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Latitudinal shift in the timing of flowering of tree species across tropical Africa: insights from field observations and herbarium collections

Published online by Cambridge University Press:  01 September 2020

Dakis-Yaoba Ouédraogo*
Affiliation:
TERRA Teaching and Research Centre, Forest is life, Gembloux Agro-Bio Tech, University of Liège, Gembloux, Belgium
Olivier J. Hardy
Affiliation:
Evolutionary Biology and Ecology, Faculté des Sciences, Université Libre de Bruxelles, Brussels, Belgium
Jean-Louis Doucet
Affiliation:
TERRA Teaching and Research Centre, Forest is life, Gembloux Agro-Bio Tech, University of Liège, Gembloux, Belgium
Steven B. Janssens
Affiliation:
Meise Botanic Garden, Meise, Belgium
Jan J. Wieringa
Affiliation:
National Herbarium of the Netherlands, Naturalis Biodiversity Centre, Leiden, the Netherlands
Piet Stoffelen
Affiliation:
Meise Botanic Garden, Meise, Belgium
Bhely Angoboy Ilondea
Affiliation:
Institut National pour l’Etude et la Recherche Agronomiques, Kinshasa, Democratic Republic of the Congo
Fidèle Baya
Affiliation:
MEFCP/ICRA, BP 830, Bangui, Central African Republic
Hans Beeckman
Affiliation:
Service of Wood Biology, Royal Museum for Central Africa, Tervuren, Belgium
Kasso Daïnou
Affiliation:
Nature+ asbl s/c BIOSE, Management of Forest Resources, Gembloux Agro-Bio Tech, University of Liège, Gembloux, Belgium
Emilien Dubiez
Affiliation:
CIRAD, UR Forêts et Sociétés, University of Montpellier, Montpellier, France
Sylvie Gourlet-Fleury
Affiliation:
CIRAD, UR Forêts et Sociétés, University of Montpellier, Montpellier, France
Adeline Fayolle
Affiliation:
TERRA Teaching and Research Centre, Forest is life, Gembloux Agro-Bio Tech, University of Liège, Gembloux, Belgium
*
Author for correspondence:*Dakis-Yaoba Ouédraogo, Email: dakis.ouedraogo@gmail.com

Abstract

Temporal and spatial patterns in flowering phenology were assessed for eight tropical African tree species. Specifically, the frequency and seasonality of flowering at seven sites in central Africa were determined using field data, graphical analysis and circular statistics. Additionally, spatial variation in the timing of flowering across species range was investigated using herbarium data, analysing the relative influence of latitude, longitude and timing of the dry season with a Bayesian circular generalized linear model. Annual flowering was found for 20 out of the 25 populations studied. For 21 populations located at the north of the climatic hinge flowering was occurring during the dry season. The analysis of herbarium collections revealed a significant shift in the timing of flowering with latitude for E. suaveolens, and with the timing of the dry season for M. excelsa (and to a lesser extent L. alata), with the coexistence of two flowering peaks near the equator where the distribution of monthly rainfall is bimodal. For the other species, none of latitude, longitude or timing of the dry season had an effect on the timing of flowering. Our study highlights the need to identify the drivers of the flowering phenology of economically important African tree species.

Type
Research Article
Copyright
© The Author(s), 2020. Published by Cambridge University Press

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References

Literature cited

Adamescu, GS, Plumptre, AJ, Abernethy, KA, Polansky, L, Bush, ER, Chapman, CA, Shoo, LP, Fayolle, A, Janmaat, KRL, Robbins, MM, Ndangalasi, HJ, Cordeiro, NJ, Gilby, IC, Wittig, RM, Breuer, T, Breuer-Ndoundou Hockemba, M, Sanz, CM, Morgan, DB, Pusey, AE, Mugerwa, B, Gilagiza, B, Tutin, C, Ewango, CEN, Sheil, D, Dimoto, E, Baya, F, Bujo, F, Ssali, F, Dikangadissi, JT, Jeffery, K, Valenta, K, White, L, Masozera, M, Wilson, ML, Bitariho, R, Ndolo Ebika, ST, Gourlet-Fleury, S and Beale, CM (2018) Annual cycles dominate reproductive phenology of African tropical trees. Biotropica 50, 418430.CrossRefGoogle Scholar
Akinnagbe, A, Gailing, O and Finkeldey, R (2010) Genetic diversity of Mansonia altissima A. Chev. under different regimes of human impact in the Akure Forest Reserve, Nigeria. Forestry Studies in China 12, 193200.CrossRefGoogle Scholar
Angoboy Ilondea, B, Beeckman, H, Ouédraogo, DY, Bourland, N, De Mil, T, Van den Bulcke, J, Van Acker, J, Couralet, C, Ewango, C, Hubau, W, Toirambe, B, Doucet, JL and Fayolle, A (2019) Une forte saisonnalité du climat et de la phénologie reproductive dans la forêt du Mayombe : l’apport des données historiques de la Réserve de Luki en République démocratique du Congo. Bois et Forêts des Tropiques 341, 3953.CrossRefGoogle Scholar
Bastin, JF, Barbier, N, Réjou-Méchain, M, Fayolle, A, Gourlet-Fleury, S, Maniatis, D, De Haulleville, T, Baya, F, Beeckman, H, Beina, D, Couteron, P, Chuyong, G, Dauby, G, Doucet, JL, Droissart, V, Dufrêne, M, Ewango, C, Gillet, JF, Gonmadje, C, Hart, T, Kavali, T, Kenfack, D, Libalah, M, Malhi, Y, Makana, JR, Pélissier, R, Ploton, P, Serckx, A, Sonké, B, Stevart, T, Thomas, DW, De Cannière, C and Bogaert, J (2015) Seeing Central African forests through their largest trees. Scientific Reports 5, 13156.CrossRefGoogle ScholarPubMed
Bayol, N, Demarquez, B, De Wasseige, C, Atyi, RE, Fisher, JF, Nasi, R, Pasquier, A, Rossi, X, Steil, M and Vivien, C (2012) Forest management and the timber sector in central Africa. In de Wasseige, C, de Marcken, P, Bayol, N, Hiol Hiol, F, Mayaux Ph, Desclée B, Nasi, R, Billand, A, Defourny, P and Eba’a, R (eds), The Forests of the Congo Basin: State of the Forests 2010. Luxembourg: Publications Office of the European Union, pp. 4361.Google Scholar
Biwolé, A (2015) Origine et dynamique des populations d’arbres des forêts denses humides d’Afrique Centrale, le cas de Lophira alata Banks ex Gaertn C.F. (Ochnaceae). PhD Dissertation: Université de Liège – Gembloux Agro-Bio Tech, Gembloux, Belgique.Google Scholar
Blatrix, R, Peccoud, J, Born, C, Piatscheck, F, Benoit, L, Sauve, M, Djiéto-Lordon, C, Atteke, C, Wieringa, JJ and Harris, DJ (2017) Comparative analysis of spatial genetic structure in an ant–plant symbiosis reveals a tension zone and highlights speciation processes in tropical Africa. Journal of Biogeography 44, 18561868.CrossRefGoogle Scholar
Borchert, R (1996) Phenology and flowering periodicity of Neotropical dry forest species: evidence from herbarium collections. Journal of Tropical Ecology 12, 6580.CrossRefGoogle Scholar
Borchert, R, Meyer, SA, Felger, RS and Porter-Bolland, L (2004) Environmental control of flowering periodicity in Costa Rican and Mexican tropical dry forests. Global Ecology and Biogeography 13, 409425.CrossRefGoogle Scholar
Bourland, N, Kouadio, YL, Lejeune, P, Sonké, B, Phillipart, J, Daïnou, K, Fétéké, F and Doucet, JL (2012) Ecology of Pericopsis elata (Fabaceae), an endangered timber species in Southeastern Cameroon. Biotropica 44, 840847.Google Scholar
Bush, ER, Abernethy, KA, Jeffery, K, Tutin, C, White, L, Dimoto, E, Dikangadissi, JT, Jump, AS and Bunnefeld, N (2017) Fourier analysis to detect phenological cycles using long-term tropical field data and simulations. Methods in Ecology and Evolution 8, 530540.CrossRefGoogle Scholar
CaraDonna, PJ, Iler, AM and Inouye, DW (2014) Shifts in flowering phenology reshape a subalpine plant community. PNAS 111, 49164921.CrossRefGoogle ScholarPubMed
Cleland, EE, Chuine, I, Menzel, A, Mooney, HA and Schwartz, MD (2007) Shifting plant phenology in response to global change. Trends in Ecology and Evolution 22, 357365.CrossRefGoogle ScholarPubMed
Couralet, C, Van Den Bulcke, J, Ngoma, LM, Van Acker, J and Beeckman, H (2013) Phenology in functional groups of Central African rainforest trees. Journal of Tropical Forest Science 25, 361374.Google Scholar
Daïnou, K, Doucet, JL, Sinsin, B and Mahy, G (2012 a) Identité et écologie des espèces forestières commerciales d’Afrique centrale: le cas de Milicia spp. (synthèse bibliographique). Biotechnologie, Agronomie, Société et Environnement 16, 229241.Google Scholar
Daïnou, K, Laurenty, E, Mahy, G, Hardy, OJ, Brostaux, Y, Tagg, N and Doucet, JL (2012 b) Phenological patterns in a natural population of a tropical timber tree species, Milicia excelsa (Moraceae): evidence of isolation by time and its interaction with feeding strategies of dispersers. American Journal of Botany 99, 14531463.CrossRefGoogle Scholar
Dauby, G, Zaiss, R, Blach-Overgaard, A, Catarino, L, Damen, T, Deblauwe, V, Dessein, S, Dransfield, J, Droissart, V, Duarte, MC, Engledow, H, Fadeur, G, Figueira, R, Gereau, RE, Hardy, OJ, Harris, DJ, De Heij, J, Janssens, S, Klomberg, Y, Ley, AC, Mackinder, BA, Meerts, P, Van de Poel, JL, Sonké, B, Sosef, MSM, Stévart, T, Stoffelen, P, Svenning, JC, Sepulchre, P, Van Der Burgt, X, Wieringa, JJ and Couvreur, TLP (2016) RAINBIO: a mega-database of tropical African vascular plants distributions. PhytoKeys 74, 118.Google Scholar
Davis, CC, Willis, CG, Connolly, B, Kelly, C and Ellison, AM (2015) Herbarium records are reliable sources of phenological change driven by climate and provide novel insights into species’ phenological cueing mechanisms. American Journal of Botany 102, 15991609.CrossRefGoogle ScholarPubMed
Deblauwe, V, Droissart, V, Bose, R, Sonké, B, Blach-Overgaard, A, Svenning, JC, Wieringa, JJ, Ramesh, BR, Stévart, T and Couvreur, TLP (2016) Remotely sensed temperature and precipitation data improve species distribution modelling in the tropics. Global Ecology and Biogeography 25, 443454.CrossRefGoogle Scholar
Demenou, BB, Doucet, JL and Hardy, OJ (2018) History of the fragmentation of the African rain forest in the Dahomey Gap: insight from the demographic history of Terminalia superba. Heredity 120, 547561.CrossRefGoogle ScholarPubMed
Dormann, CF, Elith, J, Bacher, S, Buchmann, C, Carl, G, Carré, G, Marquéz, JRG, Gruber, B, Lafourcade, B, Leitão, PJ, Münkemüller, T, McClean, C, Osborne, PE, Reineking, B, Schröder, B, Skidmore, AK, Zurell, D and Lautenbach, S (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36, 2746.CrossRefGoogle Scholar
Doucet, JL (2003) L’alliance délicate de la gestion forestière et de la biodiversité dans les forêts du centre du Gabon. PhD Dissertation: Université Gembloux Agro-Bio Tech, Gembloux, Belgique.Google Scholar
Fayolle, A, Swaine, MD, Bastin, JF, Bourland, N, Comiskey, JA, Dauby, G, Doucet, JL, Gillet, JF, Gourlet-Fleury, S, Hardy, OJ, Kirunda, B, Kouamé, FN and Plumptre, AJ (2014) Patterns of tree species composition across tropical African forests. Journal of Biogeography 41, 23202331.CrossRefGoogle Scholar
Fétéké, F, Fayolle, A, Daïnou, K, Bourland, N, Dié, A, Lejeune, P, Doucet, JL and Beeckman, H (2016) Variations saisonnières de la croissance diamétrique et des phénologies foliaire et reproductive de trois espèces ligneuses commerciales d’Afrique centrale. Bois et Forêts des Tropiques 330.Google Scholar
Funk, C, Peterson, P, Landsfeld, M, Pedreros, D, Verdin, J, Shukla, S, Husak, G, Rowland, J, Harrison, L, Hoell, A and Michaelsen, J (2015) The climate hazards infrared precipitation with stations – a new environmental record for monitoring extremes. Scientific Data 2150066.CrossRefGoogle Scholar
Gelman, A, Carlin, JB, Stern, HS and Rubin, DB (2003) Bayesian Data Analysis. Boca Raton, FL: CRC Press.CrossRefGoogle Scholar
Gond, V, Fayolle, A, Pennec, A, Cornu, G, Mayaux, P, Camberlin, P, Doumenge, C, Fauvet, N and Gourlet-Fleury, S (2013) Vegetation structure and greenness in Central Africa from Modis multi-temporal data. Philosophical Transactions of the Royal Society B: Biological Sciences 36820120309.CrossRefGoogle Scholar
Gonmadje, CF, Doumenge, C, Sunderland, TCH, Balinga, MPB and Sonké, B (2012) Analyse phytogéographique des forêts d’Afrique Centrale: le cas du massif de Ngovayang (Cameroun). Plant Ecology and Evolution 145, 152164.CrossRefGoogle Scholar
Gorel, AP, Fayolle, A and Doucet, JL (2015) Ecologie et gestion des espèces multi-usages du genre Erythrophleum (Fabaceae-Caesalpinioideae) en Afrique (synthèse bibliographique). Biotechnologie, Agronomie, Société et Environnement 19, 415429.Google Scholar
Guan, K, Wolf, A, Medvigy, D, Caylor, KK, Pan, M and Wood, EF (2013) Seasonal coupling of canopy structure and function in African tropical forests and its environmental controls. Ecosphere 4, 121.CrossRefGoogle Scholar
Hardy, OJ, Born, C, Budde, K, Daïnou, K, Dauby, G, Duminil, J, Ewédjé, EEB, Gomez, C, Heuertz, M and Koffi, GK (2013) Comparative phylogeography of African rain forest trees: a review of genetic signatures of vegetation history in the Guineo-Congolian region. Comptes rendus Geoscience 345, 284296.CrossRefGoogle Scholar
Hijmans, RJ, Cameron, SE, Parra, JL, Jones, PG and Jarvis, A (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25, 19651978.CrossRefGoogle Scholar
Janzen, DH (1967) Synchronization of sexual reproduction of trees within the dry season in Central America. Evolution 21, 620637.CrossRefGoogle ScholarPubMed
Kouadio, YL (2009) Mesures sylvicoles en vue d’améliorer la gestion des populations d’essences forestières commerciales de l’Est du Cameroun. PhD Dissertation: Université de Liège – Gembloux Agro-Bio Tech, Gembloux, Belgique. 241 pp.Google Scholar
Letouzey, R (1985) Notice de la carte phytogeographique du Cameroun au 1:500,000 (1985). Institut de la Carte Internationale de la Végétation, Toulouse and Institut de la Recherche Agronomique, Yaoundé Cameroon.Google Scholar
Menga, P, Nasi, R, Bayol, N and Fayolle, A (2012) Phénologie et diamètre de fructification du wengé, Millettia laurentii De Wild: implications pour la gestion. Bois et Forêts des Tropiques 312.CrossRefGoogle Scholar
Meunier, Q, Moumbogou, C and Doucet, JL (2015) Les arbres utiles du Gabon. Gembloux: Presses Agronomiques de Gembloux.Google Scholar
Monks, A, Monks, JM and Tanentzap, AJ (2016) Resource limitation underlying multiple masting models makes mast seeding sensitive to future climate change. New Phytologist 210, 419430.CrossRefGoogle ScholarPubMed
Morellato, LPC, Talora, DC, Takahasi, A, Bencke, CC, Romera, EC and Zipparro, VB (2000) Phenology of Atlantic rain forest trees: a comparative study. Biotropica 32, 811823.CrossRefGoogle Scholar
Mulder, K and Klugkist, I (2017) Bayesian estimation and hypothesis tests for a circular generalized linear model. Journal of Mathematical Psychology 80, 414.CrossRefGoogle Scholar
Newstrom, LE, Frankie, GW and Baker, HG (1994) A new classification for plant phenology based on flowering patterns in lowland tropical rain forest trees at La Selva, Costa Rica. Biotropica 26, 141159.CrossRefGoogle Scholar
Norden, N, Chave, J, Belbenoit, P, Caubère, A, Châtelet, P, Forget, PM and Thébaud, C (2007) Mast fruiting is a frequent strategy in woody species of Eastern South America. PLoS ONE 2, e1079.CrossRefGoogle ScholarPubMed
Ouédraogo, DY, Doucet, JL, Daïnou, K, Baya, F, Biwolé, AB, Bourland, N, Fétéké, F, Gillet, JF, Kouadio, YL and Fayolle, A (2018) The size at reproduction of canopy tree species in central Africa. Biotropica 50, 465476.CrossRefGoogle Scholar
Palla, F and Louppe, D (2002) Obéché. Fiche technique, écologique et sylvicole. Montpellier: Cirad-Forêt.Google Scholar
Palla, F, Louppe, D and Doumenge, C (2002 a) Azobé. Fiche technique, écologique et sylvicole. Montpellier: Cirad-Forêt.Google Scholar
Palla, F, Louppe, D and Forni, E (2002 b) Sapelli. Fiche technique, écologique et sylvicole. Montpellier: Cirad-Forêt.Google Scholar
Pau, S, Wolkovich, EM, Cook, BI, Nytch, CJ, Regetz, J, Zimmerman, JK and Wright, SJ (2013) Clouds and temperature drive dynamic changes in tropical flower production. Nature Climate Change 3, 838842.CrossRefGoogle Scholar
Réjou-Méchain, M and Cheptou, PO (2015) High incidence of dioecy in young successional tropical forests. Journal of Ecology 103, 725732.CrossRefGoogle Scholar
Rosenzweig, C, Casassa, G, Karoly, DJ, Imeson, A, Liu, C, Menzel, A, Rawlins, S, Root, TL, Seguin, B and Tryjanowski, P (2007) Assessment of observed changes and responses in natural and managed systems. In Parry, ML, Canziani, OF, Palutikof, JP, van der Linden, PJ and Hanson, CE (eds), Climate Change 2007: Impacts, Adaptation and Vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge: Cambridge University Press, pp. 79131.Google Scholar
Sakai, S (2001) Phenological diversity in tropical forests. Population Ecology 43, 7786.CrossRefGoogle Scholar
Van Schaik, CP, Terborgh, JW and Wright, SJ (1993) The phenology of tropical forests: adaptive significance and consequences for primary consumers. Annual Review of Ecology and Systematics 24, 353377.CrossRefGoogle Scholar
Sosef, MSM, Dauby, G, Blach-Overgaard, A, Van Der Burgy, X, Catarino, L, Damen, T, Deblauwe, V, Dessein, S, Dransfield, J, Droissart, V, Duarte, MC, Engledow, H, Fadeur, G, Figueira, R, Gereau, RE, Hardy, OJ, Harris, DJ, De Heij, J, Janssens, S, Klomberg, Y, Ley, AC, Mackinder, BA, Meerts, P, Van De Poel, JL, Sonké, B, Stévart, T, Stoffelen, P, Svenning, JC, Sepulchre, P, Zaiss, R, Wieringa, JJ and Couvreur, TLP (2017) Exploring the floristic diversity of tropical Africa. BMC Biology 15, 15.CrossRefGoogle ScholarPubMed
Stropp, J, Ladle, RJ, Malhado, ACM, Hortal, J, Gaffuri, J, Temperley, WH, Skoien, JO and Mayaux, P (2016) Mapping ignorance: 300 years of collecting flowering plants in Africa. Global Ecology and Biogeography 25, 10851096.CrossRefGoogle Scholar
Sun, C, Kaplin, BA, Kristensen, KA, Munyaligoga, V, Mvukiyumwami, J, Kajondo, KK and Moermond, TC (1996) Tree phenology in a tropical montane forest in Rwanda. Biotropica 28, 668681.CrossRefGoogle Scholar
Walther, GR, Post, E, Convey, P, Menzel, A, Parmesan, C, Beebee, TJC, Fromentin, JM, Hoegh-Guldberg, O and Bairlein, F (2002) Ecological responses to recent climate change. Nature 416, 389395.CrossRefGoogle ScholarPubMed
White, F (1983) The Vegetation of Africa: A Descriptive Memoir to Accompany the UNESCO/AETFAT/UNSO Vegetation Map of Africa. Paris: UNESCO.Google Scholar
Wieringa, JJ (1999) Monopetalanthus exit.: a systematic study of Aphanocalyx, Bikinia, Icuria, Michelsonia and Tetraberlinia (Leguminosae, Casalpinioideae). Wageningen Agricultural University Papers 99 4, 1320.Google Scholar
Willis, CG, Ellwood, ER, Primack, RB, Davis, CC, Pearson, KD, Gallinat, AS, Yost, JM, Nelson, G, Mazer, SJ, Rossington, NL, Sparks, TH and Soltis, PS (2017) Old plants, new tricks: phenological research using herbarium specimens. Trends in Ecology and Evolution 32, 531546.CrossRefGoogle ScholarPubMed
Wright, SJ and Calderón, O (2018) Solar irradiance as the proximate cue for flowering in a tropical moist forest. Biotropica 50, 374383.CrossRefGoogle Scholar
Wright, SJ and van Schaik, CP (1994) Light and the phenology of tropical trees. American Naturalist 143, 192199.CrossRefGoogle Scholar
Zalamea, PC, Munoz, F, Stevenson, PR, Paine, CET, Sarmiento, C, Sabatier, D and Heuret, P (2011) Continental-scale patterns of Cecropia reproductive phenology: evidence from herbarium specimens. Proceedings of the Royal Society of London B: Biological Sciences rspb20102259.CrossRefGoogle Scholar
Zhang, H, Yuan, W, Liu, S, Dong, W and Fu, Y (2015) Sensitivity of flowering phenology to changing temperature in China. Journal of Geophysical Research: Biogeosciences 120, 16581665.Google Scholar