Skip to main content
SpringerLink
Log in

How a non-pioneer tree attains the canopy of a tropical semideciduous forest

  • Original Article
  • Published:
Trees Aims and scope Submit manuscript

Abstract

Key message

A non-pioneer canopy tree having Aubréville architectural model overcomes seasonal water-light shortage alternation in tropical seasonal semideciduous forest with the same allometric shifts along the ontogeny as a rainforest tree.

Abstract

In tropical rainforests (TRF), the gap–understory gradient is occupied by a shade-tolerant/intolerant tree species continuum, and is among the main mechanisms explaining tree species distribution and coexistence. In tropical seasonal forests (TSF), the effects of gap formation are poorly known and are much subtler due to canopy deciduousness. In both forest types, light intensity increases from the ground to the canopy. We investigated whether the life-history pathway along the ontogeny of TRF shade-tolerant canopy trees holds true for a functionally similar TSF tree species. We identified seven ontogenetic stages in a population of Esenbeckia leiocarpa Engl. (Rutaceae): seedling, infant, juvenile, immature, vegetative adult, reproductive adult, and senile. Esenbeckia leiocarpa conforms to the Aubréville architectural model, which is well adapted to understory dimness. Little overlap in size was found among the different ontogenetic stages, indicating that changes in height and diameter play an important role along ontogeny. Seedlings responded to spatial variability in light, and other early stages exhibited plagiotropic branches and greater investment in height per unit of diameter as a strategy for resisting dimness. In the adults, the investment in diameter was greater, thus allowing the tree to support crown reiteration and reproductive structures and to resist wind forces and liana load. These findings show that the studied species has the same shade-tolerant strategy as tropical rainforest canopy species, and support the idea that light gradient in the forest profile is an important driver of canopy tree ontogeny.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Andrade P, Santos F, Martins F (2007) Size structure and fertility in an Eriocnema fulva Naudin (Melastomataceae) population in Southeastern Brazil. Braz J Biol 67:685–693

    Article  CAS  PubMed  Google Scholar 

  • Baker TR, Swaine MD, Burslem DF (2003) Variation in tropical forest growth rates: combined effects of functional group composition and resource availability. Perspect Plant Ecol Evol Syst 6:21–36

    Article  Google Scholar 

  • Bégin C, Filion L (1999) Black spruce (Picea marianna) architecture. Can J Bot 77:664–672

    Google Scholar 

  • Canham CD, Denslow JS, Platt WJ, Runkle JR, Spies TA, White PS (1990) Light regimes beneath closed canopies and tree-fall gaps in temperate and tropical forests. Can J For Res 20:620–631

    Article  Google Scholar 

  • Cielo-Filho R, Gneri MA, Martins FR (2007) Position on slope, disturbance, and tree species coexistence in a seasonal semideciduous forest in SE Brazil. Plant Ecol 190:189–203

    Article  Google Scholar 

  • Clark DA, Clark DB (1992) Life history diversity of canopy and emergent trees in a neotropical rain forest. Ecol Monogr 62:315–344

    Article  Google Scholar 

  • Cordero RA, Fetcher N, Voltzow J (2007) Effects of wind on the allometry of two species of plants in an elfin cloud forest. Biotropica 39:177–185

    Article  Google Scholar 

  • Franci LC, Pereira L, Machado RS, Haddad CRB, Martins FR (2015) Strategies of a light-demanding emergent tree to thrive in a neotropical seasonal forest with alternating light or water shortage. Braz J Bot 39:207–218. doi:10.1007/s40415-015-0211-5

    Article  Google Scholar 

  • Dean T, Long JN (1986) Validity of constant-stress and elastic instability principles of stem formation in Pinus contorta and Trifolium pratense. Ann Bot 58:833–840

    Google Scholar 

  • Ferreira-Fedele L, Tomazello-Filho M, Botosso P, Giannotti E (2004) Periodicidade do crescimento de Esenbeckia leiocarpa Engl. (guarantã) em duas áreas da região Sudeste do Estado de São Paulo. Sci Florest 65:141–149

    Google Scholar 

  • Fisher JB, Hibbs DE 1982 Plasticity of tree architecture: specific and ecological variations found in Aubreville’s model. Am J Bot:690–702

  • Frazer GW, Canham C, Lertzman K (1999) Gap Light Analyzer (GLA), Version 2.0: imaging software to extract canopy structure and gap light transmission indices from true-colour fisheye photographs, users manual and program documentation. Simon Fraser University, Burnaby, British Columbia, and the Institute of Ecosystem Studies, Millbrook, New York

  • Gandolfi S (2000) História natural de uma Floresta Estacional Semidecidual no município de Campinas (São Paulo, Brasil). PhD, Universidade Estadual de Campinas

  • Gandolfi S, Joly CA, Rodrigues RR (2007) Permeability-impermeability: canopy trees as biodiversity filters. Sci Agricol 64:433–438

    Article  Google Scholar 

  • Gandolfi S, Joly CA, Leitão Filho HDF (2009) “Gaps of deciduousness”: cyclical gaps in tropical forests. Sci Agricol 66:280–284

    Article  Google Scholar 

  • Gatsuk LE, Smirnova OV, Vorontzova LI, Zaugolnova LB, Zhukova LA (1980) Age states of plants of various growth forms: a review. J Ecol 68:675–696

    Article  Google Scholar 

  • Greig-Smith P (1983) Quantitative plant ecology. University of California Press, California

    Google Scholar 

  • Hallé F, Oldeman RAA, Tomlinson PB (1978) Tropical trees and forests: an architectural analysis. Springer, New York

    Book  Google Scholar 

  • Henry HA, Thomas SC (2002) Interactive effects of lateral shade and wind on stem allometry, biomass allocation, and mechanical stability in Abutilon theophrasti (Malvaceae). Am J Bot 89:1609–1615

    Article  PubMed  Google Scholar 

  • Hernandes JL, Pedro Júnior MJ, Bardin L (2004) Variação estacional na radiação solar em ambiente externo e no interior de floresta semidecídua. Revis Árvore 22:167–172

    Google Scholar 

  • Holbrook NM, Putz FE (1989) Influence of neighbors on tree form: effects of lateral shade and prevention of sway on the allometry of Liquidambar styraciflua (sweet gum). Am J Bot 76:1740–1749

    Article  Google Scholar 

  • Hutchings MJ (1997) The structure of plant populations. In: Crawley MJ (ed) Plant ecology, vol 2. Blackwell, London, pp 342–348

  • Iqbal RM, Rao AR, Rasul E, Wahid A (1997) Mathematical models and response functions in photosynthesis: an exponencial model. In: Pessaraki M (ed) Handbook of photosynthesis. Marcel Dekker Press, Inc., New York, pp 803–810

    Google Scholar 

  • IUSS Working Group WRB 2006. Working Group WRB (2007). World reference base for soil resources

  • King DA (1990) Allometry of saplings and understorey trees of a Panamanian forest. Funct Ecol 4:27–32

    Article  Google Scholar 

  • King DA (1996) Allometry and life history of tropical trees. J Trop Ecol 12:25–44

    Article  Google Scholar 

  • Kohyama T (1987) Significance of architecture and allometry in saplings. Funct Ecol 1:399–404

    Article  Google Scholar 

  • Kohyama T, Hotta M (1990) Significance of allometry in tropical saplings. Funct Ecol 4:515–521

    Article  Google Scholar 

  • Kohyama T, Suzuki E, Partomihardjo T, Yamada T, Kubo T (2003) Tree species differentiation in growth, recruitment and allometry in relation to maximum height in a Bornean mixed dipterocarp forest. J Ecol 91:797–806

    Article  Google Scholar 

  • Lorenzi H (1992) Árvores brasileiras: manual de identificação e cultivo de plantas arbóreas nativas do Brasil. Editora Plantarum

  • McLaren KP, McDonald MA (2003) The effects of moisture and shade on seed germination and seedling survival in a tropical dry forest in Jamaica. For Ecol Manag 183:61–75. doi:10.1016/S0378-1127(03)00100-2

    Article  Google Scholar 

  • McMahon T (1973) Size and shape in biology. Science 179:1201–1204

    Article  CAS  PubMed  Google Scholar 

  • Mello MDA, Pedro Junior M, Ortolani A, Alfonsi R (1994) Chuva e temperatura: cem anos de observações em Campinas. Instituto Agronômico de Campinas

  • Millet J (2012) L’architecture des arbres des régions tempérées: son histoire, ses concepts, ses usages. Les Éditions MultiMondes

  • Millet J, Bouchard A, Édelin C (1998) Plant succession and tree architecture: an attempt at reconciling two scales of analysis of vegetation dynamics. Acta Biotheor 46:1–22

    Article  Google Scholar 

  • Miquel S (1987) Morphologie fonctionelle de plantules d’especes forestières du Gabon. Bull Mus natn Hist nat Paris, ser 4:101–121

    Google Scholar 

  • Niklas KJ (1993) The scaling of plant height: a comparison among major plant clades and anatomical grades. Ann Bot 72:165–172

    Article  Google Scholar 

  • Niklas KJ (1994) Plant allometry—the scaling of form and process. The University of Chicago Press, Chicago

    Google Scholar 

  • Niklas KJ (1995) Size-dependent allometry of tree height, diameter and trunk-taper. Ann Bot 75:217–227

    Article  Google Scholar 

  • Nogueira A, Martinez C, Ferreira L, Prado C (2004) Photosynthesis and water use efficiency in twenty tropical tree species of differing succession status in a Brazilian reforestation. Photosynthetica 42:351–356

    Article  CAS  Google Scholar 

  • O’Brien ST, Hubbell SP, Spiro P, Condit R, Foster RB (1995) Diameter, height, crown, and age relationship in eight neotropical tree species. Ecology 76:1926–1939

    Article  Google Scholar 

  • Oldeman RAA (1979) Quelques aspects quantifiables de l’aborigenèse et de la sylvigenèse. Oecol Plant 14:289–312

    Google Scholar 

  • Peel MC, Finlayson BL, McMahon TA (2007) Updated world map of the Köppen–Geiger climate classification. Hydrol Earth Syst Sci 11:1633–1644

    Article  Google Scholar 

  • Pereira L (2011) Resistência a seca em plântulas de espécies arbóreas da Floresta Estacional Semidecídua. Master, Departamento de Biologia Vegetal. Universidade Estadual de Campinas (UNICAMP), p 70

  • Portela R, Santos F (2009) Mortality and mechanical damage of seedlings in different size fragments of the Brazilian Atlantic Forest. Trop Ecol 50:267–275

    Google Scholar 

  • Portes M, Alves T, Souza G (2008) Time-course of photosynthetic induction in four tropical woody species grown in contrasting irradiance habitats. Photosynthetica 46:431–440

    Article  CAS  Google Scholar 

  • Pulido F, Moreno G, García E, Obrador JJ, Bonal R, Díaz M (2014) Resource manipulation reveals flexible allocation rules to growth and reproduction in a Mediterranean evergreen oak. J Plant Ecol 7:77–85

    Article  Google Scholar 

  • Rahman L, Umeki K, Honjo T (2014) Modeling qualitative and quantitative elements of branch growth in saplings of four evergreen broad-leaved tree species growing in a temperate Japanese forest. Trees 28:1539–1552

    Article  Google Scholar 

  • Ressel K, Guilherme FA, Schiavini I, Oliveira PE (2004) Ecologia morfofuncional de plântulas de espécies arbóreas da Estação Ecológica do Panga, Uberlândia, Minas Gerais. Revista Brasileira de Botânica 27:311–323

    Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution:223–225

  • Rich PM, Helenurm K, Kearns D, Morse SR, Palmer MW, Short L (1986) Height and stem diameter relationships for dicotyledonous trees and arborescent palms of Costa Rican tropical wet forest. Bull Torrey Bot Club 113:241–246

    Article  Google Scholar 

  • Rosenberg MS (2001) PASSaGE: pattern analysis, spatial statistics, and geographic exegesis

  • R Core Team (2016). R: a language and environment for statistical computing. R Foundation for Statistical Computing. http://www.R-project.org

  • Sánchez-Humanes B, Sork VL, Espelta JM (2011) Trade-offs between vegetative growth and acorn production in Quercus lobataduring a mast year: the relevance of crop size and hierarchical level within the canopy. Oecologia 166:101–110

    Article  PubMed  Google Scholar 

  • Santos FAM (1997) Ancova33: Programa para cálculo de regressão e covariância. Versão 3.3. Universidade Estadual de Campinas

  • Santos K, Kinoshita LS, Santos FAM (2007) Tree species composition and similarity in semideciduous forest fragments of southeastern Brazil. Biol Conserv 135:268–277

    Article  Google Scholar 

  • Schnitzer SA, Carson WP (2001) Treefall gaps and the maintenance of species diversity in a tropical forest. Ecology 82:913–919

    Article  Google Scholar 

  • Seoane CES, Kageyama PK, Sebben AM (2000) Efeitos da fragmentação florestal na estrutura genética de populações de Esenbeckia leiocarpa Engl. (Guarantã). Sci Florest 57:123–139

    Google Scholar 

  • Smirnova O, Palenova M, Komarov A (2002) Ontogeny of different life forms of plants and specific features of age and spatial structure of their populations. Ontogenez 33(1):5–15

    CAS  PubMed  Google Scholar 

  • Souza RP, Válio IFM (2001) Seed size, seed germination, and seedling survival of brazilian tropical tree species differing in successional status. Biotropica 33:447–457

    Article  Google Scholar 

  • Souza AF, Martins FR, Matos DMS (2000) Detecting ontogenetic stages of the palm Attalea humilis in fragments of the Brazilian Atlantic forest. Can J Bot 78:1227–1237

    Google Scholar 

  • Souza AF, Martins FR, Bernacci LC (2003) Clonal growth and reproductive strategies of the understory tropical palm Geonoma brevispatha: an ontogenetic approach. Can J Bot 81:101–112

    Article  Google Scholar 

  • Sposito TC, Santos FAM (2001) Scaling of stem and crown in eight Cecropia (Cecropiaceae) species of Brazil. Am J Bot 88:939–949

    Article  CAS  PubMed  Google Scholar 

  • Sterck F, Bongers F (1998) Ontogenetic changes in size, allometry, and mechanical design of tropical rain forest trees. Am J Bot 85:266

    Article  CAS  PubMed  Google Scholar 

  • Sterck FJ, Bongers F, Newbery DM (2001) Tree architecture in a Bornean lowland rain forest: intraspecific and interspecific patterns. Plant Ecol 153:279–292

    Article  Google Scholar 

  • van Gelder HA, Poorter L, Sterck FJ (2006) Wood mechanics, allometry, and life-history variation in a tropical rain forest tree community. New Phytol 171:367–378

    Article  PubMed  Google Scholar 

  • Veloso HP (1992) Sistema fitogeográfico. Instituto Brasileiro de Geografia e Estatística

  • Vester HFM, Cleef AM (1998) Tree architecture and secondary tropical rain forest development: a case study in Araracuara, Colombian Amazonia. Flora 193:75–97

    Google Scholar 

  • Wilkinson L (1990) SYSTAT: the system for statisticians. SYSTAT INC, Evanston

    Google Scholar 

  • Yamada T, Yamakura T, Lee H (2000) Architectural and allometric differences among Scaphium species are related to microhabitat preferences. Funct Ecol 14:731–737

    Article  Google Scholar 

  • Zar JH (1999) Biostatistical analysis. Prentice-Hall, New York

    Google Scholar 

Download references

Acknowledgments

We thank the Condomínio Rural Colinas do Atibaia (Atibaia Hills Rural Condominium) for permission to work in the forest fragment. We thank Flavio A. M. dos Santos and Aneliza Almeida-Melo for providing materials and valuable comments on the manuscript. We thank Thiago L. da Mata for helping in the field. This research was supported by FAEPEX (University of Campinas Funding for Teaching, Research and Extension). A. G. Furtado received a scholarship from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Conselho Nacional de Pesquisa e Desenvolvimento Tecnológico (CNPq). L. P. Sims received a scholarship from the Mary Brown Foundation and Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP). F. R. Martins receives funding from CNPq, and L. C. Franci received a scholarship from CAPES.

Author information

Author notes

  1. Archimedes Grangeiro Furtado

    Present address: Instituto Nacional da Propriedade Industrial, Rua São Bento 1, Centro, Rio de Janeiro, RJ, 20090-010, Brazil

  2. Ligia Paulillo Sims

    Present address: Colégio Ideal, QNG9, Lote 1, Taguatinga, DF, 72130-090, Brazil

Authors and Affiliations

  1. Plant Biology Graduate Program, Institute of Biology, University of Campinas-UNICAMP, P.O. Box 6109, Campinas, SP, 13083-970, Brazil

    Archimedes Grangeiro Furtado

  2. Ecology Graduate Program, Institute of Biology, University of Campinas-UNICAMP, P.O. Box 6109, Campinas, SP, 13083-970, Brazil

    Ligia Paulillo Sims & Luciana de Campos Franci

  3. Department of Plant Biology, Institute of Biology, University of Campinas-UNICAMP, P.O. Box 6109, Campinas, SP, 13083-970, Brazil

    Luciano Pereira, Claudia Regina Baptista Haddad & Fernando Roberto Martins

Authors
  1. Archimedes Grangeiro Furtado
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ligia Paulillo Sims
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Luciana de Campos Franci
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Luciano Pereira
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Claudia Regina Baptista Haddad
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fernando Roberto Martins
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fernando Roberto Martins.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by A. Braeuning.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Furtado, A.G., Sims, L.P., Franci, L.d. et al. How a non-pioneer tree attains the canopy of a tropical semideciduous forest. Trees 31, 93–103 (2017). https://doi.org/10.1007/s00468-016-1458-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-016-1458-6

Keywords

Search

Navigation