Close Home
iForest - Biogeosciences and Forestry
vol. 11, pp. 221-226
Copyright © 2018 by the Italian Society of Silviculture and Forest Ecology
doi: 10.3832/ifor2074-010

Research Articles

The effect of calcium on the growth of native species in a tropical forest hotspot

Denise Teresinha Gonçalves Bizuti (1)Corresponding author, José Carlos Casagrande (2), Marcio Roberto Soares (2), Simone Daniela Sartorio (2), Caetano Brugnaro (2), Ricardo Gomes César (1)

Introduction 

The science and practice of ecological restoration have significantly advanced in the last decades. Most of the research and monitoring of areas under restoration prioritize the analysis of vegetation parameters (i.e., composition, structure, and function), while the soil compartment is rarely analyzed, though soil is considered an indicator of successful restoration ([38], [47]). Little is known about soil influence in the success of forest restoration plantings and its interactions with planted seedlings ([38], [29], [33]).

Currently, more than half of the remaining tropical forests are highly-productive second-growth forests distributed over nutrient-poor and naturally acidic soils, where most of the nutrient pool lies in the biomass and is maintained through nutrient recycling ([19], [9], [28], [39], [31]). When vegetation is removed, most nutrients stored in the biomass are lost and litterfall is interrupted, thus halting nutrient cycling and making the soil as the only source of nutrients ([45]). Nutrient availability in soils increase as succession advances and forest structure develops, therefore forest and soil development are tightly linked in forest restoration and succession ([32]). Compromising soil nutrient availability may arrest forest succession and increase the chance of failure in restoration projects.

Soil chemical degradation is common in highly weathered tropical soils, compromising its quality, reducing macro- and micro-nutrients and increasing aluminum concentrations due to pH reduction. When associated to Al toxicity, low calcium concentrations can hinder root growth (especially in deeper soil layers), leading to low plant growth rates and possibly the failure of reforestation projects in tropical forest ecosystems ([46], [6], [16], [21]). Other studies have demonstrated that calcium addition can promote aboveground biomass gains while reducing root development, which indicates complex relationships of soil fertility and allocation of plant biomass ([8], [52]).

Most studies on soil properties during ecological restoration involve nutrient enrichment by manipulating leaf litter and the dynamics of P and N along the succession, while calcium and aluminum are rarely analyzed ([20], [51], [52], [53], [1], [8], [39]). Calcium is regarded as one of the limiting nutrients in tropical forests, being essential for root structure and osmotic processes ([50]), but possibly leached from soil due to the high rainfall. Since tropical soils usually contain high aluminum concentrations, this element may interfere in nutrient absorption. Species native to tropical forests have a wide range of response to different levels of soil fertility, soil acidity, base saturation and aluminum saturation. These species-specific ranges vary in function of life-history traits, adaptation to local fertility and life stage ([12], [11], [39]). The higher the plant growth rate, the higher its sensibility to acidity, which influence (with some exception) the plant balance of Ca, Mg and P ([11]). Several studies have demonstrated that trees and forest structure contribute to the retention of several nutrients within the system, such as P, N and Ca ([42]).

Recent global agreements are increasing the demand for restoration activities ([41]). In this context, there is an urgent need to investigate how edaphic conditions affect nutrient availability in the early development stages of native seedlings used for forest restoration plantings. Our study aims to analyze the effect of calcium and soil base saturation on biomass gain and nutrient use in seedlings of eight native tree species commonly used for restoration in our study region. We expect that: (i) biomass accumulation and nutrient use will vary among seedling species according to their successional group, with pioneer trees gaining more biomass and absorbing more nutrients than non-pioneers; (ii) soil treatments with higher base saturation (V%) will favor seedling biomass gain; (iii) species with higher biomass gain will absorb more nutrients.

Materials and methods 

The Haplic Arenosol (dystric) soil used in our experiment was collected in the county of Caraguatatuba, São Paulo State, Brazil (Tab. 1), in a white-sand coastal forest (Restinga forest). This forest formation belongs to the Atlantic Forest biome (Fig. 1) - one of the richest and most threatened hotspots in the world ([22]) - and usually develops over nutrient-poor marine substrates originated in the Quaternary. These white-sand forests have been historically deforested since the early stages of colonization in Brazil, and are still threatened today, mainly by the real-estate market. Additionally, the intrinsic Haplic Arenosol (dystric) characteristics of these forests, such as sandiness, low fertility (V% < 50%), high acidity and flooding, limit tree growth and pose a challenge for forest restoration in these areas ([27], [15]).

Tab. 1 - Mean ± standard deviation of soil chemical analyses of the initial soil conditions and treatments designed in this study. (OM): organic matter; (H+Al): potential acidity; (SB): sum of bases; (CEC): cation exchange capacity; (V) base saturation; (m): aluminum saturation; (initial): soil sample before treatments; (Control, V40, V70, VMg70): mean values of the eight native tree species in each treatment at the end of the experiment. The results of the soil analysis refer to the contents available in solution and also the exchangeable contents adsorbed to soil colloids for calcium, magnesium and potassium.
Fig. 1 - Atlantic Forest biome in Caraguatatuba, São Paulo State, Brazil. (A): white-sand coastal forest (Restinga forest); (B): Haplic Arenosol (dystric). Photos: José Carlos Casagrande.

Soil was collected in the 20-40 cm deep soil layer, which typically shows low concentrations of P, K, Ca and high Al saturation, indicating severe limitations to plant growth. Such conditions were adequate to test native seedling growth limitations in this study ([27]).

Soil samples were air dried, sieved through a 2 mm sieve and characterized by routine chemical analysis, according to the methods described by Raij Van et al. ([36]). P, K, Ca and Mg contents were extracted by ion exchange resins and quantified by flame emission photometry (K) and by atomic absorption spectrophotometry (P, Ca, and Mg). We determined organic matter following the Walkley-Black method, after oxidation with a 0.167 mol L-1 potassium dichromate (K2Cr2O7) solution, in the presence of 5 mol L-1 H2SO4. The excess of K2Cr2O7 was titrated with Fe2+ ions from a standardized solution of ferrous ammonium sulfate. Soil pH was potentiometrically measured in 0.01 mol L-1 CaCl2 (1:2.5 soil:solution ratio). We extracted soil potential acidity (H+Al) by the 0.5 mol L-1 calcium acetate solution at pH 7.0. We extracted exchangeable Al content by 1 mol L-1 KCl solution and determined it by titration with 0.025 mol L-1 ammonium hydroxide solution. We calculated the following parameters: (i) sum of bases, SB = Ca+Mg+K; (ii) total cation exchange capacity, CEC = Ca+Mg+K+(H+Al); (iii) base saturation, V% = (SB/CEC) × 100; (iv) aluminum saturation, m% = (Al/SB+Al) × 100. We extracted S content by 0.01 mol L-1 CaH2PO4 solution and determined it by turbidimetry.

The experiment was conducted at the Federal University of São Carlos (UFSCAR), Araras, São Paulo State, Brazil, where the climate is mesothermal with hot and rainy summers and cold dry winters (CWa - Koppen); average annual temperature is 21.4 °C and annual rainfall is 1448.8 mm. All the following analyses were carried out at the Soil Fertility Laboratory of the University.

Limestone (hereafter “lime”) was applied to the collected soil as pure calcium and magnesium carbonate in the proportion of 3:1. The following treatments were designed: (i) control (no lime); (ii) V40 (lime for V%=40); (iii) V70 (lime for V%=70); (iv) VMg70 (calcium chloride and magnesium Ca:Mg = 4.33:1, to reach levels of Ca and Mg equivalent to V%=70, keeping soil pH unaffected). In treatment VMg70, we incorporated 0.99 g and 0.33 g of CaCl2 and MgCl2, respectively, in each vase.

We used 3 × 10-3 m3 polyethylene vases with three liters of soil each. All treatments received a solution of nutrients containing N, P, K, S, B, Cu, Fe, Mn, Mo and Zn. These nutrients were added according to the results of soil analysis and fertilization recommendations obtained from the Technical Bulletin 100 for tree species of the Atlantic Forest ([35]). The sources of these nutrients were urea, monocalcium phosphate, ammonium sulfate, boric acid, copper sulfate, manganese, zinc and sodium molybdate.

Native seedlings (2-3 cm in height) of Atlantic tropical forest trees were provided by a plant nursery located in the municipality of Ibaté (located at 98 km from the experiment site). One seedling was planted per vase. The tree species used and their successional group are listed in Tab. 2. The seedlings were watered daily by a sprinkler system for 6 minutes, previously calculated to maintain appropriate moisture content (25%). We also weekly rotated vase position in each block clockwise.

Tab. 2 - The eight native species native used in this study and their successional group.

After four months, plants were removed from their vases and dried at 65 °C for 72 hours. Shoot and root biomass were separated, grinded and weighed. We quantified shoot and root biomass dry weight, macronutrient absorption and use efficiency. To determine macronutrient content, shoot and root samples were washed in distilled water and dried in a forced-air oven at 65 °C until they reached constant mass. After drying, the plant tissue was weighed, passed through Wiley-type mill and digested by sulfuric solubilization for determination of N, and by nitric-perchloric mixture following the methodology proposed by Malavolta et al. ([26]) for the determination of P, K, Ca, Mg, and S. We determined N using the Kjeldahl method and titration with NaOH 1 mol L-1. We quantified P through photocolorimetry and content was determined by flame emission photometry. The contents of Ca and Mg were determined through atomic absorption spectrophotometry and S by turbidimetry. The amount of macronutrients absorbed (AMN) by the plants was calculated by multiplying dry mass (DM) production by the macronutrient contents MC (AMN = DM × MC) of the shoot and root systems ([12]). The nutrient use efficiency (NUE) was estimated based on the ratio of dry plant mass (DM) divided by the amount of nutrients absorbed (AMN), both in milligrams ([12]).

The experimental design consisted of a random block design with four treatments and eight native tree species, with six repetitions, summing 192 vases. We used the ANOVA procedure to analyze dry biomass, and treatment means were compared by the post-hoc Tukey’s test (α=0.05). Considering the group of nutrients (N, P, K, Ca, Mg and S) as response variables, we carried out a multivariate analysis of variance (MANOVA) for the four following metrics: shoot and root nutrient absorption and shoot and root nutrient use efficiency. In order to investigate if species of different successional groups differed regarding nutrient absorption and use efficiency, we employed four tests: Wilks, Pillai, Hotelling- Lawley and Roy. When the hypothesis of mean vector similarity was rejected for a given group, the means that caused rejection were identified as mean vectors that differed from the others; in such cases, Bonferroni’s confidence intervals were established ([18]). We carried out all the analyses using the R software version 3.0.1 ([37]).

Results 

On average, treatments that used only lime to increase the sum of bases (V40 and V70) gave similar results and increased both shoot and root dry biomass (Tab. 3, Tab. 4). In VMg70, we added enough calcium and magnesium to increase V%=70 without affecting pH (Tab. 1); nevertheless, seedlings in this treatment had lower biomass accumulation than V40 and V70 (Tab. 3, Tab. 4). We observed differences in the production of dry biomass among species of the same ecological group: Schinus terebinthifolius showed the highest values of shoot dry biomass (Tab. 3), while high values of root dry biomass were observed for S. terebinthifolius, Cecropia pachystachya, Cytharexyllum myrianthum and Psidium myrtodes (Tab. 3, Tab. 4).

Tab. 3 - Dry shoot biomass production (g) of eight native tree species under different fertilization treatments. Means followed by the same letter do not significantly differ (p>0.05) across lines (uppercase letters) or columns (lowercase letters). (Control): no lime; (V40): lime addition until V% = 40; (V70): lime addition until V% = 70; (VMg70): calcium chloride and magnesium addition until equivalent Ca and Mg reach V% = 70.
Tab. 4 - Dry root biomass (g) of eight native tree species under different fertilization treatments. Means followed by the same letter do not significantly differ (p>0.05) across lines (uppercase letters) or columns (lowercase letters). (Control): no lime; (V40): lime addition until V% = 40; (V70): lime addition until V% = 70; (VMg70): calcium chloride and magnesium addition until equivalent Ca and Mg reach V% = 70.

We also observed different absorption by species belonging to different successional groups (Tab. 5). Early successional species showed higher nutrient absorption, except for N in shoot biomass, and N and P in root biomass (Tab. 6). Overall, we observed that pioneer species absorbed approximately two times more K and S than secondary species in shoot biomass (0.0585 g kg-1 of K and 0.0105 mg kg-1 of S for pioneers, 0.0280 mg kg-1 of K and 0.0053 mg kg-1 of S for secondary species). Similarly, pioneer species absorbed 37.6%, 38.3% and 43.5% more P, Ca and Mg, respectively, than secondary species. Roots of pioneer species absorbed, on average, 1.0, 2.0 and 3.0 times more K, Ca and Mg than secondary species, respectively.

Tab. 5 - Bonferroni 95% confidence interval (CI) of absorption and nutrient use efficiency in shoots and roots and of nutrient use efficiency in the shoots of seedlings of the eight native species. No significant effect was found for root efficiency after multivariate analysis of variance (MANOVA). (Lower CI): lower limit of CI; (Upper CI): upper limit of CI; (*): p < 0.05.
Tab. 6 - Mean values of absorption and nutrient use efficiency of shoots and roots of eight native tree species. Different letters between rows within the same plant section (shoot or roots) indicate significant differences (p<0.05) between pioneer and secondary species.

Root nutrient-use efficiency was similar among pioneer and secondary species. Regarding shoot biomass, pioneer species were, on average, 1.5 times more efficient in the use of N than secondary species, while nutrient use efficiency of other components was similar between successional groups (Tab. 5, Tab. 6).

Discussion 

Overall, our results indicate the need to correct the soil through liming, in order to reach at least V%=40. A seemingly small increase in V% (i.e., from the original V% = 25 to V% = 40 in the treatment V40) considerably increased shoot and root biomass. Therefore, for these species a slight increase in base saturation to V%=40 will contribute to increase seedling quality, productivity and establishment, and reduce soil correction costs in forest restoration plantings as well. Fertilization is particularly important for restoration plantings in tropical degraded areas, where soils are usually nutrient-poor ([48], [24]). In acid soils, which exhibit high toxicity to aluminum and low cation exchange capacity, the availability of nutrients to plants is hindered and soil correction may favor nutrient absorption and incorporation in plant biomass, as observed in our results and many other studies ([10], [30], [4], [9], [28], [24], [34]).

Our findings corroborates with the study by Furtini et al. ([11]) regarding the macronutrient accumulation and use efficiency in response to phosphorus fertilization, in which late secondary species were less sensible to fertilization. Furthermore, our results also corroborates with Sorreano ([40]), who evaluated 17 tree species and showed that fast-growing species were more sensitive to the lack of nutrients and showed visual signs of deficiency faster than slow-growing species, which indicated higher nutrient demands.

The higher average nutrient absorption observed for pioneers and the higher root biomass detected for two of the three pioneer species used in this experiment (C. pachystachya and S. terebinthifolius), as well as the higher shoot biomass of S. terebinthifolius, are probably all related to the successional strategy of these species (Tab. 3, Tab. 4 and Tab. 6). As a consequence of higher growth rates, early successional species require, absorb and accumulate more nutrients, and respond positively and faster to fertilization ([12], [13]). The higher nutrient absorption of early successional species may be caused by the expansion of the root system and, consequently, the exploration of more soil ([12], [13]). The development of pioneer species in a degraded site ameliorate climatic and soil conditions and favors the establishment of late-successional species, effectively recuperating successional process ([44]).

Initially, we expected that late secondary species would have higher nutrient use efficiency; however, species of different successional groups were similar regarding nutrient use efficiency. Previous studies demonstrated different nutrient use efficiency for different species ([12]). In the field, pioneer species showed slightly higher nutrient use efficiency for N and P than secondary species, while in greenhouses the opposite trend was observed. This contrast between field and greenhouse behavior may have occurred because pioneers in the field could intensify their physiological functions, increasing nutrient use and efficiency. Our work was carried out in nutrient poor soils, and the results obtained for N in the shoot biomass of pioneers may result also from the intensification of their physiology for this nutrient (Tab. 5). In the early stages of restoration plantings, such species may show consistent differences in nutrient use and absorption when compared to older plantings ([49]).

Although Brazil is a global example of native seedlings production for forest restoration and implementation of large-scale restoration programs, there is a lack of studies on white sands ecosystems ([2], [25], [7]). On the other hand, the effect of liming on soil acidity, nutrient availability and plant responses have been thoroughly reported in agricultural and silvicultural investigations ([5], [43]). The few studies in the Atlantic white sand forests (Restinga) that evaluate liming for seedling production point out that native species show a variety of responses to liming and nutrientpoor environments and, in most cases, native species benefited from the reduction in soil acidity, as observed for the averages of treatments V40 and V70 in our study (Tab. 3, Tab. 4).

Other studies on coastal white-sand forests have reported a low vegetation resilience due to soil characteristics. Higher fertility is found in the first 10 cm of soil and, given its high leaching rates, this soil layer has a high density of fine roots for quick nutrient absorption. In these ecosystems, 70% of the root system is located in the 0-10 cm layer and 90% of the root biomass is found up to only 20 cm depth. High Al concentration in these soils hampers downward root growth ([3]). The white sand forests that were the subject of this study show structure and species richness and diversity similar to other forests established on sandy and nutrient-poor soils around the world ([23]).

The patterns for pioneer and secondary species found in this study could contribute to decision-making in restoration projects and to native seedling production of white-sand forest species. However, the existence of species-specific responses has to be taken into consideration ([17]).

Conclusions 

Seedling fertilization increases the chances of success of restoration plantings in degraded areas by favoring native seedling biomass gain and nutrient absorption, and increasing overall soil base saturation through lime fertilization. Although nutrient use efficiency was similar among the studied species, nutrient absorption and biomass gain were related to the successional role of each species, with pioneers showing higher rates. Our results point out the need of further research in this field, as scientific knowledge about the fertilization of native species and their potential to convert nutrients in biomass is still scarce, particularly in field experiments ([14]). Increasing our knowledge on the specific requirements of native forests, particularly in nutrient absorption, is an important step to create guidelines for fertilization in reforestation projects and obtain higher seedling development in restoration plantings, thus reducing maintenance costs and promoting a quick recover of ecological processes of restoration areas.

Acknowledgements 

The authors would like to thank the São Paulo Research Foundation (FAPESP) for the scholarship of the first author of this work.

Authors’ contributions 

DTGB: conducted the experiment and leaded the writing of the manuscript; JCC: tutor of the first author and contributed to the writing of the manuscript and discussion of the results; MRS: contributed to the writing of the manuscript and discussion of the results; SDS and CB: carried out statistical analysis of the data; RGC: contributed to the writing of the manuscript and discussion of the results.

References

(1)
Amazonas NT, Martinelli LA, Piccolo MC, Rodrigues RR (2011). Nitrogen dynamics during ecosystem development in tropical forest restoration. Forest Ecology and Management 262: 1551-1557.
::CrossRef::Google Scholar::
(2)
Bernardino DCS, Paiva HN, Neves JCL, Gomes JM, Marques VB (2007). Influência da saturação por bases e da relação Ca: Mg do substrato sobre o crescimento inicial de jacarandá-da-bahia (Dalbergia nigra (Vell.) Fr. All. ex Benth.). [Growth and seedling quality of Dalbergia nigra (Vell.) FR. All. Ex Benth.) in response to base saturation in the substrate]. Revista Árvore 31: 567-573. [in Portuguese]
::CrossRef::Google Scholar::
(3)
Bonilha RM, Casagrande JC, Soares MR, Reis-Duarte RM (2012). Characterization of the soil fertility and root system of restinga forests. Revista Brasileira de Ciência do Solo 36: 1804-1813.
::CrossRef::Google Scholar::
(4)
Campos CNS, Mingotte FLC, Prado RM, Wadt PGS (2014). Introdução à nutrição e adubação de plantas [Introduction to plant nutrition and fertilization]. In: “Nutrição e Adubação de Espécies Florestais e Palmeiras” (Prado RM, Wadt PGS eds). FCAV/CAPES, Jaboticabal, Brazil, pp. 9-26. [in Portuguese]
::Google Scholar::
(5)
Chatzistathis T, Alifragis D, Papaioannou A (2015). The influence of liming on soil chemical properties and on the alleviation of manganese and copper toxicity in Juglans regia, Robinia pseudoacacia, Eucalyptus sp. and Populus sp. plantations. Journal of environmental management 150: 149-156.
::CrossRef::Google Scholar::
(6)
Chazdon RL (2014). Second growth: the promise of tropical forest regeneration in an age of deforestation. University of Chicago Press, Chicago, IL, USA. pp. 449.
::Online::Google Scholar::
(7)
Coneglian A, Ribeiro PH, Melo BS, Pereira RF, Dorneles JJ (2016). Initial growth of Schizolobium parahybae in Brazilian Cerrado soil under liming and mineral fertilization. Revista Brasileira de Engenharia Agrícola e Ambiental 20: 908-912.
::CrossRef::Google Scholar::
(8)
Fahey TJ, Heinz AK, Battles JJ, Fisk MC, Driscoll CT, Blum JD, Johnson CE (2016). Fine root biomass declined in response to restoration of soil calcium in a northern hardwood forest. Canadian Journal of Forest Research 46: 738-744.
::CrossRef::Google Scholar::
(9)
Fujii K (2014). Soil acidification and adaptations of plants and microorganisms in Bornean tropical forests. Ecological Research 29: 371-381.
::CrossRef::Google Scholar::
(10)
Furtini AEN, Resende AV, Vale FR, Faquin V, Fernandes LA (1999). Acidez do solo, crescimento e nutrição mineral de algumas espécies arbóreas, na fase de muda [Soil acidity, growth and mineral nutrition of some tree species at seedling phase]. Cerne 5: 1-12. [in Portuguese]
::Google Scholar::
(11)
Furtini AEN, Siqueira JO, Curi N, Moreira FMS (2000). Fertilização em reflorestamento com espécies nativas [Fertilization in native species tree plantings]. In: “Nutrição e Fertilização Florestal” (Gonçalves JLM, Benedetti V eds). IPEF, Piracicaba, SP, Brazil, pp. 351-383. [in Portuguese]
::Google Scholar::
(12)
Gonçalves JLM, Kageyama PY, Freixedas VM, Gonçalves JC, Geres WLA (1992). Capacidade de absorção e eficiência nutricional de algumas espécies arbóreas tropicais [Absorption capacity and nutriente use efficiency of some tropical tree species]. In: Proceedings of the “Congresso Nacional sobre Essências Nativas”. Revista do Instituto Florestal, São Paulo, Brazil, pp. 463-469. [in Portuguese].
::Online::Google Scholar::
(13)
Gonçalves JLM, Nogueira LRJ, Ducatti F (2008). Recuperação de solos degradados [Restoration of degraded soils]. In: “Restauração Ecológica de Ecossistemas Naturais” (Kageyama PY, Oliveira RE, Moraes LFM, Engel VL, Gandara FB eds). FEPAF, Botucatu, Brazil, pp. 113-163. [in Portuguese]
::Google Scholar::
(14)
Gonçalves EO, Paiva HN, Neves JCL, Gomes JM (2012). Nutrição de mudas de angico-vermelho (Anadenanthera macrocarpa (Benth.) Brenan) submetidas a doses de N, P, K, Ca e Mg [Nutrition of red angico seedlings (Anadenanthera macrocarpa (Benth.) Brenan) under different macronutrient doses]. Revista Árvore 36: 219-228. [in Portuguese]
::CrossRef::Google Scholar::
(15)
IUSS Working Group WRB (2015). World reference base for soil resources 2014 (update 2015). International soil classification system for naming soils and creating legends for soil maps. Food and Agriculture Organization of the United Nations (FAO), Rome, Italy, pp. 106.
::Google Scholar::
(16)
Jager MM, Richardson SJ, Bellingham PJ, Clearwater MJ, Laughlin DC (2015). Soil fertility induces coordinated responses of multiple independent functional traits. Journal of Ecology 103:374-385.
::CrossRef::Google Scholar::
(17)
Jamaluddin AS, Abdu A, Abdul-Hamid H, Akbar MH, Banga TS, Jusop S, Majid NM (2013). Assessing soil fertility status of rehabilitated degraded tropical rainforest. American Journal of Environmental Science 9: 280-291.
::CrossRef::Google Scholar::
(18)
Johnson RA, Wichern DW (2007). Applied multivariate statistical analysis. Prentice Hall, New Jersey, USA, pp. 773.
::Google Scholar::
(19)
Jordan H, Herrera R (1981). Tropical rain forests: are nutrients really critical? American Naturalist 117: 167-180.
::CrossRef::Google Scholar::
(20)
Kaspari M, Garcia MN, Harms KE, Santana M, Wright SJ, Yavitt JB (2008). Multiple nutrients limit litterfall and decomposition in a tropical forest. Ecology letters 11: 35-43.
::CrossRef::Google Scholar::
(21)
Lal R (2015). Restoring soil quality to mitigate soil degradation. Sustainability 7: 5875-5895.
::CrossRef::Google Scholar::
(22)
Laurance WF (2009). Conserving the hottest of the hotspots. Biological Conservation, 142: 1137.
::CrossRef::Google Scholar::
(23)
Lima RAFD, Oliveira AAD, Martini AMZ, Sampaio D, Souza VC, Rodrigues RR (2011). Structure, diversity, and spatial patterns in a permanent plot of a high Restinga forest in Southeastern Brazil. Acta Botanica Brasilica 25: 633-645.
::CrossRef::Google Scholar::
(24)
Lima-Perim JE, Romagnoli EM, Dini-Andreote F, Durrer A, Dias ACF, Andreote FD (2016). Linking the composition of bacterial and archaeal communities to characteristics of soil and flora composition in the Atlantic Rainforest. PLoS ONE 11: 1-19.
::CrossRef::Google Scholar::
(25)
Macedo ST, Teixeira PC (2011). Calagem e adubação fosfatada para formação de mudas de araçá-boi. [Lime and phosphorus for araza seedling formation]. Acta Amazônica 42: 3. [in Portuguese]
::Google Scholar::
(26)
Malavolta E, Vitti GC, Oliveira SA (1997). Avaliação do estado nutricional das plantas: princípios e aplicações [Evaluation of the Nutritional Status of Plants: principles and applications] (2nd edn). POTAFOS, Piracicaba, Brazil, pp. 319. [in Portuguese]
::Google Scholar::
(27)
Marques MCM, Silva SM, Liebsch D (2015). Coastal plain forests in southern and southeastern Brazil: ecological drivers, floristic patterns and conservation status. Brazilian Journal of Botany 38: 1-18.
::CrossRef::Google Scholar::
(28)
Martins SC, Sousa EN, Piccolo MC, Almeida DQA, Camargo PB, Carmo JB, Porder S, Lins SRM, Martinelli LA (2015). Soil texture and chemical characteristic along an elevation range in the coastal Atlantic Forest of Southeast Brazil. Geoderma Regional 5: 106-116.
::CrossRef::Google Scholar::
(29)
Melo FPL, Pinto SRR, Brancalion PHS, Castro OS, Rodrigues RR, Aronson J, Tabarelli M (2013). Priority setting for scaling-up tropical forest restoration: early lessons from the Atlantic Forest Restoration Pact. Environmental Science and Policy 33: 395-404.
::CrossRef::Google Scholar::
(30)
Meriño-Gergichevich C, Alberdi M, Ivanov AG, Reyes-Díaz M (2010). Al3+-Ca2+ interaction in plants growing in acid soils: Al-phytotoxicity response to calcareous amendments. Journal of Soil Science and Plant Nutrition 10: 217-243.
::Online::Google Scholar::
(31)
Nagy R, Rastetter EB, Neill C, Porder S (2017). Nutrient limitation in tropical secondary forests following different management practices. Ecological Applications 27: 734-755.
::CrossRef::Google Scholar::
(32)
Paul M, Catterall CP, Pollard PC, Kanowski J (2010). Recovery of soil properties and functions in different rainforest restoration pathways. Forest Ecology and Management 259: 2083-2092.
::CrossRef::Google Scholar::
(33)
Perring MP, Standish RJ, Price JN, Craig MD, Erickson TE, Ruthrof KX, Andrew S, Whiteley Whiteley AS, Valentin EL, Hobbs RJ (2015). Advances in restoration ecology: rising to the challenges of the coming decades. Ecosphere 6: 1-25.
::CrossRef::Google Scholar::
(34)
Raboin LM, Razafimahafaly AHD, Rabenjarisoa MB, Rabary B, Dusserre J, Becquer T (2016). Improving the fertility of tropical acid soils: Liming versus biochar application? A long term comparison in the highlands of Madagascar. Field Crops Research 199: 99-108.
::CrossRef::Google Scholar::
(35)
Raij Van B, Cantarella H, Quaggio JA, Furlani AMC (1996). Recomendações de adubação e calagem para o Estado de São Paulo [Recommendation of fertilization and liming for the São Paulo State]. Instituto Agronômico, Campinas, Brazil, pp. 285. [in Portuguese]
::CrossRef::Google Scholar::
(36)
Raij Van B, Andrade JC, Cantarella H, Quaggio JA (2001). Análise química para avaliação da fertilidade de solos tropicais [Chemical analysis to evaluate tropical soil fertility]. Instituto Agronômico, Campinas, Brazil, pp. 285. [in Portuguese]
::Google Scholar::
(37)
R Core Team (2015). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
::Online::Google Scholar::
(38)
Ruiz-Jaen MC, Aide TM (2005). Restoration success: how is it being measured? Restoration Ecology 13: 569-577.
::CrossRef::Google Scholar::
(39)
Sayer EJ, Banin LF (2016). Tree nutrient status and nutrient cycling in tropical forestâlessons from fertilization experiments. Tropical Tree Physiology 6: 275-297.
::CrossRef::Google Scholar::
(40)
Sorreano MCM (2006). Avaliação da exigência nutricional na fase inicial do crescimento de espécies florestais nativas [Evaluation of the nutritional requirements of native forest species in their initial plant growth]. Doctorate Thesis, Applied Ecology Department, University of São Paulo, Brazil, pp. 296. [in Portuguese]
::Google Scholar::
(41)
Suding K, Higgs E, Palmer M, Callicott JB, Anderson CB, Baker M, Gutrich JJ, Hondula KL, LaFevor MC, Larson BMH, Randall A, Ruhl JB, Schwartz KZS (2015). Committing to ecological restoration. Science 348: 638-640.
::CrossRef::Google Scholar::
(42)
Sullivan BW, Alvarez-Clare S, Sarah C, Castle SC, Porder S, Reed SC, Schreeg L, Townsend AR, Cleveland CC (2014). Assessing nutrient limitation in complex forested ecosystems: alternatives to large-scale fertilization experiments. Ecology 95: 668-681.
::CrossRef::Google Scholar::
(43)
Tiritan CS, Büll LT, Crusciol CA, Carmeis Filho AC, Fernandes DM, Nascente AS (2016). Tillage system and lime application in a tropical region: Soil chemical fertility and corn yield in succession to degraded pastures. Soil and Tillage Research 155: 437-447.
::CrossRef::Google Scholar::
(44)
Trindade DFV, Coelho GC (2012). Woody species recruitment under monospecific plantations of pioneer trees - facilitation or inhibition? iForest 5: 1-5.
::CrossRef::Google Scholar::
(45)
Uriarte M, Turner BL, Thompson J, Zimmerman JK (2015). Linking spatial patterns of leaf litterfall and soil nutrients in a tropical forest: a neighborhood approach. Ecological Applications 25: 2022-2034.
::CrossRef::Google Scholar::
(46)
Uroz S, Bispo A, Buee M, Cebron A, Cortet J, Decaens T, Hedde M, Peres G, Vennetier M, Villenave C (2014). Highlights on progress in forest soil biology. Revue Forestière Française, AgroParisTech, Nancy, France, pp. 8.
::CrossRef::Google Scholar::
(47)
Viani RA, Holl KD, Padovezi A, Strassburg BB, Farah FT, Garcia LC, Chaves RB, Rodrigues RR, Brancalion PHS (2017). Protocol for monitoring tropical forest restoration: perspectives from the Atlantic Forest Restoration Pact in Brazil. Tropical Conservation Science 10: 1-8.
::CrossRef::Google Scholar::
(48)
Villalobos EB, Cetina VMA, López MAL, Aldrete A, Paniagua DHDV (2014). Nursery practices increase seedling performance on nutrient-poor soils in Swietenia humilis. iForest 8: 552-557.
::CrossRef::Google Scholar::
(49)
Waring G, Becknell JM, Powers JS (2015). Nitrogen, phosphorus, and cation use efficiency in stands of regenerating tropical dry forest Bonnie. Oecologia 178: 887-897.
::CrossRef::Google Scholar::
(50)
White PJ (1998). Calcium channels in the plasma membrane of root cells. Annals of Botany 81: 173-183.
::CrossRef::Google Scholar::
(51)
Wood TE, Lawrence D, Clark DA, Chazdon RL (2009). Rain forest nutrient cycling and productivity in response to large-scale litter manipulation. Ecology 90: 109-121.
::CrossRef::Google Scholar::
(52)
Wright SJ, Yavitt JB, Wurzburger N, Turner BL, Tanner EV, Sayer EJ, Santiago LS, Kaspari M, Hedin LO, Harms KE, Garcia MN, Corre MD (2011). Potassium, phosphorus, or nitrogen limit root allocation, tree growth, or litter production in a lowland tropical forest. Ecology 92: 1616-1625.
::CrossRef::Google Scholar::
(53)
Yavitt JB, Harms KE, Garcia MN, Mirabello MJ, Wright SJ (2011). Soil fertility and fine root dynamics in response to 4 years of nutrient (N, P, K) fertilization in a lowland tropical moist forest, Panama. Austral Ecology 36: 433-445.
::CrossRef::Google Scholar::

Download

Paper Contents

Paper Sections

Paper Figures

Paper Tables

 
 
Close

 

Gonçalves Bizuti DT, Casagrande JC, Soares MR, Sartorio SD, Brugnaro C, Gomes César R (2018).
The effect of calcium on the growth of native species in a tropical forest hotspot
iForest - Biogeosciences and Forestry 11: 221-226. - doi: 10.3832/ifor2074-010
Close
First Previous Next Last
 
Close
© iForest

Download Reference

Paper ID# ifor2074-010
Title The effect of calcium on the growth of native species in a tropical forest hotspot
Authors Gonçalves Bizuti DT, Casagrande JC, Soares MR, Sartorio SD, Brugnaro C, Gomes César R
Format
Close Download