**2. Hemipteran pests of soybean**

The soybean aphid, various stink bug species and kudzu bug are the major Hemipteran pests of soybean (Figure 1). Although soybean aphid and stink bugs share basic features of Hemi‐ pteran insects, there is much evolutionary divergence between them, their suborders having diverged more than 250 million years ago [9]. Aphids belong to the suborder Homoptera which have uniform, membranous forewings and hindwings. In homopteran insects, wings are held roof-like over their abdomen. Stink bugs belong to suborder Heteroptera having forewings that are leathery basally and membranous distally, in contrast to membranous hindwings. In Heteroptera, wings are folded flat over the abdomen [10]. Stink bugs can also be identified by five-segmented antennae and a conspicuous scutellum [10].

#### **2.1. Soybean aphid**

The soybean aphid is a recent invasive species in North-America [4,5,11]. This species was first detected during the summer of 2000 and is believed to have been introduced from its native Asian range [11,12]. Soybean aphid is a pest of significant economic importance as it can cause up to 58% yield losses in soybean [13]. Losses due to yield have been estimated to be \$2.4 billion annually [14-15].

stink bug, *Nezara viridula (L.)*; green stink bug*, Acrosternum hilare* (Say); brown stink bug, *Euschistus servus* (Say)] constituted the stink bug complex that attacked soybean crop in southern US [6,17]. Amongst these, *N. viridula* is the most abundant [18] which has caused the most severe damage to the field crop [17]. In more northern latitudes, the relative abundance of *A. hilare* is higher compared to that of *N. viridula* [6]. During the last decade, redbanded stink bug, *Piezodorus guildinii* (Westwood), and brown marmorated stink bug (BMSB), *Halyomorpha halys* (Stål) have established themselves as important members of stink bug complex that attack soybean in the US [7, 19,20]. From 1960 onwards, the redbanded stink bug has been detected in US soybean but without causing any economic damage. However during last decade, redbanded stink bug infestations have reached above the threshold levels. By 2009, it was the most serious stink bug species attacking soybean in southern US [21, 22]. The BMSB is native to North and South Korea, Japan, China [23] and is invasive in North America and Europe. In US, BMSB has been confirmed as pest of soybean crop with a high damaging potential [24, 25]. Although not in the Pentatomidae, the kudzu bug (Plataspididae: *Megacopta cribraria*) is another recent invasive pest, first detected in Georgia in 2009 [26] and has now spread to 8 southeastern states of US [8]. It is known to feed on both kudzu and soybean, and damage on

**Figure 1.** Approximate distribution of the main, invasive Hemipteran pests of soybean. For BMSB, shaded range is

Developing Host-Plant Resistance for Hemipteran Soybean Pests: Lessons from Soybean Aphid and Stink Bugs

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where damage is heaviest, \* represent states where detection has been observed.

soybean can be quite severe [27].

The biology of soybean aphid in North-America has been reviewed recently [4,5]. In general, it is a typical holocyclic (asexual and sexual reproduction) heterecious (alternates between 2 hosts) aphid species. In autumn, sexual reproduction occurs on its primary host, buckthorn (*Rhamnus* spp.), and the resulting eggs undergo overwintering. The following spring, the eggs hatch, and the fundatrices (i.e. stem mothers) begin to produce female clones. After 2-3 asexual generations, winged females are formed that disperse to emerging soybean, where about 15 additional asexual generations occur, and when damage to soybean is most severe. Upon soybean maturity, sexual forms are formed and migrate back to buckthorn.

#### **2.2. Stink bugs**

In Hemiptera, stink bugs are in the family Pentatomidae. The name stink bug is attributed to the malodorous substance they emit for defense [16]. In the past, three species [southern green Developing Host-Plant Resistance for Hemipteran Soybean Pests: Lessons from Soybean Aphid and Stink Bugs http://dx.doi.org/10.5772/54597 21

[4], and the BMSB has already been detected in 38 US states since first being seen in Pennsyl‐

Both soybean aphid and stink bug belong to order Hemiptera which also includes other economic pests such as whiteflies and leafhoppers. To minimize the damage by Hemipteran pests, host-plant resistance in soybean cultivars should constitute an integral part of an integrated pest management (IPM) program. In the current chapter, we attempt to review the recent research advances made on soybean resistance to Hemipteran pests. In the light of various challenges to manage Hemipteran pests, we have proposed strategies for successful

The soybean aphid, various stink bug species and kudzu bug are the major Hemipteran pests of soybean (Figure 1). Although soybean aphid and stink bugs share basic features of Hemi‐ pteran insects, there is much evolutionary divergence between them, their suborders having diverged more than 250 million years ago [9]. Aphids belong to the suborder Homoptera which have uniform, membranous forewings and hindwings. In homopteran insects, wings are held roof-like over their abdomen. Stink bugs belong to suborder Heteroptera having forewings that are leathery basally and membranous distally, in contrast to membranous hindwings. In Heteroptera, wings are folded flat over the abdomen [10]. Stink bugs can also be identified by

The soybean aphid is a recent invasive species in North-America [4,5,11]. This species was first detected during the summer of 2000 and is believed to have been introduced from its native Asian range [11,12]. Soybean aphid is a pest of significant economic importance as it can cause up to 58% yield losses in soybean [13]. Losses due to yield have been estimated to be \$2.4 billion

The biology of soybean aphid in North-America has been reviewed recently [4,5]. In general, it is a typical holocyclic (asexual and sexual reproduction) heterecious (alternates between 2 hosts) aphid species. In autumn, sexual reproduction occurs on its primary host, buckthorn (*Rhamnus* spp.), and the resulting eggs undergo overwintering. The following spring, the eggs hatch, and the fundatrices (i.e. stem mothers) begin to produce female clones. After 2-3 asexual generations, winged females are formed that disperse to emerging soybean, where about 15 additional asexual generations occur, and when damage to soybean is most severe. Upon

In Hemiptera, stink bugs are in the family Pentatomidae. The name stink bug is attributed to the malodorous substance they emit for defense [16]. In the past, three species [southern green

soybean maturity, sexual forms are formed and migrate back to buckthorn.

and sustainable use of host plant resistance (HPR) in soybean against these pests.

vania in 1996 [7].

20 Soybean - Pest Resistance

**2.1. Soybean aphid**

annually [14-15].

**2.2. Stink bugs**

**2. Hemipteran pests of soybean**

five-segmented antennae and a conspicuous scutellum [10].

**Figure 1.** Approximate distribution of the main, invasive Hemipteran pests of soybean. For BMSB, shaded range is where damage is heaviest, \* represent states where detection has been observed.

stink bug, *Nezara viridula (L.)*; green stink bug*, Acrosternum hilare* (Say); brown stink bug, *Euschistus servus* (Say)] constituted the stink bug complex that attacked soybean crop in southern US [6,17]. Amongst these, *N. viridula* is the most abundant [18] which has caused the most severe damage to the field crop [17]. In more northern latitudes, the relative abundance of *A. hilare* is higher compared to that of *N. viridula* [6]. During the last decade, redbanded stink bug, *Piezodorus guildinii* (Westwood), and brown marmorated stink bug (BMSB), *Halyomorpha halys* (Stål) have established themselves as important members of stink bug complex that attack soybean in the US [7, 19,20]. From 1960 onwards, the redbanded stink bug has been detected in US soybean but without causing any economic damage. However during last decade, redbanded stink bug infestations have reached above the threshold levels. By 2009, it was the most serious stink bug species attacking soybean in southern US [21, 22]. The BMSB is native to North and South Korea, Japan, China [23] and is invasive in North America and Europe. In US, BMSB has been confirmed as pest of soybean crop with a high damaging potential [24, 25]. Although not in the Pentatomidae, the kudzu bug (Plataspididae: *Megacopta cribraria*) is another recent invasive pest, first detected in Georgia in 2009 [26] and has now spread to 8 southeastern states of US [8]. It is known to feed on both kudzu and soybean, and damage on soybean can be quite severe [27].

Boththe soybeanaphidandstinkbugs canfeedonvarious above-groundplantparts like leaves, stems,flowers,andpods.Soybeanaphidprefers tofeedontheundersidesofleaves [15]whereas stink bugs prefer to feed on pod and seeds [6]. During the early seedling stages of soybean, soybean aphids are mostly found on freshly growing trifoliate leaves or the stems [30]. Later in the season, soybean aphids are more likely to be found lower in the canopy, on leaves that are attached to nodes further away from the terminal bud. During feeding, soybean aphid with‐ draws sap from soybean leaves which results in loss of photosynthates. Heavy infestations by soybean aphid can result in yellow and wrinkled leaves, reduction in plant height, reduced pod set and lesser number of seeds within pods [15,31]. Infested leaves may turn black due to sooty mold growing on the sugary excretions or "honeydew" produced by soybean aphid [5,15]. The severityofplantlosses causedbysoybeanaphidis largelydependentonthephysiological status of the soybean plant. Soybean aphid populations that reach their peak density during the earlyvegetativeormid-reproductivestages(R3-R5)aremorelikelytocauseseriousdamagecompared

Developing Host-Plant Resistance for Hemipteran Soybean Pests: Lessons from Soybean Aphid and Stink Bugs

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Except the first instar which is a non-feeding stage, all other developmental stages of stink bugs feed upon plants. In soybean, the most damage is caused by adults and/or fifth instars stages [10]. Due to their preference for pods and seeds, reproductive stages of soybean are the most susceptible to damage by stink bugs [17]. Further, stink bugs prefer to feed upon pods present on upper half of the plant. However in case of severe infestation, these insects may also feed on lower pods. Stink bugs cause injury to soybean seeds as they insert the stylets through the pod wall into the seed for feeding on plant juices. In immature seeds, discolored necrotic areas may occur around these punctures [10]. Mature seeds show puncturing marks, discoloration, and internal irregular white spots which may have a chalky appearance [33]. Heavy feeding on mature seeds may result in smaller size, irregular shape, including wrinkled areas around punctures (Figure 3) [33, 34]. Stink bug damage in soybean results in decreased pod number, fewerseedperpod,lowerseedweight,changesinfattyacidscomposition,andlowerseedquality [10]. The germination of soybean seeds may be prevented due to single puncture in radiclehypocotylaxisof seeds [35].Ontheotherhand, severalpunctures incotyledonsmaynotprevent germination but affect the vigor. Heavy infestation of stink bugs can result in foliar retention,

Hemipteran pests also cause indirect damage to crops by vectoring the transmission of microbial pathogens. The virus transmission by soybean aphid to various crops has been reviewed [4]. In soybean, soybean aphid has the potential to transmit *Soybean mosaic virus* [4] but so far, there is no report of significant damage. Stink bugs generally transmit fungal pathogens [36] but recently, they were also found to transmit bacterial pathogens [37]. Besides vectoring of fungal pathogens, feeding by stink bugs provides the entrance points for microbial

In agriculture, HPR represents the ability of a certain plant variety to produce a larger yield of better quality compared to other varieties of the same crop at the same level of insect

to populations that peak during late reproductive stages (R6-R7) [32].

delayed maturation and abnormal growth of the soybean crop [10].

pathogens [10].

**3. Host Plant Resistance (HPR)**

**Figure 2.** Generalized mouthpart structure of Hemiptera. Redrawn from [29.]

The biology of various stink bug species has been described in detail [10]. In general, stink bugs pass through five nymphal instars and an adult stage during their life cycle [10]. These insects overwinter as adults beneath the leaf litter of various host plants including grasses, shrubs and trees. Several species can also overwinter in homes and these infestations can be severe as seen with the BMSB [7]. In early summer (April-June), overwintered and first generation adults feed on crops like tomato, okra, crucifers, and legumes, but for BMSB, may also feed on woody trees like *Paulownia* or *Ailanthus altissima* (tree of heaven) early in the spring before moving into crops [28]. However, they will feed on soybean if early planted crop is available. In most cases, stink bugs will move into soybean to feed on the developing pods and seeds. In North America, the number of generations per year is largely dependent upon environmental factors but usually varies between 1 in the north to 5 in the south.

#### **2.3. Hemiptera feeding and damage to soybean**

Hemipteran pests inflict the damage on soybean by feeding on plant juices. These insects possess piercing and sucking mouthparts, the most characteristic feature of Hemiptera which are highly adapted for extracting the liquid contents of plants. The mouthparts' structures are held in a grove present on the anterior side of the insect's lower tip i.e. labium (also called as rostrum) (Figure 2, [29]). On the either side of maxillae, two mandibles are present. The mandibles, which are often barbed at the tip, form the main piercing structure called the stylet. Two opposing maxillae which are held together by a system of tongues and groves, form two canals: a food canal and a salivary canal. The food canal is used for uptake of plant liquids whereas salivary canal is for egestion of saliva into the plant structures. Because of the segmented structure, labium can fold itself when stylets penetrate into the plant surface.

Boththe soybeanaphidandstinkbugs canfeedonvarious above-groundplantparts like leaves, stems,flowers,andpods.Soybeanaphidprefers tofeedontheundersidesofleaves [15]whereas stink bugs prefer to feed on pod and seeds [6]. During the early seedling stages of soybean, soybean aphids are mostly found on freshly growing trifoliate leaves or the stems [30]. Later in the season, soybean aphids are more likely to be found lower in the canopy, on leaves that are attached to nodes further away from the terminal bud. During feeding, soybean aphid with‐ draws sap from soybean leaves which results in loss of photosynthates. Heavy infestations by soybean aphid can result in yellow and wrinkled leaves, reduction in plant height, reduced pod set and lesser number of seeds within pods [15,31]. Infested leaves may turn black due to sooty mold growing on the sugary excretions or "honeydew" produced by soybean aphid [5,15]. The severityofplantlosses causedbysoybeanaphidis largelydependentonthephysiological status of the soybean plant. Soybean aphid populations that reach their peak density during the earlyvegetativeormid-reproductivestages(R3-R5)aremorelikelytocauseseriousdamagecompared to populations that peak during late reproductive stages (R6-R7) [32].

Except the first instar which is a non-feeding stage, all other developmental stages of stink bugs feed upon plants. In soybean, the most damage is caused by adults and/or fifth instars stages [10]. Due to their preference for pods and seeds, reproductive stages of soybean are the most susceptible to damage by stink bugs [17]. Further, stink bugs prefer to feed upon pods present on upper half of the plant. However in case of severe infestation, these insects may also feed on lower pods. Stink bugs cause injury to soybean seeds as they insert the stylets through the pod wall into the seed for feeding on plant juices. In immature seeds, discolored necrotic areas may occur around these punctures [10]. Mature seeds show puncturing marks, discoloration, and internal irregular white spots which may have a chalky appearance [33]. Heavy feeding on mature seeds may result in smaller size, irregular shape, including wrinkled areas around punctures (Figure 3) [33, 34]. Stink bug damage in soybean results in decreased pod number, fewerseedperpod,lowerseedweight,changesinfattyacidscomposition,andlowerseedquality [10]. The germination of soybean seeds may be prevented due to single puncture in radiclehypocotylaxisof seeds [35].Ontheotherhand, severalpunctures incotyledonsmaynotprevent germination but affect the vigor. Heavy infestation of stink bugs can result in foliar retention, delayed maturation and abnormal growth of the soybean crop [10].

Hemipteran pests also cause indirect damage to crops by vectoring the transmission of microbial pathogens. The virus transmission by soybean aphid to various crops has been reviewed [4]. In soybean, soybean aphid has the potential to transmit *Soybean mosaic virus* [4] but so far, there is no report of significant damage. Stink bugs generally transmit fungal pathogens [36] but recently, they were also found to transmit bacterial pathogens [37]. Besides vectoring of fungal pathogens, feeding by stink bugs provides the entrance points for microbial pathogens [10].
