Skip to main content

Advertisement

Log in

Compound Specific Trends of Chemical Defences in Ficus Along an Elevational Gradient Reflect a Complex Selective Landscape

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Elevational gradients affect the production of plant secondary metabolites through changes in both biotic and abiotic conditions. Previous studies have suggested both elevational increases and decreases in host-plant chemical defences. We analysed the correlation of alkaloids and polyphenols with elevation in a community of nine Ficus species along a continuously forested elevational gradient in Papua New Guinea. We sampled 204 insect species feeding on the leaves of these hosts and correlated their community structure to the focal compounds. Additionally, we explored species richness of folivorous mammals along the gradient. When we accounted for Ficus species identity, we found a general elevational increase in flavonoids and alkaloids. Elevational trends in non-flavonol polyphenols were less pronounced or showed non-linear correlations with elevation. Polyphenols responded more strongly to changes in temperature and humidity than alkaloids. The abundance of insect herbivores decreased with elevation, while the species richness of folivorous mammals showed an elevational increase. Insect community structure was affected mainly by alkaloid concentration and diversity. Although our results show an elevational increase in several groups of metabolites, the drivers behind these trends likely differ. Flavonoids may provide figs with protection against abiotic stressors. In contrast, alkaloids affect insect herbivores and may provide protection against mammalian herbivores and pathogens. Concurrent analysis of multiple compound groups alongside ecological data is an important approach for understanding the selective landscape that shapes plant defences.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Barbehenn R, 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

    PubMed  CAS  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting Linear Mixed-Effects Models Using lme4. J Stat Softw 67:1–48

    Google Scholar 

  • Baumgartner B, Erdelmeier CA, Wright AD, Rali T, Sticher O (1990) An antimicrobial alkaloid from Ficus septica. Phytochemistry 29:3327–3330

    CAS  Google Scholar 

  • Becerra JX (2007) The impact of herbivore-plant coevolution on plant community structure. Proc Natl Acad Sci USA 104:7483–7488

    PubMed  CAS  Google Scholar 

  • Berg C, Corner E (2005) Moraceae (Ficus). In: Flora Malesiana, Series I (Seed plants), vol 17. National Herbarium of the Netherlands, Leiden

    Google Scholar 

  • Brown CD, Vellend M (2014) Non-climatic constraints on upper elevational plant range expansion under climate change. Proc R Soc Lond B Biol Sci 281:20141779

    Google Scholar 

  • Bruneton J, Shamma M, Minard RD, Freyer AJ, Guinaudeau H (1983) Novel biogenetic pathways from (+)-reticuline. Three dimeric alkaloids:(+)-vanuatine,(+)-vateamine, and (+)-malekulatine. J Org Chem 48:3957–3960

    CAS  Google Scholar 

  • Cruaud A et al (2012) An extreme case of plant-insect codiversification: Figs and fig-pollinating wasps. Syst Biol 61:1029–1047

    PubMed  PubMed Central  Google Scholar 

  • Cui L et al (2004) On-line identification of phenanthroindolizidine alkaloids in a crude extract from Tylophora atrofolliculata by liquid chromatography combined with tandem mass spectrometry. Rapid Commun Mass Spectrom 18:184–190

    PubMed  CAS  Google Scholar 

  • Damu AG, Kuo PC, Shi LS, Li CY, Kuoh CS, Wu PL, Wu TS (2005) Phenanthroindolizidine alkaloids from the stems of Ficus septica. J Nat Prod 68:1071–1075

    PubMed  CAS  Google Scholar 

  • Defossez E, Pellissier L, Rasmann S (2018) The unfolding of plant growth form-defence syndromes along elevation gradients. Ecol Lett 21:609–618

    PubMed  Google Scholar 

  • Engström MT, Palijarvi M, Fryganas C, Grabber JH, Mueller-Harvey I, Salminen J-P (2014) Rapid qualitative and quantitative analyses of proanthocyanidin oligomers and polymers by UPLC-MS/MS. J Agric Food Chem 62:3390–3399

    PubMed  Google Scholar 

  • Engström MT, Pälijärvi M, Salminen J-P (2015) Rapid fingerprint analysis of plant extracts for ellagitannins, gallic acid, and quinic acid derivatives and quercetin-, kaempferol- and myricetin-based flavonol glycosides by UPLC-QqQ-MS/MS. J Agric Food Chem 63:4068–4079

    PubMed  Google Scholar 

  • Escobar-Bravo R, Klinkhamer PG, Leiss KA (2017) Interactive effects of UV-B light with abiotic factors on plant growth and chemistry, and their consequences for defense against arthropod herbivores. Front Plant Sci 8:278

    PubMed  PubMed Central  Google Scholar 

  • Ezedin Z, Weiblen G (2019) Additions and changes to Ficus (Moraceae) in New Guinea with comments on the world’s largest fig. Gardens’ Bulletin Singapore 71:197–216

    Google Scholar 

  • Flannery TF (1995) Mammals of New Guinea, 2nd edn. Comstock/Cornell, Ithaca

    Google Scholar 

  • Foley W, Iason G, McArthur C Role of plant secondary metobolites in the nutritional ecology of mammalian herbivores: how far have we come in 25 years? In: 5th Internaional Symposium on the Nutrition of Herbivores (1999) pp 130–209

  • Garibaldi LA, Kitzberger T, Chaneton EJ (2011) Environmental and genetic control of insect abundance and herbivory along a forest elevational gradient. Oecologia 167:117–129

    PubMed  Google Scholar 

  • Geml J et al (2014) Large-scale fungal diversity assessment in the Andean Yungas forests reveals strong community turnover among forest types along an altitudinal gradient. Mol Ecol 23:2452–2472

    PubMed  CAS  Google Scholar 

  • Givnish TJ (1999) On the causes of gradients in tropical tree diversity. J Ecol 87:193–210

    Google Scholar 

  • Hagerman AE, Butler LG (1978) Protein precipitation method for the quantitative determination of tannins. J Agric Food Chem 26:809–812

    CAS  Google Scholar 

  • Han G, Liu Y, Wang Q (2013) Total synthesis of phenanthroindolizidine alkaloids through an amidyl radical cascade/rearrangement reaction. Org Lett 15:5334–5337

    PubMed  CAS  Google Scholar 

  • Harborne JB, Williams CA (2000) Advances in flavonoid research since 1992. Phytochemistry 55:481–504

    PubMed  CAS  Google Scholar 

  • Kanowski J, Irvine A, Winter J (2003) The relationship between the floristic composition of rain forests and the abundance of folivorous marsupials in north-east. Qld J  Anim Ecol 72:627–632

    CAS  Google Scholar 

  • Khan IA, Rali T, Sticher O (1993) Alkaloids from Ficus pachyrhachis. Planta Med 59:286–286

    PubMed  CAS  Google Scholar 

  • Konno K, Hirayama C, Nakamura M, Tateishi K, Tamura Y, Hattori M, Kohno K (2004) Papain protects papaya trees from herbivorous insects: role of cysteine proteases in latex. Plant J 37:370–378

    PubMed  CAS  Google Scholar 

  • Kursar TA et al (2009) The evolution of antiherbivore defenses and their contribution to species coexistence in the tropical tree genus Inga. Proc Natl Acad Sci U S A 106:18073–18078

  • Lee Y-Z et al (2011) Isolation and biological activities of phenanthroindolizidine and septicine alkaloids from the Formosan Tylophora ovata. Planta Med 77:1932–1938

    PubMed  CAS  Google Scholar 

  • Malisch CS, Salminen J-P, Kölliker R, Engström MT, Suter D, Studer B, Lüscher A (2016) Drought effects on proanthocyanidins in sainfoin (Onobrychis viciifolia Scop.) are dependent on the plant’s ontogenetic stage. J Agric Food Chem 64:9307–9316

    PubMed  CAS  Google Scholar 

  • Miller JS, Feeny P (1983) Effects of benzylisoquinoline alkaloids on the larvae of polyphagous Lepidoptera. Oecologia 58:332–339

    PubMed  Google Scholar 

  • Mogg C et al (2008) Tests of the antibiotic properties of the invasive vine Vincetoxicum rossicum against bacteria, fungi and insects. Biochem Syst Ecol 36:383–391

    CAS  Google Scholar 

  • Moilanen J, Sinkkonen J, Salminen J-P (2013) Characterization of bioactive plant ellagitannins by chromatographic, spectroscopic and mass spectrometric methods. Chemoecology 23:165–179

  • Moore B, Marsh K, Wallis I, Foley W (2005) Taught by animals: how understanding diet selection leads to better zoo diets. Int Zoo Yearb 39:43–61

    Google Scholar 

  • Moreira X, Petry WK, Mooney KA, Rasmann S, Abdala-Roberts L (2018) Elevational gradients in plant defences and insect herbivory: recent advances in the field and prospects for future research. Ecography 41:1485–1496

    Google Scholar 

  • Novotny V et al (2005) An altitudinal comparison of caterpillar (Lepidoptera) assemblages on Ficus trees in Papua New Guinea. J Biogeogr 32:1303–1314

    Google Scholar 

  • Novotny V et al (2010) Guild-specific patterns of species richness and host specialization in plant-herbivore food webs from a tropical forest. J Anim Ecol 79:1193–1203

    PubMed  Google Scholar 

  • Novotny V, Toko P (2015) Ecological research in Papua New Guinean rainforests: insects, plants and people. In: Bryan JE, Shearman PL (eds) The State of Forests of Papua New Guinea: Measuring Change over the Period 2002–2014. University of Papua New Guinea, Port Moresby, pp 71–85

    Google Scholar 

  • Pellissier L, Roger A, Bilat J, Rasmann S (2014) High elevation Plantago lanceolata plants are less resistant to herbivory than their low elevation conspecifics: is it just temperature? Ecography 37:950–959

    Google Scholar 

  • Perrigo A, Hoorn C, Antonelli A (2020) Why mountains matter for biodiversity. J Biogeogr 47:315–325

    Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, Team RDC (2019) nlme: Linear and Nonlinear Mixed Effects Models. R package version 31–140, https://CRANR-projectorg/package=nlme

  • Rasmann S, Pellissier L, Defossez E, Jactel H, Kunstler G (2014) Climate-driven change in plant–insect interactions along elevation gradients. Funct Ecol 28:46–54

    Google Scholar 

  • Ratnasingham S, Hebert PD (2007) BOLD: The Barcode of Life Data System (http://www. barcodinglife. org). Mol Ecol Resour 7:355–364

    CAS  Google Scholar 

  • Ratnasingham S, Hebert PD (2013) A DNA-based registry for all animal species: the Barcode Index Number (BIN) system. PloS One 8:e66213

    PubMed  PubMed Central  CAS  Google Scholar 

  • Richards LA, Dyer LA, Forister ML, Smilanich AM, Dodson CD, Leonard MD, Jeffrey CS (2015) Phytochemical diversity drives plant–insect community diversity. Proc Natl Acad Sci U S A 112:10973–10978

    PubMed  PubMed Central  CAS  Google Scholar 

  • Roslin T, Salminen JP (2008) Specialization pays off: contrasting effects of two types of tannins on oak specialist and generalist moth species. Oikos 117:1560–1568

    Google Scholar 

  • Salgado AL, Suchan T, Pellissier L, Rasmann S, Ducrest A-L, Alvarez N (2016) Differential phenotypic and genetic expression of defence compounds in a plant–herbivore interaction along elevation. R Soc Open Sci 3:160226

    PubMed  PubMed Central  Google Scholar 

  • Salminen JP (2014) The chemistry and chemical ecology of ellagitannins in plant–insect interactions: from underestimated molecules to bioactive plant constituents. Recent Adv Polyphenol Res 4:83–113

    CAS  Google Scholar 

  • Salminen JP, Karonen M (2011) Chemical ecology of tannins and other phenolics: we need a change in approach. Funct Ecol 25:325–338

    Google Scholar 

  • Sam K et al (2020) Insect herbivory and herbivores of Ficus species along a rainforest elevational gradient in Papua New Guinea. Biotropica. https://doi.org/10.1111/btp.12741

  • Sam K, Koane B, Bardos DC, Jeppy S, Novotny V (2019) Species richness of birds along a complete rain forest elevational gradient in the tropics: Habitat complexity and food resources matter. J Biogeogr 46:279–290

  • Segar ST et al (2017a) Variably hungry caterpillars: predictive models and foliar chemistry suggest how to eat a rainforest. Proc R Soc Lond B Biol Sci 284:20171803

  • Segar ST et al (2017b) Speciation in a keystone plant genus is driven by elevation: a case study in New Guinean Ficus. J Evol Biol 30:512–523

  • Shanahan M, So S, G GS, RICHARD G (2001) Fig-eating by vertebrate frugivores: a global review. Biol Rev 76:529–572

  • Sourakov A, Emmel TC (2001) On the toxic diet of day-flying moths in the Solomon Islands (Lepidoptera: Arctiidae). Trop Lepidoptera Res 12:5–6

    Google Scholar 

  • Souto-Vilarós D et al (2018) Pollination along an elevational gradient mediated both by floral scent and pollinator compatibility in the fig and fig‐wasp mutualism. J Ecol 106:2256–2273

    Google Scholar 

  • Souto-Vilarós D et al (2019) Faster speciation of fig‐wasps than their host figs leads to decoupled speciation dynamics: snapshots across the speciation continuum. Mol Ecol 28:3958–3976

  • Stærk D, Christensen J, Lemmich E, Duus J, Olsen CE, Jaroszewski JW (2000) Cytotoxic activity of some phenanthroindolizidine N-oxide alkaloids from Cynanchum vincetoxicum. J Nat Prod 63:1584–1586

    PubMed  Google Scholar 

  • Tallowin O, Allison A, Algar AC, Kraus F, Meiri S (2017) Papua New Guinea terrestrial-vertebrate richness: elevation matters most for all except reptiles. J Biogeogr 44:1734–1744

    Google Scholar 

  • Ter Braak CJ, Smilauer P (2012) Canoco Reference Manual and User’s Guide: Software for Ordination (version 5.0). Microcomputer Power, Ithaca

    Google Scholar 

  • Toussaint EF, Sagata K, Surbakti S, Hendrich L, Balke M (2013) Australasian sky islands act as a diversity pump facilitating peripheral speciation and complex reversal from narrow endemic to widespread ecological supertramp. Ecol Evol 3:1031–1049

    PubMed  PubMed Central  Google Scholar 

  • Volf M et al (2018) Community structure of insect herbivores is driven by conservatism, escalation and divergence of defensive traits in Ficus. Ecol Lett 21:83–92

    PubMed  Google Scholar 

  • Volf M, Hrcek J, Julkunen-Tiitto R, Novotny V (2015) To each its own: differential response of specialist and generalist herbivores to plant defence in willows. J Anim Ecol 84:1123–1132

    PubMed  Google Scholar 

  • Volf M, Salminen J-P, Segar ST (2019) Evolution of defences in large tropical plant genera: perspectives for exploring insect diversity in a tri-trophic context. Curr Opin Insect Sci 32:91–97

    PubMed  Google Scholar 

  • Whitfeld TJ, Weiblen GD (2010) Five New Ficus Species (Moraceae) from Melanesia. Harv Pap Bot 15:1–11

    Google Scholar 

  • Wilson JJ (2012) DNA barcodes for insects. In: Kress WJ, Erickson DL (eds) DNA Barcodes: Methods and Protocols. Springer, New York, pp 17–46

    Google Scholar 

  • Xiang Y, Abliz Z, Li L, Xs H, Yu Ss (2002) Study of structural characteristic features of phenanthriondolizidine alkaloids by fast atom bombardment with tandem mass spectrometry. Rapid Commun Mass Spectrom 16:1668–1674

Download references

Acknowledgements

We thank the staff of the New Guinea Binatang Research Centre in Papua New Guinea, especially Bradley Gewa and Grace Luke, for their assistance and Nicholas Silverson and Julia Englund at the Smithsonian who harvested most of the Lepidoptera for sequencing at the Biodiversity Institute of Ontario, as part of the International Barcode of Life project. MV acknowledges funding from Czech Academy of Sciences, and Programme for Research and Mobility Support of Starting Researchers (MSM200962004), Alexander von Humboldt Foundation and the Federal Ministry for Education and Research (Ref.3.3-CZE-1192673-HFST-P), and Grant Agency of the Czech Republic 20-10543Y. KS acknowledges the ERC grant BABE 805189. FV acknowledges support by the Grant Agency of the University of South Bohemia (GAJU n. 048/2019/P). JPS acknowledges funding from the Academy of Finland (grant no 258992), and the help of Saku Valkamaa, Atte Tuominen, Anne Koivuniemi, and Valtteri Virtanen in the chemical analyses. VN acknowledges the ESF grant 669609 and Grant Agency of the Czech Republic 17-23862S and 19-28126X. STS acknowledges funding from a USB Postdoc project reg.no. CZ.1.07/2.3.00/30.0006 (funded by the European Social Fund and the Czech State Budget) and Grant Agency of the Czech Republic 15-24571S. He also acknowledges departmental support from Harper Adams University. We thank the Papua New Guinea Forest Research Institute, in particular Kipiro Damas, for assistance granting export permits.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Martin Volf.

Electronic supplementary material

ESM 1

(DOCX 14 kb)

ESM 2

(PDF 313 kb)

ESM 3

(PDF 4660 kb)

ESM 4

(DOCX 25 kb)

ESM 5

(DOCX 46 kb)

ESM 6

(DOCX 73 kb)

ESM 7

(DOCX 26 kb)

ESM 8

(DOCX 114 kb)

ESM 9

(DOCX 20.7 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Volf, M., Laitila, J.E., Kim, J. et al. Compound Specific Trends of Chemical Defences in Ficus Along an Elevational Gradient Reflect a Complex Selective Landscape. J Chem Ecol 46, 442–454 (2020). https://doi.org/10.1007/s10886-020-01173-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-020-01173-7

Keywords

Navigation