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'True aphids' - their Biology and MorphologyOn this page: Biology Morphology Subfamilies
Introduction & taxonomy
This page summarises the biology and external morphology of 'true' aphids: known colloquially as 'plant lice' in USA, or greenfly / blackfly in UK. More than 5200 species of aphid have been described, of which at least 5000 are true aphids - insects in the family Aphididae. The Aphididae currently has 510 genera, and is one of three families in the superfamily Aphidoidea (as defined by Remaudière & Remaudière, 1997). The other two Aphidoidea families, the Adelgidae and Phylloxeridae have a mere 51 and 66 and species each. Although closely related, those families are not considered 'true aphids'.
The infraorder Aphidomorpha comprises the Aphididae, Adelgidae and Phylloxeridae, plus various extinct taxa. Other related groups in the suborder Sternorrhyncha are the superfamilies Aleyrodoidea (white flies) which have more than 1500 species, Coccoidea (scale insects and mealy bugs) with about 8000 species and Psylloidea (jumping plant lice) which has over 3000 species worldwide.
Habitats & distribution
Aphididae have been recorded from all terrestrial habitats globally, aside from ice-bound regions. There are even a few species that can feed underwater, for example Pemphigus trehernei feeds on the roots of sea aster and is dispersed by wind and tides.
Pemphigus trehernei first-instar nymph, floating.
Most Aphididae are northern temperate species, where they have been recorded feeding on at least 25% of plant species. Whilst nearly all Aphididae subfamilies are centred upon one continent-ecozone (e.g. Holarctic, nearctic, oriental) their speciation is primarily plant- and niche-specific. Some 'anholocyclic species' (presumably clones) are pan-global. Surprisingly few Aphididae species are specific to the tropics or to tropical tree species, and compared to temperate trees, many tropical trees have very few Aphididae species compared with those of other sternorrhynchan groups (such as the psyllids, superfamily Psylloidea).
Aphididae feed on plant sap, specifically phloem sap, and sometimes a little xylem sap (Pompom et al., 2011) by fine puncture of the plant conductive vessels. One exception is Paracletus cimiciformis, one morph of which has evolved to feed on ant larvae haemolymph (Salazar et al., 2015). There are also occasional reports of aphids trying exploratory probes on humans, for example Acyrthosiphon pisum, by Culliney & Ruberson (1986) and Ceratoglyphina styracicola, by Aoki & Kurosu (2010) - albeit they are ill-adapted for a high-protein diet! Defensive morphs of some eusocial species employ sclerotized stylets (Pike & Foster, 2008) to inject venom into predators, but don't seem to feed from them. Aphididae are primarily high-sugar, low-nitrogen, leaf or needle feeders. A smaller proportion are stem feeders, or specialize in other parts such as roots, some seasonally so. Some species are quite flexible feeding on both stems and leaves (for example Periphyllus testudinaceus).
Aphis lamiorum third instar nymph amongst flowers.
Also a few produce galls, usually on their primary host. Aphids prosper when and where phloem-movement is greatest (during growth and senescence). Aphididae are known from about 300 families of vascular plants including bryophytes (mosses only), gymnosperms, pteridophytes and angiosperms. The hosts most used by aphids are Compositae (by 15% of species), conifers (by 9%), Rosaceae (7%), Grasses (6%), Salicaceae (5.5%) and Fagaceae (5%).
Whereas most Aphididae species are restricted to a few closely-related host species, the commonly-encountered Aphididae are on plant monocultures, or are polyphagous species. Note, however, that even Myzus persicae, the most polyphagous aphid known, has been recorded on fewer than 1% of angiosperm species. 58% of Aphididae species feed on non-woody hosts. Of those, 10% of species alternate between a 'primary' usually-woody perennial host (where they would normally sexually reproduce) and 'secondary' herbaceous hosts (sometimes of many unrelated species, where they reproduce asexually). Such host alternating behaviour is termed dioecious or heteroecious, whilst remaining on one host is termed monoecious or autoecious (such needless duplication of terminology is sadly common in aphidology). Host alternation is common in the Aphidinae, Anoeciinae and Pemphigini, but unknown in the Chaitophorinae Chaitophorinae Drepanosiphinae, Greenideinae, and Lachninae, although in some of these there may be a movement between roots and upper parts of the same host. (Adelgidae & Phylloxerids also host alternate, but to fewer, generally woody, secondary host species.) Whether monoecy or heteroecy is 'primitive' is unknown. Ancestral Aphididae are thought to have radiated from gymnosperms (Podocarpaceae or Araucariaceae) to Pinaceae and angiosperms. The most favoured woody hosts tend to be older evolutionary groups such as Coniferae, Lauraceae, Fagaceae, Betulaceae, Hamamelidaceae, Ulmaceae and Juglandaceae.
Reproduction & lifecycle
All non-clone species undergo cyclical parthenogenesis - in other words, they alternate one sexual generation with multiple asexual generations. This is commonly assumed to be an ancient adaptation to temperate climates.
Sexual reproduction is oviparous (Melaphis rhois & Schlechtendalia chinensis are ovoviviparous), asexual reproduction is viviparous (cf. Adelgidae & Phylloxerids, which are uniformly oviparous). Some Aphididae only reproduce sexually in part of their range, and elsewhere exist clonally. Quite a few species have never been recorded reproducing sexually. However, some species once thought to be entirely clonal (such as Myzus ornatus) are now known to (very rarely) produce sexual forms (in India for Myzus ornatus). Parthenogenetic viviparity enables aphids to produce embryos within embryos, telescoping generations - thus increasing the potential reproductive rate (r).
Paramyzus heraclei aptera giving birth.
Although aphids as a group are justifiably regarded as r-strategists, most species of aphids seldom exhibit such a potential and remain unnoticed or rare. A few r-strategists, especially polyphagous host alternating species on their secondary hosts, can produce enormous usually apterous colonies. The common response to dense overcrowded colonies is to develop alatae which migrate to unutilized hosts. Almost all Aphididae produce multiple distinct role-specialized morphs, many with neotenic features. Most species develop their sexual morphs in autumn, and 99% of species have wingless oviparae (the exceptions being Aiceoninae, Phloeomyzinae, Tamaliinae, and most Neophyllaphidinae). Host alternating species produce winged gynoparae and (somewhat later) males on the secondary host which migrate back to the primary host. There the gynoparae produce oviparae which mate with males returning from the secondary host. Non host-alternating species produce sexuparae which generally yield wingless males and oviparae. Most, but not all, host alternating species produce many differing morphs (reproductive, sexual, dispersive, host, diapausal, defensive, seasonal & feeding-site specific).
Ant attendance plays an important role in protection against predators and parasitoids for many, but certainly not all, aphid species. Despite their pre-Linnean English name, 'ant cow', most species (including many 'pest aphids') are not ant tended. For those that are attended, ant attendance is generally facultative and can vary over time and between locations.
Chaitophorus salicti attended by Myrmica ant.
Ant-attractive honeydew requires extra melezitose production by the aphid, but other options such as wax production are also energy-intensive. Some ant and Aphididae species are very intimately associated, for example the speciation of Stomaphis wojciechowskii was specifically due to its association with Lasius brunneus (Depa et al., 2017). Very few aphid species cannot survive without ant-attendants, but many do better with it, often markedly so. Some ant species mix attendance with predation, attending aphids early in the year for the honeydew but later predating them for the protein.
Buchneria aphidicola are gut-symbiont bacteria obligatory to almost all Aphididae. Buchneria produce most of the aphids' essential amino acids (via trans-amination), and probably mediated the rapid divergence of Aphididae species during the Cretaceous radiation to angiosperms (Bennet & Moran, 2015); hence the greater number of species in the Aphididae compared to either the Adelgidae or Phylloxerids. Their strictly clonal heritability (disputed by Heie) has been used to deduce Aphididae phylogeny. At least some Aphididae also host Wolbachia, a reproductive parasite.
Morphs & forms
Aphid morphology is simpler than sternorrhynchans such as Psylloidea, but identification is complicated by aphids having multiple, seasonal morphs (as do the Phylloxerids). Adults tend to be apterous and nymph-like. As a result nymphs and adult apterae, especially of flattened forms, look much like other Sternorrhyncha nymphs (Adelgidae and Phylloxeridae also have apterous forms). In Aphididae alate morphs are assumed to be primitive. Common morph specializations are the fundatrix (apterous, with a rounder often hairy body); vivipara (apterous, sensoria reduced), male (winged, small, may lack mouthparts), ovipara (usually apterous sometimes with elongate abdomen), defensive (thicker legs), alata (enhanced sensoria, longer legs, smaller abdomen).
Body size, shape & appearance
The average body length of adult apterae is about 2 mm, but this ranges from 0.4 mm in Neothoracaphis querciphaga, to 7.8 mm in Cinara confinis and Longistigma caryae. Aphid body length commonly varies 2-fold within a species, mostly due to differing nutrition, but island populations may deviate further. Alatae, males and aestivating forms are smaller. Compared to many insects aphids are lightly sclerotized (the head and thorax of alatae are more sclerotized). Aphididae are mostly greenish, brown or grey, but may be of any colour, and range from pear-shaped to oval, elongate, coccid-like or flattened.
Laingia psammae aptera.
Species are variably waxed depending on species, age, ant-attendance and feeding location. They are ornamented with tubercles, processes, and various hair-types.
Head, antennae & rhinaria
The aphid head is deflexed, meaning it is bent abruptly downward, and not extended forward and out as in Heteroptera. Its sclerites are completely fused (cf. Psylloidea, whose head sclerites are not completely fused). The head bears 2 antennae, often on 'tubercles'. In adult viviparae each antenna has 5-6 (rarely 4) 'segments'. The two short, broad basal segments are independently muscularized (the first usually longer than the second); the remaining up to four slender terminal segments (correctly termed flagellomeres) are non-muscularized. The last segment (usually segment VI) terminates in a thinner process called the 'terminal process' (Phylloxerids and Aleyrodidae antennae also have a small terminal process). The relative lengths of the terminal process and the base of segment VI differ consistently between subfamilies (e.g. Aphidinae and Calaphidinae have the terminal process longer than the base of segment VI; Lachninae and Eriosomatinae have the terminal process shorter than the base). The antennae have no arista. There is one primary rhinarium on the base of antennal segment VI (just prior to the terminal process), plus usually one on segment V, and rarely one on segment IV. Secondary rhinaria of varying shapes, numbers and distributions are also present.
Eriosoma ulmi antenna with annular secondary rhinaria.
Alatae usually have longer antennae, a longer terminal process and more secondary rhinaria (an exception is alatae of Aphis cottieri, a New Zealand endemic which lack secondary rhinaria). Early instars have proportionally shorter antennae, with fewer segments, fewer rhinaria and a shorter terminal process.
Aphididae have one pair of compound eyes of relatively few ommatidia. These eyes are reduced in some species, absent in early nymphs of many species (and absent in Phylloxeridae). Several members of the Thelaxinae and Pemphigini lack compound eyes, except as adult alatae. Usually postero-lateral to each compound eye is a 3-lensed ocular tubercle specific to Aphidoidea, known as a triommatidium (but Saltusaphidinae have triommatidia without ocular tubercles). The triommatidium is below the compound eye in Nippolachnus, reduced in Pehuenchaphis and absent in Capraphis and Brevicorynella. In the Greenideinae the tubercle is especially large, and especially small in Lachnidae. In most Aphididae, compound eyes are present in addition to triommatidia from the larval stage, but there is no triommatidium in the first instar larva of some subfamilies (e.g. Aphidinae and Chaitophorinae). Early instars of some species only have triommatidia, as do larval Adelgidae, Phylloxerids - and larval and female coccids. Ancestral Aphidomorpha nymphs are assumed to have triommatidia, but lack compound eyes. Aphididae often also have 3 ocelli - in common with larvae and adults of most exopterygote insects. Alate morphs are always provided with three ocelli.
Like other Hemiptera, Aphididae stylets are sheathed within a beak-like rostrum comprised of the labium, the modified mandible and the maxilla. The base originates between the front coxae (hence Sternorrhyncha: from sternon=breast-bone + rhunkhos=snout) but this is invisible externally. The rostrum emerges beneath the head through a small membranous gula (cf. Heteroptera, which have the gula larger, sclerotized & frontal). The rostrum has 5 segments but, except in the Lachninae, the two apical segments are fused so just 4 are apparent (Razaq, 2000, reported only 3 apparent segments in the rostrum of Aphis spiraecola).
Macrosiphum daphnidis aptera, head. Sample courtesy Mark & Heather Wilson.
The second segment sometimes has a wishbone-like stiffening: for example it is well developed in Macropodaphidinae, Saltusaphidinae; usually so in Calaphidinae; variably in Phyllaphidinae; poorly or absent in Taiwanaphidinae; and absent in Baltichaitophorinae, Chaitophorinae, Israelaphidinae, Mindarinae and Pterastheniinae. The rostrum is longer in the Aphididae than in the Adelgidae or Phylloxerids, albeit it is absent in the males of species such as Stomaphis (Eriosomatinae & Phylloxeridae sexuales are also arostrate). When feeding the labium is folded and/or partially retracted into the aphid. When resting, the rostrum is stiff and usually retracted; it extends backwards between the legs and in most species reaches the coxa of the third pair of legs. In crevice-feeding species like Stomaphis it is more than twice the body length and held laterally along the body.
Thorax & legs
The thorax is comprised of three segments (the prothorax, mesothorax, and metathorax) each bearing a pair of legs. In alatae the two hindmost segments each bear a pair of wings (reduced in brachypterous forms). The pronotum is small. The head, thorax, and abdomen are usually broadly and immovably joined. Aphid legs are borne ventrally. They are comparatively long and thin in many species, but reduced in groups such as root feeders. Each leg has 5-6 segments: the coxa, trochanter, femur, tibia, and typically 2 jointed non-muscularized tarsal segments (a short basitarsus, TI, and a longer distitarsus, TII). The trochanter & femur are fused in apterae of subfamilies Aiceoninae, Phyllaphidinae & Tamaliinae. The distitarsus bears an empodium and a pair of curved, pointed tarsal claws (interesting exceptions are the American Atarsos grindeliae which have no tarsi, and many Dermaphis which have tarsi lacking claws). Oviparae generally have hind legs bearing pseudosensoria (=scent plaques), and thickened in some species.
Wings & wing veins
Alate Aphididae have forewings and hindwings which are thin, flexible, of uniform consistency throughout, and usually largely unpigmented (cf. Aleyrodoidea, where the wings are opaque whitish clouded or mottled). Most Aphididae hold them 'tent-like' over the abdomen at rest (as do the Adelgidae) but some genera e.g. Aploneura in the Fordini, and Monellia in the Panaphidini, hold the wings flat (as do the Phylloxerids).
The forewing anterior margin is strengthened by a thick subcostal band consisting of parallel costal and subcostal veins ending in a well-developed variably-pigmented pterostigma. From the pterostigma a curved radial sector (Rs) usually arises that terminates near the tip of the wing (Rs is absent in Pseudochromaphis & some Calaphis, and does not meet the tip in Cinara fresai). From the subcostal vein arise three 3 oblique veins: 2 unbranched cubitus veins (Cu1a & Cu1b) (also termed CuA1 and CuA2) separated at their bases, and a media (M) usually with one or two branches (an exception is Kugegania ageni the forewings of which lack a radius in more than 90% of specimens, and have hindwings without oblique veins) (cf. Adelgidae, whose forewings lack a separate Rs, have an unbranched media, have the Cu arising separately from the anal vein, and have the two branches of cubitus leaving at the same point on the main vein; cf. Phylloxeridae whose forewings lack a radial sector, have an unbranched media, a fork-shaped Cubitus, and Cu1a and A arise on a common stalk).
Aphididae hindwings are much smaller than the forewings and have reduced venation. There is normally only one oblique vein, and a maximum of 2 oblique veins. Oblique veins are absent in some Greenideoida, Quernaphis, and Kugegania ageni. (Adelgidae hind wings normally have only one oblique vein and Phylloxeridae lack any.) Like other Sternorrhyncha, the hind wing has no vannus (=anal wing area) or vannal fold.
Abdomen, siphunculi & cauda
The aphid abdomen has 8 visible segments, with a maximum of 7 pairs of spiracles borne laterally by the posterior segments (cf. Adelgidae, which have 6 pairs of spiracles, and Phylloxerids, which have 1). The 5th or 6th segment usually bears a pair of siphunculi (= cornicles, USA) used for emitting alarm pheromones and defensive waxy secretions. Siphunculi come in many different forms, from long cylinders (Aphidinae and Calaphidinae), which may be swollen in parts, to short cones or pores (Eriosomatinae and Thelaxinae).
Siphunculi are much reduced or absent in a variety of other groups or genera (which may be a 'primitive' feature), often related to whether they are root feeding and/or attended by ants. In some Macrosiphini, tergite VIII is produced into a cowl-like supracaudal process. In adult Aphididae the abdomen ends in a modified 9th tergite: an elongate, triangular or rounded hair-bearing cauda. This is reduced in some species and late-instar immatures, and absent in early instars. The cauda of some species has hairs which retain honeydew for attending ants. Siphunculi and cauda are specific to Aphididae, albeit they may be reduced or absent in immatures and some species.
Uroleucon cichorii adults with white cauda.
The last abdominal sternite (IX) forms the sclerotic subanal plate (present in adults, reduced in late instars) which may be entire or with a posterior median cleft or emargination. Anterior to this in adult female morphs lies the subgenital plate (=genital plate) - a transverse oval, reniform or oblong sternite, behind the posterior margin of which opens the inconspicuous genital orifice. Between the subgenital and subanal plates, and behind the genital orifice, occur 2-4 small hair-bearing lobes which are the rudiments of the primitive gonapophyses. In males the external genitalia are much more complex and conspicuous, consisting basically of a subcircular sclerotic apodeme providing leverage for the erection and extrusion of a pair of bristly claspers and a tubular sclerotic aedeagus terminating in a thin-walled extrusible penis (from Stroyan, 1984). Like Coccidae, Aphididae have no ovipositor, albeit the pointed abdomen of some species' oviparae resembles one. (Phylloxerids also have no ovipositor, but Adelgidae have a sclerotized one, reduced in parthenogenetic females).
Aphididae eggs are smooth, round, oval or chisel-shaped (Greenideinae & Taiwanaphidinae are flat). Except for Aiceoninae and some Greenideinae, the eggs are not stalked (nor are Phylloxerids eggs, but Adelgidae attach theirs to a substrate by wax threads). The eggs darken post laying, and are variably wax covered (unwaxed if ant-protected). Aphididae eggs are only produced sexually. Most reproduction of Aphididae is asexual and viviparous (cf. Adelgidae & Phylloxeridae, where all females are oviparous, both parthenogenetic and sexual). In anholocyclic Aphididae reproduction is entirely asexual and viviparous.
Subfamilies in the Aphididae
Using the classification of Remaudiére and Remaudiére (1997), the family Aphididae consists of 24 extant subfamilies. Recently a former 25th subfamily, the Pterocommatinae has been moved into the Aphidinae as a subtribe. Roughly half of the estimated 5200 species are in the Aphidinae subfamily. Classification and phylogeny within the Aphidoidea are still disputed. Heie & Wegierek (2009b) for example, put 13 of these subfamilies (Calaphidinae, Chaitophorinae, Drepanosiphinae, Israelaphidinae, Lizerinae, Macropodaphidinae, Mindarinae, Neophyllaphidinae, Phyllaphidinae, Pterastheniinae, Saltusaphidinae, Spicaphidinae, Taiwanaphidinae) into the family Drepanosiphidae, and gave most other subfamilies full family status. Given the phylogeny amongst subfamilies is so far unresolved, we list them in alphabetical order.