Skip to main content
Log in

Fertilization influences the nutrient acquisition strategy of a nomadic vine in a lowland tropical forest understory

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aims

Tropical tree and lianas in the understory are limited by soil nutrients despite growing in extremely low light. It is not known if nomadic vines are also limited by nutrients in low light conditions.

Methods

We measured differences in root architecture and mycorrhizal colonization, and leaf nutrients of a nomadic vine, Philodendron fragrantissimum (Araceae), in nitrogen (N) and phosphorus (P) fertilization plots in a lowland tropical moist forest in central Panama to measure potential nutrient limitation.

Results

Relative to plants in control plots, leaf P concentration was 54% higher and leaf N concentration was 10% higher for plants in the P- and N-addition treatments, respectively. The N:P of leaves suggested P-limitation in the N-addition treatment and the control but not in the P-addition treatment. Root branching was highest in the P-addition treatment, and P-addition reduced mycorrhizal colonization.

Conclusions

The large effect of P fertilization suggests that, like many tropical plants, P. fragrantissimum has the potential to be P-limited. Although further study is needed, we suggest that nomadic vines be added to the growth forms that respond to nutrient addition in the forest understory and conclude that nutrient-limitation seems like the rule rather than the exception in the light-limited understory.

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
Fig. 4

Similar content being viewed by others

References

  • Arsenault JL, Pouleur S, Messier C, Guay R (1995) WinRhizo, a root measuring system with a unique overlap correction method. HortScience 30:906

    Google Scholar 

  • Balcázar-Vargas MP, Peñuela-Mora MC, van Andel TR, Zuidema PA (2012) The quest for a suitable host: size distributions of host trees and secondary hemiepiphytes search strategy. Biotropica 44:19–26

    Google Scholar 

  • Benner JW, Vitousek PM (2007) Development of a diverse epiphyte community in response to phosphorus fertilization. Ecol Lett 10:628–636

    PubMed  Google Scholar 

  • Benzing DH (1990) Vascular epiphytes. General biology and related biota. Cambridge University Press, Cambridge

    Google Scholar 

  • Bigelow SW (1993) Leaf nutrients in relation to stature and life form in tropical rain forest. J Veg Sci 4:401–408. https://doi.org/10.2307/3235599

    Article  Google Scholar 

  • Bloom AJ, Chapin FS III, Mooney HA (1985) Resource limitation in plants - an economic analogy. Annu Rev Ecol Evol Syst 16:363–392

    Google Scholar 

  • Burslem DFRP, Grubb PJ, Turner IM (1996) Responses to simulated drought and elevated nutrient supply among shade-tolerant tree seedlings of lowland tropical forest in Singapore. Biotropica 28:636–648

    Google Scholar 

  • Chapin FS III (1980) The mineral nutrition of wild plants. Annu Rev Ecol Evol Syst 11:233–260

    CAS  Google Scholar 

  • Chazdon RL, Fetcher N (1984) Light environments of tropical forests. In: Medina E, Mooney HA, Vásquez-Yanes C (eds) Physiol. Ecol. Plants Wet Trop. Dr. W. Junk Publishers, The Hague, pp 553–564

    Google Scholar 

  • Clark RB, Zeto SK (2000) Mineral acquisition by arbuscular mycorrhizal plants. J Plant Nutr 23:867–902

    CAS  Google Scholar 

  • Coley PD, Bryant JP, Chapin FS III (1985) Resource availability and plant antiherbivore defense. Science 230:895–900

    CAS  PubMed  Google Scholar 

  • Collins CG, Wright SJ, Wurzburger N (2016) Root and leaf traits reflect distinct resource acquisition strategies in tropical lianas and trees. Oecologia 180:1037–1047

    PubMed  Google Scholar 

  • Condit R, Engelbrecht BMJ, Pino D, Perez R, Turner BL (2013) Species distributions in responses to individual soil nutrients and seasonal drought across a community of tropical trees. Proc Natl Acad Sci 110:5064–5068

    CAS  PubMed  PubMed Central  Google Scholar 

  • Coomes DA, Grubb PJ (2000) Impacts of root competition in forests and woodlands: a theoretical framework and review of experiments. Ecol Monogr 70:171–207

    Google Scholar 

  • Cuevas E, Medina E (1988) Nutrient dynamics within Amazonian forests: fine root growth, nutrient availability, and leaf litter decomposition. Oecologia 76:222–235

    PubMed  Google Scholar 

  • D’Angelo E, Crutchfield J, Vandiviere M (2001) Rapid, sensitive, microscale determination of phosphate in water and soil. J Environ Qual 30:2206–2209

    PubMed  Google Scholar 

  • Drew MC (1975) Comparison of the effects of a localized supply of phosphate, nitrate, ammonium and potassium on the growth of the seminal root system, and the shoot, in barley. New Phytol 75:479–490

    CAS  Google Scholar 

  • Drew MC, Saker LR (1978) Nutrient supply and the growth of the seminal root system in barley. III. Compensatory increases in growth of lateral roots, and in rates of phosphate uptake in response to a localised supply of phosphate. J Exp Bot 29:435–451

    CAS  Google Scholar 

  • Dubuisson J-Y, Hennequin S, Bary S, Ebihara A, Boucheron-Dubuisson É (2011) Anatomical diversity and regressive evolution in the trichomanoid filmy ferns (Hymenophyllaceae): a phylogenetic approach. C R Biol 334:880–895

    PubMed  Google Scholar 

  • Eissenstat DM, Yanai RD (1997) The ecology of root lifespan. Adv Ecol Res 27:1–60

    Google Scholar 

  • Elser J, Bracken MES, Cleland EE et al (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142

    PubMed  Google Scholar 

  • Farley RA, Fitter AH (1999) The response of seven co-occuring woodland herbaceous perennials to localized nutrient-rich patches. J Ecol 87:849–859

    Google Scholar 

  • Fitter AH (1985) Functional significance of root morphology and root system architecture. In: Fitter AH, Atkinson D, Read DJ, Usher MB (eds) Ecol. Interact. soil. Blackwell Scientific Publications, Oxford, pp 87–106

    Google Scholar 

  • Fitter AH (1991) Costs and benefits of mycorrhizae: implications for functioning under natural conditions. Experientia 47:350–355

    Google Scholar 

  • Fitter AH, Williamson L, Linkohr B, Leyser O (2002) Root system architecture determines fitness in an Arabidopsis mutant in competition for immobile phosphate ions but not for nitrate ions. Proc R Soc London B 269:2017–2022

    CAS  Google Scholar 

  • Güsewell S (2004) N:P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266

    PubMed  Google Scholar 

  • Hättenschwiler S (2002) Liana seedling growth in response to fertilisation in a neotropical forest understorey. Basic Appl Ecol 3:135–143

    Google Scholar 

  • Hodge A (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol 162:9–24

    Google Scholar 

  • Holdridge LR, Budowski G (1956) Report on an ecological survey of the Republic of Panama. Caribb For 17:92–110

    Google Scholar 

  • Jackson RB, Manwaring JH, Caldwell MM (1990) Rapid physiological adjustment of roots to localized soil enrichment. Nature 344:58–60

    CAS  PubMed  Google Scholar 

  • Jones JB, Case BW (1996) Soil testing and plant analysis no. 3. In: Sparks DL (ed) Methods soil anal. Part 3 Chem. Methods. Soil Science Society of America, Madison, pp 389–415

    Google Scholar 

  • Kaspari M, Garcia MN, Harms KE, Santana M, Wright SJ, Yavitt JB (2008) Multiple nutrients limit litterfall and decomposition in a tropical forest. Ecol Lett 11:35–43

    PubMed  Google Scholar 

  • Koske RE, Gemma JN (1989) A modified procedure for staining roots to detect VA mycorrhizas. Mycol Res 92:486–505

    Google Scholar 

  • Lambers H, Raven JA, Shaver GR, Smith SE (2008) Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evol 23:95–103

    PubMed  Google Scholar 

  • LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379

    PubMed  Google Scholar 

  • Marschner P (2012) Mineral nutrition of wild plants, 3rd edn. Academic Press, San Diego

    Google Scholar 

  • Marschner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant Soil 159:89–102

    CAS  Google Scholar 

  • Mayor JR, Wright SJ, Turner BL (2014) Species-specific responses of foliar nutrients to long-term nitrogen and phosphorus additions in a lowland tropical forest. J Ecol 102:36–44. https://doi.org/10.1111/1365-2745.12190

    Article  CAS  Google Scholar 

  • McCormack ML, Dickie IA, Eissenstat DM et al (2015) Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes. New Phytol 207:505–518

    PubMed  Google Scholar 

  • McGonigle TP, Miller MH, Evans DG et al (1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115:495–501

    PubMed  Google Scholar 

  • Mirabello MJ, Yavitt JB, Garcia M, Harms KE, Turner BL, Wright SJ (2013) Soil phosphorus responses to chronic nutrient fertilisation and seasonal drought in a humid lowland forest, Panama. Soil Res 51:215–221

    CAS  Google Scholar 

  • Mirmanto E, Proctor J, Green J, Nagy L, Suriantata (1999) Effects of nitrogen and phosphorus fertilization in a lowland evergreen rainforest. Philos Trans R Soc Lond Ser B Biol Sci 354:1825–1829. https://doi.org/10.1098/rstb.1999.0524

    Article  CAS  Google Scholar 

  • Mo Q, Zou B, Li Y et al (2015) Response of plant nutrient stoichiometry to fertilization varied with plant tissues in a tropical forest. Sci Rep 5:1–12

    Google Scholar 

  • Moffett MW (2000) What’s “up”? A critical look at the basic terms of canopy biology. Biotropica 32:569–596

    Google Scholar 

  • Nielsen SL, Enríquez S, Duarte CM, Sand-Jensen K (1996) Scaling maximum growth rates across photosynthetic organisms. Funct Ecol 10:167–175

    Google Scholar 

  • Ostertag R (2001) Effects of nitrogen and phosphorus availability on fine-root dynamics in Hawaiian montane forests. Ecology 82:485–499

    Google Scholar 

  • Pasquini SC, Wright SJ, Santiago LS (2015) Lianas always outperform tree seedlings regardless of soil nutrients: results from a long-term fertilization experiment. Ecology 96:1866–1876

    PubMed  Google Scholar 

  • Putz FE, Holbrook NM (1986) Notes on the natural history of hemiepiphytes. Selbyana 9:61–69

    Google Scholar 

  • R Development Core Team (2009) R: A language and environment for statistical computing

  • Robinson D, Rorison IH (1983) A comparison of the responses of Lolium perenne L., Holcus lanatus L., and Deschampsia flexuosa (L.) Trin. To a localized supply of nitrogen. New Phytol 94:263–273

    Google Scholar 

  • Santiago LS, Wright SJ, Harms KE, Yavitt JB, Korine C, Garcia MN, Turner BL (2012) Tropical tree seedling growth responses to nitrogen, phosphorus and potassium addition. J Ecol 100:309–316

    CAS  Google Scholar 

  • Sayer EJ, Wright SJ, Tanner EVJ et al (2012) Variable responses of lowland tropical forest nutrient status to fertilization and litter manipulation. Ecosystems 15:387–400

    CAS  Google Scholar 

  • Schnitzer SA, Bongers F (2002) The ecology of lianas and their role in forests. Trends Ecol Evol 17:223–230

    Google Scholar 

  • Schnitzer SA, Kuzee ME, Bongers F (2005) Disentangling above- and below-ground competition between lianas and trees in a tropical forest. J Ecol 93:1115–1125

    Google Scholar 

  • Sheldrake M, Rosenstock NP, Revillini D, Olsson PA, Wright SJ, Turner BL (2017) A phosphorus threshold for mycoheterotrophic plants in tropical forests. Proc R Soc London B 284:20162093

    Google Scholar 

  • Soil Staff Survey (1999) Soil taxonomy: a basic system of soil classification for making and interpreting soil surveys

  • Stewart RH, Stewart JL, Woodring WP (1980) Geologic map of the Panama Canal and vicinity, Republic of Panama. U.S. Geol. Surv. Misc. Investig. Ser. Map I-232

  • Strong DR, Ray TS (1975) Host tree location behavior of a tropical vine (Monstera gigantea) by skototropism. Science 190:804–806

    Google Scholar 

  • Tanner EVJ, Kapos V, Franco W (1992) Nitrogen and phosphorus fertilization effects on Venezuelan montane forest trunk growth and litterfall. Ecology 73:78–86. https://doi.org/10.2307/1938722

    Article  Google Scholar 

  • Tibbet M (2000) Roots, foraging and the exploitation of soil nutrient patches: the role of mycorrhizal symbioses. Funct Ecol 14:397–399

    Google Scholar 

  • Toledo-Aceves T, Swaine MD (2008) Above- and below-ground competition between the liana Acacia kamerunensis and tree seedlings in contrasting light environments. Plant Ecol 196:233–244

    Google Scholar 

  • Treseder KK (2004) A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol 164:347–355. https://doi.org/10.1111/j.1469-8137.2004.01159.x

    Article  PubMed  Google Scholar 

  • Tripler CW, Kaushal SS, Likens GE, Walter MT (2006) Patterns in potassium dynamics in forest ecosystems. Ecol Lett 9:451–466

    PubMed  Google Scholar 

  • Turner BL, Yavitt JB, Harms KE, Garcia MN, Romero TE, Wright SJ (2013) Seasonal changes and treatment effects on soil inorganic nutrients following a decade of fertilization in a lowland tropical forest. Soil Sci Soc Am J 77:1357–1369

    CAS  Google Scholar 

  • van Vuuren MMI, Robinson D, Griffiths BS (1996) Nutrient inflow and root proliferation during the exploitation of a temporally and spatially discrete source of nitrogen in soil. Plant Soil 178:185–192

    Google Scholar 

  • Vitousek PM, Farrington H (1997) Nutrient limitation and soil development: experimental test of a biogeochemical theory. Biogeochemistry 37:63–75

    CAS  Google Scholar 

  • Wanek W, Zotz G (2011) Are vascular epiphytes nitrogen or phosphorus limited? A study of plant 15N fractionation and foliar N:P stoichiometry with the tank bromeliad Vriesea sanguinolenta. New Phytol 192:462–470

    CAS  PubMed  Google Scholar 

  • Wang L, Mou PP, Jones RH (2006) Nutrient foraging via physiological and morphological plasticity in three plant species. Can J For Res 36:164–173

    CAS  Google Scholar 

  • Williams-Linera G, Lawton RO (1995) The ecology of hemiepiphytes in forest canopies. In: Lowman MD, Nadkarni NM (eds) For. Canopies. Academic Press, New York, New York, pp 255–283

    Google Scholar 

  • Winkler U, Zotz G (2009) Highly efficient uptake of phosphorus in epiphytic bromeliads. Ann Bot 103:477–484

    CAS  PubMed  Google Scholar 

  • Woods CL, DeWalt SJ (2013) The conservation value of secondary forests for vascular epiphytes in Central Panama. Biotropica 45:119–127

    Google Scholar 

  • Wright SJ, Yavitt JB, Wurzburger N, Turner BL, Tanner EVJ, Sayer EJ, Santiago LS, Kaspari M, Hedin LO, Harms KE, Garcia MN, Corre MD (2011) Potassium, phosphorus, or nitrogen limit root allocation, tree growth, or litter production in a lowland tropical forest. Ecology 92:1616–1625

    PubMed  Google Scholar 

  • Wright SJ, Turner BL, Yavitt JB, Harms KE, Kaspari M, Tanner EVJ, Bujan J, Griffin EA, Mayor JR, Pasquini SC, Sheldrake M, Garcia MN (2018) Plant responses to fertilization experiments in lowland, species-rich, tropical forests. Ecology 99:1129–1138. https://doi.org/10.1002/ecy.2193

    Article  PubMed  Google Scholar 

  • Wurzburger N, Wright SJ (2015) Fine-root responses to fertilization reveal multiple nutrient limitation in a lowland tropical forest. Ecology 96:2137–2146

    PubMed  Google Scholar 

  • Yavitt JB, Wright SJ, Wieder RK (2004) Seasonal drought and dry-season irrigation influence leaf-litter nutrients and soil enzymes in a moist, lowland forest in Panama. Austral Ecol 29:177–188

    Google Scholar 

  • Yavitt JB, Harms KE, Garcia MN, Wright SJ, He F, Mirabello MJ (2009) Spatial heterogeneity of soil chemical properties in a lowland tropical moist forest, Panama. Aust J Soil Res 47:674–687

    CAS  Google Scholar 

  • Yavitt JB, Harms KE, Garcia MN et al (2011) Soil fertility and fine root dynamics in response to 4 years of nutrient (N, P, K) fertilization in a lowland tropical moist forest, Panama. Austral Ecol 36:433–445

    Google Scholar 

  • Zhu G, Yoh M, Gilliam FS et al (2013) Nutrient limitation in three lowland tropical forests in southern China receiving high nitrogen deposition: insights from the fine root responses to nutrient additions. PLoS One 8:e82661

    PubMed  PubMed Central  Google Scholar 

  • Zotz G (2013) “Hemiepiphyte”: confusing term and its history. Ann Bot 111:1015–1020

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors thank Mark Wagner for field support and data collection; Christina Wells for the use of her lab to conduct root mycorrhizal analyses as well as use of the WinRhizo program; and the Smithsonian Tropical Research Institute and Barro Colorado Island for logistical support. We thank G. Zotz and an anonymous reviewer for helpful comments and edits on previous versions of our manuscript. Funding for this research was provided by Clemson University and a Wade T. Batson award for field botany to CLW. Financial support for the Gigante Fertilization Project is provided by grants from the Andrew W. Mellon Foundation and the Smithsonian Scholarly Studies program.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Carrie L. Woods.

Additional information

Responsible Editor: Hans Lambers.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Woods, C.L., DeWalt, S.J., Cardelús, C.L. et al. Fertilization influences the nutrient acquisition strategy of a nomadic vine in a lowland tropical forest understory. Plant Soil 431, 389–399 (2018). https://doi.org/10.1007/s11104-018-3772-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-018-3772-9

Keywords

Navigation