Aphids Temporal range: Permian–Present PreЄ Є O S D C P T J K Pg N
Pea aphids, Acyrthosiphon pisum. Nymph aphids surrounding the mother aphid were produced parthenogenetically and viviparously; sexual reproduction can be induced by shorter amounts of daylight.
Scientific classification
Kingdom:	Animalia
Phylum:	Arthropoda
Class:	Insecta
Order:	Homoptera
Suborder:	Sternorrhyncha
Superfamily:	Aphidoidea Latreille, 1802
Families
Anoeciidae Aphididae Drepanosiphidae Greenideidae Hormaphididae Lachnidae Mindaridae Pemphigidae Phloeomyzidae Thelaxidae

Aphids, also known as plant lice and in Britain and the Commonwealth as greenflies, blackflies or whiteflies, (not to be confused with "jumping plant lice" or true whiteflies) are small sap sucking insects, and members of the superfamily Aphidoidea.^[1] Aphids are among the most destructive insect pests on cultivated plants in temperate regions.^[1] The damage they do to plants has made them enemies of farmers and gardeners the world over, but from a zoological standpoint they are a very successful group of organisms.^[2] Their success is in part due to the asexual reproduction capability of some species.

About 4,400 species of 10 families are known. Historically, many fewer families were recognised, as most species were included in the family Aphididae. Around 250 species are serious pests for agriculture and forestry as well as an annoyance for gardeners. They vary in length from 1 to 10 millimetres (0.04 to 0.39 in).

Natural enemies include predatory ladybirds, hoverfly larvae, parasitic wasps, aphid midge larvae, crab spiders, lacewings and entomopathogenic fungi like Lecanicillium lecanii and the Entomophthorales.

Distribution[link]

Aphids are distributed worldwide, but are most common in temperate zones. In contrast to many taxa, aphid species diversity is much lower in the tropics than in the temperate zones. They can migrate great distances, mainly through passive dispersal by riding on winds. For example, the currant lettuce aphid, Nasonovia ribisnigri, is believed to have spread from New Zealand to Tasmania in this way.^[3] Aphids have also been spread by human transportation of infested plant materials.

Taxonomy[link]

Aphids are in the superfamily Aphidoidea in the homopterous division of the order Hemiptera. Recent classification within Hemiptera has reduced the old taxon "Homoptera" to two suborders: Sternorrhyncha (e.g., aphids, whiteflies, scales, psyllids, etc.) and Auchenorrhyncha (e.g., cicadas, leafhoppers, treehoppers, planthoppers, etc.) with the suborder Heteroptera containing a large group of insects known as the true bugs. More recent reclassifications have substantially rearranged the families within Aphidoidea: some old families were reduced to subfamily rank (e.g., Eriosomatidae), and many old subfamilies elevated to family rank. Taxonomically woolly conifer aphids like the pine aphid, the spruce aphid and the balsam woolly aphid are not true aphids, but adelgids, and lack the cornicles of true aphids.

Relation to phylloxera and adelgids[link]

Aphids, adelgids, and phylloxerids are very closely related, and are either placed in the insect super family Aphidoidea,^[4] or into two superfamilies (Phylloxeroidea and Aphidoidea) within the suborder Homoptera, the plant-sucking bugs.^[5]

Like aphids, phylloxera feed on the roots, leaves and shoots of grape plants, but unlike aphids do not produce honeydew or cornicle secretions.^[6] Phylloxera (Daktulosphaira vitifoliae) are insects which caused the Great French Wine Blight that devastated European viticulture in the 19th century.

Similarly, adelgids also feed on plant phloem. Adelgids are sometimes described as aphids, but more properly as classified as aphid-like insects, because they have no cauda or cornicles.^[1]

Anatomy[link]

The life stages of the green apple aphid (Aphis pomi)

Most aphids have soft bodies, which may be green, black, brown, pink or almost colourless. Aphids have antennae with as many as six segments.^[1] Aphids feed themselves through sucking mouthparts called stylets, enclosed in a sheath called a rostrum, which is formed from modifications of the mandible and maxilla of the insect mouthparts.^[7] They have long, thin legs and two-jointed, two-clawed tarsi.

Most aphids have a pair of cornicles (or "siphunculi"), abdominal tubes through which they exude droplets of a quick-hardening defensive fluid^[7] containing triacylglycerols, called cornicle wax. Other defensive compounds can also be produced by some types of aphids.^[1]

Aphids have a tail-like protrustion called a "cauda" above their rectal apertures. They have two compound eyes, and an ocular tubercle behind and above each eye, made up of three lenses (called triommatidia).^[5][8]

When host plant quality becomes poor or conditions become crowded, some aphid species produce winged offspring, "alates", that can disperse to other food sources. The mouthparts or eyes are smaller or missing in some species and forms.^[1]

Diet[link]

Many aphid species are monophagous (that is, they feed on only one plant species). Others, like the green peach aphid Myzus persicae, feed on hundreds of plant species across many families.

Aphids passively feed on sap of phloem vessels in plants, as do many of their fellow members of Hemiptera such as scale insects and cicadas. Once a phloem vessel is punctured, the sap, which is under high pressure, is forced into the aphid's food canal. Occasionally, aphids also ingest xylem sap, which is a more dilute diet than phloem sap as the concentration of sugars and amino acids are 1% of those in the phloem.^[9][10] Xylem sap is under negative hydrostatic pressure and requires active sucking, suggesting an important role in aphid physiology.^[11] As xylem sap ingestion has been observed following a dehydration period, it was suspected that aphids consume xylem sap to replenish their water balance; the consumption of the dilute sap of xylem permitting aphids to rehydrate.^[12] However, recent data showed that aphids consume more xylem sap than expected and that they notably do so when they are not dehydrated and when their fecundity decreases.^[13] This suggests that aphids, and potentially, all the phloem-sap feeding species of the order Hemiptera, consume xylem sap for another reason than replenishing water balance.

It was suggested that xylem sap consumption is related to osmoregulation.^[13] High osmotic pressure in the stomach, caused by high sucrose concentration, can lead to water transfer from the hemolymph to the stomach, thus resulting in hyperosmotic stress and eventually to the death of the insect. Aphids avoid this fate by osmoregulating through several processes. Sucrose concentration is directly reduced by assimilating sucrose toward metabolism and by synthesizing oligosaccharides from several sucrose molecules, thus reducing the solute concentration and consequently the osmotic pressure.^[14][15] Oligasaccharides are then excreted through honeydew, explaining its high sugar concentrations, which can then be used by other animals such as ants. Furthermore, water is transferred from the hindgut, where omostic pressure has already been reduced, to the stomach to dilute stomach content.^[16] Eventually, aphids consume xylem sap to dilute the stomach osmotic pressure.^[13] All these processes function synergetically, and enable aphids to feed on high sucrose concentration plant sap as well as to adapt to varying sucrose concentrations.

Plant sap is an unbalanced diet for aphids as it lacks essential amino acids, which aphids, like all animals, cannot synthesise, and possesses a high osmotic pressure due to its high sucrose concentration.^[10][17] Essential amino acids are provided to aphids by bacterial endosymbionts, harboured in special cells, bacteriocytes.^[18] These symbionts recycle glutamate, a metabolic waste of their host, into essential amino acids.^[19][20]

As they feed, aphids often transmit plant viruses to the plants, such as to potatoes, cereals, sugarbeets and citrus plants.^[7] These viruses can sometimes kill the plants.

Symbioses[link]

Ant mutualism[link]

Ant tending aphids

Ant extracting honeydew from an aphid

Some species of ants "farm" aphids, protecting them on the plants they eat, eating the honeydew that the aphids release from the terminations of their alimentary canals. This is a "mutualistic relationship".

These "dairying ants" "milk" the aphids by stroking them with their antennae.^{[Note 1][21]}

Some farming ant species gather and store the aphid eggs in their nests over the winter. In the spring, the ants carry the newly hatched aphids back to the plants. Some species of dairying ants (such as the European yellow meadow ant, Lasius flavus)^[22] manage large "herds" of aphids that feed on roots of plants in the ant colony. Queens that are leaving to start a new colony take an aphid egg to found a new herd of underground aphids in the new colony. These farming ants protect the aphids by fighting off aphid predators.^[21]

An interesting variation in ant-aphid relationships involves lycaenid butterflies and Myrmica ants. For example, Niphanda fusca butterflies lay eggs on plants where ants tend herds of aphids. The eggs hatch as caterpillars which feed on the aphids. The ants do not defend the aphids from the caterpillars but carry the caterpillars to their nest. In the nest, the ants feed the caterpillars, which produce honeydew for the ants. When the caterpillars reach full size, they crawl to the colony entrance and form cocoons. After two weeks, butterflies emerge and take flight.^[23]:78–79

Some bees in coniferous forests also collect aphid honeydew to make "forest honey".^[7]

Bacterial endosymbiosis[link]

Endosymbiosis with micro-organism is common in insects, with more than 10% of insect species relying upon intracellular bacteria for their development and survival ^[24] Aphids harbour a vertically transmitted (from parent to its offspring) obligate symbiosis with Buchnera aphidicola (Buchner) (Proteobacteria:Enterobacteriaceae), referred to as the primary symbiont, which is located inside specialised cells, the bacteriocytes.^[25] The original contamination occurred in a common ancestor 280 to 160 million years ago and has enabled aphids to exploit a new ecological niche, phloem-sap feeding on vascular plants. Buchnera aphidicola provides its host with essential amino acids, which are present in low concentrations in plant sap. The stable intracellular conditions as well as the bottleneck effect experienced during the transmission of a few bacteria from the mother to each nymph increase the probability of transmission of mutations and gene deletions.^[26][27] As a result the size of the B. aphidicola genome is greatly reduced, compared to its putative ancestor.^[28] Despite the apparent loss of transcription factors in the reduced genome, gene expression is highly regulated, as shown by the tenfold variation in expression levels between different genes under normal conditions.^[29] Buchnera aphidicola gene transcription, although not well understood, is thought to be regulated by a small number of global transcriptional regulators and/or through nutrient supplies from the aphid host.

Some aphid colonies also harbour other bacterial symbionts, referred to as secondary symbionts due to their facultative status. They are vertically transmitted, although some studies demonstrated the possibility of horizontal transmission (from one lineage to another and possibly from one species to another).^[30][31] So far, the role of only some of the secondary symbionts has been described; Regiella insecticola plays a role in defining the host-plant range,^[32][33] Hamiltonella defensa provides resistance to parasitoids,^[34] and Serratia symbiotica prevents the deleterious effects of heat.^[35]

Carotenoid synthesis[link]

Some species of aphids have acquired the ability to synthesise red carotenoids, by horizontal gene transfer from fungi. This allows otherwise green aphids to be coloured red. Aphids are the only known member of the animal kingdom with the ability to synthesise carotenoids.^[36]

Reproduction[link]

Aphid giving birth to live young

Juvenile and adult aphids, aphid eggs and moulting individual on Helleborus niger

Some aphid species have unusual and complex reproductive adaptations, while others have fairly simple reproduction. Adaptations include having both sexual and asexual reproduction, creation of eggs or live nymphs and switches between woody and herbaceous types of host plant at different times of the year.^{[Note 2]}

Only females are present in the population (although, a few species of aphids have been found to have both male and female sexes). The overwintering eggs that hatch in the spring result in females, called fundatrices. Reproduction is typically parthenogenetic and viviparous. Eggs are parthenogenetically produced without meioisis^[37][38] and the offspring are clonal to their mother. The embryos develop within the mothers' ovarioles, which then give live birth to first instar female nymphs (viviparous). The offspring resemble their parent in every way except size, and are called virginoparae.

This process iterates throughout the summer, producing multiple generations that typically live 20 to 40 days. Thus one female hatched in spring may produce thousands of descendants. For example, some species of cabbage aphids (like Brevicoryne brassicae) can produce up to 41 generations of females.

In autumn, aphids undergo sexual, oviparous reproduction. A change in photoperiod and temperature, or perhaps a lower food quantity or quality, causes females to parthenogenetically produce sexual females and males. The males are genetically identical to their mothers except that they have one less sex chromosome.^[37] These sexual aphids may lack wings or even mouthparts.^[1] Sexual females and males mate, and females lay eggs that develop outside the mother. The eggs endure the winter and emerge as winged or wingless females the following spring. This is, for example, the life cycle of the rose aphid (Macrosiphum rosae, or less commonly Aphis rosae), which may be considered typical of the family. However in warm environments, such as in the tropics or in a greenhouse, aphids may go on reproducing asexually for many years.^[7]

Some species produce winged females in the summer, sometimes in response to low food quality or quantity. The winged females migrate to start new colonies on a new plant, often of quite a different kind. For example, the apple aphid (Aphis pomi), after producing many generations of wingless females on its typical food-plant, gives rise to winged forms which fly away and settle on grass or corn-stalks.

Some aphids have telescoping generations. That is, the parthenogenetic, viviparous female has a daughter within her, who is already parthenogenetically producing her own daughter. Thus a female's diet can affect the body size and birth rate of more than two generations (daughters and granddaughters).^[39][40]

Aphid reproduction jargon:

Heteroecious – host alternating

• Egg
• Fundatrix (foundress from the first egg)
• Fundatrigeniae (daughter clones)
• Emigrant (winged female; in spring, winged aphids migrating from primary hosts infest Poaceae)
• Apterous exule (wingless female)
• Alate exule (winged female)
• Gynoparae (produce sexual females)
• Male
• Oviparae (sexual females that mate with the males)

Autoecious – single host

• Egg
• Fundatrix
• Apterous exule
• Alate exule
• Sexuparae (Parthenogenetic viviparous females of aphids giving rise to the sexual generation and usually developing on the secondary host, the alate forms migrating to the primary host at the end of the summer (holocyclic and heteroecious aphids).)
• Oviparae
• Males

Within these two host life cycles, there exist 2 other forms of life cycle, holocyclic (sex involved; will lead to egg production which facilitates overwintering), anholocyclic (no sex or egg involved, reproduce parthenogenetically), androcyclic (reproduction at end of season by parthenogenesis to produce males to contribute to holocyclic phase).

The bird cherry-oat aphid is an example of a host alternating species (as implied by the double barrelled name), that starts its life cycle with a large, highly fecund fundatrix. Her offspring then proceed to grow and produce emigrants which develop on the bird cherry before flying to the oat species where they continue feeding. The subsequent apterous exules feed solely on the oats and eventually lead to growth of gynoparae which will return to the bird cherry where they will produce males and oviparae, which in turn will reproduce, giving eggs for the next year.

In heteroecious species, the aphids spend winter on tree or bush aka primary host, in summer they migrate to their secondary host on a herbaceous plant, then the gynoparae return to the tree in autumn. The pea aphid has a primary host of a perennial vetch and secondary of the annual pea. This is likely due to the decline of food quality in trees during the summer as well as overcrowding amongst aphids which they sense when they bump into each other too often. The heteroecious life cycle (which is mainly linked to consumption of angiosperms and represents 10% of all aphids) is believed to have evolved from the ancestral autoecious form (on conifers); this is believed to have reverted to the ancestral form in some species that were once heteroecious.

Four types of alate (winged) aphid morphs exist, known as polymorphisms

• Emigrants (heteroecious only). They are produced on primary host and migrate to secondary host, this is once again due to quality of food decreasing AND to a lesser extent overcrowding. These aphids are capable of eating off of both hosts.
• Alate exules (produced on secondary host if heteroecious, if autoecious will be produced on host anyway). For the alate exules the same factors apply as for emigrants EXCEPT that crowding is more important.
• Gynoparae (heteroecious only and produced on secondary host in response to longer nights and falling temperature).Nymphs can only feed on secondary host, they are unable to consume the primary host,
• Males (produced on secondary host in heteroecious, in autoecious, normal host). These too are produced in response to longer nights and decreased temperature.

Of these, only 0.6% of autumn alate migrants will find host plants i.e. gynoparae.

Why do aphids host alternate?

• Nutritional optimization (right)
• Temperature tolerance – morphs adapted to part temperature.
• Oviposition and rendezvous sites
• Induced host-plant defences - plants abscise galled tissue; evidence shows that some plants selectively drop galled leaves earlier than ungalled ones.
• Increasing chance of new clones produced

  Autoecious (increase likelihood to meet same individual

  Heteroecious (decreases chance of meeting self therefore mating with different clone). Better oviposition sites on trees than herbaceous plants as dies and rots in winter. Problem: survival rate of autoecious vs heteroecious is similar.

• Enemy escape – same tree all year round increases risk of predator finding you, also you can’t escape, however if you move to a secondary host, you can circumvent them for a period of time. One of the problems with this is that on species of primary host, you will find the autoecious aphid that will continue feeding the predator.
• Fundatrix specialisation – host alternation a constraint imposed by specialised feeding requirements of the fundatrix morph as heteroecious life cycle is not the optimal one.
• Many host alternating species are the biggest aphid pests:

Aphis fabae

Metopolophium dirhodum

Myzus persicae

Rhopalosiphum padi

Aphid in Baltic amber

Evolution[link]

Aphids probably appeared around 280 million years ago, in the early Permian period. They probably fed on plants like Cordaitales or Cycadophyta. The oldest known aphid fossil is of the species Triassoaphis cubitus from the Triassic.^[41] The number of species was small, but increased considerably with the appearance of angiosperms 160 million years ago. Angiosperms allowed aphids to specialise. Organs like the cornicles did not appear until the Cretaceous period.

Threats[link]

Aphids are soft-bodied, and have a wide variety of insect predators. Aphids also are often infected by bacteria, viruses and fungi. Aphids are affected by the weather, such as precipitation,^[42] temperature^[43] and wind.^[44]

Insects that attack aphids include predatory Coccinellidae (lady bugs or ladybirds), hoverfly larvae (Diptera: Syrphidae), parasitic wasps, aphid midge larvae, "aphid lions" (the larvae of green lacewings), crab spiders and lacewings (Neuroptera: Chrysopidae).

Predators of aphids

Ladybird larva consuming an aphid

Hoverfly larva consuming an aphid

The ladybird beetle Propylea quatuordecimpunctata consuming an aphid

Fungi that attack aphids include Neozygites fresenii, Entomophthora, Beauveria bassiana, Metarhizium anisopliae and entomopathogenic fungi like Lecanicillium lecanii. Aphids brush against the microscopic spores. These spores stick to the aphid, germinate and penetrate the aphid's skin. The fungus grows in the aphid hemolymph (i.e., the counterpart of blood for aphids). After about 3 days, the aphid dies and the fungus releases more spores into the air. Infected aphids are covered with a woolly mass that progressively grows thicker until the aphid is obscured. Often the visible fungus is not the type of fungus that killed the aphid, but a secondary fungus.^[42]

Aphids can be easily killed by unfavourable weather, such as late spring freezes.^[45] Excessive heat kills the symbiotic bacteria that some aphids depend on, which makes the aphids infertile.^[46] Rain prevents winged aphids from dispersing, and knocks aphids off plants and thus kills them from the impact or by starvation.^[42][47][48] However, rain cannot be relied on for aphid control.^[49]

Defences[link]

Aphid excreting defensive fluid from the cornicles

Aphids are soft-bodied, and have little protection from predators and diseases. Some species of aphid interact with plant tissues forming a gall, an abnormal swelling of plant tissue. Aphids can live inside the gall, which provides protection from predators and the elements. A number of galling aphid species are known to produce specialised "soldier" forms, sterile nymphs with defensive features which defend the gall from invasion.^[7][50] For example, Alexander's horned aphids are a type of soldier aphid that has a hard exoskeleton and pincer-like mouthparts.^[23]:144 Infestation of a variety of Chinese trees by Chinese sumac aphids (Melaphis chinensis) can create a "Chinese gall" which is valued as a commercial product. As "Galla Chinensis", Chinese galls are used in Chinese medicine to treat coughs, diarrhoea, night sweats, dysentery and to stop intestinal and uterine bleeding. Chinese galls are also an important source of tannins.^[7]

Some species of aphid, known as "woolly aphids" (Eriosomatinae), excrete a "fluffy wax coating" for protection.^[7]

The cabbage aphid, Brevicoryne brassicae, stores and releases chemicals that produce a violent chemical reaction and strong mustard oil smell to repel predators.

It was common at one time to suggest that the cornicles were the source of the honeydew, and this was even included in the Shorter Oxford English Dictionary^[51] and the 2008 edition of the World Book Encyclopedia.^[52] In fact, honeydew secretions are produced from the anus of the aphid,^[53] while cornicles mostly produce defensive chemicals such as waxes. There also is evidence of cornicle wax attracting aphid predators in some cases.^[54] Aphids are also known to defend themselves from attack by parasitoid wasps by kicking.

Effects on plants[link]

Plants exhibiting aphid damage can have a variety of symptoms, such as decreased growth rates, mottled leaves, yellowing, stunted growth, curled leaves, browning, wilting, low yields and death. The removal of sap creates a lack of vigour in the plant, and aphid saliva is toxic to plants. Aphids frequently transmit disease-causing organisms like plant viruses to their hosts. The green peach aphid, Myzus persicae, is a vector for more than 110 plant viruses. Cotton aphids (Aphis gossypii) often infect sugarcane, papaya and peanuts with viruses.^[1] Aphids contributed to the spread of late blight (Phytophthora infestans) among potatoes in the Irish potato famine of the 1840s.^[55]

The cherry aphid or black cherry aphid, Myzus cerasi, is responsible for some leaf curl of cherry trees. This can easily be distinguished from 'leaf curl' caused by Taphrina fungus species due to the presence of aphids beneath the leaves.

The coating of plants with honeydew can contribute to the spread of fungi which can damage plants.^[56][57] Honeydew produced by aphids has been observed to reduce the effectiveness of fungicides as well.^[58]

A hypothesis that insect feeding may improve plant fitness was floated in the mid-1970s by Owen and Wiegert. It was felt that the excess honeydew would nourish soil micro-organisms, including nitrogen fixers. In a nitrogen poor environment, this could provide an advantage to an infested plant over a noninfested plant. However, this does not appear to be supported by the observational evidence.^[59]

The damage of plants, and in particular commercial crops, has resulted in large amounts of resources and efforts being spent attempting to control the activities of aphids.^[1]

Control[link]

There are various insecticides that can be used to control aphids. Nowadays, there are many plant extracts and plant products that are eco-friendly and control aphids as effectively as chemical insecticides. Shreth et al. suggested use of neem products and lantana products to protect plants against aphids.^[60] It is important to inspect the undersides of leaves and especially new growth for aphids. Contact pesticides as well as detergents are the most effective means of bringing down an aphid population.

Alternatively, biological control can be used. This involves using a natural predator, such as lacewings, to control the population of aphids^{[citation needed]}. The predator is introduced as eggs or larvae which then develop by eating aphids, bringing down the aphid population^{[citation needed]}. Aphids also dislike the smell of garlic, catnip, and mint^{[citation needed]}. If you add those plants next to infested plants, aphids will soon relocate themselves^{[citation needed]}.

Integrated pest management of various species of aphids can be achieved using biological insecticides based on microbes such as Lecanicillium lecanii or Beauveria bassiana or Paecilomyces fumosoroseus.

Synthesised neuropeptide analogues are another form of biological control that is being explored by researchers at the United States Agricultural Research Service. Neuropeptide is a chemical signal that aphids use to regulate and control body functions such as digestion, respiration, and water intake. Researchers are seeking ways to alter the molecular structure of neuropeptide so that it cannot be broken down by other enzymes, therefore disrupting the body functions that the chemical controls. In experimental tests, one neuropeptide mimic killed 90%–100% of the aphids within three days.^[61] The neuropeptide mimic's rate of mortality is comparable to commercial insecticides; however, the mimic must be thoroughly tested before it can be used as an effective biological agent.^[61]

See also[link]

• Aeroplankton
• Pineapple gall
• Economic entomology

Notes[link]

References[link]

External links[link]

Wikisource has the text of the 1911 Encyclopædia Britannica article Aphides.

Wikimedia Commons has media related to: Aphidoidea

• Aphids of southeastern U.S. woody ornamentals
• Acyrthosiphon pisum, MetaPathogen – facts, life cycle, life cycle image
• Sequenced Genome of Pea Aphid, Agricultural Research Service
• Insect Olfaction of Plant Odour: Colorado Potato Beetle and Aphid Studies
• Asian woolly hackberry aphid, Center for Invasive Species Research

On the University of Florida / Institute of Food and Agricultural Sciences Featured Creatures website:

• Aphis gossypii, melon or cotton aphid
• Aphis nerii, oleander aphid
• Hyadaphis coriandri, coriander aphid
• Longistigma caryae, giant bark aphid
• Myzus persicae, green peach aphid
• Sarucallis kahawaluokalani, crapemyrtle aphid
• Shivaphis celti, an Asian woolly hackberry aphid
• Toxoptera citricida, brown citrus aphid