Biology and Management of the Threecornered Alfalfa Hopper (Hemiptera: Membracidae) in Alfalfa, Soybean, and Peanut

Biology and Management of the Threecornered Alfalfa Hopper (Hemiptera: Membracidae) in Alfalfa,... The threecornered alfalfa hopper, Spissistilus festinus (Say) (Hemiptera: Membracidae), was first described in 1831. Since its discovery, it has been observed feeding on> 20 plant species across seven plant families; pre- ferred hosts include species in the family Fabaceae. Spissistilus festinus has been identified as a serious eco- nomic pest of alfalfa, Medicago sativa L.; soybean, Glycine max L; and recently peanut, Arachis hypogaea L. Damage by S. festinus results from feeding and girdle formation on the plant stems; stem girdles inhibit the transportation of photosynthate through the phloem. Photosynthates accumulate above girdles, and the insects feed preferentially at these locations. Girdles can also reduce the structural stability of stems, resulting in signif- icant stand loss in extreme circumstances. The timing of chemical applications for management of S. festinus is critical for successfully reducing insect populations, but information regarding S. festinus’ economic impact in modern alfalfa, soybean, and peanut production systems is scarce. The following is a review of the biology, life history, distribution, pest status, and management of S. festinus on alfalfa, soybean, and peanut. Key words: threecornered alfalfa hopper, Spissistilus festinus, soybean, peanut, alfalfa Biology (Mitchell and Newsom 1984a, Rice and Drees 1985). The number of eggs laid in each slit varies by plant species. In soybean, ap- Description and Behavior proximately six eggs are laid per slit, but in alfalfa, Medicago sat- The Spissitilus festinus (Say) adult is light green and 6–7 mm long, iva L., 1–2 eggs were found per slit (Wildermuth 1915, Jordan with an elongated pronotum that extends to the tip of the abdomen 1952). Meisch and Randolph (1965) reported that oviposition (Wildermuth 1915). Spissistilus festinus receives its common name slits damage tissue and can be harmful to plants when oviposition from its pronotum; when observed from the front (Fig. 1A), it pos- is heavy. sesses three corners, one at each “shoulder” and one at the apex of Spissistilus festinus undergoes hemimetabolous development. It the pronotum. Adult males (Fig. 2A) are readily distinguishable progresses through four to six instars depending on nutrition and from females (Fig. 2B) by a red tint on the dorsal surface of the weather conditions; five total instars is most commonly reported male’s pronotum, marginally smaller male body size, and lack of an (Wildermuth 1915, Moore and Mueller 1976, Deitz and Wallace ovipositor (Fig. 1B; Wildermuth 1915). 2012). The first and second instars (Fig. 2B and C) are 1.6 mm and Eggs (Fig. 3A) range in size from 0.9 to 1.3 mm long. They are 2.1 mm in length, respectively; they are pale green or straw colored, white in color and oblong in shape, with one end larger than the with a series of dorsal spine-like protrusions. At each successive other. The larger end of the egg is covered in papillae, which are nymphal stage, the spines grow and develop divergent lateral spurs thought to secure the egg within the plant tissue (Wildermuth 1915). that occur along the length of each spine. Wing pads and pro- Eggs are inserted under the epidermis in a slit created by the oviposi- nounced development of the pronotum appear in the third nymphal tor (Fig. 4). Oviposition behavior has been shown to vary depending stage; third instars (Fig. 2D) are darker yellow-brown color with on the host species and the maturity of that species. For example, in green markings, and are 2.9 mm in length. Fourth and fifth instars soybean, Glycine max L., oviposition occurs near the base of the (Fig. 2E and F) are similar in appearance and grow progressively main stem early in the season (Wildermuth 1915), and occurs in greener with pronounced wing pads, dorsal spikes, and pronotum. softer tissues such as terminals and nodes as the season progresses V C The Authors 2017. Published by Oxford University Press on behalf of Entomological Society of America. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact Downloaded from https://academic.oup.com/jipm/article-abstract/8/1/10/3745632 journals.permissions@oup.com 1 by Ed 'DeepDyve' Gillespie user on 13 July 2018 2 Journal of Integrated Pest Management, 2017, Vol. 8, No. 1 Fig. 1. (A) Frontal perspective of adult S. festinus, exhibiting the three corners at the “shoulders” and dorsally. (B) Ventral perspective showing female (left) and male (right) S. festinus. Fig. 2. Side by side perspective of adult S. festinus displaying sexual dimorphism. Males (A) possess a red coloration that runs along the dorsal edges of the pronounced pronotum. Females (B) possess a slight red tinge posteriorly on the pronotum, as well as an elongated abdomen. Third through fifth instars are more mobile than the first and However, Mitchell and Newsom (1984b)and Newsom et al. (1983) second instars (Wildermuth 1915). When disturbed, nymphs will documented that sex ratios vary throughout the season; the proportion sometimes produce a globule from the abdomen as a defense mecha- of males to females was equal at overwintering habitats. The first mi- nism and quickly move to the opposite side of the stem (Wildermuth gration skews the ratio toward females, suggesting that only the fe- 1915). Adults will also attempt to conceal themselves in a similar males migrate from overwintering sites. Ratios equalize after the first manner, though they commonly fly away when disturbed spring generation (Mitchell and Newsom 1984b, Newsom et al. 1983). (Wildermuth 1915). Adults generally fly within 33 cm above the soil An egg-laying female can be found with an average of 21–30 eggs in or just above the plant canopy (Johnson and Mueller 1989, 1990). her ovaries at any one time, and can produce up to 220 eggs over her lifetime (Mitchell and Newsom 1984b). Life History The embryo’s development lasts from 6 to 27 d, with an average Spissistilus festinus can have multiple generations per year depending of 16.5 d from oviposition to eclosion (Meisch and Randolph 1965). on weather conditions and availability of host plants (Wildermuth The first three instars are completed in 3–5 d each, depending on 1915, Mitchell and Newsom 1984b). Adults overwinter in a state of temperature, humidity, and nutrition. The fourth and fifth instars reproductive diapause (Newsom et al. 1983, Mitchell and Newsom last 4–8 d each (Wildermuth 1915, Jordan 1952, Meisch and 1984b), though reproduction has been reported to continue during Randolph 1965, Spurgeon and Mack 1990). Total nymphal develop- mild winters (Wildermuth 1915). A nascent adult female reaches sex- ment time has been shown to vary with temperature. Wildermuth ual maturity in 7–14 d; she will mate and lay eggs soon after (Jordan (1915) observed that nymphal development required 69 and 32 d when 1952, Meisch 1964, Meisch and Randolph 1965). Males reportedly mean temperatures were 16 C and 30 C, respectively. Other reports die soon after copulation, but females live for an average of 38.6 d estimate development time to be 18–24 d at temperatures of 32 Cand postcopulation (Mitchell and Newsom 1984b). Wildermuth (1915) re- 26.6 C and 75–80% relative humidity (Jordan 1952, Meisch 1964, ported that populations generally consist of more males than females. Meisch and Randolph 1965, Spurgeon and Mack 1990). Downloaded from https://academic.oup.com/jipm/article-abstract/8/1/10/3745632 by Ed 'DeepDyve' Gillespie user on 13 July 2018 Journal of Integrated Pest Management, 2017, Vol. 8, No. 1 3 Fig. 3. Life stages of the S. festinus.(A) Egg (B–F) Instars 1–5. suitable habitat for breeding and development (Moellenbeck et al. 1993, Deitz and Wallace 2012). The host range of S. festinus consists of many plant species in a number of families. The insect was first identified as a potential pest of tomato in personal communications between Oemler and the University of Georgia in 1888 (Oemler 1888). Cockerell (1899) first reported S. festinus as a pest on alfalfa 11 yr later. The known host range of S. festinus includes alfalfa; cowpeas, Vigna unguiculata (L.); clover, Trifolium spp; various trees; shrubs; grasses; herbs; sug- arcane, Saccharum officinarum L.; potato, Solanum tuberosum L.; cotton, Gossypium hirsutum L.; and field pea, Pisum sativum L. (Wildermuth 1915, Van Zwaluwenburg 1926, Swezey 1937). Plant species in the Fabaceae have been shown to be better reproductive and developmental hosts, and the insect is considered an economic pest of alfalfa, soybean (Caviness and Miner 1962, Tugwell et al. 1972, Mitchell and Newsom 1984a, Sparks and Newsom 1984, Sparks and Boethel 1987a, Johnson et al. 1988), and peanut (King et al. 1961, Fig. 4. Eggs of S. festinus in the base of a soybean, G. max, stem. Todd et al. 1979, Andersen et al. 2002, Rahman et al. 2007). In Louisiana, overwintering adults have been observed on pine, Pinus spp.; in spring, adults were found on vetch, Vicia spp. and clover, be- Distribution and Host Range fore moving onto newly emerged soybean (Newsom et al. 1983). Wildermuth (1915) reported that S. festinus had been observed from Ottawa, Canada, to Mexico; this distribution was refined by Caldwell 1949. His description of the different species of Spissistilus Economic Importance using the genitalia revealed that the original reported distribution was based on misidentified Spissistilus species. The upper limits of Direct and Indirect Injury the distribution are closer to the Midwest United States as opposed Spissistilus festinus is a phloem feeder with piercing–sucking mouth- to Canada. In the United States, S. festinus is prevalent in the parts and two distinct feeding behaviors. The first behavior involves Southeast and Midsouth, where the abundance of preferred host sporadic probing and consumption of phloem sap (Andersen et al. plants such as soybean and peanut, Arachis hypogaea L., provides 2002). The other behavior involves the formation of a continuous Downloaded from https://academic.oup.com/jipm/article-abstract/8/1/10/3745632 by Ed 'DeepDyve' Gillespie user on 13 July 2018 4 Journal of Integrated Pest Management, 2017, Vol. 8, No. 1 series of lateral punctures around the circumference of a stem Alfalfa (Wildermuth 1915). Commonly referred to as a girdle (Fig. 5), the Spissitilus festinus was first described as a pest of alfalfa in 1899 aforementioned ring of punctures often results in a gall-like growth (Cockerell 1899). Alfalfa is a perennial forage and hay crop that can (Fig. 5A) in the area surrounding the feeding site (Wildermuth be harvested multiple times a year, but S. festinus feeding girdles can 1915). Smith (1933) found that after the insect feeds, insoluble sali- cause significant loss in quality of the new growth (Wilson and vary sheaths are left in the plant tissue. Mitchell and Newsom Quisenberry 1987). Entire fields can require reseeding when heavy (1984a) discovered that it is these sheaths that disorganize and dis- infestations result in high stem girdle counts owing to the persistent rupt the vascular bundles of the phloem, as well as induce cellular nature of the girdles (Graham and Ellisor 1938). hyperplasia (Johnson et al. 1988). Multiple studies across different Spissistilus festinus has multiple and overlapping generations an- plant species have shown that the third through fifth instars (as well nually on alfalfa, with two population peaks occurring late June to as adults) are capable of creating stem girdles (Meisch and early July and late August through September in Louisiana (Farlow Randolph 1965, Moore and Mueller 1976, Mitchell and Newsom et al. 1981, Moellenbeck et al. 1993). The latter peak is often much 1984a, Andersen et al. 2002). greater than the former, and as a result, the amount of damage to Girdling interrupts the flow of nutrients in the phloem and the new growth can be considerable (Wilson and Quisenberry causes an accumulation of photosynthates in the area above the gir- 1987). Nymphs in a greenhouse study did not have any measurable dle (Osborn 1911, Wildermuth 1915, Mitchell and Newsom 1984a, effect on “Florida 77” alfalfa at one and three nymphs per plant Andersen et al. 2002). Andersen et al. (2002) reported that many of (Wilson and Quisenberry 1987). However, when the densities in- the amino acids that increase in concentration above the stem gir- creased to six nymphs per plant, protein content decreased, fiber dle are likely the result of plant responses to feeding and are not density increased, and root carbohydrate levels decreased essential to insect development. Nevertheless, concentrations of (Moellenbeck and Quisenberry 1991). Although overall dry weight amino acids required for S. festinus development are also elevated was not affected, the quality of harvested hay was reduced. It is pos- by the girdling process (Andersen et al. 2002). On peanut and sible that the regrowth capability of the plants was affected owing other host plants, nymphs gather within 5 mm above the girdle, to reduced root carbohydrate concentrations (Moellenbeck and andfeed forupto7d (Moellenbeck and Quisenberry 1991, Quisenberry 1991). Andersen et al. 2002). New girdles are formed above existing gir- Currently, S. festinus is not considered a major pest of alfalfa. dles, and nymphs will relocate to continue feeding (Moellenbeck The insect is either not mentioned (Undersander et al. 2011, and Quisenberry 1991, Andersen et al. 2002). In alfalfa and soy- Whitworth et al. 2015) or is described as a minor, occasional pest bean, heavy girdling reduces the forage quality owing to lowered (Summers et al. 2007) in the most recently published alfalfa pest levels of carbohydrates and amino acids, as well as increased lev- management handbooks. Recent pest management handbooks for els of detergent fibers (Wilson and Quisenberry 1987, Tennessee, Georgia, and Alabama suggest that insecticides may be Moellenbeck and Quisenberry 1991). needed if adults or nymphs are present on 10% of seedlings and Nutrient loss is not the only consequence of girdling. Girdles on young plants (up to 10–12 inches tall) or if 10% of lateral stems are the main stem of soybean seedlings can impact the structural stabil- being killed from damage (Flanders and Everest 2014, Buntin 2016, ity of the plant, leaving the girdled stem susceptible to lodging from Stewart and McClure 2016). For older plants, an economic thresh- wind and mechanical disturbance (Sparks and Boethel 1987a). In old of two adults or nymphs per sweep with a 0.38-m sweep net has peanut, which has a more prostrate growth habit and multiple been published (Stewart and McClure 2016). In Tennessee, how- branches, stand loss owing to lodging is not a serious concern. ever, a study showed that a 25% reduction in stand count did not Sparks and Newsom (1984) speculated that high levels of late-sea- cause any economic impact in alfalfa (Bates et al. 2005). son petiole feeding could lead to leaf death and reduce both effective leaf area and yield in soybean. Spissistilus festinus damage has been linked to an increase in the Soybean likelihood of disease complexes in soybean. Herzog et al. (1975) ob- Spissistilus festinus has long been considered a pest of soybean. It served increased incidence of blight caused by Sclerotium rolfsii was first detected on soybean in the early 1900s, but significant (Sacc.) infection in girdled versus nongirdled stems. Although S. fes- damage was not reported until 1957 (Caviness and Miner 1962). It tinus did not actively transmit the pathogen, the presence of girdles was initially thought that yield loss resulted from early-season gir- close to the soil where S. rolfsii occurred significantly increases fre- dling of the main stem (V1–V5 growth stages). The damage to the quency of infection. Sclerotium rolfsii is one of the most damaging main stem caused large swathes of soybean plants to lodge. peanut pathogens. It can cause up to 12% yield loss in Georgia, However, Caviness and Miner (1962) found evidence that lodging where losses and accompanying treatment costs associated with S. had minimal effects on yield. Artificially reduced stands had the rolfsii are estimated to be US$41 million annually (Woodward highest loss in yield (up to 15%) when stand loss occurred after 2010, 2011, 2012, 2013). No work has been published on the inter- bloom, and less yield loss (up to 7%) when damage occurred 2 wk action of S. festinus infestation and S. rolfsii incidence in peanut, but prior to bloom. It should be noted that lodging simulations in this it should be noted that S. rolfsii incidence in soybean increases with study were evenly distributed throughout the plots, allowing max- mechanical damage. Therefore, S. festinus infestation on peanut imum compensation from adjacent plants. In studies simulating could increase the occurrence of infection (Herzog et al. 1975, the effect of early-season S. festinus girdling of main stems, Cook Russin et al. 1986). A study of soybean with symptoms of stem can- et al. (2014) found that yield of indeterminate Maturity Group IV ker, Diaporthe phaseolorum (Cke. and Ell.), found that girdle pres- soybean was significantly reduced by stand loss occurring from R1 ence resulted in larger cankers and reduced yields (Russin et al. to R5. Yield response was inconsistent across reproductive growth 1986). Russin et al. (1987) found that girdles on soybean did not in- stages in this study, and it is unknown what levels of insect gir- crease infection rate of pod or stem blight, Phomopsis sojae and dling would result in the rates of stand loss tested. Bailey (1975) Colletotrichum truncatum (Schw.), but did increase symptom sever- reported a yield reduction of >14 bushels per acre when S. festinus ity of both diseases and reduced yields. adults were caged at densities of four adult insects per plant Downloaded from https://academic.oup.com/jipm/article-abstract/8/1/10/3745632 by Ed 'DeepDyve' Gillespie user on 13 July 2018 Journal of Integrated Pest Management, 2017, Vol. 8, No. 1 5 Fig. 5. Girdles on peanut, A. hypogaea.(A) Stem girdle resulting in gall formation as well as adventitious root growth. (B) Spissitilus festinus nymph forming a girdle on a peanut leaf petiole. compared with one adult per five plants on 1.5–2-inch tall soy- Boethel (1987a) found that yield reductions occurred at 60% of the bean seedlings. aforementioned threshold, and introduced the hypothesis that pod or The number of generations of S. festinus occurring annually in peduncle feeding contributes more to yield loss than petiole girdling. soybean varies. Mueller (1980) found three overlapping genera- A relatively recent shift from traditional timings of soybean tions, whereas Mitchell and Newsom (1984b) found only two. planting (late May and early June) to early-season planting (mid- These differences suggest that the number of generations occurring April) occurred in the midsouthern United States primarily as an ef- annually fluctuates and is likely affected by local environmental fort to avoid periods of drought (Heatherly 1998). This early soy- conditions. When observing the effects of individual generations bean production system (ESPS) incorporates earlier maturing on the host, Sparks and Newsom (1984) found that early-season varieties and can result in greater yield, and can result in less late- damage (when there is the highest danger of lodging from girdles season damage resulting from caterpillar feeding compared with the on the main stem) did not significantly impact yield. However, traditional production system (Heatherly 1998). Early-planted soy- Bailey (1975) found significant reduction in yield at a rate of one bean production may affect many of the previously established eco- hopper per plant when plants were 1.5–2.0 inches tall, indicating nomic thresholds for pests of soybean, including S. festinus. In ESPS, that it is possible that damage occurring in the early season has the S. festinus populations are higher early in the season, and late season capability to impact yield. No difference in yield between individ- infestations are largely avoided (Bauer et al. 2000, McPherson et al. ual girdled and nongirdled plants was observed, indicating that 2001). Pulakkatu-Thodi (2010) and Ramsey (2015) were unable to lodging is a cause of yield reduction when girdling rates are high. observe any impact on yield in reproductive, early-planted soybeans, Nevertheless, Caviness and Miner (1962) artificially removed as a result of adult numbers at 3 the established threshold of one plants from the stand and demonstrated that soybeans have in- adult per sweep. Infestations occurring prior to or after pod fill ap- credible compensatory power. Mueller and Jones (1983) showed pear to have little or no consistent effect on yield. It should be noted that yield was reduced only when 70% or more of plants had a that only adults were included in both of these studies, and as such, main stem girdle. The lack of yield response at lower feeding levels the full impact of S. festinus in contemporary early-planted season was attributed to compensation and high seeding rates (12 seed soybean production systems is as of yet undetermined. There are no per 0.33 m row). In one study, late season damage during the sec- recently published or validated thresholds for S. festinus on early- ond in-field generation of S. festinus resulted in significant reduc- planted soybean. tions in yield (Sparks and Boethel 1987a). This result was most likely related to S. festinus feeding on the succulent petioles, pe- duncles, and pedicels after the soybean’s R1 stage (Mitchell and Peanut Newsom 1984a). Though nutrient flow on a girdled petiole re- Spissistilus festinus has been observed feeding on peanut for the past sumes after 10 d (Spurgeon and Mueller 1993), the damage may half-century, though there have been no intensive investigations of be enough to decrease the number of seedpods produced or the its economic impact (King et al. 1961, Todd et al. 1979). In Georgia number of seed per pod, thereby reducing yield (Sparks and and surrounding states, growers now see S. festinus in great abun- Newsom 1984). dance in peanut fields, and there are concerns about possible yield The first economic threshold for S. festinus was established by loss associated with feeding. Though there have been estimates of Sparks and Newsom (1984), who determined that one adult per sweep the economic impact of S. festinus in peanut ranging from US$1.5 at soybean pod set until leaf yellowing is enough to cause economic million in yield loss (Brown et al. 1997) to no impact other than damage and should be treated. This threshold was based on the hy- treatment costs (Adams 2008), no science-based economic injury pothesis that late season damage consisting of mostly petiole girdling level has been determined. is the cause of significant yield loss. Sparks and Newsom (1984) also Two nymphal S. festinus population peaks are observed in pea- hypothesized that when the threshold for adults is met, the nymphs nut annually in the Southeast. The first generation of nymphs ap- have already done a substantial amount of damage. Sparks and pears in late June to early August after an initial appearance of Downloaded from https://academic.oup.com/jipm/article-abstract/8/1/10/3745632 by Ed 'DeepDyve' Gillespie user on 13 July 2018 6 Journal of Integrated Pest Management, 2017, Vol. 8, No. 1 Table 1. Insecticides registered for management of S. festinus in Alfalfa (Georgia Pest Management Handbook–2016 Commercial Edition) Insecticide AI Common names Insecticide Type IRAC Amount/acre Lbs AI/acre REI/PHI Alpha-cypermethrin Pyrethroid 3A Fastac 0.83 2.2–3.8 fl oz 0.012–0.025 12 h/3 d Beta-cyfluthrin Pyrethroid 3A Baythroid XL 1.0EC 1.6–2.8 fl oz 0.0125–0.022 12 h/7 d Carbaryl Carbamate 1A Sevin 80S 1.25 lb 1.0 12 h/48 d Sevin XLR Plus, 4F 1.0 qt 1.0 Cyfluthrin Pyrethroid 3A Tombstone 2.0 1.6–2.8 fl oz 0.025–0.044 12 h/7 d Gamma-cyhalothrin Pyrethroid 3A Declare 1.25 1.02–154 fl oz 0.01–0.015 12 h/ Proaxis 0.5 2.56–3.84 fl oz 0.01–0.015 7 d Lambda-cyhalothrin Pyrethroid 3A Karate Zeon 2.08 1.28–1.92 fl oz 0.02–0.03 12 h/ Silencer 1 2.56–3.84 fl oz 0.02–0.03 7 d Zeta-cypermethrin Mustang MAX, Pyrethroid 3A 12 h/ Respect 0.8EC 2.24–4.0 fl oz 0.014–0.025 3 d aRe-entry interval/plant harvest interval. adults, and the second generation develops during late August into field; therefore, plant injury can be assessed within 10 m of field bor- early September (Rahman et al. 2007). The majority of girdling oc- ders to adequately estimate whole field injury levels according to curs 3 wk after the initial appearance of nymphs in June (Rahman Rahman et al (2007). Whole plant observations provide an accurate et al. 2007); this coincides with the approximate development time assessment of nymph populations (Spurgeon and Mueller 1991), but from eclosion to fourth instar (Meisch 1964, Meisch and Randolph this method is impractical for IPM because of the time required for 1965, Spurgeon and Mack 1990). The fourth instar is thought to be each sample. Beat sheet sampling is less time consuming than whole responsible for most of the girdling in peanut (Moore and Mueller plant observations, but it is not ideal for detecting the younger, 1976, Johnson and Mueller 1988). smaller nymphs in soybean, as their small mass reduces the chance Although S. festinus is capable of girdling peanut, no published of dislodging from the plant (Spurgeon and Mueller 1991). The beat reports correlate peanut damage with yield loss. Andersen et al. (2002) net (Sparks and Boethel 1987b) and vertical beat sheet (Drees and reported reduced biomass, nitrogen content, and carbon content in gir- Rice 1985) are alternatives to the beat sheet for sampling nymphs. dled peanut stems in northern Florida, but this effect was not consistent The former involves utilizing a standard 33-cm sweep net held at a over years of the study. Spissistilus festinus damage, characterized by 45-degree angle to the plant base; the plant is then beat into the net number of girdles, was shown to vary by cultivar, with runner-type at 10 different locations in the field. The latter method involves a Georgia Green and Virginia-types AT VC2, GA-HI-O/L, Virugard, similar technique, where a beat sheet is held parallel to the plants, Wilson, and Phillips being particularly susceptible. Nevertheless, no with a trough at the bottom to collect the nymphs that are shaken or measurable effect on yield was detected from girdling alone, with dam- beaten off the plant. Sparks and Boethel (1987b) utilized these meth- age rates up to six girdles per plant (Rahman et al. 2007). ods to good effect for sampling S. festinus nymphs, finding that the The economic injury level for S. festinus in peanut is unknown, beat net was the most efficient and effective. and there are no experimentally validated economic thresholds. Adult populations can be assessed effectively with a sweep net in However, at least one set of anecdotal thresholds has been reported, soybean (Kogan and Herzog 1980) and peanut (Rahman et al. where one adult per 6 feet of row at 75 d prior to digging or one adult 2007). Adults can also be monitored in soybean with yellow sticky or nymph per 3 feet of row 25–75 d prior to digging warrants treat- traps (Johnson and Mueller 1988) placed 33 cm above the ground or ment (Brown 2006). Preliminary studies conducted recently at the at just above canopy level (Johnson and Mueller 1989); however, University of Georgia suggest that these thresholds overestimate the trap counts were not as accurate as sweep samples for predicting ac- economic impact of S. festinus and trigger insecticide applications at tual field populations (Johnson and Mueller 1988, Johnson and population levels that are not yield limiting. It is important to know Mueller 1990). at what point S. festinus damage impacts peanut yield. Growers in the Southeastern United States currently treat S. festinus as a pest and manage populations with insecticides. The broad-spectrum insecti- Sampling Timing cidesusedtotarget S. festinus can flare secondary pests, negatively Critical sampling periods differ from crop to crop and may even impact natural enemies and pollinators, and reduce net profits when vary within a crop depending on production practices as with soy- applied unnecessarily (Ware 1980, Adams 2008). bean planting date. Feeding in alfalfa was most injurious during the second population peak (Wilson and Quisenberry 1987). Managing S. festinus in alfalfa requires monitoring plant stands for stem death resulting from girdles, as well as monitoring for sudden increases in Monitoring populations of S. festinus adults. Sampling Methods Though the economic impact of S. festinus in modern U.S. soy- In soybean (Sparks and Boethel 1987a) and peanut (Rahman et al. bean production systems is not clear, research suggests the crop may 2007), S. festinus females are randomly distributed throughout the be vulnerable to damage at distinct development periods. Prior to Downloaded from https://academic.oup.com/jipm/article-abstract/8/1/10/3745632 by Ed 'DeepDyve' Gillespie user on 13 July 2018 Journal of Integrated Pest Management, 2017, Vol. 8, No. 1 7 Table 2. Insecticides registered for management of S. festinus in Soybean (2016 Insecticide Recommendations for Arkansas [Studebaker]) Insecticide AI Common names Insecticide Type IRAC Amount/acre Lbs AI/acre REI/PHI Beta-cyfluthrin Pyrethroid 3A Baythroid XL 1.0EC 1.6–2.8 fl oz 0.013–0.022 12 h/45 d Clothianidin Neo-nicotinoi 4A Belay 2.13 EC d 3–6 fl oz 0.05–0.1 12 h/21 d Cyfluthrin Pyrethroid 3A Tombstone 2 EC 1.6–2.8 fl oz 0.025–0.044 12 h/45 d Esfenvalerate Carbamate 1A Asana XL 0.66 EC 5.8–9.6 fl oz 0.03–0.05 12 h/21 d Gamma-cyhalothrin 1.25 Pyrethroid 3A Prolex/Declare CS 0.77–1.28 fl oz 0.0075–0.013 12 h/30 d Lambda-cyhalothrin Pyrethroid 3A Karate Zeon 2.08 CS 0.96–1.6 fl oz 0.015–0.025 12 h/30 d Lambda-cyhalothrin þchlorantranilipole Pyrethroid 3A Diamide 28 Beseige 1.252 5.0–8.0 fl oz 0.049–0.08 12 h/30 d Zeta-cypermethrin Pyrethroid 3A Mustang Maxx 2.8–4.0 fl oz 0.0175–0.25 12 h/21 d Zeta-cypermethrin þ bifenthrin Pyrethroid 3A Hero 1.24 EC Pyrethroid 3A 4.0–10.3 fl oz 0.04–0.1 12 h/21 d aRe-entry interval/plant harvest interval. Table 3. Insecticides registered for management of S. festinus in peanut (Georgia Pest Management Handbook–2016 Commercial Edition) Insecticide AI Common names Insecticide Type IRAC Amount/acre Lbs AI/acre REI/PHI Carbaryl Carbamate 1A Sevin 80S 1.25 lb 1.0 12 h/48 d Sevin XLR Plus, 4F 1.0 qt 1.0 Bifenthrin Pyrethroid 3A Brigade 2EC 2.1–6.4 fl oz 0.33–0.1 12 h/14 d Beta-cyfluthrin Pyrethroid 3A Baythroid XL 1.0EC 1.6–2.8 fl oz 0.0125–0.022 12 h/7 d Lambda-cyhalothrin Pyrethroid 3A Karate Zeon 2.08 1.28–1.92 fl oz 0.02–0.03 12 h/7 d Silencer 1 2.56–3.84 fl oz 0.02–0.03 aRe-Entry Interval/Plant Harvest Interval. the shift to early-season planting, the critical sampling and treatment time is unknown, using adults as a predictor of damage could over period to prevent early-season damage resulting from main stem gir- or under estimate the impact of S. festinus. dles in soybean was when the plants were around the V3 stage (Spurgeon and Mueller 1992). Averting late-season damage in soybean Management required sampling for S. festinus populations before V12 growth stage (Fehr et al. 1971, Spurgeon and Mueller 1992). Sparks and Newsom’s Insecticides are the most effective tool to quickly reduce S. festinus 1984 treatment threshold in soybean was based on the observation populations in the crops discussed here. Pyrethroid and organophos- that economic losses could occur from pod set to leaf yellowing. phate insecticides are commonly recommended, though published Additional research is needed to quantify the economic impact of S. efficacy of individual products in these classes varies. There are no festinus on soybean and to determine optimal monitoring time(s). recent, experimentally validated economic thresholds for S. festinus Rahman et al. (2007) recommend monitoring peanut for nymph in any crop. Because most of the damage caused by threecornered al- and girdle presence in the first 2–3 wk of July. Damage increased in falfa hopper is attributed to feeding by the third, fourth, and fifth in- the third week of July, after consistent weekly increases in nymph stars (Andersen et al. 2002), management strategies should focus on numbers, indicating that early July is the optimal time for scouting reducing population levels of this life stage. In some crops, it may be nymphs (Rahman et al. 2007). An increase in adult S. festinus abun- possible to prevent infestations of immature stages by targeting im- dance was observed a few weeks before damage levels rose in pea- migrating adults with insecticides. This strategy can fail if adult nut. This is likely a result of the earliest nascent adults from the first movement into a crop occurs over a long period of time and residual generation appearing when the majority of nymphs are still forming insecticide efficacy is short. Applying insecticides only when the girdles. Using these adults as a direct, numerical indicator of injury nymphs are present on a susceptible crop stage is an ideal strategy, may result in an appropriate diagnosis, but only after the damage but accurately assessing nymph populations is difficult. Regardless has been done (Rahman et al. 2007). Because the correlation be- of the life stage targeted by insecticides, coverage of the crop canopy tween the number of adults and nymphs in the field at any given will affect control. Downloaded from https://academic.oup.com/jipm/article-abstract/8/1/10/3745632 by Ed 'DeepDyve' Gillespie user on 13 July 2018 8 Journal of Integrated Pest Management, 2017, Vol. 8, No. 1 Georgia 2006. Miscellaneous Publication Number 106. University of Alfalfa Georgia, Athens, GA. In alfalfa, cultural practices that reduce the impact of S. festinus in- Andersen, P. C., V. Brodbeck, and D. C. Herzog. 2002. Girdling-induced nu- clude increasing seeding rate to mitigate stand loss and removing trient accumulation in above ground tissue of peanuts and subsequent feed- weedy borders around fields to eliminate overwintering sites (Bates ing by Spissistilus festinus, the three-cornered alfalfa hopper. Entomologia et al. 2005). Insecticides listed in the 2015 Georgia Pest Management Experimentalis Et Applicata 103: 139–149. Handbook for management of S. festinus in alfalfa when adults or Bailey, J. C. 1975. Three-cornered Alfalfa Hoppers (Homoptera: nymphs are found on 10% of alfalfa seedlings, or losses exceed 10% Membracidae): Effect of four population levels on soybeans. Journal of the of lateral stems are provided in Table 1 (Buntin 2016). Kansas Entomological Society 48: 519–520. Bates, G., G. Burgess, D. Hensley, M. Newman, and R. Patrick. 2005. Crop profile for alfalfa in Tennessee. Regional IPM Centers. (http://www.ipmcen Soybean ters.org/cropprofiles/docs/TNalfalfa.pdf) (accessed 3 April 2017). Spissistilus festinus is still regarded as a soybean pest, though recent Bauer, M. E., J. Boethel, M. L. Boyd, G. R. Bowers, M. O. Way, L. G. studies suggest its pest status may have diminished in the early-soy- Heatherly, J. Rabb, and L. Ashlock. 2000. Arthropod populations in early bean production system (Pulakkatu-Thodi 2010, Ramsey 2015). soybean production systems in the Mid-South. Environmental Entomology Current soybean thresholds may not be valid for early-soybean pro- 29: 312–328. duction systems, and the lack of consistency found in state manage- Brown, S. L. 2006. Threecornered alfalfa hopper damage continues to ment guides is indicative of the lack of consensus regarding the increase. In E.P. Prostko (ed.), 2016 Peanut Update. Athens GA: UGA insect’s pest status. The thresholds published in the 2016 Insecticide Extension Publication CSS-06-0115. p.69. Brown, S. L., D. C. Jones, and J. W. Todd. 1997. Peanut Insects, p. 28. In D. Recommendations for Arkansas (Studebaker 2016) recommend G. Riley, G. K. Douce, and R. M. McPherson (eds.), Summary of losses treatment when "50% of the plants are girdled, or if fewer than 4–6 from insect damage and costs of control in Georgia 1996. (http://www. ungirdled plants per row foot remain in conventional rows, 30 bugwood.org/sl96/images/Sl96.pdf) (accessed 3 April 2017). [inches] to 38 [inches], and hopper nymphs are still present” for Buntin, D. 2016. Alfalfa insect control, pp. 108–112. In D. Horton (ed.), plants still under 10”. Insecticides recommended by the University Georgia pest management handbook. Special Bulletin 28:1. University of of Arkansas in 2016 for management of S. festinus in soybeans are Georgia, Athens, GA. given in Table 2. These recommendations and those published by Caldwell, J. S. 1949. A generic revision of the treehoppers of the tribe Ceresini Mississippi State University include neonicotinoid seed treatments in America north of Mexico, based on a study of the male genitalia. which can provide control of S. festinus for 3–4 wk (Catchot 2016). Proceedings of the United States Natural Museum 98: 491–521. A recently published survey of U.S. soybean producers showed that Catchot, A. 2016. 2016 Insect control guide for aronomic crops. Mississippi State University, Publication Number 2471, pp. 22–44. 51% used insecticide (neonicotinoid) seed treatments (Hurley and Caviness, C. E., and F. D. Miner. 1962. Effects of stand reduction in soybeans Mitchell 2017). Only 1.4% of survey respondents indicated that simulating Three-Cornered Alfalfa Hopper injury. Agronomy Journal 54: they actively managed S. festinus, but no Southeastern soybean 300–302. growers were included in the study. Louisiana State University rec- Chapin, J. W. (ed.) 2015. South Carolina pest management handbook 2015: ommends treatment when three or more nymphs or one or more Clemson cooperative extension. Clemson University, South Carolina. adults are present beginning at pod set, and no neonicotinoids are Cockerell, T.D.A. 1899. Some insect pests of Salt River Valley and the reme- included in published recommendations (Davis 2017). dies for them. Arizona Agricultural Experiment Station Bulletin 32: 273–295. Cook, D. R., D. Stewart, J. E. Howard, D. S. Akin, J. Gore, B. R. Leonard, G. Peanut M. Lorenz, and J. A. Davis. 2014. Impactof simulated threecornered alfalfa The impact of S. festinus feeding on peanut is poorly understood. hopper (Hemiptera: Membracidae) induced plant loss on yield of Maturity Clemson Cooperative Extension suggests treating peanut with insec- group IV and V soybean. Journal of Entomological Science 49: 176–189. ticide at 45–60 d after planting to reduce damage caused by S. festi- Davis, J. 2017. Soybean. In Louisiana insect pest management guide. LSU AG nus (Chapin 2015). Though the University of Georgia Cooperative Center Publication, vol. 1838, pp. 40–46. Extension Service has not published validated thresholds or recommen- Deitz, L. L., and M. S. Wallace. 2012. Richness of the Nearctic treehopper dations for optimum treatment timing, growers in Georgia commonly fauna (Hemiptera: Aetalionidae and Membracidae). Zootaxa 3423: 1–26. target S. festinus populations with pyrethroid insecticides. Mississippi Drees, B. M., and M. E. Rice. 1985. The vertical beat sheet: A new device for State University recommends treatment when fresh damage and two in- sampling soybean insects. Journal of Economic Entomology 78: 1507–1510. sects per six-row feet are present (Catchot 2016). The insecticides listed Farlow, R. A., A. Wilson, J. R. Rabb, and K. L. Koonce. 1981. Insects infesting in the Georgia Pest Management Handbook for management of S. fes- alfalfa in northwest Louisiana: Their effect on production, their control with tinus in peanut are given in Table 3 (Abney 2016). insecticides. Louisiana Agricultural Experiment Station Bulletin 731: 1–22. Fehr, W. R., E. Caviness, D. T. Burmood, and J. S. Pennington. 1971. Stage of development descriptions for soybeans, Glycine max (L.) Merrill. Crop Acknowledgments Science 11: 929–931. We thank Stormy Sparks for his critical review of this manuscript. This proj- Flanders, K. L., J. W. Everest (eds.) 2014. Alfalfa: Insect and Weed control rec- ect was supported by the Crop Protection and Pest Management, Applied ommendations for 2014. In Alabama cooperative extension system. Auburn Research and Development Program (award number: 2014-70006-22518) University, Alabama. from the USDA National Institute of Food and Agriculture. Graham, L. T., and L. O. Ellisor. 1938. Early spring cutting assists in the con- trol of the three-cornered alfalfa hopper, Stictocephala festina (Say). Louisiana Agricultural Experiment Station Bulletin 298: 4–5. References Cited Heatherly, L. G. 1998. Early soybean production system, pp. 103–118. In L. G. Heatherly and H. F. Hodges (eds.), Soybean production in Mid-South Abney, M. R. 2016. Peanut insect control, pp. 195–200. In D. Horton (ed.), CRC Press LLC, Boca Raton, FL. Georgia pest management handbook. Special Bulletin 28:1. University of Herzog, D. C., W. Thomas, R. L. Jensen, and L. D. Newsom. 1975. Georgia, Athens, GA. Association of sclerotial blight with Spissistilus festinus girdling injury on Adams, D. 2008. Peanut insect, p. 20. In Guillebeau, Hinkle, and Roberts soybean. Environmental Entomology 4: 986–988. 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Journal of Entomological Science 23: 333–341. soybeans. Journal of Economic Entomology 78: 829–834. Johnson, M. P., and A. J. Mueller. 1988. Threecornered alfalfa hopper re- Russin, J. S., J. Boethel, G. T. Berggren, and J. P. Snow. 1986. Effects of gir- sponse to six sticky trap colors. Southwestern Entomologist 13: 101–105. dling by the threecornered alfalfa hopper on symptom expression of soy- Johnson, M. P., and A. J. Mueller. 1989. Flight activity of threecornered al- bean stem canker and associated soybean yields. Plant Disease 70: falfa hopper (Homoptera: Membracidae) in soybean. Journal of Economic 759–761. EntomoIogy 82: 1101–1105. Russin, J. S., D. Newsom, D. J. Boethel, and A. N. Sparks. 1987. Multiple pest Johnson, M. P., and A. J. Mueller. 1990. Flight and diel activity of the complexes on soybean: Influences of threecornered alfalfa hopper injury on Threecornered Alfalfa Hopper (Homoptera: Membracidae). Environmental pod and stem blight and stem anthracnose diseases and seed vigor. Crop Entomology 19: 677–683. Protection 6: 320–325. Jordan, C. R. 1952. The biology and control of the threecornered alfalfa Smith, F. F. 1933. The nature of the sheath material in the feeding punctures hopper,Spissistilus festinus (Say). Ph. D. dissertation, Texas A&M produced by the potato leaf hopper and the three-cornered alfalfa hopper. University, College Station. Journal of Agricultural Research 47: 475–485. King, D. R., A. Harding, and B. C. Langley.1961. Peanut insects in Texas. Sparks, A. N., and L. D. Newsom. 1984. Evaluation of the pest status of the Texas Agricultural Experiment Station Miscellaneous Publication. Texas Threecornered Alfalfa Hopper (Homoptera: Membracidae) on soybean in Agricultural Experiment Station, College Station, TX. Louisiana. Journal of Economic Entomology 77: 1553–1558. Kogan, M., and D. C. Herzog. 1980. Sampling methods in soybean entomol- Sparks, A. N., and D. J. Boethel. 1987a. Late-season damage to soybeans by ogy. Springer-Verlag, New York, NY. Threecornered Alfalfa Hopper (Homoptera: Membracidae) adults and McPherson, R. M., L. Wells, and C. S. Bundy. 2001. Impact of the early soy- nymphs. Journal of Economic Entomology 80: 471–477. bean production system on arthropod pest populations in Georgia. Sparks, A. N., and D. J. Boethel. 1987b. Evaluation of sampling techniques Environmental Entomology 30: 76–81. and development of sequential sampling plans for Threecornered Alfalfa Meisch, M. V. 1964. Life history of the threecornered alfalfa Hopper (Homoptera: Membracidae) on soybeans. Journal of Economic hopper,Spissistilus festinus (Say) and evaluation of the uses of chemicals and Entomology 80: 369–375. resistant alfalfa varieties for its control. M.S. Thesis. Texas A&M Spurgeon, D. W., and T. P. Mack. 1990. Development and survival of University, College Station. Threecornered Alfalfa Hopper (Homoptera: Membracidae) nymphs at con- Meisch, M. V., and N. M. Randolph. 1965. Life-history studies and rearing stant temperatures. Environmental Entomology 19: 229–233. techniques for the Three-Cornered Alfalfa Hopper. Journal of Economic Spurgeon, D. W., and A. J. Mueller. 1991. Sampling methods and spatial dis- Entomology 58: 1057–1059. tribution patterns for threecornered alfalfa hopper nymphs (Homoptera: Mitchell, P. L., and L. D. Newsom. 1984a. Histological and behavioral studies Membracidae) on soybean. Journal of Economic Entomology 84: of threecornered alfalfa hopper (Homoptera: Membracidae) feeding on soy- 1108–1116. bean. Annals of the Entomological Society of America 77: 174–181. Spurgeon, D. W., and A. J. Mueller. 1992. Girdle and plant part associations Mitchell, P. L., and L. D. Newsom. 1984b. Seasonal history of the of Threecornered Alfalfa Hopper nymphs (Homoptera: Membracidae) on Threecornered Alfalfa Hopper (Homoptera: Membracidae) in Louisiana. soybean. Environmental Entomology 21: 345–349. Journal of Economic Entomology 77: 906–914. Spurgeon, D. W., and A. J. Mueller. 1993. Soybean leaf responses to threecor- Moellenbeck, D., and S. Quisenberry. 1991. Effects of nymphal populations nered alfalfa hopper petiole girdling. Entomologia Experimentalis Et of Three cornered Alfalfa Hopper (Homoptera: Membracidae) on ‘Florida Applicata 67: 209–216. 77’ alfalfa plants. Journal of Economic Entomology 84: 1889–1893. Stewart, S., and A. McClure. 2016. Insect control recommendations for field Moellenbeck, D. J., S. Quisenberry, and M. W. Alison. 1993. Resistance of al- crops. UT Extension Institute of Agriculture. University of Tennessee, falfa cultivars to the Threecornered Alfalfa Hopper (Homoptera: Tennessee. Membracidae). Journal of Economic Entomology 86: 614–620. Studebaker, G. 2016. Insecticide recommendations for Arkansas. University Moore, G. C., and A. J. Mueller. 1976. Biological observation of threecor- of Arkansas, Division of Agriculture, Research and Extension. 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Georgia plant disease loss estimates 2013. Athens, and field study. Journal of Economic Entomology 80: 185–189. GA: UGA Extension Annual Publication, pp. 102–106. Downloaded from https://academic.oup.com/jipm/article-abstract/8/1/10/3745632 by Ed 'DeepDyve' Gillespie user on 13 July 2018 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Journal of Integrated Pest Management Oxford University Press

Biology and Management of the Threecornered Alfalfa Hopper (Hemiptera: Membracidae) in Alfalfa, Soybean, and Peanut

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Abstract

The threecornered alfalfa hopper, Spissistilus festinus (Say) (Hemiptera: Membracidae), was first described in 1831. Since its discovery, it has been observed feeding on> 20 plant species across seven plant families; pre- ferred hosts include species in the family Fabaceae. Spissistilus festinus has been identified as a serious eco- nomic pest of alfalfa, Medicago sativa L.; soybean, Glycine max L; and recently peanut, Arachis hypogaea L. Damage by S. festinus results from feeding and girdle formation on the plant stems; stem girdles inhibit the transportation of photosynthate through the phloem. Photosynthates accumulate above girdles, and the insects feed preferentially at these locations. Girdles can also reduce the structural stability of stems, resulting in signif- icant stand loss in extreme circumstances. The timing of chemical applications for management of S. festinus is critical for successfully reducing insect populations, but information regarding S. festinus’ economic impact in modern alfalfa, soybean, and peanut production systems is scarce. The following is a review of the biology, life history, distribution, pest status, and management of S. festinus on alfalfa, soybean, and peanut. Key words: threecornered alfalfa hopper, Spissistilus festinus, soybean, peanut, alfalfa Biology (Mitchell and Newsom 1984a, Rice and Drees 1985). The number of eggs laid in each slit varies by plant species. In soybean, ap- Description and Behavior proximately six eggs are laid per slit, but in alfalfa, Medicago sat- The Spissitilus festinus (Say) adult is light green and 6–7 mm long, iva L., 1–2 eggs were found per slit (Wildermuth 1915, Jordan with an elongated pronotum that extends to the tip of the abdomen 1952). Meisch and Randolph (1965) reported that oviposition (Wildermuth 1915). Spissistilus festinus receives its common name slits damage tissue and can be harmful to plants when oviposition from its pronotum; when observed from the front (Fig. 1A), it pos- is heavy. sesses three corners, one at each “shoulder” and one at the apex of Spissistilus festinus undergoes hemimetabolous development. It the pronotum. Adult males (Fig. 2A) are readily distinguishable progresses through four to six instars depending on nutrition and from females (Fig. 2B) by a red tint on the dorsal surface of the weather conditions; five total instars is most commonly reported male’s pronotum, marginally smaller male body size, and lack of an (Wildermuth 1915, Moore and Mueller 1976, Deitz and Wallace ovipositor (Fig. 1B; Wildermuth 1915). 2012). The first and second instars (Fig. 2B and C) are 1.6 mm and Eggs (Fig. 3A) range in size from 0.9 to 1.3 mm long. They are 2.1 mm in length, respectively; they are pale green or straw colored, white in color and oblong in shape, with one end larger than the with a series of dorsal spine-like protrusions. At each successive other. The larger end of the egg is covered in papillae, which are nymphal stage, the spines grow and develop divergent lateral spurs thought to secure the egg within the plant tissue (Wildermuth 1915). that occur along the length of each spine. Wing pads and pro- Eggs are inserted under the epidermis in a slit created by the oviposi- nounced development of the pronotum appear in the third nymphal tor (Fig. 4). Oviposition behavior has been shown to vary depending stage; third instars (Fig. 2D) are darker yellow-brown color with on the host species and the maturity of that species. For example, in green markings, and are 2.9 mm in length. Fourth and fifth instars soybean, Glycine max L., oviposition occurs near the base of the (Fig. 2E and F) are similar in appearance and grow progressively main stem early in the season (Wildermuth 1915), and occurs in greener with pronounced wing pads, dorsal spikes, and pronotum. softer tissues such as terminals and nodes as the season progresses V C The Authors 2017. Published by Oxford University Press on behalf of Entomological Society of America. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact Downloaded from https://academic.oup.com/jipm/article-abstract/8/1/10/3745632 journals.permissions@oup.com 1 by Ed 'DeepDyve' Gillespie user on 13 July 2018 2 Journal of Integrated Pest Management, 2017, Vol. 8, No. 1 Fig. 1. (A) Frontal perspective of adult S. festinus, exhibiting the three corners at the “shoulders” and dorsally. (B) Ventral perspective showing female (left) and male (right) S. festinus. Fig. 2. Side by side perspective of adult S. festinus displaying sexual dimorphism. Males (A) possess a red coloration that runs along the dorsal edges of the pronounced pronotum. Females (B) possess a slight red tinge posteriorly on the pronotum, as well as an elongated abdomen. Third through fifth instars are more mobile than the first and However, Mitchell and Newsom (1984b)and Newsom et al. (1983) second instars (Wildermuth 1915). When disturbed, nymphs will documented that sex ratios vary throughout the season; the proportion sometimes produce a globule from the abdomen as a defense mecha- of males to females was equal at overwintering habitats. The first mi- nism and quickly move to the opposite side of the stem (Wildermuth gration skews the ratio toward females, suggesting that only the fe- 1915). Adults will also attempt to conceal themselves in a similar males migrate from overwintering sites. Ratios equalize after the first manner, though they commonly fly away when disturbed spring generation (Mitchell and Newsom 1984b, Newsom et al. 1983). (Wildermuth 1915). Adults generally fly within 33 cm above the soil An egg-laying female can be found with an average of 21–30 eggs in or just above the plant canopy (Johnson and Mueller 1989, 1990). her ovaries at any one time, and can produce up to 220 eggs over her lifetime (Mitchell and Newsom 1984b). Life History The embryo’s development lasts from 6 to 27 d, with an average Spissistilus festinus can have multiple generations per year depending of 16.5 d from oviposition to eclosion (Meisch and Randolph 1965). on weather conditions and availability of host plants (Wildermuth The first three instars are completed in 3–5 d each, depending on 1915, Mitchell and Newsom 1984b). Adults overwinter in a state of temperature, humidity, and nutrition. The fourth and fifth instars reproductive diapause (Newsom et al. 1983, Mitchell and Newsom last 4–8 d each (Wildermuth 1915, Jordan 1952, Meisch and 1984b), though reproduction has been reported to continue during Randolph 1965, Spurgeon and Mack 1990). Total nymphal develop- mild winters (Wildermuth 1915). A nascent adult female reaches sex- ment time has been shown to vary with temperature. Wildermuth ual maturity in 7–14 d; she will mate and lay eggs soon after (Jordan (1915) observed that nymphal development required 69 and 32 d when 1952, Meisch 1964, Meisch and Randolph 1965). Males reportedly mean temperatures were 16 C and 30 C, respectively. Other reports die soon after copulation, but females live for an average of 38.6 d estimate development time to be 18–24 d at temperatures of 32 Cand postcopulation (Mitchell and Newsom 1984b). Wildermuth (1915) re- 26.6 C and 75–80% relative humidity (Jordan 1952, Meisch 1964, ported that populations generally consist of more males than females. Meisch and Randolph 1965, Spurgeon and Mack 1990). Downloaded from https://academic.oup.com/jipm/article-abstract/8/1/10/3745632 by Ed 'DeepDyve' Gillespie user on 13 July 2018 Journal of Integrated Pest Management, 2017, Vol. 8, No. 1 3 Fig. 3. Life stages of the S. festinus.(A) Egg (B–F) Instars 1–5. suitable habitat for breeding and development (Moellenbeck et al. 1993, Deitz and Wallace 2012). The host range of S. festinus consists of many plant species in a number of families. The insect was first identified as a potential pest of tomato in personal communications between Oemler and the University of Georgia in 1888 (Oemler 1888). Cockerell (1899) first reported S. festinus as a pest on alfalfa 11 yr later. The known host range of S. festinus includes alfalfa; cowpeas, Vigna unguiculata (L.); clover, Trifolium spp; various trees; shrubs; grasses; herbs; sug- arcane, Saccharum officinarum L.; potato, Solanum tuberosum L.; cotton, Gossypium hirsutum L.; and field pea, Pisum sativum L. (Wildermuth 1915, Van Zwaluwenburg 1926, Swezey 1937). Plant species in the Fabaceae have been shown to be better reproductive and developmental hosts, and the insect is considered an economic pest of alfalfa, soybean (Caviness and Miner 1962, Tugwell et al. 1972, Mitchell and Newsom 1984a, Sparks and Newsom 1984, Sparks and Boethel 1987a, Johnson et al. 1988), and peanut (King et al. 1961, Fig. 4. Eggs of S. festinus in the base of a soybean, G. max, stem. Todd et al. 1979, Andersen et al. 2002, Rahman et al. 2007). In Louisiana, overwintering adults have been observed on pine, Pinus spp.; in spring, adults were found on vetch, Vicia spp. and clover, be- Distribution and Host Range fore moving onto newly emerged soybean (Newsom et al. 1983). Wildermuth (1915) reported that S. festinus had been observed from Ottawa, Canada, to Mexico; this distribution was refined by Caldwell 1949. His description of the different species of Spissistilus Economic Importance using the genitalia revealed that the original reported distribution was based on misidentified Spissistilus species. The upper limits of Direct and Indirect Injury the distribution are closer to the Midwest United States as opposed Spissistilus festinus is a phloem feeder with piercing–sucking mouth- to Canada. In the United States, S. festinus is prevalent in the parts and two distinct feeding behaviors. The first behavior involves Southeast and Midsouth, where the abundance of preferred host sporadic probing and consumption of phloem sap (Andersen et al. plants such as soybean and peanut, Arachis hypogaea L., provides 2002). The other behavior involves the formation of a continuous Downloaded from https://academic.oup.com/jipm/article-abstract/8/1/10/3745632 by Ed 'DeepDyve' Gillespie user on 13 July 2018 4 Journal of Integrated Pest Management, 2017, Vol. 8, No. 1 series of lateral punctures around the circumference of a stem Alfalfa (Wildermuth 1915). Commonly referred to as a girdle (Fig. 5), the Spissitilus festinus was first described as a pest of alfalfa in 1899 aforementioned ring of punctures often results in a gall-like growth (Cockerell 1899). Alfalfa is a perennial forage and hay crop that can (Fig. 5A) in the area surrounding the feeding site (Wildermuth be harvested multiple times a year, but S. festinus feeding girdles can 1915). Smith (1933) found that after the insect feeds, insoluble sali- cause significant loss in quality of the new growth (Wilson and vary sheaths are left in the plant tissue. Mitchell and Newsom Quisenberry 1987). Entire fields can require reseeding when heavy (1984a) discovered that it is these sheaths that disorganize and dis- infestations result in high stem girdle counts owing to the persistent rupt the vascular bundles of the phloem, as well as induce cellular nature of the girdles (Graham and Ellisor 1938). hyperplasia (Johnson et al. 1988). Multiple studies across different Spissistilus festinus has multiple and overlapping generations an- plant species have shown that the third through fifth instars (as well nually on alfalfa, with two population peaks occurring late June to as adults) are capable of creating stem girdles (Meisch and early July and late August through September in Louisiana (Farlow Randolph 1965, Moore and Mueller 1976, Mitchell and Newsom et al. 1981, Moellenbeck et al. 1993). The latter peak is often much 1984a, Andersen et al. 2002). greater than the former, and as a result, the amount of damage to Girdling interrupts the flow of nutrients in the phloem and the new growth can be considerable (Wilson and Quisenberry causes an accumulation of photosynthates in the area above the gir- 1987). Nymphs in a greenhouse study did not have any measurable dle (Osborn 1911, Wildermuth 1915, Mitchell and Newsom 1984a, effect on “Florida 77” alfalfa at one and three nymphs per plant Andersen et al. 2002). Andersen et al. (2002) reported that many of (Wilson and Quisenberry 1987). However, when the densities in- the amino acids that increase in concentration above the stem gir- creased to six nymphs per plant, protein content decreased, fiber dle are likely the result of plant responses to feeding and are not density increased, and root carbohydrate levels decreased essential to insect development. Nevertheless, concentrations of (Moellenbeck and Quisenberry 1991). Although overall dry weight amino acids required for S. festinus development are also elevated was not affected, the quality of harvested hay was reduced. It is pos- by the girdling process (Andersen et al. 2002). On peanut and sible that the regrowth capability of the plants was affected owing other host plants, nymphs gather within 5 mm above the girdle, to reduced root carbohydrate concentrations (Moellenbeck and andfeed forupto7d (Moellenbeck and Quisenberry 1991, Quisenberry 1991). Andersen et al. 2002). New girdles are formed above existing gir- Currently, S. festinus is not considered a major pest of alfalfa. dles, and nymphs will relocate to continue feeding (Moellenbeck The insect is either not mentioned (Undersander et al. 2011, and Quisenberry 1991, Andersen et al. 2002). In alfalfa and soy- Whitworth et al. 2015) or is described as a minor, occasional pest bean, heavy girdling reduces the forage quality owing to lowered (Summers et al. 2007) in the most recently published alfalfa pest levels of carbohydrates and amino acids, as well as increased lev- management handbooks. Recent pest management handbooks for els of detergent fibers (Wilson and Quisenberry 1987, Tennessee, Georgia, and Alabama suggest that insecticides may be Moellenbeck and Quisenberry 1991). needed if adults or nymphs are present on 10% of seedlings and Nutrient loss is not the only consequence of girdling. Girdles on young plants (up to 10–12 inches tall) or if 10% of lateral stems are the main stem of soybean seedlings can impact the structural stabil- being killed from damage (Flanders and Everest 2014, Buntin 2016, ity of the plant, leaving the girdled stem susceptible to lodging from Stewart and McClure 2016). For older plants, an economic thresh- wind and mechanical disturbance (Sparks and Boethel 1987a). In old of two adults or nymphs per sweep with a 0.38-m sweep net has peanut, which has a more prostrate growth habit and multiple been published (Stewart and McClure 2016). In Tennessee, how- branches, stand loss owing to lodging is not a serious concern. ever, a study showed that a 25% reduction in stand count did not Sparks and Newsom (1984) speculated that high levels of late-sea- cause any economic impact in alfalfa (Bates et al. 2005). son petiole feeding could lead to leaf death and reduce both effective leaf area and yield in soybean. Spissistilus festinus damage has been linked to an increase in the Soybean likelihood of disease complexes in soybean. Herzog et al. (1975) ob- Spissistilus festinus has long been considered a pest of soybean. It served increased incidence of blight caused by Sclerotium rolfsii was first detected on soybean in the early 1900s, but significant (Sacc.) infection in girdled versus nongirdled stems. Although S. fes- damage was not reported until 1957 (Caviness and Miner 1962). It tinus did not actively transmit the pathogen, the presence of girdles was initially thought that yield loss resulted from early-season gir- close to the soil where S. rolfsii occurred significantly increases fre- dling of the main stem (V1–V5 growth stages). The damage to the quency of infection. Sclerotium rolfsii is one of the most damaging main stem caused large swathes of soybean plants to lodge. peanut pathogens. It can cause up to 12% yield loss in Georgia, However, Caviness and Miner (1962) found evidence that lodging where losses and accompanying treatment costs associated with S. had minimal effects on yield. Artificially reduced stands had the rolfsii are estimated to be US$41 million annually (Woodward highest loss in yield (up to 15%) when stand loss occurred after 2010, 2011, 2012, 2013). No work has been published on the inter- bloom, and less yield loss (up to 7%) when damage occurred 2 wk action of S. festinus infestation and S. rolfsii incidence in peanut, but prior to bloom. It should be noted that lodging simulations in this it should be noted that S. rolfsii incidence in soybean increases with study were evenly distributed throughout the plots, allowing max- mechanical damage. Therefore, S. festinus infestation on peanut imum compensation from adjacent plants. In studies simulating could increase the occurrence of infection (Herzog et al. 1975, the effect of early-season S. festinus girdling of main stems, Cook Russin et al. 1986). A study of soybean with symptoms of stem can- et al. (2014) found that yield of indeterminate Maturity Group IV ker, Diaporthe phaseolorum (Cke. and Ell.), found that girdle pres- soybean was significantly reduced by stand loss occurring from R1 ence resulted in larger cankers and reduced yields (Russin et al. to R5. Yield response was inconsistent across reproductive growth 1986). Russin et al. (1987) found that girdles on soybean did not in- stages in this study, and it is unknown what levels of insect gir- crease infection rate of pod or stem blight, Phomopsis sojae and dling would result in the rates of stand loss tested. Bailey (1975) Colletotrichum truncatum (Schw.), but did increase symptom sever- reported a yield reduction of >14 bushels per acre when S. festinus ity of both diseases and reduced yields. adults were caged at densities of four adult insects per plant Downloaded from https://academic.oup.com/jipm/article-abstract/8/1/10/3745632 by Ed 'DeepDyve' Gillespie user on 13 July 2018 Journal of Integrated Pest Management, 2017, Vol. 8, No. 1 5 Fig. 5. Girdles on peanut, A. hypogaea.(A) Stem girdle resulting in gall formation as well as adventitious root growth. (B) Spissitilus festinus nymph forming a girdle on a peanut leaf petiole. compared with one adult per five plants on 1.5–2-inch tall soy- Boethel (1987a) found that yield reductions occurred at 60% of the bean seedlings. aforementioned threshold, and introduced the hypothesis that pod or The number of generations of S. festinus occurring annually in peduncle feeding contributes more to yield loss than petiole girdling. soybean varies. Mueller (1980) found three overlapping genera- A relatively recent shift from traditional timings of soybean tions, whereas Mitchell and Newsom (1984b) found only two. planting (late May and early June) to early-season planting (mid- These differences suggest that the number of generations occurring April) occurred in the midsouthern United States primarily as an ef- annually fluctuates and is likely affected by local environmental fort to avoid periods of drought (Heatherly 1998). This early soy- conditions. When observing the effects of individual generations bean production system (ESPS) incorporates earlier maturing on the host, Sparks and Newsom (1984) found that early-season varieties and can result in greater yield, and can result in less late- damage (when there is the highest danger of lodging from girdles season damage resulting from caterpillar feeding compared with the on the main stem) did not significantly impact yield. However, traditional production system (Heatherly 1998). Early-planted soy- Bailey (1975) found significant reduction in yield at a rate of one bean production may affect many of the previously established eco- hopper per plant when plants were 1.5–2.0 inches tall, indicating nomic thresholds for pests of soybean, including S. festinus. In ESPS, that it is possible that damage occurring in the early season has the S. festinus populations are higher early in the season, and late season capability to impact yield. No difference in yield between individ- infestations are largely avoided (Bauer et al. 2000, McPherson et al. ual girdled and nongirdled plants was observed, indicating that 2001). Pulakkatu-Thodi (2010) and Ramsey (2015) were unable to lodging is a cause of yield reduction when girdling rates are high. observe any impact on yield in reproductive, early-planted soybeans, Nevertheless, Caviness and Miner (1962) artificially removed as a result of adult numbers at 3 the established threshold of one plants from the stand and demonstrated that soybeans have in- adult per sweep. Infestations occurring prior to or after pod fill ap- credible compensatory power. Mueller and Jones (1983) showed pear to have little or no consistent effect on yield. It should be noted that yield was reduced only when 70% or more of plants had a that only adults were included in both of these studies, and as such, main stem girdle. The lack of yield response at lower feeding levels the full impact of S. festinus in contemporary early-planted season was attributed to compensation and high seeding rates (12 seed soybean production systems is as of yet undetermined. There are no per 0.33 m row). In one study, late season damage during the sec- recently published or validated thresholds for S. festinus on early- ond in-field generation of S. festinus resulted in significant reduc- planted soybean. tions in yield (Sparks and Boethel 1987a). This result was most likely related to S. festinus feeding on the succulent petioles, pe- duncles, and pedicels after the soybean’s R1 stage (Mitchell and Peanut Newsom 1984a). Though nutrient flow on a girdled petiole re- Spissistilus festinus has been observed feeding on peanut for the past sumes after 10 d (Spurgeon and Mueller 1993), the damage may half-century, though there have been no intensive investigations of be enough to decrease the number of seedpods produced or the its economic impact (King et al. 1961, Todd et al. 1979). In Georgia number of seed per pod, thereby reducing yield (Sparks and and surrounding states, growers now see S. festinus in great abun- Newsom 1984). dance in peanut fields, and there are concerns about possible yield The first economic threshold for S. festinus was established by loss associated with feeding. Though there have been estimates of Sparks and Newsom (1984), who determined that one adult per sweep the economic impact of S. festinus in peanut ranging from US$1.5 at soybean pod set until leaf yellowing is enough to cause economic million in yield loss (Brown et al. 1997) to no impact other than damage and should be treated. This threshold was based on the hy- treatment costs (Adams 2008), no science-based economic injury pothesis that late season damage consisting of mostly petiole girdling level has been determined. is the cause of significant yield loss. Sparks and Newsom (1984) also Two nymphal S. festinus population peaks are observed in pea- hypothesized that when the threshold for adults is met, the nymphs nut annually in the Southeast. The first generation of nymphs ap- have already done a substantial amount of damage. Sparks and pears in late June to early August after an initial appearance of Downloaded from https://academic.oup.com/jipm/article-abstract/8/1/10/3745632 by Ed 'DeepDyve' Gillespie user on 13 July 2018 6 Journal of Integrated Pest Management, 2017, Vol. 8, No. 1 Table 1. Insecticides registered for management of S. festinus in Alfalfa (Georgia Pest Management Handbook–2016 Commercial Edition) Insecticide AI Common names Insecticide Type IRAC Amount/acre Lbs AI/acre REI/PHI Alpha-cypermethrin Pyrethroid 3A Fastac 0.83 2.2–3.8 fl oz 0.012–0.025 12 h/3 d Beta-cyfluthrin Pyrethroid 3A Baythroid XL 1.0EC 1.6–2.8 fl oz 0.0125–0.022 12 h/7 d Carbaryl Carbamate 1A Sevin 80S 1.25 lb 1.0 12 h/48 d Sevin XLR Plus, 4F 1.0 qt 1.0 Cyfluthrin Pyrethroid 3A Tombstone 2.0 1.6–2.8 fl oz 0.025–0.044 12 h/7 d Gamma-cyhalothrin Pyrethroid 3A Declare 1.25 1.02–154 fl oz 0.01–0.015 12 h/ Proaxis 0.5 2.56–3.84 fl oz 0.01–0.015 7 d Lambda-cyhalothrin Pyrethroid 3A Karate Zeon 2.08 1.28–1.92 fl oz 0.02–0.03 12 h/ Silencer 1 2.56–3.84 fl oz 0.02–0.03 7 d Zeta-cypermethrin Mustang MAX, Pyrethroid 3A 12 h/ Respect 0.8EC 2.24–4.0 fl oz 0.014–0.025 3 d aRe-entry interval/plant harvest interval. adults, and the second generation develops during late August into field; therefore, plant injury can be assessed within 10 m of field bor- early September (Rahman et al. 2007). The majority of girdling oc- ders to adequately estimate whole field injury levels according to curs 3 wk after the initial appearance of nymphs in June (Rahman Rahman et al (2007). Whole plant observations provide an accurate et al. 2007); this coincides with the approximate development time assessment of nymph populations (Spurgeon and Mueller 1991), but from eclosion to fourth instar (Meisch 1964, Meisch and Randolph this method is impractical for IPM because of the time required for 1965, Spurgeon and Mack 1990). The fourth instar is thought to be each sample. Beat sheet sampling is less time consuming than whole responsible for most of the girdling in peanut (Moore and Mueller plant observations, but it is not ideal for detecting the younger, 1976, Johnson and Mueller 1988). smaller nymphs in soybean, as their small mass reduces the chance Although S. festinus is capable of girdling peanut, no published of dislodging from the plant (Spurgeon and Mueller 1991). The beat reports correlate peanut damage with yield loss. Andersen et al. (2002) net (Sparks and Boethel 1987b) and vertical beat sheet (Drees and reported reduced biomass, nitrogen content, and carbon content in gir- Rice 1985) are alternatives to the beat sheet for sampling nymphs. dled peanut stems in northern Florida, but this effect was not consistent The former involves utilizing a standard 33-cm sweep net held at a over years of the study. Spissistilus festinus damage, characterized by 45-degree angle to the plant base; the plant is then beat into the net number of girdles, was shown to vary by cultivar, with runner-type at 10 different locations in the field. The latter method involves a Georgia Green and Virginia-types AT VC2, GA-HI-O/L, Virugard, similar technique, where a beat sheet is held parallel to the plants, Wilson, and Phillips being particularly susceptible. Nevertheless, no with a trough at the bottom to collect the nymphs that are shaken or measurable effect on yield was detected from girdling alone, with dam- beaten off the plant. Sparks and Boethel (1987b) utilized these meth- age rates up to six girdles per plant (Rahman et al. 2007). ods to good effect for sampling S. festinus nymphs, finding that the The economic injury level for S. festinus in peanut is unknown, beat net was the most efficient and effective. and there are no experimentally validated economic thresholds. Adult populations can be assessed effectively with a sweep net in However, at least one set of anecdotal thresholds has been reported, soybean (Kogan and Herzog 1980) and peanut (Rahman et al. where one adult per 6 feet of row at 75 d prior to digging or one adult 2007). Adults can also be monitored in soybean with yellow sticky or nymph per 3 feet of row 25–75 d prior to digging warrants treat- traps (Johnson and Mueller 1988) placed 33 cm above the ground or ment (Brown 2006). Preliminary studies conducted recently at the at just above canopy level (Johnson and Mueller 1989); however, University of Georgia suggest that these thresholds overestimate the trap counts were not as accurate as sweep samples for predicting ac- economic impact of S. festinus and trigger insecticide applications at tual field populations (Johnson and Mueller 1988, Johnson and population levels that are not yield limiting. It is important to know Mueller 1990). at what point S. festinus damage impacts peanut yield. Growers in the Southeastern United States currently treat S. festinus as a pest and manage populations with insecticides. The broad-spectrum insecti- Sampling Timing cidesusedtotarget S. festinus can flare secondary pests, negatively Critical sampling periods differ from crop to crop and may even impact natural enemies and pollinators, and reduce net profits when vary within a crop depending on production practices as with soy- applied unnecessarily (Ware 1980, Adams 2008). bean planting date. Feeding in alfalfa was most injurious during the second population peak (Wilson and Quisenberry 1987). Managing S. festinus in alfalfa requires monitoring plant stands for stem death resulting from girdles, as well as monitoring for sudden increases in Monitoring populations of S. festinus adults. Sampling Methods Though the economic impact of S. festinus in modern U.S. soy- In soybean (Sparks and Boethel 1987a) and peanut (Rahman et al. bean production systems is not clear, research suggests the crop may 2007), S. festinus females are randomly distributed throughout the be vulnerable to damage at distinct development periods. Prior to Downloaded from https://academic.oup.com/jipm/article-abstract/8/1/10/3745632 by Ed 'DeepDyve' Gillespie user on 13 July 2018 Journal of Integrated Pest Management, 2017, Vol. 8, No. 1 7 Table 2. Insecticides registered for management of S. festinus in Soybean (2016 Insecticide Recommendations for Arkansas [Studebaker]) Insecticide AI Common names Insecticide Type IRAC Amount/acre Lbs AI/acre REI/PHI Beta-cyfluthrin Pyrethroid 3A Baythroid XL 1.0EC 1.6–2.8 fl oz 0.013–0.022 12 h/45 d Clothianidin Neo-nicotinoi 4A Belay 2.13 EC d 3–6 fl oz 0.05–0.1 12 h/21 d Cyfluthrin Pyrethroid 3A Tombstone 2 EC 1.6–2.8 fl oz 0.025–0.044 12 h/45 d Esfenvalerate Carbamate 1A Asana XL 0.66 EC 5.8–9.6 fl oz 0.03–0.05 12 h/21 d Gamma-cyhalothrin 1.25 Pyrethroid 3A Prolex/Declare CS 0.77–1.28 fl oz 0.0075–0.013 12 h/30 d Lambda-cyhalothrin Pyrethroid 3A Karate Zeon 2.08 CS 0.96–1.6 fl oz 0.015–0.025 12 h/30 d Lambda-cyhalothrin þchlorantranilipole Pyrethroid 3A Diamide 28 Beseige 1.252 5.0–8.0 fl oz 0.049–0.08 12 h/30 d Zeta-cypermethrin Pyrethroid 3A Mustang Maxx 2.8–4.0 fl oz 0.0175–0.25 12 h/21 d Zeta-cypermethrin þ bifenthrin Pyrethroid 3A Hero 1.24 EC Pyrethroid 3A 4.0–10.3 fl oz 0.04–0.1 12 h/21 d aRe-entry interval/plant harvest interval. Table 3. Insecticides registered for management of S. festinus in peanut (Georgia Pest Management Handbook–2016 Commercial Edition) Insecticide AI Common names Insecticide Type IRAC Amount/acre Lbs AI/acre REI/PHI Carbaryl Carbamate 1A Sevin 80S 1.25 lb 1.0 12 h/48 d Sevin XLR Plus, 4F 1.0 qt 1.0 Bifenthrin Pyrethroid 3A Brigade 2EC 2.1–6.4 fl oz 0.33–0.1 12 h/14 d Beta-cyfluthrin Pyrethroid 3A Baythroid XL 1.0EC 1.6–2.8 fl oz 0.0125–0.022 12 h/7 d Lambda-cyhalothrin Pyrethroid 3A Karate Zeon 2.08 1.28–1.92 fl oz 0.02–0.03 12 h/7 d Silencer 1 2.56–3.84 fl oz 0.02–0.03 aRe-Entry Interval/Plant Harvest Interval. the shift to early-season planting, the critical sampling and treatment time is unknown, using adults as a predictor of damage could over period to prevent early-season damage resulting from main stem gir- or under estimate the impact of S. festinus. dles in soybean was when the plants were around the V3 stage (Spurgeon and Mueller 1992). Averting late-season damage in soybean Management required sampling for S. festinus populations before V12 growth stage (Fehr et al. 1971, Spurgeon and Mueller 1992). Sparks and Newsom’s Insecticides are the most effective tool to quickly reduce S. festinus 1984 treatment threshold in soybean was based on the observation populations in the crops discussed here. Pyrethroid and organophos- that economic losses could occur from pod set to leaf yellowing. phate insecticides are commonly recommended, though published Additional research is needed to quantify the economic impact of S. efficacy of individual products in these classes varies. There are no festinus on soybean and to determine optimal monitoring time(s). recent, experimentally validated economic thresholds for S. festinus Rahman et al. (2007) recommend monitoring peanut for nymph in any crop. Because most of the damage caused by threecornered al- and girdle presence in the first 2–3 wk of July. Damage increased in falfa hopper is attributed to feeding by the third, fourth, and fifth in- the third week of July, after consistent weekly increases in nymph stars (Andersen et al. 2002), management strategies should focus on numbers, indicating that early July is the optimal time for scouting reducing population levels of this life stage. In some crops, it may be nymphs (Rahman et al. 2007). An increase in adult S. festinus abun- possible to prevent infestations of immature stages by targeting im- dance was observed a few weeks before damage levels rose in pea- migrating adults with insecticides. This strategy can fail if adult nut. This is likely a result of the earliest nascent adults from the first movement into a crop occurs over a long period of time and residual generation appearing when the majority of nymphs are still forming insecticide efficacy is short. Applying insecticides only when the girdles. Using these adults as a direct, numerical indicator of injury nymphs are present on a susceptible crop stage is an ideal strategy, may result in an appropriate diagnosis, but only after the damage but accurately assessing nymph populations is difficult. Regardless has been done (Rahman et al. 2007). Because the correlation be- of the life stage targeted by insecticides, coverage of the crop canopy tween the number of adults and nymphs in the field at any given will affect control. Downloaded from https://academic.oup.com/jipm/article-abstract/8/1/10/3745632 by Ed 'DeepDyve' Gillespie user on 13 July 2018 8 Journal of Integrated Pest Management, 2017, Vol. 8, No. 1 Georgia 2006. Miscellaneous Publication Number 106. University of Alfalfa Georgia, Athens, GA. In alfalfa, cultural practices that reduce the impact of S. festinus in- Andersen, P. C., V. Brodbeck, and D. C. Herzog. 2002. Girdling-induced nu- clude increasing seeding rate to mitigate stand loss and removing trient accumulation in above ground tissue of peanuts and subsequent feed- weedy borders around fields to eliminate overwintering sites (Bates ing by Spissistilus festinus, the three-cornered alfalfa hopper. Entomologia et al. 2005). Insecticides listed in the 2015 Georgia Pest Management Experimentalis Et Applicata 103: 139–149. Handbook for management of S. festinus in alfalfa when adults or Bailey, J. C. 1975. Three-cornered Alfalfa Hoppers (Homoptera: nymphs are found on 10% of alfalfa seedlings, or losses exceed 10% Membracidae): Effect of four population levels on soybeans. Journal of the of lateral stems are provided in Table 1 (Buntin 2016). Kansas Entomological Society 48: 519–520. Bates, G., G. Burgess, D. Hensley, M. Newman, and R. Patrick. 2005. Crop profile for alfalfa in Tennessee. Regional IPM Centers. (http://www.ipmcen Soybean ters.org/cropprofiles/docs/TNalfalfa.pdf) (accessed 3 April 2017). Spissistilus festinus is still regarded as a soybean pest, though recent Bauer, M. E., J. Boethel, M. L. Boyd, G. R. Bowers, M. O. Way, L. G. studies suggest its pest status may have diminished in the early-soy- Heatherly, J. Rabb, and L. Ashlock. 2000. Arthropod populations in early bean production system (Pulakkatu-Thodi 2010, Ramsey 2015). soybean production systems in the Mid-South. Environmental Entomology Current soybean thresholds may not be valid for early-soybean pro- 29: 312–328. duction systems, and the lack of consistency found in state manage- Brown, S. L. 2006. Threecornered alfalfa hopper damage continues to ment guides is indicative of the lack of consensus regarding the increase. In E.P. Prostko (ed.), 2016 Peanut Update. Athens GA: UGA insect’s pest status. The thresholds published in the 2016 Insecticide Extension Publication CSS-06-0115. p.69. Brown, S. L., D. C. Jones, and J. W. Todd. 1997. Peanut Insects, p. 28. In D. Recommendations for Arkansas (Studebaker 2016) recommend G. Riley, G. K. Douce, and R. M. McPherson (eds.), Summary of losses treatment when "50% of the plants are girdled, or if fewer than 4–6 from insect damage and costs of control in Georgia 1996. (http://www. ungirdled plants per row foot remain in conventional rows, 30 bugwood.org/sl96/images/Sl96.pdf) (accessed 3 April 2017). [inches] to 38 [inches], and hopper nymphs are still present” for Buntin, D. 2016. Alfalfa insect control, pp. 108–112. In D. Horton (ed.), plants still under 10”. Insecticides recommended by the University Georgia pest management handbook. Special Bulletin 28:1. University of of Arkansas in 2016 for management of S. festinus in soybeans are Georgia, Athens, GA. given in Table 2. These recommendations and those published by Caldwell, J. S. 1949. A generic revision of the treehoppers of the tribe Ceresini Mississippi State University include neonicotinoid seed treatments in America north of Mexico, based on a study of the male genitalia. which can provide control of S. festinus for 3–4 wk (Catchot 2016). Proceedings of the United States Natural Museum 98: 491–521. A recently published survey of U.S. soybean producers showed that Catchot, A. 2016. 2016 Insect control guide for aronomic crops. Mississippi State University, Publication Number 2471, pp. 22–44. 51% used insecticide (neonicotinoid) seed treatments (Hurley and Caviness, C. E., and F. D. Miner. 1962. Effects of stand reduction in soybeans Mitchell 2017). Only 1.4% of survey respondents indicated that simulating Three-Cornered Alfalfa Hopper injury. Agronomy Journal 54: they actively managed S. festinus, but no Southeastern soybean 300–302. growers were included in the study. Louisiana State University rec- Chapin, J. W. (ed.) 2015. South Carolina pest management handbook 2015: ommends treatment when three or more nymphs or one or more Clemson cooperative extension. Clemson University, South Carolina. adults are present beginning at pod set, and no neonicotinoids are Cockerell, T.D.A. 1899. Some insect pests of Salt River Valley and the reme- included in published recommendations (Davis 2017). dies for them. Arizona Agricultural Experiment Station Bulletin 32: 273–295. Cook, D. R., D. Stewart, J. E. Howard, D. S. Akin, J. Gore, B. R. Leonard, G. Peanut M. Lorenz, and J. A. Davis. 2014. Impactof simulated threecornered alfalfa The impact of S. festinus feeding on peanut is poorly understood. hopper (Hemiptera: Membracidae) induced plant loss on yield of Maturity Clemson Cooperative Extension suggests treating peanut with insec- group IV and V soybean. Journal of Entomological Science 49: 176–189. ticide at 45–60 d after planting to reduce damage caused by S. festi- Davis, J. 2017. Soybean. In Louisiana insect pest management guide. LSU AG nus (Chapin 2015). Though the University of Georgia Cooperative Center Publication, vol. 1838, pp. 40–46. Extension Service has not published validated thresholds or recommen- Deitz, L. L., and M. S. Wallace. 2012. Richness of the Nearctic treehopper dations for optimum treatment timing, growers in Georgia commonly fauna (Hemiptera: Aetalionidae and Membracidae). Zootaxa 3423: 1–26. target S. festinus populations with pyrethroid insecticides. Mississippi Drees, B. M., and M. E. Rice. 1985. The vertical beat sheet: A new device for State University recommends treatment when fresh damage and two in- sampling soybean insects. Journal of Economic Entomology 78: 1507–1510. sects per six-row feet are present (Catchot 2016). The insecticides listed Farlow, R. A., A. Wilson, J. R. Rabb, and K. L. Koonce. 1981. Insects infesting in the Georgia Pest Management Handbook for management of S. fes- alfalfa in northwest Louisiana: Their effect on production, their control with tinus in peanut are given in Table 3 (Abney 2016). insecticides. Louisiana Agricultural Experiment Station Bulletin 731: 1–22. Fehr, W. R., E. Caviness, D. T. Burmood, and J. S. Pennington. 1971. Stage of development descriptions for soybeans, Glycine max (L.) Merrill. Crop Acknowledgments Science 11: 929–931. We thank Stormy Sparks for his critical review of this manuscript. This proj- Flanders, K. L., J. W. Everest (eds.) 2014. Alfalfa: Insect and Weed control rec- ect was supported by the Crop Protection and Pest Management, Applied ommendations for 2014. In Alabama cooperative extension system. Auburn Research and Development Program (award number: 2014-70006-22518) University, Alabama. from the USDA National Institute of Food and Agriculture. Graham, L. T., and L. O. Ellisor. 1938. 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