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Aphids are small sap-sucking insects and members of the superfamily Aphidoidea. Common names include greenfly and blackfly, but the insects can also be brown or pink, and the group includes the fluffy white woolly aphids. A typical life cycle involves flightless females giving living birth to female nymphs without the involvement of males. Maturing rapidly, females breed profusely so that the number of these insects multiplies quickly. Winged females may develop later in the season, allowing the insects to colonise new plants. In temperate regions, a phase of sexual reproduction occurs in the autumn, with the insects often overwintering as eggs.

The life cycle of some species involves an alternation between two host plants, for example between an annual crop and a woody plant. Some species feed on only one type of plant, while others are generalists, colonising many plant groups. About 5,000 species of aphid have been described, all included in the family Aphididae. Around 400 of these are found on food and fibre crops, and many are serious pests of agriculture and forestry, as well as an annoyance for gardeners. So-called dairying ants have a mutualistic relationship with aphids, tending them for their honeydew, and protecting them from predators.

Aphids are among the most destructive insect pests on cultivated plants in temperate regions. In addition to weakening the plant by sucking sap, they act as vectors for plant viruses and disfigure ornamental plants with deposits of honeydew and the subsequent growth of sooty moulds. Because of their ability to rapidly increase in numbers by asexual reproduction, they are a highly successful group of organisms from a zoological standpoint.

Control of aphids is not easy. Insecticides do not always produce reliable results, given resistance to several classes of insecticide and the fact that aphids often feed on the undersides of leaves. On a garden scale, water jets and soap sprays are quite effective. Natural enemies include predatory ladybugs, hoverfly larvae, parasitic wasps, aphid midge larvae, crab spiders, lacewing larvae, and entomopathogenic fungi. Biological pest control as part of an integrated pest management strategy is possible but difficult to achieve except in enclosed environments such as glasshouses.


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Distribution

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. Aphids have also been spread by human transportation of infested plant materials.


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Evolution

Fossil history

Aphids, and the closely related adelgids and phylloxerans, probably evolved from a common ancestor some 280 million years ago, in the early Permian period. They probably fed on plants like Cordaitales or Cycadophyta. With their soft bodies, aphids do not fossilize well, and the oldest known fossil is of the species Triassoaphis cubitus from the Triassic. They do however sometimes get stuck in plant exudates which solidify into amber. In 1967, when Professor Ole Heie wrote his monograph Studies on Fossil Aphids, about sixty species have been described from the Triassic, Jurassic, Cretaceous and mostly the Tertiary periods, with Baltic amber contributing another forty species. The total number of species was small, but increased considerably with the appearance of the angiosperms 160 million years ago, as this allowed aphids to specialise, the speciation of aphids going hand-in-hand with the diversification of flowering plants. The earliest aphids were probably polyphagous, with monophagy developing later. Organs like the cornicles did not appear until the Cretaceous period.

Taxonomy

Aphids are in the superfamily Aphidoidea in the Sternorrhyncha division of the order Hemiptera. Late 20th-century reclassification within the Hemiptera reduced the old taxon "Homoptera" to two suborders: Sternorrhyncha (aphids, whiteflies, scales, psyllids, etc.) and Auchenorrhyncha (cicadas, leafhoppers, treehoppers, planthoppers, etc.) with the suborder Heteroptera containing a large group of insects known as the true bugs. Early 21st-century reclassifications substantially rearranged the families within Aphidoidea: some old families were reduced to subfamily rank (e.g., Eriosomatidae), and many old subfamilies were elevated to family rank. The most recent authoritative classifications place all extant taxa into a single large family Aphididae.

Phylogeny

External

Aphids, adelgids, and phylloxerids are very closely related, and are all within the suborder Sternorrhyncha, the plant-sucking bugs. They are either placed in the insect superfamily Aphidoidea or into the superfamily Phylloxeroidea which contains the family Adelgidae and the family Phylloxeridae. Like aphids, phylloxera feed on the roots, leaves, and shoots of grape plants, but unlike aphids, do not produce honeydew or cornicle secretions. Phylloxera (Daktulosphaira vitifoliae) are insects which caused the Great French Wine Blight that devastated European viticulture in the 19th century. Similarly, adelgids or woolly conifer aphids, also feed on plant phloem and are sometimes described as aphids, but are more properly classified as aphid-like insects, because they have no cauda or cornicles.

The phylogeny of the Sternorrhyncha, inferred from analysis of small subunit (18S) ribosomal RNA, is shown in the cladogram.

Internal

The cladogram based on V. Papasotiropoulos et al., 2013, and H. Kim et al., 2011, shows the internal phylogeny of the aphids, not yet fully resolved.


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Anatomy

Most aphids have soft bodies, which may be green, black, brown, pink, or almost colorless. Aphids have antennae with two short, broad basal segments and up to four slender terminal segments. They have a pair of compound eyes, with an ocular tubercle behind and above each eye, made up of three lenses (called triommatidia). They 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.

They have long, thin legs with two-jointed, two-clawed tarsi. The majority of aphids are wingless, but winged forms are produced at certain times of year in many species. Most aphids have a pair of cornicles (siphunculi), abdominal tubes on the dorsal surface of their fifth abdominal segment, through which they exude droplets of a quick-hardening defensive fluid containing triacylglycerols, called cornicle wax. Other defensive compounds can also be produced by some species. Aphids have a tail-like protrusion called a cauda above their rectal apertures.

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.


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Diet

Many aphid species are monophagous (that is, they feed on only one plant species). Others, like the green peach aphid feed on hundreds of plant species across many families. About 10% of species feed on different plants at different times of year.

A new host plant is chosen by a winged adult by using visual cues, followed by olfaction; if the plant smells right, the next action is probing. The stylus is inserted and saliva secreted, the sap is sampled, the xylem is tasted and finally the phloem is tested. Non-host plants can be rejected at any stage of the probe, but the transfer of viruses occurs early in the investigation process, at the time of the introduction of the saliva, so non-host plants can become infected.

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 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 concentrations of sugars and amino acids are 1% of those in the phloem. Xylem sap is under negative hydrostatic pressure and requires active sucking, suggesting an important role in aphid physiology. As xylem sap ingestion has been observed following a dehydration period, aphids are thought to consume xylem sap to replenish their water balance; the consumption of the dilute sap of xylem permitting aphids to rehydrate. However, recent data showed aphids consume more xylem sap than expected and they notably do so when they are not dehydrated and when their fecundity decreases. This suggests aphids, and potentially, all the phloem-sap feeding species of the order Hemiptera, consume xylem sap for another reason than replenishing water balance.

Xylem sap consumption may be related to osmoregulation. 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. 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 osmotic pressure has already been reduced, to the stomach to dilute stomach content. Eventually, aphids consume xylem sap to dilute the stomach osmotic pressure. 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. Essential amino acids are provided to aphids by bacterial endosymbionts, harboured in special cells, bacteriocytes. These symbionts recycle glutamate, a metabolic waste of their host, into essential amino acids.


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Carotenoids and photoheterotrophy

Some species of aphids have acquired the ability to synthesise red carotenoids by horizontal gene transfer from fungi. They are the only animals other than two-spotted spider mites with this capability. Using their carotenoids, aphids may well be able to absorb solar energy and convert it to a form that their cells can use, ATP. This is the only known example of photoheterotrophy in animals. The carotene pigments in aphids form a layer close to the surface of the cuticle, ideally placed to absorb sunlight. The excited carotenoids seem to reduce NAD to NADH which is oxidized in the mitochondria for energy.


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Reproduction

Aphid reproduction is often complex. Some aphid species alternate between sexual and asexual reproduction, between creation of eggs or live nymphs, and (in some 10% of species) between woody and herbaceous host plants at different times of the year.

When a sophisticated reproductive strategy is used, only females are present in the population at the beginning of the seasonal cycle (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 (stem mothers). Reproduction typically does not involve males (parthenogenesis) and results in live birth (viviparity). Eggs are parthenogenetically produced without meiosis and the offspring are clonal to their mother. The embryos develop within the mothers' ovarioles, which then give birth to live (already hatched) first-instar female nymphs. As the eggs begin to develop immediately after ovulation, an adult female can house developing nymphs which already have developing embryos inside them. This telescoping of generations enables aphids to increase in number with great rapidity. The offspring resemble their parent in every way except size.

This process repeats itself throughout the summer, producing multiple generations that typically live 20 to 40 days. For example, some species of cabbage aphids (like Brevicoryne brassicae) can produce up to 41 generations of females in a season. Thus, one female hatched in spring can theoretically produce billions of descendants, were they all to survive.

In autumn, aphids reproduce sexually and lay eggs. 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 they have one fewer sex chromosome. These sexual aphids may lack wings or even mouthparts. Sexual females and males mate, and females lay eggs that develop outside the mother. The eggs endure the winter and emerge as winged (alate) or wingless females the following spring. This occurs in, for example, the life cycle of the rose aphid (Macrosiphum 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.

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. For example, the apple aphid (Aphis pomi), after producing many generations of wingless females gives rise to winged forms which fly to other branches or trees of its typical food plant. In the autumn, flightless sexual forms occur and lay eggs on shoots.

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).

Some host-alternating (heteroecious) species such as Aphis fabae (blackfly of beans), Metopolophium dirhodum (rose-grain aphid), Myzus persicae (peach-potato aphid), and Rhopalosiphum padi (bird cherry-oat aphid) and Aphis glycines (soybean aphid) are serious pests. They overwinter on tree or bush primary hosts; in summer, they migrate to their secondary host on a herbaceous plant, often a crop, then the gynoparae return to the tree in autumn. Another example is the soybean aphid (Aphis glycines). As fall approaches, the soybean plants begin to senesce from the bottom upwards. The aphids are forced upwards and start to produce winged forms, first females and later males, which fly off to the primary host, buckthorn. Here they mate and overwinter as eggs.


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Ecology

Ant mutualism

Some species of ants farm aphids, protecting them on the plants they eat, eating the honeydew 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.

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) manage large herds of aphids that feed on roots of plants in the ant colony. Queens 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.

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, since the caterpillar produce a pheromone which deceives the ants into treating it as an ant, but carry the caterpillars to their nest. Once there, the ants feed the caterpillars, which in return produce honeydew for the ants. When the caterpillars reach full size, they crawl to the colony entrance and form cocoons. After two weeks, the adult butterflies emerge and take flight. At this point, the ants attack the butterflies, but the butterflies have a sticky wool-like substance on their wings that disables the ants' jaws, allowing them to take flight without being harmed.

Some bees in coniferous forests collect aphid honeydew to make forest honey.

Another ant-mimicking gall aphid, Paracletus cimiciformis (Eriosomatinae), has evolved a complex double strategy involving two morphs of the same clone and Tetramorium ants. Aphids of the round morph cause the ants to farm them, as with many other aphids. The flat morph aphids are aggressive mimics with a "wolf in sheep's clothing" strategy: they have hydrocarbons in their cuticle that mimic those of the ants, and the ants carry them into the brood chamber of the ants' nest and raise them like ant larvae. Once there, the flat morph aphids behave as predators, drinking the body fluids of ant larvae.

Bacterial endosymbiosis

Endosymbiosis with micro-organisms is common in insects, with more than 10% of insect species relying upon intracellular bacteria for their development and survival. Aphids harbour a vertically transmitted (from parent to its offspring) obligate symbiosis with Buchnera aphidicola, the primary symbiont, inside specialised cells, the bacteriocytes. 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. B. 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. As a result, the size of the B. aphidicola genome is greatly reduced, compared to its putative ancestor. Despite the apparent loss of transcription factors in the reduced genome, gene expression is highly regulated, as shown by the ten-fold variation in expression levels between different genes under normal conditions. 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 secondary or facultative (optional extra) bacterial symbionts. These are vertically transmitted, and sometimes also horizontally (from one lineage to another and possibly from one species to another). 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, Hamiltonella defensa provides resistance to parasitoids, and Serratia symbiotica prevents the deleterious effects of heat.

Predators

Aphids are eaten by many bird and insect predators. In a study on a farm in North Carolina, six species of passerine bird consumed nearly a million aphids per day between them, the top predators being the American goldfinch, with aphids forming 83% of its diet, and the vesper sparrow. Insects that attack aphids include the adults and larvae of predatory ladybirds, hoverfly larvae, parasitic wasps, aphid midge larvae, "aphid lions" (the larvae of green lacewings), and arachnids such as crab spiders. Among ladybirds, Myzia oblongoguttata is a dietary specialist which only feeds on conifer aphids, whereas Adalia bipunctata and Coccinella septempunctata are generalists, feeding on large numbers of species. The eggs are laid in batches, each female laying several hundred. Female hoverflies lay several thousand eggs. The adults feed on pollen and nectar but the larvae feed voraciously on aphids; Eupeodes corollae adjusts the number of eggs laid to the size of the aphid colony.

Aphids are often infected by bacteria, viruses, and fungi. They are affected by the weather, such as precipitation, temperature and wind. Fungi that attack aphids include Neozygites fresenii, Entomophthora, Beauveria bassiana, Metarhizium anisopliae, and entomopathogenic fungi such as Lecanicillium lecanii. Aphids brush against the microscopic spores. These stick to the aphid, germinate, and penetrate the aphid's skin. The fungus grows in the aphid's hemolymph. After about three 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 one that killed the aphid, but a secondary infection.

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

Anti-predator defences

Most aphids have little protection from predators. Some species 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. A woolly aphid, Colophina clematis, has first instar "soldier" larvae that protect the aphid colony, killing larvae of ladybirds, hoverflies and the flower bug Anthocoris nemoralis by climbing on them and inserting their stylets.

Though aphids cannot fly for most of their life cycle, they can escape predators and accidental ingestion by herbivores by dropping off the plant onto the ground. Others species use the soil as a permanent protection, feeding on the vascular systems of roots and remaining underground all their lives. They are often attended by ants, for the honeydew they produce, and are carried from plant to plant by the ants through their underground tunnels.

Some species of aphid, known as "woolly aphids" (Eriosomatinae), excrete a "fluffy wax coating" for protection. The cabbage aphid, Brevicoryne brassicae, sequesters secondary metabolites from its host, stores them 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 the 2008 edition of the World Book Encyclopedia. In fact, honeydew secretions are produced from the anus of the aphid, while cornicles mostly produce defensive chemicals such as waxes. There also is evidence of cornicle wax attracting aphid predators in some cases.

Plant-aphid interactions

Plants mount local and systemic defences against aphid attack. Young leaves in some plants contain chemicals which discourage attack while the older leaves have lost this resistance, while in other plant species, resistance is acquired by older tissues and the young shoots are vulnerable. Volatile products from interplanted onions have been shown to prevent aphid attack on adjacent potato plants by encouraging the production of terpenoids, a benefit exploited in the traditional practice of companion planting, while plants neighbouring infested plants showed increased root growth at the expense of the extension of aerial parts.

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 plant viruses to their hosts, such as to potatoes, cereals, sugarbeets, and citrus plants. 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. Aphids contributed to the spread of late blight (Phytophthora infestans) among potatoes in the Irish potato famine of the 1840s. In plants which produce the phytoestrogen coumestrol, such as alfalfa, damage by aphids is linked with higher concentrations of coumestrol.

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

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.


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Sociality

Some aphids have taken the first steps along the road to eusociality, joining insects such as ants, bees and termites. However, there are differences between these sexual social insects and the clonal aphids, which are all descended from a single female parthenogenetically and share an identical genome. About fifty species of aphid, scattered among the closely related, host-alternating families Pemphigidae and Hormaphididae, have some type of defensive morph. These are gall-creating species, with the colony living and feeding inside a gall that they form in the host's tissues. Among the clonal population of these aphids there may be a number of distinct morphs and this lays the foundation for a possible specialisation of function, in this case, a defensive caste. The larval soldiers are altruistic individuals, unable to advance to breeding adults but acting permanently in the interests of the colony. Another requirement for the development of sociality is provided by the gall, a colonial home to be defended by the soldiers.

The soldiers of gall forming aphids also carry out the job of cleaning the gall. The honeydew secreted by the aphids is coated in a powdery wax to form "liquid marbles" that the soldiers roll out of the gall through small orifices. Aphids that form closed galls use the plant's vascular system for their plumbing: the inner surfaces of the galls are highly absorbent and wastes are absorbed and carried away by the plant.


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Interactions with humans

Pest status

About 5000 species of aphid have been described and of these, some 450 species have colonised food and fibre crops. As direct feeders on plant sap, they damage crops and reduce yields, but they have a greater impact by being vectors of plant viruses. The transmission of these viruses depends on the movements of aphids between different parts of a plant, between nearby plants and further afield. In this respect, the probing behaviour of an aphid tasting a host is more damaging than lengthy aphid feeding and reproduction by stay-put individuals. The movement of aphids influences the timing of virus epidemics.

Dispersal can be by walking or flight, appetitive dispersal or by migration. Winged aphids are weak fliers, lose their wings after a few days and only fly by day. Dispersal by flight is affected by impact, air currents, gravity, precipitation and other factors, or dispersal may be accidental, caused by movement of plant materials, animals, farm machinery, vehicles or aircraft.

Control

Insecticide control of aphids is difficult, as they breed rapidly, so even small areas missed may enable the population to recover promptly. Aphids may occupy the undersides of leaves where spray misses them, while systemic insecticides do not move satisfactorily into flower petals. Finally, some aphid species are resistant to common insecticide classes including carbamates, organophosphates, and pyrethroids.

For small backyard infestations, spraying plants thoroughly with a strong water jet every few days may be sufficient protection. An insecticidal soap solution can be an effective household remedy to control aphids, but it only kills aphids on contact and has no residual effect. Soap spray may damage plants, especially at higher concentrations or at temperatures above 32 °C (90 °F); some plant species are sensitive to soap sprays.

Integrated pest management of various species of aphids can be achieved using biological insecticides based on fungi such as Lecanicillium lecanii, Beauveria bassiana or Isaria fumosorosea.

Aphids may also be controlled by the release of natural enemies, in particular lady beetles and parasitoid wasps. However, since adult lady beetles tend to fly away within 48 hours after release, without laying eggs, repeated applications of large numbers of lady beetles are needed to be effective. For example, one large, heavily infested rose bush may take two applications of 1500 beetles each.

In human culture

Aphids are familiar to farmers and gardeners, mainly as pests. Peter Marren and Richard Mabey record that Gilbert White described an invading "army" of black aphids that arrived in his village of Selborne in August 1774 in "great clouds", covering every plant, while in the unusually hot summer of 1783, White found that honeydew was so abundant as to "deface and destroy the beauties of my garden", though he thought the aphids were consuming rather than producing it.

Infestation of the Chinese sumac (Rhus chinensis) by Chinese sumac aphids (Schlechtendalia chinensis) can create "Chinese galls" which are valued as a commercial product. As "Galla Chinensis", they are used in traditional 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.

Source of the article : Wikipedia



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