Skip to main content
SpringerLink
Log in

Seasonal variations in phenological traits: leaf shedding and cambial activity in Parkia nitida Miq. and Parkia velutina Benoist (Fabaceae) in tropical rainforest

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

Abstract

Key message

In French Guiana, the leaf and cambium phenologies should not be considered only as exogenous-driven processes, as the dry season, but also as endogenous-driven, as tree development stage.

Abstract

Studies of the periodicity of wood formation provide essential data on tree age and on factors that control tree growth. The aim of this work was to investigate cambial phenology and its relation with leaf phenology and climatic seasonality in two briefly deciduous tropical rainforest species belonging to the genus Parkia. Wood microcores were collected every 15 days from April 2009 to February 2012 from five trees of each species. The microcores were stained with cresyl violet acetate to facilitate counting the number of cells in the cambial zone, in the radial enlargement zone and wall-thickening zone. At the same time, we observed leaf shedding pattern in the crown of the same trees. In both species, cambial activity was significantly reduced during the leafless period. In P. nitida, these two concomitant events were observed during the dry season whereas in P. velutina they can occur anytime in the year with no apparent link with seasonality. In conclusion, the period of reduced cambial activity in some tropical rainforest trees may be independent of rainfall seasonality and not necessarily follow an annual cycle. It appears that leaf phenology is a good proxy to estimate cambial activity.

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

  • Alvim PT, Alvim R (1978) Relation of climate to growth periodicity in tropical trees. In: Zimmermann MH (ed) Tomlinson PB. Tropical trees as living systems Cambridge University Press, London, pp 445–464

    Google Scholar 

  • Antonova GF, Cherkashin VP, Stasova VV, Varaksina TN (1995) Daily dynamics in xylem cell radial growth of Scots Pine (Pinus sylvestris L.). Trees 10:24–30

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2014) lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1–7

  • Bäucker E, Bues CT, Vogel M (1998) Radial growth dynamics of spruce (Picea abies) measured by micro-cores. IAWA J 19:301–309

    Article  Google Scholar 

  • Boninsegna JA, Argollo J, Aravena JC, Barichivich J, Christie D, Ferrero ME, Lara A, Le Quesne C, Luckman BH, Masiokas M, Morales M, Oliveira JM, Roig F, Srur A, Villalba R (2009) Dendroclimatological reconstructions in South America: a review. Palaeogeogr Palaeocl 281:210–228

    Article  Google Scholar 

  • Borchert R (1999) Climatic periodicity, phenology, and cambium activity in tropical dry forest trees. IAWA J 20:239–247

    Article  Google Scholar 

  • Borchert R, Rivera G (2001) Photoperiodic control of seasonal development and dormancy in tropical stem-succulent trees. Tree Physiol 21:213–221

    Article  CAS  PubMed  Google Scholar 

  • Boulet R, Brunet D (1983) Prospection pédologique en vue de l’implantation des blocs de l’opération CTFT “Forêt Naturelle”.Technical report. ORSTOM, Cayenne, p 7

  • Bouriaud O, Leban JM, Bert D, Deleuze C (2005) Intra-annual variations in climate influence growth and wood density of Norway spruce. Tree Physiol 25:651–660

    Article  CAS  PubMed  Google Scholar 

  • Brienen RJW (2005) Tree rings in the tropics: a study on growth and ages of Bolivian rain forest trees. Dissertation, University of Utrecht

  • Brousseau L, Bonal D, Cigna J, Scotti I (2013) Highly local environmental variability promotes intrapopulation divergence of quantitative traits: an example from tropical rain forest trees. Ann Bot 112(6):1169–1179

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bullock SH (1997) Effects of seasonal rainfall on radial growth in two tropical tree species. Int J Biometeorol 41:13–16

    Article  Google Scholar 

  • Bullock SH, Solismagallanes JA (1990) Phenology of canopy trees of a tropical deciduous forest in Mexico. Biotropica 22:22–35

    Article  Google Scholar 

  • Caldararu S, Palmer PI, Purves DW (2012) Inferring Amazon leaf demography from satellite observations of leaf area index. Biogeosciences 9:1389–1404

    Article  Google Scholar 

  • Callado CH, Neto SJD, Scarano FR, Costa CG (2001) Periodicity of growth rings in some flood-prone trees of the Atlantic Rain Forest in Rio de Janeiro, Brazil. Trees 15:492–497

    Google Scholar 

  • Callado CH, Roig FA, Tomazello-Filho M, Barros CF (2013) Cambial growth periodicity studies of South American woody species—a review. IAWA J 34:213–230

    Article  Google Scholar 

  • Cardoso FCG, Marques R, Botosso PC, Marques MCM (2012) Stem growth and phenology of two tropical trees in contrasting soil conditions. Plant Soil 354:269–281

    Article  CAS  Google Scholar 

  • Deslauriers A, Morin H (2005) Intra-annual tracheid production in balsam fir stems and the effect of meteorological variables. Trees 19:402–408

    Article  Google Scholar 

  • Deslauriers A, Morin H, Begin Y (2003) Cellular phenology of annual ring formation of Abies balsamea in the Quebec boreal forest (Canada). Can J For Res 33:190–200

    Article  Google Scholar 

  • Détienne P (1989) Appearance and periodicity of growth rings in some tropical woods. IAWA J 10:123–132

    Article  Google Scholar 

  • Dezzeo N, Worbes M, Ishii I, Herrera R (2003) Annual tree rings revealed by radiocarbon dating in seasonally flooded forest of the Mapire River, a tributary of the lower Orinoco River, Venezuela. Plant Ecol 168:165–175

    Article  Google Scholar 

  • Die A, Kitin P, Kouame FN, Van den Bulcke J, Van Acker J, Beeckman H (2012) Fluctuations of cambial activity in relation to precipitation result in annual rings and intra-annual growth zones of xylem and phloem in teak (Tectona grandis) in Ivory Coast. Ann Bot 110:861–873

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Do FC, Goudiaby VA, Gimenez O, Diagne AL, Diouf M, Rocheteau A, Akpo LE (2005) Environmental influence on canopy phenology in the dry tropics. Forest Ecol Manag 215:319–328

    Article  Google Scholar 

  • Elliott S, Baker PJ, Borchert R (2006) Leaf flushing during the dry season: the paradox of Asian monsoon forests. Global Ecol Biogeogr 15:248–257

    Article  Google Scholar 

  • Forster T, Schweingruber FH, Denneler B (2000) Increment puncher —a tool for extracting small cores of wood and bark from living trees. IAWA J 21:169–180

    Article  Google Scholar 

  • Franceschini T, Longuetaud F, Bontemps JD, Bouriaud O, Caritey BD, Leban JM (2013) Effect of ring width, cambial age, and climatic variables on the within-ring wood density profile of Norway spruce Picea abies (L.) Karst. Trees 27:913–925

    Article  Google Scholar 

  • Frankenstein C, Eckstein D, Schmitt U (2005) The onset of cambium activity—a matter of agreement? Dendrochronologia 23:57–62

    Article  Google Scholar 

  • Frankie GW, Baker HG, Opler PA (1974) Comparative phenological studies of trees in tropical wet and dry forests in the lowlands of Costa Rica. J Ecol 62:881–919

    Article  Google Scholar 

  • Gourlet-Fleury S, Guehl JM, Laroussinie O (2004) Ecology and management of a neotropical rainforest—lessons drawn from Paracou, a long-term experimental research site in French Guiana. Elsevier, Paris

    Google Scholar 

  • Gricar J, Zupancic M, Cufar K, Oven P (2007) Regular cambial activity and xylem and phloem formation in locally heated and cooled stem portions of Norway spruce. Wood Sci Technol 41:463–475

    Article  CAS  Google Scholar 

  • Grogan J, Schulze M (2012) The impact of annual and seasonal rainfall patterns on growth and phenology of emergent tree species in southeastern Amazonia, Brazil. Biotropica 44:331–340

    Article  Google Scholar 

  • Huete AR, Didan K, Shimabukuro YE, Ratana P, Saleska SR, Hutyra LR, Yang WZ, Nemani RR, Myneni R (2006) Amazon rainforests green-up with sunlight in dry season. Geophys Res Lett 33:1–4

    Article  Google Scholar 

  • Jacoby GC (1989) Overview of tree ring analysis in tropical regions. IAWA Bull 10:99–108

    Article  Google Scholar 

  • Krepkowski J, Bräuning A, Gebrekirstos A, Strobl S (2011) Cambial growth dynamics and climatic control of different tree life forms in tropical mountain forest in Ethiopia. Trees 25:59–70

    Article  Google Scholar 

  • Kuo Y-L, Huang M-K, Yang Y-L (2013) Dynamic variations in the photosynthetic capacity in a leaf’s lifetime for five Taiwanese tree species at different successional stages Taiwan J For Sci 28:17–28

    CAS  Google Scholar 

  • Lieberman D (1982) Seasonality and phenology in a dry forest in Ghana. J Ecol 70:791–806

    Article  Google Scholar 

  • Lisi CS, Tomazello M, Botoss PC, Roig FA, Maria VRB et al (2008) Tree-ring formation, radial increment periodicity, and phenology of tree species from a seasonal semi-deciduous forest in southeast Brazil. IAWA J 29:189–207

    Article  Google Scholar 

  • Loubry D (1994) Phenology of deciduous trees in a French-Guianan forest (5 degrees latitude north)—case of a determinism with endogenous and exogenous components. Can J Bot 72:1843–1857

    Article  Google Scholar 

  • Lüttge U, Hertel B (2009) Diurnal and annual rhythms in trees. Trees 23:683–700

    Article  Google Scholar 

  • Mangenet T (2013) Approche rétrospective des cycles phénologiques chez quelques espèces guyanaises. Vers une nouvelle branche de la dendrochronologie. Diploma thesis, University of Montpellier

  • Marcati CR, Angyalossy V, Evert RF (2006) Seasonal variation in wood formation of Cedrela fissilis (Meliaceae). IAWA J 27:199–211

    Article  Google Scholar 

  • Marcati CR, Milanez CRD, Machado SR (2008) Seasonal development of secondary xylem and phloem in Schizolobium parahyba (Vell.) Blake (Leguminosae : Caesalpinioideae). Trees 22:3–12

    Article  Google Scholar 

  • Marion L, Gricar J, Oven P (2007) Wood formation in urban Norway maple trees studied by the micro-coring method. Dendrochronologia 25:97–102

    Article  Google Scholar 

  • Mendez-Alonzo R, Pineda-Garcia F, Paz H, Rosell JA, Olson ME (2013) Leaf phenology is associated with soil water availability and xylem traits in a tropical dry forest. Trees 27:745–754

    Article  Google Scholar 

  • Morel H (2013) Dynamique de croissance radiale saisonnière et annuelle des arbres en forêt tropicale humide guyanaise. Diploma thesis, University of Antilles-Guyane

  • Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142

    Article  Google Scholar 

  • Nicolini E, Beauchene J, Leudet de la Vallée B, Ruelle J, Mangenet T, Heuret P (2012) Dating branch growth units in a tropical tree using morphological and anatomical markers: the case of Parkia velutina Benoist (Mimosoïdeae). Ann For Sci 69:543–555

    Article  Google Scholar 

  • Oliveira BRU, Latorraca JVD, Tomazello M, Garcia RA, de Carvalho AM (2011) Dendroclimatology correlations of Eucalyptus grandis Hill ex Maiden of Rio Claro, RJ State—Brazil. Ciencia Florestal 21:499–508

    Google Scholar 

  • Osada N, Tokuchi N, Takeda H (2012) Continuous and fluctuating leaf phenology of adults and seedlings of a shade-tolerant emergent tree, Dipterocarpus sublamellatus, in Malaysia. Biotropica 44:618–626

    Article  Google Scholar 

  • Pennec A, Gond V, Sabatier D (2011) Tropical forest phenology in French Guiana from MODIS time series. Remote Sens Lett 2:337–345

    Article  Google Scholar 

  • Pumijumnong N (2013) Dendrochronology in Southeast Asia. Trees 27:343–358

    Article  Google Scholar 

  • Pumijumnong N, Buajan S (2013) Seasonal cambial activity of five tropical tree species in central Thailand. Trees 27:409–417

    Article  Google Scholar 

  • Pumijumnong N, Wanyaphet T (2006) Seasonal cambial activity and tree-ring formation of Pinus kesiya in northern Thailand in dependence on climate. Forest Ecol Manag 226:279–289

    Article  Google Scholar 

  • Pumijumnong N, Eckstein D, Sass U (1995) Tree-ring research on Tectona grandis on northern Thailand. IAWA J 16:385–392

    Article  Google Scholar 

  • R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Reich PB, Borchert R (1982) Phenology and ecophysiology of the tropical tree, Tabebuia neochrysantha (Bignoniaceae). Ecology 63:294–299

    Article  Google Scholar 

  • Reich PB, Borchert R (1984) Water-stress and tree phenology in a tropical dry forest in the lowlands of Costa-Rica. J Ecol 72:61–74

    Article  Google Scholar 

  • Rossi S, Anfodillo T, Menardi R (2006a) Trephor: a new tool for sampling microcores from tree stems. IAWA J 27:89–97

    Article  Google Scholar 

  • Rossi S, Deslauriers A, Anfodillo T (2006b) Assessment of cambial activity and xylogenesis by microsampling tree species: an example at the alpine timberline. IAWA J 27:383–394

    Article  Google Scholar 

  • Rozendaal DMA, Zuidema PA (2011) Dendroecology in the tropics: a review. Trees 25:3–16

    Article  Google Scholar 

  • Sabatier D, Prévost MF (1989) Quelques données sur la composition floristique et la diversité des peuplements forestiers. Bois et forêts des tropiques 219:31–55

    Google Scholar 

  • Samuels AL, Kaneda M, Rensing KH (2006) The cell biology of wood formation: from cambial divisions to mature secondary xylem. Can J Bot 84:631–639

    Article  CAS  Google Scholar 

  • Schöngart J, Piedade MTF, Ludwigshausen S, Horna V, Worbes M (2002) Phenology and stem-growth periodicity of tree species in Amazonian floodplain forests. J Trop Ecol 18:581–597

    Article  Google Scholar 

  • Schöngart J, Piedade MTF, Wittmann F, Junk WJ, Worbes M (2005) Wood growth patterns of Macrolobium acaciifolium (Benth.) Benth. (Fabaceae) in Amazonian black-water and white-water floodplain forests. Oecologia 145:454–461

    Article  PubMed  Google Scholar 

  • Schrader J, Baba K, May ST, Palme K, Bennett M, Bhalerao RP, Sandberg G (2003) Polar auxin transport in the wood-forming tissues of hybrid aspen is under simultaneous control of developmental and environmental signals. P Natl Acad Sci USA 100:10096–10101

    Article  CAS  Google Scholar 

  • Schrader J, Nilsson J, Mellerowicz E, Berglund A, Nilsson P, Hertzberg M, Sandberg G (2004) A high-resolution transcript profile across the wood-forming meristem of poplar identifies potential regulators of cambial stem cell identity. Plant Cell 16:2278–2292

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Seyoum Y, Fetene M, Strobl S, Beck E (2012) Foliage dynamics, leaf traits, and growth of coexisting evergreen and deciduous trees in a tropical montane forest in Ethiopia. Trees 26:1495–1512

    Article  Google Scholar 

  • Singh KP, Kushwaha CP (2005) Emerging paradigms of tree phenology in dry tropics. Curr Sci 89:964–975

    Google Scholar 

  • Singh ND, Venugopal N (2011) Cambial activity and annual rhythm of xylem production of Pinus kesiya Royle ex. Gordon (Pinaceae) in relation to phenology and climatic factors growing in sub-tropical wet forest of north east India. Flora 206:198–204

    Article  Google Scholar 

  • Skene DS (1969) Period of time taken by cambial derivatives to grow and differentiate into tracheids in Pinus radiata. Ann Bot 33:253–262

    Google Scholar 

  • ter Steege H, Persaud CA (1991) The phenology of Guyanese timber species: a compilation of a century of observations. Vegetatio 95:177–198

    Google Scholar 

  • Trouet V, Mukelabai M, Verheyden A, Beeckman H (2012) Cambial growth season of brevi-deciduous Brachystegia spiciformis trees from south central Africa restricted to less than four months. PLoS One 7:1–9

    Article  Google Scholar 

  • Valdez-Hernández M, Andrade JL, Jackson PC, Rebolledo-Vieyra M (2010) Phenology of five tree species of a tropical dry forest in Yucatan, Mexico: effects of environmental and physiological factors. Plant Soil 329:155–171

    Article  Google Scholar 

  • van Schaik CP, Terborgh JW, Wright SJ (1993) The phenology of tropical forests - Adaptative significance and consequence for primary consumers. Ann Rev Ecol Syst 24:353–377

    Article  Google Scholar 

  • Venugopal N, Liangkuwang MG (2007) Cambial activity and annual rhythm of xylem production of elephant apple tree (Dillenia indica Linn.) in relation to phenology and climatic factor growing in sub-tropical wet forest of northeast India. Trees 21:101–110

    Article  Google Scholar 

  • Wagner F, Hérault B, Stahl C, Bonal D, Rossi V (2011) Modeling water availability for trees in tropical forests. Agr Forest Meteorol 151:1202–1213

    Article  Google Scholar 

  • Williams LJ, Bunyavejchewin S, Baker PJ (2008) Deciduousness in a seasonal tropical forest in western Thailand: interannual and intraspecific variation in timing, duration and environmental cues. Oecologia 155:571–582

    Article  PubMed  Google Scholar 

  • Wils THG, Robertson I, Eshetu Z, Sass-Klaassen UGW, Koprowski M (2009) Periodicity of growth rings in Juniperus procera from Ethiopia inferred from crosSDating and radiocarbon dating. Dendrochronologia 27:45–58

    Article  Google Scholar 

  • Worbes M (1995) How to measure growth dynamics in tropical trees: a review. IAWA J 16(4):337–351

    Article  Google Scholar 

  • Worbes M (1999) Annual growth rings, rainfall-dependent growth and long-term growth patterns of tropical trees from the Caparo forest reserve in Venezuela. J Ecol 87:391–403

    Article  Google Scholar 

  • Worbes A, Raschke N (2012) Carbon allocation in a Costa Rican dry forest derived from tree ring analysis. Dendrochronologia 30:231–238

    Article  Google Scholar 

  • Worbes A, Staschel R, Roloff A, Junk WJ (2003) Tree ring analysis reveals age structure, dynamics and wood production of a natural forest stand in Cameroon. Forest Ecol Manag 173:105–123

    Article  Google Scholar 

  • Wright SJ, Cornejo FH (1990) Seasonal drought and leaf fall in a tropical forest. Ecology 71:1165–1175

    Article  Google Scholar 

  • Wright SJ, van Schaik CP (1994) Light and the phenology of tropical trees. Am Nat 143:192–199

    Article  Google Scholar 

  • Xiao XM, Hagen S, Zhang QY, Keller M, Moore B (2006) Detecting leaf phenology of seasonally moist tropical forests in South America with multi-temporal MODIS images. Remote Sens Environ 103:465–473

    Article  Google Scholar 

  • Yàñez-Espinosa L, Terrazas T, Lopez-Mata L (2006) Integrated analysis of tropical trees growth: a multivariate approach. Ann Bot 98:637–645

    Article  PubMed Central  PubMed  Google Scholar 

  • Yàñez-Espinosa L, Terrazas T, Lopez-Mata L (2010) Phenology and radial stem growth periodicity in evergreen subtropical rainforest trees. IAWA J 31:293–307

    Article  Google Scholar 

  • Yoshizawa N, Inami A, Miyake S, Ishiguri F, Yokota S (2000) Anatomy and lignin distribution of reaction wood in two Magnolia species. Wood Sci Technol 34:183–196

    Article  CAS  Google Scholar 

  • Zalamea PC, Sarmiento C, Stevenson PR, Rodriguez M, Nicolini E, Heuret P (2013) Effect of rainfall seasonality on the growth of Cecropia sciadophylla: intra-annual variation in leaf production and node length. J Trop Ecol 29:361–365

    Article  Google Scholar 

Download references

Author contribution statement

HM, TM, JR, and JB helped to the data acquisition. HM, TM, and PH participated in the data analysis. HM, TM, JR, JB, PH, EN, and BT contributed to the writing of this paper.

Acknowledgments

We are grateful to CIRAD, Dendrotropic, and Guyaflux. We also thank Maryline Harroué and Cyrille Rathgeber for allowing us to use their technical facilities (Xylosciences platform, LERFOB) for the embedding and inclusion processes and for sharing their knowledge about cambial activity. H. Morel received an assistantship from CNES (50 %) and FSE (50 %).

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. UAG, UMR ECOFOG, ECOlogie des FOrêts de Guyane, BP 701, Kourou, 97387, French Guiana, France

    Hélène Morel

  2. INRA, UMR AMAP, botAnique et bioinforMatique de l’Architecture des Plantes, Montpellier, France

    Thomas Mangenet

  3. CIRAD, UMR ECOFOG, ECOlogie des FOrêts de Guyane, Kourou, French Guiana, France

    Thomas Mangenet & Jacques Beauchêne

  4. INRA, UMR Laboratoire d’Etude des Ressources Forêt-Bois, Champenoux, Nancy, France

    Julien Ruelle

  5. CIRAD, UMR AMAP, botAnique et bioinforMatique de l’Architecture des Plantes, Montpellier, France

    Eric Nicolini

  6. INRA, UMR ECOFOG, ECOlogie des FOrêts de Guyane, Kourou, French Guiana, France

    Patrick Heuret

  7. CNRS, UMR Laboratoire de Mécanique et Génie Civil de Montpellier, Montpellier, France

    Bernard Thibaut

Authors
  1. Hélène Morel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Thomas Mangenet
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jacques Beauchêne
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Julien Ruelle
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Eric Nicolini
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Patrick Heuret
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Bernard Thibaut
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hélène Morel.

Additional information

Communicated by A. Franco.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 203 kb)

Supplementary material 2 (DOCX 463 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Morel, H., Mangenet, T., Beauchêne, J. et al. Seasonal variations in phenological traits: leaf shedding and cambial activity in Parkia nitida Miq. and Parkia velutina Benoist (Fabaceae) in tropical rainforest. Trees 29, 973–984 (2015). https://doi.org/10.1007/s00468-015-1177-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-015-1177-4

Keywords

Search

Navigation