, Volume 51, Issue 1, pp 27–36 | Cite as

Tropical rainforests as dynamic symbiospheres of life



The remote Tiputini-Yasuni tropical forest region of the northwest Amazon (eastern Ecuador) represents a rich biodiversity likely unsurpassed anywhere else on earth. The myriad ecosystems, habitats and organisms are embedded in layers of symbiotic expressions. This region and particularly its Tiputini Biodiversity Station operated by the Universidad San Francisco de Quito offer unique and significant opportunities for symbiosis research and needed habitat conservation support. The centrality of symbioses in tropical rainforests is discussed through a review of selected literature and based on recent first-hand field experiences.


Tropical rainforest ecology Symbiosis Tiputini Biodiversity Yasuni Conservation biology Northwest Amazon ecosystems 


  1. Anthony PA, Holtum JAM, Jackes BR (2002) Shade acclimation of rainforest leaves to colonization by lichens. Funct Ecol 16(6):808–816CrossRefGoogle Scholar
  2. Aproot A (2001) Lichenized and saprobic fungal biodiversity of a single Elaeocarpus tree in Papua, New Guinea, with the report of 200 species of ascomycetes associated with one tree. Fungal Divers 6:1–11Google Scholar
  3. Aristizabel, C., Ribera, E.L., and Janos, D.P. 2004. Arbuscular mycorrhizae fungi colonizing decomposing leaves of Myrica parvifolia, M. pubescens, and Paepalanthus sp. Mycorrhiza 14(4): 221–228.Google Scholar
  4. Bass, M., Finer, M., Jenkins, C.N., Kreft, H., Cisneros-Heredia, D.F., McCracken, S., Pitman, N.C., English, P.H., Swing, K., Villa, G., DiFiore, A., Voigt, C.C., and Kunz, T. 2010. PLoS Biology, 5:1 e8767.
  5. Bentley BJ (1977) Extrafloral nectaries and protection by pugnacious bodyguards. Annu Rev Ecol Syst 8:407–427CrossRefGoogle Scholar
  6. Benzing DH (1998) Vulnerabilities of tropical forests to climate change: The significance of resident epiphytes. Climatic Change 39(2–3):519–540CrossRefGoogle Scholar
  7. Blüthgen N, Verhaugh M, Goitia W, Morawetz KJW, Barthlott W (2000) How plants shape the ant community in the Amazonian rainforest canopy: The key role of extrafloral nectaries and Homopteran honeydew. Oecologia 125(2):229–240CrossRefGoogle Scholar
  8. Blüthgen N, Fiedler K (2004) Competition for composition: Lessons from nectar-feeding ant communities. Ecology 85(8):1479–1485CrossRefGoogle Scholar
  9. Bourguignon T, Sobotnik J, Lepoint G, Martin JM, Roisin Y (2009) Niche differentiation among neotropical soldierless soil-feeding termites as revealed by stable isotope ratios. Soil Biol Biochem 41:2038–2043CrossRefGoogle Scholar
  10. Brauman A, Kane MD, Labat M, Breznak J (1992) Genesis of acetate and methane by gut bacteria of nutritionally diverse termites. Science 257:1384–1388CrossRefPubMedGoogle Scholar
  11. Breznak J (1982) Intestinal microbiota of termites and other xylophagous insects. Annu Rev Microbiol 36:323–343CrossRefPubMedGoogle Scholar
  12. Burnham RJ, Johnson KR (2004) South American paleobotany and the origins of neotropical forests. Philos Trans Biol Sci 359(1450):1595–1610CrossRefGoogle Scholar
  13. Bush MB (2000) Ecology of a Changing Planet, 2nd edn. New Jersey, Prentice-HallGoogle Scholar
  14. Cafaro MJ, Currie C (2005) Phylogenic analysis of mutualistic filamentous bacteria associated with fungus-growing ants. Can J Microbiol 51(6):441–446CrossRefPubMedGoogle Scholar
  15. Carpenter EJ (1992) Nitrogen fixation in the epiphyllae and root nodules of trees in the lowland tropical rainforest of Costa Rica. ACTA Oecologica Int J Ecol 13(2):153–160Google Scholar
  16. Cherrett JM (1972) Some factors involved in the selection of vegetable substrate by Atta cephalotes (L.) (Hymenoptera: Formicidae) in tropical rainforest. J Anim Ecol 41(3):647–660CrossRefGoogle Scholar
  17. Cornelissen JHC, Lang SI, Soudzilovskaia NA, During HJ (2007) Comparative cryptogam ecology: A review of bryophyte and lichen traits that drive biogeochemistry. Ann Bot 99:987–1001CrossRefPubMedGoogle Scholar
  18. Currie C (2001) A community of ants, fungi, and bacteria: A multilateral approach to studying symbiosis. Annu Rev Microbiol 55:357–380CrossRefPubMedGoogle Scholar
  19. Dejean A, Solano PJ, Ayroles J, Corbara B, Orivel J (2005) Arboreal ants build traps to capture prey. Nature 434:972CrossRefGoogle Scholar
  20. Defossez, E., Selosse, M.A., Dubois, M.P., Mondolot, l., Faccio, A., Dileto-Lordon, C., McKey, D., and Blatrix, R. 2009. New Phytologist 182: 942–949.Google Scholar
  21. Diaye DN, Duponnois R, Braumann A, Lepage M (2003) Impact of a soil feeding termite. Cubitermes niokoloensis on the symbiotic microflora associated with a fallow leguminous plant Crotalaria ochroleuca. Biol Fertil Soils 37:313–318Google Scholar
  22. Dixon RK (1994) Carbon pools and flux of global forest ecosystems. Science 263:185–190CrossRefPubMedGoogle Scholar
  23. Dominguez-Bello MG, Michelangeli F, Ruiz MC, Garcia A, Rodriguez E (1994) Ecology of the folivorous hoatzin (Opisthocomus hoazin on the Venezuelan plains. The Auk 111(3):643–651Google Scholar
  24. Donovan SE, Eggleton P, Dubbin WE, Batchelder M, Dubog L (2001) The effect of a soil-feeding termite, Cubitermes fungifaber (Isoptera: Termitidae) on soil properties: termites may be an important source of soil microhabitat heterogeneity in tropical forests. Pedobiologica 45:1–11CrossRefGoogle Scholar
  25. Edwards DP, Frederickson ME, Shepard GH, Yu DW (2009) Natural history note: A plant needs ants like a dog needs fleas: Mymelachista schumanni ants gall many tree species to create housing. Am Nat 175(5):734–740CrossRefGoogle Scholar
  26. Eilmus S, Heil M (2009) Bacterial associates of arboreal ants and their putative functions in an obligate ant-plant mutualism. Appl Environ Microbiol 75(13):4324–4332CrossRefPubMedGoogle Scholar
  27. Fiala B, Linsenmair KE (2004) Distribution and abundance of plants with extrafloral nectaries in the woody flora of as lowland primary forest in Malaysia. Biodivers Conserv 4(2):165–182CrossRefGoogle Scholar
  28. Finer, M., Vijay, V., Ponce, F., Jenkins, C.N., and Kahn, T.R. 2009. Ecuador’s Yasuni biosphere reserve: a brief modern history and conservation challenges. Environmental Research Letters 4(3)Google Scholar
  29. Frederickson ME, Gordon DM (2007) Devil to pay: accost of mutualism with Myrmelachista schumanni ants in “devils’ gardens” is increased herbivory on Duroia hirsuta trees. Proc R Soc B 274:1117–1123CrossRefPubMedGoogle Scholar
  30. Frederickson ME, Gordon DM (2009) The intertwined population biology of two Amazonian myrmecophytes and their symbiotic ants. Ecology 90(6):1595–1607CrossRefPubMedGoogle Scholar
  31. Frederickson ME, Greene MJ, Gordon DM (2005) “Devil’s Gardens” bedeviled by ants. Nature 437:495–496CrossRefPubMedGoogle Scholar
  32. Freiberg M, Freiberg E (2000) Epiphyte diversity and biomass in the canopy of lowland and montane forests of Ecuador. J Trop Biol 16(5):673–688CrossRefGoogle Scholar
  33. Forman RTT (1975) Canopy lichens with blue-green algae: A nitrogen source in a Colombian rainforest. Ecology 56:1176–1184CrossRefGoogle Scholar
  34. Freymann BP, Buitenwerf R, Desouza O, Olff H (2008) The importance of termites (Isoptera) for the recycling of herbivore dung in tropical ecosystems: a review. Eur J Entomol 105:165–173Google Scholar
  35. Godoy-Vitorino F, Ley RE, Gao Z, Pei Z, Ortiz-Zuazaga H, Pericchi LR, Garcia-Amado MA, Michelangeli F, Blaser MJ, Gordon JI, Dominguez-Bello MG (2008) Bacterial community in the crop of the hoatzin, a neotropical folivorous flying bird. Appl Environ Microbiol 74:5905–5912CrossRefPubMedGoogle Scholar
  36. Grajal A (1995) Structure and function of the digestive tract of the hoatzin (Opisthocomus hoazin): A folivorous bird with foregut fermentation. The Auk 122(1):20–28Google Scholar
  37. Harrison RD (2003) Fig wasp dispersal and the stability of a keystone plant resource in Borneo. Proc Biol Soc 270(supplement):s76–s79CrossRefGoogle Scholar
  38. Harrison RD (2005) Figs and the diversity of tropical rainforests. Bioscience 55(12):1053–1064CrossRefGoogle Scholar
  39. Hauck M (2009) Global warming and alternative causes of decline in arctic-alpine and boreal-montane lichens in northwestern Central Europe. Glob Change Biol 15(11):2653–2661CrossRefGoogle Scholar
  40. Hedin LO, Brookshire ENJ, Menge DNL, Barron AR (2009) The nitrogen paradox in tropical forest ecosystems. Annu Rev Ecol Evol Syst 40:613–635CrossRefGoogle Scholar
  41. Herre EA, Charlotte Handér K, Machado CA (2008) Evolutionary ecology of figs and their associates: Recent progress and outstanding puzzles. Annu Rev Ecol Sys 39:439–458CrossRefGoogle Scholar
  42. Husband R, Herre EA, Turner SL, Gallery R, Young PW (2002) Molecular diversity of arbuscular mycorrhizal fungi and patterns of host association over time and space in a tropical forest. Mol Ecol 11:2669–2678CrossRefPubMedGoogle Scholar
  43. Janos DP (1980) Mycorrhizae influence tropical succession. Biotropica 12(2):55–64CrossRefGoogle Scholar
  44. Janos DP (1987) Tropical mycorrhizas, nutrient cycles, and plant growth. In: Sutton EL, Whitmore TC, Chadwick AC (eds) Tropical Rainforest: Ecology and Management. Blackwell Scientific, Oxford, pp 317–345Google Scholar
  45. Janos DP (1993) Vesicular-Arbuscular mycorrhizae of epiphytes. Mycorrhiza 4(1):1–4CrossRefGoogle Scholar
  46. Janos DP, Sahley CT, Emmons LH (1995) Rodent dispersal of vesicular-arbuscular mycorrhizal fungi in Amazonian Peru. Ecology 76(6):1852–1858CrossRefGoogle Scholar
  47. Janzen DH (1979) How to be a fig. Annu Rev Ecol Syst 10:13–51CrossRefGoogle Scholar
  48. Kaufmann S, McKey DB, Hossaert-McKey M, Horvitz CC (1991) Adaptations for a Two-Phase seed dispersal system involving vertebrates and ants in a hemi-epiphytic fig (Ficus microcarpa, Moraceae). Am J Bot 78(7):971–977CrossRefGoogle Scholar
  49. Keeler KH (1977) The extrafloral nectaries of Ipomoea carnea (Convolvulaceae). Am J Bot 64(10):1182–1188CrossRefGoogle Scholar
  50. Kreft H, Koster N, Kuper W, Nieder J, Barthlott W (2004) Diversity and biogeography of vascular epiphytes in western Amazonia, Yasuni, Ecuador. Jourmal Biogeogr 31(9):1463–1476CrossRefGoogle Scholar
  51. Lakatos M, Lange-Bertalot H, Budel B (2004) Diatoms living inside the thallus of the green algal lichen Coenogonium linkii in neotropical lowland rainforests. J Phycol 40(1):70–73CrossRefGoogle Scholar
  52. Langley JA, Hungate B (2003) Mycorrhizal controls on belowground litter quality. Ecology 84(9):2302–2312CrossRefGoogle Scholar
  53. Lattman H, Milberg P, Palmer MW, Mattsson JE (2009) Changes in the distributions of epiphytic lichens in southern Sweden using a new statistical method. Nord J Bot 27(5):413–418CrossRefGoogle Scholar
  54. Lesica P, Antibus RK (1990) The occurrence of mycorrhizae in vascular epiphytes of two Costa Rican rainforests. Biotropica 22(3):250–258CrossRefGoogle Scholar
  55. Libralato S, Christiensen V, Pauly D (2006) A method for identifying keystone species in food web models. Ecol Model 195(3–4):153–171CrossRefGoogle Scholar
  56. Little AE, Currie CR (2007) Symbiotic complexity: discovery of a fifth symbiont in the attine ant-microbe symbiosis. Biol Lett 3:501–4CrossRefPubMedGoogle Scholar
  57. Little AE, Currie CR (2008) Indirect interaction web reveals how black yeast symbionts compromise the efficiency of antibiotic defenses in fungus-growing ants. Ecology 89:1216–1222CrossRefPubMedGoogle Scholar
  58. Lovelock CE, Wright SE, Clark DA, Ruess RW (2004) Soil stocks of glomalin produced by arbuscular mycorrhizal fungi across a tropical forest landscape. J Ecol 92:278–287CrossRefGoogle Scholar
  59. Lucking R, Matzer M (2001) High folicolous lichen alpha-diversity on individual leaves in Costa Rica and Amazonian Ecuador. Biodivers Conserv 10(12):2139–2152CrossRefGoogle Scholar
  60. Malhi Y, Roberts T, Betts R, Killeen T, Li W (2009) Climate change, deforestation, and the fate of the Amazon. Science 319:169–172CrossRefGoogle Scholar
  61. Mandl, N., Lehnert, M., Kessler, M., and Gradstein, S.R. 2010. A comparison of alpha and beta diversity patterns of ferns, bryophytes, and macrolichens in tropical montane forests of southern Ecuador. Biodiversity Conservation 1572–9710 (Online), doi:10.1007/s10531-010-9839-4.
  62. McKey D (1994) Legumes and nitrogen: the evolutionary ecology of a nitrogen-demanding lifestyle. In: Sprent JL, McKey D (eds) Advances in Legume Systematics: Part 5—The Nitrogen Factor. Royal Botanic Gardens, Kew, England, pp 211–228Google Scholar
  63. Moreira FMS, Haukka K, Young JPW (1998) Biodiversity of Rhizobia isolated from a wide range of legumes in Brazil. Mol Ecol 7:889–895CrossRefPubMedGoogle Scholar
  64. Moutinho P, Nepstad DC, Davidson EA (2003) Influence of leaf-cutting ant nests on secondary forest growth and soil properties of Amazonia. Ecology 84(5):1265–1276CrossRefGoogle Scholar
  65. Onguene NA, Kuyper TW (2001) Mycorrhizal associations in the rainforest of South Cameroon. For Ecol Manage 140(2–3):277–287CrossRefGoogle Scholar
  66. Opik M, Moora, Zobel M, Saks U, Wheatley R, Wright F, Daniell T (2008) High diversity of arbuscular mycorrhizal fungi in a boreal herb-rich forest. New Phytol 179:867–876CrossRefPubMedGoogle Scholar
  67. Orme CDL, Davies RG, Burgess M, Eigenbrod F, Pickup N (2005) Global hotspots of species richness are not congruent with endemism or threat. Nature 436:1016–1019CrossRefPubMedGoogle Scholar
  68. Pinoklyo A, Singh KP, Singh JS (2006) Leaf-colonizing lichens: their diversity, ecology, and future prospects. Curr Sci 90(4):509–518Google Scholar
  69. Pitman NCA, Terborgh JW, Silman MR, Núñez PV, Neill DA, Cerón CE, Palacios WA, Aulestia M (2001) Dominance and distribution of tree species in upper Amazonian terra firme forests. Ecology 82(8):2101–2117CrossRefGoogle Scholar
  70. Pons TL, Perreijn K, van Kessel C, Werger MJA (2007) Symbiotic nitrogen fixation in a tropical rainforest: 15N natural abundance measurements supported by experimental isotopic enrichment. New Phytol 173:154–167CrossRefPubMedGoogle Scholar
  71. Porras-Alfaro A, Bayman P (2007) Mycorrhizal fungi of Vanilla: diversity, specificity, and effects on seed germination and plant growth. Mycologia 99(4):510–525CrossRefPubMedGoogle Scholar
  72. Powell C (1980) Mycorrhizal infectivity of eroded soils. Soil Biol Biochem 12:247–250CrossRefGoogle Scholar
  73. Reddell P, Spain AV, Hopkins M (1997) Dispersal of spores of mycorrhizal fungi in scats of native mammals in tropical forests of northern Australia. Biotropica 29(2):184–192CrossRefGoogle Scholar
  74. Reed SC, Cleveland CC, Townsend AR (2008) Tree species control rates of free-living nitrogen fixation in a tropical rainforest. Ecology 89(10):2924–2934CrossRefPubMedGoogle Scholar
  75. Rex K, Kelm DH, Detlev H, Weisner K, Kunz TH, Voigt CC (2008) Species richness and structure of three neotropical bat assemblages. Biol J Linn Soc 94(3):617–629CrossRefGoogle Scholar
  76. Rillig MC, Wright SF, Nichols KA, Schmidt WF, Torn MS (2001) Large contribution of arbuscular mycorrhizal fungi to soil carbon pools in tropical forests. Plant Soil 233(2):167–177CrossRefGoogle Scholar
  77. Seaward MRD (1988) Contributions of lichens to ecosystems. In: Galun M (ed) CRC Handbook of Lichenology, volume 2. CRC Press, Florida, pp 107–129Google Scholar
  78. Shanahan M, Samson SO, Compton SG, Corlett R (2001) Fig-eating by vertebrate frugivores: A global review. Biol Rev 76:529–572PubMedGoogle Scholar
  79. Smith N, Mori SA, Henderson A, Stevenson DW, Heald SV (2004) Flowering Plants of the Neotropics. Princeton University Press, New Jersey, p xviiiGoogle Scholar
  80. Solano PJ, Dejean A (2004) Ant-fed plants: comparison between three geophytic myrmecophytes. Biol J Linn Soc 83:433–439CrossRefGoogle Scholar
  81. Stark NM, Jordan CF (1978) Nutrient retention by the root mat of an Amazonian rainforest. Ecology 59(3):434–437CrossRefGoogle Scholar
  82. Stephenson AG (1982) The role of the extrafloral nectaries of Catalpa speciosa in limiting herbivory and increasing fruit production. Ecology 63(3):663–669CrossRefGoogle Scholar
  83. Valencia R, Condit R, Foster RB, Romoleroux K, Villa Munoz G (2004) Yasunı´ Forest Dynamics Plot, Ecuador. In: Losos EC, Leigh EG Jr (eds) Tropical forest diversity and dynamism: Findings from a large-scale plot network. University of Chicago Press, Chicago, pp 609–620Google Scholar
  84. Vasconcelos HL, Cherrett JM (1997) Leaf-cutting ants and early forest regeneration in Central Amazonia: Effects of herbivory on tree seedling establishment. J Trop Ecol 13(3):357–370CrossRefGoogle Scholar
  85. Vitousek PM, Cassman K, Cleveland C, Crews T, Field CB, Grimm NN, Howarth RW, Marino R, Martinelli L, Rastetter EN, Sprent J (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57(58):1–45CrossRefGoogle Scholar
  86. Weiblen GD (2002) How to be a fig wasp. Annu Rev Entomol 47:299–330CrossRefPubMedGoogle Scholar
  87. Wilke Ryder KT, Mertl AL, Traniello JFA (2007) Biodiversity below ground:Probing the subterranean ant fauna of Amazonia. Naturwissenschaften 94:725–731CrossRefGoogle Scholar
  88. Wojciechowski MF, Lavin M, Sanderson ML (2004) A phylogeny of legumes (Leguminosae) based on analysis of the plastid matK gene resolves many well-supported subclades within the family. Am J Bot 91:1846CrossRefGoogle Scholar
  89. Yu DW, Davidson DW (1997) Experimental studies of species specificity in Cecropia-ant relationships. Ecol Monogr 67(3):273–294Google Scholar
  90. Zhang MM, Poulsen M, Currie C (2007) Symbiont recognition of mutualistic bacteria by Acromyrex leaf-cutting ants. ISME J 1:313–320PubMedGoogle Scholar
  91. Zook DP (2001) Prioritizing symbiosis to sustain biodiversity: Are symbionts keystone species? In: Seckbach J (ed) Symbiotic Mechanisms. Kluwer, Dordrecht, pp 3–12Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  1. 1.Science Education and Global EcologyBoston UniversityBostonUSA

Personalised recommendations