Abstract
The rapid growth and prolific reproduction of many insect herbivores depend on the efficiencies and rates with which they acquire nutrients from their host plants. However, little is known about how nutrient assimilation efficiencies are affected by leaf maturation or how they vary between plant species. Recent work showed that leaf maturation can greatly decrease the protein assimilation efficiency (PAE) of Lymantria dispar caterpillars on some tree species, but not on species in the willow family (Salicaceae). One trait of many species in the Salicaceae that potentially affects PAE is the continuous (or “indeterminate”) development of leaves throughout the growing season. To improve our understanding of the temporal and developmental patterns of nutrient availability for tree-feeding insects, this study tested two hypotheses: nutrients (protein and carbohydrate) are more efficiently assimilated from immature than mature leaves, and, following leaf maturation, nutrients are more efficiently assimilated from indeterminate than determinate tree species. The nutritional physiology and growth of a generalist caterpillar (L. dispar) were measured on five determinate and five indeterminate tree species while their leaves were immature and again after they were mature. In support of the first hypothesis, caterpillars that fed on immature leaves had significantly higher PAE and carbohydrate assimilation efficiency (CAE), as well as higher protein assimilation rates and growth rates, than larvae that fed on mature leaves. Contrary to the second hypothesis, caterpillars that fed on mature indeterminate tree leaves did not have higher PAE than those that fed on mature determinate leaves, while CAE differed by only 3% between tree development types. Instead, “high-PAE” and “low-PAE” tree species were found across taxonomic and development categories. The results of this study emphasize the importance of physiological mechanisms, such as nutrient assimilation efficiency, to explain the large variation in host plant quality for insect herbivores.
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References
Abrams MD (1998) The red maple paradox. What explains the widespread expansion of red maple in eastern forests? Bioscience 48:355–364
Addy ND (1969) Rearing the forest tent caterpillar on an artificial diet. J Econ Entomol 62:270–271
Awmack CS, Leather SR (2002) Host plant quality and fecundity in herbivorous insects. Annu Rev Entomol 47:817–844
Ayres MP, MacLean SF (1987) Development of birch leaves and the growth energetics of Epirrita autumnata (Geometridae). Ecology 68:558–568
Barbehenn RV, Constabel CP (2011) Tannins in plant–herbivore interactions. Phytochemistry 72:1151–1565
Barbehenn RV, Weir Q, Salminen JP (2008) Oxidation of ingested phenolics in the tree-feeding caterpillar Orgyia leucostigma depends on foliar chemical composition. J Chem Ecol 34:748–756
Barbehenn R, Dukatz C, Holt C, Reese A, Martiskainen O, Salminen J-P (2010) Feeding on poplar leaves by caterpillars potentiates foliar peroxidase action in their guts and increases plant resistance. Oecologia 164:993–1004
Barbehenn RV, Niewiadomski J, Kochmanski J, Constabel CP (2012) Limited effect of reactive oxygen species on the composition of susceptible essential amino acids in the midguts of Lymantria dispar caterpillars. Arch Insect Biochem Physiol 81:160–177
Barbehenn RV, Niewiadomski J, Kochmanski J (2013a) Importance of protein quality versus quantity in alternative host plants for a leaf-feeding insect. Oecologia 173:1–12
Barbehenn RV, Niewiadomski J, Pecci C, Salminen J-P (2013b) Physiological benefits of feeding in the spring by Lymantria dispar caterpillars on red oak and sugar maple leaves: nutrition versus oxidative stress. Chemoecology 23:59–70
Barbehenn RV, Haugberg N, Kochmanski J, Menachem B, Miller C (2014) Physiological factors affecting the rapid decrease in protein assimilation efficiency by a caterpillar on newly-mature tree leaves. Physiol Entomol 39:69–79
Barbehenn RV, Knister J, Marsik F, Jahant-Miller C, Nham W (2015a) Nutrients are assimilated efficiently by Lymantria dispar caterpillars from the mature leaves of trees in the Salicaceae. Physiol Entomol 40:72–81
Barbehenn RV, Haugberg N, Kochmanski J, Menachem B (2015b) Effects of leaf maturity and wind stress on the nutrition of the generalist caterpillar Lymantria dispar feeding on poplar. Physiol Entomol 40:212–222
Barbosa P, Krischik VA (1987) Influence of alkaloids on feeding preference of eastern deciduous forest trees by the gypsy moth Lymantria dispar. Am Nat 130:53–69
Baron-Epel O, Gharyal PK, Schindler M (1988) Pectins as mediators of wall porosity in soybean cells. Planta 175:389–395
Barton KE, Koricheva J (2010) The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis. Am Nat 175:482–493
Behmer ST (2009) Insect herbivore nutrient regulation. Annu Rev Entomol 54:165–187
Bernays E, Graham M (1988) On the evolution of host specificity in phytophagous arthropods. Ecology 69:886–892
Bosch M, Berger S, Schaller A, Stintzi A (2014) Jasmonate-dependent induction of polyphenol oxidase activity in tomato foliage is important for defense against Spodoptera exigua but not against Manduca sexta. BMC Plant Biol 14:257–271
Boudet A-M (2003) Towards an understanding of the supramolecular organization of the lignified cell wall. In: Rose JKC (ed) The plant cell wall. Blackwell, UK, pp 155–182
Brisson LF, Tenhaken R, Lamb C (1994) Function of oxidative cross-linking of cell wall structural proteins in plant disease resistance. Plant Cell 6:1703–1712
Bursell E (1967) The excretion of nitrogen in insects. Adv Insect Physiol 4:33–67
Castro-Diez P, Puyravaud JP, Cornelissen JHC (2000) Leaf structure and anatomy as related to leaf mass per area variation in seedlings of a wide range of woody plant species and types. Oecologia 124:476–486
Choong MR (1996) What makes a leaf tough and how this affects the pattern of Castanopsis fissa leaf consumption by caterpillars. Funct Ecol 10:668–674
Cipollini DF, Bergelson J (2000) Environmental and developmental regulation of trypsin inhibitor activity in Brassica napus. J Chem Ecol 26:1411–1422
Clissold FJ, Tedder BJ, Conigrave AD, Simpson SJ (2010) The gastrointestinal tract as a nutrient-balancing organ. Proc R Soc Lond Biol Sci 277:1751–1759
Coley PD, Bateman ML, Kursar TA (2006) The effects of plant quality on caterpillar growth and defense against natural enemies. Oikos 115:219–228
Constabel CP, Barbehenn R (2008) Defensive roles of polyphenol oxidase in plants. In: Schaller A (ed) Induced plant resistance to herbivory. Springer, New York, pp 253–269
Dale JE (1982) The growth of leaves. Edward Arnold, London
DeGabriel JL, Moore BD, Foley WJ, Johnson CN (2009) The effects of plant defensive chemistry on nutrient availability predict reproductive success in a mammal. Ecology 90:711–719
Despland E, Noseworthy M (2006) How well do specialist feeders regulate nutrient intake? Evidence from a gregarious tree-feeding caterpillar. J Exp Biol 209:1301–1309
Doblin MS, Vergara CE, Read S, Newbigin E, Bacic A (2003) Plant cell wall biosynthesis: making the bricks. In: Rose JKC (ed) The plant cell wall. Blackwell, UK, pp 183–222
Feeny PP (1970) Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars. Ecology 51:565–581
Felton G (1996) Nutritive quality of plant protein: sources of variation and insect herbivore responses. Arch Insect Biochem Physiol 32:107–130
Felton GW (2005) Indigestion is a plant’s best defense. Proc Nat Acad Sci 102:18771–18772
Hanley ME, Lamont BB, Fairbanks MM, Rafferty CM (2007) Plant structural traits and their role in anti-herbivore defence. Persp Plant Ecol Evol Syst 8:157–178
Haruta M, Major IT, Christopher ME, Patton JJ, Constabel CP (2001) A Kunitz trypsin inhibitor gene family from trembling aspen (Populus tremuloides Michx.): cloning, functional expression, and induction by wounding and herbivory. Plant Mol Biol 46:347–359
Harvey GT (1975) Nutritional studies of eastern spruce budworm (Lepidoptera: Tortricidae). II. Starches. Can Entomol 107:717–728
Haukioja E (2003) Putting the insect into the birch–insect interaction. Oecologia 136:161–168
Hemming JDC, Lindroth RL (1995) Intraspecific variation in aspen phytochemistry: effects on performance in gypsy moths and forest tent caterpillars. Oecologia 103:79–88
Horie Y, Nakasone S, Watanabe K, Nakamura M, Suda H (1985) Daily ingestion and utilization of various kinds of nutrients by the silkworm, Bombyx mori (Lepidoptera: Bombycidae). Appl Entomol Zool 20:159–172
Horton DR, Redak RA (1993) Further comments on analysis of covariance in insect dietary studies. Entomol Exp Appl 69:263–275
Hough JA, Pimentel D (1978) Influence of host foliage on development, survival and fecundity of the gypsy moth. Env Entomol 7:97–102
Hunter AF, Lechowicz MJ (1992) Foliage quality changes during canopy development of some northern hardwood trees. Oecologia 89:316–323
Jones CG, Hare JD, Compton SJ (1989) Measuring plant protein with the Bradford assay. J Chem Ecol 15:979–992
Lawson DL, Merritt RW, Klug MJ, Martin JS (1982) The utilization of late season foliage by the orange striped oakworm, Anisota senatoria. Entomol Exp Appl 32:242–248
Liebhold AM, Gottschalk KW, Muzika RM, Montgomery ME, Young R, O’Day K, Kelley B (1995) Suitability of North American tree species to the gypsy moth: a summary of field and laboratory tests. United States Department of Agriculture Forest Service, Northeastern Forest Experimental Station, General Technical Report NE-211, Radnor
Lindroth RL, Anson BD, Weisbrod AV (1990) Effects of protein and juglone on gypsy moths: growth performance and detoxification enzyme activity. J Chem Ecol 16:2533–2547
Maksymowych R (1973) Analysis of leaf development. Cambridge University Press, London
Martin MM, Van’t Hof HM (1988) The cause of reduced growth of Manduca sexta larvae on a low-water diet: increased metabolic processing costs or nutrient limitation? J Insect Physiol 34:515–525
Mattson WJ (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119–161
Milton K, Dintzis FR (1981) Nitrogen-to-protein conversion factors for tropical plant samples. Biotropica 13:177–181R
Parry D, Spence JR, Volney WJA (1998) Budbreak phenology and natural enemies mediate survival of first-instar forest tent caterpillar (Lepidoptera: Lasiocampidae). Environ Entomol 27:1368–1374
Raubenheimer D, Simpson SJ (1992) Analysis of covariance: an alternative to nutritional indices. Entomol Exp Appl 62:221–231
Read J, Stokes A (2006) Plant biomechanics in an ecological context. Am J Bot 93:1546–1565
Rickleffs RE, Matthew KK (1982) Chemical characteristics of the foliage of some deciduous trees in southeastern Ontario. Can J Bot 60:2037–2045
Riipi M, Ossipov V, Lempa K, Haukioja E, Koricheva J, Ossipova S, Pihlaja K (2002) Seasonal changes in birch leaf chemistry: are there trade-offs between leaf growth and accumulation of phenolics? Oecologia 130:380–390
Rossiter MC (1991) Maternal effects generate variation in life history: consequences of egg weight plasticity in the gypsy moth. Funct Ecol 5:38–393
Ruhnke H, Schadler M, Klotz S, Matthies D, Brandl R (2009) Variability in leaf traits, insect herbivory and herbivore performance within and among individuals of four broad-leaved tree species. Basic Appl Ecol 10:726–736
Ruhnke H, Matthies D, Brandl R (2013) Experiments with Lymantria dispar do not support the idea of physiological adjustment to host individuals by insect herbivores. Web Ecol 13:79–84
Ruuhola T, Ossipov V, Lempa K, Haukioja E (2003) Amino acids during development of mountain birch leaves. Chemoecology 13:95–101
Salminen J-P, Roslin T, Karonen M, Sinkkonen J, Pihlaja K, Pulkkinen P (2004) Seasonal variation in the content of hydrolyzable tannins, flavonoid glycosides, and proanthocyanidins in oak leaves. J Chem Ecol 30:1693–1711
SAS Institute (2010) The SAS system for Windows, Version 9.3. SAS Institute, Cary
Schmidt D, Reese J (1986) Sources of error in nutritional index studies of insects on artificial diet. J Insect Physiol 32:193–198
Schroeder LA (1986) Changes in tree leaf quality and growth performance of lepidopteran larvae. Ecology 67:1628–1636
Scriber JM, Feeny P (1979) Growth of herbivorous caterpillars in relation to feeding specialization and to the growth form of their food plants. Ecology 60:829–850
Scriber JM, Slansky F (1981) The nutritional ecology of immature insects. Annu Rev Entomol 26:183–211
Shingfield KJ, Offer NW (1999) Simultaneous determination of purine metabolites, creatine and pseudouridine in ruminant urine by reversed-phase high performance liquid chromatography. J Chromatogr Biomed Sci Appl 723:81–94
Slansky F, Feeny P (1977) Stabilization of the rate of nitrogen accumulation by larvae of the cabbage butterfly on wild and cultivated food plants. Ecol Monogr 47:209–228
Thaler JS, Stout MJ, Karban R, Duffey SS (1996) Exogenous jasmonates simulate insect wounding in tomato plants (Lycopersicon esculentum) in the laboratory and field. J Chem Ecol 22:1767–1781
Trier TM, Mattson WJ (2003) Diet-induced thermogenesis in insects: a developing concept in nutritional ecology. Environ Entomol 32:1–8
Waldbauer GP (1968) The consumption and utilization of food by insects. Adv Insect Physiol 5:229–289
Wu L, Zhou J, Xue X, Li Y, Zhao J (2009) Fast determination of 26 amino acids and their content changes in royal jelly during storage using ultra-performance liquid chromatography. J Food Compos Anal 22:242–249
Yeoh H-H, Wee Y-C (1994) Leaf protein contents and nitrogen-to-protein conversion factors for 90 plant species. Food Chem 49:245–250
Zanotto FP, Simpson SJ, Raubenheimer D (1993) The regulation of growth by locusts through post-ingestive compensation for variation in the levels of dietary protein and carbohydrate. Physiol Entomol 18:425–434
Zhao D, MacKown CT, Starks PJ, Kindiger BK (2010) Rapid analysis of nonstructural carbohydrates in grass forage using microplate enzymatic assays. Crop Sci 50:1537–1545
Acknowledgements
This work is dedicated to four of the outstanding mentors of RVB: Paul Feeny, Douglas Futuyma, Elizabeth Bernays, and Michael Martin. In addition, we thank Chris Andrews for statistical consultation, Christine Lokerson and Hannah Nadel (USDA) for providing L. dispar eggs, David Borneman, Kerry Gray, Robert Grese, and Marvin Pettway for permitting the use of trees in the Ann Arbor area, and Jennifer Thaler and two anonymous reviewers for many helpful comments. Support for Sara Kileen was provided by a Winnifred B. Chase Fellowship, K.L. Jones Award, and Program in Biology Fellowship, and support for Caleb Nusbaum was provided by the University of Michigan Undergraduate Research Opportunities Program.
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RVB conceived and designed the experiments. RVB, MK, SK and CPN performed the experiments. RVB analyzed the data. RVB wrote the manuscript. MK, SK and CPN provided editorial advice.
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Communicated by Jennifer Thaler.
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Barbehenn, R.V., Kapila, M., Kileen, S. et al. Acquiring nutrients from tree leaves: effects of leaf maturity and development type on a generalist caterpillar. Oecologia 184, 59–73 (2017). https://doi.org/10.1007/s00442-017-3854-z
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DOI: https://doi.org/10.1007/s00442-017-3854-z