Aphid

Aphids, also known as plant lice, are small plant-eating insects, and members of the superfamily Aphidoidea. Oxford University entomologist George C. McGavin has written that aphids are the among the most destructive insect pests on earth.

About 4,400 species of aphids are known, which are presently classified into ten different families. Historically there were many fewer families of aphids, with most species 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 size from one to ten millimetres in length.

Important natural enemies of aphids include predatory lady beetles (Coleoptera: Coccinellidae), hoverfly larvae ( Diptera: Syrphidae), parasitic wasps, aphid midge larvae, aphid lions, crab spiders lacewings ( Neuroptera: Chrysopidae), and entomopathogenic fungi like Lecanicillium lecanii and the Entomophthorales.

Aphids are distributed world-wide, but are most common in temperate zones. It is possible for aphids to migrate great distances, mainly through passive dispersal by riding on winds. For example, the currant lettuce aphid (Nasonovia ribisnigri Mosley) is believed to have been spread from New Zealand to Tasmania in this manner. Aphids have also been spread by human transportation of infested plant materials.

Taxonomy

Aphids are in the superfamily Aphidoidea in the homopterous division of the order Hemiptera. Recent classification within the 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 resulted in a substantial rearrangement of the constituent families within the Aphidoidea superfamily, with some old families reduced to subfamily rank (e.g., Eriosomatidae), and numerous old subfamilies elevated to family rank. To confuse matters further, woolly conifer aphids like the pine aphid, the spruce aphid and the balsam woolly aphid are not actually aphids, but adelgids.

Anatomy

Most aphids have soft bodies, and are green, although other colors such as black, brown, and pink are not uncommon. Aphids have antennas with as many as six segments. Aphids feed themselves through sucking mouthparts called stylets, enclosed in a sheath called a rostrum, which is formed from modified versions of the mandible and maxilla. They have long, thin legs and two-jointed, two-clawed tarsi.

Aphids usually have a pair of cornicles, abdominal tubes through which droplets of a quick-hardening defensive fluid containing triacylglycerols called cornicle wax are exuded. Other defensive compounds can also be produced by some types of aphids.

Aphids have a tail-like protrustion called a " cauda" above their rectal apertures. Aphids have two compound eyes and two ocular tubercles made up of three lenses (which are called triommatidia), each of which is located behind and above the compound eyes. When host plant quality becomes poor or conditions become crowded, female aphids will produce winged offspring, or " alates", that can disperse to other food sources. The mouthparts and eyes are reduced in size, or even missing, in some species and forms of aphids.

Diet

Many aphids are monophagous (i.e. feeding only on one species of plant), but not all are. Some aphid species, 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 stored under high pressure, is forced into the aphid's food canal. As they feed, aphids often transmit plant viruses to the plants, such as potatoes, cereals, sugarbeets and citrus plants. These viruses can sometimes kill the plants.

Plants contain low densities of the nitrogenous compounds needed for building proteins, requiring aphids to consume an excess of sap to satisfy their nutritional requirements. The excess is expelled as " honeydew", out of the recta of aphids, in sufficient volumes that in some circumstances it can "fall like rain". Aphid honeydew is rich in carbohydrates, of which the aphids ingest an excess, being phloem-feeders.

Mutualism

Some species of ants "farm" aphids, protecting them on the plants they eat, and 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. Therefore, sometimes aphids are called "ant cows".

Some of these farming ants 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, or Lasius flavus) manage large "herds" of aphids that feed on roots of plants in the ant colony. Queens that are leaving to start a new colony will take an aphid egg with them to found a new herd of underground aphids in the new colony. These farming ants protect the aphids by fighting off aphid predators.

An interesting variation in ant-aphid relationships involves the Lycaenid butterflies (such as the Sievers blue butterfly and the Japanese copper butterfly) and the Myrmica ants. For example, Niphanda fusca butterflies lay their eggs on plants where ants tend herds of aphids. The eggs hatch as caterpillars which feed on the aphids. The ants in this case do not defend the aphids from the caterpillars, but carry the caterpillars to their nest. The ants feed the caterpillars in their nest, and the caterpillars produce honeydew for the ants in return. When the caterpillars reach full size, they crawl to the colony entrance and form cocoons. After two weeks, butterflies emerge and take flight.

There are also some bees in coniferous forests that collect aphid honeydew to make "forest honey"..

Many aphids are host to endosymbiont bacteria, Buchnera, which live in specialized cells called bacteriocytes inside the aphid. These bacteria synthesize some essential amino acids that are absent in the phloem that the aphids eat.

Reproduction

Aphids are known for having unusual reproductive adaptations in some species. In some species, reproduction is fairly simple. In other aphid species, reproduction can be very complicated with both sexual and asexual forms, creation of eggs or live nymphs and even be associated with switches between woody and herbaceous host plant types at different times of the year.

Many aphids undergo cyclical parthenogenesis. In the spring and summer, only females are present in the population. The overwintering eggs that hatch in the spring result in females, called fundatrices. Reproduction is typically parthenogenetic and viviparous. Females undergo a modified meiosis that results in eggs that are genetically identical to their mother (parthenogenetic). The embryos develop within the mothers' ovarioles, which then give live birth to first instar nymphs (viviparous). The resulting parthenogenic female offspring are called virginoparae. Aphids typically live from 20-40 days and thus undergo multiple parthenogenetic, viviparous generations each summer.

In the fall, a change in photoperiod and temperature cause females to parthenogenetically produce sexual females and males. The males are genetically identical to their mothers except they have one less sex chromosome. These sexual aphid forms might be lacking wings or even mouthparts. Sexual females and males mate and females lay eggs that will develop outside of the mother. Thus in the fall aphids undergo sexual, oviparous reproduction. The aphids spend the winter as eggs and emerge as females in the following spring.

Aphids have been known to have what is called telescoping generations. The parthenogenetic, viviparous female aphid will have a daughter within her, who is already parthenogenetically producing her own daughter at the same time. This leads to the situation where the diet of a female aphid can have inter-generational effects on the body size and birth rate of aphids. In other words, what the aphid eats can directly change the size and fertility of the aphid's daughters and granddaughters.

The life cycle of the rose aphid ( Aphis rosae) may be regarded as typical of the family, though exceptions occur in other species. Eggs produced in the autumn by fertilized females remain on the plant through the winter and hatching in the spring give rise to female individuals which may be winged or wingless. From these, females are born parthenogenetically: that is to say, without the intervention of males, and by a process that has been compared to internal budding, large numbers of young resembling their parents in every respect except size are produced, which themselves reproduce their kind in the same way. This process continues throughout the summer, generation after generation being produced until the number of descendants from a single individual of the spring-hatched brood may amount to many thousands. In the autumn winged males appear; union between the sexes takes place and the females lay the fertilized eggs which are destined to carry the species through the cold months of winter. If, however, the food-plant is grown in a glasshouse or greenhouse where protection against cold is afforded, the aphids may go on reproducing agamogenetically (asexually) without cessation for many years. Similarly, in the tropics, aphids exhibit only parthenogentic reproduction.

The young may be born by the oviparous or viviparous methods and either gamogenetically or agamogenetically, and may develop into winged forms or remain wingless. Males are not produced in significant numbers until the close of the season. Although the factors which determine these phenomena are not clearly understood, it is believed that the appearance of the males is connected with the increasing cold of autumn and the growing scarcity of food, and that the birth of winged females is similarly associated with decrease in the quantity or vitiation of the quality of the nourishment imbibed. Sometimes the winged females migrate from the plant they were born on to start fresh colonies on others often of quite a different kind. Thus the apple aphid (Aphis mali), after producing many generations of apterous females on its typical food-plant, gives rise to winged forms which fly away and settle upon grass or corn-stalks.

Some species of cabbage aphids (like Brevicoryne brassicae) reproduce rapidly during the summer. They are all females, and can produce up to 41 generations of offspring. If none of these died, a female would have more than one and a half billion billion billion offspring (1.5 x 10²⁷) by the end of the season.

Evolution

Aphids probably first 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 one of the species Triassoaphis cubitus Evans from the Triassic. There were relatively few species of aphids at that time, and the number of species only considerably increased since the appearance of angiosperms 160 millions of years ago. This is due to the fact that angiosperms provide an occasion for aphids to become specialized. Organs like the cornicles did not appear until the Cretaceous period.

Threats

Aphids are soft-bodied, and have a wide variety of insect enemies. Aphids also are often infected by bacteria, viruses and fungi. Aphids are affected by the weather, such as precipitation, temperature and wind.

Insects that attack aphids include predatory lady beetles (Coleoptera: Coccinellidae), hoverfly larvae ( Diptera: Syrphidae), parasitic wasps, aphid midge larvae, aphid lions, crab spiders and lacewings ( Neuroptera: Chrysopidae).

Fungi that attack aphids include Neozygites fresenii, Entomophthora, Beauveria bassiana, Metarhizium anisopliae and entomopathogenic fungi like Lecanicillium lecanii. Aphids brush against the spores, which are typically about 1/4 inch long. 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 to continue the cycle. Aphids that have become infected with fungi are covered with a woolly mass that progressively grows thicker and thicker until the aphid is obscured. Often the visible fungus is not the type of fungus that killed the aphid, but a secondary fungus.

Aphids can be easily killed by unfavorable weather conditions. Late spring freezes can kill aphids. If it is too hot, the symbiotic bacteria that some aphids depend on for reproduction are killed, and the aphids are rendered infertile. Rain prevents winged aphids from dispersing and knocks aphids off plants and kills them from the impact or by starvation as they are dislodged from their sources of nourishment. However, Ken Ostlie, an entomologist with the University of Minnesota Extension Service, suggests that rain should not be relied on for aphid control.

Defenses

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. For example, Alexander's horned aphids are a type of soldier aphid that has a hard exoskeleton and pincer-like mouthparts. Infestation of a variety of Chinese trees by Chinese sumac aphids (Melaphis chinensis Bell) can create a "Chinese gall" which is valued as a commercial product. As "Galla Chinensis", Chinese galls are used as a medication used in Chinese medicine to treat coughs, diarrhea, night sweats, dysentry and to stop intestinal and uterine bleeding. Chinese galls are also an important source of tannins.

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

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 and even appears in the 2008 edition of the World Book Encyclopedia.. In fact, honeydew secretions are produced from the anus of the aphid, and cornicles mostly produce defensive chemicals such as waxes. There also is evidence in the literature of cornicle wax attracting aphid predators in some cases. Aphids are also known to defend themselves from attack by parasitoid wasps by kicking.

Effects on plants

Plants exhibiting aphid damage can have a variety of symptoms, such as mottled leaves, yellowing, stunted growth, curled leaves, browning, wilting, low yields and decreased growth rates and even death. Not only can the removal of sap from plants create a lack of vigour, but 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 groundnuts with viruses. Aphids contributed to the spread of late blight (Phytophthora infestans) among potatoes in the Great Irish Potato Famine of the 1840s. Aphids, by coating plants with honeydew, can contribute to the spread of fungi which can damage plants as well. Honeydew produced by aphids has been observed to reduce the effectiveness of fungicides as well.

A hypothesis by Owen and Wiegert that plant fitness might be improved by insect feeding was floated in the mid-1970s. It was felt that the excess honeydew would provide nourishment for 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.

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.

Relation to phylloxera and adelgids

There is a lot of inconsistency in the literature about whether grape phylloxera (Daktulosphaira vitifoliae), the cause of the Great French Wine Blight and a plague that devastated European viticulture in the 19th century, is an aphid or not. Some sources list it as an aphid, and some list it as an aphid-like insect. The yellow phylloxera insects feed on the roots, leaves and shoots of grape plants. However, phylloxera do not produce honeydew or cornicle secretions, and so by these criteria at least, are not aphids. Similarly, adelgids are sometimes described in the literature as aphids, and sometimes as aphid-like insects, but have no cauda or cornicles.

Entomologist Anothony Dixon expresses the ambiguity as: ­

Aphids, adelgids, and phylloxerids are very closely related and are either placed in the insect super family Aphidoidea (Blackman and Eastop, 1994) or into two super families the Phylloxeroidea and Aphidoidea, within the order Homoptera, the plant-sucking bugs.

Oxford University entomologist George McGavin weighs in:

Like adelgids, phylloxerids are distinct from aphids in that they do not have abdominal cornicles or a tail-like cauda.

Aphids in popular culture

• In the movie Antz, Weaver says to Zee "Don't you want your aphid beer?" Zee replies "I can't help it. I have a thing about drinking from the anus of another creature. Call me crazy."

• In the movie A Bug's Life, the Ant Queen has a pet aphid named Aphie.