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Nutritional and defensive properties of Fagaceae nuts dispersed by animals: a multiple species study

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Abstract

Seeds usually exhibit physical and chemical defensive properties; however, it is still debated whether there is trade-off between the two defensive traits. Moreover, the relationship between nutritional and defensive properties of seeds is rarely investigated. In this study, we measured chemical compositions and physical properties of 29 species/varieties in Fagaceae with different seed traits, to investigate variations in nutritional and defensive properties at interspecific level. Our study provided evident nutritional trade-off in Fagaceae nuts, i.e., the concentration of protein and fat was negatively correlated with that of starch. However, no clear trade-off between physical and chemical defensive traits was found, indicating coordinated defense syndromes in these Fagaceae species. Chemical defense in Fagaceae nuts was positively associated with fat and protein but negatively with the content of starch. The congruence between phylogenetic tree and seed trait cladogram indicated conservative evolution of seed traits. In addition, large nuts had high concentration of protein and fat, resulting in a positive relationship between seed coat thickness and caloric values. Fagaceae nuts with high nutrition tended to invest more energy into physical defenses, indicating that the trade-off between chemical and physical defenses might be seed size dependent across plant species.

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References

  • Adamczyk B, Salminen JP, Smolander A, Kitunen V (2012) Precipitation of proteins by tannins: effects of concentration, protein/tannin ratio and pH. Int J Food Sci Technol 47:875–878

    Article  CAS  Google Scholar 

  • Agrawal AA, Fishbein M (2006) Plant defense syndromes. Ecology 87:S132–S149

    Article  PubMed  Google Scholar 

  • Banko PC, Cipollini ML, Breton GW, Paulk E, Wink M, Izhaki I (2002) Seed chemistry of Sophora chrysophylla (mamane) in relation to diet of specialist avian seed predator Loxioides bailleui (Palila) in Hawaii. J Chem Ecol 28:1393–1410

    Article  CAS  PubMed  Google Scholar 

  • Carrillo CM, Moreno E, Valera F, Barbosa A (2007) Seed selection by the trumpeter finch, Bucanetes githagineus. What currency does this arid land species value? Ann Zool Fenn 44:377–386

    Google Scholar 

  • Chang G, Zhang Z (2014) Functional traits determine formation of mutualism and predation interactions in seed–rodent dispersal system of a subtropical forest. Acta Oecol 55:43–50

    Article  Google Scholar 

  • Chen X, Cannon CH, Conklin-Brittan NL (2012) Evidence for a trade-off strategy in stone oak (Lithocarpus) seeds between physical and chemical defense highlights fiber as an important antifeedant. PLoS One 7:e32890

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Díaz M (1996) Food choice by seed-eating birds in relation to seed chemistry. Comp Biochem Physiol A 113:239–246

    Article  Google Scholar 

  • Eichenberg D, Purschke O, Ristok C, Wessjohann L, Bruelheide H (2015) Trade-offs between physical and chemical carbon-based leaf defence: of intraspecific variation and trait evolution. J Ecol 103:1667–1679

    Article  CAS  Google Scholar 

  • Fleck DC, Tomback DF (1996) Tannin and protein in the diet of a food-hoarding granivore, the Western Scrub-Jay. Condor 98:474–482

    Article  Google Scholar 

  • Fox JF (1982) Adaptation of gray squirrel behaviour to autumn germination by white oak acorns. Evolution 36:800–809

    Article  Google Scholar 

  • Gershenzon J (1994) The cost of plant chemical defense against herbivory: a biochemical perspective. In: Bernays EA (ed) Insect–plant interactions, vol 5. CRC Press, Boca Raton, pp 105–173

    Google Scholar 

  • Goslee SC, Urban DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22:1–19

    Article  Google Scholar 

  • Hadj-Chikh LZ, Steele MA, Smallwood PD (1996) Caching decisions by grey squirrels: a test of the handling time and perishability hypotheses. Anim Behav 52:941–948

    Article  Google Scholar 

  • Hanley ME, Lamont BB (2002) Relationships between physical and chemical attributes of congeneric seedlings: how important is seedling defence? Funct Ecol 16:216–222

    Article  Google Scholar 

  • Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335

    Article  Google Scholar 

  • Koricheva J, Nykanen H, Gianoli E (2004) Meta-analysis of trade-offs among plant antiherbivore defenses: are plants jacks-of-all-trades, masters of all? Am Nat 163:E64–E75

    Article  PubMed  Google Scholar 

  • Lai X, Guo C, Xiao Z (2014) Trait-mediated seed predation, dispersal and survival among frugivore-dispersed plants in a fragmented subtropical forest, southwest China. Integr Zool 9:246–254

    Article  PubMed  Google Scholar 

  • Moles AT, Peco B, Wallis IR et al (2013) Correlations between physical and chemical defences in plants: tradeoffs, syndromes, or just many different ways to skin a herbivorous cat? New Phytol 198:252–263

    Article  PubMed  Google Scholar 

  • R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/

  • Read J, Sanson GD, Caldwell E et al (2009) Correlations between leaf toughness and phenolics among species in contrasting environments of Australia and New Caledonia. Ann Bot 103:757–767

    Article  CAS  PubMed  Google Scholar 

  • Ríos JM, Mangione A, Marone L (2012) Effects of nutritional and anti-nutritional properties of seeds on the feeding ecology of seed-eating birds of the Monte desert, Argentina. Condor 114:44–55

    Article  Google Scholar 

  • Schnurr JL, Ostfeld RS, Canham CD (2014) Direct and indirect effects of masting on rodent populations and tree seed survival direct and indirect effects of casting on rodent populations and tree seed survival. Oikos 96:402–410

    Article  Google Scholar 

  • Shimada T, Saitoh T (2006) Re-evaluation of the relationship between rodent populations and acorn masting: a review from the aspect of nutrients and defensive chemicals in acorns. Popul Ecol 48:341–352

    Article  Google Scholar 

  • Shimada T, Saitoh T, Sasaki E, Nishitani Y, Osawa R (2006) Role of tannin-binding salivary proteins and tannase-producing bacteria in the acclimation of the Japanese wood mouse to acorn tannins. J Chem Ecol 32:1165–1180

    Article  CAS  PubMed  Google Scholar 

  • Steele MA, Manierre S, Genna T, Contreras T, Smallwood PD, Pereira M (2006) The innate basis of food hoarding decisions in grey squirrels: evidence for behavioral adaptations to the oaks. Anim Behav 71:155–160

    Article  Google Scholar 

  • Steele MA, Rompre G, Stratford JA, Zhang H, Suchocki M, Marino S (2015) Scatter-hoarding rodents favor higher predation risks for cache sites: the potential for predators to influence the seed dispersal process. Integr Zool 10:257–266

    Article  PubMed  Google Scholar 

  • Sundaram M, Willoughby JR, Lichti NI, Steele MA, Swihart RK (2015) Segregating the effects of seed traits and common ancestry of hardwood trees on eastern gray squirrel foraging decisions. PLoS One 10:e0130942

    Article  PubMed  PubMed Central  Google Scholar 

  • Twigg LE, Socha LV (1996) Physical versus chemical defence mechanisms in toxic Gastrolobium. Oecologia 108:21–28

    Article  Google Scholar 

  • Vander Wall SB (1990) Food hoarding in animals. University of Chicago Press, Chicago

    Google Scholar 

  • Vander Wall SB (2001) The evolutionary ecology of nut dispersal. Bot Rev 67:74–117

    Article  Google Scholar 

  • Vander Wall SB (2010) How plants manipulate the scatter-hoarding behaviour of seed-dispersing animals. Philos Trans R Soc B Biol Sci 365:989–997

    Article  Google Scholar 

  • Venable DL, Brown JS (1988) The selective interactions of dispersal, dormancy, and seed size as adaptations for reducing risk in variable environments. Am Nat 161:360–384

    Article  Google Scholar 

  • Wang B, Chen J (2012) Effects of fat and protein levels on foraging preferences of tannin in scatter-hoarding rodents. PLoS One 7:e40640

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Z, Cao L, Zhang Z (2014) Seed traits and taxonomic relationships determine the occurrence of mutualisms versus seed predation in a tropical forest rodent and seed dispersal system. Integr Zool 9:309–319

    Article  PubMed  Google Scholar 

  • Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505

    Article  Google Scholar 

  • Whitehead SR, Quesada MFO, Bowers MD (2015) Chemical tradeoffs in seed dispersal: defensive metabolites in fruits deter consumption by mutualist bats. Oikos 125:927–937

    Article  Google Scholar 

  • Xiao Z, Gao X, Steele MA, Zhang Z (2010) Frequency-dependent selection by tree squirrels: adaptive escape of nondormant white oaks. Behav Ecol 21:169–175

    Article  Google Scholar 

  • Yang XP (2002) Animal physiology. Higher Education Press, Beijing (in Chinese)

    Google Scholar 

  • Yi X, Wang Z (2016) The importance of cotyledons for early-stage oak seedlings under different nutrient levels: a multi-species study. J Plant Growth Regul 35:183–189

    Article  CAS  Google Scholar 

  • Zhang H, Zhang Z (2008) Endocarp thickness affects seed removal speed by small rodents in a warm-temperate broad-leafed deciduous forest, China. Acta Oecol 34:285–293

    Article  Google Scholar 

  • Zhang Z, Wang Z, Chang G, Yi X, Lu J, Xiao Z, Zhang H, Cao L, Wang F, Li H, Yan C (2016) Trade-off between seed defensive traits and impacts on relationship between seeds and rodents in forest ecosystems. Plant Ecol 217:253–265

    Article  Google Scholar 

  • Zungu MM, Downs CT (2015) Effects of tannins on fruit selection in three southern African frugivorous birds. Behav Proc 111:84–89

    Article  Google Scholar 

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Acknowledgments

Funding for this study was supported by the Natural Science Foundation of Jiangxi Province (No. 20161ACB20017), the State Key Laboratory of Forest and Soil Ecology (No. LFSE2015-01), and the National Natural Science Foundation of China (No. 31470113).

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Authors and Affiliations

  1. College of Life Sciences, Jiangxi Normal University, Nanchang, 330022, China

    Zhenyu Wang, Yihao Zhang, Dongyuan Zhang, Jia Li & Xianfeng Yi

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  1. Zhenyu Wang
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  2. Yihao Zhang
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  3. Dongyuan Zhang
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  4. Jia Li
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  5. Xianfeng Yi
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Correspondence to Xianfeng Yi.

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Communicated by Jarmo Holopainen, Ph.D.

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Wang, Z., Zhang, Y., Zhang, D. et al. Nutritional and defensive properties of Fagaceae nuts dispersed by animals: a multiple species study. Eur J Forest Res 135, 911–917 (2016). https://doi.org/10.1007/s10342-016-0983-6

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  • DOI: https://doi.org/10.1007/s10342-016-0983-6

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