Aphids are remarkable, evolutionarily exquisite creatures,and are among the most successful insects. Aphid evolution has been shaped through nutrient-driven selection and by the host plants on which they feed, and aphids have responded by developing intricate life cycles and complex polymorphisms. These sap-feeding hemipterans have coped with a hostile world through developing an exceptionally high reproductive rate and passive wind-borne dispersal, a strategy in which individuals are quite expendable, but survival and prosperity of their genes are guaranteed. Because of their intriguing evolutionary adaptations, aphids were among our most worthy competitors as humans entered the agricultural era.
MAJOR GROUPS AND HOST AFFILIATIONS
Aphids, as the superfamily Aphidoidea, belong to the Hemipteran Sternorrhyncha with Aleyrodoidea (whiteflies), Psylloidea (jumping plant lice), and Coccoidea (scale insects and mealybugs). Aphidoidea has three families: Adelgidae (adelgids), Phylloxeridae (phylloxerids), and Aphididae. Some workers place the Adelgidae and Phylloxeroidea in a separate superfamily, Phylloxeroidea. Adelgids and phylloxerids are primitive “aphids” and older groups, each with about 50 species. They differ from Aphididae by having an ovipositor and reproducing by means of ovipary, whereas Aphididae lack an ovipositor and are parthenogenetically viviparous, bearing live young. Adelgids are restricted to conifers in Pinaceae where some form characteristic galls. Phylloxerids, which may also form galls, occur as the tribe Phylloxerinini on Salicaceae, or as the tribe Phylloxerini on Fagaceae, Juglandaceae, Rosaceae, Ulmaceae, and Vitaceae. An important phylloxerid, Daktulosphaira vitifoliae, grape phylloxera, can kill European grapevine cultivars unless they are grafted to resistant rootstocks developed from American grape species. This species devastated the wine industry a century ago.
Aphids (Fig. 1) are diverse and have many specialized morphological structures that vary among groups. The most unique are paired siphunculi (cornicles) that release an alarm pheromone. These vary from being mere pores on the abdominal surface to being very elongate and sometimes elaborate tubes. Aphids also have a cauda, used to manage honeydew, on the abdominal terminus. This may vary from rounded, to knobbed, to long and fingerlike. Some aphids produce waxy cuticular excretions and can resemble other Sternorrhyncha. Aphids probably had a Permian origin, but their oldest fossils are Triassic (230mya). Modern aphids began diversification with angiosperms in the lower Cretaceous (140 mya). Most fossil aphid groups became extinct during the Cretaceous-Tertiary boundary, and most current groups radiated during the Miocene. Aphids originally evolved on woody plants in the Northern Hemisphere, and are functionally replaced by whiteflies and psyllids in the Southern Hemisphere.
The taxonomy of Aphididae is quite difficult and subfamily demarcation has been argued through many classifications. Remaudiere and Remaudiere’s 1997 classification, followed here, recognizes about 25 aphid subfamilies, with tribal groupings for about 600 genera and 4700 species of aphids. Many aphid lineages coevolved with, and radiated among, their host plant groups. Often during their phylogenetic history, however, some aphid groups opportunistically switched to radically unrelated host groupings, driven by developmental requirements but tempered by evolutionary constraints.
Many aphid subfamilies are small, but several are larger and important: Chaitophorinae on Salicaceae and Gramineae; the closely related Myzocallidinae, Drepanosiphinae, and Phyllaphidinae, often considered to be one subfamily and usually on dicotyledonous trees, but also Fabaceae and bamboo; Lachninae, mostly on Pinaceae, but also Fagaceae, Rosaceae, and roots of Asteraceae; and Pemphiginae, often on roots and host alternating to dicotyledonous trees forming galls. Other noteworthy subfamilies include Pterocommatinae, on Salicaceae; Greenideinae, on Fagaceae; Mindarinae, on Pinaceae; and the host-alternating Anoeciinae and Hormaphidinae.
The largest and most evolutionarily recent subfamily, Aphidinae, has two large, diverse, and agriculturally important tribes: Macrosiphini and Aphidini. Macrosiphini is diverse in genera; its species usually lack attendance by ants. Aphidini is diverse in species, which are often ant attended, but less diverse in genera. Tribe Aphidini has two important subtribes. Subtribe Rhopalosiphina host alternates between Rosaceae and Gramineae or Cyperaceae.
Subtribe Aphidina host alternates mostly among Rosidae and Asteridae and is home to the large and agriculturally important genus Aphis.
FIGURE 1 Aphid diversity and morphs: (A) Aphis nerii apterae, (B) Uroleucon ambrosiae apterae, (C) Acyrthosiphon kondoi aptera giving birth, (D) Dysaphis plantaginea apterae, (E) Neophyllaphis podocarpi apterae with flocculent wax, (F) Prociphilus americanus apterae with filamentous wax and pseudococcidlike appearance, (G) Aphis spiraecola alata and apterae, (H) Cerataphis orchidearum aptera with wax fringe resembling an aleyrodid, (I) Rhopalosiphum nymphae ovipara and winged male in copula, and (J) Acyrthosiphon kondoi (left) and A. pisum (right) alatae.
NUTRITION-DRIVEN EVOLUTION: LIFE CYCLES AND POLYMORPHISM
The complex life cycles of aphids have caused many specialized morphs to evolve. These have many confusing, synonymous names, but the names are minimized here. Aphid life cycles can be either monoecious or dioecious and involve holocycly or anholocycly.
In the simple and generalized monoecious holocyclic aphid life cycle (Fig. 2A) , a single host plant species is used throughout the year and sexual morphs are produced in the fall, usually in response to decreasing day length. The males and oviparae mate, producing genetically recombinant eggs that overwinter on the host plant and often experience high mortality. In the spring, the fundatrix emerges from the egg, matures, and gives parthenogenetic live birth to nymphs that become viviparae and continue in that reproductive mode through the summer. If the aphid group produces plant galls, the fundatrix is responsible for their production.
The viviparae may be apterae (wingless) or alatae (winged), but in some groups all viviparae are alatae. The parthenogenetic reproduction of viviparae allows a very rapid population buildup. At birth, each viviparous nymph has within it the embryos of its daughters and granddaughters, creating a “telescoping” of generations. Apterae, lacking wings and their associated musculature, are optimized for reproduction, and have more offspring per female than do alatae. Alatae invest resources in their flight apparatus and are optimized for dispersal. Alatae, however, begin progeny production earlier in life than do apterae, giving the alatae relatively reduced number of offspring and a better generational turnaround time. Apterae are produced selectively when nutrient production by their hosts is high. Once an aphid population has increased enough to induce crowding and stress its host’s nutrient levels, the population usually switches to alatae production. This allows dispersal to better feeding situations and optimizes the genetic survival of the clone. Alate flight is mostly passive in the wind, and after successfully alighting on their proper host, often by chance, alatae feed for a short time before beginning autolysis of their flight musculature. While precluding further flight, the autolysis self-cannibalistically provides nutrients for their offspring. The production of viviparae continues until fall conditions trigger production of the sexuals.
A second, more complicated dioecious life cycle (Fig. 2B) has independently evolved among several different aphid groups that show seasonal alternation between differing hosts. This cycle probably evolved in response to the seasonally inadequate supply of nitrogen-based nutrients, especially amino acids, on the primary host. The phloem sap that aphids feed upon has limited nitrogen availability, which inhibits adequate protein synthesis during aphid development. Woody deciduous plants normally translocate amino acids in quantity only during spring foliation and fall leaf senescence. The latter breaks down leaf protein allowing nitrogen translocation to the roots for overwinter storage and future spring plant growth. Aphid groups evolving on, and restricted to, such plants face a nitrogen deficit during summer, when active plant growth ceases and phloem sap is low or devoid of nitrogen. Such groups (e.g., Periphyllus spp.) may develop an aestivating nymph that halts growth until fall.
Other groups, such as Aphidinae, whose ancestors originated on deciduous woody plants, have evolved to leave those primary hosts during the late spring, after the nitrogen flush of foliation has ceased. In doing so, their spring alatae, as emigrants, migrate to herbaceous secondary hosts that actively grow and translocate nitrogen during summer. In fall, however, as these secondary hosts die back, the aphids return to their woody primary host by producing winged migrating males and gynoparae, the latter giving rise to oviparae. Upon returning, the aphid’s sexuals (its males and oviparae) capture the primary host’s fall nitrogen flush and mate to lay their overwintering eggs in anticipation of the spring nitrogen flush.
Among most aphid lineages, the primary hosts are often specific as to plant genus. Secondary hosts for lineages, however, may vary from being quite specific as to host species to using a broad number of botanical groups. Most lineages use a particular type of secondary host, such as grasses, roots, other woody plants, or herbs. Some aphids specialize on secondary hosts of a particular environmental ecotype. For example, Rhopalosiphum nymphae, water lily aphid, uses aquatic plants in many plant families. Among aphid lineages, nearly all morphs may be winged or wingless, depending on the aphid group, its adaptation to its host(s), or their alternation.
FIGURE 2 Evolutionary development of generalized aphid life cycles. Initially, (A) aphids developed monoecious holocycly on an ancestral woody primary host, where aestivation occurred because sap amino acids were unavailable during summer growth cessation. Next, (B) multiple subfamilies independently evolved dioecious holocycly, where viviparae moved to summer-growing herbaceous secondary hosts but returned to their ancestral host in autumn. In some aphids, (C) secondarily monoecious holocycly developed on the secondary host when the primary host was lost. Often in warm areas, where selection for an overwintering egg is not imposed, some populations of dioecious and secondarily monoecious holocyclic aphids may lapse into (D) facultative anholocycly on their secondary hosts; this condition may become obligate anholocycly if the ability to produce sexuals is lost.
Some aphid lineages have evolved beyond dioecious holocycly to secondary monoecious holocycly (Fig. 2C), by entirely leaving their primary woody host to remain on their secondary herbaceous host and producing overwintering eggs on it. Another important form of year-round residence on the secondary host occurs in warmer climates, where populations do not require an egg for overwintering survival. Under such conditions, otherwise holocyclic dioecious or monoecious populations may lapse facultatively into anholocycly on their secondary hosts (Fig. 2D). If such populations remain anholocyclic long enough, they may eventually evolve into obligate anholocycly by losing the ability to produce sexual morphs, despite undergoing environmental conditions that normally trigger their production. In the U.S. Midwest, the anholocyclic clones of some aphid species are blown, on seasonal winds, south in the fall to the warmer Gulf States and back north in the spring, effectively allowing a passive “migration” to avoid clonal mortality in the northern winter.
APHID BEHAVIOR
Evolutionary selection has dictated efficiency in aphid behaviors as well as the expendability of individuals. To feed proficiently, aphids insert and ratchet their rostrum-borne stylets between plant cells, seldom penetrating any until reaching the phloem sieve tubes to extract sap. The stylets are lubricated by pectinase-containing saliva that both loosens plant cell bonding and forms a stylet sheath that is left behind when the stylets are withdrawn. To cope with a sap diet, aphid guts have specialized groups of cells, mycetomes, containing rickettsialike symbiotic bacteria, mycetocytes, which aid in synthesis of nutrients. These bacteria are passed between aphid generations and have coevolved with, and differentiated between, aphid phyletic lineages.
Morph-specific behaviors promote genetic survival of the individual and its clones. Alatae initially taking flight are attracted to the short wavelengths that predominate in the sky, which they fly toward to optimize dispersion. During descent their preference changes to the longer light wavelengths reflected by plants, especially the yellow hue of senescent plants that are better nitrogen sources. After alighting, they accept a plant for feeding only after briefly probing their rostral tip below the plant’s epidermis to sense the presence of specialized secondary plant compounds that are of no nutritional value, but are specific to their given host. Apterae, in contrast, move only when necessary to procure a better feeding site or avoid pre-dation. Ants may tend some aphid groups in a form of facultative mutualism in which the ants may actively “farm” their aphid “cattle,” moving them among locations. In exchange for the aphid’s sugary honeydew, the ants protect them from predation and parasitism. When stroked by an ant’s antennae, the aptera will raise the tip of its abdomen extruding a honeydew drop, which may be retracted if not accepted by the ant. In the absence of a tending ant, the aphid will revert to its normal flicking of the honeydew drop away with its hind leg or cauda to prevent an accumulation of honeydew from fouling the aphid colony. Generally, aphid groups with elongate siphunculi are less likely to be tended by ants.
Aphids use chemical and sound communication, especially to foil parasites and predators. When molested, aphids exude microdrop-lets of “rans-p-farnesene, an alarm pheromone, from their siphun-cular pores. In response, adjacent aphids quickly drop to the ground to escape. Aphid oviparae use sexual pheromones released from specialized pores on their hind tibiae to attract males. Toxoptera spp. emit audible warning stridulatory sounds to which their aggregation responds. The stridulatory mechanism in this genus consists of a row of short pegs on the hind legs that are rubbed against filelike ridges on the lower abdominal epidermis below the siphunculi.
Some aphids use morph-specific behaviors to wound plants, creating galls and leaf necrosis or distortion, thereby manipulating their host to promote nutrition and protection (Fig. 3 ). Fundatrices of gall-forming species use species-specific patterns of feeding or probing behavior to induce characteristically shaped galls on their specialized hosts. Not only do plant galls provide a protective encasement for aphid development, but aphids of even nongalling species do better on galled tissue, probably because of a local increase in plant nutrients in that tissue. Some non-gall-making species employ phytotoxins to induce leaf distortion or necrosis to similarly promote additional nutrient production by their host.
FIGURE 3 Aphid damage: (A) necrotic feeding damage on pecan, (B) leaf curling on ivy by Aphis hederae f. pseudohederae, (C) conelike galls on spruce by Adelges sp., (D) leaf edge galls on poplar by Thecabius sp., (E) leaf petiole gall on poplar by Pemphigus sp.- gall split showing yellow fundratrix, and (F) leaf galls on manzanita by Tamalia sp.
Aphid social behavior is usually expressed as gregarious-ness within colonies, probably to confer better protection or response to attack. This is usually seen in apterae and nymphs, but occurs in alatae of some species as clustering with tactile contact (e.g., Drepanosiphum platanoides). Some genera of the tribe Cerataphidini of Hormaphidinae have evolved sociality further to produce defensive soldier morphs with enlarged forelegs. These soldiers discriminate between other soldiers and nonsoldiers but do not attack soldiers of their own species. The investment in soldier production by the colony is related to areas needing defense, such as a gall’s nutrient-rich surface.
AGRICULTURAL IMPORTANCE
Aphid damage is among the most serious of agricultural and horticultural problems. A pest aphid species may affect only a very specific crop, a group of related crop hosts (e.g., crucifers), or may be quite polyphagous within and between plant families. Many of the notoriously polyphagous aphid pests represent sibling species complexes that are morphologically identical but differ in karyotype. Generally, such aphid pests comprise anholocyclic clones, or bio-types, that differ in host preferences, the ability to transmit diseases, or resistance to pesticides.
Blackman and Eastop, in Van Emden and Harrington’s 2007 topic, estimate that although about 450 species occur on crops, only about 100 species pose significant economic problems. They list and discuss in detail 14 aphids as the most serious agricultural pests. Thirteen of these are in the Aphidinae, the largest aphid subfamily, which contains a high proportion of herbaceous plant feeders. Of these, Aphis craccivora, Aphis fabae, Aphis gossypii, and Aphis spiraecola are in tribe Aphidini, subtribe Aphidina; Rhopalosiphum maidis, Rhopalosiphum padi, and Schizaphis graminum are in tribe Aphidini, subtribe Rhopalosiphina; and Acyrthosiphon pisum, Diuraphis noxia, Lipaphis pseudobrassicae (sensu Eastop), Macrosiphum euphorbiae, Myzus persicae, and Sitobion avenae are in tribe Macrosiphini. The fourteenth species, Therioaphis trifolii, is in tribe Myzocallidini of subfamily Myzocallidinae (=Calaphidinae sensu Eastop), a group normally found on trees, but in which Therioaphis has diverged on to herbaceous Fabaceae.
Aphids cause damage and lower agricultural yields in several ways. They can build to high population densities, removing plant nutrients, and may damage plants by removing enough sap to cause withering and death. If not washed off, aphid honeydew excrement can build enough on plants to be a growth medium for sooty molds that impair photosynthesis and promote other fungal diseases. Salivary secretions of some aphids are phytotoxic, causing stunting, leaf deformation, and gall formation, which is of particular concern to horticulture. Even if otherwise asymptomatic, aphid-feeding effects may affect plant hormone balances changing host metabolism to their advantage and essentially hijacking the plant’s physiological functions.
The most serious problem posed by aphids is the vectoring of plant viruses. Virus-infected plants often show an aphid-attractive yellowing and have increased free amino acids, so aphids benefit by virus transmission. Stylet-borne viruses, occurring on the aphid’s epidermis, are not aphid specific. They are acquired quickly and transmitted during rostral probing of the plant’s epidermis. These are nonpersistent viruses whose infectiousness is lost when the aphid molts. Circulative viruses, in contrast, live in the aphid’s gut and require an incubation period before successful transmission. They are persistent viruses and an aphid, once infected, remains a vector for life. Circulative viruses have fairly specific virus-aphid-plant linkages and any given virus is transmitted by only one or few aphid species.
APHID CONTROL IN AGRICULTURAL CROPS AND HOME GARDENS
Agricultural control of aphids best uses an integrated pest management (IPM) strategy, where species are identified and tactics reflect allowable tolerances on a crop. Cultivation of aphid-resistant crop varieties is important. Aphids may be monitored using yellow water pans or sticky traps in fields. In some agricultural regions, especially seed-growing areas with plant virus sensitivities, aerial suction trap networks are used to detect alatae and forecast population levels. IPM of aphids minimizes effects on nontarget species (i.e., biological control agents, vertebrates). Tactics include cultural control methods (e.g., minimizing ant populations, using ultraviolet-reflecting films to repel alatae, or interplanting pollen and nectar source plants among crop rows to promote natural enemies). Parasitic wasps or predators can be released for biological control. Effective predators include immature lacewings, aphid midges, and ladybird beetles, all of which voraciously consume aphids but are less likely to disseminate when released than adults. The spores of entomopathic fungi can be used. Aphid growth regulators can be applied by spray to prevent maturation. Chemical poisons, ranging from pyrethroids to toxic organophosphates, should be minimized but may be necessary sometimes. These may be applied as contact sprays or dusts, or as systemic insecticides. Poisons not only hamper biological control agents, but their heavy use promotes the insecti-cidal resistance and secondary resurgence of aphid populations.
In residential settings, nontoxic controls should be emphasized after aphid detection by inspecting congregation sites such as buds, stems, fruits, and leaf undersides. Effective aphid control may simply involve frequently hosing off leaf undersides with water. Safe spray applications involve repellent garlic and water mixtures, or cuticle-disrupting/desiccating insecticidal soaps. Problems from aphid sooty molds under overhanging trees are best controlled by hosing off driveway, patio, and walkway surfaces. Control for aphid galls or leaf distortion can be problematic. Sometimes deciduous trees require the winter application of dormant oil to kill overwintering eggs. Landscape tree species should be carefully selected and placed, considering their aphid pests, because ultimately elimination of the tree may be required to solve the problems.
