Abstract

The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is a significant insect pest of soybean in the north-central region of the United States and southern Canada, and if left untreated can reduce yield value by $2.4 billion annually. The soybean aphid is native to eastern Asia, where soybean was first domesticated, and was first detected in the United States in 2000. It quickly spread within 4 years of its discovery across 22 states and three provinces of Canada. Heavy infestations can result in a covering of sooty mold, yellow and wrinkled leaves, stunted plants, and aborted pods leading to significant yield loss of 40% or more. It can also transmit plant viruses such as Soybean mosaic virus and Alfalfa mosaic virus. The soybean aphid has a complex life cycle that involves different physical forms, sexual stages, and two host plant species-soybean and buckthorn (the overwintering host). Plant nutrition, natural enemies, climate, and weather all affect population growth rate, but the typical population doubling time is ≈6-7 days. Though at present management is primarily through broad-spectrum insecticides, biological control has a significant impact on soybean aphid population growth, and aphid-resistant soybean varieties are becoming increasingly available.

The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is a significant insect pest of soybean in the north-central region of the United States, and if left untreated can reduce yield by $2.4 billion annually (Song et al. 2006). The soybean aphid is an invasive pest that was first detected in the United States in 2000 (Alleman et al. 2002), and quickly became the dominant insect pest in soybean throughout the Midwest, which had previously experienced relatively little regionwide pressure from other insect pests of this crop. Soybean aphid populations have the potential to increase rapidly, and heavy infestations can stunt plant growth and development, leading to significant yield loss.

This article reviews the invasion history and distribution of the soybean aphid, as well as its biology and the feeding damage it causes. Biological control, host plant resistance, and other factors affecting soybean aphid populations will also be discussed.

Invasion History and Distribution

The soybean aphid is native to eastern Asia, where soybean was first domesticated. Its Asian range includes China, Indonesia, Japan, Korea, Malaysia, the Philippines, Taiwan, and Thailand (Wang et al. 1994, Van den Berg et al. 1997, Blackman and Eastop 2000). Although soybean aphid was noted as an important pest of soybean in Asia by Kogan and Turnipseed (1987), and a sporadic pest in China (Wang et al. 1994), its impact in the United States has been markedly greater than that within its native range (Liu et al. 2004, Ragsdale et al. 2004, Wu et al. 2004). It is not surprising for invasive species, like soybean aphid, to have notably different population levels within their exotic ranges (Elton 2000). The first specimens in the United States were confirmed on soybean, Glycine max (L.), in Wisconsin in 2000 (Alleman et al. 2002), and quickly spread within 4 years of its discovery across 22 states and three provinces of Canada (Hunt et al. 2003, Venette and Ragsdale 2004). Its establishment across a large area of the soybean growing region of the United States was facilitated by the previous establishment and spread of its overwintering host, common buckthorn, Rhamnus cathartica L. (Ragsdale et al. 2004). Buckthorn was previously established in the United States before soybeans were widely cultivated and can be found throughout the north-central region, especially in the upper-Midwest (Ragsdale et al. 2004). The rapid population expansion of soybean aphid suggests high mobility and few limits to migration and gene flow (Ragsdale et al. 2004, Venette and Ragsdale 2004).

The soybean aphid is a pest predominantly in middle to high latitudes in the Midwestern United States and the provinces of Manitoba, Ontario and Québec, Canada. It is seldom found south of Kansas, Missouri, Kentucky, or Virginia. In southern states it can sometimes be confused with cotton aphid (Aphis gossypii Glover), which can occur on soybean in that region.

Description

Soybean aphid was first described by Matsumura (1917), but more defined body characters were published by Voegtlin et al. (2004a). In soybean, wingless soybean aphids are pear-shaped, 1/16th inch (1.5 mm) long, and range from pale yellow to lime green in color (Fig. 1) (though on late-season soybeans, some aphids may be pale and smaller in appearance). Adults have dark-tipped cornicles ("tailpipes" ) at the posterior end (Fig. 1). Winged soybean aphids have a dark thorax (central body segment) and cornicles, and transparent wings that extend well past the abdomen (Fig. 2).

Fig. 1

Soybean aphids range from yellow to pale green. Dark-tipped cornicles ("tailpipes" ) are found on the abdomens of adults. Note the female in the upper left giving live birth to another female. Photo by Roy Scott.

Fig. 1

Soybean aphids range from yellow to pale green. Dark-tipped cornicles ("tailpipes" ) are found on the abdomens of adults. Note the female in the upper left giving live birth to another female. Photo by Roy Scott.

Fig. 2

Winged soybean aphid (left) and an immature soybean aphid with developing wing buds (right) that will be a winged aphid upon maturation. Photo by Roy Scott.

Fig. 2

Winged soybean aphid (left) and an immature soybean aphid with developing wing buds (right) that will be a winged aphid upon maturation. Photo by Roy Scott.

Feeding and Injury

Soybean aphids have piercing-sucking mouthparts that are used to feed on phloem sap. Although soybean aphid will feed on leaves, stems, and pods, they are most often found on the undersides of leaves. The distribution of soybean aphids on the plant varies during the growing season (McCornack et al. 2008). Early in the season, aphids are more likely to be found on newly expanding trifoliate leaves (Fig. 3). As the season progresses and the plant matures, soybean aphids are more likely to be found lower in the canopy, on leaves that are attached to nodes further from the terminal bud. Soybean aphids may occur in low density of only a few aphids per plant, or may form large, persistent colonies of several hundred or even thousands per plant.

Fig. 3

Soybean aphids infesting a young soybean trifoliate. Photo by Roy Scott.

Fig. 3

Soybean aphids infesting a young soybean trifoliate. Photo by Roy Scott.

Soybean aphid colony size and infestation levels are influenced by ecological factors such as temperature and biological control (discussed below), but also by their nutritional feeding environment. Like most aphids, soybean aphid growth is limited by the nutritional quality of its host plant. The limiting component of the soybean aphids diet is often nitrogen, which has a relatively low concentration within the phloem. Studies have linked the population growth rate of the soybean aphid to nitrogen availability in soybeans. Population growth increases in plants with increased nitrogen concentration in phloem, such as plants growing in fields with potassium-deficient soils (Myers et al. 2005, Walter and DiFonzo 2007, Noma et al. 2010), or growth stages of the plant when nitrogen is more readily available.

The injury caused by phloem feeding insects like soybean aphids may go undetected without close visual inspection, and feeding damage may become readily apparent only after large, yield-reducing populations have developed. At moderate infestation levels (i.e., <50 aphids per leaflet), soybean aphid can significantly reduce gas exchange and negatively affect photosynthetic rates (Macedo et al. 2003). Heavily infested plants are stunted (Fig. 4) and may be covered with dark sooty mold growing on the sugary excretions or “honeydew” that aphids produce. Heavy infestations can result in yellow and wrinkled leaves, stunted plants and aborted pods (Lin et al. 1993) leading to significant yield loss of 40% or more (Ragsdale et al. 2007). Large infestations can negatively impact seed quality and size, pod number, plant height, and photosynthesis (Beckendorf et al. 2008).

Fig. 4

A soybean plant (left) stunted by heavy aphid pressure (thousands per plant). The plant on the right contains the Rag1 aphid resistance gene. Photo by Roy Scott.

Fig. 4

A soybean plant (left) stunted by heavy aphid pressure (thousands per plant). The plant on the right contains the Rag1 aphid resistance gene. Photo by Roy Scott.

Soybean aphid, like many aphids, can transmit plant viruses (Clark and Perry 2002). It has been shown to transmit both Soybean mosaic virus and Alfalfa mosaic virus to soybean (Hill et al. 2001). It may also vector plant pathogens, typically nonpersistent viruses, to other temporally visited crops, such as Alfalfa mosaic virus and Cucumber mosaic virus in snap bean, Phaseolus vulgaris L. (Gildow et al. 2008), and Potato virus Y in potato, Solanum tuberosum L. (Davis et al. 2005). Soybean aphid is able to transmit several other viruses (Wang et al. 2006), but its economic importance as a vector in North American soybean and other crops is still to be determined.

Biology and Life Cycle

The life cycle of the soybean aphid in the United States is similar to its native range (Wu et al. 2004). Like many aphid species, it has a complex life cycle that involves different physical forms (morphs) and two types of host plants. It is heteroecious (host-alternating) and holocyclic (generates sexual morphs with an egg that overwinters) (Ragsdale et al. 2004).

Through the spring and summer, soybean aphids reproduce asexually (without mating) on soybean, which is actually considered the secondary host; the aphids are all female and give live birth (Fig. 1) to all-female offspring. These features give soybean aphids the ability to increase very rapidly when conditions are favorable. The optimal developmental temperature is 82°F/27.8°C (McCornack et al. 2004). The upper developmental temperature is 94.8°F/34.9°C, and the lower developmental temperature is 47.5°F/8.6°C (McCornack et al. 2004). In general, aphid reproduction is affected by the growth stage of the host plant, with greater rates of reproduction during vegetative and late reproductive stages when senescence occurs (Dixon 1985), but these plant growth stage effects do not prove to be strong (Rutledge and O' Neil 2006, Rhainds et al. 2010). Under favorable conditions (e.g., 77–86°F/25–30°C), soybean aphids are highly reproductive and can double in population size in as little as 1.5 to 2 days (McCornack et al. 2004). However, in the field where aphids experience multiple forms of mortality (weather, natural enemies, diseases) population doubling time is typically 6–7 days (Ragsdale et al. 2007). During the entire growing season, soybean aphid has ≈15 asexual generations on soybean and three or more generations on the primary host (buckthorn, see below), which is equivalent to the 18–20 generations that were recorded in China (Li et al. 2000).

During midsummer population increase, many wingless aphids will produce winged offspring that can colonize other areas within-field or can disperse great distances on the wind in mid- to late-summer (Hodgson et al. 2005, 2009), and later-season influx of aphids into fields may be an important contributing factor in outbreaks. Factors that typically contribute to aphids producing migrants in other systems include plant nutrition, crowding (Dixon 1985), temperature (Johnson and Birks 1960), plant phenology (Howard and Dixon 1992), and the presence of beneficial insects (Roitberg et al. 1979). Several of these factors are currently under investigation for soybean aphid.

At the end of the soybean growing season soybean aphids migrate in September and October back to their primary host plant, common buckthorn (Rhamnus cathartica L.) (Fig. 5), a deciduous shrub common in shelterbelts and woods in northern states. Buckthorn is a critical part of the soybean aphid life cycle; without this plant, they cannot spend the winter in a given area. R. cathartica is most widely infested, though it may also overwinter on Rhamnus alnifolia L‘Héritier, among other Rhamnus species (Voegtlin et al. 2004b, 2005; Hill et al. 2010). Common buckthorn is itself an invasive species and is widespread across North America, particularly north of 41°N latitude where plant densities of >10,000/acre are known to occur (Ragsdale et al. 2004). It often appears as a shrub around 8 feet/2.4 m high but can also resemble a small tree up to 25 feet/7.6 m tall. It has gray bark, and glossy dark green leaves with curved veins and notched edges (Fig. 5).

Fig. 5

Common buckthorn (Rhamnus cathartica). (a) Leaves have toothed edges and curved veins. (b) Plants are shrub-like and often occur in undergrowth. Photos by Kelley Tilmon.

Fig. 5

Common buckthorn (Rhamnus cathartica). (a) Leaves have toothed edges and curved veins. (b) Plants are shrub-like and often occur in undergrowth. Photos by Kelley Tilmon.

The fall migration of soybean aphids to buckthorn is regulated by photoperiod and temperature. Winged females (gynoparae) leave soybean in search of buckthorn, where they feed and deposit a cohort of wingless, sexual females (oviparae). Winged males from soybean seek the oviparae on buckthorn, where mating occurs, followed by oviposition. Overwintering eggs are deposited along buckthorn buds (Fig. 6) (Ragsdale et al. 2004).

Fig. 6

A newly laid soybean aphid egg (green) and an older egg (black) at the base of a buckthorn bud. Photo by Robert O' Neil.

Fig. 6

A newly laid soybean aphid egg (green) and an older egg (black) at the base of a buckthorn bud. Photo by Robert O' Neil.

The overwintering egg is cold-hardy and can survive temperatures as low as −29°F/−34°C (McCornack et al. 2005). Eggs suffer significant mortality on buckthorn, likely because of a combination of abiotic and biotic factors including predators. Survivors hatch during spring and three or more generations develop on buckthorn (Welsman et al. 2007, Bahlai et al. 2008). During the time when soybeans germinate, colonies on buckthorn produce winged females, which colonize soybeans in the early vegetative growth stage (V1-V5) in late spring/early summer (Bahlai et al. 2008). Soybean fields in close proximity to buckthorn may be at greater risk of early infestation (Bahlai et al. 2010); however, soybean fields distant from buckthorn are also at risk of secondary infestations occurring later in the growing season.

Biological Control

Field studies of soybean reveal a diverse community of natural enemies, which help suppress soybean aphid colonization and population growth. These natural enemies include ladybeetles, lacewings, pirate bugs, predatory flies, and entomopathogenic (insect disease-causing) fungi (Rutledge et al. 2004, Nielsen and Hajek 2005, Mignault et al. 2006, Brewer and Noma 2010) (Fig. 7). The community of insect predators within soybean has apparently been altered by the arrival of the soybean aphid, and now includes more species that focus on aphids (Schmidt et al. 2008). Included in this community is the multicolored Asian ladybeetle, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) (Fig. 7a, b), which contributes to biological control of soybean aphid in its native range (Van den Berg et al. 1997), and is one of the dominant soybean aphid predators in the United States (Gardiner et al. 2009a, 2009b).

Fig. 7

Many predatory insects help provide background suppression of soybean aphids. (a) Asian ladybeetle adults range in color from pale orange-yellow to orange-red, and vary greatly in the number of spots. A pattern of black dots resembling the letter “M” behind the head is typical. Photo by Bill Ree, Bugwood.org (b) Asian ladybeetle larva. Photo by Allan Knutson, Bugwood.org (c) Green lacewing adult. Photo by Sonya Broughton, Bugwood.org (d) Green lacewing larva. Photo by USDA-ARS (e) immature Orius sp. bug feeding on a soybean aphid. Photo by Robert O' Neil.

Fig. 7

Many predatory insects help provide background suppression of soybean aphids. (a) Asian ladybeetle adults range in color from pale orange-yellow to orange-red, and vary greatly in the number of spots. A pattern of black dots resembling the letter “M” behind the head is typical. Photo by Bill Ree, Bugwood.org (b) Asian ladybeetle larva. Photo by Allan Knutson, Bugwood.org (c) Green lacewing adult. Photo by Sonya Broughton, Bugwood.org (d) Green lacewing larva. Photo by USDA-ARS (e) immature Orius sp. bug feeding on a soybean aphid. Photo by Robert O' Neil.

Natural enemies cause significant mortality of soybean aphid. Several field studies have demonstrated the contributions of existing communities of natural enemies to soybean aphid suppression (Fox et al. 2004; Rutledge and O' Neil 2005; Costamagna and Landis 2006, 2007). In the absence of predation, soybean aphid population growth is significantly faster (2–7 times) (Costamagna and Landis 2006). Prophylactic application of broad-spectrum insecticides (Ohnesorg et al. 2009) or fungicides (Koch et al. 2010) has the potential to ultimately exacerbate aphid pressure or cause secondary outbreak of other pests such as spider mites by removing the natural enemies that often keep pest populations in check. Conversely, management practices that encourage the recruitment and preservation of natural enemies in soybean have the potential to provide future conservation biological control strategies (Brewer and Noma 2010).

Landscape ecology can have a significant impact on biological control of soybean aphid. The soybean aphid is typically a pest of soybeans in areas where the crop is grown in large monocultures. This setting can influence the insect predators that provide biological control. In areas where the landscape is comprised mostly of corn and soybeans, the impact of insect predators will be lower than in regions where there is more landscape diversity (Gardiner et al. 2009a). Soybean fields located in landscapes that have a greater amount of perennial habitat are more likely to have a greater abundance of ladybeetles (Gardiner et al. 2009b). Such habitats include woodlots, where important predators like the multi-colored Asian ladybeetle overwinter. Noma et al. (2010) found that landscapes with more diverse land cover tend to have lower aphid populations. Soybean fields in landscapes comprised of grassland habitats and annual crops are likely to have a lower density of natural enemies and, subsequently, less biological control. Landis et al. (2008) have suggested that as more land is used for corn production, the current level of soybean aphid biological control may decline, and Noma et al. (2010) found that habitats more dominated by corn and soybean were associated with greater soybean aphid populations.

Though soybean aphid can be heavily impacted by the natural enemies that already exist in the United States, as an invasive species it is also a candidate for classical (importation) biological control. Invasive species often have higher populations in their introduced ranges than in their native ranges; in part this is related to an escape from natural enemies, which are typically less abundant for a given pest across its introduced range than in its native range (Colautti et al. 2004). Though surveys of natural enemies in the United States reveal a rich community of natural enemies, parasitoids—a type of parasitic insect that is often nearly as large as its host and can specialize on particular prey species—have been notably lacking from this community (Rutledge et al. 2004, Kaiser et al. 2007, Noma and Brewer 2008, Schmidt et al. 2008,).

Parasitoids that attack soybean aphids are an important part of the community of predators that suppress soybean aphid in China (Liu et al. 2004); however, it is not uncommon for a newly introduced pest insect to arrive without its specialist natural enemies. A classical biological control program, whose goal is to introduce parasitoid species from the native range that specialize on soybean aphid, is underway. One particular species, Binodoxys communis (Gahan) (Hymenoptera: Braconidae) (Fig. 8) has undergone intense scrutiny for environmental impact, host specificity, and ecological interactions with soybean and other aphids (Wyckhus et al. 2007a, 2007b, 2008, 2009). Based on these studies, B. communis received federal approval for release in the United States in 2007. Releases of B. communis in the Midwest are on-going, though their impact on soybean aphid has not been measured, and depends in large part on the ability of populations of the parasitoid to establish and spread within the new range. Additional candidate species are in quarantine and may be released in the future (Heimpel et al. 2004).

Fig. 8

Binodoxys communis, a specialist parasitoid imported from Asia for biological control of soybean aphid. (a) Adult parasitoid, (b) “mummies” the pupal form of the parasitoid inside the killed aphid' s body. Photos by Roy Scott.

Fig. 8

Binodoxys communis, a specialist parasitoid imported from Asia for biological control of soybean aphid. (a) Adult parasitoid, (b) “mummies” the pupal form of the parasitoid inside the killed aphid' s body. Photos by Roy Scott.

Host Plant Resistance and Biotypes

Aphid-resistant varieties have the potential to augment natural enemies by reducing insecticide load, in addition to serving as important management tools in their own right. Host-plant resistance in the form of both antibiosis (reduced survival and number of offspring) and antixenosis (nonattractive or repellent plants) to the soybean aphid have been found (Hill et al. 2004a, 2004b; Mensah et al. 2005; Mian et al. 2008a; Zhang et al. 2009). Molecular mapping is ongoing (Li et al. 2007, Mian et al. 2008b, Zhang et al. 2009), but at least four genes have been identified: Rag1 (Hill et al. 2006a, 2006b), Rag2 (Mian et al. 2008b), and rag3 and rag4 (Zhang et al. 2009). [Capital letters indicate a dominant trait and lower case letters indicate a recessive trait.] Rag1 (an abbreviation for Resistance to Aphis glycines gene 1), is a single-gene source of antibiosis developed at the University of Illinois. It significantly reduces aphid populations compared with susceptible controls (Fig. 4) (Hill et al. 2004b, 2006a, 2006b). Rag1 soybean lines first became commercially available in the United States on a limited basis in 2009; varieties containing additional resistance genes are likely to follow.

Despite the promise of aphid-resistant varieties, it should be noted that Rag1-containing soybeans are not aphid-free, and economically relevant populations sometimes occur. Biotypes have already been identified which can overcome Rag1 and Rag2 resistance (Kim et al. 2008, Hill et al. 2010) as well as a yet-unnamed source of resistance (Michel et al. 2010). How quickly and to what extent biotypes will arise that significantly limit the usefulness of host plant resistance is not yet known, and relates to the invasion history and genetic diversity of the soybean aphid. One consequence of the fact that soybean aphid is an invasive species is a possible reduction in its genetic variability because of a small founder-population. It is not clear how many times the soybean aphid has invaded the United States and how much genetic diversity was present in the invasion(s). Michel et al. (2009) observed a limited amount of genetic diversity in soybean aphids in North America in 2008, 8 years after the first observations of the soybean aphid. Nonetheless, the appearance of biotypes indicates that the genetic diversity to overcome resistant varieties is present to at least some extent.

Integrated Pest Management

Though natural enemies can have a significant impact on soybean aphid population growth (Costamagna and Landis 2006, Noma and Brewer 2008) and host plant resistance is an emerging tool, insecticides are currently the most-used control method for soybean aphid. Before the arrival of the soybean aphid, very little insecticide was used on soybean for insect pests in the north-central region (Fernandez-Cornejo and Jans 1999). In response to soybean aphid, growers have dramatically increased the use of insecticides for soybean production (USDA-NASS; www.nass.usda.gov), in some cases spraying up to three times in outbreak years, usually with broad-spectrum insecticides. Insecticides from multiple classes (organophosphates, pyrethroids, neonicotinoids) are effective for rapid soybean aphid control, but are most profitably used in an Integrated Pest Management (IPM) program based on scouting and the use of economic thresholds to guide application decisions. Significant field-based research has demonstrated that IPM strategies can limit yield loss while preventing unnecessary input-costs (Ragsdale et al. 2007, Johnson et al. 2009). A great deal of research has been conducted on the scouting and management of soybean aphid, which will be comprehensively reviewed in a separate article on consensus-based pest management recommendations, to appear at a later date in the Journal of Integrated Pest Management.

We wish to acknowledge the considerable investment by state soybean checkoff programs, the North Central Soybean Research Program, and the many federal and other funding programs and Agricultural Experiment Stations, and the hard work of our colleagues; all of which have allowed a large amount of useful information to be gathered about this invasive pest in a relatively short period of time.

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