Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-28T02:48:32.517Z Has data issue: false hasContentIssue false
  • English
  • Français

Nitrogen-fixing and non-fixing trees differ in leaf chemistry and defence but not herbivory in a lowland Costa Rican rain forest

Published online by Cambridge University Press:  27 August 2019

Benton N. Taylor Open the ORCID record for Benton N. Taylor [Opens in a new window]  and
Laura R. Ostrowsky
Benton N. Taylor*
Affiliation:
Smithsonian Environmental Research Center, 647 Contees Wharf Rd., Edgewater, MD, USA21037
Laura R. Ostrowsky
Affiliation:
Yale University, School of Forestry & Environmental Studies, 195 Prospect St., New Haven, CT, USA06511
*
*Author for correspondence: Benton N. Taylor, Email: bentonneiltaylor@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Nitrogen-fixing plants provide critical nitrogen inputs that support the high productivity of tropical forests, but our understanding of the ecology of nitrogen fixers – and especially their interactions with herbivores – remains incomplete. Herbivores may interact differently with nitrogen fixers vs. non-fixers due to differences in leaf nitrogen content and herbivore defence strategies. To examine these potential differences, our study compared leaf carbon, nitrogen, toughness, chemical defence and herbivory for four nitrogen-fixing tree species (Inga oerstediana, Inga sapindoides, Inga thibaudiana and Pentaclethra macroloba) and three non-fixing species (Anaxagorea crassipetala, Casearia arborea and Dipteryx panamensis) in a lowland tropical rain forest. Leaf chemical defence, not nutritional content, was the primary driver of herbivore damage among our species. Even though nitrogen fixers exhibited 21.1% higher leaf nitrogen content, 20.1% lower C:N ratios and 15.4% lower leaf toughness than non-fixers, we found no differences in herbivory or chemical defence between these two plant groups. Our results do not support the common hypotheses that nitrogen fixers experience preferential herbivory or that they produce more nitrogen-rich defensive compounds than non-fixers. Rather, these findings suggest strong species-specific differences in plant–herbivore relationships among both nitrogen-fixing and non-fixing tropical trees.

Keywords

Chemical leaf defenceherbivoryIngaleaf toughnessnitrogen fixationPentaclethra
Type
Research Article
Information
Journal of Tropical Ecology , Volume 35 , Issue 6 , November 2019 , pp. 270 - 279
Copyright
© Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature cited

Adams, MA, Turnbull, Tl, Sprent, JI and Buchmann, N (2016) Legumes are different: leaf nitrogen, photosynthesis, and water use efficiency. Proceedings of the National Academy of Sciences USA 113, 4098–4113.CrossRefGoogle ScholarPubMed
Agrawal, AA and Weber, MG (2015) On the study of plant defence and herbivory using comparative approaches: how important are secondary plant compounds? Ecology Letters 18, 985–991.CrossRefGoogle Scholar
Batterman, SA, Hedin, LO, Van Breugel, M, Ransijn, J, Craven, DJ and Hall, JS (2013a) Key role of symbiotic dinitrogen fixation in tropical forest secondary succession. Nature 502, 224–227.CrossRefGoogle ScholarPubMed
Batterman, SA, Wurzburger, N and Hedin, LO (2013b) Nitrogen and phosphorus interact to control tropical symbiotic N2 fixation: a test in Inga punctata. Journal of Ecology 101, 1400–1408.CrossRefGoogle Scholar
Bentley, BL (1977) Extrafloral nectaries and protection by pugnacious bodyguards. Annual Review of Ecology and Systematics 8, 407–427.CrossRefGoogle Scholar
Binkley, D and Giardina, C (1997) Nitrogen fixation in tropical forest plantations. ACIAR Monograph Series 43, 297–337.Google Scholar
Binkley, D, Cromack, K , Jr and Baker, D (1994) Nitrogen fixation by red alder: biology, rates, and controls. In Hibbs, DE, DeBell, DS and Tarrant, RF (eds), The Biology and Management of Red Alder. Corvallis, OR: Oregon State University Press, pp. 57–72.Google Scholar
Coley, PD (1983) Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecological Monographs 53, 209–234.CrossRefGoogle Scholar
Coley, PD (1986) Costs and benefits of defense by tannins in a neotropical tree. Oecologia 70, 238–241.CrossRefGoogle Scholar
Coley, PD and Barone, JA (1996) Herbivory and plant defenses in tropical forests. Annual Review of Ecology and Systematics 27, 305–335.CrossRefGoogle Scholar
Coley, PD and Kursor, T (1996) Anti-herbivore defenses of young tropical leaves: physiological constraints and ecological trade-offs. In Mulkey, SS, Chazdon, RL and Smith, AP (eds), Tropical Forest Plant Ecophysiology. New York, NY: Chapman & Hall, pp. 305–336.CrossRefGoogle Scholar
Doyle, JJ and Luckow, MA (2003) The rest of the iceberg: legume diversity and evolution in a phylogenetic context. Plant Physiology 131, 900–910.CrossRefGoogle Scholar
Dyer, LA (1995) Tasty generalists and nasty specialists? Antipredator mechanisms in tropical Lepidopteran larvae. Ecology 76, 1483–1496.CrossRefGoogle Scholar
Dyer, LA, Dodson, CD, Stireman, JO, Tobler, MA, Smilanich, AM, Fincher, RM and Letourneau, DK (2003a) Synergistic effects of three Piper amides on generalist and specialist herbivores. Journal of Chemical Ecology 29, 2499–2514.CrossRefGoogle ScholarPubMed
Dyer, LA, Dodson, CD and Gentry, G (2003b) A bioassay for insect deterrent compounds found in plant and animal tissues. Phytochemical Analysis 14, 381–388.CrossRefGoogle ScholarPubMed
Elser, JJ, Fagan, WF, Denno, RF, Dobberfuhl, DR, Folarin, A, Huberty, A, Interlandi, S, Kilham, SS, McCauley, E, Schulz, KL, Siemann, EH and Sterner, RW (2000) Nutritional constraints in terrestrial and freshwater food webs. Nature 408, 578–580.CrossRefGoogle ScholarPubMed
Fyllas, NM, Patiño, S, Baker, TR, Nardoto, GB, Martinelli, LA, Quesada, CA, Paiva, R, Schwarz, M, Horna, V, Mercado, LM, Santos, A, Arroyo, L, Jimenez, EM, Luizao, FJ, Neill, DA, Silva, N, Prieto, A, Rudas, A, Silviera, M, Vieira, ICG, Lopez-Gonzalez, G, Malhi, Y, Phillips, OL and Lloyd, J (2009) Basin-wide variations in foliar properties of Amazonian forest: phylogeny, soils and climate. Biogeosciences 6, 2677–2708.CrossRefGoogle Scholar
Gutschick, V (1981) Evolved strategies in nitrogen acquisition by plants. American Naturalist 118, 607–637.CrossRefGoogle Scholar
Hamilton, JG, Zangerl, AR, Delucia, EH and Berenbaum, MR (2001) The carbon-nutrient balance hypothesis: its rise and fall. Ecology Letters 4, 86–95.CrossRefGoogle Scholar
Hothorn, T, Bretz, F and Westfall, P (2008) Simultaneous Inference in General Parametric Models. Munich: University of Munich, pp. 4–9.Google ScholarPubMed
Houlton, BZ, Wang, Y-P, Vitousek, PM and Field, CB (2008) A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454, 327–30.CrossRefGoogle ScholarPubMed
Hulme, PE (2008) Herbivores and the performance of grassland plants: a comparison of arthropod, mollusc and rodent herbivory. Journal of Ecology 84, 43–51.CrossRefGoogle Scholar
Hungate, BA, Stiling, PD, Dijkstra, P, Johnson, DW, Ketterer, ME, Hymus, GJ, Hinkle, CR and Drake, BG (2004) CO2 elicits long-term decline in nitrogen fixation. Science 304, 1291.CrossRefGoogle ScholarPubMed
Karban, R and Baldwin, I (1997) Induced Responses to Herbivory. Chicago, IL: University of Chicago Press.CrossRefGoogle Scholar
King, D and Maindonald, J (1999) Tree architecture in relation to leaf dimensions and tree stature in temperate and tropical rain forest. Journal of Ecology 87, 1012–1024.CrossRefGoogle Scholar
Knops, JMH, Ritchie, ME and Tilman, D (2000) Selective herbivory on a nitrogen fixing legume (Lathyrus venosus) influences productivity and ecosystem nitrogen pools in an oak savanna. Ecoscience 7, 166–174.CrossRefGoogle Scholar
Lucas, PW and Pereira, B (1990) Estimation of the fracture toughness of leaves. Functional Ecology 4, 819–822.CrossRefGoogle Scholar
Mattson, W (1980) Herbivory in relation to plant nitrogen content. Annual Review of Ecology and Systematics 11, 119–161.CrossRefGoogle Scholar
McDade, L and Hartshorn, G (1994) La Selva: Ecology and Natural History of a Neotropical Rain Forest. Chicago, IL: University of Chicago Press.Google Scholar
McKey, D (1994) Legumes and nitrogen: The evolutionary ecology of a nitrogen-demanding lifestyle. In Sprent, J. and McKey, D (eds), Advances in Legume Systematics 5: The Nitrogen Factor. Kew, London: Royal Botanic Gardens, pp. 211–228.Google Scholar
Menge, DNL and Chazdon, RL (2016) Higher survival drives the success of nitrogen-fixing trees through succession in Costa Rican rainforests. New Phytologist 209, 965–977.CrossRefGoogle ScholarPubMed
Menge, DNL, Levin, SA and Hedin, LO (2008) Evolutionary tradeoffs can select against nitrogen fixation and thereby maintain nitrogen limitation. Proceedings of the National Academy of Sciences USA 105, 1573–1578.CrossRefGoogle ScholarPubMed
Menge, D, Lichstein, J and Angeles-Perez, G (2014) Nitrogen fixation strategies can explain the latitudinal shift in nitrogen-fixing tree abundance. Ecology 95, 2236–2245.CrossRefGoogle ScholarPubMed
Metcalfe, DB, Asner, GP, Martin, RE, Silva Espejo, JE, Huasco, WH, Farfan Amezquita, FF, Carranza-Jimenez, L, Galiano Cabrera, DF, Baca, LD, Sinca, F, Huaraca Quispe, LP, Taype, IA, Mora, LE, Davila, AR, Solorzano, MM, Puma Vilca, BL, Laupa Roman, JM, Guerra Bustios, PC, Revilla, NS, Tupayachi, R, Girardin, CAJ, Doughty, CE and Malhi, Y (2014) Herbivory makes major contributions to ecosystem carbon and nutrient cycling in tropical forests. Ecology Letters 17, 324–332.CrossRefGoogle ScholarPubMed
Myster, RW (2006) Light and nutrient effects on growth and allocation of Inga vera (Leguminosae), a successional tree of Puerto Rico. Canadian Journal of Forest Research 36, 1121–1128.CrossRefGoogle Scholar
Nasto, MK, Alvarez-Clare, S, Lekberg, Y, Sullivan, BW, Townsend, AR and Cleveland, CC (2014) Interactions among nitrogen fixation and soil phosphorus acquisition strategies in lowland tropical rain forests. Ecology Letters 17, 1282–1289.CrossRefGoogle ScholarPubMed
Poorter, L, Van De Plassche, M, Willems, S and Boot, RGA (2004) Leaf traits and herbivory rates of tropical tree species differing in successional status. Plant Biology 6, 746–754.CrossRefGoogle ScholarPubMed
Reich, P, Walters, M and Ellsworth, D (1992) Leaf life-span in relation to leaf, plant, and stand characteristics among diverse ecosystems. Ecological Monographs 62, 365–392.CrossRefGoogle Scholar
Ritchie, ME and Tilman, D (1995) Responses of legumes to herbivores and nutrients during succession on a nitrogen-poor soil. Ecology 76, 2648–2655.CrossRefGoogle Scholar
Ritchie, ME, Tilman, D and Knops, JMH (1998) Herbivore effects on plant and nitrogen dynamics in oak savanna. Ecology 79, 165–177.CrossRefGoogle Scholar
Schlesinger, W and Bernhardt, ES (2013) Biogeochemistry: An Analysis of Global Change (3rd edition). Oxford: Elsevier.Google Scholar
Sedio, BE, Parker, JD, McMahon, SM and Wright, SJ (2018) Comparative foliar metabolomics of a tropical and a temperate forest community. Ecology 99, 2647–2653.CrossRefGoogle Scholar
Simonsen, AK and Stinchcombe, JR (2014) Herbivory eliminates fitness costs of mutualism exploiters. New Phytologist 202, 651–661.CrossRefGoogle ScholarPubMed
Sprent, JI (2009) Legume Nodulation: A Global Perspective. Oxford: Wiley-Blackwell.CrossRefGoogle Scholar
ter Steege, H, Pitman, NCA, Phillips, OL, Chave, J, Sabatier, D, Duque, A, Molino, J-F, Prévost, M-F, Spichiger, R, Castellanos, H, Von Hildebrand, P and Vásquez, R (2006) Continental-scale patterns of canopy tree composition and function across Amazonia. Nature 443, 444–447.CrossRefGoogle ScholarPubMed
Swain, T (1977) Secondary compounds as protective agents. Annual Review of Plant Physiology 28, 479–501.CrossRefGoogle Scholar
Taylor, BN and Menge, DNL (2018) Light regulates tropical symbiotic nitrogen fixation more strongly than soil nitrogen. Nature Plants 4, 655–661.CrossRefGoogle ScholarPubMed
Taylor, BN, Chazdon, RL and Menge, DNL (2019) Successional dynamics of nitrogen fixation and forest growth in regenerating Costa Rican rainforests. Ecology 100, 1–13.CrossRefGoogle ScholarPubMed
Townsend, AR, Cleveland, CC, Asner, GP and Bustamante, MMC (2007) Controls over foliar N:P ratios in tropical rain forests. Ecology 88, 107–118.CrossRefGoogle Scholar
Vitousek, P and Field, C (1999) Ecosystem constraints to symbiotic nitrogen fixers: a simple model and its implications. Biogeochemistry 46, 179–202.CrossRefGoogle Scholar
Vitousek, P and Howarth, R (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13, 87–115.CrossRefGoogle Scholar
Vitousek, P, Cassman, K and Cleveland, C (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57, 1–45.CrossRefGoogle Scholar
Vitousek, PM, Menge, DNL, Reed, SC and Cleveland, CC (2013) Biological nitrogen fixation: rates, patterns and ecological controls in terrestrial ecosystems. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 368, 1–9.CrossRefGoogle ScholarPubMed
Weber, M, Porturas, L and Keeler, K (2015) World List of Plants with Extrafloral Nectaries. www.extrafloralnectaries.org.Google Scholar
Williams, A and Whitham, T (1986) Premature leaf abscission: an induced plant defense against gall aphids. Ecology 67, 1619–1627.CrossRefGoogle Scholar
Wolf, AA, Funk, JL and Menge, DNL (2017) The symbionts made me do it: legumes are not hardwired for high nitrogen concentrations but incorporate more nitrogen when inoculated. New Phytologist 213, 690–699.CrossRefGoogle Scholar
Wright, IJ, Reich, PB, Westoby, M, Ackerly, DD, Baruch, Z, Bongers, F, Cavender-Bares, J, Chapin, T, Cornelissen, JHC, Diemer, M, Flexas, J, Garnier, E, Groom, PK, Gulias, J, Hikosaka, K, Lamont, BB, Lee, T, Lee, W, Lusk, C, Midgley, JJ, Navas, M-L, Niinemets, U, Oleksyn, J, Osada, N, Poorter, H, Poot, P, Prior, L, Pyankov, VI, Roumet, C, Thomas, SC, Tjoelker, MG, Veneklaas, EJ and Villar, R (2004) The worldwide leaf economics spectrum. Nature 428, 821–827.CrossRefGoogle ScholarPubMed