Photosynthesis, growth, and biomass allocation responses of two Inga species to contrasting light

• Autorzy: Pereira H.A.S. , da Costa G.S. , Schilling A.C. , Mielke M.S. , Sanches M.C. , Dalmolin A.C.
• Języki publikacji: EN

Abstrakty

EN

Inga marginata and Inga subnuda are evergreen N-fixing tree species that are frequently found in the initial stages of forest regeneration. I. marginata has a wide geographic distribution, encompassing the Brazilian Atlantic Rainforest and dry forests of central Brazil, whereas I. subnuda is endemic to the Brazilian Atlantic Rainforest. We conducted this study to compare the physiological, growth, and biomass allocation responses of I. marginata and I. subnuda to contrasting light environments. Considering that I. marginata and I. subnuda have a similar position in the forest succession and different geographic distributions, we tested a hypothesis that these two congeneric species have similar photosynthetic and growth responses to light availability but different biomass allocation. The plants were grown under three light conditions (36, 15, and 6 mol photons m⁻² day⁻¹) for 105 days. Growth, biomass allocation, light–response curves, and leaf pigments were compared among the light conditions and between species by using two-way ANOVA. Our hypothesis was partially supported because the two species had similar photosynthetic responses to changes in light availability, but differences in growth and biomass allocation. The higher relative growth rate in mass of I. subnuda is associated with its higher allocation of biomass to light capture, as shown by the higher values of leaf mass fraction (LMF) and leaf area ratio (LAR). Conversely, the higher values of root mass fraction for I. marginata were in contrast to the higher values of LMF, LAR, and specific leaf area for I. subnuda; this indicates that I. marginata should be better adapted to environments where water could be a limiting factor, which is consistent with its wide geographic distribution.

• Wydawca: -
• Czasopismo: Acta Physiologiae Plantarum
• Rocznik: 2019
• Tom: 41
• Numer: 10
• Opis fizyczny: Article 174 [9p.], ref.

Twórcy

autor

Pereira H.A.S.

• Departamento de Ciencias Biologicas, Universidade Estadual de Santa Cruz, Rodovia Jorge Amado km 16, Ilheus, BA, Brazil

autor

da Costa G.S.

• Departamento de Ciencias Biologicas, Universidade Estadual de Santa Cruz, Rodovia Jorge Amado km 16, Ilheus, BA, Brazil

autor

Schilling A.C.

• Departamento de Ciencias Agrarias e Ambientais, Universidade Estadual de Santa Cruz, Rodovia Jorge Amado km 16, Ilheus, BA, Brazil

autor

Mielke M.S.

• Departamento de Ciencias Biologicas, Universidade Estadual de Santa Cruz, Rodovia Jorge Amado km 16, Ilheus, BA, Brazil

autor

Sanches M.C.

• Instituto de Biologia, Campus Umuarama, Bloco 2D, Universidade Federal de Uberlandia, Rua Joao Naves de Avila 2121, Uberlandia, MG, Brazil

autor

Dalmolin A.C.

• Centro de Formacao em Ciencias e Tecnologias Agroflorestais, Universidade Federal do Sul da Bahia, Rodovia Jorge Amado km 22, Ilheus, BA, Brazil

Bibliografia

• Aidar MPM, Schmidt S, Moss G, Stewart GR, Joly CA (2003) Nitrogen use strategies of neotropical rainforest trees in threatened Atlantic Forest. Plant Cell Environ 26:389–399
• Aleric KM, Kirkman LK (2005) Growth and photosynthetic responses of the federally endangered shrub Lindera melissifolia (Lauraceae) to varied light environments. Am J Bot 92:682–689
• Amissah L, Godefridus MJM, Kyereh B, Poorter L (2015) The effects of drought and shade on the performance, morphology and physiology of Ghanaian tree species. PLoS One 10:1–22
• Ashton PMS, Gunatilleke CVS, Gunatilleke IAUN (1995) Seedling survival and growth of four Shorea species in a Sri Lankan rain forest. J Trop Ecol 11:263–279
• Barros FV, Goulart MF, Sá Telles SB, Lovato MB, Valladares F, Lemos-Filho JP (2012) Phenotypic plasticity to light of two congeneric trees from contrasting habitats: Brazilian Atlantic Forest versus cerrado (savanna). Plant Biol 14:208–215
• Bazzaz EA, Pickett STA (1980) Physiological ecology of tropical succession: a comparative review. Annu Rev Ecol Syst 11:287–310
• Bevill RL, Louda SM (1999) Comparisons of related rare and common species in the study of plant rarity. Conserv Biol 13:493–498
• Boardman NK (1977) Comparative photosynthesis of sun and shade plants. Ann Rev Plant Physiol 28:355–377
• Chapin FS III, Bloom AJ, Field CB, Waring RH (1987) Plant responses to multiple environmental factors. Bioscience 37:49–57
• Chaves MM, Pereira JS, Maroco J, Rodrigues ML, Ricardo CPP, Osório ML, Carvalho I, Faria T, Pinheiro C (2002) How plants cope with water stress in the field. Photosynthesis and growth. Ann Bot 89:907–916
• Cortina J, Vilagrosa A, Trubat R (2013) The role of nutrients for improving seedling quality in drylands. New For 44:719–732
• Davidson R, Mauffette Y, Gagnon D (2002) Light requirements of seedlings: a method for selecting tropical trees for plantation forestry. Basic Appl Ecol 3:209–220
• Davies SJ (1998) Photosynthesis of nine pioneer Macaranga species from Borneo in relation to life history. Ecology 79:2292–2308
• de Lobo FA, Barros MP, Dalmagro HJ, Dalmolin AC, Pereira WE, Souza EC, Vourlitis GL, Rodriguez-Ortiz CE (2013) Fitting net photosynthetic light-response curves with Microsoft Excel a critical look at the models. Photosynthetica 51:445–456
• DeLucia EH, Sipe TW, Herrick J, Maherali H (1998) Sapling biomass allocation and growth in the understory of a deciduous hardwood forest. Am J Bot 85:955–963
• Demmig-Adams B (1990) Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020:1–24
• Demmig-Adams B (1998) Survey of thermal energy dissipation and pigment composition in sun and shade leaves. Plant Cell Physiol 39:474–482
• Feijó NSA, Mielke MS, Gomes FP, França S, Lavinsky A (2009) Growth and photosynthetic responses of Gallesia integrifolia (Spreng.) Harms and Schinus terebinthifolius Raddi seedlings in dense shade. Agrofor Syst 77:49–58
• Ferreira WC, Botelho AS, Davide AC, Faria JMR (2007) Avaliação do crescimento do estrato arbóreo de área degradada revegetada à margem do rio Grande, na usina hidroelétrica de Camargos, MG. Rev Árvore 31:177–185
• Givnish TJ (1988) Adaptations to sun and shade: a whole plant perspective. Aust J Plant Physiol 15:63–92
• Gleeson SK, Tilman D (1992) Plant allocation and the multiple limitation hypothesis. Am Nat 139:1322–1343
• Gong HD, Wang H, Jiao DY, Cai ZQ (2016) Phenotypic plasticity of seedlings of five tropical tree species in response to different light and nutrient availability. Trop Ecol 57:727–737
• Goodale UM, Berlyn GP, Gregoire TG, Tennakoon KU, Ashton MS (2014) Differences in survival and growth among tropical rain forest pioneer tree seedlings in relation to canopy openness and herbivory. Biotropica 46:183–193
• Griffin JJ, Ranney TG, Pharr DM (2004) Photosynthesis, chlorophyll fluorescence and carbohydrate content of Illicium taxa grown under varied irradiance. J Am Soc Hort Sci 129:46–53
• Guaratini MTG, Gomes EPC, Tamashiro JY, Rodrigues RR (2008) Composição florística da Reserva Municipal de Santa Genebra, Campinas, SP. Rev Bras Bot 31:323–337
• Hallik L, Niinemets U, Kull O (2012) Photosynthetic acclimation to light in woody and herbaceous species: a comparison of leaf structure, pigment content and chlorophyll fluorescence characteristics measured in the field. Plant Biol 14:88–99
• Hiscox JD, Israelstam GE (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57:1332–1334
• Hoffmann WA, Franco AC (2003) Comparative growth analysis of tropical forest and savanna woody plants using phylogenetically independent contrasts. J Ecol 91:475–484
• Hunt T (1990) Basic growth analysis: plant growth analysis for beginners. Unwin Hyman, London
• Jassby AD, Platt T (1976) Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol Oceanogr 21:540–547
• Kelly J (2009) Growth and physiological response of six Australian rainforest tree species to a light gradient. For Ecol Manage 257:287–293
• Kitajima K (1994) Relative importance of photosynthetic traits and allocation patterns as correlates of seedling shade tolerance of 13 tropical trees. Oecologia 98:419–428
• Lambers H, Chapin STIII, Pons TJ (2008) Plant physiological ecology. Springer, New York
• Lee WD (1996) Irradiance and spectral quality affect asian tropical rain forest tree seedling development. Ecology 77:568–580
• Lenhard NR, Paiva Neto VB, Scalon Sde PQ, Alvarenga AA (2013) Crescimento de mudas de pau-ferro sob diferentes níveis de sombreamento. Pesqu Agropecu Trop 43:178–186
• Lloyd KM, Lee WG, Wilson JB (2002) Competitive abilities of rare and common plants: comparisons using Acaena (Rosaceae) and Chionochloa (Poaceae) from New Zealand. Conserv Biol 16:975–985
• Lusk CH, Jorgensen MA (2013) The whole-plant compensation points as a measure of juvenile tree light requirements. Funct Ecol 27:1286–1294
• Lüttge U (2008) Physiological ecology of tropical plants. Springer, Berlin
• Marchiori NM, Rocha HR, Tamashiro JY, Aidar MPM (2016) Tree community composition and aboveground biomass in a secondary Atlantic forest, Serra do Mar State Park, São Paulo, Brazil. Cerne 22:501–514
• Markesteijn L, Poorter L (2009) Seedling root morphology and biomass allocation of 62 tropical tree species in relation to drought- and shade-tolerance. J Ecol 97:311–325
• Mata MF (2009) O Gênero Inga (Leguminosae, Mimosoideae) no Nordeste do Brasil: Citogenética, Taxonomia e Tecnologia de Semente. Tese de Doutorado, Programa de Pós-Graduação em Agronomia. Universidade Federal da Paraíba, Areia, PA. p 229
• Matsubara S, Krause GH, Seltmann M, Virgo A, Kursar TA, Jahns P, Winter K (2008) Lutein epoxide cycle, light harvesting and photoprotection in species of the tropical tree genus Inga. Plant Cell Environ 31:548–561
• Nicholls JA, Pennington RT, Koenen EJM, Hughes CE, Hearnl J, Bunnefeld L, Dexer KG, Stonel GN, Kidner CA (2015) Using targeted enrichment of nuclear genes to increase phylogenetic resolution in the neotropical rain forest genus Inga (Leguminosae: Mimosoideae). Front Plant Sci 6:1–20
• Palow DT, Oberbauer SF (2009) Soil type affects seedling shade response at low light for two Inga species from Costa Rica. Plant Soil 319:25–35
• Pearcy RW (2007) Responses of plants to heterogeneous light environments. In: Pugnaire FI, Valladares F (eds) Handbook of functional plant ecology. CRC Press, Boca Raton, pp 213–257
• Peterle PL, Chagas AP, Thomaz LD, Dutral VF, Valadares RT (2015) Mimosoideae (Leguminosae) do Parque Estadual Paulo César Vinha, Espírito Santo, Brasil. Rodriguesia 66:245–257
• Poorter L (1999) Growth responses of 15 rain-forest tree species to a light gradient: the relative importance of morfological and physiological traits. Func Ecol 13:396–410
• Poorter L, Markesteijn L (2008) Seedling traits determine drought tolerance of tropical tree species. Biotropica 40:321–331
• Poorter H, van der Werf A (1998) Is inherent variation in RGR determined by LAR at low irradiance and by NAR at high irradiance? A review of herbaceous species. In: Lambers H, Poorter H, Van Vuuren MMI (eds) Inherent variation in plant growth. Physiological mechanisms and ecological consequences. Backhuys Publishers, Leiden, pp 309–336
• Poorter L, Bongers L, Bongers F (2006) Architecture of 54 moist-forest tree species: traits, trade-offs, and functional groups. Ecology 87:1289–1301
• Ramos Silva LC, Corrêa RS (2008) Sobrevivência e crescimento de seis espécies arbóreas submetidas a quatro tratamentos em área minerada no Cerrado. Rev Árvore 32:731–740
• Rolim SG, Ivanauskas NM, Rodrigues RR, Nascimento MT, Gomes JML, Folli DA, Couto HTZ (2006) Composição florística do estrato arbóreo da Floresta Estacional Semidecidual na planície aluvial do rio Doce, Linhares, ES, Brasil. Acta Bot Bras 20:549–561
• Rossatto DR, Hoffmann WA, Ramos Silva LC, Haridasan M, Sternberg LSL, Franco AC (2013) Seasonal variation in leaf traits between congeneric savanna and forest trees in Central Brazil: implications for forest expansion into savana. Trees 27:1139–1150
• Saldanã-Acosta A, Meave JA, Sanchez-Velasquez LR (2009) Seedling biomass allocation and vital rates of cloud forest tree species: responses to light in shade house conditions. For Ecol Manage 258:1650–1659
• Santelices R, Espinoza S, Cabrera AM (2014) Effect of four levels of shade on survival, morphology and chlorophyll fluorescence of Nothofagus alessandrii container-grown seedlings. iForest 8:638–641
• Santos TA, Mielke MS, Peireira HAS, Gomes FP, da Silva DC (2012) Leaf gas exchange and growth of Protium heptaphyllum March (Burseraceae) seedlings subjected to soil flooding under two light environments. Sci For 40:047–056
• Silva ED, de Tozzi AMGA, Meireles LD (2015) Distribution of Leguminosae tree species in different altitudinal levels along the Atlantic Rain Forest in the Brazilian coast. J Syst Evol 53:266–279
• Silva ED, de Tozzi AMGA, Meireles LD (2016) Leguminosae in an altitudinal gradient in the Atlantic Forest of Serra do Mar State Park, São Paulo, Brazil. Biota Neotrop 16:1–15
• Siminski A, Fantini AC, Guries RP, Ruschel AR, Reis MS (2011) Secondary forest succession in the Mata Atlantica, Brazil: floristic and phytosociological trends. ISRN Ecol 11:1–19
• Simonelli M, Magnago LFS, Martins SV, Matos FAR, Demuner VG (2010) Composição de espécies arbóreas em três estádios sucessionais de floresta ciliar na Lagoa Jacunem, Espírito Santo, Brasil. Bol Mus Biol Mello Leitão 28:5–19
• Singhakumara BMP, Gamage HK, Ashton MS (2003) Comparative growth of four Syzygium species within simulated shade environments of a Sri Lankan rain forest. For Ecol Manage 174:511–520
• Souza RP, Válio IFM (2003) Seedling growth of fifteen Brazilian tropical tree species differing in successional status. Rev Bras Bot 26:35–47
• Souza RD, Correia MEF, Pereira MG, Silva EMR, Paula RR, Menezes LFT (2008) Estrutura da comunidade da fauna edáfica em fragmentos florestais na Restinga da Marambaia, RJ. Ver Bras de Ciências Agrárias 3:49–57
• Souza HN, Goede RGM, Brussaard L, Cardoso IM, Duarte EMG, Fernandes RBA, Gomes LC, Pulleman MM (2012) Protective shade, tree diversity and soil properties in coffee agroforestry systems in the Atlantic Rainforest biome. Agric Ecosyst Environ 146:179–196
• Steege H, Pitman N, Sabatier D, Baraloto C, Salomão JE, Guevara JE et al (2013) Hyperdominance in Amazonian tree the flora. Science. https://doi.org/10.1126/science.1243092
• Strauss-Debenedetti S, Bazzaz F (1996) Photosynthetic characteristics of tropical trees along successional gradients. In: Mulkey SS, Chazdon RL, Smith AP (eds) Tropical forest plant ecophysiology. Chapman and Hall, New York, pp 162–186
• Swaine MD, Whitmore TC (1988) On the definition of ecological species groups in tropical rainforest. Veget 75:81–96
• Swenson NG, Enquist BJ, Pither J, Thompson J, Zimmerman J (2006) The problem and promise of scale dependency in community phylogenetics. Ecology 87:2418–2424
• Tang H, Hu YY, Yu -Y, Song LL, Wu JS (2015) Photosynthetic and physiological responses of Torreya grandis seedlings to varied light environments. Trees 29:1011–1022
• Teixeira AP, Assis MA, Siqueira FR, Casagrande JC (2008) Tree species composition and environmental relationships in a Neotropical swamp forest in Southeastern Brazil. Wetlands Ecol Manage 16:451–461
• Valencia R, Balslev H, Miño GP (1994) High tree alpha diversity in Amazonian Ecuador. Biodivers Conserv 3:21–28
• Valladares F, Niinemets Ü (2008) Shade tolerance, a key plant feature of complex nature and consequences. Annu Rev Ecol Evol Syst 39:237–257
• Valladares F, Wright SJ, Lasso E, Kitajima K, Pearcy RW (2000) Plastic phenotypic response to light of 16 congeneric shrubs from a Panamanian rainforest. Ecology 81:1925–1936
• Walters MB, Reich PB (1999) Low-light carbon balance and shade tolerance in the seedlings of woody plants: do winter deciduous and broad-leaved evergreen species differ? New Phytol 143:143–154
• Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313
• Wiggins NL, Forrister DL, Endara MJ, Coley PD, Kursar TA (2016) Quantitative and qualitative shifts in defensive metabolites define chemical defense investment during leaf development in Inga, a genus of tropical trees. Ecol Evol 6:478–492
• Wright IJ, Westoby M, Reich PB (2002) Convergence towards higher leaf mass per area in dry and nutrient-poor habitats has different consequences for leaf life span. J Ecol 90:534–543
• Yang W, Liu F, Zhou L, Zhang S, An L (2013) Growth and photosynthetic responses of Canarium pimela and Nephelium topengii seedlings to a light gradient. Agrofor Syst 87:505–516
• Yano S, Terashima I (2004) Developmental process of sun and shade leaves in Chenopodium album L. Plant Cell Environ 27:781–793
• Zamith LR, Scarano FR (2004) Produção de mudas de espécies das Restingas do município do Rio de Janeiro, RJ, Brasil. Acta Bot Bras 18:161–176
• Zhang J, Song B, Li B, Ye J, Wang X, Hao Z (2010) Spatial patterns and associations of six congeneric species in an old-growth temperate forest. Acta Oecol 36:29–38

Identyfikatory

DOI

10.1007/s11738-019-2966-y