoring M. euphorbiae in tomato in California, USA; a chemical treatment threshold was determined to be 37% aphid-occupied leaflets or two aphids/leaflet. A threshold for vine-ripe harvested tomatoes of 50% infested leaves when using broad-spectrum insecticides, and 25% when using narrow-spectrum aphidicides, was recommended by Walgenbach (1997). A threshold scheme for M. euphorbiae on outdoor lettuce in France and Switzerland was described by Fischer and Terrettaz (1999): from mid-May to early July a threshold of 10% of plants occupied initiated two insecticide treatments, while after early July a 40% occupation threshold prompted a single aphicide spraying. An economic threshold for M. euphorbiae in flax was established as three aphids/plant at full bloom, and eight aphids/plant at the green boll stage, based on crop prices and control costs from 1990 to 1992 (Wise et al., 1995).

The use of tolerant varieties, biological control, and sprays of thyme oil, pyrethrin and insecticidal soap are acceptable for use against M. euphorbiae on organically certified crops in the USA (UC IPM Online, 2005).