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Spatio-Temporal, Genotypic, and Environmental Effects on Plant Soluble Protein and Digestible Carbohydrate Content: Implications for Insect Herbivores with Cotton as an Exemplar

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Abstract

Plant soluble protein and digestible carbohydrate content significantly affect insect herbivore fitness, but studies reporting plant protein and carbohydrate content are rare. Instead, the elements nitrogen and carbon often are used as surrogates for plant protein and digestible carbohydrate content, respectively. However, this is problematic for two reasons. First, carbon is found in all organic molecules, which precludes strong correlations with ecologically important dietary macronutrients (e.g., digestible carbohydrates, the primary energy source for most insect herbivores). Second, some elements (e.g., nitrogen) are present in both macronutrients (e.g., protein) and non-nutritive secondary compounds (e.g., alkaloids, protease inhibitors); in these cases N values would greatly overestimate protein available for an insect herbivore. Thus, the objective of this study was to explicitly document plant protein-carbohydrate content and assess its variation in cotton (Gossypium hirsutum and G. barbadense), which is a nutritional resource for a number of insect herbivores. We did this by measuring plant soluble protein (P) and digestible carbohydrate (C) content across seven plant tissues, five varieties, and two growing environments. Significant differences in P and C concentration, total macronutrient content (P + C), and P:C ratio were observed across plant tissues, plant age and environment; smaller differences were seen across plant genotype. Foliar tissues had higher total P + C content compared to reproductive tissues, except for developing seeds and developing flowers, which contained twice the total P + C content; these two tissues also had the highest P content. Our data show that even agricultural monocultures offer a highly heterogeneous protein-carbohydrate landscape for insect herbivores. Characterizing plant resources using nutritional currencies (e.g., protein and carbohydrates) that are ecologically and physiologically-relevant to insect herbivores can be used to enhance our understanding of plant-insect interactions.

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References

  • Auclair JL (1969) Nutrition of plant-sucking insects on chemically defined diets. Entomol Exp Appl 12:623–641

    Article  Google Scholar 

  • Backus EA, Cline AR, Ellerseick MR, Serrano MS (2007) Lygus hesperus (Hemiptera: Miridae) feeding on cotton: new methods and parameters for analysis of nonsequential electrical penetration graph data. Ann Entomol Soc Am 100:296–310

    Article  Google Scholar 

  • Bardgett RD, Chan KF (1999) Experimental evidence that soil fauna enhance nutrient mineralization and plant nutrient uptake in montane grassland ecosystems. Soil Biol Biochem 31:1007–1014

    Article  CAS  Google Scholar 

  • Behmer ST (2009) Insect herbivore nutrient regulation. Annu Rev Entomol 54:167–187

    Article  Google Scholar 

  • Behmer ST, Joern A (2008) Coexisting generalist herbivores occupy unique nutritional feeding niches. Proc Natl Acad Sci U S A 105:1977–1982

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Behmer ST, Raubenheimer D, Simpson SJ (2001) Frequency-dependent food selection in locusts: a geometric analysis of the role of nutrient balancing. Anim Behav 61:995–1005

    Article  Google Scholar 

  • Behmer ST, Simpson SJ, Raubenheimer D (2002) Herbivore foraging in chemically heterogeneous environments: nutrients and secondary metabolites. Ecology 83:2489–2501

    Article  Google Scholar 

  • Bernays EA (1998) Evolution of feeding behavior in insect herbivores. Bioscience 48:35–44

    Article  Google Scholar 

  • Bernays EA, Chapman RF (1994) Host-plant selection by phytophagous insects. Chapman & Hall, NY

    Book  Google Scholar 

  • Bernays EA, Singer MS, Rodrigues D (2004) Foraging in nature: foraging efficiency and attentiveness in caterpillars with different diet breadths. Ecol Entomol 29:389–397

    Article  Google Scholar 

  • Biswas JC, Ladha JK, Dazzo FB (2000) Rhizobia inoculation improves nutrient uptake and growth of lowland rice. Soil Sci Soc Am J 64:1644–1650

    Article  CAS  Google Scholar 

  • Boisen S, Bech-Andersen S, Eggum BO (1987) A critical view of the conversion factor 6.25 from total nitrogen to protein. Acta Agric Scand 37:299–304

    Article  CAS  Google Scholar 

  • Bottrell DG, Adkisson PL (1977) Cotton insect pest management. Annu Rev Entomol 22:451–481

    Article  Google Scholar 

  • Boyd ML, Phipps BJ, Wrather JA, Newman M, Sciumbato GL (2004) Cotton pests: Scouting and management. Extension publications, University of Missouri

    Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Bunce JA (1977) Leaf elongation in relation to leaf water potential in soybean. J Exp Bot 28:156–161

    Article  Google Scholar 

  • Clissold FJ, Sanson GD, Read J (2006) The paradoxical effects of nutrient ratios and supply rates on an outbreaking insect herbivore, the Australian plague locust. J Anim Ecol 75:1000–1013

    Article  CAS  PubMed  Google Scholar 

  • Clissold FJ, Sanson GD, Read J, Simpson SJ (2009) Gross vs. net income: how plant toughness affects performance of an insect herbivore. Ecology 90:3393–3405

    Article  PubMed  Google Scholar 

  • Compton SJ, Jones CG (1985) Mechanism of dye response and interference in the Bradford protein assay. Anal Biochem 151:369–374

    Article  CAS  PubMed  Google Scholar 

  • Cotter SC, Simpson SJ, Raubenheimer D, Wilson K (2010) Macronutrient balance mediates trade-offs between immune function and life history traits. Funct Ecol 25:186–198

    Article  Google Scholar 

  • do Amarante L, Lima JD, Sodek L (2006) Growth and stress conditions cause similar changes in xylem amino acids for different legume species. Env. Exp Biol 58:123–129

    Google Scholar 

  • Davies WJ (1977) Stomatal responses to water stress and light in plants grown in controlled environments and in the field. Crop Sci 17:735–740

    Article  Google Scholar 

  • Deans CA, Sword GA, Behmer ST (2015) Revisiting macronutrient regulation in the polyphagous herbivore Helicoverpa zea (Lepidoptera: Noctuidae): new insights via a nutritional geometry. J Insect Physiol 81:21–27

    Article  CAS  PubMed  Google Scholar 

  • Deans CA, Sword GA, Behmer ST (2016) Nutrition as a neglected factor in insect herbivore susceptibility to Bt toxins. Curr Opin Insect Sci 15:97–103

    Article  CAS  PubMed  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colormetric method for determination of sugars and related substances. Anal Chem 28:350–358

    Article  CAS  Google Scholar 

  • Egamberdiyeva D (2007) The effect of plant growth promoting bacteria on growth and nutrient uptake of maize in two different soils. Appl Soil Ecol 36:184–189

    Article  Google Scholar 

  • Egamberdiyeva D, Höflich G (2004) Effect of plant growth-promoting bacteria on growth and uptake of cotton and pea in a semi-arid region of Uzbekistan. J Arid Environ 56:293–301

    Article  Google Scholar 

  • Ezeagu IE, Petzke JK, Metges CC, Akinsoyinu AO, Ologhobo AD (2002) Seed protein contents and nitrogen-to-protein conversion factors for some uncultizated tropical plant seeds. Food Chem 78:105–109

    Article  CAS  Google Scholar 

  • Fitt GP (1989) The ecology of Heliothis Species in relation to agroecosystems. Annu Rev Entomol 34(1):17–53

  • Grassi G, Millard P, Wendler R, Minotta G, Tagliavini M (2002) Measurement of xylem sap amino acid concentrations in conjunction with whole tree transpiration estimates spring N remobilization by cherry (Prunus avium L.) trees. Plant Cell Environ 25:1689–1699

    Article  CAS  Google Scholar 

  • Hedin PA, Parrott WL, Jenkins JN (1991) Effects of cotton plant allelochemicals and nutrients on behavior and developments of tobacco budworm. J Chem Ecol 17:1171–1121

    Article  Google Scholar 

  • Hill DS (1987) Agricultural insect pests of temperate regions and their control. Cambridge University Press, UK

    Google Scholar 

  • Hunt ER, Jaffe MJ (1980) Thigmomorphogenesis: The interaction of wind and temperature in the field on the growth of Phaseolus vulgaris L. Ann Bot-London 45:665–672

    Google Scholar 

  • Hwang BK, Ibenthal WD, Heitefuss R (1983) Age, rate of growth, carbohydrate and amino acid contents of spring barley plants in relation to their resistance to powdery mildew (Erysiphe graminis f.Sp. hordei. Physiol Plant Pathol 22:1–14

    Article  CAS  Google Scholar 

  • Izhaki I (1993) Influence of nonprotein nitrogen on estimation of protein from total nitrogen in fleshy fruits. J Chem Ecol 19:2605–2615

    Article  CAS  PubMed  Google Scholar 

  • Jermy T (1984) Evolution of insect/host plant relationships. Am Nat 124

  • Joern A, Provin T, Behmer ST (2012) Not just the usual suspects: insect herbivore populations and communities are associated with multiple plant nutrients. Ecology 93:1002–1015

    Article  PubMed  Google Scholar 

  • Karley AJ, Douglas AE, Parker WE (2002) Amino acid composition and nutritional quality of potato leaf phloem sap for aphids. J Exp Biol 205:3009–3018

    CAS  PubMed  Google Scholar 

  • Layton MB (2000) Biology and damage of the tarnished plant bug, Lygus lineolaris. cotton Southwest Entomol 23:7–20

    Google Scholar 

  • Le Gall M, Behmer ST (2014) Effects of protein and carbohydrate on an insect herbivore: the vista from a fitness landscape. Integr Comp Biol 54:942–954

    Article  PubMed  Google Scholar 

  • Lee KP, Behmer ST, Simpson SJ, Raubenheimer D (2002) A geometric analysis of nutrient regulation in the generalist caterpillar Spodoptera littoralis (Boisduval. J Insect Physiol 48:655–665

    Article  CAS  PubMed  Google Scholar 

  • Lee KP, Cory JS, Wilson K, Raubenheimer D, Simpson SJ (2006) Flexible diet choice offsets protein costs of pathogen resistance in a caterpillar. Proc Roy Soc Lond B Bio 273:823–829

    Article  CAS  Google Scholar 

  • Lee KP, Simpson SJ, Wilson K (2008) Dietary protein-quality influences melanization and immune function in an insect. Funct Ecol 22:1052–1061

    Article  Google Scholar 

  • Lenhart PA, Eubanks MD, Behmer ST (2015) Water stress in grasslands: dynamic responses of plants and insect herbivores. Oikos 124:381–390

    Article  Google Scholar 

  • Li R, Volenec JJ, Joern BC, Cunningham SM (1996) Seasonal changes in nonstructural carbohydrates, protein, and macronutrients in roots of alfalfa, red clover, sweetclover, and birdsfoot trefoil. Crop Sci 36:617–623

    Article  CAS  Google Scholar 

  • Machado AR, Arce CCM, Ferrieri AP, Baldwin IT, Erb M (2015) Jasmonate-dependent depletion of soluble sugars compromises plant resistance to Manduca sexta. New Phytol 207:91–105

    Article  CAS  PubMed  Google Scholar 

  • Matthews GA (1989) Cotton insect pests and their management. Longman Scientific and Technical, UK

    Google Scholar 

  • Mossé J (1990) Nitrogen to protein conversion factor for ten cereals and six legume or oilseeds. A reappraisal of its definition and determination. Variation according to species and to seed protein content. J Agric Food Chem 38:18–24

    Article  Google Scholar 

  • Ponder KL, Pritchard J, Harrington R, Bale JS (2000) Difficulties in location and acceptance of phloem sap combined with reduced concentration of phloem amino acids explain lowered performance of the aphid Rhopalosiphum padi on nitrogen deficient barely (Hordeum vulgare) seedlins. Entomol Exp Appl 97:203–210

    Article  Google Scholar 

  • Ponton F, Wilson K, Holmes AJ, Cotter SC, Raubenheimer D, Simpson SJ (2013) Integrating nutrition and immunology: a new frontier. J Insect Physiol 59:130–137

    Article  CAS  PubMed  Google Scholar 

  • Povey S, Cotter SC, Simpson SJ, Lee KP, Wilson K (2008) Can the protein costs of bacterial resistance be offset by altered feeding behavior? J Anim Ecol 78:437–446

    Article  PubMed  Google Scholar 

  • Preece JE, Sutter EG (1991) Acclimatization of micropropagated plants to the greenhouse and field. In: Debergh P, Zimmerman RH (eds) Micropropagation. Springer, The Netherlands, pp. 71–93

    Chapter  Google Scholar 

  • Quaintance AL, Brues CT (1905) The cotton bollworm: Bureau of entomology bulletin (No. 50). U.S. Department of Agriculture, Washington

    Book  Google Scholar 

  • Raubenheimer D (1992) Tannic acid, protein, and digestible carbohydrate: dietary imbalance and nutritional compensation in locusts. Ecology 73:1012–1027

    Article  CAS  Google Scholar 

  • Raubenheimer D, Simpson SJ (1997) Integrative models of nutrient balancing: application to insects and vertebrates. Nutr Res 10:151–179

    Article  CAS  Google Scholar 

  • Roeder KA, Behmer ST (2014) Lifetime consequences of food protein-carbohydrate content for an insect herbivore. Funct Ecol 28:1135–1143

    Article  Google Scholar 

  • Sánchez E, Rivero RM, Ruiz JM, Romero L (2004) Changes in biomass, enzymatic activity and protein concentration in roots and leaves of green bean plants (Phaseolus vulgaris L. cv. Strike) under high NH4NO3 application rates. Sci Hortic-Amsterdam 99:237–248

    Article  Google Scholar 

  • Showler AT, Moran PJ (2003) Effects of drought stressed cotton, Gossypium hirsutum L., on beet armyworm, Spodoptera exigua (Hübner), oviposition, and larval feeding preferences and growth. J Chem Ecol 29:1997–2011

    Article  CAS  PubMed  Google Scholar 

  • Simpson SJ, Raubenheimer D (1993) A multi-level analysis of feeding behaviour: The geometry of nutritional decisions. Philos T Roy Soc B 342:381–402

    Article  Google Scholar 

  • Simpson SJ, Raubenheimer D (1995) The geometric analysis of feeding and nutrition: a user’s guide. J Insect Physiol 41:545–553

    Article  CAS  Google Scholar 

  • Simpson SJ, Raubenheimer D (2001) The geometric analysis of nutrient-allelochemical interactions: a case study using locusts. Ecology 82:422–439

    Google Scholar 

  • Simpson SJ, Raubenheimer D (2012) The nature of nutrition: a unifying framework from animal adaptation to human obesity. Princeton University Press, Princeton, NJ

  • Simpson SJ, Raubenheimer D, Behmer ST, Whitworth A, Wright GA (2002) A comparison of nutritional regulation in solitarious- and gregarious-phase nymphs of the desert locust Schistocerca gregaria. J Exp Biol 205:121–129

    CAS  PubMed  Google Scholar 

  • Simpson SJ, Sibly RM, Lee KP, Behmer ST, Raubenheimer D (2004) Optimal foraging when regulating intake of multiple nutrients. Anim Behav 68:1299–1311

    Article  Google Scholar 

  • Simpson SJ, Sword GA, Lorch PD, Couzin ID (2006) Cannibal crickets on a forced march for protein and salt. Proc Natl Acad Sci U S A 103:4152–4156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singer M, Stireman J (2001) How foraging tactics determine host-plant use by a polyphagous caterpillar. Oecologia 129:98–105

    Article  Google Scholar 

  • Singer MS, Bernays EA, Carriere Y (2002) The interplay between nutrient balancing and toxin dilution in foraging by a generalist insect herbivore. Anim Behav 64:629–643

    Article  Google Scholar 

  • Snodgrass GL (1998) Distribution of the tarnished plant bug (Heteroptera: Miridae) within cotton plants. Environ Entomol 27:1089–1093

    Article  Google Scholar 

  • Stieger PA, Feller U (1994) Senescence and protein remobilization in leaves of maturing wheat plants grown on waterlogged soil. Plant Soil 166:173–179

    Article  CAS  Google Scholar 

  • Warbrick-Smith J, Behmer ST, Lee KP, Raubenheimer D, Simpson SJ (2006) Evolving resistance to obesity in an insect. Proc Natl Acad Sci U S A 103:14045–14049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Warbrick-Smith J, Raubenheimer D, Simpson SJ, Behmer ST (2009) Three hundred and fifty generations of extreme food specialization: testing predictions of nutritional ecology. Entomol Exp Appl 132:65–75

    Article  Google Scholar 

  • Wilkinson TL, Douglas AE (2003) Phloem amino acids and the host plant range of the polyphagous aphid, Aphis fabae. Entomol Exp Appl 106:103–113

    Article  CAS  Google Scholar 

  • Wilson LT, Waite GK (1982) Feeding pattern of Australian Heliothis on cotton. Environ Entomol 11(2):297–300

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Acknowledgments

We thank all who have contributed to this project, either through assistance with field collection, chemical analyses, or general feedback, including: Paul Lenhart, Marion Le Gall, Rebecca Clark, Fiona Clissold, Mickey Eubanks, Cesar Valencia, Lauren Kalns, Diana Castillo-Lopez, Maria Julissa Ek-Ramos, Nicole Locke, and Steve Hague. Charlie Cook from All-Tex Seed Inc. provided seed for use in these experiments. Aspects of this study were supported by the Biotechnology Risk Assessment Grants (BRAG) program from the U.S. Department of Agriculture (2015-33522-24099) awarded to GAS and STB, as well as the C. Everette Salyer Fellowship in Cotton Entomology and the Dissertation Fellowship offered by Texas A&M University and awarded to CAD.

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Authors and Affiliations

  1. Department of Entomology, Texas A&M University, TAMU 2475, College Station, TX, 77843, USA

    Carrie A. Deans, Spencer T. Behmer & Gregory A. Sword

  2. Department of Entomology, University of Minnesota, St. Paul, MN, 55108, USA

    Carrie A. Deans

  3. Ecology & Evolutionary Biology Graduate Program, Texas A&M University, College Station, TX, 77843, USA

    Spencer T. Behmer & Gregory A. Sword

  4. Department of Environmental and Forest Biology, SUNY-ESF, 1 Forestry Drive, Syracuse, NY, 13210, USA

    Justin Fiene

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  1. Carrie A. Deans
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Correspondence to Carrie A. Deans.

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Deans, C.A., Behmer, S.T., Fiene, J. et al. Spatio-Temporal, Genotypic, and Environmental Effects on Plant Soluble Protein and Digestible Carbohydrate Content: Implications for Insect Herbivores with Cotton as an Exemplar. J Chem Ecol 42, 1151–1163 (2016). https://doi.org/10.1007/s10886-016-0772-1

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