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Identification & Distribution

Adult apterae of Aphis spiraecola are bright greenish yellow to apple green. The abdominal dorsum is pale and usually entirely membranous. The fused last two rostral segments are less than 120 μm in length (cf. Aphis pomi  which has the fused last two segments more than 130 μm in length). Marginal tubercles are restricted to abdominal tergites 1 & 7, with none present on abdominal tergites 2-4 (cf. Aphis pomi which has marginal tubercles on tergites 2-4 ). The femoral hairs are long and fine, the longest of them being longer than the diameter of the femur at its base. The siphunculi and cauda are black. The cauda usually has less than 12 hairs (7-15) (cf. Aphis pomi on which the cauda usually has more than 13 hairs (10-19)). The body length of an adult Aphis spiraecola aptera is 1.2-2.2 mm.

Alatae (see second picture above) have a dark brown head and thorax, and a yellowish-green abdomen with dusky marginal sclerites.

The micrographs below show an adult aptera in dorsal & lateral view in alcohol.

Aphis spiraecola is easy to confuse with the apple aphid Aphis pomi, not least because both aphid species tend to colonize the same plant species. Discriminating characteristics are given above - probably the clearest of which is whether marginal tubercles are present (Aphis pomi) or absent (Aphis spiraecola) on abdominal tergites 2-4. Both species tend to have them on abdominal tergites 1 (see first picture above) and (sometimes) on tergite 7. Footit et al. (2009)  have used molecular characterization to assess the reliability of morphological characters in distinguishing the two species. They concluded that length of the distal rostral segment and the number of marginal tubercles were both robust indicators of species membership.

The secondary hosts of Aphis spiraecola are in over 20 plant families, especially shrubs in the Caprifoliaceae, Asteraceae, Rosaceae, Rubiaceae, and Rutaceae. In North America, Brazil and Japan the species also produce sexual forms on primary host - meadowsweets (Spiraea species), or sometimes citrus or apple. Aphis spiraecola is thought to have had its origin in the Far East. In most of the rest of the world it reproduces parthenogenetically on its secondary hosts all year round. Aphis spiraecola is a major pest of citrus fuits, mountain yarrow, apple (North America) and pears (China). It has a worldwide distribution in temperate and tropical regions.

Our observations are the third field-record of Aphis spiraecola in UK to date.
First recordby: Martin, J.H. et al.June 1995in: London
Secondby: Baker, E.A.May 2007in: Cardiff Bay, Wales
Thirdby: Influential PointsSept. 2018in: Clifton, Bedfordshire

 

Biology & Ecology

Life cycle

Where Aphis spiraecola is holocyclic and produces sexual morphs the usual primary hosts are spirea (Spiraea) or citrus fruits (Citrus). In North America, and Brazil, spirea is the primary host (de Menezes, 1970 ). In Japan, both spirea and citrus fruits are recorded primary hosts (Komazaki et al., 1979 ). Hodjat and Eastop (1983)  also recorded sexual forms on apple (Malus) in Iran. However, over most of its geographical range, Aphis spiraecola is anholocyclic and reproduces entirely parthenogenetically. As is the norm, Aphis spiraecola undergoes four larval instars (see picture below of immatures, mostly fourth instar).

In Japan, aphids overwintering on spirea and citrus fruits represent two distinct biotypes of Aphis spiraecolaa (Komazaki, 1998 ). Timing of the overwintered egg hatch differed between populations on spirea and citrus fruits; a difference which was apparently genetically determined. Spring migrants of the citrus biotype increased rapidly on citrus and pear but only slowly on apple and spirea, while the spirea biotype increased rapidly on spirea and pear, but slowly on apple and not at all on citrus (Komazaki, 1991 ). The alate migrants from citrus play a major part in the spring infestation of citrus groves in Japan and other citrus growing regions.

Population dynamics

Tsai & Wang (2001)  looked at the development, survivorship, longevity, reproduction, and life table  parameters of the spirea aphid, at 25 °C, on seven commonly grown plants. Spirea aphid failed to survive on orange jessamine (Murraya paniculata). Jackknife estimates  of the intrinsic rate of natural increase varied from 0.308 on the chicken gizzard plant (Polyscias crispata) to 0.177 on pineapple orange (Citrus sinensis). It was suggested that the ability of spirea aphid to feed and develop on a wide range of host plants increases its chance to infest citrus and thereby spreading the citrus tristeza virus.

In Henan Province, China, holocyclic populations occur on apple, with overwintering as eggs in bud axils. Around 15-18 generations a year occur, with two population peaks during the year. The first population peak in the spring can result in severe damage to apple trees. The second in autumn can affect the formation of buds and flowers, although overall damage to crop yields is less severe (Zhang et al., 1997 ).

Heinze (1977)  looked at populations of Aphis spiraecola in the Mediterranean region. The first small colonies on new citrus growth occur by early February, and up to 14 generations may be produced in one year. An increased proportion of winged forms are produced in response to both over-crowding and a deteriorating food supply. The aphid cannot feed on citrus leaves that become hardened after the first growth 'flush'. When the production of young leaves stops, alates began to comprise nearly all of the adult population. These alates migrate in search of fresh young hosts. In the autumn, fruit formation enriches the sap in favour of the aphid and populations start to build up again. In winter, in temperate areas, few adults survive. However, in the tropics, where new shoot production is year-round, and population levels can remain relatively high.

Dubey & Singh (2011)  looked at the population dynamics of Aphis spiraecola on the medicinal plant Cosmos bipinnatus in Eastern Uttar Pradesh, India. The green citrus aphid appeared during the first week of November on Cosmos bipinnatus and attained a peak during the third week of December. The population increased during the first half of the November in the field with favourable temperature (around 25°C) and humidity (above 40% RH) and little predation and parasitism. The decline after the peak was attributed to lower humidity, higher levels of predation and parasitism and the crop's maturity. It was thought that the population could be easily be regulated by enhancing the activities of predators, particularly ladybird beetles.

Aphis spiraecola often occurs in mixed species colonies - the picture below shows Aphis spiraecola (green) along with Aphis fabae  (black) on hibiscus.

Mostefaouia et al. (2014)  found that both Aphis spiraecola and Aphis gossypii  cause damage to clementine tree orchards. Aphid abundance and nutritional factors were monitored weekly. The two aphid species showed similar temporal variations, but Aphis spiraecola was consistently more abundant. Amino acids had a positive effect on both aphid species abundance, but condensed tannins did not seem to affect aphid populations. Interestingly, the leaf carbohydrate content was positively correlated with the abundance of Aphis spiraecola, but not with that of Aphis gossypii. Moreover, Aphis gossypii's abundance was significantly reduced by high proline concentrations. The authors suggested that the higher abundance of Aphis spiraecola could be explained by a better tolerance to high proline contents and a better conversion of foliar energy metabolites.

Ant attendance

Although the colony we found did not appear to be ant attended, they are usually attended. Dartigues (1991) ) found that the ant species Tapinoma simrothi had a positive influence on the growth and survival of Aphis spiraecola on citrus in Algeria. Shindo (1972)  recorded five species of ant tending Aphis spiraecola on citrus in Japan, with Pristomyrmex pungens being the most common species. It was assumed that this ant interfered with the activity of aphid predators. The ant Crematogaster depressa tended the aphid on cocoa in Cameroon (Dejean et al., 1991 ).

British status

Aphis spiraecola is included on Baker's 2015 Checklist of aphids in Britain.  Information on its status in Britain is given by FERA (2014).  In 2014 Aphis spiraecola was considered absent from the UK, but there is uncertainty regarding its current status. 'Temporary colonies' of Aphis spiraecola had been recorded in 1995 on Cotoneaster in London (Martin, 1996 ) and in 2007 on Viburnum tinus in Cardiff Bay, Wales (Baker, 2009 ). Difficulties over its identification mean that Aphis spiraecola may be present in Britain, but unrecognised and unreported. The Royal Horticultural Society's advisory service has not recorded Aphis spiraecola, but does not normally identify aphids to species. Similarly, not all Aphis caught by the Rothamsted Insect Survey's suction trap network are identified to species. Aphis spiraecola has been found 13 times by UK plant health inspectors since 1999, on a range of woody and herbaceous ornamental plants from within and outside the EU.

We found Aphis spiraecola in Britain, in a garden in Bedfordshire, in September 2018. It was present on the flowers and flower buds of common hibiscus (Hibiscus syriacus) in mixed-species colonies with another polyphagous pest species, Aphis fabae,  (see picture below).

Aphis spiraecola is often found on hibiscus, but Aphis pomi (the species with this species is often confused with) has never been recorded on that host. Examination of adult apterous specimens under the microscope revealed a complete absence of marginal tubercles on abdominal segments 2-4, thus confirming the species identity as Aphis spiraecola.

 

Other species on the same host

Primary hosts
Secondary hosts

 

Damage and control

Damage

When Aphis spiraecola feed on leaves, the leaves are rolled tightly, sometimes almost spirally, inwards from the tip. On citrus, aphid colonies cause curling, crinkling and distortion of young leaves. On apple, aphids cause abnormal growth of terminal shoots, and by reducing photosynthesis, reduce the greenness and quality of young apple leaves. The earlier the attack on crop hosts the more shoots are stunted. On distorted shoot tips several leaves can be rolled together. Leaves with heavy feeding damage are reduced in size and can die prematurely, and flowers and fruits are also damaged. Damage is of particular economic significance in young citrus orchards and on soft-skinned citrus varieties (Heinze (1977) ).

Aphis spiraecola also transmits a range of viruses, including citrus tristeza virus (CTV), citrus psorosis virus, cucumber mosaic virus, papaya ringspot virus, plum pox virus, potato virus Y, viburnum strain of alfalfa mosaic virus, watermelon mosaic virus and zucchini yellow mosaic virus. Symptoms of citrus tristeza on citrus include leaf cupping, vein-clearing and stem-pitting. Aphis spiraecola is also an important vector of plum pox virus in the USA and Spain.

Chemical control

CABI (1997)  provide an excellent review of the biology and control of Aphis spiraecola, from which we have drawn much of what follows. Control efforts have mainly been focused on this aphid in citrus groves and apple orchards. Cho et al. (1997)  tested a range of insecticides in citrus groves, Park et al. (1993)  compared treatments in apple orchards, and Segeren (1983)  described the efficacy of different insecticide treatments on cucurbits in Suriname. Heinze (1977)  listed ethion, parathion-ethyl, dimethoate, fenitrothion and propoxur as suitable insecticides. Pirimicarb has also been recommended, particularly in the context of integrated control. Stem bandages soaked with insecticide have been used in citrus orchards. Drenching of nursery plants with dimefox has also been recommended.

In recent years imidocloprid has become the favoured insecticide for Aphis spiraecola control in orchards. Lowery et al. (2005)  compared the susceptibility of Aphis pomi and Aphis spiraecola to imidacloprid in apple orchards; while Paulson et al. (2005)  showed that the effects of imidacloprid were synergized by prohexadione-calcium, a plant growth regulator used on apple and pear trees. In a six-year study of brown citrus and spirea aphid populations in a citrus grove in Florida, imidacloprid treatments controlled the aphids, although in some years at least two annual treatments per year were required to control Aphis spiraecola (Powell et al., 2006 ).

The extensive use of insecticides has resulted in Aphis spiraecola becoming resistant to a number of them, including pirimicarb (Benfatto et al., 1970;   Hohn et al., 2003 ). Song et al. (1995)  investigated the mechanism of tolerance to organophosphorus insecticides after resistance to that group of insecticides was found in Korea.

Biological control

The braconid, Lysiphlebus testaceipes was imported from Cuba to Mediterranean France for the biological control of spirea aphid and other citrus aphids in 1973-74, and has since spread to mainland Italy, Sicily and other areas without further human intervention (Stáry et al., 1988 ). Biological control of spirea aphid by Lysiphlebus testaceipes on citrus in Italy is described by Viggiani (1990) . However, this braconid parasitoid cannot complete its development in Aphis spiraecola. Parasitized aphids die or stop producing offspring, but no further parasites are produced from the mummies. This may be true for a number of generalist parasites observed ovipositing in this aphid, because of its relatively small size. Another braconid, Trioxys angelicae (= Binodoxys angelicae), can complete its development in Aphis spiraecola however, an important factor in biological control programmes.

The aphelinid parasitoid Aphelinus spiraecolae, which has a preference for spirea aphid in its native China, was introduced from China into the USA and has potential as a biological control agent in Citrus in Florida, USA (Tang and Yokomi, 1996 ). Stáry and Zeleny (1983)   suggested that Lipolexis scutellaris would be a good export from Vietnam for control of spirea aphid in other citrus growing regions of the world.

Raupp et al. (1994)   described releases of two coccinellids, the convergent lady beetle (Hippodamia convergens) and seven spotted lady beetle (Coccinella septempunctata), against pests of ornamental landscape plants; the predators reduced populations of spirea aphid on firethorn (Pyracantha lalandei). Katsoyannos et al. (1997)  described how the coccinellid Harmonia axyridis (see picture below) was imported to Greece from France for citrus aphid control.

Kuznetsov (1988)  reported that coccinellids (Harmonia species) from the far East of the former USSR were released in citrus orchards in the Transcaucasus, where they overwintered successfully and controlled large populations of spirea aphid the following year. Qin (1985)  described the mass rearing of insects, including the anthocorid Orius minutus, for release against Aphis spiraecola and other pests in apple orchards in China.

In a study of integrated biological control of pests on Viburnum tinus plants in open tunnels in France, Aphis spiraecola was recorded as the major pest and was controlled by the release of Aphidius sppecies and Aphidoletes aphidimyza, augmented by the native auxiliary fauna, notably syrphids (Ferre, 2008 ).

Integrated control

Harmonia axyridis is the major natural enemy controlling aphid numbers in integrated pest management programmes in citrus in the Korean Republic, and Cho et al. (1997)  took toxicity of insecticides to this coccinellid into account when recommending which insecticides to use against spirea aphid. In apple orchards in the Korean Republic, Lee et al. (1994)  likewise recommended insecticides which preserved the main natural enemies for use against the aphid. Uygun et al. (1987)   described integrated control in citrus in Turkey, where Aphis spiraecola is kept at low levels by predatory Coleoptera and Neuroptera.

It has been suggested that flowering companion plants and plants producing extrafloral nectar could enhance biological control in apple orchards. Spellman et al (2006)  looked at the impact of floral and extrafloral resources on predation of spirea aphid on apple by adult Harmonia axyridis coccinellids under greenhouse conditions. Predation of spirea aphids was not affected either positively or negatively by the presence of flowering buckwheat (Fagopyrum esculentum). However, there was a significant reduction in predation of spirea aphids on an apple shoot in the presence of a peach shoot with extrafloral nectar glands. The authors concluded that alternative food resources could interfere rather than enhance rates of biological control, so should be carefully evaluated before incorporating in an orchard design.

The study above was done under greenhouse conditions, so Brown et al. (2008)  investigated the effect of providing floral and extrafloral resources under field conditions. Two pairs of apple orchards, each having one interplanted with 50% trees bearing extrafloral nectar and one a monoculture, were studied for aphid and predator populations from 1999 to 2005. There were no differences in spirea aphid or predator populations between interplanted and monoculture orchards. However, Harmonia axyridis adults arrived earlier in the interplanted than in the monoculture orchards. In another apple orchard, the effect of peach extrafloral nectar on sentinel spirea aphid colonies surrounding a cluster of potted peach trees, or a cluster of apple trees as a control, was tested. Only the closest spirea colonies to the potted peach trees, trees within 3 meters, showed an increase in biological control. Although there was some indication of enhancement of predation by adult Harmonia axyridis on spirea aphids, adding alternative food resources in the form of peach trees bearing extrafloral nectar resulted in no detectable increase in biological control.

Brown et al. (2011)  investigated how quickly adult Harmonia axyridis need to arrive at newly established Aphis spiraecola colonies on apple to provide population control. A total of 100 newly established spirea aphid colonies were caged in an experimental apple orchard in West Virginia, USA. A single adult Harmonia axyridis was added to each of ten, caged, colonies at different interevals (0-20 days) after caging. An additional ten caged colonies were opened for exposure to natural levels of predation at each of the treatment intervals as a control. The single Harmonia axyridis eliminated the aphid colonies significantly more quickly than natural predation for up to ten days after colony establishment. The probability of an aphid colony producing alates was significantly lower in the presence of a single Harmonia axyridis adult than when exposed to natural predation for the first ten days. It was concluded that adult Harmonia axyridis beetles are capable of completely controlling individual spirea aphid colonies on apple only if they are abundant enough to find colonies within one week of colony establishment.

Gomez-Marco et al. (2015)  investigated whether hyperparasitoids can disrupt biological control of spirea aphid on clementines. Binodoxys angelicae (see picture below) is its dominant primary parasitoid, but it is attacked by a complex of hyperparasitoids. At least six hymenopteran hyperparasitoid species were confirmed to hyperparasitize Binodoxys angelicae. The most abundant hyperparasitoids were the chalcid Syrphophagus aphidivorus and the cynipid Alloxysta sp. Both were abundant from the beginning of the season, and hyperparasitism rates remained high throughout the season in the two study years. Hyperparasitoids also increased the secondary sex ratio of Binodoxys angelicae. It was concluded that hyperparasitism probably explains the low impact of Binodoxys angelicae on Aphis spiraecola populations.

Image of Binodoxys angelicae copyright CBG Photography Group under a Creative Commons - Attribution Non-Commercial Share-Alike License. 

Gomez-Marco et al. (2016)  investigated why the complex of predators that prey on spirea aphid colonies do not result in satisfactory control of the aphids on clementines. In a three year study, predators attacked one-third of the colonies. This did not significantly differ among orchards for the years studied. The maximum number of aphids and longevity of spirea aphid colonies were not related to the ratio of colonies attacked by predators, but were negatively correlated with the time of their first attack. More importantly, the percentage of shoots occupied by spirea aphid remained below or close to the intervention threshold when colonies were attacked prior to about 200 degree days from the beginning of the aphid colonization. These results suggested that (1) the presence of predators at the beginning of the season should be considered to develop new intervention thresholds and (2) biological control programs should promote the early presence of predators in clementine orchards.

Acknowledgements

We especially thank Alan Outen Bedfordshire Invertebrate Group  for all his help in assisting us to obtain photographs of Aphis spiraecola.

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 

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