Critical Reviews in Plant Sciences, 32:458–482, 2013 Copyright C Taylor & Francis Group, LLC ISSN: 0735-2689 print / 1549-7836 online DOI: 10.1080/07352689.2013.809293

Resistance Mechanisms Against Herbivores in Cotton and Their Interactions with Natural Enemies

S. Hagenbucher,1 D. M. Olson,2 J. R. Ruberson,3 F. L. Wackers,¨ 4 and J. Romeis1 1Agroscope Reckenholz-Tanikon¨ Research Station ART, Reckenholzstr. 191, 8046 Zurich, Switzerland 2Crop Protection and Management Research Unit, USDA-ARS, Tifton, Georgia, USA 3Department of Entomology, University of Georgia, Tifton, Georgia, USA 4Lancaster Environment Centre, Lancaster University, LA1 4YQ Lancaster, United Kingdom

Table of Contents

I. INTRODUCTION ...... 459

II. DIRECT RESISTANCE MECHANISMS ...... 461 A. Morphological Traits ...... 461 1. Impact of trichomes on herbivores ...... 462 2. Impact of trichomes on natural enemies ...... 462 B. Plant Secondary Metabolites ...... 463 1. Terpenoids ...... 463 1.1. Terpenoid distribution ...... 463 1.2. Impact of terpenoids on herbivores ...... 464 1.3. Induction of glands and terpenoids ...... 466 2. Impact of other plant metabolites on herbivores ...... 468 3. Impact of secondary plant metabolites on natural enemies ...... 469

III. INDIRECT RESISTANCE MECHANISMS ...... 469 A. Volatiles ...... 469 1. Release of volatile compounds ...... 469 2. Arthropod response to cotton volatiles ...... 470 B. Extrafloral Nectaries ...... 471

IV. -RESISTANT TRANSGENIC COTTON ...... 472

V. INFLUENCE OF ENVIRONMENTAL CONDITIONS ON COTTON ARTHROPOD RESISTANCE ...... 473

Downloaded by [Agroscope Liebefeld Posieux], [Joerg Romeis] at 01:19 04 July 2013 VI. CONCLUSIONS ...... 474

ACKNOWLEDGMENTS ...... 475

REFERENCES ...... 475

Address correspondence to J. Romeis, Agroscope ART, Reckenholzstrasse 59, 8046 Zurich, Switzerland. E-mail: joerg.romeis@ agroscope.admin.ch

458 ARTHROPOD HERBIVORES IN COTTON 459

cluding specialists like the boll weevil, Anthonomus grandis Cotton plants ( Gossypium)aregrownonmorethan30 (Coleoptera: Curculionidae) and polyphagous like He- million hectares worldwide and are a major source of fiber. The liothis/Helicoverpa spp. (: ) (Matthews plants possess a wide range of direct and indirect resistance mech- and Tunstall, 1994). Additionally, cotton supports a high diver- anisms against herbivorous . Direct resistance mecha- sity of entomophagous arthropods: over 600 of preda- nisms include morphological traits such as trichomes and a range of secondary metabolites. The best known insecticidal compounds tors, including dragonflies, beetles, and spiders were reported are the terpenoid gossypol and its precursors and related com- from cotton fields in Arkansas (U.S.) alone (Whitcomb and Bell, pounds. Indirect resistance mechanisms include herbivore-induced 1964). volatiles and extrafloral nectaries that allow plants to attract and Despite intensive pest management, the many arthropod her- sustain natural enemy populations. We discuss these resistance bivores of cotton cause considerable damage (Matthews and traits of cotton, their induction by herbivores, and their impact on herbivores and natural enemies. In addition, we discuss the use of Tunstall, 1994; King et al., 1996). For example, in the United genetically engineered cotton plants to control pest Lepidoptera States, yield losses due to arthropod pests averaged 3.1% be- and the influence of environmental factors on the resistance traits. tween 2006 and 2012 (Figure 1). It needs to be taken into account that even a small percentage of yield loss translates Keywords Bt-cotton, Gossypium, gossypol, host plant resistance, op- into a high economic loss. In 2012 total yield reduction from timal defense theory, plant defense arthropod pests in the United States was 2.04%, represent- ing a loss of >700,000 bales of cotton valued at >381 mil- I. INTRODUCTION lion US$. If management costs are included, the total eco- Cotton (Gossypium spp.) is one of the most important natu- nomic damage was >1 billion US$ (http://www.biochemistry. ral sources of textile fiber, accounting for around 50% of all msstate.edu/resources/cottoncrop.asp). fibers used by humans (Matthews and Tunstall, 1994). The Many key pests of cotton are in the order Lepidoptera, a genus Gossypium belongs to the tribe Gossypiae, together with number of which damage the reproductive organs, and thereby the genera Cephalohibiscus, Cienfuegosia, Gossypioides, Ham- causing severe losses to fiber production. Some of the most pea, Kokia, Lebronnecia and Thespesia (Fryxell, 1979). Among notorious pest species belong to the family Noctuidae, namely other traits, this tribe is characterized by small lysigenous glands the polyphagous New World species Heliothis virescens and (glands formed through cell lysis) on the plants’ surface. The Helicoverpa zea and the Old World and Australasia species genus Gossypium contains around 50 species (Wendell et al., Helicoverpa armigera and Helicoverpa punctigera (the latter 2010) that have evolved in tropical and subtropical parts of occurring only in Australia). The globally distributed pink boll- South and Central America, the Caribbean, Australasia, Africa worm Pectinophora gossypiella (Gelechiidae) is a highly spe- and Oceania (Fryxell, 1979). A distinct group of six Gossyp- cialized cotton herbivore and a serious pest. In the United States, ium species (G. hirsutum, G. barbadense, G. tomentosum, G. however, this species has been nearly eradicated (section IV). lancelotum, G. darwinii and, G. mustelinum) in South and Cen- Other important pests include species, such as E. vitella, tral America are tetraploid, whereas all other cotton species are E. fabia, E. insulana, E. biplaga, and E. cupreoviridis (Noc- diploid (Fryxell, 1979). tuidae), which also act as stem borers, and Diparopsis species Four species of Gossypium are of economic importance: (Noctuidae), which are major cotton pests in Africa. Defoliat- G. hirsutum, G. barbadense, G. arboreum and G. herbaceum. ing caterpillars can also contribute to yield losses, although a They were most likely domesticated independently of one an- healthy cotton plant can tolerate losses of up to 20% of its total other (Fryxell, 1979). Whereas the dominant cultivated cotton leaf area with little or no yield reduction (Sadras and Felton, species is G. hirsutum, the so-called upland cotton, the other 2010). Foliage feeders that can be of considerable importance three Gossypium species are grown only on comparably small include Spodoptera spp. (Noctuidae) and Alabama argillacea areas. accounts for at least 90% of all cotton (Noctuidae). produced (PROTA4U 2013). In the United States, for example, There are few coleopteran pest species of cotton, mostly Downloaded by [Agroscope Liebefeld Posieux], [Joerg Romeis] at 01:19 04 July 2013 it is predicted for 2013 that more than 12 million acres of G. from the family Curculionidae (Matthews and Tunstall, 1994; hirsutum and 238,000 acres, or 1.9%, of G. barbadense (Pima Naranjo et al., 2008), of which A. grandis is devastating to the cotton) will be planted (http://www.cotton.org). More than 33 cotton industry in the Americas. The weevil’s original distribu- million hectares of cotton were grown in 2010, producing ca. tion was probably in Central America. Since the immigration 23 million metric tons of lint and ca. 43 million metric tons of of the weevil into the United States from Mexico (ca. 1890s), seed (http://faostat.fao.org; James, 2011). The top three cotton accumulated costs of control and yield loss reached 15 billion producers are China (5 million hectares, 6 million metric tons US$ (http://www.cotton.org), justifying the initiation of the boll of lint), India (11.1 million hectares, 5.7 million metric tons) weevil eradication program in 1978. This program succeeded and the United States (4.3 million hectares, 3.9 million metric in eliminating the weevil as a serious pest from all previously tons) (http://faostat.fao.org; James, 2011). infested states of the United States except Texas, where the pro- Cotton harbors a rich arthropod biodiversity. Hargreaves gram is still in active phases (Hardee and Henneberry, 2004; (1948) lists more than 1300 herbivore species in cotton, in- Allen, 2008). Elsewhere in the Americas the weevil is still a 460 S. HAGENBUCHER ET AL.

FIG. 1. Summary of major arthropod pests of cotton in the USA. Numbers indicate the average percent yield loss for the period 2006 to 2012 across the entire United States. Bold letters denote the major production regions where the pest group primarily impacts cotton production: W, West; SW, Southwest; MS, Midsouth; SE, Southeast. Insects attacking cotton bolls (fruit) generally attack squares (flower buds) as well. Lines pointing to lint indicate that whiteflies and aphids can affect yield quality through the deposition of honeydew. Shaded boxes indicate pests, which are affected significantly by Bt-transgenic cotton. Figure redrawn from Naranjo and Luttrell (2009), which provide comparable yield loss data for the periods 1986–1995 and 1996–2005. Loss figures summarized from the Mississippi State University archive of Beltwide Cotton Crop Loss data: http://www.biochemistry.msstate.edu/resources/cottoncrop.asp (color figure available online).

serious pest. In Brazil it is estimated to cause 51 to 74 million 2005). Plant bugs (Miridae), such as Lygus spp., and stink bugs US$ economic losses/year (Oliveira et al., 2013). (Pentatomidae), such as Nezara viridula, attack squares, devel- The order Hemiptera contains a number of important cot- oping seeds in bolls, and the meristematic tissue. Other pests ton pest species, including the two aphid species Acyrthosiphon of cotton include Orthoptera, Thysanoptera and spider mites

Downloaded by [Agroscope Liebefeld Posieux], [Joerg Romeis] at 01:19 04 July 2013 gossypii and Aphis gossypii (Aphididae). Damage is mainly (Acari: Tetranychidae) (Matthews and Tunstall, 1994). caused by the transmission of viral diseases and by contamina- Historically, cotton has been among the crops most heavily tion of cotton fibers with honeydew (causing so-called sticky treated with insecticides, with up to 22.5% of all global in- cotton). In Africa, A. gossypii is responsible for losses in cot- secticides being applied to cotton, of which about half used to ton of up to 6.5% (Matthews and Tunstall, 1994). Whiteflies manage pest Lepidoptera (Naranjo et al., 2008; Fitt, 2008). This (Aleyrodidae), especially Bemisia tabaci, cause similar prob- pattern has changed, however, with the introduction of new tech- lems. The cotton stainers, Dysdercus spp. (Pyrrhocoridae), at- nologies (primarily, genetically engineered insect-resistant cul- tack cotton and cause regional yield losses in the tropics. Several tivars) and improved Integrated Pest Management (IPM) strate- species of leafhoppers (Cicadellidae), such as Amrasca devas- gies that reduced insecticide use significantly (Naranjo et al., tans in India and Pakistan, can seriously damage cotton by 2008; Naranjo, 2011). injecting toxins that interfere with photosynthesis, thus causing Cotton plants have evolved a range of direct and indirect symptoms known as hopperburn. In Pakistan, yield losses of mechanisms that contribute to their resistance against arthropod nearly 25% due to A. devastans were reported (Ahmad et al., herbivores in natural ecosystems (Figure 2). The complex of ARTHROPOD HERBIVORES IN COTTON 461

FIG. 2. Arthropod resistance mechanisms of cotton.

resistance mechanisms makes cotton plants an ideal model- it competes for light and nutrients (van Dam et al., 2000, 2001; system to study the evolution and functioning of multiple resis- Wackers¨ et al., 2007; Anderson et al., 2011). tances in plant-herbivore-carnivore interactions. In this review we describe the various resistance mechanisms of cotton and A. Morphological Traits their impact on pest species and their antagonists. Several morphological features of cotton provide some de- gree of resistance to arthropod pests. These include frego bracts, II. DIRECT RESISTANCE MECHANISMS -shaped leaves, and trichomes. There is evidence that the Plant arthropod resistance can be divided in two basic cate- open twisted bracts of cotton with the frego bract genotype are gories, direct and indirect resistance (Price et al., 1980; Sabelis less preferred for oviposition by A. grandis (Jenkins and Parrott, et al., 1999). Direct resistance mechanisms can be chemical or 1971; Mitchell et al., 1973). Compared to normal leaf plants, Downloaded by [Agroscope Liebefeld Posieux], [Joerg Romeis] at 01:19 04 July 2013 physical and are defined by having a direct impact on the her- cotton cultivars with spiny, okra-shaped leaves (i.e., a leaf shape bivore by negatively affecting important life-history parameters with lengthened lobes and decreased lamina expansion) tend such as survival, development time, size, longevity, or fecundity to suffer less damage from different herbivores, including the (Zangerl and Berenbaum, 1993; Li et al., 2000; Awmack and cotton specialist P. gossypiella (Wilson et al., 1986; Naranjo Leather, 2002; Gols et al., 2008). Direct resistance mechanisms and Martin, 1993). The mechanisms underlying this effect are are often not lethal, but they frequently help protect the plant by little understood. Wilson et al. (1986) observed a 13% reduction triggering avoidance behavior in the mobile stages of the herbi- in the number of P. gossypiella larvae penetrating the boll wall vore. The adult herbivore may reject the plant as an oviposition of okra-leaf cotton, and Naranjo and Martin (1993) found that site, while larval stages can respond by moving to tissues, which the mechanism was a combination of reduced oviposition on feature lower levels of resistance, or migrate to more suscepti- bolls coupled with fewer eggs being deposited once a boll is ble neighboring plants (Anderson et al., 2011). The plant may selected for oviposition. In support of this, choice-experiments thereby deflect herbivores onto neighboring plants with which with Creontiades signatus (Hemiptera: Miridae) revealed that 462 S. HAGENBUCHER ET AL.

females laid an average of three times more eggs on the normal- idoptera: Noctuidae) laid fewer eggs and had 60% increased leaf than on the okra-leaf cotton (Armstrong et al., 2009). How- mortality on pubescent cotton cultivars compared to glabrous ever, the authors could not rule out the possibility that higher cultivars (Kamel, 1965). Female L. hesperus preferred pilose trichome density on the okra-shape leaves played a role. Com- plants for oviposition (about 30% higher) over hirsute and paring different okra- and normal-leaf cotton cultivars in a field glabrous leaf plants in the greenhouse, although the nymphs study in Arizona, Chu et al. (2002) recorded 30–40% fewer performed poorer on the pilose plants (nymphal weights 37% B. tabaci eggs, nymphs and adults on the okra-leaf cultivars. lower) than on glabrous plants (Benedict et al., 1983). Un- The authors suggested that the reduction in whitefly coloniza- der field conditions, this adverse effect resulted in significantly tion was partly caused by less favorable micro-environmental lower damage caused by Lygus spp. to hirsute plants when conditions on the okra-shaped leaves. An unfavorable micro- compared to glabrous plants (Wilson and George, 1986). Sim- environment was also implicated in the increased resistance of ilarly, increased larval mortality on highly pubescent cotton okra-leaf cotton to the spider mite Tetranychus urticae (Koch) has been observed for P. gossypiella and H. virescens, possi- (Acari: Tetranychidae) (Wilson, 1994). bly because of impaired mobility (Smith et al., 1975; Ramalho et al., 1984). However, these effects on herbivores are not nec- 1. Impact of trichomes on herbivores essarily caused exclusively by trichomes. For example, Navon Trichomes are hair-like structures on the plant surface that et al. (1991) reported that H. armigera larval weight gain was can protect the plant by forming a physical barrier, or, in the reduced by about 90% on the highly pubescent cotton culti- case of glandular trichomes, by producing chemical repellents, var Texas 172 when compared to the less pubescent cultivar toxins or sticky substrates. Trichomes provide antixenotic and Acala SJ-2. Since the trichome density was four times higher antibiotic plant resistance in numerous plant species (Peter on Texas 172 compared to Acala SJ-2 trichomes appeared to et al., 1995; Smith, 2005) and can affect plant surface-dwelling be responsible for the reduced weight gain. However, the effect arthropods by hampering their movement. As a consequence, on H. armigera larval weight was still present after shaving the arthropods need more time to move between feeding sites and pubescent cultivar, which points to another factor(s) playing a increases their exposure to natural enemies and unfavorable role. environmental conditions (e.g., Smith et al., 1975; Ramalho In other instances, trichomes may also benefit herbivores. et al., 1984). Several studies report that plants with higher trichome densities The density and types of trichomes vary among Gossypium are more attractive as oviposition sites. This positive ovipo- species (Kosmidou-Dimitropoulou et al., 1980; Desai et al., sition response to trichomes has been reported for E. fabia 2008) and cultivars (Kosmidou-Dimitropoulou et al., 1980; (Mehta and Saxena, 1970), H. virescens and H. zea (Luke- Bryson et al., 1983; Navasero and Ramaswamy, 1991). The dif- fahr et al., 1971), L. lineolaris and L. hesperus (Benedict et al., ferent trichome types are best described for G. hirsutum, which 1983), and B. tabaci (Wilson and George, 1986; Gruenhagen and possesses unicellular needle-like, single or multiple branched Perring, 2001; Ashfaq et al., 2011). Oviposition by H. virescens trichomes, stellate (star-like) trichomes and globose (spherical) and H. zea was by a factor of 1.6 to 5.2 higher on hirsute cot- glanded trichomes (Navasero and Ramaswamy, 1991; Bondada ton types compared to glabrous plants (Lukefahr et al., 1971). and Oosterhuis, 2000). Three principal trichome phenotypes In addition, some herbivores also perform better on pubescent are defined: (i) glabrous = smooth leaf without trichomes; (ii) plants than on glabrous cotton. For example, feeding damage hirsute = medium length trichomes of normal density; and by Bucculatrix thurberiella (Lepidoptera: ) was (iii) pilose = high density of short trichomes. In general, tri- increased by 76% on hirsute cotton compared to glabrous cot- chome density is higher on the lower leaf surface compared to ton (Wilson and George, 1986). Similarly, the abundance of the upper surface (Navasero and Ramaswamy, 1991). A. gossypii nearly doubled in pubescent cotton when compared The interactions between herbivores and trichomes are com- to glabrous cotton (Weathersbee and Hardee, 1994). Tetranychus plex and not all species are equally affected by trichomes. urticae developed faster on hairy than on glabrous cotton, but Downloaded by [Agroscope Liebefeld Posieux], [Joerg Romeis] at 01:19 04 July 2013 Several studies reported decreased feeding damage by pest this did not result in yield differences (Reddall et al., 2011). In species and/or increased yields in cotton cultivars with high the field, B. tabaci abundance increased linearly with increasing pubescence (hairiness). The species affected include P. gossyp- trichome density up to about 70 trichomes per 13.7 mm2 where iella (Wilson and George, 1986), the boll weevil A. gran- abundance declined thereafter (Butler et al., 1991). These ef- dis (Wannamaker, 1957; Wessling et al., 1958), Lygus line- fects may partly be due to reduced attack by natural enemies as olaris (Hemiptera: Miridae) (Meredith and Schuster, 1979), has been suggested by Gruenhagen and Perring (2001). and Pseudatomoscelis seriatus (Miridae) (Walker et al., 1974). Other studies on pubescent cotton genotypes reported a reduced 2. Impact of trichomes on natural enemies abundance of pest species, including A. gossypii (Kamel and Attributes that restrict the movement of an herbivore can Elkassaby, 1965), Empoasca lybica (Hemiptera: Cicadellidae) have the same effect on natural enemies. Trichomes can (Butler et al., 1991), and A. devastans (Sikka et al., 1966; reduce the efficacy of parasitoids and predators and influ- Batra and Gupta, 1970). In the field Spodoptera litura (Lep- ence the structure of predator communities (Schuster and ARTHROPOD HERBIVORES IN COTTON 463

Calderon, 1986; Obrycki, 1986; Hare, 2002). For example, sev- less plants contain less than 0.001% gossypol and are thereby eral studies have reported a lower efficacy of Trichogramma acceptable for human and consumption (Fisher et al., spp. (Hymenoptera: Trichogrammatidae) egg parasitoids on 1988). However, as an unintended consequence, the glandless pubescent versus glabrous cotton cultivars (Romeis et al., 2005). plants became highly susceptible to arthropod pests (Bottger Thus, cotton trichomes can contribute to an enemy-free space et al., 1964; Jenkins et al., 1966). This provided the first indi- and thereby increase herbivore survival on pubescent plants cation that gossypol is an important arthropod resistance com- (Gruenhagen and Perring, 2001). pound. Subsequent spray experiments with purified gossypol Overall, trichomes appear to be an important resistance fac- confirmed its insecticidal activity (Bottger et al., 1964). In re- tor in cotton. Their net effect, however, is often difficult to assess cent years, RNAi-knockdown of δ-cadinene synthase gene(s) since they can reduce damage by some herbivores but promote has been used to engineer plants that produce ultra-low gossy- others and impair the efficacy of some natural enemies. Indi- pol cottonseed without affecting terpenoid production in the rest vidual studies are furthermore difficult to compare due to the of the plant (Sunilkumar et al., 2006; Palle et al., 2013; Rathore use of different plant types, environmental conditions, measure- et al., 2012). The seeds of these plants contain 0.5 μg gossy- ment end-points (e.g., yield vs. herbivore abundance) and often pol/mg seed, which is less than 10% of the concentration in the undefined trichome densities. parental line, Coker 312 (6 μg/mg) (Sunilkumar et al., 2006). The trait was stable under field conditions suggesting that the B. Plant Secondary Metabolites RNAi-based product has the potential to be commercially viable Gossypium plants produce a range of compounds with insec- (Palle et al., 2013). ticidal properties. This includes terpenoids, flavonoids, tannins, After examining wild strains of G. hirsutum that were partic- and anthocyanins. Of those the cotton terpenoids received the ularly resistant to H. virescens, it became clear that cotton must greatest attention, and are the best studied resistance mechanism possess more insecticidal compounds than gossypol (Shaver of cotton. and Lukefahr, 1971). The increased resistance found in these plants could not be explained with gossypol alone (Shaver and 1. Terpenoids Lukefahr, 1971), giving the first indication that cotton produces Cotton plants produce a set of closely related terpenoids. The several antibiotic compounds. A few years later those were iden- best known are gossypol; hemigossypol; hemigossypolone; and tified and described as hemigossypolone and the heliocides H1, heliocides H1, H2, H3, and H4 (Stipanovic et al., 1988; Altmann H2, H3 and H4 (Gray et al., 1976; Stipanovic et al., 1977a, et al., 1990; Benson et al., 2001; Bezemer et al., 2004; Meyer 1978a, b). In addition, cotton plants produce a range of other ter- et al., 2004). All of these are closely related, with H1 and H4, as penoids, like caryophyllene, raimondal, ocimene, myrcene and well as H2 and H3, being isomers of each other. Several other limonene, which also appear to be involved in plant resistance compounds from the “family” of gossypol-related terpenoids, (Stipanovic et al., 1980; Elzen et al., 1985; Smith et al., 1992). e.g., hemigossypol or desoxyhemigossypol, are known, but their 1.1. Terpenoid distribution. In general, terpenoid concen- function is not well understood (Howell et al., 2000; Stipanovic tration, composition and distribution differ among Gossypium et al., 1977b). The terpenoids are contained in small subepider- species (Altmann et al., 1990; Stipanovic et al., 2005) and culti- mal and intracellular pigment glands that are characteristic for vars (Stipanovic et al., 1988; Altmann et al., 1990; Hedin et al., all Gossypium species (Fryxell, 1979; Gershenzon and Croteau, 1991, 1992a; Wu et al., 2010) and can be dependent on en- 1992), and in cytoplasmic granules of the root epidermis (Mace vironmental conditions (Section V). Also within the plants a et al., 1974). The pigment glands can be found in all exter- considerable variation in concentration and composition of ter- nal tissues, including the seed, but are mainly concentrated on penoids exists (Table 1). As predicted by the optimal defense leaves and squares. The final root tips, however, do not contain theory (ODT) (Figure 3), terpenoid concentrations are highest pigment glands. Similar glands are also present in other genera in tissues that are most valuable to the plant. For example, young of the tribe Gossypiae, such as Kokia (Fryxell, 1979). leaves contain 2.5 to 5 times more terpenoids compared to ma- Downloaded by [Agroscope Liebefeld Posieux], [Joerg Romeis] at 01:19 04 July 2013 The best studied cotton terpenoid is gossypol, which is an op- ture leaves (McAuslane et al., 1997; Bezemer et al., 2004; Ha- tically active substance that occurs as an enantiomeric mixture of genbucher et al., 2013). Another example is the way terpenoids (+)-gossypol and (-)-gossypol (Jaroszewski et al., 1992a). The are allocated to the individual parts of the squares (flower bud), ratio of the enantiomers varies among plant tissues (Jaroszewski where stigma and anthers contain about 10 times more gossypol et al., 1992b). Since gossypol is toxic to humans and non- than the bracts (Hedin et al., 1992a). ruminant (Risco and Chase, 1997), its presence in cot- Gossypol is the only terpenoid found in seeds (Stipanovic ton seeds limits their use as food and feed, despite the fact et al., 1988; Sunilkumar et al., 2006). It is the predominant that cottonseed is very rich in oil and high-quality protein (Cai terpenoid in squares and, together with hemigossypol, in roots et al., 2009). Consequently, one of the breeding goals in cotton (Hedin et al., 1984; Stipanovic et al., 1988; Khoshkoo et al., has been to select cultivars with low gossypol content resulting 1993; Benson et al., 2001; Bezemer et al., 2004). In contrast, the in cultivars that do not possess the gossypol-producing glands mixture of terpenoids in leaves is dominated by the heliocides (McMichael, 1960; Cai et al., 2009). Seeds of these gland- (esp. H1 and H2) and hemigossypolone (Stipanovic et al., 1988), 464 S. HAGENBUCHER ET AL.

TABLE 1 Terpenoid Content (μg/g Dry Weight) in Different Cotton Plant Parts (Selected Studies). G – Gossypol, HGQ – Hemigossypolone, HG – Hemigossypol, H1-H4 – Helicocides 1–4 Plant Gossypium species (cultivar) part G HGQ HG H1 H2 H3 H4 Reference G. hirsutum (Acala1517-70) Leaf 387 NA NA NA NA NA NA Meyer et al., 2004 Stem 143 NA NA NA NA NA NA Seed 6780 NA NA NA NA NA NA G. hirsutum (OR19) Leaf 798 NA NA NA NA NA NA Meyer et al., 2004 Stem 275 NA NA NA NA NA NA Seed 10980 NA NA NA NA NA NA G. hirsutum (Sikora 1-4/649) Leaf 929 3010 ND 2170 1090 390 1450 Benson et al., 2001 Square 3620 585 ND 1850 989 351 1210 Bollcoat 701 331 ND 5210 952 396 3450 G. hirsutum (Stoneville 213) Square 1400 400 NA 600 700 NA NA Hedin et al., 1992 G. hirsutum (DH118) Square 1400 1500 NA 1900 1100 NA NA Hedin et al., 1992 G. hirsutum (DPL 147RF) Leaf 2014 6764 NA 284∗ 642∗ 642∗ 284∗ Hagenbucher et al., (young) 2013 G. hirsutum (Stoneville 213) Leaf 191 3062 NA 321 780 317 94 McAuslane and (young) Alborn, 1998 G. herbaceum Leaf 23 825 ND 163∗ 389∗ 389∗ 163∗ Bezemer et al., 2004 Roots 10717 ND 1060 ND ND ND ND

NA = not analyzed; ND = not detected; ∗H1+H4 and H2+H3 were not analyzed separately.

while gossypol is a minor compound and hemigossypol appears 1.2. Impact of terpenoids on herbivores. Cotton ter- to be completely absent (Table 1). For a semiquantative overview penoids have direct toxic effects on a range of cotton herbi- of the terpenoid composition in different cotton tissues see also vores. Most research has been conducted with gossypol and Stipanovic et al. (1977b). lepidopteran larvae. Feeding a gossypol-rich artificial diet to caterpillars increased mortality and reduced growth rates in a number of species, including H. virescens (Bottger and Patana, 1966; Lukefahr et al., 1977), H. zea (Bottger and Patana, 1966), H. armigera (Mao et al., 2007), P. gossypiella (Lukefahr et al., 1977), Trichoplusia ni (Lepidoptera: Noctuidae) (Bottger and Patana, 1966), Estigmene acrea (Lepidoptera: Arctiidae) (Bottger and Patana, 1966), E. insulana (Meisner et al., 1977c), and E. vitella (Dongre and Rahalkar, 1980). Studies with both H. zea and H. virescens did not detect any difference in the activity of the two gossypol enantiomers (Stipanovic et al., 2006, 2008). The sensitivity to gossypol differs among herbivore species. For example, the percentage of gossypol in artificial diets that Downloaded by [Agroscope Liebefeld Posieux], [Joerg Romeis] at 01:19 04 July 2013 caused 50% mortality (LD50) varied from 0.04% (w/w) for E. acrea to 0.2% for H. zea (Bottger and Patana, 1966). For comparison, the gossypol content in cotton tissue is typically around 0.1% of the dry mass of leaves and even higher in squares and seeds (Table 1). Thus, gossypol and related compounds can be a tremendous obstacle for herbivores to overcome. At low concentrations, however, gossypol can have a hormetic effect as demonstrated for H. virescens and H. armigera where larvae on diets with a low gossypol concentration (ca. around 0.0125%, w/v) performed better than those on pure diet (Stipanovic et al., 1986; Celorio-Mancera et al., 2011). Susceptibility to cotton terpenoids also tends to vary among larval instars, with older FIG. 3. The Optimal Defense Theory. larvae being less sensitive (Lukefahr and Houghtaling, 1969; ARTHROPOD HERBIVORES IN COTTON 465

Shaver and Parrott, 1970; Belcher et al., 1983; Hedin et al., pol and individual heliocides up to a concentration of 0.2%, 1992a). which corresponds to the LD50 of the relatively insensitive There is little information available on the comparative H. zea (Bottger and Pattana, 1966). In contrast, Moore et al. toxicity of the different cotton terpenoids. Studies with H. (1983) observed a decrease in fecundity and reduced resistance virescens revealed the following order of toxicity (from most to abiotic stresses in the weevil when this particular concentra- to least toxic): gossypol > H1 > H3 > hemigossypolone > H2 tion was mixed into artificial diets. Other experiments indicated (Lukefahr et al., 1977; Stipanovic et al., 1977b). For P. that a broad range of arthropods from mirids (L. hesperus)to gossypiella, however, toxicity was equal for gossypol, leafhoppers (Spanogonicus albofasciatus; Hemiptera: Miridae) hemigossypolone, H1 and H2 (Lukefahr et al., 1977; and pill bugs (Porcellio spp.; Isopoda: Porcellionidae), suffered Stipanovic et al., 1977b). less mortality and thus caused more damage on glandless com- Effects of cotton terpenoids on caterpillars were also ob- pared to glanded cotton (Bottger et al., 1964). Du et al. (2004) served in planta. Larvae of H. virescens maturing on glandless found that the life span and fecundity of A. gossypii was reduced cotton had a significantly higher growth rate than those matur- by half after feeding on a high gossypol cultivar (gossypol con- ing on glanded cotton (Lukefahr et al., 1966). In contrast, the centration of 1.12%) compared to a cultivar with a gossypol specialist cotton-feeder A. argillacea appears to be unaffected content that was 20 times lower. In support of this, Hagenbucher by terpenoids as it survived equally well on leaves of a glanded et al. (2013) showed that aphid abundance was significantly re- and glandless cotton cultivar and even gained more weight on duced on caterpillar-induced plants that had higher terpenoid the glanded plants (Montadon et al., 1986, 1987). In general, levels than undamaged plants. Studies with glanded and gland- it is difficult to relate the sensitivity of caterpillars measured less cotton suggest that cotton terpenoids do not affect spider in artificial-diet studies to their performance on cotton plants mites (Agrawal and Karban, 2000). It is not clear, however, if because larvae on plants can avoid feeding on glands or prefer- the mites are unaffected by the terpenoids or simply avoid the entially feed on tissue with lower terpenoid content (Lukefahr glands due to their unique feeding patterns (Brody and Karban, and Houghtaling, 1969; Belcher et al., 1983; Parrott et al., 1983, 1989; Agrawal and Karban, 2000). 1990; Hedin et al., 1992a; Anderson et al., 2001). Relatively few data exists about the mode of action and fate Terpenoids also affect larval feeding behavior. Gossypol for of gossypol after ingestion by herbivores. Binding to proteins example is a strong feeding deterrent, as shown for Spodoptera could explain the toxicity of gossypol to insects, since it is an littoralis (Lepidoptera: Noctuidae) (Meisner et al., 1977a) and alkylating agent that can react with the amino group of amino neonate H. virescens that avoid consuming glands (Belcher acids (Felton, 1996). For example, Meisner et al. (1977b) re- et al., 1983; Parrott et al., 1983; Parrott, 1990; Hedin et al., ported that gossypol inhibits amylase and protease activity in 1992a). Female H. virescens typically oviposit on the terminals S. littoralis. When larvae had fed on cotyledons of glanded cot- of cotton plants. After hatching the larvae consume some leaf ton for three days their protease activity was reduced by 73.8% material and quickly move to small squares where they prefer- and amylase activity by 79% when compared to larvae feeding entially feed on the margin of the calyx, which contains about on glandless cotton. A study with A. grandis showed a reversal 10% of the gossypol present in the anthers and petals (Hedin of toxic effects of gossypol when weevils were maintained on a et al., 1992a). When larvae are older (late 2nd or 3rd instar) and high-protein diet. While a 0.2% (w/w) gossypol concentration less sensitive to gossypol, they burrow through the calyx, and the in the diet reduced the fecundity of females from 9.8 eggs/day petals into the anthers (Belcher et al., 1983; Parrott, 1990; Hedin to 4.8 eggs/day compared to a control diet (containing 0.0055% et al., 1992a). Larvae of H. zea feed less, increase searching be- gossypol), the fecundity increased from 4.8 to 11.7 eggs/day havior on glanded compared to glandless plants, and also prefer when the protein concentration in the gossypol-containing diet older leaves on glanded plants for feeding (Schmidt et al., 1988). was raised from 3.25% to 6.5% (Moore, 1983). Some herbi- Additionally, the rate at which larvae dropped off the plant was vores appear to adapt to cotton terpenoids, as has been shown between 4 and 5.5 times higher on glanded plants (Schmidt for S. exigua for which larval survival and adult fecundity on Downloaded by [Agroscope Liebefeld Posieux], [Joerg Romeis] at 01:19 04 July 2013 et al., 1988). A similar avoidance strategy has been reported for high terpenoid cotton cultivars increased with generations (Wu Spodoptera exigua (Lepidoptera: Noctuidae) and S. littoralis et al., 2010). larvae that avoid gossypol-rich young leaves by migrating to Studies with the generalist H. virescens and the specialist A. older leaves (McAuslane and Alborn, 2000; Anderson et al., argillacea revealed that the larvae are very efficient in excreting 2001; Bezemer et al., 2003). gossypol (Montadon et al., 1987). During the last two instars, Less is known about the effect of cotton terpenoids on non- A. argillacea excreted 71% and 83% of the ingested gossypol, lepidopteran herbivores. Spray applications of gossypol to host while the excretion levels were 45% and 68% for H. virescens plants exerted adverse effects on L. hesperus, A. gossypii and A. (Montadon et al., 1987). Studying the metabolic fate of 14C- grandis (Bottger et al., 1964). Compared to most lepidopteran labeled gossypol in H. virescens, Rojas et al. (1992) observed species, the coleopteran A. grandis appears to be less sensitive that most (52%) of the ingested gossypol was eliminated with to gossypol (Stipanovic et al., 1977b; Moore, 1983), possibly the frass, nearly 10% was metabolized to CO2, while only 24% because it is a specialist herbivore of Gossypium. Stipanovic of the gossypol or its products remained in the insect. Within the et al. (1977b) reported that the weevil is insensitive to gossy- caterpillars, radioactivity accumulated mainly in the fat body, 466 S. HAGENBUCHER ET AL.

cuticle, and gut tissues, and was transferred to a limited extent also respond to the application of jasmonic acid (Omer et al., (2.4%) to the adult stage (Rojas et al., 1992). Gossypol can 2001; Opitz et al., 2008; Mesz´ aros´ et al., 2011) or growth reg- thus be used as a marker to identify that have devel- ulators (Hedin and McCarty, 1991; Khoshkhoo et al., 1993). oped on cotton (Orth et al., 2007). For the aphid A. gossypii, Mechanical damage can also induce terpenoid production, but hemigossypolone and gossypol were found to pass through the the response tends to be weaker than following herbivory or gut and were detectable in the honeydew (Hagenbucher, 2012). jasmonic acid treatment (Karban, 1985; Opitz et al., 2008). A recent study with H. armigera larvae demonstrated a key role Some herbivores can suppress the induction of terpenoid pro- of the P450 mono-oxygenase CYP6AE14 in the detoxification duction. The best documented case is H. zea (Bi et al., 1997; of gossypol (Mao et al., 2007). The same enzyme appears to Olson et al., 2008), where suppression of resistance induction participate in the metabolism of some insecticides (Tao et al., is most likely caused by the caterpillar’s saliva. Studies with to- 2012). bacco revealed that glucose oxidase, a protein from the saliva of Cotton terpenoids are also reported to be toxic to the root-knot H. zea, is responsible for this suppression (Musser et al., 2005). nematode Meloidogyne incognita (Tylenchidae: Heteroderi- Damage caused by H. zea caterpillars appears to induce a dis- dae) (Veech, 1979; Hedin et al., 1984) and to play a role in tinct set of non-terpenoid resistance compounds in cotton, such resistance against different pathogens, including Verticillium as several oxidases, including peroxidases and lipoxygenase, re- dahlia (Hypocreales: Insertae sedis) (Mace et al., 1990), Fusar- active oxygen species and phenolic compounds (Bi et al., 1997). ium oxysoporum f.sp. vasinfectum (Hypocreales: Nectriaceae) In addition, feeding by H. zea causes an overall reduction in the (Zhang et al., 1993), and Rhizoctonia solani (Cantharellales: nutritional quality of cotton plant tissue and leads to increased Ceratobasidiaceae) (Puckhaber et al., 2002). lignification and strengthening of cell walls (Bi et al., 1997). Several minor terpenoids with insecticidal properties are Also the mealybug Phenacoccus solenopsis (Hemiptera: Pseu- found in cotton plants. Caryophyllene and caryophyllene ox- dococcidae) appears to actively suppress terpenoid induction. ide, two terpenes found together with gossypol in the glands While mealybugs perform better on cotton plants that were al- of G. hirsutum and other cotton species, are not lethal to H. ready damaged by P. solenopsis, they were adversely affected virescens, but they cause sublethal effects on larval weight, and when the plants were induced with jasmonic acid (Zhang et al., act synergistically with gossypol. Adding caryophyllene ox- 2011). ide to a gossypol rich diet reduced the larval weight by about The induction of secondary metabolites in cotton is systemic, 30% compared to larvae exposed only to the same amount of but depends on the age of the plant and the site of damage gossypol (Gunasena et al., 1988). In G. raimondii, the predom- (McAuslane et al., 1997; Anderson et al., 2001; Anderson and inant terpenoid is a unique sesquiterpenoid called raimondal. Agrell, 2005). When the plant is attacked above-ground, no This compound is also concentrated in the glands and is sev- or only weak responses are induced in mature leaves, while eral times more toxic to H. virescens than gossypol (Stipanovic newly developing leaves exhibit a strong increase in terpenoids et al., 1980, 1990; Smith et al., 1992). regardless of where the attack occurs on the plant (McAuslane 1.3. Induction of glands and terpenoids. For a plant, in- et al., 1997; Bezemer et al., 2004; Anderson and Agrell, 2005) duction of resistance in response to pest attack is a way to (Figure 4). These findings fit well with the ODT, as mature optimize the allocation of resistance, increase its efficacy and leaves are less valuable to the plant compared to young leaves minimize associated costs (Karban and Myers, 1989). Induc- (Anderson and Agrell, 2005). As a consequence, caterpillars tion can be herbivore-specific, is triggered by a range of elicitors may migrate to the less defended, less valuable mature leaves and regulated by complex biochemical pathways. Key signals in or they may leave the induced plant altogether (McAuslane these processes are jasmonic acid-, salicylic acid-, and ethylene- and Alborn, 2000; Bezemer et al., 2003; Anderson and Agrell, dependent pathways, which interact with each other (Beckers 2005). In choice experiments (McAuslane and Alborn, 1998), S. and Spoel, 2006). exigua larvae preferred leaves from glanded undamaged plants The cotton plant’s response to an attack by herbivores typi- 33 times more than leaves from glanded damaged plants. In the Downloaded by [Agroscope Liebefeld Posieux], [Joerg Romeis] at 01:19 04 July 2013 cally consists of an increase in gland density as well as in their case of glandless plants, undamaged leaves were only preferred terpenoid content in young or developing leaves (McAuslane 2.6-fold over damaged leaves. et al., 1997; Agrawal and Karban, 2000; Opitz et al., 2008). The systemic induction of terpenoids can mediate indirect This induction can be elicited by a range of different above- and competition between different species of herbivores. Recently, below-ground herbivores, including caterpillars (Alborn et al., Hagenbucher et al. (2013) reported a 40% reduction in A. 1996; McAuslane et al., 1997; Agrawal and Karban, 2000; Ha- gossypii abundance on caterpillar-induced cotton plants that genbucher et al., 2013), spider mites (Karban and Carey, 1984), contained 2.5 times more terpenoids compared to undamaged thrips (Spence et al., 2007), wireworms (Coleoptera: Elateri- plants. That the induction of plant resistance can mediate inter- dae) (Bezemer et al., 2003, 2004), and root-knot nematodes actions between below- and above-ground herbivores was first (Veech, 1979; Khoshkhoo et al., 1993). In addition, terpenoid described in cotton. The growth rate of S. exigua larvae was induction can be elicited by infection with bacterial and fun- reduced on G. herbaceum plants that suffered below-ground gal pathogens (Mace et al., 1990; Zhang et al., 1993; Abraham damage by A. lineatus (Bezemer et al., 2003, 2004). Feeding by et al., 1999; Howell et al., 2000; Puckhaber et al., 2002). Plants A. lineatus triggered below-ground terpenoid production as well ARTHROPOD HERBIVORES IN COTTON 467

FIG. 4. Patterns of systemic resistance induction in cotton plants after foliar herbivory by caterpillars (damaged leaf indicated by the arrow) or below-ground herbivory on the roots. The darker the grey, the greater the level of induction of terpenoids, volatiles and extrafloral nectaries (EFN). Question mark indicates that no information is available about this plant part. Downloaded by [Agroscope Liebefeld Posieux], [Joerg Romeis] at 01:19 04 July 2013 as above-ground. Terpenoid concentrations in immature leaves and foliar terpenoid content did increase but to a lesser extent increased by a factor of 2.3 as a response to root herbivory, than above- or below-ground herbivory alone (Bezemer et al., while above-ground feeding by S. littoralis increased the ter- 2004). Below-ground herbivory by A. lineatus also has a strong penoid concentration by a factor of 13.5 (Bezemer et al., 2004). effect on the behavior of above-ground herbivores. When given Even though below-ground damage also caused an increase in a choice between plants damaged by A. lineatus and undamaged terpenoid levels of mature leaves (by a factor of 4.2), the absolute plants, S. littoralis females deposited 81% of their eggs on the terpenoid content of mature leaves was still about 50% lower undamaged plants; the difference in the distribution of eggs was than in immature leaves. In contrast, leaf damage did not trigger manifested both in the number of egg masses and in the mean a higher rate of terpenoid synthesis in the roots (Bezemer et al., number of eggs per mass deposited (Anderson et al., 2011). 2003, 2004) (Figure 4). When the cotton plants were exposed Terpenoid induction in cotton can also be triggered by differ- to above- and below-ground herbivores at the same time, root ent plant pathogens including F. oxysporum f.sp. vasinfectum 468 S. HAGENBUCHER ET AL.

(Zhang et al., 1993), Rhizobium rhizogenes (Rhizobiales: The ratio of hemigossypolone to all heliocides changed over Rhizobiacae) (Triplett et al., 2008), V. dahlia (Bianchini et al., time; from 10.6: 1 at the first day to 1.3: 1 seven days after 1999), and Xanthomonas spp. (Xanthomonadales: Xanthomon- induction (McAuslane et al., 1997). Such a shift in terpenoid adaceae) (Abraham et al., 1999). The biocontrol agent Tricho- ratios could be explained by a photochemical reaction between derma virens (Hypocreales: Hypocreaceae) mediates resistance hemigossypolone and the volatile terpenoid ocimene, with the against R. solani via an increase of hemigossypol and the closely end product being H1 (McAuslane et al., 1997). Other factors related desoxyhemigossypol (Howell et al., 2000; Puckhaber that affect the induction of terpenoids include plant age and size et al., 2002). It is not clear if nematodes can induce resistance in (McAuslane et al., 1997; Agrawal and Karban, 2000; Anderson cotton. While Olson et al. (2008) found that M. incognita does et al., 2001; Anderson and Agrell, 2005) and the site where the not induce terpenoid production, Khoshkhoo et al. (1993) found damage occurs (section II B 1.3). that damage from the same species in combination with plant There is evidence that factors other than terpenoid glands growth regulators did induce resistance. The induction found also contribute to the increased resistance of induced plants. For by Khoshkhoo et al. (1993) may have been facilitated by the example, Agrawal and Karban (2000) reported an equal reduc- growth regulators. tion in spider mite population growth on damaged glanded and Little is known about the lag time between the onset of glandless cotton plants, implying that terpenoids are not a major damage and the expression of the terpenoid-based resistance. factor in spider mite population growth. Further evidence comes Terpenoid-induction by the pathogen R. solani in the roots of from studies with the glandless line WbMgl, in which the pro- cotton seedlings was detectable within 8 h after inoculation duction of terpenoids like hemigossypol and desoxyhemigossy- (Rathore et al., 2012). McAuslane et al. (1997) reported that pol is inducible by the pathogen Xanthomonas campestris pv. young leaves expressed a high feeding deterrence for S. exigua malvacearum (Xcm) (Davis and Essenberg 1995; Davis et al., larvae within one day after being damaged by conspecifics. El- 1996; Abraham et al., 1999). evated terpenoid levels were still present after seven days, and the amount of terpenoids was even higher than that recorded one day after the initial damage. Studies with S. littoralis indicate 2. Impact of other plant metabolites on herbivores that terpenoid levels were still elevated 14 days after caterpillars Cotton produces other compounds that might contribute to ceased feeding (Anderson et al., 2001), while terpenoid levels the plant’s resistance against herbivores. These include different were back to constitutive levels four weeks after feeding by H. flavonoids (Hedin et al., 1968, 1988), some of which have been virescens larvae had stopped (Hagenbucher, 2012). shown to inhibit growth of lepidopteran larvae when added to Changes in terpenoid concentration in G. hirsutum af- artificial diet (Shaver and Lukefahr, 1969; Chan et al., 1978a; ter arthropod damage differ among compounds and cultivars b) or in planta (Hedin et al., 1992b). Flavonoids appear to be (Table 2). Seven days after caterpillar damage, terpenoid lev- a particularly important resistance factor in the Asian cotton els in G. hirsutum was increased by 47–149% for hemigossy- species G. arboreum, which contains three to four times less polone, 112–124% for gossypol, 339–772% for H1, 149–883% gossypol (Altman et al., 1990; Hedin et al., 1992b) than G. for H4, 26–79% for H2, and 25–135% for H3 (McAuslane hirsutum, but is as resistant to H. virescens (Hedin et al., 1992b). et al., 1997; McAuslane and Alborn, 1998; Anderson and Agrell, There is evidence that two flavonoids absent in G. hirsutum are 2005; Opitz et al., 2008). The total terpenoid amount increased responsible for this resistance: gossypetin 8-0-glucoside and by 89–144% (McAuslane et al., 1997; McAuslane and Alborn, gossypetin 8-0-rhamnoside (Hedin et al., 1992b). 1998; Anderson and Agrell, 2005; Opitz et al., 2008). The ratio Artificial diet studies indicate that cotton tannins can also of H1 + H4 to H2 + H3 changed from 0.38–0.69 to 1.28–1.48. adversely affect several insect species, including H. virescens

TABLE 2

Downloaded by [Agroscope Liebefeld Posieux], [Joerg Romeis] at 01:19 04 July 2013 Relative Increase of Terpenoid Concentration (%) in Terminal Cotton Leaves, Seven Days after Spodoptera spp. Damage, Compared to Undamaged Control Plants (Selected Studies). TT – Total Terpenoid; G – Gossypol, HGQ – Hemigossypolone, HG – Hemigossypol, H1-H4 – Helicocides 1–4 Gossypium species (cultivar) TT G HGQ H1 H2 H3 H4 Reference G. hirsutum (Deltapine 90) 144 112 118 772 68 61 883 Anderson and Agrell, 2005 G. hirsutum (Deltapine 90) 89 141 47 339 79 135 179 McAuslane et al., 1997 G. hirsutum (Stoneville 213) 118 124 149 487 42 45 351 McAuslane and Alborn, 1998 G. hirsutum (Deltapine 115 NA 97 386 26 25 149 Opitz et al., 2008 acala-90) G. herbaceum 103 113 114∗ 126∗ 69∗ 69∗ 126∗ Bezemer et al., 2004

∗H1+H4 and H2+H3 were not analyzed separately. ARTHROPOD HERBIVORES IN COTTON 469

and P. gossypiella (Waiss et al., 1977; Chan et al., 1978a, b). to assess the impact of cotton terpenoids on natural enemies are While there is evidence from field experiments that tannins rare and have only been conducted with gossypol. When the provide some level of resistance to pests such as A. gossypii, B. predatory bug Podius nigrispinus (Hemiptera: Pentatomidae) tabaci and T. urticae (Lane and Schuster, 1980; Mansour et al., was presented with gossypol solutions of various concentra- 1997) the impact on caterpillars is inconclusive (Zummo et al., tions together with Tenebrio molitor (Coleoptera: Tenebrion- 1983, 1984; Smith et al., 1992). Anthocyanins, like cyanidin- idae) pupae as prey throughout its entire life, adverse effects 3-β-glucoside, can also contribute to insect resistance (Hedin on development time, egg production and hatching rate were et al., 1983). observed at certain gossypol concentrations (Evangelista Junior et al., 2011). Bugs feeding on a high gossypol diet (0.2%; w/v) 3. Impact of secondary plant metabolites on natural enemies lived longer (43.6 days) than those feeding on a diet containing The effects of plant arthropod resistance can cascade into 0.1% (w/v) gossypol (39.2 days), while those on a gossypol free higher trophic levels and have consequences for the natural diet lived 48.5 days (Evangelista Junior et al., 2011). A possible enemies of herbivores (Turlings and Benrey, 1998; Ode et al., explanation is that the binding of gossypol forces the females 2006). Such effects can be negative (Turlings and Benrey, 1998) to reabsorb eggs, thus prolonging their longevity. Comparable or positive; for example, when the immune system of the host results were found for the two parasitoids L. testaceipes and is weakened due to the ingestion of toxic compounds (Rhoades, Eretmocerus eremicus (Hymenoptera: Aphelinidae) when fed 1983; Benrey and Denno, 1997) or when the development time sugar solutions containing different concentrations of gossypol. of hosts is prolonged, providing predators or parasitoids with a Female longevity was reduced by gossypol only at intermedi- larger window of attack (Clancy and Price, 1987; Benrey and ate concentrations (0.000001 to 0.0001%, w/v) while a higher Denno, 1997). concentration (0.001%) had no effect (Hagenbucher, 2012). Little is known about the impact of cotton terpenoids on nat- Another mechanism by which induced resistance in cotton ural enemies. Adverse effects on Campoletis sonorensis (Hy- can influence arthropod food-webs is indicated by a study with menoptera: Ichneumonidae), an endoparasitoid of H. virescens, the omnivorous thrips Frankliniella occidentalis (Thysanoptera: were reported when the host consumed a diet containing gossy- Thripidae). This species feeds directly on cotton tissue as well pol at a concentration of more than 0.1% (w/w): the parasitoids as on other arthropods living on the plant. On plants previously developed slower, had a lower emergence rate, and adults were damaged by spider mites, F. occidentalis adults reduced their smaller (Gunasena et al., 1989). Low concentrations of gossy- uptake of plant material by 50% and doubled the consumption of pol (0.013%, w/w) in the host’s diet, however, had a positive spider mites compared to thrips on undamaged plants (Agrawal impact on the weight of the adult parasitoid. In a study with et al., 1999). This might be a way of avoiding the increased Propylaea japonica (Coleoptera: Coccinellidae), the ladybirds terpenoid levels in the plant tissue resulting from mite herbivory. were fed aphids reared on one of three different cotton cultivars with gossypol concentrations of 0.06%, 0.44% and 1.12% (Du III. INDIRECT RESISTANCE MECHANISMS et al., 2004). While the life-span of adult aphids was roughly Instead of acting on herbivores directly, indirect resistance halved on the cultivar with the highest gossypol concentration mechanisms act by attracting or enhancing the effectiveness compared to the other cultivars, no negative impact on P. japon- of natural enemies (Price et al., 1980; Sabelis et al., 1999; ica survival and fecundity was detected. In contrast, predators Turlings and Wackers,¨ 2004). Examples of such indirect resis- feeding on aphids from the high-gossypol cultivar did show tance mechanisms include the emission of signals that are used a 10% shorter development time and a ca. 30% higher adult as host-/prey-finding cues by natural enemies, the provisioning weight compared to the low gossypol cultivar. This might be of food, and the provisioning of shelter or oviposition substrates. explained by an increased fatty acid content in aphids reared on the high gossypol cultivars (Du et al., 2004). For the aphid par- A. Volatiles asitoid Lysiphlebus japonica (Hymenoptera: Braconidae), Sun Plants emit a blend of volatile compounds that typically Downloaded by [Agroscope Liebefeld Posieux], [Joerg Romeis] at 01:19 04 July 2013 et al. (2011) did not observe a difference in parasitism when change in quantity and in composition after herbivore damage. parasitoids were provided A. gossypii reared on the same culti- As such, they can be used by herbivores and their natural ene- vars as used by Du et al. (2004). Similar results were reported mies as host location cues. A number of studies have assessed for Lysiphlebus testaceipes (Hymenoptera: Braconidae) when the impact of cotton volatiles for plant-arthropod interactions. comparing the parasitism rate for aphids feeding on caterpillar- induced or uninduced cotton despite the fact that the aphids 1. Release of volatile compounds contained terpenoids at a concentration of 270–800 ng/mg dry Cotton produces a large number of volatiles, mainly terpenes weight (Hagenbucher, 2012). and lipoxygenase-derived compounds (Minyard et al., 1965, These tri-trophic studies provide only limited insights into 1966; Elzen et al., 1985; Loughrin et al., 1994). Similar to the the terpenoid sensitivity of natural enemies as the observed ef- terpenoids, the volatile blends differ among cotton species and fects could also be a consequence of other factors, e.g., an altered cultivars (Elzen et al., 1985). Glands may play a role in stor- quality of the herbivore as a prey or host. Direct feeding studies age and production of volatiles since glandless cotton cultivars 470 S. HAGENBUCHER ET AL.

release fewer volatile compounds at lower concentrations when tified elicitor present in the salivary glands that activates the compared to glanded cultivars (Elzen et al., 1985). same biosynthetic pathway as caterpillar damage. Ovipositing Undamaged cotton plants emit a limited range of volatiles L. hesperus females also caused the emission of constitutive at relatively small amounts. These mainly comprise green- volatiles, most likely as a result of mechanical damage to the leaf volatiles and terpenoid compounds (McCall et al., 1994; glands on the plant surface when the bug punctured the leaf sur- Loughrin et al., 1994, 1995; Rose¨ et al., 1996, 1998). The face to insert eggs into the plant tissue (Rodriguez-Saona et al., amount and range of emitted volatiles is typically increased in 2002). response to damage by lepidopteran herbivores (McCall, 1994; The influence of phloem-feeding herbivores with piercing- Rose¨ et al., 1996). Similar to the induction of terpenoids, me- sucking mouthparts on the induction and release of volatiles chanical damage is not as effective in inducing the release of is inconclusive. While B. tabaci could not induce the release volatiles as actual herbivory. This is attributed to the presence of volatiles (Rodriguez-Saona et al., 2003), the cotton aphid of certain elicitors in the saliva of herbivores, like volicitin from A. gossypii could (Hegde et al., 2011). Among the compounds beet armyworm, S. exigua (Alborn et al., 1997; Rose¨ and Tum- were green-leaf volatiles, methyl salicylate and homoisoprenoid linson, 2004). Like other plants such as tobacco and , the compounds, but no terpenoids (Hegde et al., 2011). This means volatile blend emitted by cotton plants varies when damaged that the aphid volatile blend is distinctly different from the by different lepidopteran species (DeMoraes et al., 1998; Rose¨ caterpillar-induced volatiles. The mealybug P. solenopsis also et al., 1998). triggers volatile release in cotton, but primarily causes the emis- The process of volatile release by cotton following dam- sion of 3-hexen-1-ol acetate, cyclohexane, and β-caryophyllene, age by caterpillars is not static and the blend changes over resulting in a volatile blend different from that released as a re- time (Loughrin et al., 1994; Rose¨ et al., 1996; Pare´ and Tum- sponse to A. gossypii or caterpillar infestation (Zhang et al., linson, 1997a; Turlings and Wackers,¨ 2004). A mixture of 2011). lipoxygenase-derived volatiles (green-leaf volatiles, e.g., (Z)- The impact of above- versus below-ground damage for cot- 3-hexenal, (Z)-3-henxenyl acetate) and terpenes (e.g., α-pinene ton volatile induction has not been as well-studied as it has and myrcene) dominate the blend in the first hours after the for other resistance mechanisms. However, Olson et al. (2008) damaging event. These volatiles are either stored in the glands, found that below-ground damage by the nematode M. incog- synthesized by stored intermediates, or created quickly from nita did not affect volatile emissions above-ground, whereas the fatty acids by hydroperoxidation (Loughrin et al., 1994; Pare´ combination of leaf–feeding by H. zea and root herbivory by and Tumlinson, 1997a, b). The release of these volatiles is also M. incognita increased the concentrations of volatiles compared triggered by mechanical damage (Rose¨ et al., 1996). After in- to plants with leaf damage only. duction, the early or constitutive volatiles are complemented by Like most resistance mechanisms, volatile release in cotton a broad range of acyclic terpenes that are produced de novo is under the control of the jasmonic acid pathway and emission as a response to damage (e.g., (E)-β-ocimene, linalool, (E)- of de novo produced volatiles can be induced by application of α-farnesene, (E)-β-farnesene) (Loughrin et al., 1994; McCall methyl-jasmonate. The constitutive volatiles are not affected by et al., 1994; Pare´ and Tumlinson, 1997a, b). The volatiles are this, as they are mainly released by physical damage to the tissue induced systemically (Figure 4), and the elevated release can (Rodriguez-Sanoa et al., 2001; Zhang et al., 2011). Treatment be detected for at least 48 h (Rose¨ et al., 1996; Rose¨ and Tum- with salicylic acid also triggers the release of volatiles with linson, 2004). The volatile blend emitted from leaves does not a blend similar to that released after P. solenopsis infestation differ when damage occurs on leaves or squares (Rose¨ and (Zhang et al., 2011). Tumlinson, 2004). However, the volatile blend released from Under field conditions, plants are often attacked concurrently damaged squares differs from that of damaged leaves since the by a range of arthropod species. As plants react differently to latter contains more green-leaf volatiles (Rose¨ and Tumlinson, different herbivores, such concurrent infestations can lead to 2004). Loughrin et al. (1995) reported that during the first 24 h surprising results. For example, the total amount of emitted Downloaded by [Agroscope Liebefeld Posieux], [Joerg Romeis] at 01:19 04 July 2013 after caterpillar damage, naturalized cotton (cultivated cotton volatiles from cotton plants infested with both B. tabaci and that spread into the wild) released up to 10 times the amount S. exigua larvae were decreased by about 60% compared to of volatiles measured in commercial cultivars, indicating that plants that were attacked by caterpillars only (Rodriguez-Saona there could be some scope for preservation and/or enhancement et al., 2003). A possible explanation for this effect is cross- of innate arthropod resistance properties in breeding programs. talk between the jasmonic acid pathway (induced by caterpillar Studies on the plant bug L. hesperus, revealed that piercing- feeding) and the salicylic acid pathway (induced by whitefly sucking herbivores can also systemically induce volatiles in feeding) (Zarata et al., 2007). Another explanation could be the cotton (Rodriguez-Saona et al., 2002; Williams et al., 2005). suppression of induced plant resistance by B. tabaci. Extracts from the salivary glands of L. hesperus were capable of inducing the emission of the same volatile blend as measured for 2. Arthropod response to cotton volatiles plants damaged by caterpillars (Rodriguez-Saona et al., 2002). Many cotton volatiles are attractive to parasitic wasps in Thus, the volatile emission appears to be triggered by an uniden- wind tunnel and olfactometer studies (e.g., Elzen et al., 1983; ARTHROPOD HERBIVORES IN COTTON 471

McCall, 1993; Rose¨ et al., 1998), or induce a positive response in the terpene α-pinene (Yan et al., 2004). Spodoptera littoralis electroantennogram recordings (e.g., Li et al., 1992; Hou et al., females were reported to preferentially lay eggs on undamaged 1997; Gouinguene et al., 2005; Williams et al., 2008; Ngumbi cotton plants, as compared to plants damaged by conspecific et al., 2009). Thus, the volatiles that are released in response to larvae (Anderson and Alborn, 1999) or wireworms (Anderson herbivore attack might benefit the plant by attracting parasitoids. et al., 2011). This oviposition preference for undamaged plants This includes parasitoids of caterpillars (e.g., McCall et al., was only visible in older plants (6 leaf stage) and was even re- 1993; Cortesero et al., 1997; DeMoraes et al., 1998; Rose¨ et al., versed in young plants (3-4 leaf stage) (Anderson and Alborn, 1998; Olson et al., 2008, 2009), lepidopteran eggs (Moraes 1999). The role of plant volatile cues in those experiments was et al., 2011), aphids (Hou et al., 1997), and eggs of Lygus spp. demonstrated recently (Zakir et al., 2013). The recognition and (Manrique et al., 2005; Williams et al., 2008). Loughrin et al. avoidance of damaged plants allows herbivores to avoid infe- (1994) reported that volatile emissions by cotton vary over the rior host plants and competition (Anderson and Alborn, 1999; course of a day, but the peak coincides with the main activity Anderson et al., 2011). The plant benefits by receiving fewer window of caterpillar parasitoids like Cotesia marginiventris and smaller herbivore egg batches and by deflecting the herbi- (Hymenoptera: Braconidae). In addition to the volatiles that are vore to nearby plants competing for light, water and nutrients emitted by the cotton plant, some parasitoids also respond to (Anderson et al., 2011). volatiles released from the feces of caterpillar hosts (Rose¨ et al., 1997). These volatiles act as specific host-finding cues for the B. Extrafloral Nectaries wasps and include unprocessed cotton volatiles and compounds Cotton provides sugars to attract and sustain natural enemies modified by caterpillar metabolism (Alborn et al., 1996; Rose¨ in the form of extrafloral nectaries (EFN). Such nectaries are et al., 1997). found in all Gossypium species, except G. tomentosum and G. The reaction of parasitoids to cotton volatiles may vary ac- gossypioides (Fryxell, 1979). Nectaries are located on the lower cording to their level of specialization. While both the generalist surface of the leaves, on one or more of the principal veins, and C. marginiventris and the specialist Microplitis croceipes(Hy- also on the bracts (Fryxell, 1979). The most common predators menoptera: Braconidae) were attracted by herbivore-damaged that attend extrafloral nectar are ants (Wackers¨ and Bonifay, cotton plants, only the generalist showed a preference for freshly 2004). Indirect evidence that EFNs have evolved to attract ants and artificially (mechanical) damaged plants over undamaged comes from the two species lacking extrafloral nectaries (Wack-¨ plants (Rose¨ et al., 1998). Apparently, the largely unspecific ers and Bonifay, 2004). is endemic to green leafy volatiles and constitutive compounds released from Hawaii (Fryxell, 1979), an area of the world devoid of ants until freshly damaged plants serve as host-finding cue for the gen- recently (Wilson, 1996), while G. gossypioides is atypical in eralist (Rose¨ et al., 1998). The Helicoverpa specialist M. cro- that it grows at high altitudes where ant activity is suppressed ceipes can differentiate between volatiles emitted as a response (Wackers¨ and Bonifay, 2004). Rudgers (2002) and Rudgers to damage caused by its host H. zea and damage caused by the et al. (2003) describe a mutualistic association between the wild non-host species S. exigua when both feed on cotton, but not G. thurberi and the ant Forelius pruinosus (Hymenoptera: when they feed on cowpea (McCall et al., 1993). Similarly the Formicidae). The ants reduce herbivory by preying on cater- H. virescens parasitoid Toxoneuron nigriceps (Hymenoptera: pillars or by disturbing their feeding activities and consequently Braconidae) can distinguish cotton volatiles induced by its host enhance seed production. There is some evidence that cotton from those released in response to damage by the non-host plants with EFNs support a larger beneficial arthropod com- species H. zea (De Moraes et al., 1998). munity (Schuster et al., 1976; Hennenberry et al., 1977; Adjei- Few studies dealt with the response of predators to cotton Maafo and Wilson, 1983) and can have positive effects on differ- volatiles. Hegde et al. (2011) reported that adult Chrysoperla lu- ent life-history parameters of nectar feeding predators and par- casina (Neuroptera: Chrysopidae) showed antennal responses to asitoids (Lindgren and Lukefahr, 1977; Schuster and Calderon, odors released by aphid-infested cotton plants. Green lacewings, 1986). Under agricultural conditions, the direct correlation be- Downloaded by [Agroscope Liebefeld Posieux], [Joerg Romeis] at 01:19 04 July 2013 Chrysoperla carnea (Neuroptera: Chrysopidae) and the preda- tween the availability of EFN and the abundance of predators, tory beetle Collops vittatus (Coleoptera: Melyridae) were at- however, may be masked by confounding factors like abundance tracted to insect traps distributed in cotton fields that contained of prey, weed coverage, and plot size. Most importantly, agro- caryophyllene and its derivates, compounds emitted in the bou- nomic practices, such as tillage destroy ant nests and the use of quet of undamaged and damaged cotton plants (Flint et al., 1979, pesticides eliminates many (predatory) arthropods (Naranjo and 1981). Gibson, 1996). When predator numbers are restricted, it is likely Herbivores also detect and respond to cotton volatiles. that the value of EFNs as a resistance factor is also limited. Olfactometer studies revealed that A. gossypii prefers the The production of extrafloral nectar appears to follow the volatile blend released from uninfested cotton plants over that ODT. Constitutive foliar nectar production by undamaged from aphid-infested plants (Hegde et al., 2011). Similarly, G. hirsutum plants ranged between 79 and 204 μg per plant H. armigera is capable of detecting several typical volatile com- per day, while nectaries on the bracts exceed foliar nectar secre- pounds of cotton that are induced after herbivore damage; e.g., tion by a factor of between 80 and 110 (Wackers¨ and Bonifay, 472 S. HAGENBUCHER ET AL.

2004). The production of bracteal nectar shows a distinct peak largely controlled by resistant cotton cultivars derived through on the day of anthesis (where an average 11.7 mg of nectar was genetic engineering (Naranjo and Luttrell, 2009; Naranjo 2011). produced per day), followed by a prolonged secretion during Plants that express Cry toxins derived from the bacterium Bacil- fruit maturation (Wackers¨ and Bonifay, 2004). Valuable repro- lus thuringiensis Berliner (Bt) with high specificity to lepi- ductive tissue is thus considerably better resourced for defenders dopteran species, were produced (Schnepf et al., 1998; Bravo than the less valuable vegetative tissue. Similar to terpenoids and and Soberon, 2008). The first generation of Bt cotton expressed volatiles, foliar nectar production can be induced by above- and the single protein Cry1Ac. Second generation Bt cotton plants below-ground herbivore damage (Wackers¨ and Bezemer, 2003; produce a combination of two insecticidal proteins, which in- Wackers¨ and Bonifay, 2004). After induction by S. littoralis creases their efficacy against the lepidopteran pest complex and feeding, foliar nectar production was enhanced by a factor of helps to delay development of resistance in the target pests. The 12, primarily at the damaged leaf (Wackers¨ et al., 2001). This most common dual-gene Bt cotton plants grown today are Boll- allows the plant to “guide” ants and other predators to the site of gard IIR plants, which produce Cry1Ac and Cry2Ab2 (Naranjo attack. In addition, there was a limited systemic response: nec- et al., 2008). tar production also showed some increase on adjacent younger In 2012, Bt-transgenic cotton cultivars were grown on a total leaves (Wackers¨ et al., 2001) (Figure 4). Four days after removal of 22.5 million hectares worldwide (James, 2012). The high- of the herbivore, nectar production decreased to pre-treatment est adoption rate was reached in Australia (95% of the cotton levels (Wackers¨ et al., 2001). Damage of roots by wireworms area), followed by India (93%), Pakistan (82%), China (80%), (A. lineatus) also increased foliar nectar production. However, the United States (88%), and Burkina Faso (58%) (James, 2012; in this instance the induced nectar is evenly distributed over the USDA Economic Research Service, http://www.ers.usda.gov/). plant (Wackers¨ and Bezemer, 2003) (Figure 4). Using comparative farm-level data in adopting countries, In contrast to the foliar nectar, the bracteal nectar shows high Brookes and Barfoot (2011) estimated that the use of Bt cotton levels of constitutive production, and is not further induced by led to a global reduction in the volume of insecticidal active herbivory. This indicates that the cotton plant has evolved two ingredients applied by 153 million kilograms globally between separate strategies for nectar-mediated resistance in its foliage 1996 and 2009, a 22% change over the 14-year period. In some and its reproductive organs. The high level of bracteal nectar world areas, however, savings in insecticide use were signifi- secreted irrespective of herbivore damage represents a preven- cantly higher (Fitt, 2008; Qaim et al., 2009; Krishna and Qaim, tative strategy, recruiting ants as a standing army that will help 2012). to prevent damage to valuable flowers and squares. In contrast, The high efficacy of Bt cotton and high adoption levels have the low levels of constitutive foliar nectar production, combined caused area-wide suppression in the populations of some impor- with the high level of nectar induction, represents a curative tant cotton pests. For example, Bt cotton has been an important strategy, recruiting ants once herbivores initiate feeding (Wack-¨ factor in the successful eradication program for P. gossypiella ers and Bonifay, 2004). in the southwestern United States (Carriere´ et al., 2003; An- Similar to natural enemies, herbivores may also utilize cotton tilla and Liesner, 2008; Naranjo and Ellsworth, 2010). In six extrafloral nectar as a food source. Several studies comparing provinces of China, Wu et al. (2008) observed a linear decline herbivore pressure between nectariless cotton cultivars and cul- in populations of H. armigera on cotton associated with increas- tivars producing extrafloral nectar have shown larger herbivore ing yields since the adoption of Bt cotton in 1997. This pattern populations on the latter (Lukefahr and Rhyne, 1960; Lukefahr of decline was also observed in many other crops in the region et al., 1965; Schuster et al., 1976; Henneberry et al., 1977; affected by this polyphagous pest. In addition, the high speci- Adjei–Maafo and Wilson, 1983; Flint et al., 1988; Scott et al., ficity of the expressed Cry proteins together with the decline in 1988). However, these studies were conducted in agricultural insecticide use had significant positive effects on the arthropod fields that are characterized by impoverished ant populations. fauna in cotton fields (Romeis et al., 2006; Marvier et al., 2007; Studies done in natural habitats typically show the reverse pat- Wolfenbarger et al., 2008; Naranjo et al., 2008; Naranjo, 2011; Downloaded by [Agroscope Liebefeld Posieux], [Joerg Romeis] at 01:19 04 July 2013 tern (Rudgers 2002, 2003). Lu et al., 2012). This can benefit biological control by creating an environment, in which natural enemies can flourish (Romeis et al. 2008; Naranjo 2011; Lu et al., 2012). Lu et al. (2012) IV. INSECT-RESISTANT TRANSGENIC COTTON demonstrated a marked increase in the abundance of three types Cotton cultivars with improved arthropod resistance are con- of generalist predators (ladybirds, lacewings and spiders) and tinuously developed through methods of conventional breed- decreased aphid abundance in six provinces in China. This was ing and genetic engineering (Hardee and Henneberry, 2004; caused by the adoption of Bt cotton and the reduced insecticide Naranjo et al., 2008; Naranjo, 2011). After the success of the boll sprays for the 1990 to 2010 period. The reduction in insecticide weevil eradication program in the USA (USDA-Aphis, 2006), use, however, can also lead to the development of non-target caterpillars, especially the so called budworm-bollworm com- pests. An example is the increased crop damage attributed to plex of Helicoverpa spp., H. virescens and P. gossypiella, be- plant and stink bugs in Bt cotton (Naranjo et al., 2008; Lu came the most serious cotton pests. This pest complex has been et al., 2008, 2010). Additional factors that may contribute to the ARTHROPOD HERBIVORES IN COTTON 473

development of non-target pests in Bt cotton include the release possible reason for the observation that Cry1Ac-resistant Lep- from direct resource competition by caterpillars (Whitehouse idoptera strains suffer higher mortality on Cry1Ac-expressing et al., 2007; Zeilinger et al., 2011) or from indirect competition, cotton compared to Cry1Ac-containing artificial diets (Tabash- as Bt cotton plants produce less terpenoids due to lower feeding nik et al., 2003; Bird and Akhurst, 2004; Anilkumar et al., damage from caterpillars (Hagenbucher et al., 2013). 2009; Gassmann et al., 2009). For example, Cry1Ac-resistant P. New arthropod-resistant cotton cultivars are continuously de- gossypiella larvae were found to be more vulnerable to gossypol veloped using tools of genetic engineering. Cotton plants ex- than Cry1Ac-susceptible larvae (Carriere´ et al., 2004; Williams pressing other Cry proteins or vegetative insecticidal proteins et al., 2011). The fitness cost related to the Cry1Ac resistance (VIP) from B. thuringiensis have already been commercialized was displayed in reduced larval growth on an artificial diet. The or will reach the market soon (Whitehouse et al., 2007; Naranjo resistant larvae gained less weight on the control diet than the et al., 2008; CERA, 2012). A recent study has also shown the susceptible larvae (5.8% weight reduction), suggesting a resis- potential of controlling emerging hemipteran pests with a newly tance costs even in the absence of gossypol. This resistance cost identified B. thuringiensis crystal protein (TIC807) in the future was magnified in the presence of gossypol leading to an even (Baum et al., 2012). lower weight gain (12.9% weight reduction) than on the control A novel strategy to control cotton pests adapts RNA inter- diet (Williams et al., 2011). In contrast, susceptibility to gossy- ference (RNAi) techniques (Price and Gatehouse, 2008). This pol did not differ between Cry1Ac-resistant and susceptible comprises the use of genetically engineered plants that ex- larvae of H. zea (Anilkumar et al., 2009). It has been hypothe- press double-stranded RNA (dsRNA) of the cytochrome P450 sized that the difference in gossypol sensitivity between the two CYP6AE14 of H. armigera. This enzyme plays an important lepidopteran species is due to differences in the mechanisms of role in the detoxification of gossypol (Luo et al., 2001). Stud- Cry1Ac-resistance (Gassmann et al., 2009). In P. gossypiella, ies by Mao et al. (2007) showed that caterpillars feeding on resistance to Cry1Ac is caused by mutations in genes encoding these plants are more susceptible to gossypol, due to silencing cadherin proteins that bind the Bt toxin (Morin et al., 2003; of the cytochrome caused by the ingested dsRNA. Thereby the Fabrick et al., 2011). It has been postulated that those mutations caterpillars lose an important part of their detoxification system. may disturb the integrity of the midgut membrane and increase The novel insecticidal traits added to cotton will interact its permeability for gossypol, thereby amplifying its toxic effect with the plant’s natural arthropod resistance mechanisms. Un- (Carriere´ et al., 2004, 2006). Indeed, P. gossypiella strains car- derstanding these interactions is important because it likely af- rying these cadherin alleles contain 4.4 (heterozygote strain) or fects the sustainability of genetic engineering as a pest control 13.6 (homozygote strain) times more gossypol after feeding on tool. For example, the arthropod resistance compounds in cot- gossypol-rich artificial diet than Cry1Ac-susceptible larvae with ton could help to increase the durability of Bt cotton. A number a normal cadherin genotype (Williams et al., 2011). In contrast, of studies have shown that the efficacy of the Cry proteins is Cry1Ac resistance in H. zea appears to be due to altered pro- enhanced by cotton insecticidal compounds. For example, the teolysis, and thus gossypol uptake is not affected (Anilkumar resistance of Bt (Cry1Ab) cotton to H. virescens was increased et al., 2008, 2009). when crossed with a high-terpenoid cultivar (Sachs et al., 1996). Furthermore, the effectiveness of Bt cotton against H. armigera was increased by a factor of 4 to 15 when plants had previ- V. INFLUENCE OF ENVIRONMENTAL CONDITIONS ously been induced by caterpillar damage (Olsen et al., 2005a). ON COTTON ARTHROPOD RESISTANCE A similar effect was reported by Mesz´ aros´ et al. (2011) for Numerous abiotic factors influence arthropod resistance in Spodoptera frugiperda (Lepidoptera: Noctuidae) when Bt cot- cotton. For example, Stipanovic et al. (1988) found that ter- ton plants were induced by the application of jasmonic acid. penoid concentrations in leaves of 14 cotton cultivars differed In contrast are the results of Olson and Daly (2000), were ex- among plants grown in five different locations. The impact of periments revealed that the age of plants could influence the environmental factors on cotton arthropod resistance, however, Downloaded by [Agroscope Liebefeld Posieux], [Joerg Romeis] at 01:19 04 July 2013 toxicity of Cry1Ac. When leaves of fruiting cotton plants and has mainly been investigated for Bt-transgenic cotton cultivars. presquare cotton were incorporated in various diets containing Temperature appears to be particularly important. For example, Cry1Ac protein it was found that leaves from the older, fruit- Chen et al. (2005a) provide some evidence for reduced Cry pro- ing cotton plants reduced the toxicity of the toxin by 14 to tein levels in cotton grown at high temperatures. Olsen et al. 726-fold (Olsen and Daly, 2000). The authors suggested that (2005a) reported that Bt cotton exposed to cool temperatures tannins were a main reason for this effect by either limiting in the early part of the growing season suffered increased H. the availability of the Cry protein or by reducing its toxicity, armigera damage. Since the expression of the cry1Ac transgene a fact suggested earlier for example by Navon et al. (1993). remained unaffected by temperature in that study, the factors Cotton terpenoids may also play a role in delaying the evolu- responsible for the observed effects were likely due to some tion of resistance against certain Cry proteins in the target pests. other plant compounds and/or their interactions. Resistance is often linked to fitness costs, which can result in Herbivore-induced cotton plants grown under conditions increased susceptibility against cotton terpenoids. This is one with limited available water (125 ml/day) were preferred 474 S. HAGENBUCHER ET AL.

feeding sites for S. exigua when compared to “normal-water” such as gossypol and condensed tannins increased, resulting in a plants (500 ml/day); in a choice experiment larvae consumed stronger induced response after herbivory (Coviella et al., 2002; about 9 times more leaf tissue from water-stressed plants, in- Chen et al., 2005b; Wu et al. 2007, 2011; but see Sun et al., dicating reduced terpenoid production in these plants (Olson 2011). In spite of this, H. armigera larvae consumed more Bt et al., 2009). The parasitoid M. croceipes did not prefer water- or non-Bt cotton material under elevated CO2 conditions, most stressed plants: in a wind-tunnel assay only about 10% of all likely to compensate for the reduced N content (Chen et al., parasitoids landed on the water-stressed plants while the rest fa- 2005b). Thus, an increase in CO2 levels might lead to higher vored the unstressed plants (Olson et al., 2009). This preference plant damage by herbivores. It is, however, unclear if cotton of parasitoids for unstressed plants was explained by a reduc- will adapt to elevated CO2 levels as has been reported for other tion of emitted volatiles in water-stressed plants. A sufficient plants (Lee et al., 2001; Chen et al., 2010). supply of water seems to be crucial for a high gossypol content in cotton plants as irrigation was found to increase the gossypol content in cotton seeds by 21% (Pettigrew and Dowd, 2011). VI. CONCLUSIONS Even water-logging (an overabundance of water) had a positive Cotton possesses a broad range of arthropod resistance traits. impact on terpenoids as it increased the foliage terpenoid con- Most of the studies on cotton-herbivore interactions have been centration by as much as 100% (Luo et al., 2008). Bt toxins conducted with lepidopteran species since they represent most are also influenced by water availability. Water deficiency was of the major cotton pests. The impact of the resistance traits on reported to decrease Cry protein levels in Bt cotton (Benedict other cotton pests and natural enemies has received relatively et al., 1996). These findings fit with an earlier report that under little attention. drought and heat conditions, cotton plants produce heat shock Direct resistance mechanisms include morphological traits proteins at the expense of normal protein synthesis (Burke et al., like trichomes. The most important mechanism of direct re- 1985). However, water-logging reduced Cry1Ac toxin levels by sistance in cotton plants, however, is a group of closely re- as much as much 38–50%, depending on cultivar and duration lated terpenoids: gossypol, hemigossypolone and the heliocides of exposure (Luo et al., 2008). 1–4. These compounds affect herbivores and provide resistance Another environmental factor that could influence cotton her- against pathogens. Terpenoid production is inducible and their bivore resistance is the salt content of the soil. While a high distribution follows the optimal-defense theory. Several minor salinity (up to 0.05% NaCl) increased the foliar terpenoid con- secondary metabolites, like tannins and flavonoids also con- centration by 20–59%, it had the opposite effect on Cry1Ac tribute to direct resistance. Furthermore, cotton plants possess levels, which were reduced by 11.3–22.4%. If salt-stress was inducible indirect resistance traits, like the emission of volatiles combined with waterlogging, Cry1Ac concentrations were re- and the production of extrafloral nectar that attract and sustain duced by as much as 72% (Luo et al., 2008). The exact effects of populations of beneficial insects. this stress, however, depend on the cultivar used and the duration Despite the number of resistance mechanisms, cotton is at- of exposure. tacked by a complex of arthropod pests and still receives a The plants’ C:N ratio can be affected by the extensive use lot of insecticide treatments. Therefore the wealth of resistance of nitrogen fertilizers. On the one hand, high nitrogen levels mechanisms provided by the plant should be explored by se- increase the total protein in plants (Baker et al., 1980), which lecting for cultivars and production methods that enhance the can also increase the Bt protein levels (Pettigrew and Adamczyk, plants’ direct and/or indirect resistance traits. This needs to be 2006). On the other hand, application of nitrogen fertilizers has supplemented with production methods that conserve predators been found to reduce the induction of terpenoids, jasmonic acid and parasitoids; e.g., reduced insecticide use, use of selective and volatiles, in response to herbivory damage (Chen et al., insecticides, reduced tillage to increase ant densities or habitat 2008; Olson et al., 2009). Consequently, both under- and over- management to provide beneficials with alternative food sources fertilized plants were preferred feeding sites for S. exigua larvae or overwintering sites. Downloaded by [Agroscope Liebefeld Posieux], [Joerg Romeis] at 01:19 04 July 2013 and less attractive to the parasitoid M. croceipes (Olson et al., Since 1996, genetically engineered cotton cultivars that pro- 2009). duce insecticidal Cry proteins derived from Bacillus thuringien- The rising CO2 levels in our atmosphere will influence the sis have become an important component of IPM in the major defensive chemistry of Gossypium species. Elevated CO2 levels cotton producing regions in the world. The deployment of these increase the photosynthetic rate in plants, thereby increasing Bt cotton cultivars has had a major impact on the control of growth rate and the carbon to nitrogen (C:N) ratio (Chen et al., key lepidopteran pests and has caused a significant decline in 2010). According to the carbon–nutrient balance hypothesis the use of chemical insecticides, with benefits for biological (Bryant et al., 1983), the allocation of resistance resources will pest control and biodiversity in general. Bt cotton technology, likewise shift to substances that do not contain nitrogen. This however, targets only lepidopteran pests, which while very im- has been reported from studies with Bt cotton where elevated portant, represent only a fraction of the arthropod complex that CO2 levels resulted in a significant decrease in the Cry protein, affects cotton production globally. Consequently, conventional which contains nitrogen. In contrast, carbon-based compounds host plant resistance and other components of IPM are still ARTHROPOD HERBIVORES IN COTTON 475

essential to control pests and diseases that are not currently tar- thuringiensis Cry1Ac-resistant cotton bollworm Helicoverpa zea (Boddie). geted by transgenic crop technology. This includes the plant and Appl. Environ. Microbiol. 74: 462–469. stink bugs that have benefited from the reduction in insecticide Anilkumar, K. J., Sivasupramaniam, S., Head, G., Orth, R., Van Santen, E., and Moar, W. J. 2009. Synergistic interactions between Cry1Ac and natural cotton use in Bt cotton. In addition, these is evidence that secondary defenses limit survival of Cry1Ac–resistant Helicoverpa zea (Lepidoptera: plant compounds in cotton, terpenoids in particular, can enhance Noctuidae) on Bt cotton. J. Chem. Ecol. 35: 785–795. the efficacy of Cry toxins and also increase the fitness costs as- Antilla, L. and Leisner, L. 2008. Program advances in the eradication of Pink sociated with the resistance against the Cry toxins in the target Bollworm Pectinophora gossypiella in Arizona cotton. 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