Mean (± SE) water potential (bar), and numbers of dry leaves, Mexican rice borer egg clusters, total eggs, entry holes, and exit holes per stalk of two sugarcane varieties maintained under well watered or drought stressed greenhouse conditions (Showler & Castro, 2010a)
1. Introduction
When the availability of water is insufficient to maintain plant growth, photosynthesis, and transpiration, plants become water deficit stressed (Fan et al., 2006), a serious problem that reduces world crop production (Boyer, 1982; Vincent et al., 2005). While drought has profound direct detrimental effects against plants, including rendering otherwise arable regions less, or non-, arable, herbivorous arthropod populations and the injuries they cause can be affected by stress-related changes that occur in the plant. Moderate stress is known to heighten the nutritional value of some plants’ tissues and juices, in some instances to reduce concentrations of plant defense compounds, and even to select against predators and parasitoids that otherwise help reduce pest populations to economically tolerable levels, each of which can contribute toward greater pest infestations. Sometimes the injury inflicted on water deficit stressed plants is intensified even if numbers of the pest haven’t been affected, as in the instances of honeylocust spider mites,
Although severe water deficit stress that causes plant mortality usually renders plants useless to herbivores, chronic lower level or pulsed water deficit stress can enhance the nutritional value of plants to arthropods, resulting in selection preference, heightened populations, intensified injury to crops, and even outbreaks that affect production on area-wide scales. Twospotted spider mite,
Water deficit stress in plants can affect the amounts and composition of volatile compounds, and the concentrations of several kinds of nutrients beneficial to arthropod pests. Its associations with free amino acids and carbohydrates are chiefly described in this chapter because those two kinds of nutrients have been researched to an appreciable extent, permitting some conclusions to be drawn about arthropod host plant selection and levels of infestation.
2. Water deficit, host plant nutrient accumulation, and associations with phytophagous arthropods
Water deficit stress alters plant metabolism and biochemistry (Hsiao, 1973; Beck et al., 2007), and consequent changes to plant physiological processes have been reported as being factors affecting herbivorous arthropod host plant preferences, growth, and development (Mattson & Haack, 1987; Showler, 2012 ). Although soil dries in association with drought, evapotranspiration rates in affected plants are often maintained (Jordan & Ritchie, 1971) by elevated accumulations of free amino acids, especially proline, and other organic solutes (Janagouar et al., 1983). Osmotic stress in plants involves several interlinked molecular pathways that transmit signals and produce stress-responsive metabolites (Ingram & Bartels, 1996; Zhu, 2002), and gene transcripts associated with signaling can be up- or down-regulated minutes after stress induction (Seki et al., 2001; Showler et al., 2007). Water deficit stressed plants often have diminished osmotic potential (Labanauskas et al., 1981; Golan-Goldhirsch et al., 1989; Bussis & Heineke, 1998), heightened oxidative stress (Becana et al., 1998; Knight & Knight, 2001), and accumulations of osmolytes such as antioxidants, amino acids, carbohydrates, and inorganic ions, altering the attractiveness and nutritional value of the plant (Jones, 1991; Showler & Castro, 2010a). Reduced leaf water content relative to dry biomass in water deficit stressed plants, in combination with the increased quantities of nutritional metabolites (White, 1984; Dubey, 1999; Ramanulu et al., 1999; Garg et al., 2001), may contribute toward the increased nutritional value of plants per unit of surface area consumed by arthropods. It is likely that arthropods can perceive cues about host plant suitability from emission of plant volatile compounds, or semiochemicals.
Chemical cues from plants play a major, perhaps decisive, role in host plant selection and utilization by herbivorous arthropods (Schur & Holdaway, 1970; Fenemore, 1980; Waladde, 1983; Burton & Schuster, 1981; Ramaswamy, 1988; Salama et al., 1984; Udayagiri & Mason, 1995). Water deficit stress in plants alters plant metabolism which can affect quantities and combinations of volatile compounds (Apelbaum & Yang, 1981; Hansen & Hitz, 1982; Zhang & Kirkham, 1990). Apple trees,
Once the phytophagous arthropod has found or selected the host plant, contact chemoreceptors on many are important in the acceptance or rejection of a host plant based on the presence or absence of stimulant (
In addition to elevated levels of free essential amino acids, free proline, a nonessential amino acid that accumulates in most water deficit-afflicted plants, is a feeding stimulant for many phytophagous arthropods (Mattson & Haack, 1987; Städler, 1984). Dadd (1985) reported that a number of amino acids, particularly glycine, alanine, serine, methionine, histidine, proline, and γ-aminobutyric acid, were phagostimulants to a number of insect species. Amino acids that elicited the greatest response as feeding stimulants to southwestern corn borer larvae were determined to be arginine, histidine, lysine, methionine, phenylanaline, valine (essentials), alanine, glycine, and serine (nonessentials) (Hedin et al., 1990), but not proline.
Water deficit stress has also been associated with increased concentrations of carbohydrates (which have important roles in osmotic adjustment) in many plants (Schubert et al., 1995; Kameli & Lösel, 1996; Massacci et al., 1996; Mohammadkhani & Heidari, 2008). Corn plants with elevated soluble carbohydrate concentrations were preferred by the European corn borer for oviposition (Derridj & Fiala, 1983; Derridj et al., 1986), and styloconic sensilla of larvae and adults of three noctuid species were highly responsive to sugars, especially sucrose and fructose (Blaney & Simmonds, 1988). These two sugars are known to be important feeding stimulants for both life stages (Frings & Frings, 1956; Blom, 1978), and fructose, glucose, maltose, and sucrose have been identified as phagostimulants for other insects (Bernays, 1985). Electrophysiological recordings revealed that the maxillary sensilla styloconica of fifth instar African armyworm,
3. Water is a nutrient, too
Water deficit affects both the availability of water, which is a nutrient itself, to herbivores as well as the nutritional quality of dietary biochemical components that accumulate as osmoprotectants or for other purposes. When herbivorous arthropods are unable to have access to sufficient amounts of wager, their populations can decline. For example, aphid populations are reduced under conditions of continued and severe host plant water deficit (
Showler, 2012
). Black bean aphid,
The greater nutritional quality of water deficit stressed plants can be offset by the condition that causes it: insufficient water. When provided with dried, ground material from water-deficit stressed tomato plants,
4. Some non-nutrient-related associations of water deficit with phytophagous arthropods
Host plant selection among insects also involves visual and physical factors such as leaf shape, color, and size (Ramaswamy, 1988; Renwick & Radke, 1988; Renwick & Chew, 1994; Showler & Castro, 2010b), and both constitutive and inducible plant chemical defenses can vary in response to water deficit stress (Lombardero et al., 2000), but visual and physical cues, and defensive compounds are not considered as being nutritional for the purposes of this chapter (although defensive compounds might loosely be considered as being types of nutrients, they mostly repel, interfere with feeding, or act as toxins). Concentrations of several classes of defensive secondary compounds tend to increase in plant tissues in response to moderate drought, including terpenoids (some of which are attractants (Mattson & Haack, 1987) and alkaloids (Gershenson, 1984; Hoffmann et al., 1984; Sharpe et al., 1985; Lorio, 1986; Mattson & Haack, 1987; Showler, 2012 ), but intensified drought stress can lead to reductions of these compounds (Mattson and Haack, 1987). Drought can also influence predator and parasitoid guilds that affect phytophagous arthropod populations ( Showler, 2012 ), but plant stress is not directly involved. Other mechanisms that might also contribute toward plant vulnerability to herbivorous arthropods under conditions of water deficit stress have been suggested (Mattson & Haack, 1987), including acoustical cues, detoxification of foods by drought stressed insects, and drought-induced genetic changes in arthropods, but they have not been well substantiated.
5. Multiple effects of water deficit: case study on sugarcane and the Mexican rice borer
The Mexican rice borer,
Eggs are mostly deposited in clusters within folds of dry sugarcane leaves, although eggs are also laid in folded green living tissue if available (Showler & Castro, 2010b). Van Leerdam et al. (1986) found 96% of the pest’s eggs on the basal 80 cm of sugarcane plants where most dry leaf tissue is located. The Mexican rice borer is not so much stress-oriented as it is nutritionally-oriented in that it prefers to lay eggs on dry foliage of plants stressed by limited water and of plants growing in enriched soil (Showler & Castro, 2010a; Showler & Reagan, 2012). Water deficit stress in sugarcane plants, however, unlike over-fertilized plants, offers increased quantities of dry, folded leaf tissue per plant, contributing to the crop’s vulnerability (Reay-Jones et al., 2005; Showler & Castro, 2010b). In a greenhouse no-choice cage experiment using sugarcane plants from which all dry leaf tissue was excised and removed from the cages, or placed at the bottom of the cages like a mulch, and intact (dry leaf tissue remained on the plants) sugarcane plants (controls), numbers of eggs and the degree of larval infestation was distinctly greater on the controls (Figs. 1 & 2; Showler & Castro, 2010b).
Early instars feed on living leaf tissue, under fresh leaf sheaths, and some tunnel into the leaf midrib; later instars bore into the main stalk (Wilson, 2011). Injury from stalk tunneling results in deadheart, decreased sugar production, and stunting or lodging of stalks sometimes so severe that harvest becomes unfeasible (Johnson, 1985; Legaspi et al., 1997; Hummel et al., 2008). Tunnels within host plant stalks are packed with frass, blocking entry of predators and parasitoids (Hummel et al., 2008). Pupation occurs within the stalk after mature larvae make emergence holes protected with a thin window of outer plant tissue (Hummel et al., 2008). In the Lower Rio Grande Valley, a life cycle takes 30–45 days, and there are 4–6 overlapping generations per year (Johnson, 1985; Legaspi et al., 1997). Tunneling damage and the insect’s prevalence has made it the key sugarcane pest of south Texas, displacing the sugarcane borer,
Approximately 20% of sugarcane internodes are injured by Mexican rice borers in south Texas, and larval entry holes also provide portals for red rot, resulting in additional loss of sugar (Van Zwaluwenberg, 1926; Osborn & Phillips, 1946; Johnson, 1985). On some varieties of sugarcane, up to 50% bored internodes have been reported ( Johnson, 1981 ); Mexican rice borer injury results in losses of US$575 per hectare of sugarcane (Meagher et al., 1994) and US$10–20 million annually (Legaspi et al., 1997, 1999). Projected economic consequences of Mexican rice borer infestation of Louisiana includes US$220 million in sugarcane and US$45 million in rice (Reay-Jones et al., 2008). In corn, stalk boring and secondary infection by stalk rot pathogens can cause shattering, lodging, and complete collapse of stalks (Showler et al., 2011) such that by season’s end >50% of stalks of susceptible varieties are destroyed (Showler, unpublished data).
A connection between irrigation practices and severity of Mexican rice borer infestation was first suggested by Meagher et al. (1993), and later studies indicated that drought stressed sugarcane is preferred for oviposition because there is more dry leaf tissue and the nutritional value, at least in terms of a number of important free amino acids, is enhanced (Tables 1 & 2) (Muquing & Ru-Kai, 1998; Reay-Jones et al., 2005, 2007; Showler & Castro, 2010a). Although severe water deficit stress of sugarcane reduces sugar production, some cultivars under moderate stress accumulate sugars (Hemaprabha et al., 2004), and Mexican rice borer preference among species of host plants (Showler et al., 2011) has been associated with concentrations of fructose (Showler, unpublished data). Differences in oviposition preference were not observed on excised dry leaf tissue regardless of whether the sugarcane plant from which it originated was water deficit stressed or well watered; hence, the expression of sugarcane vulnerability or resistance appears to require the pest’s ability to detect nutrients in living leaf tissue (Showler & Castro, 2010b). Although a sugarcane cultivar with some degree of resistance to the Mexican rice borer was still better protected than a susceptible variety under drought conditions, water deficit increased injury to the crop by ≈2.5-fold in each (Reay-Jones et al., 2005). Reay-Jones et al. (2003) also reported that high soil salinity, a stress factor that also heightens free amino acid accumulations in plants (Labanauskas et al., 1981; Cusido et al., 1987), increases Mexican rice borer infestations in sugarcane. Further, relatively high concentrations of organic matter incorporated into soil of the Lower Rio Grande Valley (and conventionally fertilized with nitrogen) resulted in 18% more stalk production per sugarcane stool but this effect was offset by substantial increases in Mexican rice borer infestation, causing stalk weight, length, and percentage brix reductions relative to sugarcane fertilized with conventional nitrogen fertilizer or chicken litter (Showler, unpublished data). The composted soil was associated with greater accumulations of free amino acids and fructose (Showler, unpublished data). These associations reveal that the pest is not responding simply to water deficit, but instead to nutritional enhancement of the plant whether moderated by stress or by other factors.
|
|
In addition to water deficit stress associations with Mexican rice borer preferences for physical (
6. Conclusion
Water deficit might initially appear to affect herbivorous arthropod populations because of a single factor, but the associations of the Mexican rice borer with water indicate a more complex relationship that can involve physical, biochemical, and ecological factors. Levels of Mexican rice borer infestation are likely influenced by low water availability in at least three ways, only one of which is directly related to the nutritional status of the crop. Drought changes many environmental conditions relative to arthropods, such as soil condition, leaf size and color, lignification of plant cell walls, secondary protective compounds, and natural enemy activity, but accumulations of nutrients, particularly free amino acids and carbohydrates, unlike the other drought-related conditions, directly result from water deficit stress to the plant. This plant stress response to water deficit influences levels of pest infestations by causing the plant emit volatile semiochemicals and by enhancing the nutritional quality of the plant. Water deficit can also make it difficult for some plant sucking insects (
References
- 1.
Akbar W. Showler A. T. White W. H. Reagan T. E. 2010 Categorizing sugarcane cultivars for resistance to the sugarcane aphid and yellow sugarcane aphid (Hemiptera: Aphididae).Journal of Economic Entomology 103 1431 1437 0022-0493 - 2.
Apelbaum A. Tang S. F. 1981 Biosynthesis of stress ethylene induced by water deficit 68 594 596 0981-9428 - 3.
Archer T. L. Bynum E. D. Jr Onken A. B. Wendt C. W. 1995 Influence of water and nitrogen fertilizer on biology of the Russian wheat aphid (Homoptra: Aphdidae) on wheat.Crop Protection 14 165 169 0261-2194 - 4.
Assefa Y. Conlong D. E. Van den Berg. J. Le Rü B. P. 2008 The wider distribution ofEldana saccharina (Lepidoptera: Pyralidae) in South Africa and its potential risk to maize production.Proceedings of the South African Sugarcane Technologists Association 81 290 297 0370-1816 - 5.
Auclair J. L. 1963 Aphid feeding and nutrition. 8 439 491 0066-4170 - 6.
Bailey W. 2000 Notes from Missouri’s fields.Integrated Pest and Crop Management Newsletter 10 1 2 0838-0937 - 7.
Becana M. Moran J. F. Iturbe-Ormaete I. 1998 Iron-dependent oxygen free radical generation in plants subjected to environmental stress: toxicity and antioxidant protection 201 137 147 0003-2079 X. - 8.
Beck E. H. Fettig S. Knake C. Hartig K. Bhattarai T. 2007 Specific and unspecific responses of plants to cold and drought stress Journal of Bioscience 32 501 510 0973-7138 - 9.
Bernays E. A. 1985 Regulation of feeding behavior. InInsect Physiology, Biochemistry, and Pharmacology: Regulation, Digestion, Nutrition, Excretion , G.A. Kerbut, G.A. & Gilbert, L.I. (eds.),1 32 Pergamon Press,100080308058 New York, USA. - 10.
Bernays E. A. Chapman R. F. 1994 Host-Plant Selection by Phytophagous Insects 100412031310 York, New York, USA. - 11.
Bjőrkman C. 2000 Interactive effects of host resistance and drought stress on the performance of a gall-making aphid living on Norway spruce.Oecologia 123 223 231 0029-8549 - 12.
Blaney W. M. Simmonds M. S. J. 1988 Food selection in adult and larvae of three species of Lepidoptera: a behavioral and electrophysiological study.Entomologia Experimentalis et Applicata 49 111 121 0013-8703 - 13.
Blom F. 1978 Sensory activity and food intake: a study of input-output relationships in two phytophagous insects. Nederlands Journal of Zoology28 277 340 0028-2960 - 14.
Boyer J. S. 1982 Plant productivity and environment. Science 218 443 448 0036-8075 - 15.
Branco M. Pereira J. S. Mateus E. Tavares C. Paiva M. R. 2010 Water stress affects Tomicus destruens host pine preference and performance during the shoot feeding phasedoi: forest/201021,1286-4560 - 16.
Brodbeck B. Strong D. 1987 Amino acid nutrition of herbivorous insects and stress to host plants. InInsect Outbreaks ; Barbosa, P. & Schultz, J. C. (eds.),346 364 Academic Press,0-12078-148-4 England. - 17.
Browning H. W. Way M. O. Drees B. M. 1989 Managing the Mexican rice borer in Texas Texas Agricultural Extension Service Bulletin B-1620. - 18.
Bultman T. L. Bell G. D. 2003 Interaction between fungal endophytes and environmental stress influences plant resistance to insects.Oikos 103 182 190 0030-1299 - 19.
Burgess A. J. Warrington S. Allen-Williams L. 1994 Cabbage aphid (Brevicoryne brassicae L.) ‘performance’ on oilseed rape (Brassica napus L.) experiencing water deficiency: roles of temperature and food quality.Acta Horticulturae 407: ISHS Brassica Symposium- IX Crucifer Genetics Workshop,16 19 0567-7572 - 20.
Burton R. L. Schuster D. J. 1981 Oviposition stimulant for tomato pinworm from surfaces of tomato plants.Annals of the Entomological Society of America 74 512 515 0013-8746 - 21.
Bussis D. Heineke D. 1998 Acclimation of potato plants to polyethylene glycol-induced water deficit. II. Contents and subcellular distribution of organic solutes. 49 1361 1370 1460-2431 - 22.
Calatayud P. A. Polania M. A. Seligmann C. D. Bellotti A. C. 2002 Influence of water-stressed cassava on Phenacoccus herreni and three associated parasitoids102 163 175 0013-8703 - 23.
Cates R. G. Redack R. A. 1988 Variation in the terpene chemistry of Douglas fir and its relationship to western spruce budworm success. InChemical Mediation of Coevolution ; Spencer, K.C. (ed.),317 344 Academic Press,978-0-12656-856-1 San Diego, California, USA. - 24.
Chen Y. Ruberson J. R. Olson D. M. 2008 Nitrogen fertilization rate affects feeding, larval performance, and oviposition preference of the beet armyworm, Spodoptera exigua, on cotton.126 244 255 0013-8703 - 25.
Chrominsky A. Visscher-Neumann S. Jurenka R. 1982 Exposure to ethylene changes nymphal growth rate and female longevity in the grasshopperMelanaphis sanguinipes .Naturwissenschaften 69 45 66 0028-1042 - 26.
Cole R. A. 1997 The relative importance of glucosinolates and amino acids to the development of two aphid pests Brevicoryne brassicae andMyzus persicae on wild and cultivated brassica species85 121 133 0013-8703 - 27.
Cusido R. M. Palazon J. Altabella T. Morales C. 1987 Effect of salinity on soluble protein, free amino acids and nicotine contents in Nicotiana rustica L102 55 60 0003-2079 X. - 28.
Dadd R. H. 1985 Nutrition: organisms. InComprehensive Insect Physiology, Biochemistry and Pharmacology: Regulation, Digestion, Nutrition, Excretion , Kerkut, G.A. & Gilbert, L.I. (eds.),315 319 Pergammon Press,100080308058 New York, USA. - 29.
Derridj S. Fiala V. 1983 Sucres solubles des feuilles de mais (Zea mays L.) et oviposition de la pyrale (Ostrinia nubilalis Hbn.).Comptes Rendues Academie Agriculture Francais 69 465 472 0001-3986 - 30.
Derridj S. Fiala V. Jolivet E. 1986 Increase of European corn borer ( Ostrinia nubilalis ) oviposition induced by a treatment of maize plants with maleic hydrazide: role of leaf carbohydrate.41 305 310 0013-8703 - 31.
Dethier V. G. 1980 Evolution of receptor sensitivity to secondary plant substances with special reference to deterrents 115 45 66 0003-0147 - 32.
Dix M. E. Cunningham A. A. King R. M. 1996 Evaluating spring cankerworm (Lepidoptera: Geometridae) preference for Siberian elm clones 25 58 62 0004-6225 X. - 33.
Dorschner K. W. Johnson R. C. Eikenbary R. D. Ryan J. D. 1986 Insect-plant interactions: greenbug (Homoptera: Aphididae) disrupt acclimation of winter wheat to drought stress.Environmental Entomology 15 118 121 0004-6225 X. - 34.
Douglas A. E. Van Emden H. F. 2007 Nutrition and symbiotes. InAphids as Crop Pests Van Emden, H.F. & Harrington, R., (eds.),112 134 CAB International,1-96399-939-6 Park, England. - 35.
Dubey R. S. 1999 Protein synthesis by plants under stressful conditions. InHandbook of Plant and Crop Stress, Pessarakli, M. (ed.),365 386 Marcel Dekker,978-1-43981-396-6 New York, New York, USA. - 36.
Dunn J. P. Kimmerer T. W. Nordin G. L. 1986 Attraction of the twolined chestnut borer, stressed white oak.Agrilus bilineatus (Weber) (Coleoptera: Buprestidae), and associated borers to volatiles ofCanadian Entomologist 118 503 509 - 37.
Ebel R. C. Mattheis J. P. Buchanan D. A. 1995 Drought stress of apple trees alters leaf emissions of volatile compounds 92 709 712 0031-9317 - 38.
English-Loeb G. Stout M. J. Duffey S. S. 1997 Drought stress in tomatoes: changes in plant chemistry and potential nonlinear consequences for insect herbivores. Oikos79 456 468 0030-1299 - 39.
Fan L. Linker R. Gepstein S. Tanimoto E. Yamamoto R. Neumann P. M. 2006 Progressive inhibition by water deficit of cell wall extensibility and growth along the elongation zone of maize roots is related to increased lignin metabolism and progressive stellar accumulation of wall phenolics. Plant Physiology140 603 612 0981-9428 - 40.
Fenemore P. G. 1980 Oviposition of potato tuber moth,Phthorimaea operculella Zell. (Lepidoptera: Gelechiidae): identification of host-plant factors influencing oviposition response.New Zealand Journal of Zoology 7 435 439 0301-4223 - 41.
Fillman D. A. Sterling W. L. 1983 Killing power of the red imported fire ant (Hym.: Formicidae): a key predator of the boll weevil (Coleoptera: Curculionidae). Entomophaga28 339 344 0013-8959 - 42.
Frings H. Frings M. 1956 The loci of contact chemoreceptors involving in feeding reactions in certain Lepidoptera.Biology Bulletin 110 291 199 0006-3185 - 43.
Garg B. K. Kathju S. Burman U. 2001 Influence of water stress on water relations, photosynthetic parameters and nitrogen metabolism of moth bean genotypes.Biologia Plant 44 289 292 1573-8264 - 44.
Gershenson J. 1984 Changes in the levels of plant secondary metabolites under water and nutrient stress. Recent Advances in Phytochemistry18 273 320 0079-9920 - 45.
Girousse C. Bournoville R. 1994 Role of phloem sap quality characteristics on performance of pea aphid grown on lucerne genotypes.Entomologia Experimentalis et Applicata 70 227 235 0013-8703 - 46.
Godfrey L. D. Holtzer T. O. Spomer S. M. Norman J. M. 1991 European corn borer (Lepidoptera:: Pyralidae) tunneling and drought stress: effects on corn yield.Journal of Economic Entomology 54 1850 1860 0022-0493 - 47.
Golan-Goldhirsch A. N. Samish S. Agami M. Lips H. 1989 The relationship between some perennial desert plants originated in different phytogeographical regions and proline concentration. Journal of Arid Environments17 327 333 0140-1963 - 48.
Haack R. A. Slansky F. Jr 1987 Nutritional ecology of wood-feeding Coleoptera, Lepidoptera, and Hymenoptera. InThe Nutritional Ecology of Insects, Mites, and Spiders ; Slansky, F., Jr. & Rodriguez, J.G. (eds.),449 486 John Wiley & Sons,10 New York, New York, USA. - 49.
Hansen A. D. Hitz W. D. 1982 Metabolic responses of mesophytes to plant water stress.Annual Review of Plant Physiology 33 163 203 0079-9920 - 50.
Harfouche A. L. Shivaji R. Stocker R. Williams P. W. Luthe D. S. 2006 Ethylene signaling mediates a maize defense response to insect herbivory. Molecular Plant-Microbe Interactions19 189 199 0094-0282 - 51.
Hedin P. A. Thompson A. C. Gueldner R. C. 1976 Cotton plant and insect constituents that control boll weevil behavior and development. InBiochemical Interactions Between Plants and Insects, Wallace, J.W. & Mansek, R.K. (eds.),271 350 Plenum,0-30634-710-5 York, New York, USA. - 52.
Hedin P. A. Davis F. M. Williams W. P. Salin M. L. 1984 Possible factors of leaf-feeding resistance in corn to the southwestern corn borer.Journal of Agricultural and Food Chemistry 32 262 267 0021-8561 - 53.
Hedin P. A. Williams W. P. Davis F. M. Buckley P. M. 1990 Roles of amino acids, protein, and fiber in leaf-feeding resistance of corn to the fall armyworm.Journal of Chemical Ecology 16 1977 1995 0098-0331 - 54.
Hemaprabha G. Nagarajan R. Alarmelu S. 2004 Responses of sugarcane genotypes to water deficit stress.Sugar Tech 6 165 168 0972-1525 - 55.
Hodges J. D. Lorio P. L. Jr 1975 Moisture stress and composition of xylem oleoresin in loblolly pine. Forest Science21 283 290 0001-5749 X. - 56.
Hoffman J. J. Kingsolver B. E. Mc Laughlin S. P. Timmermann B. N. 1984 Production of resins by arid-adapted Asteraea.Recent Advances in Phytochemistry 18 251 271 0079-9920 - 57.
Hsiao T. C. 1973 Plant responses to water stress.Annual Review of Plant Physiology 24 519 570 0079-9920 - 58.
Huffman F. R. Mueller A. J. 1983 Effects of beet armyworm (Lepidoptera: Noctuidae) infestation levels on soybean.Journal of Economic Entomology 76 744 747 0022-0493 - 59.
Hummel N. Reagan T. E. Pollet D. Akbar W. Beuzelin J. M. Carlton C. Saichuk J. Hardy T. Way M. O. 2008 Mexican rice borer,Eoreuma loftini (Dyar). Louisiana State University AgCenter Pub. 3098, Baton Rouge, LA. - 60.
Hummel N. A. Hardy T. Reagan T. E. Pollet D. Carlton C. Stout M. J. Beuzelin J. M. Akbar W. White W. H. 2010 Monitoring and first discovery of the Mexican rice borer,Eoreuma loftini (Lepidoptera: Crambidae) in Louisiana.Florida Entomologist 93 123 124 0015-4040 - 61.
Ingram J. Bartels D. 1996 The molecular basis of dehydration tolerance in plants.Annual Review of Plant Physiology and Plant Molecular Biology 47 377 403 1040-2519 - 62.
Ishii S. Azim A. Hirano C. 1959 A further experiment on the effect of dietary levels of protein and carbohydrate on the growth of the rice stem borer, Chilo suppressalis larvae. Japanese Journal of Applied Entomology and Zoology3 143 145 0021-4914 - 63.
Ishii S. 1971 Nutritional studies of the rice stem borer,Chilo suppressalis Walker, and its mass rearing.Entomophaga 16 165 173 0013-8959 - 64.
Janagouar B. S. Venkatasubbaiah D. Janardhan K. V. Panchal Y. C. 1983 Effect of short term stress on free proline accumulation, relative water content and potassium content in different plant parts of three cotton genotypes. Indian Journal of Plant Physiology26 82 87 0019-5502 - 65.
Johnson K. J. R. 1981 Acigona loftini (Lepidoptera: Pyralidae) in the Lower Rio Grande Valley of Texas, 1980-1981. InProceedings of the 2 nd Inter-American Sugar Cane Seminar (Insect and Rodent Pests) , Miami, Florida, USA,166 171 - 66.
Johnson K. J. R. 1984 Identification ofEoreuma loftini (Dyar) (Lepidoptera: Pyralidae) in Texas, 1980: forerunner for other sugarcane boring pest immigrants from Mexico?Bulletin of the Entomological Society of America 30 47 52 1046-2821 - 67.
Johnson K. J. R. 1985 Seasonal occurrence and insecticidal suppression ofEoreuma loftini (Lepidoptera: Pyralidae) in sugarcane.Journal of Economic Entomology 78 960 966 0022-0493 - 68.
Johnson K. J. R. Van Leerdam M. B. 1981 Range extension ofAcigona loftini into the Lower Rio Grande Valley of Texas.Sugar y Azucar 76: 119,0039-4742 - 69.
Jones C. G. 1991 Plant stress and insect herbivory: toward an integrated perspective. InResponses of Plants to Multiple Stresses , Mooney, H.A.: Winner, W.E. & Pell, E.J. (eds.),249 280 Academic Press,978-0-12505-355-6 New York, New York, USA. - 70.
Jordan W. R. Ritchie J. T. 1971 Influence of soil water stress on evaporation, root absorption, and internal water status of cotton.Plant Physiology 48 783 788 0981-9428 - 71.
Kameli A. Lösel D. M. 1996 Growth and sugar accumulation in durum wheat plants under water stress. New Phytology132 57 62 1469-8137 - 72.
Kennedy J. S. Mittler T. E. 1953 A method for obtaining phloem sap via the mouth-parts of aphids. Nature 171: 528,0028-0836 - 73.
Kennedy J. S. Booth C. O. 1959 Responses ofAphis fabae Scop. To water shortage in host plants in the field.Entomologia Experimentalis et Applicata 2 1 11 0013-8703 - 74.
Kennedy J. S. Lamb K. P. Booth C. O. 1958 Responses of Aphis fabae Scop. To water shortage in host plants in pots. Entomologia Experimentalis et Applicata1 274 290 0013-8703 - 75.
Kimmerer T. W. Kozlowski T. T. 1982 Ethylene, ethane, acetaldehyde, and ethanol production by plants under stress.Plant Physiology 69 840 847 0981-9428 - 76.
Klubertanz T. H. Pedigo L. P. Carlson R. E. 1990 Effects of plant moisture stress and rainfall on population dynamics of the twospotted spider mite (Acari: Tetranychidae).Environmental Entomology 19 1773 1779 0004-6225 X. - 77.
Knight H. Knight M. R. 2001 Abiotic stress signaling pathways: specificity and cross-talk. Trends in Plant Science6 262 267 1360-1385 - 78.
Komazaki S. 1982 Effects of constant temperature on population growth of three aphid species,Toxoptera citricidies (Kirkaldy),Aphis citricola van der Goot, andAphis gossypii Glover (Homoptera: Aphididae) on citrus.Applied Entomology and Zoology 17 75 81 0134-7605 X. - 79.
Krokos F. D. Konstantopoulou M. A. Mazomenos B. E. 2002 Chemical characterization of corn plant compounds by different extraction techniques and the role of potent chemicals in the reproductive behavior of the corn stalk borer,Sesamia nonagrioides .International Organization for Biological Control West Palearctic Region Section Bulletin 25 1 9 1049-9694 - 80.
Labanauskas C. K. Stolzy L. H. Handy M. F. 1981 Protein and free amino acids in field-grown cowpea seeds as affected by water stress at various growth stages.Plant and Soil 63 355 368 0003-2079 X. - 81.
Legaspi J. C. Legaspi B. C. Jr Irvine J. E. Saldana R. R. 1997 Mexican rice borer,Eoreuma loftini (Lepidoptera: Pyralidae) in the Lower Rio Grande Valley of Texas: its history and control.Subtropical Plant Science 49 53 64 1009-7791 - 82.
Legaspi J. C. Legaspi B. C. Jr Irvine J. E. Meagher R. L. Jr Rozeff N. 1999 Stalkborer damage on yield and quality of sugarcane in the Lower Rio Grande Valley of Texas.Journal of Economic Entomology 92 228 234 0022-0493 - 83.
Levitt J. 1951 Frost, drought and heat resistance.Annual Review of Plant Physiology 2 245 268 0079-9920 - 84.
Lofgren C. S. 1986 History of imported fire ants in the United States. InFire Ants and Leaf-cutting Ants: Biology and Management, Lofgren, C.S. (ed.),36 47 Westview Press,10 Boulder, Colorado, USA. - 85.
Lombardero M. J. Ayres M. P. Lorio P. L. Jr Ruel J. J. 2000 Environmental effects on constitutive and inducible resin defences ofPinus taeda .Ecology Letters 3 329 339 1461-0248 - 86.
Lorio P. L. 1986 Growth-differentiation balance: a basis for understanding southern pine beetle-tree interactions.Forest Ecology and Management 14 259 273 - 87.
Lorio P. L. Jr Stephen F. M. Paine T. D. 1995 Environment and ontogeny modify loblolly pine response to induced acute water deficits and bark beetle attack.Forest Ecology and Management 73 97 110 - 88.
Magyarosy A. C. Mittler T. E. 1987 Aphid feeding rates on healthy and beet curly top virus-infected plants.Phytoparasitica 15 335 338 0334-2123 - 89.
Maltais J. B. 1962 A simple apparatus for feeding aphids aseptically on chemically defined diets.Canadian Entomologist 84 291 294 0000-8347 X. - 90.
Massacci A. Battistelli A. Loreto F. 1996 Effect of drought stress on photosynthetic characteristics, growth and sugar accumulation of field-frown sweet sorghum. Australian Journal of Plant Physiology23 331 340 0320-7844 - 91.
Mattson W. J. J. 1980 Herbivory in relation to plant nitrogen content.Annual Review of Ecology and Systematics 11 119 161 0066-4162 - 92.
Mattson W. J. Haack R. A. 1987 The role of drought in outbreaks of plant-eating insects.Bioscience 37 110 118 0006-3568 - 93.
Mc Murtry J. A. 1962 Resistance of alfalfa to spotted alfalfa aphid in relation to environmental factors.Hilgardia 32 501 539 0073-2230 - 94.
Meagher R. L. Jr Pfannenstiel R. S. Saldana R. R. 1993 Survey and estimated injury of the Mexican rice borer in Texas sugarcane. Journal of American Sugar Cane Technologists13 22 26 0003-1216 - 95.
Meagher R. L. Jr Smith J. W. Jr Johnson K. J. R. 1994 Insecticidal management ofEoreuma loftini (Lepidoptera: Pyralidae) on Texas sugarcane: a critical review.Journal of Economic Entomology 87 1332 1344 0022-0493 - 96.
Michels G. J. Jr Undersander D. J. 1986 Temporal and spatial distribution of the greenbug (Homoptera: Aphididae) on sorghum in relation to water stress.Journal of Economic Entomology 79 1221 1225 0022-0493 - 97.
Miller J. R. Strickler K. L. 1984 Finding and accepting host plants. InChemical Ecology of Insects , Bell, W. (ed.),127 157 Sinauer,0-87893-070-1 Massachusetts, USA. - 98.
Mohammadkhani N. Heidari R. 2008 Drought-induced accumulation of soluble sugars and proline in two maize varieties.World Applied Sciences Journal 3 448 453 1818-4952 - 99.
Moran P. J. Showler A. T. 2005 Plant responses to water deficit and shade stresses in pigweed and their influence on feeding and oviposition by the beet armyworm (Lepidoptera: Noctuidae). Environmental Entomology34 929 937 0004-6225 X. - 100.
Morrill A. W. 1925 Commercial entomology on the west coast of Mexico.Journal of Economic Entomology 18 707 716 0022-0493 - 101.
Moyal P. 1995 Borer infestation and damage in relation to the maize stand density and water stress in the Ivory Coast.International Journal of Pest Management 41 114 121 0967-0874 - 102.
Muquing R. . Ku-Rai C. 1998 Osmotic adjustment in leaves of sugarcane in response to water stress. Sugar Cane5 3 7 0378-3774 - 103.
Nation J. L. 2002 Insect Physiology and Biochemistry. CRC Press,101420061771 Raton, Florida, USA. - 104.
Nguyen T. T. A. Michaud D. Cloutier C. 2007 Proteomic profiling of aphidMacrosiphum euphorbiae responses to host-plant-mediated stress induced by defoliation and water deficit.Journal of Insect Physiology 53 601 611 0022-1910 - 105.
Ormeño E. Mévy J. P. Vila B. Bousquet-Mélou A. Greff S. Bonin G. Fernandez C. 2007 Water deficit stress induces different monoterpene and sesquiterpene emission changes in Mediterranean species. Relationship between terpene emissions and plant water potential.Chemosphere 67 276 284 0045-6535 - 106.
Osborn H. T. Phillips G. R. 1946 Chilo loftini in California, Arizona, and Mexico.Journal of Economic Entomology 39 755 759 0022-0493 - 107.
Otter C. J. den 1992 Responses of the African armyworm and three species of borers to carbohydrates and phenolic substances: an electro- and behavioral physiological study.Entomologia Experimentalis et Applicata 63 27 37 0013-8703 - 108.
Popov C. Trotus E. Vasilescu S. Barbulescu A. Rasnoveanu L. 2006 Drought effect on pest attack in field crops.Romanian Agricultural Research 23 43 52 1222-4227 - 109.
Price J. T. 2002 Climate change, birds, and ecosystems- why should we care? InManaging for Healthy Ecosystems, Rapport, D.J.; Lasley, C.L.; Rolston, D.E.; Nielson, N.O.; Qualset, C.O. & Damania, A.B. (eds.),60 61 CRC Press,978-1-42003-213-0 Boca Raton, Florida, USA. - 110.
Ramanulu S. Kaiser W. Deitz K. J. 1999 Salt and drought stress differentially affect the accumulation of extracellular proteins in barley.Journal of Bioscience 54 337 347 - 111.
Ramaswamy S. B. 1988 Host finding by moths: sensory modalities and behaviors.Journal of Insect Physiology 34 235 249 0022-1910 - 112.
Ramos P. Rosales R. Sabouni I. Garrido D. Ramos J. M. 2008 Crop losses due to olive moth mediated by ethylene.Pest Management Science 64 720 724 1526-4998 - 113.
Reay-Jones F. P. F. Way M. O. Setamou M. Legendre B. L. Reagan T. E. 2003 Resistance to the Mexican rice borer (Lepidoptera: Crambidae) among Louisiana and Texas sugarcane cultivars.Journal of Economic Entomology 96 1929 1934 0022-0493 - 114.
Reay-Jones F. P. F. Showler A. T. Reagan T. E. Legendre B. L. Way M. O. Moser E. B. 2005 Integrated tactics for managing the Mexican rice borer (Lepidopotera: Crambidae) in sugarcane.Environmental Entomology 34 1558 1565 0004-6225 X.. - 115.
Reay-Jones F. P. F. Wilson L. T. Showler A. T. Reagan T. E. Way M. O. 2007 Role of oviposition on preference in an invasive crambid impacting two graminaceous host crops.Environmental Entomology 36 938 951 0004-6225 X. - 116.
Reay-Jones F. P. F. Wilson L. T. Reagan T. E. Legendre B. L. Way M. O. 2008 Predicting economic losses from the continued spread of the Mexican rice borer (Lepidoptera: Crambidae).Journal of Economic Entomology 101 237 250 0022-0493 - 117.
Renwicke J. A. A. Radke C. D. 1988 Sensory cues in host selection for oviposition by the cabbage butterfly,Pieris rapae .Journal of Insect Physiology 34 251 257 0022-1910 - 118.
Renwicke J. A. A. Chew F. S. 1994 Oviposition behavior in Lepidoptera.Annual Review of Entomology 39 377 400 0066-4170 - 119.
Salama H. S. Rizk A. F. Sharaby A. 1984 Chemical stimuli in flowers and leaves of cotton that affect behavior in the cotton moth,Spodoptera littoralis (Lepidoptera: Noctuidae).Entomologia 10 27 34 - 120.
Schoonhoven L. M. 1981 Chemical mediators between plants and phytophagous insects. InSemiochemicals: Their Role in Pest Control, Nordland, D.A.; Jones, R.L. & Lewis, W.L. (eds.),31 50 John Wiley & Sons,100471058033 York, New York, USA. - 121.
Schubert S. Serraj R. Plies-Balzer E. Mengel K. 1995 Effect of drought stress on growth, sugar concentrations and amino acid accumulations in N 2 -fixing alfalfa (Medicago sativa ).Plant Physiology 146 541 546 0981-9494 - 122.
Schur K. Holdaway F. G. 1970 Olfactory responses of femaleOstrinia nubilalis (Lepidoptera: Pyraustinae).Entomologia Experimentalis et Applicata 13 455 461 0013-8703 - 123.
Scriber J. M. 1977 Limiting effects of low leaf-water content on the nitrogen utilization, energy budget, and larval growth ofHylophora cecropia .Oecologia 28 269 287 0029-8549 - 124.
Seki M. Narusaka M. Abe H. Ksuga K. Yamaguchi-Shinozaki K. Carninci P. Hayashizaki P. Shinozaki K. 2001 Monitoring the expression pattern of 1300Arabidopsis genes under drought and cold stress by using a full-length cDNA microarray.Plant Cell Environment 13 61 72 1365-3040 - 125.
Sharpe P. J. H. Wu H. I. Cates R. G. Goeschl J. D. 1985 Energetics of pine defense systems to bark beetle attack.,206 223 InIntegrated Pest Management Research Symposium: the Proceedings , Branham, S.J. & Thatcher, R.C. (eds.), pp. 206-223. United States Department of Agriculture Forest Service General Technical Report SO-S6, Washington, DC, USA. - 126.
Showler A. T. Knaus R. M. Reagan T. E. 1989 Foraging territoriality of the imported fire ant,Solenopsis invicta Buren, in sugarcane as determined by neutron activation analysis.Insectes Sociaux 36 235 239 0020-1812 - 127.
Showler A. T. Reagan T. E. 1991 Effects of sugarcane borer, weed, and nematode cottrol strategies in Louisiana sugarcane.Environmental Entomology 20 358 370 0004-6225 X. - 128.
Showler A. T. Greenberg S. M. 2003 Effects of weeds on selected arthropod herbivore and natural enemy populations, and on cotton growth and yield. Environmental Entomology32 39 50 0004-6225 X. - 129.
Showler A. T. Moran P. J. 2003 Effects of drought stressed cotton, Gossypium hirsutum L., on beet armyworm, Spodoptera exigua (Hübner), oviposition, and larval feeding preferences and growth. Journal of Chemical Ecology95 1971 1985 0098-0331 - 130.
Showler A. T. Cavazos C. O. Moran P. J. 2007 Dynamics of free amino acid accumulations in cotton leaves measured on different timelines after irrigation. Subtropical Plant Science59 38 55 1009-7791 - 131.
Showler A. T. Castro B. A. 2010a Influence of drought stress on Mexican rice borer (Lepidoptera: Crambidae) oviposition preference in sugarcane. Crop Protection28 722 727 0261-2194 - 132.
Showler A. T. Castro B. A. 2010b Mexican rice borer (Lepidoptera: Crambidae) oviposition site selection stimuli on sugarcane, and potential field applications.Journal of Economic Entomology 103 1180 1186 0022-0493 - 133.
Showler A. T. Beuzelin J. M. Reagan T. E. 2011 Alternate crop and weed host plant oviposition preferences by the Mexican rice borer (Lepidoptera: Crambidae).Crop Protection 30 895 901 0261-2194 - 134.
Showler A. T. 2012 Drought and arthropod pests of crops. InDrought: New Research , Neves, D.F & Sanz, J.D. (eds.),131 154 Nova Science,978-1-62100-769-2 Hauppauge, New York, USA. - 135.
Showler A. T. Reagan T. E. 2012 Ecology and tactics for control of three sugarcane stalkboring species in the Western Hemisphere and Africa. InSugarcane: Production, Cultivation and Uses , Goncalves, J.F. & Correia, K.D. (eds.),1 32 Nova Science,978-1-61942-213-1 Hauppauge, New York, USA. - 136.
Sidhu H. S. Kaur P. 1976 The influence of water stress in the host plant on the reproduction of the mustard aphid,Lipaphis erysimi (Kalt.)Indian Journal of Ecology 3 163 166 0304-5250 - 137.
Smitley D. R. Peterson N. C. 1996 Interactions of water stress, honeylocust spider mites (Acari: Tetranychidae), early leaf abscission, and growth ofGleditsia tnacanthos .Journal of Economic Entomology 89 1577 1581 0022-0493 - 138.
Städler E. 1984 Contact chemoreception. InChemical Ecology of Insects , Bell, W.J. & Carde, R.T. (eds.),3 35 Sinauer, Sunderland, Massachusetts, USA. - 139.
Stotz H. U. Pittendrigh B. R. Kroyman J. Weniger K. Fritsche J. Bauke A. Mitchell-Olds T. 2000 Induced plant defense responses against chewing insects. Ethylene signaling reduces resistance of Arabidopsis against Egyptian cotton worm but not diamondback moth. Plant Physiology124 1007 1018 0981-9428 - 140.
Sturm M. M. Sterling W. L. 1990 Geographical patterns of boll weevil mortality: observations and hypotheses.Environmental Entomology 19 59 65 0004-6225 X. - 141.
Sumner L. C. Need J. T. Mc New R. W. Dorschner K. W. Elkenbary R. D. Johnson R. C. 1983 Response ofSchizaphis graminum (Homoptera: Aphididae) to drought-stressed wheat, using polyethylene glycol as ammatricum.Environmental Entomology 12 919 922 0004-6225 X. - 142.
Udayagiri S. Mason C. E. 1995 Host plant constituents as oviposition stimulants for a generalist herbivore: European corn borer.Entomologia Experimentalis et Applicata 76 59 65 0013-8703 - 143.
Van Leerdam M. B. Johnson K. J. R. Smith J. W. Jr 1984 Effects of substrate physical characteristics and orientation on oviposition byEoreuma loftini (Lepidoptera: Pyralidae).Environmental Entomology 13 800 802 0004-6225 X. - 144.
Van Leerdam M. B. Johnson K. J. R. Smith J. W. Jr 1986 Ovipositional sites ofEoreuma loftini (Lepidoptera: Pyralidae) in sugarcane.Environmental Entomology 15 75 78 0004-6225 X. - 145.
Van Zwaluenberg R. H. 1926 Insect enemies of sugarcane in western Mexico.Journal of Economic Entomology 19 664 669 0022-0493 - 146.
Vanderzant E. S. 1958 The amino acid requirements of the pink bollworm.Journal of Economic Entomology 51 309 311 0022-0493 - 147.
Vincent D. Lapierre C. Pollet B. Cornic G. Negroni L. Zivy M. 2005 Water deficits affect caffeateO -methyltransferase, lignifications, and related enzymes in maize leaves. A proteomic investigation.Plant Physiology 137 949 960 - 148.
Vité J. P. Volz H. A. Paiva M. R. Bakke A. 1986 Semiochemicals in host selection and colonization of pine trees by the pine shoot beetleTomicus piniperda .Naturwissenschaften 73 39 40 0028-1042 - 149.
Waladde S. M. 1983 Chemoreceptors of adult stem borers: tarsal and ovipositor sensilla onChilo partellus andEldana saccharina .Insect Science and its Applications 4 159 165 0191-9040 - 150.
Wearing C. H. Van Emden H. F. 1967 Studies on the relations of insect and host plant. I. Effects of water stress in host plants on infestations byAphis fabae Scop.,Myzus persicae (Sulz.) andBrevicoryne brassicae (L.).Nature 213 1051 1052 0028-0836 - 151.
Weibull J. 1987 Seasonal changes in the free amino acids of oat and barley phloem sap in relation to plant growth stage and growth of Rhopalosiphum padi. Annals of Applied Biology111 727 737 1744-7348 - 152.
White T. C. R. 1984 The abundance of invertebrate herbivores in relation to the availability of nitrogen in stressed food plants. Oecologia63 90 105 0029-8549 - 153.
Wilson B. 2011 Advanced management of the Mexican rice borer (Eoreuma loftini ) in sugarcane. M.S. thesis, Louisiana State University, Baton Rouge, Louisiana, USA. - 154.
Wright L. C. Berryman A. A. Gurusiddaiah S. 1979 Host resistance to the fir engraver beetle,Scolytus ventralis (Coleoptera: Scolytidae). IV. Effe cts of defoliation on wound monoterpene and inner bark carbohydrate concentrations.Canadian Entomologist 111 1255 1262 0000-8347 X. - 155.
Zalucki M. P. Clarke A. R. Malcom S. B. 2002 Ecology and behavior of first instar larval Lepidoptera. Annual Review of Entomology47 361 393 0066-4170 - 156.
Zhang J. X. Kirkham M. B. 1990 Variation in ethylene production by sorghum.Euphytica 46 109 117 0014-2336 - 157.
Zhu J. K. 2002 Salt and drought stress signal transduction in plants.Annual Review of Plant Biology 53 247 273 1543-5008