Abstract
Forage selection by mammalian herbivores has shown to be influenced by plant nutritional content, but the role of plant secondary compounds (PSCs) on forage selection is less well understood. Here, we studied the role of PSCs in giant panda (Ailuropoda melanoleuca) foraging strategies; examined seasonal and age class variation in PSC composition in the panda’s principal food resource, bamboo (Bashania fargesii); evaluated anti-oxidant and antibacterial effects of bamboo extract; and determined how panda’s seasonal movements and foraging patch selection which were determined by GPS collars related to patterns of PSC concentrations in bamboo. Panda’s selection of foraging sites indicated positive selection for several PSCs, including flavonoids, alkaloids, and tannins. Pandas primarily ingested bamboo leaves, as opposed other parts of the bamboo, during the time of year when many PSC concentrations were at their highest. Further, pandas prefer to forage on younger bamboo, which contains higher concentrations of alkaloids and antibacterial activity than older bamboo. As might be expected for compounds that can have positive or negative biological effects depending on dose, pandas appeared to select both for and against some PSCs depending on context. Ex situ experiments showed that flavonoids and alkaloids were influential antioxidants and tannins and alkaloids had high levels of antibacterial activity. Panda foraging sites were characterized by high anti-oxidant activity. Variation in PSC content of bamboo on the landscape may have profound effects on pandas, including parasite control, protecting against cancer, improved cardiovascular health, and disease prevention. These potential roles of PSCs should receive greater attention in ecology and conservation.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and materials
All data produced from this study are provided in this manuscript or will be available from the corresponding author upon reasonable request.
Code availability
Not applicable.
References
Agrawal AA, Weber MG (2015) On the study of plant defence and herbivory using comparative approaches: how important are secondary plant compounds. Ecol Lett 18:985–991. https://doi.org/10.1111/ele.12482
Athanasiadou S, Kyriazakis I (2004) Plant secondary metabolites: antiparasitic effects and their role in ruminant production systems. Proc Nutr Soc 63:631–639. https://doi.org/10.1079/PNS2004396
Barry TN, Manley TR (1986) Interrelationships between the concentrations of total condensed tannin, free condensed tannin and lignin in Lotus sp. and their possible consequences in ruminant nutrition. J Sci Food Agric 37:248–254. https://doi.org/10.1002/jsfa.2740370309
Barry TN, Manley TR, Duncan SJ (1986) The role of condensed tannins in the nutritional value of Lotus pedunculatus for sheep. 4. Sites of carbohydrate and protein digestion as influenced by dietary reactive tannin concentration. Br J Nutr 55(1):123–137. https://doi.org/10.1079/bjn19860016
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Stat Methodol 57:289–300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x
Boots AW, Haenen GR, Bast A (2008) Health effects of quercetin: from antioxidant to nutraceutical. Eur J Pharmacol 585(2–3):325–337. https://doi.org/10.1016/j.ejphar
Brandwilliams W, Cuvelier ME, Berset C (1995) Use of a free radical method to evaluate antioxidant activity. LWT-Food Sci Technol 28:25–30. https://doi.org/10.1016/S0023-6438(95)80008-5
Choat J, Clements K (1998) Vertebrate herbivores in marine and terrestrial environments: a nutritional ecology perspective. Annu Rev Ecol Syst 29:375–403. https://doi.org/10.1146/annurev.ecolsys.29.1.375
Clauss M, Lason K, Gehrke J, Lechner-Doll M, Fickel J, Grune T, Streich WJ (2003) Captive roe deer (Capreolus capreolus) select for low amounts of tannic acid but not quebracho: fluctuation of preferences and potential benefits. Comp Biochem Physiol B Biochem Mol Biol 136:369–382. https://doi.org/10.1016/S1096-4959(03)00244-6
CLSI (2019) Performance standards for antimicrobial susceptibility testing, 29th edn. Clinical and Laboratory Standards Institute, Wayne, Pennsylvania, USA
Conforti F, Rigano D, Menichini F, Loizzo MR, Senatore F (2009) Protection against neurodegenerative diseases of Iris pseudopumila extracts and their constituents. Fitoterapia 80:62–67. https://doi.org/10.1016/j.fitote.2008.10.005
Conklin-Brittain NL, Dierenfeld ES, Wrangham RW, Norconk M, Silver SC (1999) Chemical protein analysis: a comparison of Kjeldahl crude protein and total ninhydrin protein from wild, tropical vegetation. J Chem Ecol 25:2601–2622. https://doi.org/10.1023/A:1020835120701
Cornell HV, Hawkins BA (2003) Herbivore responses to plant secondary compounds: a test of phytochemical coevolution theory. Am Nat 161:507–522. https://doi.org/10.1086/368346
Cottigli F, Loy G, Garau D, Floris C, Caus M, Pompei R, Bonsignore L (2001) Antimicrobial evaluation of coumarins and flavonoids from the stems of Daphne gnidium L. Phytomedicine 8:302–305. https://doi.org/10.1078/0944-7113-00036
Crozier A, Clifford MN, Ashihara H (2008) Plant secondary metabolites: occurrence, structure and role in the human diet. Wiley-Blackwell, London
de Roode JC, Lefèvre T, Hunter MD (2013) Self-medication in animals. Science 340:150–151. https://doi.org/10.1126/science.1235824
Dearing MD, Foley WJ, McLean S (2005) The influence of plant secondary metabolites on the nutritional ecology of herbivorous terrestrial vertebrates. Annu Rev Ecol Evol Syst 36:169–189. https://doi.org/10.1146/annurev.ecolsys.36.102003.152617
Egert S, Bosy-Westphal A, Seiberl J et al (2009) Quercetin reduces systolic blood pressure and plasma oxidised low-density lipoprotein concentrations in overweight subjects with a high-cardiovascular disease risk phenotype: a double-blinded, placebo-controlled cross-over study. Br J Nutr 102:1065–1074. https://doi.org/10.1017/S0007114509359127
Feng Z, Li R, DeAngelis DL, Bryant JP, Kielland K, Iii FSC, Swihart RK (2009) Plant toxicity, adaptive herbivory, and plant community dynamics. Ecosystems 12:534–547. https://doi.org/10.1007/s10021-009-9240-X
Feng N, Yu Y, Wang T, Wilker P, Wang J, Li Y, Sun Z, Gao Y, Xia X (2016) Fatal canine distemper virus infection of giant pandas in China. Sci Rep 6:27518. https://doi.org/10.1038/srep27518
Freeland WJ, Janzen DH (1974) Strategies in herbivory by mammals: the role of plant secondary compounds. Am Nat 108:269–289. https://doi.org/10.1086/282907
Gemede FG, Ratta N (2014) Antinutritional factors in plant foods: potential health benefits and adverse effects. Int J Food Sci Nutr 3:284–289. https://doi.org/10.11648/j.ijnfs.20140304.18
Hagerman AE, Robbins CT (1993) Specificity of tannin-binding salivary proteins relative to diet selection by mammals. Can J Zool 71:628–633. https://doi.org/10.1139/z93-085
Hong M, Wei W, Yang Z, Yuan S, Yang X, Gu X, Huang F, Zhang Z (2016) Effects of timber harvesting on Arundinaria spanostachya bamboo and feeding-site selection by giant pandas in Liziping Nature Reserve, China. For Ecol Manag 373:74–80. https://doi.org/10.1016/j.foreco.2016.04.039
Hu Y, Wu Q, Ma S, Ma T, Shan L, Wang X, Nie Y, Ning Z, Yan L, Xiu Y, Wei F (2017) Comparative genomics reveals convergent evolution between the bamboo-eating giant and red pandas. Proc Natl Acad Sci USA 114:1081–1086. https://doi.org/10.1073/pnas.1613870114
Huang Q, Liu X, Zhao G, Hu T, Wang Y (2018) Potential and challenges of tannins as an alternative to in-feed antibiotics for farm animal production. Anim Nutr 4:137–150. https://doi.org/10.1016/j.aninu.2017.09.004
Hull V, Zhang J, Huang J, Zhou S, Viña A, Shortridge A, Li R, Liu D, Xu W, Ouyang Z, Zhang H, Liu J (2016) Habitat use and selection by giant pandas. PLoS ONE 11(9):e0162266. https://doi.org/10.1371/journal.pone.0162266
Iason G (2005) The role of plant secondary metabolites in mammalian herbivory: ecological perspectives. Proc Nutr Soc 64:123–131. https://doi.org/10.1079/PNS2004415
Iason GR, Villalba JJ (2006) Behavioral strategies of mammal herbivores against plant secondary metabolites: the avoidance–tolerance continuum. J Chem Ecol 32:1115–1132. https://doi.org/10.1007/s10886-006-9075-2
Jung H (1995) Nutritional ecology of the ruminant, second edition. J Nutr 125:1025. https://doi.org/10.1093/jn/125.4.1025
Kong L, Xu W, Zhang L, Gong M, Xiao Y, Ouyang Z (2017) Habitat conservation redlines for the giant pandas in China. Biol Conserv 210:83–88. https://doi.org/10.1016/j.biocon.2016.03.028
Li Y, Swaisgood RR, Wei W, Nie Y, Hu Y, Yang X, Gu X, Zhang Z (2017) Withered on the stem: is bamboo a seasonally limiting resource for giant pandas? Environ Sci Pollut Res Int 24:10537–10546. https://doi.org/10.1007/s11356-017-8746-6
Li YL, Ma SC, Yang YT, Ye SM, But PP (2002) Antiviral activities of flavonoids and organic acid from Trollius chinensis Bunge. J Ethnopharmacol 79:365–368. https://doi.org/10.1016/s0378-8741(01)00410-x
Lin Y, Collier AC, Liu W, Berry MJ, Panee J (2008) The inhibitory effect of bamboo extract on the development of 7, 12-dimethylbenz [a] anthracene (DMBA)-induced breast cancer. Phytother Res 22:1440–1445. https://doi.org/10.1002/ptr.2439
Lisonbee LD, Villalba JJ, Provenza FD, Hall JO (2009) Tannins and self-medication: implications for sustainable parasite control in herbivores. Behav Processes 82:184–189. https://doi.org/10.1016/j.beproc.2009.06.009
Mainka SA, Qiu X, He T, Appel MJ (1994) Serologic survey of giant pandas (Ailuropoda melanoleuca), and domestic dogs and cats in the Wolong Reserve, China. J Wildl Dis 30:86–89. https://doi.org/10.7589/0090-3558-30.1.86
Marley CL, Cook RT, Keatinge R, Barrett J, Lampkin N (2003) The effect of birdsfoot trefoil (Lotus corniculatus) and chicory (Cichorium intybus) on parasite intensities and performance of lambs naturally infected with helminth parasites. Vet Parasitol 112(1–2):147–155. https://doi.org/10.1016/s0304-4017(02)00412-0
Min BR, Barry TN, Attwood GT, McNabb WC (2003) The effect of condensed tannins on the nutrition and health of ruminants fed fresh temperate forages: a review. Anim Feed Sci Technol 106:3–19. https://doi.org/10.1016/S0377-8401(03)00041-5
Mittra B, Saha A, Chowdhury AR, Pal C, Mandal S, Mukhopadhyay S, Bandyopadhyay S, Majumder HK (2000) Luteolin, an abundant dietary component is a potent anti-leishmanial agent that acts by inducing topoisomerase II-mediated kinetoplast DNA cleavage leading to apoptosis. Mol Med 6:527–541. https://doi.org/10.1007/BF03401792
Molyneux P (2004) The use of the stable free radical diphenylpicrylhydrazyl (DPPH) for estimating antioxidant. Warasan Songkhla Nakharin 26(2):211–219
Ni Q, Zhang Y, Xu G, Gao Q, Gong L, Zhang Y (2014) Influence of harvest season and drying method on the antioxidant activity and active compounds of two bamboo grass leaves. J Food Process Preserv 38:1565–1576. https://doi.org/10.1111/jfpp.12116
Nie Y, Speakman JR, Wu Q, Zhang C, Hu Y, Xia M, Yan L, Hambly C, Wang L, Wei W (2015a) Exceptionally low daily energy expenditure in the bamboo-eating giant panda. Science 349:171–174. https://doi.org/10.1126/science.aab2413
Nie Y, Zhang Z, Raubenheimer D, Elser JJ, Wei W, Wei F (2015b) Obligate herbivory in an ancestrally carnivorous lineage: the giant panda and bamboo from the perspective of nutritional geometry. Funct Ecol 29:26–34. https://doi.org/10.1111/1365-2435.12302
Odontuya G, Hoult J, Houghton P (2005) Structure-activity relationship for antiinflammatory effect of luteolin and its derived glycosides. Phytother Res 19:782–786. https://doi.org/10.1002/ptr.1723
Orrego R, Leiva E, Cheel J (2009) Inhibitory effect of three C-glycosylflavonoids from Cymbopogon citratus (Lemongrass) on human low density lipoprotein oxidation. Molecules 14:3906–3913. https://doi.org/10.3390/molecules14103906
Panche AN, Diwan AD, Chandra SR (2016) Flavonoids: an overview. J Nutr Sci 5:e47. https://doi.org/10.1017/jns.2016.41
Pond WG, Church DB, Pond KR, Schoknecht PA (2004) Basic animal nutrition and feeding, 5nd edn. Wiley, Corvallis, Oregon
Popov IV, Andreeva IN, Gavrilin MV (2003) HPLC determination of tannins in raw materials and preparations of garden burnet. Pharm Chem J 37:360–363. https://doi.org/10.1023/A:1026319524715
Qin Q, Li D, Zhang H, Hou R, Zhang Z, Zhang C, Zhang J, Wei F (2010) Serosurvey of selected viruses in captive giant pandas (Ailuropoda melanoleuca) in China. Vet Microbiol 142:199–204. https://doi.org/10.1016/j.vetmic.2009.09.062
Qiu X, Mainka SA (1993) Basic animal nutrition and feeding. J Zoo Wildl Med 24:425–429
R Core Team (2018) R: a language and environment for statistical computing. R Foundationfor Statistical Computing, Vienna, Austria
Raubenheimer D, Simpson SJ, Mayntz D (2009) Nutrition, ecology and nutritional ecology: toward an integrated framework. Funct Ecol 23:4–16. https://doi.org/10.1111/j.1365-2435.2009.01522.x
Reid DG, Hu J (1991) Giant panda selection between Bashania fangiana bamboo habitats in Wolong Reserve, Sichuan, China. J Appl Ecol 28(1):228–243. https://doi.org/10.2307/2404127
Ren H, Feng Q, Huang W, Li X (2012) Research development on the analytical method of content determination about alkaloids component. Chin J Pharmacovigil 9:622–624 (in Chinese)
Roland WS, van Buren L, Gruppen H et al (2013) Bitter taste receptor activation by flavonoids and isoflavonoids: modeled structural requirements for activation of hTAS2R14 and hTAS2R39. J Agric Food Chem 61(44):10454–10466. https://doi.org/10.1021/jf403387p
Rosenthal GA, Berenbaum MR (1992) Herbivores: their interactions with secondary plant metabolites, vol. II: ecological and evolutionary processes. Academic Press, New York
Schaller GB, Hu J, Pan W, Zhu J (1985) The giant pandas of Wolong. University of Chicago Press, Chicago
Shibata M, Kubo K, Onoda M (1976) Pharmacological studies on bamboo grass 2: central depressant and antitoxic actions of a water-soluble fraction (folin) extracted from Sasa albomarginata. Nihon Yakurigaku Zasshi 72:531–541
Swaisgood RR, Wang DJ, Wei FW (2016) Ailuropoda melanoleuca. IUCN red list of threatened species. http://hubaogy.cn/index/news/show/id/107.html
Tian Z, Liu X, Fan Z, Liu J, Pimm SL, Liu L, Garcia C, Songer M, Shao X, Skidmore A, Wang T, Zhang Y, Chang Y, Jin X, Gong M, Zhou L, He X, Dang G, Zhu Y, Cai Q (2019) The next widespread bamboo flowering poses a massive risk to the giant panda. Biol Conserv 234:180–187. https://doi.org/10.1016/j.biocon.2019.03.030
Villalba JJ, Provenza FD (2007) Self-medication and homeostatic behaviour in herbivores: learning about the benefits of nature’s pharmacy. Animal 1(9):1360–1370. https://doi.org/10.1017/S1751731107000134
Wang L, Yuan S, Nie Y, Zhao J, Cao X, Dai Y, Zhang Z, Wei F (2020) Dietary flavonoids and the altitudinal preference of wild giant pandas in Foping National Nature Reserve, China. Glob Ecol Conserv 22:e00981. https://doi.org/10.1016/j.gecco.2020.e00981
Wei F, Swaisgood RR, Hu Y, Nie Y, Yan L, Zhang Z, Qi D, Zhu L (2015a) Progress in the ecology and conservation of giant pandas. Conserv Biol 29:1497–1507. https://doi.org/10.1111/cobi.12582
Wei W, Nie Y, Zhang Z, Hu Y, Yan L, Qi D, Li X, Wei F (2015b) Hunting bamboo: foraging patch selection and utilization by giant pandas and implications for conservation. Biol Conserv 186:260–267. https://doi.org/10.1016/j.biocon.2015.03.023
Wei F, Feng Z, Wang Z, Li M (1999) Feeding strategy and resource partitioning between giant and red pandas. Mammalia 63:417–430. https://doi.org/10.1515/mamm.1999.63.4.417
Wink M (2015) Modes of action of herbal medicines and plant secondary metabolites. Medicines 2:251–286. https://doi.org/10.3390/medicines2030251
Xu W, Viña A, Kong L, Pimm SL, Zhang J, Yang W, Xiao Y, Zhang L, Chen X, Liu J, Ouyang Z (2017) Reassessing the conservation status of the giant panda using remote sensing. Nat Ecol Evol 1:1635–1638. https://doi.org/10.1038/s41559-017-0317-1
Zhang Y, Tie X, Bao B, Wu X, Zhang Y (2007a) Metabolism of flavone C-glucosides and p-coumaric acid from antioxidant of bamboo leaves (AOB) in rats. Br J Nutr 97:484–494. https://doi.org/10.1017/S0007114507336830
Zhang Z, Swaisgood RR, Wu H, Li M, Yong Y, Hu J, Wei F (2007b) Factors predicting den use by maternal giant pandas. J Wildl Manage 71:2694–2698. https://doi.org/10.2193/2006-504
Zhang JS, Daszak P, Huang HL, Yang GY, Kilpatrick AM, Zhang S (2008) Parasite threat to panda conservation. EcoHealth 5:6–9. https://doi.org/10.1007/s10393-007-0139-8
Zhang Z, Zhan X, Yan L, Li M, Hu J, Wei F (2009) What determines selection and abandonment of a foraging patch by wild giant pandas (Ailuropoda melanoleuca) in winter? Environ Sci Pollut Res Int 16:79–84. https://doi.org/10.1007/s11356-008-0066-4
Zhang L, Wu Q, Hu Y, Wu H, Wei F (2015) Major histocompatibility complex alleles associated with parasite susceptibility in wild giant pandas. Heredity 114:85–93. https://doi.org/10.1038/hdy.2014.73
Zhao S, Zheng P, Dong S et al (2012) Whole-genome sequencing of giant pandas provides insights into demographic history and local adaptation. Nat Genet 45:67–71. https://doi.org/10.1038/ng.2494
Zhu L, Wu Q, Dai J, Zhang S, Wei F (2011) Evidence of cellulose metabolism by the giant panda gut microbiome. Proc Natl Acad Sci USA 108:17714–17719. https://doi.org/10.1073/pnas.1017956108
Acknowledgements
We are grateful to the Foping National Nature Reserve Administration Bureau for their assistance with field surveys. We are grateful to San Diego Zoo for their help during the preparation of this manuscript. Finally, we are also grateful to all authors for their contributions to this manuscript.
Funding
This study was supported by the Natural Science Foundation of China (Nos 32370557, 32200346) and Sichuan Province (2022NSFSC1717), Talent Foundation Project of China West Normal University (17YC357) and Nanchong Key Laboratory of Wildlife Nutrition Ecology and Disease Control (NCKL202201).
Author information
Authors and Affiliations
Contributions
SY, MAO, ZZ and RRS conceived and designed the experiments. TF and YL performed the fieldwork. FY and YD analyzed the data. FY wrote the manuscript and LW revised it. All authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Ethics approval
Fieldwork was conducted with the permission of the law of the People's Republic of China on the protection of wildlife. The giant pandas involved in this study are approved by the National Forestry and Grassland Bureau.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Handling editor: Heiko Georg Rödel.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Yang, F., Swaisgood, R.R., Liu, Y. et al. The beneficial role of plant secondary compounds in giant panda foraging ecology. Mamm Biol 104, 41–54 (2024). https://doi.org/10.1007/s42991-023-00386-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42991-023-00386-z