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Identification & Distribution:

Acyrthosiphon pisum apterae are pale green or pink with red eyes. The antennae of Acyrthosiphon pisum are 1.0-1.6 times as long as the body. The antennal segments, tibiae and siphunculi have dark apices (see below right - this distinguishes pisum from related Acyrthosiphon species which do not have the antennal joints darkened).

The siphunculi are tapering and very thin with the diameter of a siphunculus in the middle less than the diameter of the hind tibia. The siphunculi are 1.2-1.9 times the length of the cauda. The cauda is long and tapered. The body length of Acyrthosiphon pisum apterae ranges from 2.2 to 5.0 mm long.

The alate viviparous female has the head and thorax only slightly darker than the abdomen which is pale with small marginal sclerites.

The clarified slide mounts below are of adult viviparous female Acyrthosiphon pisum : wingless, and winged.

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

The pea aphid can be found feeding on about 20 genera in the family Fabaceae but especially on Medicago, Melilotus, Trifolium, Dorycnium and Lotus. Acyrthosiphon pisum is a major pest of peas and alfalfa, partly because of direct feeding damage and partly because of virus transmission. Adults readily fall to the ground if the plant is disturbed. The pea aphid is found worldwide in temperate climates.

 

Biology & Ecology:

Pea aphid genome

The pea aphid is regarded as a model species for studying a range of biological phenomena including polymorphisms, insect -bacterial symbioses, the genetics of adaptation and plant virus transmission. (Brisson & Stern, 2006 ). Partly for this reason it was selected for genome sequencing. Results from The International Aphid Genomics Consortium (2010)  have shown an expanded total gene set with remarkable levels of gene duplication, as well as aphid lineage-specific gene losses. Gene family expansions relative to other published genomes include genes involved in chromatin modification and sugar transport. The inventory of metabolic genes in the pea aphid genome suggests that there is extensive metabolite exchange between the aphid and the symbiont Buchnera, including sharing of amino acid biosynthesis. It is anticipated that the genome sequencing will be of great help in clarifying the situation with regards to two topics below - biotypes and the source of the carotenoid pigment in the red morph of the pea aphid.  

Biotypes

The pea aphid Acyrthosiphon pisum includes a number of different host races termed biotypes. These are sympatric populations in partial reproductive isolation that are specialized to different host plants. Peccoud et al. (2009)  investigated host specialization and gene flow among populations of the pea aphid complex. Genetic markers and tests of host plant specificity indicated the existence of at least 11 well distinguished host specialized sympatric populations in Western Europe. Three of these, biotype A on broom (Cytisus scoparius), biotype B on restharrows (Ononis repens and Ononis spinosa) and biotype I on meadow vetchling (Lathyrus pratensis) are nearing complete speciation because no hybrid could be detected with any other sympatric biotype. The other 8 constitute host specialized races and likely belong to the same species.

The two pictures below show aphids of biotype A on Cytisus scoparius. On broom we have always found Acyrthosiphon pisum predominantly on the developing pods, although they are presumably also found on other parts of the plant.

 

We have also found large numbers of pea aphids on sweet peas (Lathyrus odoratus) (see pictures below). We suspect this is identical to biotype I, which lives on Lathyrus pratensis.

 

It seems likely that the two biotypes (A & I) pictured above will soon be recognised as separate species.

 

Colour polymorphism

Until recently it was assumed that all the carotenoid pigments in aphids were either obtained from plants or from intracellular symbionts. But then Moran & Jarvik (2010) unexpectedly found that the pea aphid genome itself encodes multiple enzymes for carotenoid biosynthesis. Phylogenetic analyses showed that these aphid genes are derived from fungal genes, which have been integrated into the aphid genome and duplicated. (see also Not exactly rocket science ).

The polymorphism appears to be maintained by balanced selection from two predatory species - the predator Coccinella septempunctata and the parasitoid Aphidius ervi. Losey et al. (1997)  found that when parasitism rates were high relative to predation rates, the proportion of red morphs increased relative to green morphs. The converse was true when predation rates were high relative to parasitism rates. Detailed laboratory and field studies confirmed that green morphs suffer higher rates of parasitism than red morphs, whereas red morphs are more likely to be preyed on by predators than green morphs are. Quite why there are these differences is less clear. Further evidence that predation drives the stable coexistence ratios between red and green pea aphid morphs is given by Balog & Schmitz (2013)  and Farhoudi et al. (2014). 

Caillud & Losey (2009)  explored the genetic basis of colour polymorphism in the pea aphid. The polymorphism proved to be determined by a single biallelic locus (named colorama) with alleles P and p being dominant to green. The putative genotypes are Pp or PP for pink morphs and pp for green morphs. Cytoplasmic effects and or maternally inherited symbionts appear to play no role in the inheritance of colour polymorphism in pea aphids.

For a discussion on aposematic  and cryptic  colour in aphids, see our blog.

Natural enemies

Numerous studies have looked at the diverse natural enemy complex which attacks Acyrthosiphon pisum. In the USA several Aphidius parasitoid have been found attacking Acyrthosiphon pisum on alfalfa. Several of these have been introduced in recent years to aid in biological control (Gonzalez et al., 1995 ). The native Aphidius pulcher (= A. pisivorus) was displace by A. smithi, introduced from India. van den Bosch et al. (1967)  described the density dependent parasitism of the pea aphid by Aphidius smithi. Then Aphidius smithi was itself displaced by Aphidius ervi introduced from France.

The pictures below show an aphid in the process of being mummified, and a completely mummified aphid.

 

The emergent parasitoids are shown below. They are as yet unidentified but are most likely Aphidius ervi.

 

There has been increasing interest in the impact of what is called intraguild predation on the efficacy of biological control agents. This is where one predator eats another predator. It is not uncommon, for example, for predatory coccinellid larvae to eat other coccinellid larvae, or even younger larvae of their own species. Snyder and Ives (2001)   found that predatory carabid beetles diminished pea aphid biological control by feeding on parasitoid pupae. However, they did not determine the impact of the rest of the predator guild on the interaction.

Hence Snyder and Ives (2003)   assessed whether predation by other predators in the community might compensate for the negative effects of carabid predation. Parasitoids were able to suppress aphid densities, but the effect occurred with a time delay so that aphids still reached high densities before the decline started. The generalist predator guild had an immediate effect on aphid population dynamics, but only reduced the rate of aphid increase. Thus, aphids still reached high densities when generalists were the only abundant natural enemy. Because specialists and generalists contributed additively to aphid biological control, biological control was the most effective when both types of natural enemy were present.

A recent study looked at seasonal, spatial and diel partitioning of Acyrthosiphon pisum predators in alfalfa fields (Ximenez-Embuna et al., 2014).   Coccinellids were the most abundant predators, followed by syrphid larvae. Coccinellids were also responsible for high levels of predation throughout the year whilst syrphids were only found in spring and summer. The two main predator groups also showed distinct diel patterns, with coccinellids observed only during day and syrphids only during night. The picture below shows a predatory syrphid larvae possibly with its 'eye' on a nice young nymph for breakfast...

Fungal parasites (Entomophthora species) are also important natural enemies of the pea aphid. Wilding (1975)   found three species of Entomophthora affecting Acyrthosiphon pisum on beans at Rothamsted, UK. E. thaxteriana, the commonest species occurred each year. Entomophthora aphidis and Entomophthora planchoniana were more sporadic in occurrence.

The image above shows the brownish, unevenly-swollen cadaver of an Entomophthora-infected Acyrthosiphon pisum: note the hyphae anchoring its underside to the leaf.

Entomophthora may also fall victim to intraguild predation. Roy et al (2008)   found that whilst the native ladybird Coccinella septempunctata largely avoided fungal-infected cadavers of Acyrthosiphon pisum, the invasive ladybird Harmonia axyridis consumed them nearly as readily as uninfected aphids.

The aphid alarm pheromone (E)-β-farnesene (EBF) is one of the best examples of defence communication in the insect world. This alarm pheromone is released when aphids are attacked by predators, and induces behavioural reactions such as walking or dropping off the host plant. Kunert et al. (2005)  showed that the exposure to alarm pheromone also induced aphids to give birth to winged dispersal morphs that leave their host plants. They suggested that the pheromone leads to a "pseudo crowding" effect whereby alarm pheromone perception causes increased walking behaviour in aphids resulting in an increase in the number of physical contacts between individuals, similar to what happens when aphids are crowded. Previous reports that parasitoid activity induces production of alates by Acyrthosiphon pisum (Sloggett & Weisser, 2002  ) may operate by the same mechanism.

 

Damage & Control:

Acyrthosiphon pisum is considered one of the 14 aphid species of most agricultural importance (Blackman & Eastop, 2007).  It does not form dense colonies, so direct feeding damage is limited. However, Acyrthosiphon pisum is a vector of more than 30 virus diseases of Fabaceae which can cause serious crop losses.

Small Acyrthosiphon pisum infestations can be treated by spraying with a strong jet of water. For more serious infestations insecticidal soaps or oils, such as neem or canola oil, are usually the best method of control. For commercial legumes, such as alfalfa, the emphasis is usually on habitat management to encourage natural enemies (especally Aphidius ervi and Entomophthora). Classical biological control, by release of natural enemies, has been used in the USA.

Acknowledgements

Our particular thanks 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

  •  Balog, A. & Schmitz, O.J. (2013). Predation drives stable coexistence ratios between red and green pea aphid morphs. Journal of Evolutionary Biology 26(3), 545-552. Abstract 

  • Blackman, R.L. & Eastop, V.F. (2007). Taxonomic issues. In: Van Emden, H.F. & Harrington, R. (Ed). Aphids as crop pests. Cabi Publishing.Full text 

  •  Brisson, J.A, & Stern, D.L. (2006). The pea aphid, Acyrthosiphon pisum: An emerging genomic model system for ecological, developmental, and evolutionary studies. BioEssays 10, 747-755. Full text 

  •  Caillud, M.C. & Losey, J.E. (2010). Genetics of colour polymorphism in the pea aphid, Acyrthosiphon pisum. The Journal of Insect Science 10, 95.Full text 

  •  Farhoudi et al. (2014). Prey preference of Aphidoletes aphidimyza on Acyrthosiphon pisum: Effect of prey color and size. Journal of Insect Behaviour 27(6), 776-785. Abstract 

  • Gonzalez, D. et al. (1995). Pea aphid and blue alfalfa aphid. In: Nechols, J.R. (Ed), Biological Control in the Western United States. UCANR Publications.

  •  The International Aphid Genomics Consortium (2010). Genome sequence of the pea aphid Acyrthosiphon pisum. PLOS Biology 8(2): e4000313. Full text 

  •  Kunert, G. (2005). Alarm pheromone mediates production of winged dispersal morphs in aphids. Ecology Letters, 8(6), 596-603.Abstract 

  • Losey, J.E. et al. (1997) A polymorphism maintained by opposite patterns of parasitism and predation. Nature 388, 269-272. Abstract 

  • Moran, N.A. & Jarvik, T. (2010). Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science 328 no. 5978, 624-627. Abstract 

  • Peccoud, J. et al. (2009) A continuum of genetic divergence from sympatric host races to species in the pea aphid complex. Proceedings of the National Academy of Sciences USA 106(18), 7495-7500. Full text 

  • Roy, H.E. (2008). Intraguild predation of the aphid pathogenic fungus Pandora neoaphidis by the invasive coccinellid Harmonia axyridis. Ecological Entomology 33, 175-182. Full text 

  • Sloggett, J.J. and Weisser, W.W. (2002). Parasitoids induce production of the dispersal morph of the pea aphid, Acyrthosiphon pisum. Oikos 98: 323-333. Full text 

  • Snyder, W.E. & Ives, A.R. (2001). Generalist predators disrupt biological control by a specialist parasitoid. Ecology 82(3), 705-716. Full text 

  • Snyder, W.E. & Ives, A.R. (2003). Interactions between specialist and generalist natural enemies: parasitoids, predators, and pea aphid biocontrol. Ecology, 84(1), 91-107. Full text 

  • van den Bosch, R. et al. (1966). Parasitization of Acyrthosiphon pisum by Aphidius smithi, a density-dependent process in nature. (Homoptera: Aphidae) (Hymenoptera: Aphidiidae). Ecology 47, 1049-1055. Abstract 

  •  Wilding, N. (1975). Entomophthora species infecting pea aphids. Transactions of the Royal Entomological Society 127 (2), 171-183. Abstract 

  • Ximenez-Embuna, M.G. et al. (2014). Seasonal, spatial and diel partitioning of Acyrthosiphon pisum (Hemiptera: Aphididae) predators and predation in alfalfa fields. Biological Control 69, 1-7. Abstract