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Soybean aphid

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Soybean aphid
Scientific classificationEdit this classification
Domain: Eukaryota
Kingdom: Animalia
Phylum: Arthropoda
Class: Insecta
Order: Hemiptera
Suborder: Sternorrhyncha
Family: Aphididae
Genus: Aphis
Species:
A. glycines
Binomial name
Aphis glycines

Thesoybean aphid(Aphis glycines) is aninsectpestofsoybean(Glycine max) that isexotictoNorth America.[1]The soybean aphid is native toAsia.[2]It has been described as a commonpestofsoybeansinChina[3]and as an occasional pest of soybeans inIndonesia,[4]Japan,[5]Korea,[6]Malaysia,[2]thePhilippines,[7]andThailand.[8]The soybean aphid was first documented in North America inWisconsinin July 2000.[9]Ragsdaleet al.(2004) noted that the soybean aphid probably arrived in North America earlier than 2000, but remained undetected for a period of time.[1]Venette and Ragsdale (2004) suggested that Japan probably served as the point of origin for the soybean aphid's North American invasion.[10]By 2003, the soybean aphid had been documented inDelaware,Georgia,Illinois,Indiana,Iowa,Kansas,Kentucky,Michigan,Minnesota,Mississippi,Missouri,Nebraska,New York,North Dakota,Ohio,Pennsylvania,South Dakota,Virginia,West Virginia,andWisconsin.[10]Together, these states accounted for 89% of the 63,600,000 acres (257,000 km2) of soybean planted in theUnited Statesin 2007.[11]

Life history

[edit]

The soybean aphid possesses aheteroeciousholocycliclife cycle,which means the insect alternates hosts and undergoessexual reproductionfor at least part of its life cycle.[3]Soybean aphidsoverwinteras eggs on their primary hosts,buckthorn(Rhamnusspp.).[1]Eggs can be located near buds or within crevices of branches.[3]With a meansupercoolingpoint of −34°C(−29°F), eggs are well-adapted for surviving cold winters.[12]

In two studies, the quantity of overwintering eggs had a strong positive correlation with the severity of soybean aphidoutbreaksin the following spring.[3][13]

Soybean aphidlife cycle

Eggs begin to hatch intofundatriceswhen temperatures in the spring reach 10 °C (50 °F).[3][citation needed]Colonization of buckthorn by soybean aphids in the spring can lead to curling of leaves and twigs.[3]Near the blooming stage of buckthorn, fundatrices reproduceparthenogeneticallyto giveviviparousbirth toalatae.[3]These winged soybean aphids begin the springmigrationto their secondary host,soybean.[1]Soybean aphids go through approximately 15 generations on soybean, all of which are primarily composed ofapterousfemales produced through viviparous parthenogenesis.[3][10]Each generation passes through 4instarsand can range from 2 to 16 days in length, with higher temperatures increasing development and decreasing generation time.[13]

Soybean plants

Feeding by soybean aphids injures soybean by interfering withphotosyntheticpathways—more specifically, biological mechanisms responsible for restoringchlorophyllto a low energy state are impaired.[14]This restoration process is known as quenching and is important for plants to executelight reactionsproperly. Reduction in photosynthetic capacity of soybean may occur before plants begin to displaysymptomsof injury.[14]

Infestation of soybean aphids on soybean can be classified into three stages.[15]The first stage occurs when alatae migrate to soybean in late May and early June. During this stage, small colonies of soybean aphids appear patchy, occurring on single plants scattered throughout a field.[1]In these early colonies, soybean aphids are typically grouped on tender, young leaves of soybean plants.[16]As the infested plant ages, soybean aphids remain on leaves near the top of the plant. Studies have demonstrated a positivecorrelationexists between upper leafnitrogencontent of soybean and the occurrence of soybean aphids.[13][17]Damage to a soybean plant during this initial stage is a result ofstylet-feeding and can include curling and stunting of leaves and twigs, physiological delays, and underdevelopment ofroottissue.[3][18]However, the relatively low densities of soybean aphids during this stage have been found to have minimal impacts on soybeanyield.[19]

The second stage, or pre-peak stage, can begin as early as late June and is characterized by dramatic increases in densities of soybean aphids.[15]As colonies expand and temperatures increase, soybean aphids move toward lower portions of the soybean plant.[16]The optimal temperature for soybean aphid development occurs between 25 and 30 °C, and exposure to prolonged temperatures of 35 °C (95 °F) decreasesurvival ratesandfecundityof soybean aphids.[20]Extremely high population growth rates can be achieved under optimal conditions, with a colony doubling in size in as few as 1.3 days.[10]

The final stage of infestation by soybean aphids on soybean, or peak stage, begins in mid- to late July and is characterized by very high densities of soybean aphids.[15]As populations grow during this stage, plant damage may become severe. Heavy infestations of soybean aphids may cause plant stunting, distortedfoliage,prematuredefoliation,stunted stems and leaves, reduced branch, pod, and seed numbers, lower seed weight, and underdevelopment of root tissue.[13]Yield losses as high as 50 to 70% have been documented as a result of prolonged exposure to high densities of soybean aphids.[3][13][19]

When populations of soybean aphids increase, a need arises forapteraeto producealateoffspring to seek out new hosts. This can be due to both deteriorating host plant quality and crowding effects.[21]Crowding ofnymphalapterae will not cause them to develop into alate adults.[21]Crowding effects on alatae can induce alate offspring production as well, although alatae are not as sensitive to crowding as apterae.[21]Soybean plants are prevented from becoming super-saturated byemigrationof soybean aphids through alate production, which serves to maintain an equilibrium density of soybean aphids.[22]Decreased body size and lowered fecundity can be induced in soybean aphids when populations reach very high densities.[22]

As host plant quality begins to deteriorate in late August and early September, soybean aphids take on a paler color and experience decreased growth and reproductive rates.[1][3]High densities of soybean aphids during these late plant stages have less of a significant negative impact on soybean yield.[19]During this period of declining temperatures and decreasing rainfall, soybean plants undergosenescencegradually from bottom to top, causing an upward movement of soybean aphids to higher plant tissue.[16]

After going through approximately 15 generations on soybean, soybean aphids begin to transition back to their primary host, buckthorn. A generation of winged females,gynoparae,develop on soybean and leave for buckthorn when mature.[3]Simultaneously, an apterous population of soybean aphids remains on soybean to produce alate male sexualmorphs.[3]Factors that positively affect the production of gynoparae and male alatae include declining host plant quality, shortened day length, and lowered temperatures.[23]

While on buckthorn, gynoparae produce a generation of apterous female sexual morphs (oviparae) that mate with male alatae to produce overwintering eggs.[3]As buckthorn experiences increased feeding pressure by oviparae,volatileemissions from the plant are significantly decreased, possibly serving as adefense mechanismto inhibit further colonization by soybean aphids.[24]Male alatae locate oviparae on buckthorn through two sexpheromonescommonly found in aphid species, (1R,4aS,7S,7aR)-nepetalactol and (4aS,7S,7aR)-nepetalactone, that are emitted by oviparae in a species-specific combination.[24]After mating on buckthorn, oviparae deposit their eggs on the plant. Ragsdaleet al.(2004) proposed that movement from soybean to buckthorn may produce abottleneckeffect that inhibits the ability of soybean aphids to overwinter in great numbers.[1]

Host plant biology

[edit]
Abuckthornplant

More than 100speciesofRhamnusexist worldwide, and most of these species are native totemperateregions of theNorthern Hemisphere.[25]Rhamnusspecies are plentiful inNorth America.[25]Two confirmedRhamnusspecies that supportoverwinteringof soybean aphids in North America arecommon buckthorn(Rhamnus cathartica) of exotic origin andalderleaf buckthorn(Rhamnus alnifolia) ofnativeorigin.[1]Another widespreadRhamnusspeciesof exotic origin inNorth Americaisalder buckthorn(Rhamnus frangula); however, neither matureoviparaenor eggs have been documented on this potential host.[26]

In an experiment to determine alternate primary hosts for soybean aphids, only members of the genusRhamnuswere able to support development of soybean aphids.[25]InAsia,where the soybean aphid is native, dominant primary hosts includeJapanese buckthorn(Rhamnus japonica) andDahurian buckthorn(Rhamnus davurica).[5]One study indicated certain plant species may play a role in bridging colonization ofsoybeanfrom buckthorn.[25]One suchspeciesthat is readily available in early spring isred clover(Trifolium pratense). An experiment further reinforced this relationship by demonstrating that soybean aphids can develop on red clover in a laboratory setting.[1]

The most common secondary host in both Asia and North America for soybean aphids is soybean.[1]Soybean has been cultivated in Asia for 4,000 to 5,000 years and in theUnited Statessince 1904.[13][27]Duet al.(1994) demonstrated that the primary method by which soybean aphids locate soybean is througholfactorychemical signaling.[28]Interference by non-host odors diminished the ability of soybean aphids to locate and colonize soybean.

Deleterious effects of soybean aphids on soybean can be highly variable and are influenced by factors like soybean aphid density, plant stage, plant density, and temperature.[18][19]In addition, soilnutrientconditions within a soybean field may play some role in the development ofinfestationsof soybean aphids. For example, in a laboratory experiment, soybean aphids that fed onpotassium-deficient soybean experienced increasedfecundityand survivorship.[29]Field experiments failed to corroborate this finding. Myerset al.(2005a) hypothesized that potassium-stress in the laboratory may lead to increasednitrogenavailability for soybean aphids.[29]Yield data taken from this experiment showed that potassium-stress in conjunction with infestation by soybean aphids caused significant yield loss.

Specificity for soybean aphids to feed on soybean has been demonstrated by Han and Yan (1995) in an experiment utilizing an electrical penetration graph.[30]While no difference in the amount of time spent probing between soybean and other non-host plants was observed, the ingestion ofphloemby soybean aphids was either greatly reduced or did not happen at all on non-host plants.[30]Nevertheless, some alternate secondary hosts have been observed for soybean aphids. The most widespread of these alternate secondary hosts iswild soybean(Glycine soja), which has been known to support colonies of soybean aphids in Asia.[5]InKoreaand thePhilippines,kudzu(Pueraria montana) andtropical kudzu(Pueraria javanica) have been described as alternate secondary hosts, respectively.[18]

Virus transmission

[edit]

Soybean aphids may indirectly affect plant health through viral transmission.Virusesspread by soybean aphids are typicallyvectorednon-persistently, which allows for disease transmission in the first moments ofstyletpenetration.[31]Non-persistent transmission does not limit viruses vectored by soybean aphids to soybean, but rather to any plant thatalatesoybean aphids contact and probe with their stylets for a brief period of time.[32]Unlike stationaryapterae,only alatae have been shown to transmit viruses between plants.[33]Incidence of non-persistently transmitted viruses has been shown to increase when flight activity of the vector is high, leading to the belief that the risk of virus transmission by soybean aphids may increase during times of highdispersal,such as the end of the peak stage.[31]

InChina,the most important virus vectored by the soybean aphid isSoybean mosaic virus,which can cause yield loss and decreased seed quality.[13]This virus is also found inNorth Americaand has been demonstrated as being vectored by the soybean aphid in field studies.[34]In addition to Soybean mosaic virus, the soybean aphid is capable of transmittingSoybean stunt virus,Soybean dwarf virus,Abaca mosaic virus,Alfalfa mosaic virus,Beet mosaic virus,Tobacco vein-banding virus,Tobacco ringspot virus,Bean yellow mosaic virus,Mungbean mosaic virus,Peanut mottle virus,Peanut stripe poty virus,andPeanut mosaic virus.[13][35]

Host plant resistance

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Several varieties ofsoybeanhave demonstratedresistanceto the soybean aphid. Resistance may be conferred byantibiosis,antixenosis,ortolerance.In some instances, such as with the soybean cultivars 'Dowling', 'Jackson', and 'Palmetto', resistance to the soybean aphid results from a combination of both antibiosis and antixenosis.[36]In the 'Dowling' cultivar, resistance is conferred by a single dominantgene(Rag1).[36]Soybean plants that are resistant to the soybean aphid can cause both reducedfecundityandlongevityin soybean aphids.[37]In the case of antibiosis, certain life stages of the soybean aphid may be more susceptible than others. For example,nymphshave higher rates ofmetabolismthan other life stages, ingest morephloem,and are thus exposed to larger quantities of antibiotic compounds.[37]Expression of antibiotic factors in resistant soybean plants that negatively affect soybean aphids has been shown to remain constant throughout the growing season, remaining unaffected by the physiological maturity of the plant.[37]Colonization of resistant soybean cultivars can vary between years depending upon the level of infestation, with resistant plants showing lower levels of resistance in years with significant levels of soybean aphid infestation.[38]Physical characteristics of soybean, such as densepubescence,have thus far proven incapable of reducing colonization by soybean aphids.[39]

Natural enemies

[edit]
Harmonia axyridisfeeding on soybean aphids

InAsia,the soybean aphid experiences pressure from over 30 species ofpredators,8 species ofparasitoids,and some fungalpathogens.[40]InIndonesia,where the soybean aphid is considered an occasionalpest,evidence indicates the use ofinsecticidesto control soybean aphids may not always be necessary due to suppression of the insect to subeconomic densities bynatural enemiesalone.[41]InNorth America,the dominant natural enemies insoybeanare generalist predators.[42][43][44][45][46][47][48]Exclusion cage experiments have provided evidence that predators can play an important role in suppression of the soybean aphid.[42][43][44][45][47][48]Impacts from predators include both the ability to suppress colony establishment early in the season as well as respond to increased densities of soybean aphids late in the season.[42][43][49]

One of the most important predators of soybean aphids in North America is theinsidious flower bug(Orius insidiosus(Say)). The insidious flower bug has its greatest impact on early to mid-season populations of soybean aphids and is often able to keep soybean aphid densities low.[50][51]Foxet al.(2004) hypothesized that the impact from this predator early in the season could be attributed to small plant size and sparse canopies, which aid the insidious flower bug by reducingforagingtime and decreasing the number of places soybean aphids can hide (i.e., enemy-free space).[42]In addition,synomonesreleased by soybean after being colonized by soybean aphids may aid the insidious flower bug in host location.[52]When populations of soybean aphids reach very high densities, top-down pressure exerted by the insidious flower bug may fail to suppress colony growth of soybean aphids.[51]

Another group of predators that plays a key role in suppression of populations of soybean aphids in North America islady beetles(Coccinellidae spp.).[44][46][53]Some prevalent species in soybean include the twospotted lady beetle (Adalia bipunctataL.), the sevenspotted lady beetle (Coccinella septempunctataL.), the spotted lady beetle (Coleomegilla maculataDe Geer), the polished lady beetle (Cycloneda munda(Say)), the multicolored Asian lady beetle (Harmonia axyridis(Pallas)), the convergent lady beetle (Hippodamia convergensGuérin-Méneville), and the thirteen spotted lady beetle (Hippodamia tredecimpunctataL.).[40][44][46][53][54]

Green lacewinglarva

Evidence suggests that populations of lady beetles can respond to increases in populations of soybean aphids in soybean.[55]In addition, increases in populations of lady beetles have the ability to inhibit colony growth of soybean aphids throughout the growing season.[53]Asgeneralistpredators, lady beetles are able to feed on alternatepreywhen soybean aphids are at low densities.[40]Other characteristics of lady beetles that are advantageous in times of soybean aphid scarcity include developmental delays of certain life stages, decreased body weights, and reducedclutchsizes.[40]One of the most competitive lady beetles in North America, the multicolored Asian lady beetle, is of exotic origin. When soybean aphids are plentiful, an adult multicolored Asian lady beetle has the capacity to consume 160 soybean aphids per day.[56]

Other foliar-foraging predators that are present North American soybean fields that may play a role in suppression of soybean aphid populations includegreen lacewings(Chrysoperlaspp.),brown lacewings(Hemerobiusspp.),damsel bugs(Nabisspp.),big eyed bugs(Geocorisspp.),spined soldier bugs(Podisus maculiventris(Say)),hover flies(Syrphidae spp.), and theaphid midge(Aphidoletes aphidimyza(Rondani)).[40][42][44][46][53][57]Another group of predators that are present in soybean fields isground beetles(Carabidae spp.); however, field experiments have shown limited to no impact from these predators on populations of soybean aphids due to the fact that ground beetles rarely scale soybean plants for prey.[49]While parasitoids of the soybean aphid have a large impact on colonies in Asia—Lysiphlebia japonica(Ashmead) can have a soybean aphid parasitism rate as high as 52.6% inChina—parasitoids are thought to exert only minimal pressure on soybean aphids in North America.[40][58]

Management

[edit]

The use ofinsecticidesto control populations of soybean aphids in soybean is the most effective management tactic inNorth America.[59]Insecticides available to soybean producers for controlling soybean aphids include both foliar-applied treatments and seed-applied treatments.[13][60][61]Although seed-applied treatments have proven to be a convenient delivery method for insect control, studies have experienced inconsistent results regarding theirefficacyagainst the soybean aphid.[62]Management decisions should be made with an understanding of soybean aphid life history and sound scouting practices rooted in the principles ofintegrated pest management.[59][63]

The currenteconomic thresholdfor soybean aphids states that an insecticide application is warranted when soybean aphid densities reach 250 soybean aphids per plant, 80% of sampled plants are infested, the population is currently increasing, and fewnatural enemiesare observed in the field.[63]This recommendation is only valid from the R1 (beginning bloom) to R5 (beginning seed) growth stages and is based on aneconomic injury levelof 674 soybean aphids per plant. Due to the clumped spatial distribution of soybean aphids, Onstadet al.(2005) recommend that 50 plants should be sampled within a field to attain an accurate representation of densities of soybean aphids.[64]Soybean producers can choose from a variety of foliar insecticides from thecarbamate,pyrethroid,andorganophosphatechemical families to control soybean aphids.[59][65]

Evidence indicates that foliar insecticide applications can reducesymptomsassociated with soybean aphid infestations, including curled leaves, shortened stems, stunted plants, and prematuredefoliation.[66]Foliar insecticide applications can also prevent yield loss associated with high densities of soybean aphids.[67][68]However, some risks are associated with the use of foliar insecticide applications, especially if integrated pest management principles are abandoned. A single, well-timed application may not sufficiently control soybean aphids and prevent yield loss, especially if large quantities of soybean aphids are surviving on lower leaves.[59]Foliar insecticide applications can work detrimentally ifnontarget effectsare experienced, such as the unintended death of beneficialnatural enemies.[54]

Although foliar pyrethroid insectides are the current standard for soybean aphids, in 2015 in Minnesota, pyrethroid resistance was discovered. Other cases were found in 2016 in Iowa, North Dakota, South Dakota and Manitoba.[69]

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